Tree Physiology

Guillermo Goldstein
Louis S. Santiago Editors

Tropical
Tree
Physiology
Adaptations and Responses in a
Changing Environment
Tree Physiology

Volume 6

Series editors
Frederick C. Meinzer, Corvallis, USA
Ülo Niinemets, Tartu, Estonia
More information about this series at http://www.springer.com/series/6644
Guillermo Goldstein Louis S. Santiago
•

Editors

Tropical Tree Physiology

Adaptations and Responses in a Changing
Environment

123
Editors
Guillermo Goldstein Louis S. Santiago
Laboratorio de Ecología Funcional, Department of Botany & Plant Sciences
Departamento de Ecología Genética y University of California
Evolución, Instituto IEGEBA Riverside, CA
(CONICET-UBA), Facultad de Ciencias USA
Exactas y naturales
Universidad de Buenos Aires and
Buenos Aires
Argentina Smithsonian Tropical Research Institute
Balboa, Ancon, Panama
and Republic of Panama

Department of Biology
University of Miami
Coral Gables, FL
USA

ISSN 1568-2544
Tree Physiology
ISBN 978-3-319-27420-1 ISBN 978-3-319-27422-5 (eBook)
DOI 10.1007/978-3-319-27422-5

Library of Congress Control Number: 2015957228

© Springer International Publishing Switzerland 2016

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Preface

Our World is changing rapidly, yet, how tropical forests will respond to this change
and in turn dampen or accelerate its ripple effects is essentially a physiological
question. Addressing important questions regarding the impacts of changes in land
utilization, such as deforestation, and effects of global climate change will require
specific information on tropical tree physiology. Earth system modeling scientists
are clamoring for more physiological data from tropical trees. It seems that the
scarcity of information on the physiological responses of trees is the greatest source
of uncertainly in predicting how the tropical rain forests will respond to increasing
greenhouse gases and in particular increasing atmospheric CO2. For example, tree
species can adjust their physiological behavior to increasing global temperatures or
decreases in precipitation, or they can be replaced by other species better adapted to
the new environmental conditions. It is also true that the physiology of tropical trees
has not been as well-studied as the physiology of trees from temperate regions,
leading to major gaps in our understanding of how tropical trees interact with the
Earth system over a range of scales.
It is known that the physiological behavior of both tropical and temperate trees is
regulated by similar mechanisms. The differences, however, are related to the
unique selective pressures to which tropical trees have been subjected during the
evolutionary process and its adaptive consequences. The idea put forward by
Theodosius Dobzhansky in the 1950s that tropics and temperate zones are areas
where selection operates differently, generated fruitful lines of thinking and
research. His contention was that in temperate areas mortality was essentially cli-
matically determined, with little or no competition pressure, while in the tropics,
where the environment is relatively more constant, at least in terms of seasonal
changes in temperature, mortality is the result of the effects of population size and
competition. This paradigm of evolutionary pressures has changed substantially but
some aspects of it still remain as a guide for understanding differences in patterns of
adaptation between temperate and tropical plants. Negative density dependence
prevents any single tree species from dominating most tropical forest ecosystems.
The reasons for this must be sought not only in ecological and demographic

v
vi Preface

processes but also among the highly diverse physiological characteristics of tropical
trees. In the tropics, seasonal temperature variations are relatively small compared
to diurnal temperature changes and if soil water is available, growth and metabolic
activities can be maintained throughout the entire year. Heavy herbivore pressure is
continuous and the adaptive responses of tropical plants to herbivory are impres-
sive. The physiological implications of various types of mutualisms found among
tropical trees are also important. Many trees have a relatively short life span of less
than 200 years in the wet tropics compared to more than a 1000 years in some
temperate-zone trees.
There has been a substantial increase in the number of studies of tropical tree
physiology during the last few decades. The reason for this is not only that trees are
the dominant growth form in most tropical ecosystems, but also because of
increasing availability and refinement of equipment such as portable photosynthesis
systems and instruments for studying water relations of plants. Furthermore, a
substantially larger number of tropical biologists are now involved in more
mechanistic studies. The use of tower cranes during the last 25 years has allowed
scientists to reach the canopy of tropical forests, one of the ultimate frontiers for
unveiling not only new organisms but also new processes that were unthinkable just
a few years ago.
A distinct feature of tropical trees is not only their high species diversity but also
the large variety of life history traits and growth forms that are mostly unique to the
tropics such as hemiepiphytic trees, stem succulent trees such as baobab trees,
mangroves, palms and other arborescent monocots, and unusual arborescent plants
near tree line that are not traditional trees. The wide range of shade tolerance from
rapidly growing pioneer trees during gap-phase regeneration to species that can
survive by growing slowly in deep shade contribute to this diversity.
Tropical trees tend to grow in habitats where soil water availability is high all
year round or at least in habitats were it is seasonally available. They grow in arid
environments were they access deep soil water such as in the case of phreatophytic
trees. They also occur along altitudinal gradients within the tropics up to the upper
tree line and in some cases, such as the caulescent giant rosette plants, they can
grow above the continuous forest line. They extend to the subtropics, and in many
cases they share close phylogenetic relationships with subtropical tree species, and
the structure and function of subtropical forests are in many cases similar to tropical
forests, in regards to gap-phase regeneration and the high abundance of lianas.
Through 20 chapters authored by 55 people, this book captures the current state
of knowledge of the main physiological characteristics of tropical trees. The book
was as a way to not only to provide information gathered during the last few years
across the world, but also for laying the foundation for discussing controversial
paradigms and new hypothesis of physiological process and mechanisms of trees.
Thus this book will surely capture the attention not only of tropical biologists but
also of biologists working in many different types of environments around the
globe. Physiological consequences of global environmental change will permeate
most book chapters, as it provides a dynamic arena for tropical trees to respond. The
book is organized in six main parts. The first one is on the physiology of unique
Preface vii

tropical growth forms. This group of conspicuous plants is extremely important for
understanding the structure, function, and dynamics of tropical forests, as well as
understanding why certain species live where they do and not elsewhere.
Hemiepiphytic trees with an unusual progression of life stages and obligate epi-
phytes with a unique photosynthetic pathway, are plants that capture the environ-
mental and demographic wonder of forest ecosystems: Do they start their life cycle
(as in the case of hemiepiphytic trees) or spend their entire life cycle (as in the case
of obligate epiphytes) in the upper canopy to utilize higher levels of incoming solar
radiation or to escape the shady understory with high chances of damage by falling
debris and exclusion by competition with other plants? Stem succulents trees, such
as the fat-stemmed baobabs, which have captured the imagination and attention of
writers, such as in the case of “the little prince” by Antoine de Saint-Exupéry, are
fascinating trees occurring mostly in seasonally dry forests. The enlarged stem with
photosynthetic surfaces, leaves that drop during the dry season and with little
biomass allocation to root systems, appear to have a combination of physiological
and anatomical traits that at first sight is difficult to understand. Do their low wood
density trunks represent conspicuous water storage? Is stored stem water used for
new leaf growth near the end of the dry season or to maintain stem conductance
during the rainy season? Does the large size of the stem serve a biomechanical role
for providing stability to tall mature trees? Palms are another unique growth form,
nearly always associated with tropical environments. The hydraulic architectures
of these monocots have long intrigued physiologists working on plant water rela-
tions and hydraulic architecture. How can trees that do not have secondary growth,
and thus cannot produce new xylem tissue after the plants start growing in height,
cope with intensive droughts and the dysfunction of cavitated xylem vessels?
Finally lianas, which have solved the problem of reaching the upper canopy without
investment in a large diameter stem, can move large amounts of water to transpiring
leaves. How did these plants solve this important water economy constraint
imposed by a relatively narrow stem?
The second part of the book deals with adaptive responses of trees growing in
habitats that are unique to the tropics. Mangrove trees occur in coasts across all
tropical regions with roots taping seawater. Floodplain trees tolerate freshwater
inundation for several months in inland tropical regions and in some cases are
completely covered by water. At high elevation, tropical giant rosette plants rep-
resent one of the most fascinating cases of evolutionary convergence among
tropical alpine climates that are characterized as “summer during the day and winter
at night.”
The third part of the book discusses emergent paradigms on hydraulic archi-
tecture and water relations. The high diversity of tropical tree species allows the use
of a wide array of physiological and morphological traits. This provides fertile
ground for testing new hypothesis on the adaptive significance of physiological
mechanisms for how trees cope with drought, and how they may avoid or repair
cavitated xylem vessels, or how close they are to their physiological limits of water
availability in the face of extreme climatic events.
viii Preface

The fourth part of the book deals with important responses of trees to a limitation
common in tropical soils: low amounts of available nutrients. How valid is the
paradigm of widespread phosphorous limitation? What can be inferred from litter
manipulation and fertilization experiments in tropical forests? What are the
dynamics and the roles of litter accumulation and decomposition? What is the main
distinctive characteristic of nutrient cycling in tropical ecosystems dominated by
trees? Do nutrients limit the ability of tropical trees to respond to climate change, or
can trees adjust and adapt to nutrient limitations to carry on the process of pho-
tosynthetic carbon assimilation? Do N and P equally limit the photosynthetic
process in tropical trees?
Carbon economy and biomass allocation patterns in tropical trees and forests are
the focus of the fifth part of the book. Important issues related to carbon cycling and
the strength of carbon sinks across terrestrial ecosystems worldwide are analyzed.
In particular, the continuum of physiological traits from high light requiring pioneer
trees to slow growing shade-tolerant trees is discussed in terms of primary and
secondary succession in tropical forests and gap-phase regeneration. These two
groups of trees are considered as the extremes of a gradient of species requiring
high light levels for photosynthesis and rapid growth and in species tolerant to
diffuse light and the use of light flecks for carbon assimilation. Are there trade-offs
in carbon allocation between defense against herbivores and growth? Compared to
tropical and temperate forests, subtropical forests have received little attention until
now, and the contribution of this region to the global carbon cycle has not been
fully assessed. In this part the carbon balance of subtropical forests at different
spatial and temporal scales will be analyzed. The reader will be surprised to know
that many subtropical forests are strong carbon sinks, and perhaps the strongest
when compared to other terrestrial ecosystem.
In the last part, ecophysiological processes at different spatial and temporal
scales are analyzed. Until recently the trunks of tropical trees in lowland areas were
assumed not to have tree rings. Several studies have found that this is not the case,
particularly in seasonally dry environments, which opens a window of opportunities
for using tree rings to acquire insights into the ecology and climate sensitivity of
tropical trees as well as the possibility of obtaining the age of individual trees. This
part also addresses biomechanical characteristics of tree, with special references to
the constraints of being a tropical tree. Do tropical trees adhere to the same
biomechanical laws as temperate trees?
In the past 20 years since we began working together, we have seen tropical
ecophysiology evolve from single species studies to large comparative works that
embrace the high diversity of tropical forests. We have seen a transition from
descriptive and natural history studies, which provided an important foundation, to
advanced quantitative and modeling approaches that reveal broader patterns in
space and time. Plant ecophysiology in the tropics has also developed strong
linkages to disciplines that focus on larger spatial scales, including community
ecology, ecosystem ecology, and landscape ecology, as well as smaller spatial
scales such as molecular biology, stable isotope ecology, and genomics. This book
represents the work of a community of leading tropical ecophysiologists, many of
Preface ix

whom are colleagues and collaborators. We hope that it will provide a useful
resource for understanding, conserving, and sustainably managing tropical forests,
as well as predicting how these ecosystems will respond to future climate change.

Buenos Aires Guillermo Goldstein

January 2015 Louis S. Santiago
Contents

Part I Physiology and Life History Traits of Unique Tropical

Growth Forms
Hemiepiphytic Trees: Ficus as a Model System for Understanding
Hemiepiphytism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
Guang-You Hao, Kun-Fang Cao and Guillermo Goldstein
Ecophysiology and Crassulacean Acid Metabolism of Tropical
Epiphytes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 25
Katia Silvera and Eloisa Lasso
Stem-Succulent Trees from the Old and New World Tropics . . . . . . . . 45
Eleinis Ávila-Lovera and Exequiel Ezcurra
Palm Physiology and Distribution in Response to Global
Environmental Change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 67
Heidi J. Renninger and Nathan G. Phillips
Carbon Allocation and Water Relations of Lianas Versus Trees . . . . . . 103
Paula I. Campanello, Eric Manzané, Mariana Villagra,
Yong-Jiang Zhang, Adela M. Panizza, Débora di Francescantonio,
Sabrina A. Rodriguez, Ya-Jun Chen, Louis S. Santiago
and Guillermo Goldstein

Part II Adaptive Responses of Woody Plants to Particular

Tropical Habitats
Flood Tolerant Trees in Seasonally Inundated Lowland Tropical
Floodplains . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127
Pia Parolin, Leandro V. Ferreira, Maria Teresa F. Piedade,
Cátia Nunes da Cunha, Florian Wittmann and Mauricio E. Arias

xi
xii Contents

The Physiology of Mangrove Trees with Changing Climate. . . . . . . . . . 149

Catherine E. Lovelock, Ken W. Krauss, Michael J. Osland,
Ruth Reef and Marilyn C. Ball
Functional Diversity in Tropical High Elevation Giant Rosettes. . . . . . . 181
Fermín Rada

Part III Plant Hydraulics and Water Relations

Physiological Significance of Hydraulic Segmentation, Nocturnal
Transpiration and Capacitance in Tropical Trees: Paradigms
Revisited. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 205
Sandra J. Bucci, Guillermo Goldstein, Fabian G. Scholz
and Frederick C. Meinzer
Maintenance of Root Function in Tropical Woody Species During
Droughts: Hydraulic Redistribution, Refilling of Embolized Vessels,
and Facilitation Between Plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 227
F.G. Scholz, S.J. Bucci, F.C. Meinzer and G. Goldstein
Drought Survival Strategies of Tropical Trees . . . . . . . . . . . . . . . . . . . 243
Louis S. Santiago, Damien Bonal, Mark E. De Guzman
and Eleinis Ávila-Lovera

Part IV Nutrient Limitation of Ecophysiological Processes

in Tropical Trees
Nutrient Availability in Tropical Rain Forests: The Paradigm
of Phosphorus Limitation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 261
James W. Dalling, Katherine Heineman, Omar R. Lopez,
S. Joseph Wright and Benjamin L. Turner
Tree Nutrient Status and Nutrient Cycling in Tropical
Forest—Lessons from Fertilization Experiments . . . . . . . . . . . . . . . . . . 275
E.J. Sayer and L.F. Banin
Is Photosynthesis Nutrient Limited in Tropical Trees? . . . . . . . . . . . . . 299
Louis S. Santiago and Guillermo Goldstein

Part V Carbon Economy and Allocation of Tropical Trees

and Forests
Facing Shortage or Excessive Light: How Tropical and Subtropical
Trees Adjust Their Photosynthetic Behavior and Life History
Traits to a Dynamic Forest Environment . . . . . . . . . . . . . . . . . . . . . . . 319
Guillermo Goldstein, Louis S. Santiago, Paula I. Campanello,
Gerardo Avalos, Yong-Jiang Zhang and Mariana Villagra
Contents xiii

Carbon Economy of Subtropical Forests . . . . . . . . . . . . . . . . . . . . . . . 337

Yong-Jiang Zhang, Piedad M. Cristiano, Yong-Fei Zhang,
Paula I. Campanello, Zheng-Hong Tan, Yi-Ping Zhang,
Kun-Fang Cao and Guillermo Goldstein
The Ecophysiology of Leaf Lifespan in Tropical Forests: Adaptive
and Plastic Responses to Environmental Heterogeneity . . . . . . . . . . . . . 357
Sabrina E. Russo and Kaoru Kitajima
The Effects of Rising Temperature on the Ecophysiology
of Tropical Forest Trees . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 385
Martijn Slot and Klaus Winter
Tree Biomechanics with Special Reference to Tropical Trees. . . . . . . . . 413
Karl J. Niklas

Part VI Ecophysiological Processes at Different Temporal Scales

Tree Rings in the Tropics: Insights into the Ecology and Climate
Sensitivity of Tropical Trees . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 439
Roel J.W. Brienen, Jochen Schöngart and Pieter A. Zuidema

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 463
Contributors

Mauricio E. Arias Department of Organismic and Evolutionary Biology,

Cambridge, MA, USA
Gerardo Avalos Escuela de Biología, Universidad de Costa Rica, San Pedro, San
José, Costa Rica; The School for Field Studies, Center for Sustainable Development
Studies, Beverly, MA, USA
Eleinis Ávila-Lovera Department of Botany & Plant Sciences, University of
California, Riverside, CA, USA
Marilyn C. Ball Research School of Biology, The Australian National University,
Canberra, ACT, Australia
L.F. Banin Centre for Ecology and Hydrology, Bush Estate, Midlothian, Scotland
Damien Bonal INRA, UMR EEF—Université de Lorraine/INRA, Champenoux,
France
Roel J.W. Brienen School of Geography, Leeds University, Leeds, UK
Sandra J. Bucci Grupo de Estudios Biofísicos y Ecofisiológicos, Facultad de
Ciencias Naturales, Universidad Nacional de la Patagonia San Juan Bosco, Chubut,
Argentina; Consejo Nacional de Investigaciones Científicas y Técnicas
(CONICET), Buenos Aires, Argentina
Paula I. Campanello Laboratorio de Ecología Forestal y Ecofisiología, Instituto
de Biología Subtropical, CONICET, FCF, Universidad Nacional de Misiones,
Puerto Iguazú, Argentina
Kun-Fang Cao State Key Laboratory for Conservation and Utilization of
Subtropical Agro-Bioresources, and College of Forestry, School of Forestry,
Guangxi University, Nanning, China
Ya-Jun Chen Key Laboratory of Tropical Forest Ecology, Xishuangbana Tropical
Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan, China

xv
xvi Contributors

Piedad M. Cristiano Laboratorio de Ecología Funcional, Departamento de

Ecología Genética y Evolución, Instituto IEGEBA (CONICET-UBA), Facultad de
Ciencias Exactas y Naturales, Universidad de Buenos Aires, Buenos Aires,
Argentina
Cátia Nunes da Cunha Departamento de Botânica e Ecologia, Universidade
Federal de Mato Grosso, Cuiabá, Mato Grosso, Brazil
James W. Dalling Department of Plant Biology, University of Illinois at
Urbana-Champaign, Urbana, IL, USA; Smithsonian Tropical Research Institute,
Panama, Republic of Panama
Mark E. De Guzman Department of Botany & Plant Sciences, University of
California, Riverside, CA, USA
Débora di Francescantonio Laboratorio de Ecología Forestal y Ecofisiología,
Instituto de Biología Subtropical, CONICET, FCF, Universidad Nacional de
Misiones, Puerto Iguazú, Argentina
Exequiel Ezcurra Department of Botany and Plant Sciences, University of
California, Riverside, CA, USA
Leandro V. Ferreira Museu Paraense Emílio Goeldi, Belém, Pará, Brazil
Guillermo Goldstein Laboratorio de Ecología Funcional, Departamento de
Ecología Genética y Evolución, Instituto IEGEBA (CONICET-UBA), Facultad de
Ciencias Exactas y naturales, Universidad de Buenos Aires, Buenos Aires,
Argentina; Department of Biology, University of Miami, Coral Gables, FL, USA
Guang-You Hao State Key Laboratory of Forest and Soil Ecology, Institute of
Applied Ecology, Chinese Academy of Sciences, Shenyang, China
Katherine Heineman Program in Ecology, Evolution and Conservation Biology,
University of Illinois at Urbana-Champaign, Urbana, IL, USA
Kaoru Kitajima Graduate School of Agriculture, Kyoto University, Kyoto, Japan;
Smithsonian Tropical Research Institute, Balboa, Panama
Ken W. Krauss U.S. Geological Survey, Wetland and Aquatic Research Center,
Lafayette, LA, USA
Eloisa Lasso Smithsonian Tropical Research Institute, Balboa, Ancón, Republic
of Panama; Departamento de Ciencias Biológicas, Universidad de Los Andes,
Bogotá, Colombia
Omar R. Lopez Smithsonian Tropical Research Institute, Panama, Republic of
Panama; Instituto de Investigaciones Científicas y Servicios de Alta Tecnología,
Ciudad de Saber, Panama, Republic of Panama
Catherine E. Lovelock School of Biological Sciences, The University of
Queensland, Brisbane St. Lucia, QLD, Australia
Contributors xvii

Eric Manzané Smithsonian Tropical Research Institute, Panama, Republic of

Panama
Frederick C. Meinzer USDA Forest Service, Forestry Sciences Laboratory,
Corvallis, OR, USA
Karl J. Niklas Plant Biology Section, School of Integrative Plant Science Cornell
University, Ithaca, NY, USA
Michael J. Osland U.S. Geological Survey, Wetland and Aquatic Research
Center, Lafayette, LA, USA
Adela M. Panizza Laboratorio de Ecología Forestal y Ecofisiología, Instituto de
Biología Subtropical, CONICET, FCF, Universidad Nacional de Misiones, Puerto
Iguazú, Argentina
Pia Parolin Biocentre Klein Flottbek and Botanical Garden, University of
Hamburg, Hamburg, Germany; INRA French National Institute for Agricultural
Research, Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254 Institut Sophia
Agrobiotech, Sophia Antipolis, France
Nathan G. Phillips Department of Earth and Environment, Boston University,
Boston, MA, USA
Maria Teresa F. Piedade INPA, Manaus, Amazônia, Brazil
Fermín Rada Instituto de Ciencias Ambientales y Ecológicas de los Andes
Tropicales (ICAE) Facultad de Ciencias, Universidad de Los Andes, Mérida,
Venezuela
Ruth Reef School of Biological Sciences, The University of Queensland, Brisbane
St. Lucia, QLD, Australia
Heidi J. Renninger Department of Forestry, Mississippi State University,
Mississippi, MS, USA
Sabrina A. Rodriguez Laboratorio de Ecología Forestal y Ecofisiología, Instituto
de Biología Subtropical, CONICET, FCF, Universidad Nacional de Misiones,
Puerto Iguazú, Argentina
Sabrina E. Russo School of Biological Sciences, University of Nebraska,
Lincoln, USA
Louis S. Santiago Department of Botany & Plant Sciences, University of
California, Riverside, CA, USA; Smithsonian Tropical Research Institute, Balboa,
Ancon, Panama, Republic of Panama
E.J. Sayer Lancaster Environment Centre, Lancaster University, Lancaster,
England
xviii Contributors

Fabian G. Scholz Grupo de Estudios Biofísicos y Ecofisiológicos, Facultad de

Ciencias Naturales, Universidad Nacional de la Patagonia San Juan Bosco, Chubut,
Argentina; Consejo Nacional de Investigaciones Científicas y Técnicas
(CONICET), Buenos Aires, Argentina
Jochen Schöngart Instituto Nacional de Pesquisas da Amazônia (INPA), Manaus,
AM, Brazil
Katia Silvera Smithsonian Tropical Research Institute, Balboa, Ancón, Republic
of Panama; Department of Botany and Plant Sciences, University of California
Riverside, Riverside, CA, USA
Martijn Slot Smithsonian Tropical Research Institute, Balboa, Ancón, Republic
of Panama
Zheng-Hong Tan Key Laboratory of Tropical Forest Ecology, Xishuangbanna
Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan, China
Benjamin L. Turner Smithsonian Tropical Research Institute, Balboa, Panama,
Republic of Panama
Mariana Villagra Laboratorio de Ecología Forestal y Ecofisiología, Instituto de
Biología Subtropical, CONICET, FCF, Universidad Nacional de Misiones, Puerto
Iguazú, Argentina
Klaus Winter Smithsonian Tropical Research Institute, Balboa, Ancón, Republic
of Panama
Florian Wittmann Department of Biogeochemistry, Max Planck Institute for
Limnology, Mainz, Germany
S. Joseph Wright Smithsonian Tropical Research Institute, Balboa, Panama,
Republic of Panama
Yi-Ping Zhang Key Laboratory of Tropical Forest Ecology, Xishuangbanna
Tropical Botanical Garden, Chinese Academy of Sciences, Mengla, Yunnan, China
Yong-Fei Zhang Department of Geological Sciences, John A. and Katherine G.
Jackson School of Geosciences, University of Texas at Austin, Austin, Texas, USA
Yong-Jiang Zhang Department of Organismic and Evolutionary Biology,
Harvard University, Cambridge, MA, USA; Key Laboratory of Tropical Forest
Ecology, Xishuangbana Tropical Botanical Garden, Chinese Academy of Sciences,
Mengla, Yunnan, China
Pieter A. Zuidema Forest Ecology and Forest Management, Centre for
Ecosystems, Wageningen University, Wageningen, The Netherlands
 Part I
Physiology and Life History Traits
of Unique Tropical Growth Forms
Hemiepiphytic Trees: Ficus as a Model
System for Understanding
Hemiepiphytism

Guang-You Hao, Kun-Fang Cao and Guillermo Goldstein

Abstract Woody hemiepiphytes that have an epiphytic juvenile growth stage differ
crucially in physiology and ecology from common trees. A relatively high degree of
ontogenetic plasticity confers these plants stress tolerance during the epiphytic stage
and sufficient competitiveness later as independent trees. The genus Ficus consists
of about 500 hemiepiphytic and about 300 non-hemiepiphytic woody species.
Ecophysiological comparative studies between hemiepiphytic (Hs) and
non-hemiepiphytic (NHs) Ficus tree species reveal that the existence of an epi-
phytic growth habit even only for a part of their life cycle involves profound
changes that persist to a large degree in their terrestrial growth stage. When growing
under similar conditions, both as saplings and mature trees, the Hs have physio-
logical traits resulting in conservative water use and drought tolerance contrasting
with more prodigal water use and drought sensitivity in NHs. Divergence in water
related functional traits between the two groups are centrally associated with a
trade-off between xylem water flux capacity and drought tolerance. Two distinct
groups of life history traits for Hs and NHs have evolved—epiphytic regeneration
with a slow starting growth rate but enhanced ability to tolerate water deficits in the
upper canopy environment and regeneration in the forest understory with an initial

G.-Y. Hao (&)

State Key Laboratory of Forest and Soil Ecology, Institute of Applied Ecology,
Chinese Academy of Sciences, 110016 Shenyang, China
e-mail: haogy@iae.ac.cn
K.-F. Cao
School of Forestry, Guangxi University, Nanning, Guangxi, China
e-mail: caokf@xtbg.ac.cn
G. Goldstein
Laboratorio de Ecología Funcional, Departamento de Ecología Genética y Evolución,
Instituto IEGEBA (CONICET-UBA), Facultad de Ciencias Exactas y naturales, Universidad
de Buenos Aires, Buenos Aires, Argentina
e-mail: goldstein@ege.fcen.uba.ar; gold@bio.miami.edu
G. Goldstein
Department of Biology, University of Miami, Coral Gables, FL 33146, USA

© Springer International Publishing Switzerland 2016 3

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_1
4 G.-Y. Hao et al.

burst of growth to rapidly gain a relatively large seedling size that can better survive
risks related to terrestrial regeneration. Evidence shows that the underlying physi-
ology distinguishing these two growth forms mostly involves divergences in
adapting to contrasting water regimes but not light conditions, contrary to the
conventional hypothesis that hemiepiphytism evolved for gaining access to higher
irradiance in the canopy than on the forest floor.

Keywords Drought tolerance Hydraulic architecture
Plant water relations



Regeneration Shade tolerance

Introduction

Hemiepiphytes are plants that grow epiphytically for a portion, but not all, of their
life cycle. They are customarily subdivided into primary and secondary hemiepi-
phytes depending on which part of their life cycle has root connections with the
ground. Primary hemiepiphytes normally germinate and grow on other plants but
later establish substantial and permanent connections with the ground via aerial
roots (Kress 1986; Putz and Holbrook 1986). Secondary hemiepiphytes germinate
on the ground, climb up their host plants, and then lose stem connections with the
soil (Kress 1986; Putz and Holbrook 1986). Primary hemiepiphytes have a true
epiphytic stage, during which their ecophysiological traits are very similar to those
of the true epiphytes (Zotz and Winter 1994), while secondary hemiepiphytes differ
fundamentally from epiphytes, but are rather functionally similar to vines even after
the lower part of their stems die back (Holbrook and Putz 1996b; Moffett 2000). For
example, many aroid species that are called secondary hemiepiphytes can establish
connections with the soil by producing adventitious roots after severing the stem
connections with the ground and regaining access to soil resources. The current use
of the term hemiepiphyte thus confounds two radically different life cycle char-
acteristics. Zotz (2013a) suggested to entirely discard the term “secondary
hemiepiphyte” and instead use Moffett’s (2000) term “nomadic vine” for climbing
plants that germinate on the ground and lose the lower part of their stem later during
ontogeny. By doing this, the term “hemiepiphyte” is reserved exclusively for
species that were formerly called primary hemiepiphytes. We adhere to this defi-
nition hereafter in this chapter.
Hemiepiphytes are an important plant component of tropical vegetation.
According to a recent census by Zotz (2013b), there are 19 families and 28 genera
that contain more than 800 hemiepiphytic species. Among these taxa, Ficus
(Moraceae) and Clusia (Clusiaceae) are the two most important genera that are
composed of more than 600 woody hemiepiphytic species combined. In the tropics
many of these species are well known as strangers that germinate on tops of other
trees and have the potential to strangle their hosts and become structurally inde-
pendent trees (Fig. 1a–d). In tropical forests of Panama and Zimbabwe 9.8 and
Hemiepiphytic Trees: Ficus as a Model System … 5

Fig. 1 a The epiphytic growth phase of Ficus altissima growing in the canopy of a host palm tree
showing multiple dangling aerial roots; b Ficus altissima during its terrestrial growth stage
showing multiple “pseudostems” formed by fused aerial roots; c a Ficus concinna tree strangling a
tree; d a free-standing stage Ficus curtipes tree showing tangled architecture of aerial roots
defining the space occupied by a host tree that has been strangled and decomposed. All plants are
growing in the Xishuangbanna Tropical Botanical Garden (XTBG), Yunnan, China Photo credits:
GYH
6 G.-Y. Hao et al.

12.6 % of trees, respectively, were found bearing hemiepiphytic Ficus (Guy 1977;
Todzia 1986); in Venezuela 13 % of trees >10 cm DBH carried Ficus or Clusia
(Putz 1983). Hemiepiphytic Ficus species are also very commonly found on
architectural structures especially in tropical and subtropical regions, such as
ancient temples in India and old stone walls in urban Hong Kong (Sitaramam et al.
2009; Jim 2014).
It is commonly considered that there are several potential advantages to start the
life cycle as an epiphyte in tropical forests. One of the most important advantages is
that the forest canopy offers higher light availability than the forest understory. It
has been suggested that hemiepiphytism evolved in plants that colonized rocky
areas as an adaptation to access high light environments in the forest canopy
(Dobzhansky and Murea-Pires 1954; Ramirez 1977; Putz and Holbrook 1986;
Todzia 1986; Laman 1995; Williams-Linera and Lawton 1995). They may also
benefit from minimizing risks of fire, flood, terrestrial herbivores and damage or
coverage by falling debris. The advantages of spending the initial part of their life
cycle as an epiphyte, however, can be offset by the potential limitations of water
and nutrient availability (Benzing 1990; Coxson and Nadkarni 1995; Holbrook and
Putz 1996a, b, c; Swagel et al. 1997).
The hemiepiphytic Ficus (Moraceae) is the most conspicuous group of species
with such life history in terms of habitat breath, species richness, abundance and
dominance in forest ecosystems (Dobzhansky and Murca-Pires 1954; Putz and
Holbrook 1986; Holbrook and Putz 1996b). Species in the genus Ficus are among
the most important components of tropical lowland rainforests throughout the world
(Harrison 2005) and are ecologically important due to their interactions with many
frugivorous animals and other plant species (Shanahan et al. 2001). This genus
consists of about 500 hemiepiphytic species, including stranglers and banyans, and
about 300 non-hemiepiphytic woody species (Putz and Holbrook 1986; Harrison
2005). In Ficus, the hemiepiphytic habit most likely evolved four times in the
subgenera Urostigma, Sycidium, Pharmacosycea and in a closely related group
comprised of the subgenera Conosycea, Galoglychia, Americana and Malvanthera
(Harrison 2005). From the point of view of evolution, it is important to consider the
main environmental factors that selected for this specialized growing habit.
Comparative studies in ecophysiology between hemiepiphytic and non-hemiepiphytic
Ficus species provide valuable information about the main differences between these
two groups in environmental adaptation of the seedling/sapling and adult stages, which
allow us to infer major selective pressures for the evolution of hemiepiphytism.
Because of the radical changes in rooting environment between the two growth
phases, developmental and physiological plasticity is important for hemiepiphytes
and enables them first to survive the harshness of the epiphytic habitat and then to
compete successfully with other trees when they are later rooted in the ground
(Holbrook and Putz 1996b). The change from functional epiphyte to tree is
accompanied by a shift in rooting volume and characteristics of the rooting zone.
Previous studies have found that nutrient availability does not exert a major limi-
tation to the epiphytic phase of hemiepiphytic Ficus (Putz and Holbrook 1989),
Hemiepiphytic Trees: Ficus as a Model System … 7

whereas measurement of stomatal conductance and leaf phenology indicate that

water availability is frequently a major constraint as compared to terrestrially rooted
trees of the same species (Holbrook and Putz 1996a, b, c). Epiphytes face frequent
and severe water deficits even in areas with very humid climate (Benzing 1990). In
seasonally dry climates, hemiepiphytes in the epiphytic stage can experience even
more severe drought during the dry season.
In hemiepiphytes, the two different growth phases with contrasting environ-
mental conditions make it interesting and convenient for physiological comparative
studies. Some hemiepiphytes, such as species of the genus Clusia, switch to the
more water efficient facultative CAM metabolism when stressed by drought, but all
of the species of Ficus studied thus far exhibit only C3 photosynthesis regardless of
the life stage (Ting et al. 1987). Strangler Ficus in the epiphytic stage avoids water
deficit mainly through strong stomatal control to maintain relatively high leaf water
potentials (Holbrook and Putz 1996c). During both the rainy season and the dry
season, stomatal conductance of epiphytic stage strangler figs is lower than con-
specific trees. Throughout the dry season, epiphytic stage strangler figs only open
their stomata in the early morning (Holbrook and Putz 1996c). Furthermore, epi-
phytic phase Ficus can better control water loss from leaf surfaces than conspecific
tree-phase plants after stomata are closed (Holbrook and Putz 1996a). The smaller
guard cell surface area due to lower stomata density enables the epiphytic stage
Ficus to lose water more slowly compared to tree phase plants of the same species.
Due to these water conservation traits, leaf water potentials of epiphytic stage Ficus
plants are found to be similar or even less negative than conspecific tree-phase
individuals (Holbrook and Putz 1996b). Even when both epiphytic phase and tree
phase Ficus are well supplied with water during manipulative experiments, the
leaves of epiphytic plants still exhibit significantly lower stomatal conductance and
much lower epidermal conductance, indicating strong developmental changes from
the epiphytic to the terrestrial phase (Holbrook and Putz 1996a).
Physiology related to epiphytic-terrestrial phase transition in Ficus has been well
studied and reviewed by Holbrook and Putz (1996b). This chapter focuses on
ecophysiological comparisons between hemiepiphytic (Hs) and non-hemiepiphytic
(NHs) Ficus tree species grown under similar environmental conditions to better
understand intrinsic differences between these two functional groups.

Comparison of Hydraulics and Water Balance

Stem Hydraulic Conductivity

Only few studies have compared hydraulic architecture between woody hemiepi-
phytic and free-standing tree species (Patiño et al. 1995; Zotz et al. 1997; Hao et al.
2011). These studies demonstrate that hemiepiphytic plants have stems that are less
conductive as shown by relatively low leaf-specific hydraulic conductivity (Kl).
According to the studies by Patiño et al. (1995) and Zotz et al. (1997), the lower Kl
8 G.-Y. Hao et al.

found in hemiepiphytic Ficus and Clusia shoots are largely due to their low
investment in water conducting tissue, implying a lower wood cross-sectional area
per unit leaf area (Huber value; Hv), rather than less conductive sapwood tissues.
Their stem hydraulic conductivity values expressed per wood cross-sectional area
are even larger than in tropical and temperate angiosperm trees (Zotz et al. 1997).
The more recent study by Hao et al. (2011) comparing mature trees of Hs and NHs
grown in a common garden, however, found no significant difference in leaf to
sapwood area ratio between the two functional groups but substantially lower
specific hydraulic conductivity (Ks, i.e. an intrinsic measure of water transport
efficiency of the xylem) in Hs than in NHs.
The discrepancies between different studies, however, may largely be due to
methodological differences in the way Ks and Huber values are estimated. A close
examination of the Patiño et al. (1995) and Zotz et al. (1997) studies reveal that in
both studies Ks and Hv were calculated on a whole stem cross sectional area basis
rather than the sapwood area basis. This may strongly affect the interpretation of the
results of such comparative studies because non-hemiepiphytic Ficus species
usually have large pith in their stem, but the pith is negligible in the stems of
hemiepiphytic species. In the stems of non-hemiepiphytic Ficus species, the pith
can account for up to 70 % (on average 45 %) of the “wood” cross-sectional area
(G.-Y. Hao unpublished). By using only the sapwood area, excluding the pith, for
Ks calculation, we find that Hs have sapwoods that are far less efficient in con-
ducting water even when both types of species are growing as independent trees in
a common garden (Hao et al. 2011). Consistent with the differences in stem hy-
draulic conductivity, Hs and NHs show significant differences in leaf properties
related to water transport, water conservation and drought tolerance (Hao et al.
2010). These findings can be parsimoniously explained by the hypothesis that Hs
are adapted to drought conditions associated with an epiphytic growth stage in the
canopy, whereas NHs are selected for strong competitive ability given the higher
water availability that they experience during their first growth stages.

Water Flux Through the Leaf

Hemiepiphytic Ficus species have low leaf water flux capacity that parallels their
relatively low stem-level hydraulic conductivity. Compared with congeneric ter-
restrial species, Hs have significantly narrower vessels in their leaf petioles and
lower theoretical leaf area adjusted hydraulic conductance calculated from petiole
xylem vessel dimension measurements (Fig. 2a, b; P < 0.05, t-tests). The NHs have
vessel lumen diameters that are on average 30 % larger than Hs but the number of
vessels per petiole standardized by leaf area does not differ between the two growth
forms. The resultant theoretical xylem hydraulic conductance of NHs averages
104 % higher than that of Hs (Hao et al. 2010).
The lower leaf water flux capacity in Hs is consistent with their lower transpi-
rational water requirement per unit leaf area. Compared to NHs grown under similar
Hemiepiphytic Trees: Ficus as a Model System … 9

Fig. 2 a Leaf petiole average

vessel diameter (Dv) and;
b theoretical hydraulic
conductance (Kt) of five
hemiepiphytic and five
non-hemiepiphytic Ficus
species. Mean values ± SE for
each species are reported
(n = 5–6). Species name
abbreviations: Ficus
benjamina, BE; F. concinna,
CO; F. curtipes, CU; F.
religosa, RE; F. tinctoria,
TI; F. auriculata, AU; F.
esquiroliana, ES; F. hispida,
HI; F. racemosa, RA; F.
semicordata, SE (data from
Hao et al. 2010)

conditions, Hs have significantly lower stomatal conductance and higher intrinsic

water use efficiency measured both on mature trees well rooted in the soil and
saplings growing in pots supplied with sufficient water (Hao et al. 2010, 2013).
Differences in water use between Hs and NHs are most significant when diurnal
courses of leaf gas exchange are compared. Epiphytic stage Hs in their native
habitats have been found to open stomata only in the early morning during the dry
season (Holbrook and Putz 1996c). When saplings are grown in pots and are well
watered, Hs still have lower stomatal conductance and a shorter duration of active
CO2 assimilation on sunny days (Fig. 3a, b). In both groups of species, photo-
synthetic net assimilation rates reach maximum values around 11:00 h, but rates
start to decline in Hs there after until the end of the day, whereas in NHs rates
remain at high levels until 14:00 h with an afternoon peak following a slight midday
depression (Fig. 3b). The different diurnal patterns of photosynthesis between the
two growth forms of Ficus are likely associated with the intrinsically low xylem
hydraulic conductivity in Hs compared to NHs. Higher water use efficiency in Hs
suggests a constitutively conservative water use strategy (Table 1), consistent with
adaptations to cope with drought-prone canopy habitats.
In juvenile plants of Hs, more conservative water use may contribute to the
protection of their xylem vascular systems from catastrophic cavitation when facing
unpredictable drought conditions associated with canopy growth in their natural
10 G.-Y. Hao et al.

Fig. 3 Leaf net CO2 assimilation rate (An) of (a) hemiepiphytic and (b) non-hemiepiphytic Ficus
saplings grown under full sunlight. Numbers in panel a and b indicate daily cumulative net
assimilation. Ficus concinna (▼), F. tinctoria ( ), F. virens (★), F. hispida (◇), F. racemosa
( ), F. semicordata (☆). Filled and open symbols indicate hemiepiphytic and non-hemiepiphytic
species, respectively (Hao et al. 2013)

habitats. Higher leaf xylem hydraulic conductance as found in NHs indicates

adaptation of the leaf vascular system to a more prodigal water use, which is only
advantageous under conditions of reliable water sources. Considering the frequently
occurring drought stress related to a canopy growth during their early ontogeny,
high water flux capacity does not appear to be a beneficial trait for Hs.

Traits Conferring Drought Tolerance

Hemiepiphytic Ficus species exhibit traits related to greater drought tolerance

compared to NHs (Table 1). They have higher leaf mass per area and lower leaf
osmotic potential at turgor loss point (π0), typical adaptations to drought-prone
environments (Hao et al. 2010). The Hs almost completely close their stomata at
turgor loss point but all of the NHs maintain relatively high stomatal conductance,
resulting in a much larger “safety margin” between stomatal closure and turgor loss
point in Hs compared to NHs (Fig. 4). Narrow safety margins can benefit some
plants by allowing the maintenance of gas exchange and thus optimizing returns on
xylem investment (Brodribb and Holbrook 2004). A prerequisite for this set of
functional traits is a relatively reliable water supply to the leaves that may not be
Hemiepiphytic Trees: Ficus as a Model System … 11

Table 1 Ecophysiological traits of seven hemiepiphytic (H) and seven non-hemiepiphytic

(NH) Ficus species (values are means ± 1 SE). Means of the two growth forms were compared
using one-way ANOVAs
Functional traits Prediction H mean NH mean P-value
(ANOVA)
Specific hydraulic conductivity H < NH 2.00 ± 0.22 7.06 ± 1.28 0.001
(kg m−1 s−1 MPa−1)
Leaf-specific hydraulic H < NH 2.28 ± 0.45 9.55 ± 2.71 0.007
conductivity
(× 10−4 kg m−1 s−1 MPa−1)
Sapwood density (g cm−3) H > NH 0.50 ± 0.03 0.45 ± 0.03 0.100
Leaf to sapwood area ratio H < NH 128.7 ± 18.0 115.2 ± 18.5 0.291
(cm2 mm−2)
Leaf size (cm2) H < NH 84.8 ± 26.2 296.7 ± 106.6 0.030
Leaf mass per area (g m−2) H > NH 107.0 ± 12.5 69.1 ± 6.5 0.007
Leaf saturated water content (g g−1) H < NH 1.88 ± 0.14 2.30 ± 0.15 0.025
Maximum net CO2 assimilation H < NH 13.0 ± 0.8 13.7 ± 0.8 0.274
rate on leaf area basis
(μmol m−2 s−1)
Maximum net CO2 assimilation H < NH 0.126 ± 0.016 0.210 ± 0.028 0.008
rate on leaf mass basis
(μmol g−1 s−1)
Maximum stomatal conductance H < NH 0.301 ± 0.028 0.408 ± 0.021 0.003
(mol m−2 s−1)
Intercellular CO2 concentration H < NH 290.1 ± 3.5 305.2 ± 2.2 0.001
(μmol mol−1)
Intrinsic water-use efficiency H > NH 44.6 ± 2.2 34.3 ± 1.2 0.001
(μmol mol−1)
Leaf nitrogen content (%) H > NH 2.11 ± 0.18 1.69 ± 0.12 0.033
Photosynthetic nitrogen use H < NH 83.0 ± 5.9 181.6 ± 31.1 0.003
efficiency
(μmol CO2 s−1 mol−1 N)
We specified the predictions in comparison between growth forms to allow one-tailed significance
testing. P-values smaller than 0.05 are shown in bold face (Modified from Hao et al. 2011)

met by Hs with intrinsically low xylem water transport efficiency. Effective

stomatal closure in Hs may thus be important in avoiding too large of a water
potential gradient across the plant and hence catastrophic hydraulic failure.
The Hs do not only have earlier stomatal closure in response to leaf desiccation
but also exhibit more effective water retaining ability after stomata closure (Fig. 5a,
b). Average cuticle conductances are 2.1 and 10.7 mmol m−2 s−1 in Hs and NHs
(P < 0.05, t-test), respectively. Consequently, after excision Hs can keep their
relative water content above 70 %, a threshold for physiological damage to occur in
many higher plants, for a period on average 10 times that of the NHs. This may
confer Hs a greater ability to persist under severe drought. Leaf desiccation
12 G.-Y. Hao et al.

Fig. 4 Safety margin measured as the difference between leaf water potential at 50 % of
maximum stomatal conductance (Ψgs50 %) and leaf osmotic potential at turgor loss (π0) in five
hemiepiphytic and five non-hemiepiphytic Ficus species. Species name abbreviations are as in
Fig. 2

Fig. 5 a Relative water content (RWC) changes of water-saturated leaves during bench drying
after excision (n = 6). The horizontal dashed line marks 70 % RWC. Ficus benjamina (▲), F.
concinna (▼), F. curtipes (■), F. religosa (◆), F. tinctoria ( ), F. auriculata (○), F.
esquiroliana (▽), F. hispida (◇), F. racemosa ( ), F. semicordata (☆); b leaf epidermal
conductance. Species name abbreviations are as in Fig. 2 (data from Hao et al. 2010)

avoidance is determined by both the stomatal closure in response to water deficits

and water retention after stomata closure, which relates to the resistance to water
loss through the epidermal cuticle (Muchow and Sinclair 1989; Holbrook and Putz
1996c). Differences in stomatal control and cuticle conductance may explain the
commonly observed leaf wilting and plant dieback in NHs but not in Hs under
drought stress both in the field and during drought treatments in pots. The NHs on
Hemiepiphytic Trees: Ficus as a Model System … 13

Fig. 6 Percentage of leaf loss

due to simultaneous drought
treatments of the same
degrees to seedlings of
hemiepiphytic and
non-hemiepiphytic Ficus
species grown under (a) full
sunlight and (b) 5 % sunlight
(Hao et al. 2013)

average lost 30 and 70 % of their leaves during a water withholding experiment,

whereas Hs did not shed a substantial amount of leaves for a similar degree of
drought except in F. tinctoria under full daylight (Fig. 6a, b).
When photosynthetic net assimilation rates are plotted against stomatal con-
ductance following a drought treatment in potted plants, contrastingly different
patterns are seen between Hs and NHs. The Hs appear to have higher net assimi-
lation rate for a given stomatal conductance (Fig. 7a, b). Furthermore, the Hs show
a substantial increase in water use efficiency in response to the drought stress, as
shown by the increase in the slopes of the fitted curves, indicating physiological
adjustments towards a more efficient water use under drought, whereas this
adjustment is lacking in NHs (Fig. 7a, b).
14 G.-Y. Hao et al.

Fig. 7 Leaf net assimilation

rate (An) vs. stomatal
conductance (gs) following a
drought treatment in plants
grown under (a) full sunlight
and (b) 5 % sunlight.
Symbols for each species are
as in Fig. 3

Contrasting Water Use Strategies in Hs and NHs

Although conservative water use in Hs contributes to their ability to survive

drought-stressed environments typical of epiphytic habitats during their early
ontogeny, it negatively affects their photosynthetic carbon assimilation. While
light-saturated net CO2 assimilation rates per unit leaf area do not differ between the
two growth forms, assimilation rates per dry mass are significantly lower in Hs
(Table 1). The Hs also have lower photosynthetic nitrogen and phosphorous use
efficiencies than NHs (Hao et al. 2011). Differences between Hs and NHs extend
the finding that species adapted to different environments tend to differ in a cluster
of water flux-related traits, including stem hydraulic conductivity, leaf hydraulic
conductance and stomatal conductance (Sack et al. 2003, 2005; Dunbar-Co et al.
2009). These traits probably contribute to NHs having a higher photosynthetic
capacity per investment in leaf dry mass and a higher growth capacity.
The contrasts between Hs and NHs in maximum flux-related traits and drought
tolerance traits are consistent with the hypothesized trade-off between high
Hemiepiphytic Trees: Ficus as a Model System … 15

hydraulic conductivity and high resistance to hydraulic failure (e.g.

Martinez-Vilalta et al. 2002; Wheeler et al. 2005). Such a trade-off may affect the
distribution of species; species distributed in relatively wet environments are usu-
ally more vulnerable to xylem cavitation than species adapted to dry environments
(Maherali et al. 2004). The divergences in hydraulics between Hs and NHs are
analogous to the differences between xeric and humid-grown species (Bhaskar et al.
2007), indicating that sympatric species within a single genus, can diverge sig-
nificantly in numerous aspects of leaf structure and function, according to their
microhabitat for regeneration. The Hs have leaf traits conferring conservative water
use, of particular advantage to plants growing under dry conditions, whereas the
NHs exhibit leaf traits conferring prodigal water use that would be advantageous
under competitive situations.
It seems that the existence of an epiphytic habit during the juvenile stage in Hs
involves a suite of leaf water flux and drought tolerance traits that are different from
those of congeneric NHs. In Hs, an epiphytic growth stage that is frequently
exposed to water deficits appears to have selected for xylem composed of smaller
vessels with lower hydraulic transport efficiency, which carries on to the terrestrial
growth stage. These divergences between Hs and NHs persist to a large degree in
mature trees that have similar root water access.

Comparison of Adaptations to Irradiance Level

Light is a critical factor affecting the regeneration of forest plants especially in the
tropics (Chazdon 1988; Clark et al. 1996). Many tropical forest species have
evolved epiphytic growth habits that are thought to allow escape from the very low
irradiance level in the forest understory. Hemiepiphytism is commonly hypothe-
sized as an adaptation to exploit the higher irradiance in the forest canopy
(Dobzhansky and Murea-Pires 1954; Ramirez 1977; Putz and Holbrook 1986;
Laman 1995; Williams-Linera and Lawton 1995). One way to test this hypothesis is
by comparing closely related hemiepiphytic and non-hemiepiphytic species in their
functional traits related to shade tolerance and their ecophysiological responses to
growth irradiance levels. Seeds of both Hs and NHs species were sown at the same
time and later grown under four irradiance levels (100, 50, 25 and 5 % sunlight).
Different from the expectation of a conventional “light” hypothesis for hemiepi-
phytism evolution, our results show that differences in light requirement or shade
tolerance may not be the major divergence between Hs and NHs in determining
their environmental adaptation in tropical rainforests.
16 G.-Y. Hao et al.

Plastic Response to Growth Irradiance Levels

Seedlings of Hs and NHs species do not show contrasting photosynthetic responses

to irradiance as found in light-demanding and shade-tolerant species. Under full sun
and sufficient water supply, both Hs and NHs have photosynthetic rates comparable
to seedlings of typical light-demanding pioneer tree species (e.g. Oberbauer and
Strain 1984; Turnbull 1991; Davies 1998). The Hs species even show lower
average photosynthetic rates than NHs, which is opposite from what is expected if
Hs were better adapted to higher irradiance for regeneration. It has also been shown
that early-successional or pioneer species that are light demanding during regen-
eration have high plasticity in physiological traits in response to growth irradiance
(Bazzaz and Pickett 1980). However, such a contrast in plasticity to light is lacking
in the two groups of Ficus. The high plasticity to changes in both Hs and NHs traits
under different growth irradiance may thus indicate that both groups of Ficus
species are adapted to relatively high irradiance for regeneration.
Species that are more shade tolerant are expected to allocate more biomass to
leaves to gain maximum light and CO2 capture with a larger leaf area (Poorter 1999,
2001; Markesteijn et al. 2007). Moreover, plants in the shade tend to have a taller
stem per unit stem biomass to escape from low irradiance in the understory (Sasaki
and Mori 1981). Such a plastic response is substantial in light demanding species
regenerating in gaps (Bazzaz 1979; Bazzaz and Pickett 1980; Bazzaz and Wayne
1994). However, neither obvious differences in allometry nor differences in stem
height growth plasticity in response to growth irradiance have been found between
Hs and NHs (Hao et al. 2013). Both types of Ficus seedlings show a high degree of
plasticity in stem growth with height to mass ratio becoming substantially higher
under low irradiance, indicating acclimation for enhancing light capture. Although
Hs have substantially higher height to mass ratio than NHs under all light treat-
ments, this difference may not suggest adaptation to higher irradiance in Hs, but
rather a lower requirement for physical support of stems compared to NHs. The Hs
use host trees for support especially at the early stages of the life cycle and thus
thick and strong stems or branches are not required from a biomechanical point of
view.

Seedling Growth Rate

The Ficus species all have tiny seeds and initial small seedlings and thus a rapid
initial growth would be critical to them if regenerating terrestrially since tiny
seedlings are highly susceptible to risks when growing on the forest floor, such as
coverage by falling debris and shading by other fast growing plants. Larger seed-
lings in forest gaps are more likely to survive and eventually reach the canopy
(Brown and Whitmore 1992; Boot 1996; Zagt and Werger 1998). By growing in the
canopy, however, Hs seedlings can largely avoid these terrestrial risks and thus
Hemiepiphytic Trees: Ficus as a Model System … 17

surviving environmental stresses experienced at the epiphytic stage (e.g. low water
availability) would be more important than fast growth and greater competitiveness.
Despite the huge amount of seed production and numerous dispersers, hemiepi-
phytic fig trees do not appear to saturate potential epiphytic micro-sites (Laman
1996a). Ficus population densities may be limited by both biotic and abiotic factors
reducing early recruitment success (Laman 1995). In a stand of tropical dry forest of
Australia, about 95 % of all juvenile individuals of F. macrophylla and F. superba
do not proceed to the strangling phase of the life cycle (Doyle 2000). The struggle
to succeed under strong interspecific competition in NHs seedlings may have
shifted to a struggle to survive the harsh abiotic stresses in Hs, with selection
against a fast growth rate associated with prodigal resource use.
Seedlings of Hs show consistently lower growth rates than those of NHs ger-
minated at the same time under all four irradiance levels, with NHs seedlings
having 3.3 and 13.3-fold greater height and biomass, respectively, at the end of a
five-month growth period (Fig. 8; Hao et al. 2013). The substantially higher growth
rates and larger seedling sizes in NHs during the first few months may be critical for
their success, considering that small seedlings at initial stages of the life cycle are

Fig. 8 Seedlings of hemiepiphytic (upper panels) and non-hemiepiphytic (lower panels) Ficus
species growing in the nursery in XTBG. Seeds of all species were germinated at the same time in
petri dishes in an illuminated growth chamber and then transplanted at the same time to pots
18 G.-Y. Hao et al.

expected to be most vulnerable to the risks of terrestrial regeneration. The difference

in seedling biomass between the two growth forms, however, decreases as the
plants grow older. This is likely related to longer leaf lifespans in Hs seedlings,
which allow them to gain an increasingly higher leaf area ratio and leaf mass
fraction over time relative to NHs. Despite this, 1-year old Hs saplings still have
considerably smaller plant biomass than those of NHs (Hao et al. 2013).
It seems that contrasting “strategies” have evolved in two growth forms of Ficus
that are crucial for avoiding high risks during regeneration due to their tiny seed
sizes: (1) slow growing epiphytic form that escapes the terrestrial related risks at the
cost of low water availability, and (2) fast growing terrestrial form that gains a
relatively large size in a short period to avoid those risks. Correspondingly, con-
servative and prodigal water uses appear to have been selected in these two forms of
Ficus species, which are natively associated with contrasting photosynthetic char-
acteristics and responses to drought. Strong drought tolerance in Hs enables them to
regenerate in the drought-prone canopy of dense forests independent of gap for-
mation despite their many traits of pioneer species, such as tiny seed sizes. But such
an adaptation is at the cost of a strong competitiveness required for many terres-
trially regenerating species.
This finding suggests that light may have played a less important role in driving
the adaptive divergence between the two groups of Ficus than expected by the
conventional “light” hypothesis, whereas naturally contrasting water availability in
the juvenile stage likely exerted the strongest selective pressure in shaping distinct
physiology of hemiepiphytic and non-hemiepiphytic Ficus. The NHs usually
regenerate in forest gaps or edges and are most commonly found in forests of early
successional stages. In contrasts, the Hs can occupy different microhabitats along
the vertical environmental gradient in forest canopies of later succession, depending
on the species’ ability to reach and survive the potential regeneration sites on their
host trees (Laman 1996b). Such divergences may have set one of the most
important foundations for different adaptations between these closely related spe-
cies, which contributes to the high diversity of this tropical genus (Table 2).

Hemiepiphytism and Ficus Regeneration in Tropical

Forests

The Ficus genus has evolved to encompass a variety of species with different life
histories including hemiepiphytes and non-hemiepiphytic tree species, but this
genus as a group possesses typical traits of pioneer species—very small seeds, high
fecundity, high photosynthetic rates and growth rates (Harrison 2005). For example,
mature trees of neotropical Ficus, including species of both functional groups,
appear to be light demanding and have high photosynthetic rates compared to other
tree species. The photosynthetic rate of a freestanding species, Ficus insipida Willd.
Hemiepiphytic Trees: Ficus as a Model System … 19

Table 2 Presence (+) or absence of epiphytic phase and aerial roots, growth form and leaf texture
of Ficus species that naturally occur in Xishuangbanna, China
Species name Epiphytic Adult Aerial Leaf texture
phase growth roots
form
Ficus abelii shrub papery
F. altissima + large tree + leathery
F. annulata + large tree + thinly leathery
F. asperiuscula shrub thinly leathery
F. auriculata small tree + thickly papery
F. benjamina + tree + thinly leathery
F. benjamina var. nuda + tree + thinly leathery
F. callosa + large tree thickly
leathery
F. caulocarpa tree thinly leathery
F. chapaensis small tree papery
F. chrysocarpa small tree papery
F. concinna + large tree + leathery
F. concinna var. subsessilis + large tree + leathery
F. curtipes + tree + thickly
leathery
F. cyrtophylla small tree papery
F. drupacea small tree + leathery
F. esquiroliana tree papery
F. fistulosa small tree + papery
F. gasparriniana var. lacerate-folia shrub thinly leathery
F. gasparrinana var. viridescens shrub thinly leathery
F. glaberrima tree + thinly leathery
F. glaberrima var. pubescens tree + thinly leathery
F. hederacea + liana + thickly
leathery
F. heterophylla shrub papery
F. hirta + shrub papery
F. hirta var. brevipila shrub papery
F. hirta var. imberbis shrub papery
F. hirta var. roxburghii shrub papery
F. hispida tree papery
F. hookeri large tree leathery
F. ischnopoda shrub papery
F. kurzii large tree thinly leathery
F. laevis + liana papery
F. langkokensis + small tree papery
F. maclellandii + tree leathery
(continued)
20 G.-Y. Hao et al.

Table 2 (continued)
Species name Epiphytic Adult Aerial Leaf texture
phase growth roots
form
F. macleliandi var. + tree leathery
rhododendrifolia
F. microcarpa + tree + thinly leathery
F. neriifolia small tree papery
F. nervosa tree leathery
F. oligodon tree papery
F. orthoneura tree leathery
F. pisocarpa + tree leathery
F. pubigera liana leathery
F. pubigera var. anserine small tree leathery
F. pubigera var. maliformis small tree leathery
F. pubigera var. reticulate small tree leathery
F. pyrformis shrub leathery
F. racemosa large tree + thinly leathery
F. racemosa var. miquelli large tree + thinly leathery
F. religiosa + large tree + leathery
F. sagittata + tree + leathery
F. sarmentosa var. lacrymens liana + leathery
F. semicordata small tree papery
F. squamosa shrub papery
F. stenophylla shrub papery
F. stricta + tree + thinly leathery
F. subincisa shrub papery
F.subinicisa var. paucidentata shrub papery
F. subulata + small tree + papery
F. superba var. japonica small tree + papery
F. tinctoria ssp. Gibbosa + tree + leathery
F. tinctoria ssp. Parasatica + tree + thinly leathery
F. variegata var. chlorocarpa tree papery
F. variolosa small tree leathery
F. vasculosa small tree + leathery
F. virens + large tree + leathery
F. virens var. sublanceolata + large tree + leathery
In this region, there are 46 Ficus species that naturally occur in the forests as well as two
subspecies and 19 varieties. Among the 67 Ficus taxa, the 48 tree species, including 23
hemiepiphytic and 25 non-hemiepiphytic tree species are most important to the local ecosystem in
terms of abundance and dominance (Adapted from Zhu et al. 1996)
Hemiepiphytic Trees: Ficus as a Model System … 21

(33.1 μmol m−2 s−1) was found to be among the highest of any C3 trees measured
under natural conditions (Zotz et al. 1995).
The similarities in responses to growth irradiance between Hs and NHs seedlings
found by growth experiments do not support the conventional hypothesis that the
hemiepiphytic habit is an adaptation to exploit higher light environment of the
canopy (Hao et al. 2013). In tropical forests, besides the vertical irradiance change
in light intensity there are also considerable horizontal variations with much higher
irradiance in gaps compared to forest understory (e.g. Nicotra et al. 1999). In
relatively large gaps, pioneer or light-demanding tree species with higher relative
growth rates and ecophysiological plasticity have competitive advantages over
shade tolerant tree species (Denslow 1980). The seedlings of most NHs are not
found in deep shade in the understory but rather in forest gaps or clearings with
relatively strong irradiance; Hs seedlings and saplings on host trees are usually
partially shaded by the host canopy before extending to high irradiance. Thus, in
their natural habitats, the light conditions for seedlings of Ficus species of the two
growth forms may not be very different, consistent with their lack of contrasting
adaptations in physiology and morphology with respect to light requirements.
The epiphytic growth habit of Hs during early life stages may mainly be an
adaptation to avoid risks related to the initial forest floor growth, such as strong
interspecific competition, flooding, terrestrial herbivores and damage or coverage
by falling debris. These risks are common for terrestrial regenerating plants in
tropical forests (Holbrook and Putz 1996a), but may be especially high for Ficus
considering their tiny seeds and small size of young seedlings. To minimize these
risks, two contrasting types of life history traits have been selected for in Ficus—
terrestrial regeneration in gaps with an initial burst of growth to rapidly gain rel-
atively large seedling sizes (NHs) and epiphytic regeneration with slow growth but
enhanced ability for tolerating drought-prone canopy environments (Hs).
By having epiphytic growth during their early life stage, Hs seedlings can
establish in the canopy of dense tropical rainforests (Harrison et al. 2003). Thus the
regeneration of Hs does not heavily depend on forest gap formation as most late
successional species do. The high diversity and abundance of hemiepiphytic Ficus
species may thus be attributable, at least in part, to their canopy regeneration habit,
which permits these species to inhabit late succesional forests despite their many
traits of typical pioneer species (e.g. small seed sizes). In contrast, the regeneration
of non-hemiepiphytic species in dense rainforests depends on the formation of
forest gaps; for these species a high xylem water transport efficiency would enable
relatively high rates of carbon assimilation and growth rates and consequently
greater competitiveness in resource acquisition, given a reliable water supply and
favorable irradiance levels (Brodribb et al. 2002, 2005; Santiago et al. 2004a, b;
Campanello et al. 2008; Zhang and Cao 2009). In this sense, the divergence in
growth form and hence ecophysiological traits between hemiepiphytic and
non-hemiepiphytic Ficus species may have contributed to species co-existence and
the diversification of this genus in tropical rainforests.
22 G.-Y. Hao et al.

Acknowledgements GYH thanks colleagues past and present for their support and encourage-
ment. This work was made possible by a joint fellowship granted to GYH by XTBG and
University of Miami supporting oversea graduate studies. This work is partially supported by a
100-talents research grant from the Chinese Academy of Sciences awarded to GYH.

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Ecophysiology and Crassulacean Acid
Metabolism of Tropical Epiphytes

Katia Silvera and Eloisa Lasso

Abstract Epiphytes are plants that germinate and grow upon other plants without
contact with mineral soil and without parasitizing their host plant. Therefore, they
derive nutrients and water from the environment. Epiphytes are primarily tropical in
distribution and may be the most species-rich life form in very wet rainforest sites,
constituting about 10 % of all vascular plants. Nearly 80 % of all vascular epiphytes
belong to one of three families: Orchidaceae (orchids), Bromeliaceae (bromeliads),
and Polypodiaceae (ferns). Orchids in particular, are the most species rich in epi-
phytes. In this review, information on the ecophysiology of vascular epiphytes is
presented, in an attempt to find patterns that explain the ecophysiological adapta-
tions of canopy living. We highlight the ecophysiology of orchids and bromeliads,
and whenever possible, provide insight into other epiphytic families. We discuss
morphological, anatomical and physiological novelties that epiphytes have evolved
to face the challenges of living in the canopy, including adaptations to increase
water capture, to facilitate water storage or to reduce water loss. Because epiphytes
are particularly susceptible to climate change, and can be monitored as a component
of forest health, we also consider their distribution and physiological responses to
climate change as a key aspect of conservation programs.

Keywords Epiphytes Crassulacean acid metabolism (CAM)
Bromeliaceae



Orchidaceae Conservation

K. Silvera (&)
E. Lasso

Smithsonian Tropical Research Institute, P.O. Box 0843-03092, Balboa, Ancón,
Republic of Panama
e-mail: katia.silvera@ucr.edu
E. Lasso
e-mail: e.lasso@uniandes.edu.co
K. Silvera
Department of Botany and Plant Sciences, University of California Riverside, Riverside,
CA 92521, USA
E. Lasso
Departamento de Ciencias Biológicas, Universidad de Los Andes, Bogotá, Colombia

© Springer International Publishing Switzerland 2016 25

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_2
26 K. Silvera and E. Lasso

Introduction

Epiphytes are plants that germinate and grow all or most of their lives attached to
other plants without contact with mineral soil (Benzing 1990), and can grow
attached to trunks or branches of host tress and shrubs from the understory floor all
the way to tree crowns. Unlike mistletoes, epiphytes do not parasite their hosts, and
instead take nutrients and water from the environment (Benzing 1990). They occur
on the branches of trees in many biomes, but vascular epiphytes are particularly
abundant in tropical forests and can grow so profusely that they substantially
increase the mass that tropical tree branches must support (Fig. 1a; Niklas, this
volume); epiphytic biomass can be as much as 50 % of the tree leaf biomass (Lüttge
1989), especially in primary montane forests (Nadkarni et al. 2004). In tropical
forests, epiphytes form conspicuous masses that are known to support large
amounts of animal life including ant nests, arthropods and amphibians (Stuntz et al.
2002), in addition to contributing to the hydrology and nutrient cycling of the
ecosystem.
The diversity of epiphytes in tropical forest canopies is also astonishing, con-
stituting about 10 % of all vascular plants. Epiphytes are a conspicuous element of
humid tropical forests and may be the most species-rich life form in very wet
rainforest sites (Gentry and Dodson 1987). Within this diversity, there are simi-
larities between different species of epiphytes and certain characteristics that are
particular to the epiphytic syndrome allowing these species to live in the canopy.
With few exceptions, epiphyte species are generally long-lived perennials, have
small body size, tend to have small seeds that can be dispersed by wind, and have
relatively slow growth. Wind-dispersed seeds allow epiphytes to colonize new trees
rapidly. To face the challenges of access to water supply and nutrients, many
epiphytes have evolved several morphological adaptions such as leaf succulence,
water absorbing trichomes and presence of water absorbing spongy tissue (Benzing
1990; Hietz et al. 1999). Thus the particular growth form and habitat of epiphytes
leads to certain physiological outcomes, especially in vascular epiphytes, that
appear to facilitate their proclivity for growth in tropical forest canopies.
In this review, information on the ecophysiology of epiphytes is presented, with
emphasis on vascular epiphyte literature, in an attempt to find patterns that explain
the ecophysiological adaptions of living in the canopy. We emphasize vascular
epiphytes because they are the most conspicuous and unique forms of epiphytes in
tropical forest, and are particularly abundant in the tropics compared to temperate
and boreal forests where non-vascular epiphytes prevail. We also constrain our
discussion to epiphytes that germinate in the canopy (Fig. 1a, sometimes called
primary epiphytes), and do not consider “nomadic vines”, which refer to climbing
plants that germinate on the ground and later become epiphytes by losing contact
with the ground while climbing host plants (Hao, this volume; Zotz 2013a). Nearly
80 % of all vascular epiphytes belong to one of three families: Orchidaceae (orchids),
Ecophysiology and Crassulacean Acid Metabolism … 27

Fig. 1 Epiphytic
communities from tropical
rainforests. a Epiphytic
community of bromeliads and
orchids in a tropical montane
cloud forest of Panama. Photo
by Gaspar Silvera.
b Anthurium and
Phylodendron epiphytes in a
seasonal tropical forest of
Panama. Photo by Gaspar
Silvera. c Orchid epiphyte in a
seasonal lowland forest of
Panama. Photo by Katia
Silvera
28 K. Silvera and E. Lasso

Bromeliaceae (bromeliads), and Polypodiaceae (ferns), and about 85 % of these are

orchids and 8 % are bromeliads (Zotz 2013b). Thus, the ecophysiology of orchids
and bromeliads will be the main focus of this review, and whenever possible, we will
provide insight into other epiphytic families. We will discuss morphological,
anatomical and physiological novelties that epiphytes have evolved to face the
challenges of living in the canopy. Because epiphytes are particularly susceptible to
climate change, and can be monitored as a component of forest health, we also
consider their distribution and physiological responses to climate change as a key
aspect of conservation programs.

Taxonomic and Ecological Distribution of Epiphytes

Vascular epiphytes are present in 27,614 species, 913 genera and 73 families (Zotz
2013b), and are found worldwide in almost all kinds of ecosystems, especially in
tropical and subtropical regions. The real diversity, however, is in tropical rain-
forests and cloud forests where they can represent more than 50 % of the total
vascular flora of plant species in a given area (Benzing 1990; Gentry and Dodson
1987). Neotropical montane forests, in particular, are exceptionally rich in epi-
phytes (Benzing 1989, 1990).
Microclimatic gradients within the canopy of individual host trees provide a
variety of niches that can be exploited by different species (Hietz and Briones
1998). Distribution of epiphytes varies greatly within different forests, and has
distinct patterns both across environmental gradients, as well as vertically within
host tress. To understand the distribution of epiphytes, Burns and Zotz (2010)
proposed examining epiphyte assemblages that form different meta-communities as
species interaction networks between epiphytes and their host tree. In “classical”
meta-communities, epiphytes are restricted to the canopy and are referred to as
obligate epiphytes, as in the case of orchids and bromeliads of tropical regions.
These meta-communities of epiphytes from different host trees are then linked
together by seed dispersal. This differs from temperate zones, where epiphytes are
composed of species that can live on the forest floor and occasionally grow as
epiphytes.
Distribution of epiphytes also varies horizontally, and this variation occurs
between different host trees and among different forest types. Studies that address
species composition along altitudinal gradients have revealed that species richness
patterns are influenced by the mid-domain-effect (Cardelús et al. 2006), a peak of
abundance at mid-elevation. A study focusing on the distribution of CAM in
orchids of Panama and Costa Rica found that species richness was highest at sites
between 1,000 to 1,500 m altitude, consistent with a peak of abundance at
mid-elevation known as the “mid-altitudinal bulge” (Silvera et al. 2009). Almost all
epiphytic taxa show hump-shaped curves of distribution with altitude, but their
Ecophysiology and Crassulacean Acid Metabolism … 29

relative contributions change with elevation (Cardelús et al. 2006; Krömer et al.
2005). The mechanism behind this distribution has been explained by the inter-
action between temperature and water gradients caused by increasing altitude (Peet
1978; Silvera et al. 2009; Whittaker and Niering 1975). Mid elevation sites of
around 1,000 m in tropical forests commonly have the highest incidence of cloud
cover.
Vertical stratification of epiphytes in tropical forests has been linked to physi-
ological strategies related to microclimate constraints (Graham and Andrade 2004;
Reyes-Garcia et al. 2008). Vertical distribution of epiphytes is influenced by eco-
physiological adaptations, such as the ability to acclimate to varying levels of
photon flux density (PFD) and humidity (Benzing 1990). For example, species of
Phylodendron tend to clump at lower sites within branches or trunks of host trees
(Fig. 1b) where humidity levels are higher and PFD levels are lower, and because
part of the life cycle may be dependent on nutrient uptake from roots that are in
contact with mineral soil (Putz and Holbrook 1986). On the other hand, epiphytic
species that utilize Crassulacean Acid Metabolism (CAM), a water-saving mode of
photosynthesis (Ting 1985), tend to clump in areas of higher PFD and exposed sites
within branches of the host tree. For example, a study of vertical stratification of
epiphytes in a lowland forest of Panama found that >50 % of all epiphytes clustered
at intermediate canopy heights (Zotz and Schultz 2008). In a lowland forest of
central Panama, the percentage of CAM epiphytes increases with canopy height
(Fig. 2; Zotz and Ziegler 1997). In a lowland forest of the Atlantic slope of Panama,
total biomass was largest at intermediate heights within the forest, but the relative
contribution of CAM species was higher in the upper canopy (Zotz 2004). In
another study by Hietz et al. (1999) the proportion of epiphytic species showing
CAM decreased with increasing elevation and precipitation along an altitudinal
gradient from tropical dry forest to humid montane forest of eastern Mexico.

Fig. 2 Proportion of
epiphytic CAM species in
different strata of a lowland
forest of Central Panama. The
percentage of CAM epiphytes
increases with canopy height.
Percent CAM species was
extrapolated from published
work (Zotz and Ziegler 1997)
30 K. Silvera and E. Lasso

Physiological Adaptations of Epiphytes

There are also numerous ecophysiological adaptations that appear to contribute to

epiphyte success in the canopy. Epiphytes often grow in the canopies of very wet
tropical forests, with abundant precipitation and high soil water availability, but
even in such humid forests, the canopy can dry out quickly and therefore has been
described as “the desert in the rainforest”. Many epiphytic species use CAM, one of
three metabolic pathways found in vascular plants for the assimilation of atmo-
spheric CO2. CAM plants take up CO2 from the atmosphere predominantly at night,
improving the ability of plants to acquire carbon in water-limited and CO2-limited
environments (Winter and Smith 1996a). Thick leaf cuticles are also observed in
many epiphyte species. Many epiphytic species also exhibit less negative osmotic
potential compared to their terrestrial congeners (Hao et al., this volume), consistent
with careful management of internal water resources. Finally, varying degrees of
tolerance to shade and desiccation have been observed in epiphytes compared to
related terrestrial species. These characteristics allow epiphytes to survive long
periods of drought stress, especially in tropical forests with prolonged dry seasons.

Why not Rooting in Soil Leads to Certain Physiologies

The epiphytic habitat represents a highly dynamic environment, subject to temporal

and spatial variations in light, nutrient and water supply. Among these abiotic
factors, sporadic or seasonal periods of water shortage are perhaps some of the most
common challenges even for epiphytes occurring in humid tropics (Zotz and
Thomas 1999). Epiphytes do not take water or nutrients from the host plants. The
vast majority of epiphytic plants do not have contact with mineral soil, and
therefore must obtain nutrients and water from the microenvironment where they
live. Because water availability is a limiting factor for growth and survival of
epiphytic species living in the canopy (Lüttge 1989; Zotz and Hietz 2001), and
represents a strong selective pressure, epiphytes have evolved myriad physiological
and morphological adaptations (Benzing 1990; Hietz et al. 1999), in addition to
acquiring necessary nutrients from debris or organic soil from the canopy. These
adaptations can be divided into adaptations to increase water capture, to facilitate
water storage or to reduce water loss.
To maximize water uptake from rain pulses, dew, or moisture in the air and to
survive long periods of drought stress, especially in tropical forests with prolonged
dry seasons (Benzing 1990; Hietz et al. 1999), epiphytes have evolved specialized
absorptive tissues and organs, and a diversity of growth forms. Bromeliads, for
example, possess specialized absorptive trichomes—a key innovation associated
with the transition from terrestrial to epiphytic life form (Crayn et al. 2004). In
orchids, the functional equivalent to bromeliad trichomes is the “velamen”, a
Ecophysiology and Crassulacean Acid Metabolism … 31

multilayered spongy epidermis that allows orchids to absorb atmospheric moisture

and nutrients through the roots (Benzing 1987).
Adaptations related to water storage include leaf succulence, composed of
abundant hydrenchyma, an enlarged specialized spongy tissue that allows plants to
store water. Often hydrenchyma is the main reservoir for maintaining a stable water
status in photosynthetic tissues (Freschi et al. 2010). A thick leaf cuticle, on the
other hand, is thought to minimize cuticle conductance and therefore water loss
during dry periods. A study of 15 vascular epiphytic species evaluated for water
permeability of astomatous isolated cuticular membranes showed a lower leaf
cuticular permeability to water in comparison to terrestrial forms (Helbsing et al.
2000). Additionally, epiphytes tend to have lower stomatal densities compared to
terrestrial plants, thus reducing water loss. Stomatal density can vary from 1–30
stomata/mm2 in some bromeliads (Martin 1994) to 30–62 stomata/mm2 in aroids
(Lorenzo et al. 2010), to more than 180 stomata/mm2 in epiphytic Clusia species
(Holbrook and Putz 1996). In terrestrial plants, stomata densities can reach 600
stomata/mm2 (Larcher 2003). Finally, many epiphytic species utilize CAM. This
metabolic pathway is present in *19 % of epiphytic species in a lowland forest
(Zotz 2004), *50 % of tropical epiphytic orchid species (Silvera et al. 2005;
Winter and Smith 1996b) and approximately 25–38 % of epiphytic bromeliad
species (data estimated from Zotz 2004 and Crayn et al. 2004). Many epiphytic
species use combinations of these adaptive traits, which allow them to tolerate
limited water supply in the canopy. Below we highlight key adaptations from two
of the largest epiphytic plant families: Orchidaceae and Bromeliaceae, and sum-
marize generalities found in other epiphytic families.

Epiphytic Orchids

Of all epiphytic families, the Orchidaceae has been the most successful in colo-
nizing tree crowns and exposed sites (Fig. 1c). One important characteristic that
allows epiphytic orchids to colonize the canopy is the presence of roots that serve
several key functions. Orchid roots have the capability of photosynthesizing due to
presence of chlorophyll, orchids roots are surrounded by spongy velamen that
serves to quickly absorb and accumulate water and nutrients, and orchid roots
enable the plant to anchor itself securely in branches, thus providing mechanical
protection and stability (Benzing 1990). Orchids also use a different strategy during
the dry season by having access to stored water and nutrients from the pseudobulb,
a storage organ derived from a thickening of the stem between leaf nodes. Orchids
generally have long-lived thicker leaves with lower photosynthetic capacity per unit
area compared to ferns and bromeliads (Cardelús and Mack 2010). Although thick
leaves in orchids are typically associated with δ13C values in the CAM range, some
thin-leaved orchids are also capable of CAM photosynthesis, as demonstrated by
acid titration (Silvera et al. 2005).
32 K. Silvera and E. Lasso

CAM Photosynthesis in Epiphytic Orchids

In contrast to C3 and C4 plants, CAM has evolved multiple independent times

within vascular plants, and is widely distributed throughout semi-arid tropical and
subtropical environments, including epiphytic habitats in tropical regions (Silvera
et al. 2009). Several studies indicate that CAM photosynthesis may be widespread
among tropical epiphytic plants, particularly in the largest family of vascular plants,
the Orchidaceae with approximately 30,000 species (Earnshaw et al. 1987; Silvera
et al. 2009, 2005; Winter et al. 1983). It is estimated that up to 50 % of tropical
epiphytic orchid species exhibit different degrees of CAM (Silvera et al. 2005) with
a gradient of species showing C3 to weak CAM to strong CAM modes. The largest
proportion of CAM epiphytic orchid species are usually distributed at lower alti-
tudinal sites (Silvera et al. 2009). Additionally, the multiple origins of CAM and its
strong positive correlation with epiphytism has been linked to the rapid degree of
speciation in the Orchidaceae (Silvera et al. 2009). This is particularly true within
the Subfamily Epidendroideae, which represents the largest epiphytic clade within
flowering plants (Fig. 3)

Epiphytic Bromeliads

The Bromeliaceae family has approximately 3350 species that cover a wide range
of habitats; from very humid forest to extremely xeric sites, and from lowland sites
to near 5000 m altitude (Crayn et al. 2015). About half of the species are epiphytes.
The epiphytic bromeliads show a morphological progression from tank life forms,
to atmospheric or nebulophyte life forms (Zotz 2013b). The term “nebulophyte” has
been used in the literature to characterize epiphytic bromeliads with long thin leaves
and low leaf succulence, a morphology that maximizes fog-catching (Martorell and
Ezcurra 2007; Reyes-Garcia et al. 2012). Tank species have large rosette type
leaves that are arranged in such way that can hold large amounts of water after rain
events. Tank bromeliads receive nutrient inputs from rain, mist, dust, and nutrient
released from ground-rooted plants through leaching or decomposition, as well as
from remains of animals and/or organic matter (Benzing 1990; Romero et al. 2010)
These “continuously supplied” (Benzing 1990) tank epiphytes tend to have thick
leaf cuticles, high stomatal control, and are more restricted to the upper canopy, all
characteristics that allow them to resist photoinhibition and avoid dessication
(Reyes-Garcia et al. 2012). Species with large tanks, however, can be subjected to
long periods of desiccation. Accumulated water can dry out after 1–2 weeks (Zotz
and Thomas 1999), and thus tank species rely on the ability to switch from C3 to
CAM in order to survive these water shortage episodes (Benzing 2000). The tank
structure or “phytotelmata” can intercept and retain debris and water, and form a
nice microcosm where a diverse community of invertebrate and vertebrate animals
thrive (Benzing 2000). Organism debris living inside of the tank can provide
Ecophysiology and Crassulacean Acid Metabolism … 33

Fig. 3 Cladogram of the relationship among 53 Orchidaceae subtribes. The five orchid
subfamilies are represented on the right side. Presence and absence of CAM were mapped onto the
cladogram showing lineages with CAM in red. The red area within the pie chart indicates relative
support for different ancestor states. This analysis supports the multiple, independent origins of
CAM in the epiphytic Subfamily Epidendroideae
34 K. Silvera and E. Lasso

nutrition to the bromeliad, as shown by experiments with stable isotopes of nitro-

gen. Romero et al. (2010) demonstrated that treefrog feces from Scinax hayii
contributed 27.7 % of the total N to the plant, whereas dead termites contributed
49.6 % of the total N to the plant. They also showed that plants receiving additional
N through frog feces and termites had higher photosynthetic rates compared to
control plants, but only during the rainy season. Epiphyte nutrient availability is
generally less critical than water availability (Laube and Zotz 2003), but can still be
a limiting factor when water is available.
In contrast to tank bromeliads, atmospheric life forms or “pulse supplied” epi-
phytes only have access to water after a precipitation event, and maximize water
absorption through abundant leaf trichomes (Benzing 1990). Atmospheric
bromeliads receive nutrient inputs from dust, mist and rain through dense surface
trichomes. Indeed, the main adaptation of atmospheric bromeliads for living in the
canopy is the presence of specialized trichomes for both minerals and water
absorption (Benzing et al. 1985), especially because bromeliad roots do not engage
in nutrient acquisition nor have mycorrhizal fungi associations (Lesica and Antibus
1990). Trichomes, however, vary in their absorptive capabilities. For example,
some tank bromeliads within the subfamily Tillandsioideae have trichomes capable
of absorbing large organic molecules such as amino acids (Endres and Mercier
2003), and derive nutrients from predator feces and arthropod carcasses living
in their tanks (Romero et al. 2010). Species from the subfamilies Pitcairnioideae
and Bromelioideae have trichomes that absorb smaller molecules.

CAM Photosynthesis in Bromeliad Species

The appearance of CAM is considered one of the key innovations associated with
the transition from terrestrial to epiphytic life form. In Bromeliads, the epiphytic
habit has evolved a minimum of three times (Crayn et al. 2004), and bromeliad
epiphytes show great plasticity in the expression of CAM with a range of
expressions from C3 to facultative CAM to full CAM (Andrade et al. 2007; Griffiths
and Smith 1983). Some species under stress have shown high levels of recycling of
respiratory CO2 via CAM (Martin 1994; Maxwell et al. 1994). Griffiths and Smith
(1983) were able to relate the ecology of different bromeliad species to the
occurrence of CAM and C3 on the island of Trinidad. The authors found that tank
bromeliads, which include light demanding C3 species and CAM species, show a
wide range of distribution across rainfall gradients, but are always found in the
uppermost part of the canopy. The more xerophytic bromeliads all show CAM and
are restricted to sites with the lowest rainfall, whereas the shade-tolerant bromeliads
are all C3 species and are found in a wide geographical range but on sites with high
humidity. This study highlights that it is not possible to distinguish C3 and CAM
bromeliad species based only on their stratification within the forest.
Bromeliads can also be heteroblastic, changing their growth forms during their
lifetime by starting as an atmospheric life form and developing water holding tanks
Ecophysiology and Crassulacean Acid Metabolism … 35

Fig. 4 Bromeliad species Werauhia sintenisii. a Adult or tank form and b juvenile or atmospheric
form of the heteroblastic bromeliad species Werauhia sintenisii. Production of anthocyanins for
photoprotection in the adult form is common in epiphytic bromeliads. Photos by Eloisa Lasso

as adults (Fig. 4, Benzing 2000; Zotz et al. 2011). A study by Beltrán et al. (2013)
demonstrated that heteroblastic species shift anatomically and physiologically from
C3 to CAM during their development to increase the survival of juveniles that are
more susceptible to drought stress given their lack of tank. In other words, species
were able to display features of facultative CAM when exposed to drought stress
irrespective of developmental stage. The only obvious difference between the adult
and the juvenile was the size of the hydrenchyma, in which juveniles presented
thicker hydrenchyma with higher water storage (Beltrán et al. 2013). Zotz et al.
(2011) reported that the juvenile atmospheric form of Werauhia sanguinolenta
showed higher trichome density compared to the adult form. Recent work by
Meisner et al. (2013) reported similar size-related variations when studying the
functional relevance of water storage tissue, stomata and trichome densities, and
transpiration and nutrient uptake rates in seventeen homoblastic and heteroblastic
species from Panama, thus questioning the functional relevance of heteroblasty in
bromeliads.

Epiphytic Ferns and Aroids

Few species of epiphytic ferns have been studied regarding their adaptation to water
scarcity. Even in humid cloud forest, fern species have xeric adaptations including
coriaceous leaves, low rates of water loss, leaf scales and high cell wall elasticity.
Some ferns species are poikilohydric, and can tolerate high water deficit and
recover without any physiological damage (Hietz and Briones 1998), whereas
others display a variety of strategies for coping with the xeric conditions in the tree
crown, including succulence of leaves and rhizomes, early closure of stomata upon
water loss, osmotic adjustment, low rates of cuticular water loss, water-absorbing
leaf scales and low cell-wall elasticity (Hietz and Briones 1998). Fern distribution
36 K. Silvera and E. Lasso

in the canopy is correlated with the relative water content at which stomata close,
leaf thickness, and stomatal density and size (Hietz and Briones 1998).
Canopy species of Anthurium and Philodendron present morpho-physiological
adaptations to the canopy environment, such as litter-trap growth, thick cuticles,
and ramification (Jacome et al. 2004). Ontogenetic and size-related changes in
anatomy and ecophysiology relate to performance and survival of Anthurium
scandens epiphytes in the field (Lorenzo et al. 2010). For example, stomatal con-
ductance did not change with ontogenetic phase and was highly dependent on water
availability at the root level. Nevertheless, adult epiphytes had lower epidermal
conductance to water loss as well as higher values of leaf succulence and sclero-
phylly, and showed higher retranslocation rates of leaf nitrogen during senescence,
all traits that confer higher resistance to low resources in comparison to seedlings
living in the shaded humid understory (Lorenzo et al. 2010).

To CAM or not to CAM? That Is the Question

CAM is an ecophysiological adaptation to water limitation influencing the distri-

bution of plants within their natural environments. One way to predict extinction
threats is to understand the evolutionary history of drought resistance mechanisms
in plants. CAM photosynthesis is one of the best examples of convergent evolution
in vascular plants; estimates report that the CAM pathway is found in approxi-
mately 7 % of vascular plants from 35 families and 343 genera (Holtum et al. 2007;
Silvera et al. 2010; Smith and Winter 1996). It is estimated that over 57 % of all
epiphytes are capable of performing CAM (Benzing 1987; Lüttge 2004). Epiphytes
that utilize different levels of CAM photosynthesis are plastic in their responses to
environmental cues, and with elevated CO2, CAM plants have an average increase
in biomass of 35 % without the downward acclimatization of photosynthesis that is
typically observed in many C3 species (Drennan and Nobel 2000). CAM evolution
is accompanied by a series of anatomical and biochemical modifications from
common C3 photosynthesis that allows CAM species to have a competitive
advantage in drought prone epiphytic habitats (Silvera et al. 2010). As a conse-
quence, CAM species have a higher water use efficiency (WUE) when compared to
C3 species due to reduced amount of water lost per unit carbon assimilated. The
possibility that the habitats and growth potential for selected CAM species may be
favored, relative to C3 species, is important considering currents trends of increased
atmospheric CO2 and associated climate change patterns, along with predicted
increases in arid and semi-arid land area (Cushman and Borland 2002; Yang et al.
2015).
CAM has contributed to the exploitation of epiphytic habitats through mid
elevation tropical humid environments, which is especially true for the Orchidaceae
(Silvera et al. 2009). Studies using leaf carbon isotopic composition (δ13C) of
epiphytic orchids have shown a bimodal distribution with the majority of species
exhibiting values of approximately –28‰, typically associated with the C3
Ecophysiology and Crassulacean Acid Metabolism … 37

pathway, and a second peak of distribution at values around –15‰, which is

associated with strong CAM. The presence of weak CAM, as evidenced by acid
titrations, can also contribute to a second peak of abundance within the C3 pho-
tosynthesis isotopic cluster (Silvera et al. 2005). These data suggest that among
CAM orchids, there may be preferential selection for species to exhibit strong CAM
or weak CAM, rather than intermediate metabolism (Silvera et al. 2005). The role
of weak CAM as an intermediate state between C3 and strong CAM, or as an
evolutionary reservoir for CAM adaptive radiations is an unknown and interesting
question for further studies.

Nutrient Limitation

Even though roots of epiphytes are not in touch with mineral soil, nutrient alter-
ations of mineral soil can have an effect on epiphytic communities by altering the
edaphic factors of soils used by the host trees. Experimental evidence in support of
the hypothesis that epiphytes are nutritionally linked to their host tree is, however,
contradictory to date. Nutritional links between host trees and epiphytes in high
mountain trees are expected to be more nutrient limited than those in lowland
forests (Grubb 1977). Cardelús and Mack (2010) explored epiphytic nutrient status
along an elevation gradient in Costa Rica and found no relationship between foliar
chemistry and elevation for any of the epiphytic groups studied, which included
ferns, orchids and bromeliads. In contrast, a long-term fertilization experiment in
the elfin forest of Puerto Rico showed that nutrient addition to soil stimulated tree
leaf litter production (Walker et al. 1996), and increased nutrient content of litterfall
(Yang et al. 2007), which in turn affected epiphytes growing on those trees.
Epiphytic bromeliads growing on fertilized trees clearly responded to nutrient
augmentation received by their host trees, and accumulated more nutrients in their
vegetative body thus increasing their growth rate, fruit production and lifetime
fitness (Lasso and Ackerman 2013). These studies together with Benner and
Vitousek (2007), and Boelter et al. (2014), suggest that epiphytes are nutrient
limited, and that a nutritional link exists between host trees and their epiphytes. This
may be especially true for tank bromeliads since their impounding leaf rosette traps
litter and leachates from their host trees. However, epiphytes with different nutrient
acquisition mechanisms may not be strongly linked to their host tree. Different
epiphyte groups use diverse nutrient uptake mechanisms, which ultimately provide
an explanation for the coexistence and maintenance of species richness in tropical
forest canopies (Cardelús and Mack 2010).
Vascular epiphytes of lowland tropical forests are nutrient limited, mainly by P
and sometimes by N, or P and N simultaneously (Wanek and Zotz 2011; Zotz and
Asshoff 2010; Zotz and Richter 2006). Epiphytes living in tropical montane cloud
forests are more likely nutrient limited because there is constant input of water and
excessive rain that may wash out nutrients from the tank, leaf surface or even the
layer of canopy soil where epiphytes grow. Additionally, lower temperatures in
38 K. Silvera and E. Lasso

tropical mountain cloud forest reduce decomposition rate, potentially decreasing the
release of nutrients from canopy soil. Benner and Vitousek (2007) documented a
dramatic increase in the abundance and species richness of canopy epiphytes in a
forest fertilized annually with phosphorus (P) for 15 years, but found no response in
forest fertilized with nitrogen (N) or other nutrients, suggesting that P is also the
main limitation in highland forests. Studies of two bromeliad species, Werauhia
sanguinolenta from the lowlands of Panama (Zotz and Richter 2006) and Werauhia
sintenissi from the cloud mountain forest in Puerto Rico (Lasso and Ackerman
2013) also point to phosphorous limitation for growth and reproduction at all
altitudes. The accumulation of P, Zn, Al, Fe, Na in the foliar tissue of Werauhia
sintenissi growing in plots fertilized regularly for 10 years with macro and micro
nutrients (Lasso and Ackerman 2013), suggest luxury consumption and storage not
only of P, as reported before for Vriesea sanguinolenta (Wanek and Zotz 2011), but
also for other nutrients.

Epiphytes and Climate Change

Potential Responses or Indicators of Climate Change

Atmospheric CO2 levels are predicted to double that of pre-industrial levels by

2050 (IPCC Assessment Report). With increasing levels of atmospheric CO2,
tropical forests are expected to increase carbon uptake, which may lead to faster
growth. In the case of epiphytes, this may translate into higher biomass and sub-
sequently higher loads on tree branches, which might lead to increased structural
damage of host trees. Tropical species, including epiphytes, are likely to shift
upslope rather than latitudinally with climate change mostly because of the very
steep temperature gradient found per meter elevation as compared to temperate
zones (5.2–6.5 °C decrease per 1000 m elevation, Colwell et al. 2008). To estimate
the potential responses of epiphytes to climate change, it is crucial to estimate the
effects of increasing levels of CO2 in epiphytic CAM species, and on species with
facultative CAM. Whether these species would have an advantage with increased
photosynthetic flexibility remains unknown.

Are Epiphytes Really Indicators of Climate Change?

Epiphytes are one of the most sensitive plant growth forms to disturbance and
microclimate changes due to their lack of access to permanent water sources and
nutrients, which forces them to be tightly dependent on seasonal precipitation, fog
or dew. For this reason, epiphytes are thought to be exceptionally sensitive to air
quality and climate, and considered indicators of climate change and forest health.
In addition, epiphytes are an important component of watersheds because of their
Ecophysiology and Crassulacean Acid Metabolism … 39

ability to intercept cloud and fog water thus increasing net water inputs. Managing
and implementing conservation programs for epiphytes is highly dependent on
understanding which factors influence epiphytic diversity in species-rich regions,
and the physiological responses of epiphytes to environmental change. Climate
change, through its effect on temperature, is likely to have an effect, albeit small, on
evaporation rates, which in turn can have an effect on communities of animals
living in water reservoirs inside epiphytic bromeliads. Examining patterns of epi-
phytic community distribution among different climate areas may provide an early
indication of vegetation responses to climate change.
Undoubtedly, the major threat to epiphytic diversity is deforestation (Fig. 5). It is
estimated that about 21,000 square km of forest is deforested annually in South
America, which harbors one of the richest epiphytic communities in the world, most
of it in the Amazonian Basin. Conservation of tropical rainforest is key to con-
servation of epiphytes.

Fig. 5 Epiphytic habitat loss

due to deforestation.
a Deforestation for
agricultural plantations. Photo
by Katia Silvera, and
b Deforestation due to
slash-and-burn agricultural
practices. Photo by Gaspar
Silvera
40 K. Silvera and E. Lasso

Concluding Remarks

Because most studies on epiphytes are species or genus specific, we need an array
of experiments using broad species samples, in order to estimate how communities
will change over time. As Zotz (2004) pointed out, when studying epiphytic
communities it is important to distinguish prevalence of vascular epiphytes in terms
of species numbers or biomass, because many orchid species occur in very low
numbers and their contribution to community biomass can be low. Because of this
inherit bias, interpretations of whether CAM is prevalent in tropical moist forests
compared to semiarid regions remain biased by number of species (Zotz 2004).
Most of the ecophysiological studies conducted on epiphytic plants have focused on
water relations of leaves, which provide a skewed view of plant function across
communities. Integration of studies using different organs is lacking and necessary
to understand how species will respond to climate change.
Epiphytes, as indicators of climate change, may be the first to respond to global
changes; therefore how we implement conservation strategies to forests is key to
mitigate changes to tropical forests.

Acknowledgments We dedicate this chapter to the memory of Mónica Mejía-Chang, a great

friend and passionate epiphyte and bromeliad researcher in Panama. Her infectious personality and
enthusiasm for life was reflected in her work and radiated throughout her life. We kindly
acknowledge John Cushman and artist Kirah Van Sickle for providing figure 2. This work is
supported in part by funding from the National Science Foundation (Award DEB 1442199 to KS),
the Smithsonian Tropical Research Institute Tupper Fellowship (to KS), and the Panamanian
Secretaría Nacional de Ciencia, Tecnología e Innovación (SENACYT to KS). This publication was
also made possible by the Colombian Fondo de Apoyo a Profesores Asistentes (FAPA to EL) from
the Universidad de Los Andes, Bogotá.

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Stem-Succulent Trees from the Old
and New World Tropics

Eleinis Ávila-Lovera and Exequiel Ezcurra

Abstract Stem-succulent trees are common in tropical drylands. Besides their

ability to store water, these trees also possess photosynthetic bark, which can
re-assimilate internally respired CO2 at virtually no water cost. Both of these traits
are advantageous in seasonally dry ecosystems, where plants are exposed to periods
of limited water availability and, consequently, carbon gain. In most species, plants
do not use the stored water in stems to buffer daily water deficits; they use this water
to flush new leaves before the onset of rains. This gives an extra advantage to
stem-succulent trees over other functional groups because leaves are already present
when the first rain falls. Having succulent stems does not pose a mechanical con-
straint in these plants, rather the succulence of the tree stem can act as hydrostatic
pressure against the bark, contributing to the biomechanical support of tall trees.
Stem-succulent trees are also able to maintain physiological processes and growth
during drought, making them good candidates to be used in reforestation of
degraded arid lands.

Keywords Photosynthetic bark Retamoid Sarcocaulescent
Stem photosyn-



thesis Tropical dry forest Water use efficiency

Introduction

Stem-succulent trees with photosynthetic bark have evolved in association with

tropical drylands. The large mid-latitude coastal deserts of the world such as the
Namib in Southern Africa, Atacama in Chile, the Saharan Atlantic Coastal Desert,

E. Ávila-Lovera (&)
E. Ezcurra

Department of Botany and Plant Sciences, University of California,
2150 Batchelor Hall, Riverside, CA 92521, USA
e-mail: eleinis.avilalovera@email.ucr.edu
E. Ezcurra
e-mail: exequiel.ezcurra@ucr.edu

© Springer International Publishing Switzerland 2016 45

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_3
46 E. Ávila-Lovera and E. Ezcurra

and Baja California in Mexico, are found on the west side of the African and
American continents associated with cold coastal currents that move towards the
equator along the eastern fringe of the Atlantic and Pacific oceans. North and south,
these deserts are flanked by semiarid regions: Mediterranean sclerophyllous scrubs
in their high-latitude boundary, and tropical dry scrubs towards the equator. The
seasonality of precipitation in these drylands changes dramatically from the tropics
towards higher latitudes: whereas Mediterranean shrubs survive mostly with winter
rains brought in from oceanic westerly winds, moisture in the dryland tropics is
almost entirely provided by summer rains delivered by summer monsoons and,
secondarily, by late summer hurricanes and tropical storms (García-Oliva et al.
1991; Douglas et al. 1993; Stensrud et al. 1995). Even within a single ecological
region, the transition from winter to summer rains can be marked. Most coastal
deserts receive winter rains in their high-latitude, temperate reaches, but are fed
predominantly by summer monsoon rains at their tropical edge, where they tran-
sition into tropical thorn scrub and seasonally dry forest (Douglas et al. 1993).
Winter- or summer-dominated seasonality generates different types of drylands.
Winter-rain drylands are dominated by evergreen shrubs with small and/or tough
leaves (e.g., the South African fynbos, California chaparral, Chilean matorral, and
other sclerophyllous scrubs; Dimmit 2000; Ezcurra et al. 2006), while the tropical
summer-rain drylands are dominated by drought-deciduous trees and shrubs
(Bullock et al. 1995; Gordon et al. 2004; Becerra 2005).
In the tropics, dry forests (TDF, Tropical Dry Forest) are diverse ecosystems in
terms of plant life-forms (Medina 1995)—or what has been known more recently as
plant functional groups (PFG). The understory of these forests is dominated by
herbs and woody shrubs, while the canopy is dominated by trees from different
PFG: evergreen, brevi-deciduous (leaf-exchanging), deciduous, stem-succulent, and
lianas (Schnitzer and Bongers 2002). At the same time, TDFs are one of the most
endangered ecosystems worldwide (Rodríguez et al. 2010), since they are in
favorable areas for agriculture, cattle, and human settling. Currently, some efforts
are underway to recover these ecosystems. An important step to achieve this is
reforestation with key plant species, for example, stem-succulent Baobab trees
(Adansonia, Fig. 1) have been used in reforestation practices in Africa, Madagascar
and Australia where they are one of the most representative trees (Wickens and
Lowe 2008). The amount of fauna associated with these forests is high, and
attempts to increase populations of endangered animal species usually start with
re-planting trees that support wildlife. One example is the yellow-headed parrot
(Amazona barbadensis) associated with one specific type of TDF on Margarita
Island, Venezuela (Rodríguez and Rojas-Suárez 2008).
Global Climate Change has prompted many researchers to investigate possible
effects of longer, more intense, and/or more frequent drought periods on plant
physiology (Chaves and Pereira 1992; Chaves et al. 2002; McDowell et al. 2008;
Tezara et al. 2010). Attention has turned to the prevention or remediation of the
detrimental effects of these droughts worldwide. We need to know how climate
change affects vegetation and how vegetation can feed back on climate. The eco-
physiology of many plant species is known due to applied research in particular crops,
Stem-Succulent Trees from the Old and New World Tropics 47

Fig. 1 Baobab (Adansonia sp.) in Tanzania, East Africa. Photo by Pedro Piqueras

biofuel plants, timber trees, or useful dryland species. The study of natural tropical dry
forests has lagged behind but there is now a growing number of studies being pub-
lished with interest in stem-succulent trees and their physiological responses to
drought. Because plants “belong” to different PFG, they likely respond differently to
climate change. The focus of this chapter is to describe the physiology and emphasize
the role of stem-succulent trees in the seasonally dry ecosystems they inhabit.
48 E. Ávila-Lovera and E. Ezcurra

Plants have evolved a number of different strategies to cope with drought in arid
regions. In many species, drought tolerance has led to the evolution of a reduced
leaf area or to a drought-deciduous habit, both of which contribute to reduced water
loss during critically dry periods. Drought-deciduous and leafless plants in hot
deserts and tropical drylands frequently occur in the form of shrubby or arborescent
species with photosynthetic stems. These plants can have either stem net photo-
synthesis (SNP) or stem recycling photosynthesis (SRP) (Ávila et al. 2014), both of
which positively affect the carbon economy of plants. When plants have SNP, their
stems are usually more efficient in the use of water than leaves, i.e., they have
higher photosynthetic water use efficiency (WUE; photosynthetic carbon gain
divided by water loss from transpiration) (Ehleringer et al. 1987; Osmond et al.
1987; Smith and Osmond 1987; Nilsen and Sharifi 1997). When plants have SRP,
their stems do not lose water because the photosynthetic bark re-assimilates
internally respired CO2. Within plants that have photosynthetic stems one important
group is the sarcocaulescent group, which has large-sized stems with translucent
exfoliating bark, a large amount of parenchymatous tissue that serves as a water
reservoir, and non-succulent, drought-deciduous leaves (Franco-Vizcaino et al.
1990). Another group, the retamoid group, comprises leafless or almost leafless
woody plants that have stomata in the stem’s epidermis or other structures such as
lenticels in the bark surface that permit gas exchange (Schaedle 1975). A third
group, the cactoid group, is composed of succulents with Crassulacean Acid
Metabolism (CAM), such as the New World cacti or the African cactoid euphorbs.
In this chapter we will discuss the physiology, ecology, and biogeographic distri-
bution of sarcocaulescent and retamoid species, with an emphasis on sarcocauls,
trees with photosynthetic bark and possessing the ability to store large amounts of
water in their stems. The cactoid group will not be discussed here as CAM phys-
iology is addressed in an earlier chapter of this book (Silvera and Lasso, this
volume). As we will see in the following sections, the retamoid growth form tends
to be more frequent in the pole-ward edge of deserts in temperate drylands with
winter rains, whereas sarcocauls tend to be more frequent in the equator-ward edges
of deserts in tropical drylands with monsoon summer rains.

Sarcocaulescent Trees

Sarcocaulescent, or fleshy-stemmed trees, also known as “pachycauls” (thick

stems), are plants with a disproportionately thick trunk for their height and canopy.
They are often referred to as “bottle trees” for their abnormally swollen stems. In
contrast with cactoid and retamoid species, which are frequently protected by dense
spines, sarcocaulescent plants show massive trunks tapering upward into relatively
small branches. The most distinctive traits of sarcocauls are: (1) the large amount of
undifferentiated parenchyma both in the stem rays and central axis that serves as a
water reservoir for the plant, (2) the presence of smooth, translucent exfoliating
Stem-Succulent Trees from the Old and New World Tropics 49

bark with photosynthetic cells, and (3) non-succulent drought-deciduous leaves.

Although the bark of sarcocaulescent trees normally has no lenticels or stomata,
limiting the diffusion of CO2 to photosynthetic tissue, SRP, previously known as
bark or corticular photosynthesis (see Ávila et al. 2014), helps to maintain adequate
carbohydrate supplies during leafless periods by re-fixing and recycling respiratory
CO2 (Franco-Vizcaino et al. 1990).
Sarcocauls often coexist in nature with a related morphology: caudiciform
plants. Caudiciform species generally have an enlarged basal caudex or stem axis, a
thick, tuber-like structure at ground level from which the stems and roots arise
(Rowley 1987). The caudex may extend below the ground and often gives rise to
deciduous twining stems. This adaptation is well developed in species of the gourd
family (Cucurbitaceae), such as Marah macrocarpa in California, USA or
Ibervillea sonorae in Mexico.
Plants with giant fleshy stems occur in a number of families in the dry regions of
the Americas, Africa, and Australia (Wickens and Lowe 2008, see Table 1), and
sometimes in montane forests (Carlquist 1962, 2001). Remarkably, fleshy-stemmed
trees are particularly dominant and diverse in some highly isolated insular envi-
ronments such as the island of Socotra, that lies in the northwestern Indian Ocean
near the mouth of the Red Sea between the Arabian Peninsula and the Horn of
Africa (Brown and Mies 2012), or Madagascar (Fischer and Theisen 2000). The
third hotspot of sarcocaulescent plants is the Peninsula of Baja California in Mexico
(Franco-Vizcaino et al. 1990), which is not a true island now but has evolved as an
island ecosystem for most of the last 6 million years. The reason for this extraor-
dinary diversity of sarcocaulescent trees in islands is still a matter of debate.
Mabberley (1974) attributed the extraordinary concentration of pachycauly in some
islands to lineages of herbaceous ancestors evolving arborescent life-forms in
isolation from competition with other trees. Alternatively, the absence of large
herbivores in many of these insular environments during most of the Pliocene–
Pleistocene could have played an important role in the evolution of fleshy stems.
Apart from the role of isolation in the evolution of the syndrome, it seems also
clear that the sarcocaulescent life-form is particularly advantageous in hot dry
environments. In contrast with retamoid species, trees with giant fleshy stems tend
to occur in the equator-ward edge of the warm deserts and in tropical dry envi-
ronments, in places such as the Horn of Africa, the Kaokoveld and Succulent Karoo
in Namibia, the Tehuacán desert in southern Mexico, the Caatinga in Brazil, or the
Dry Chaco in Paraguay. Even within a region, the association with aridity is evi-
dent. In Baja California, for example, the largest concentration of sarcocaulescent
growth forms occurs in the dry central deserts of the peninsula (Franco-Vizcaino
et al. 1990; Perea et al. 2005). Similarly, in Madagascar, the distribution of sar-
cocauls is chiefly restricted to the TDFs and thickets of the western and south-
western regions (Fischer and Theisen 2000; Wickens and Lowe 2008).
There are some species that seem to lie somewhere in the middle of the
retamoid-to-sarcocaulescent gradient. In the American Continent, all species within
the genus Parkinsonia (‘paloverde’, formerly in the genus Cercidium; Fabaceae,
Caesalpinioideae) possess thick stems with green photosynthetic bark, but lack the
50 E. Ávila-Lovera and E. Ezcurra

Table 1 Some noteworthy sarcocaulescent genera and their geographic distribution

Plant family Genus Location References
Aizoaceae Psilocaulon South Africa Adie and Yeaton (2013)
Anacardiaceae Cyrtocarpa Mexico Wiggins (1980),
Medina-Lemos and
Fonseca (2009)
Pachycormus Mexico Nilsen et al. (1990),
Franco-Vizcaino et al.
(1990)
Spondias Costa Rica, Panama, Borchert (1994, 1996),
Mexico Goldstein et al. (1998),
Medina-Lemos and
Fonseca (2009)
Apocynaceae Adenium Tropical Africa, Wickens and Lowe (2008)
Madagascar
Frerea
Pachypodium Madagascar Wickens and Lowe (2008)
Plumeria Costa Rica, Mexico, Borchert and Rivera (2001),
Nigeria, Puerto Rico Alvarado-Cárdenas (2004),
Sloan et al. (2006)
Asteraceae Dendrosenecio Montane Tropical Wickens and Lowe (2008)
Africa
Bixaceae Cochlospermum Costa Rica Borchert (1996)
Burseraceae Bursera Mexico, Tropical Nilsen et al. (1990),
America Borchert (1996),
Medina-Lemos (2008),
Wickens and Lowe (2008)
Commiphora Africa, Mexico Medina-Lemos (2008),
Wickens and Lowe (2008)
Cactaceae Pereskia Tropical America Britton and Rose (1963),
Arias et al. (2004)
Campanulaceae Cyanea Hawaii Wickens and Lowe (2008)
Brighamia Hawaii
Lobelia Montane S. America,
Africa, India
Crassulaceae Crassula Tropical America
Cucurbitaceae Dendrosicyos Socotra, Southern Wickens and Lowe (2008)
Arabia
Didiereaceae Portulacaria South Africa Cowling and Mills (2011),
Adie and Yeaton (2013)
Euphorbiaceae Euphorbia Africa, Tropical
America
Givotia Madagascar Wickens and Lowe (2008)
Jatropha Mexico, Central Maes et al. (2009),
America Díaz-López et al. (2012),
Wickens and Lowe (2008)
Ricinus Simbo et al. (2013)
Fabaceae Enterolobium Costa Rica Borchert (1994)
(continued)
Stem-Succulent Trees from the Old and New World Tropics 51

Table 1 (continued)
Plant family Genus Location References
Dalbergia Costa Rica, Mexico Borchert (1994),
Olvera-Luna et al. (2012)
Delonix Madagascar Wickens and Lowe (2008)
Gliricidia Costa Rica Borchert (1994)
Fouquieriaceae Fouquieria Baja California, Franco-Vizcaíno et al.
Sonoran Desert (1990), Nilsen et al. (1990),
(Arizona) Pockman and Sperry (2000)
Malvaceae: Adansonia Tropical Africa, Wickens and Lowe (2008)
Bombacoideae Madagascar. NE
Australia
Bombacopsis Central America Borchert and Rivera (2001),
Borchert and Pockman
(2005), Wickens and Lowe
(2008)
Bombax Old World Tropics Coster (1923), Wickens and
Lowe (2008)
Cavanillesia Tropical America
Ceiba Tropical America Borchert and Rivera (2001),
(+ Chorisia) Wickens and Lowe (2008)
Ochroma Costa Rica, Panama Borchert (1994), Machado
and Tyree (1994)
Pseudobombax Argentina, Brazil, Machado and Tyree (1994),
Costa Rica, Panama Borchert (1996), Borchert
and Rivera (2001),
Schöngart et al. (2002)
Malvaceae: Brachychiton Australia Wickens and Lowe (2008)
Sterculioideae Hildegardia Nigeria Borchert and Rivera (2001)
Moraceae Dorstenia Tropical Africa, Wickens and Lowe (2008),
Socotra, India, González-Castañeda and
Mexico Ibarra-Manríquez (2012)
Moringaceae Moringa Madagascar Wickens and Lowe (2008)
Vitaceae Cyphostemma Africa, Madagascar Wickens and Lowe (2008)

fleshy parenchymatic tissues or the ability to store water of the true sarcocauls
(Fig. 3 of Santiago et al. this volume). Roots of these species can also be green if
they grow exposed to sunlight (Fig. 2). A similar intermediate case is posed by the
arid-zone tree Geoffroea decorticans (Fabaceae, Caesalpinoidea) in Argentina and
Chile, which has drought-deciduous leaves and large stems with exfoliating green
bark, but lacks fleshy parenchyma and the ability to store water.
52 E. Ávila-Lovera and E. Ezcurra

Fig. 2 Roots of Parkinsonia praecox when growing exposed to sunlight. Tropical dry forest in
Margarita Island, Venezuela. Photo by Wilmer Tezara

Retamoid Shrubs

The retamoid syndrome (Zohary 1962; Shmida and Whittaker 1981) is common in
certain Old World Mediterranean legumes in genera such as Retama (from where the
syndrome takes its name), Calcycotome, Cytissus, Genista, Spartium, and Ulex, all
common in southern Europe, northern Africa, and the Near East. Retamoid species
are mostly shrubs with highly reduced leaves, photosynthetic stems (Table 2), and,
often, spinescent shoots that give them a characteristic “crown of thorns” appearance.
In North American drylands, a diverse array of species with similar morphology
occur in different families. The most outstanding example is that of the largely
leafless green spiny shrubs which resemble Castela emoryi, a member of the
Simaroubaceae. The convergent forms are Koeberlinia spinosa in the Koeberliniaceae,
Canotia holacantha in the Celastraceae, Thamnosma montana in the Rutaceae,
Adolphia californica in the Rhamnaceae, and Glossopetalon spinescens in the
Crossosomataceae, all having leaves reduced to scales and persistently green stems
that carry out photosynthesis. Compared to North America, the retamoid habit is more
common, and taxonomically more diverse in South America, where retamoid forms
frequently occur outside of strict drylands, in environments such as the Puna of Chile,
the Patagonian steppe, or the Chaco forests (Johnston 1940). The genus Colletia, in
Stem-Succulent Trees from the Old and New World Tropics 53

the family Rhamnaceae, forms the most common set of retamoid plants in South
America, including five species widely dispersed in Chile, Argentina, Bolivia, and
Uruguay. Other notable retamoid species in South America include Cassia aphylla
(Caesalpinioideae), Prosopidastrum globosum (Fabaceae-Mimosoideae), Retanilla
ephedra (Rhamnaceae), and Bulnesia retama, the only retamoid species within the
New World Zygophyllaceae. Following the name of the dominant genera with this
characteristic green-stem morphology, retamoid species have also been referred to as
“holacanthoid” plants in North America (Muller 1941), or “colletoid” species in South
America (Johnston 1940).

The Evolution of Stem Succulence and Photosynthetic Bark

In the primary shoot of dicotyledons the vascular bundles that run along the stem
perform the basic function of connecting the leaves to the rest of the plant (Gibson
1978; Tomlinson and Wheat 1979). When the stem’s secondary growth begins, a
continuous cambial layer develops and the vascular bundles give way to a con-
tinuous woody tissue made of xylem, inside the cambial layer, and surrounded by
an external layer of phloem covered externally by bark. In short, the main difference
between primary and secondary stems lies in the arrangement of conductive tissues
in the form of vascular bundles surrounded by large amounts of undifferentiated
parenchyma in primary shoots as opposed to a continuous cambium in secondary
stems, and the presence of a photosynthetic epidermis in the former as opposed to a
suberous bark in the latter.
The trunks of both retamoid and sarcocaulescent growth forms show one or both
of these juvenile traits: retamoid plants are characterized by their green photo-
synthetic stems with a stomata-bearing epidermis, while sarcocauls are character-
ized by their fleshy stems with large parenchymatic radii, and often by the presence
of photosynthetic chlorenchyma in their externally smooth, non-suberous bark. At
an anatomical level, Carlquist (1962, 2001) described ancestral juvenile traits in the
wood anatomy of sarcocauls, and hypothesized that the evolutionary mechanism for
the development of the sarcocaulescent growth form was the retention of juvenile
characteristics in the adult trees, a phenomenon he called paedomorphism.
Carlquist’s hypothesis has been challenged by other authors, such as Mabberley
(1982), who believes that pachycauly in islands has evolved from ancestral
herbaceous plants becoming larger and larger individuals in the absence of tree
competitors, and Olson (2003) who showed that the main morphologic traits in
sarcocauls, namely wide parenchymatic rays and abundant axial parenchyma, are
present also in vines and lianas. Olson suggests that pachycauly in many taxa
evolved repeatedly from lianas in the core eudicots.
So while Carlquist hypothesizes that sarcocaulescence evolved from woody trees
with non-fleshy stems, Mabberly believes the syndrome evolved from herbaceous
plants that in the absence of competitors became large and tree-like, while Olson
supports the idea that giant fleshy stems evolved from vines and lianas. In practice,
54 E. Ávila-Lovera and E. Ezcurra

because the evolution of sarcocaulescence is polyphyletic, all three models could

have operated independently in different taxa. Mabberly’s model seems a likely
hypothesis for the origin of pachycauly in the case of some arborescent Asteraceae
(Dendrosenecio) and Campanulaceae (Cyanea, Brighamia, and Lobelia), all plants
whose nearest relatives are herbaceous, and Olson’s model seems plausible in the
case of sarcocaulescent Cucurbitaceae (Dendrosicyos) and Vitaceae (Cyphostemma),
two families dominated by vines and creepers. In many other woody taxa [e.g.,
Anacardiaceae, Burseraceae (Fig. 3), or bombacoid Malvaceae (Fig. 4)], however, the
evolutionary pathway is less clearly defined and Carlquist’s hypothesis cannot be
ruled out. Beyond the details of the discussion, these three models jointly constitute
an appealing and evolutionarily parsimonious idea: paedomorphism, the retention of
primary shoot traits in enlarged adult stems, could be a simple mechanism of evo-
lution in response to selective forces favoring either reduced leaves and photosyn-
thetic shoots, or a succulent stem with a large proportion of parenchymatic cells

Fig. 3 Bursera simaruba in

an early successional forest in
Gamboa, Panama. Note the
photosynthetic bark. Photo by
Eleinis Ávila-Lovera
Stem-Succulent Trees from the Old and New World Tropics 55

Fig. 4 Ceiba speciosa in Riverside, California, USA. Photo by Louis S. Santiago

capable of storing water. It is important to note that both of these characteristics are
advantageous in seasonally dry ecosystems, where water is scarce during at least one
period of the year. One way or another, these three evolutionary models involve
heterochrony, the evolution of changes in the timing of morphologic development
events in one taxon relative to another, as their driving mechanism. Conceptually,
they might explain why the retamoid and the sarcoculescent syndromes are so
common in drylands throughout the world, and why they have arisen independently
in so many taxonomically unrelated families.

Ecophysiology of Trees with Succulent Stems

When we think of trees with succulent stems the first that come to mind are the
Baobabs (Fig. 1). These trees might be the most famous among stem-succulent
trees, and Wickens and Lowe (2008) have described them as “grotesque trees
dominating the landscape”; the landscape usually being African savannas. These
singular trees usually store water in their stems during the rainy season and it is
thought that the water is used during the dry season. In this section we will describe
the use of water by this type of tree and how they physiologically respond to
environmental stresses such as drought.
56 E. Ávila-Lovera and E. Ezcurra

Physiology of Succulent Trees

Plants with succulent stems are found in families spread among the Angiosperms
(Table 1). Representative genera mostly belong to the family Malvaceae-
Bombacoideae, followed by Apocynaceae, Euphorbiaceae and Fabaceae.
A common characteristic is that they all inhabit seasonally dry environments.

Table 2 Ratio of stem net photosynthesis to leaf photosynthesis in retamoid species from North
American Deserts (taken and modified from Ávila et al. 2014)
Species Family Location Stem-to-leaf References
A ratioa
Bebbia juncea Asteraceae Sonoran Desert 0.52 Ehleringer et al.
(1987)
Chrysothamnus Asteraceae Sonoran Desert 0.64
paniculatus
Dyssodia Asteraceae Sonoran Desert 0.83
porophylloides
Gutierrezia Asteraceae Sonoran Desert 0.85
microcephala
G. sarothrae Asteraceae Sonoran Desert 0.26
Hymenoclea Asteraceae Sonoran Desert 0.67
salsola
Lepidium fremontii Brassicaceae Sonoran Desert 0.70
Porophyllum Asteraceae Sonoran Desert 0.63
gracile
Psilostrophe Asteraceae Sonoran Desert 1.01
cooperi
Salazaria mexicana Lammiaceae Sonoran Desert 1.11
Senecio douglasii Asteraceae Sonoran Desert 0.06
Sphaeralcea Malvaceae Sonoran Desert 0.61
parvifolia
Stephanomeria Asteraceae Sonoran Desert 1.04
pauciflora
Thamnosma Rutaceae Sonoran Desert 0.48
montana
Eriogonum Polygonaceae Mojave Desert 0.50 Osmond et al. (1987)
inflatum
Hymenoclea Asteraceae Arizona 0.60 Comstock and
salsola Ehleringer (1988)
Spartium junceum Fabaceae California 0.38 (Nilsen and Bao
1990)
Justicia californica Acantaceae Sonoran Desert 1.29 Tinoco-Ojanguren
(2008)
a
Photosynthetic rate of stems were expressed in projected area before calculating the ratio of
stem-to-leaf photosynthesis
Stem-Succulent Trees from the Old and New World Tropics 57

Usually, succulence in stems is associated with the presence of chlorenchymatic

tissue underneath the periderm which can re-assimilate CO2 released by respiration
(Nilsen et al. 1990). Stem recycling photosynthesis has been found in African
Baobab (Adansonia digitata) and Castor bean (Ricinus communis), and effectively
contributes to bud development in both plants (Simbo et al. 2013). The stem
contribution to bud development was estimated by excluding light from penetrating
the stem periderm; a reduction of 50 and 67 % in dry biomass of developed buds
was found in drought and watered Adansonia digitata plants, respectively, while
the reduction was lower in Ricinus communis (25 and 40 % in drought and watered
plants, respectively) (Simbo et al. 2013).
When comparing leaf and stem photosynthesis, rain was found to be detrimental
for CO2 diffusion in leaves because it can clog stomata, but wetting the stem
periderm decreases reflectance which subsequently increases light absorption by the
chlorenchyma, electron transport rate (ETR), and photosynthesis in Quercus coc-
cifera (Manetas 2004). For plants with SRP, CO2 diffusion does not decrease with
stem wetting because the CO2 source is derived from respiration and not from the
atmosphere.
Similarities and differences have also been found when comparing leaf and
SNP. In general terms, stem photosynthesis functions just like leaf photosynthesis.
Stem net photosynthesis has the same responses to environmental variables such as
photosynthetic photon flux density (PPFD), internal concentration of CO2 (Ci),
temperature and vapor pressure deficit (VPD). Both stem and leaf photosynthesis
show C3 metabolism, and both organs have high stomatal density (Osmond et al.
1987; Nilsen et al. 1989; Nilsen and Sharifi 1994; Aschan and Pfanz 2003).
However, WUE has been found to be higher in stems, which can be incredibly
valuable in periods of water deficit when most plants with SNP are leafless (Ávila
et al. 2014). On the other hand, stem photosynthesis in plants with SRP occurs at no
water cost, making these plants very successful during periods of water deficit
and/or low temperature, where they can re-assimilate respired CO2 without losing
any water.
Since stem-succulent trees are typically found in seasonally dry ecosystems, one
advantage that has been associated with this trait is the use of stored water during
the dry season to buffer daily water deficits. However, some studies have evaluated
this assumption and have found that daily use of stored water is usually negligible
in Adansonia species (Chapotin et al. 2006a, b, c). In Adansonia rubostripa and
Adansonia za, stored water does not buffer daily water potential (Ψ) because of the
difficulty in withdrawing water from the storage tissue (Chapotin et al. 2006c).
Instead, stored water is used to flush new leaves before the onset of the rainy season
in Adansonia species, giving them an advantage over other species since leaves are
already present when the first rain comes, thus maximizing photosynthetic capacity
and extending the growing season of the plants (Chapotin et al. 2006b). This
phenology also takes place in Plumeria alba from Guánica, Puerto Rico, where the
peak of leaf flushing occurs 2–4 months before the peak of rainfall when water
availability of the soil is low (Sloan et al. 2006).
58 E. Ávila-Lovera and E. Ezcurra

Other species show daily use of stored water during the lag between leaf tran-
spiration and stem basal sap flow, as demonstrated in five species of tropical canopy
trees from a lowland seasonal moist forest in Panama (Goldstein et al. 1998). Here,
the use of stored water and recharge of reservoirs is a dynamic process that can even
be altered by fluctuating environmental conditions (Goldstein et al. 1998). In drier
ecosystems, such as thornscrubs and deserts, seasonal and diurnal variation in leaf
Ψ is small due to the buffering capacity of succulent stems as is found in Fouquieria
colummnaris, Pachycormus discolor, and Bursera microphylla in Baja California
(Nilsen et al. 1990). The SRP found in Fouquieria colummnaris and Pachycormus
discolor, in addition to the capacity to store water in their stems, may ensure
survival during extreme drought conditions (Franco-Vizcaino et al. 1990).
Not only leaf-flushing but also flowering has been associated with stored water
in stem-succulent trees. In a study performed in a TDF in Costa Rica where five
PFG were evaluated (deciduous hardwood, deciduous lightwood, deciduous soft-
wood, evergreen lightwood and evergreen softwood), deciduous lightwood trees
were found to have the highest capacity to store water during the rainy season
(Borchert 1994). On average, stem water content of stem-succulent trees was 63 %
compared to 31 % in deciduous hardwood, 47 % in deciduous softwood, 46 % in
evergreen lightwood and 51 % in evergreen softwood (Borchert 1994). This
capacity to store water in stem-succulent trees was associated with low wood
density (0.40 g cm−3), and the water stored during the wet season was found to be
used at the end of the dry season for leaf flushing and flowering (Borchert 1994). It
was also found that deciduous lightwood trees experienced less water deficit, and
both their leaf and stem Ψ remained high during the dry season after leaf shedding
(Borchert 1994).
Water storage capacity of stems is highly correlated to wood anatomy and
biochemical support (Borchert and Pockman 2005; Chapotin et al. 2006a).
Stem-succulent plants among other plant types have the highest capacity to store
water and can maintain higher Ψ than deciduous and leaf-exchanging species
during drought (Borchert and Pockman 2005). One might think that succulence is a
disadvantage for stability and mechanical support. However, in six species of
Adansonia, lighter wood and its intrinsic high capacity of water storage acts as
hydrostatic pressure against the bark which can contribute to biomechanical sta-
bility in tall trees (Chapotin et al. 2006a; Niklas 2016 this volume). It seems that
succulent plants are better armed to face drought since water uptake during rehy-
dration and minimum Ψ in the dry season are correlated to water storage capacity
(Borchert and Pockman 2005), and they suffer less from collapse when fully
hydrated (Chapotin et al. 2006a).
Leaf and root morphology are often indicative of where plants live or can live.
Baobab trees can have smaller leaves with higher stomatal density in drier and hotter
areas than in wetter areas (Cuni Sanchez et al. 2010). Also, while rooting depth is
sometimes deeper in arid than in sub-humid ecosystems, stem succulents have an
intermediate depth, with widely spread shallow roots (Schenk and Jackson 2002).
Furthermore, pruning has a significant effect on leaf size: Baobab trees growing in the
Stem-Succulent Trees from the Old and New World Tropics 59

same environment have smaller leaves on pruned branches than on non-pruned

branches (Cuni Sanchez et al. 2010). The genetics of different populations and the
phenotypic plasticity in physiological traits of a single population found in Baobabs
may also play a role in drought responses (Cuni Sanchez et al. 2010).
Plant functional groups (evergreen, deciduous, brevi-deciduous, and
stem-succulent trees) were studied in Guanacaste, Costa Rica to determine what
trait or suite of traits are part of the strategies tropical trees use to respond to drought
periods in terms of water balance, wood traits, and phenological behavior (Worbes
et al. 2013). In a Principal Component Analysis (PCA), the two first axes were
related to hydraulic conductivity, control of transpiration and water loss (Worbes
et al. 2013). In Cochlospermum vitifolium, plants flush leaves all year round despite
the seasonality of rainfall in Guanacaste (Fallas-Cedeño et al. 2010). Stem succu-
lents also have higher leaf and wood carbon isotopic composition (δ13C) when
comparing to deciduous, brevi-deciduous and evergreen species, suggesting that
they have tighter control over their stomata, making them water conservative
species and successful pioneers in this TDF (Worbes et al. 2013). In another TDF in
Belize, stem succulents flush leaves early in the dry season, likely using water
stored during the previous rainy season (Sayer and Newbery 2003).
Most stem-succulent trees occur in TDF, yet there is some evidence of stem
succulents in Amazonian forests. Schöngart et al. (2002) studied the same PFGs as
Worbes et al. (2013) and their phenological and stem-growth responses to
flood-pulses and found that Pseudobombax munguba, a stem-succulent tree species,
flushed new leaves only after the end of the flooded period. The whole reproductive
phase was completed within one single aquatic phase in contrast with the others
PFGs, and maturation of fruits finished by the end of the aquatic phase or with a
little extension intro the terrestrial phase (Schöngart et al. 2002). Stem diameter
increment had the highest correlation with monthly precipitation among the PFGs
studied (Schöngart et al. 2002). It was argued that the phenological processes are
correlated to the flood-period and not to photoperiod (Parolin et al. 2016, this
volume), as it has been stated for TDF trees in Costa Rica and Puerto Rico by
Borchert and Rivera (2001) and Sloan et al. (2006), respectively.

Physiological Responses to Drought

In terms of drought, numerous experiments have been performed to assess pho-

tosynthesis and growth responses to water deficit. Most of these studies are con-
ducted in pots and in greenhouses under controlled conditions using juvenile plants.
Despite the lack of realism compared to field-based studies, these data are needed to
advance our understanding of the mechanisms driving plant processes. Some
studies have directly compared adult populations of the same species or closely
related species in contrasting environments. Some of the plant species listed in
Table 1 have been used in drought experiments and the most relevant results are
presented below.
60 E. Ávila-Lovera and E. Ezcurra

Two populations of Adansonia digitata from West and Southeast Africa were
compared in terms of physiological and morphological responses to drought (De
Smedt et al. 2012). Seedlings were used to investigate the mechanisms by which
Baobab juveniles cope with soil drought and it was found that the population from
West Africa had the strongest drought-avoidance mechanism, making them more
water conservative than seedlings from Southeast Africa (De Smedt et al. 2012). In
another comparative study, Adansonia grandidieri, Adansonia madagascariensis
and Adansonia rupostripa from Madagascar, the species with the lowest drought
tolerance came from the highest rainfall ecosystem (Randriamanana et al. 2012).
All species cope with drought by reducing stomatal conductance (gs) and having
water stored in the taproot, with a high WUE at the expense of maintaining high
photosynthetic rates (Randriamanana et al. 2012).
Seedlings of Adansonia digitata have been used to study sap flow and water use
in drought experiments, which include a drought + recovery treatment (Van den
Bilcke et al. 2013). The mechanisms associated with survival during drought
included succulence of the taproot, which represented 17.5 % of total daily water
use, and SRP which takes place in the chlorenchyma below the periderm (Van den
Bilcke et al. 2013).
Drought can affect different aspects of the physiology of stem-succulent trees,
depending on the species. Jatropha curcas shows no changes in specific leaf area,
Ψ range, relative water content, transpiration efficiency, or aboveground biomass,
but phenology (Maes et al. 2009) and biomass production did change (Achten et al.
2010; Díaz-López et al. 2012). Drought-induced production of new leaves with
reduced leaf area and higher stomatal density (Maes et al. 2009), as has been found
in populations of Adansonia digitata, as well as reduced leaf, stem and root growth
(Achten et al. 2010), leaf Ψ, pressure potential, photosynthetic rate, gs, WUE, and
maximum quantum efficiency of photosystem II (Díaz-López et al. 2012). These
morphological and physiological responses to drought allow plants to have a
conservative water use strategy.
Contrary to what is expected, photosynthetic WUE and crop WUE (kg fruits m−3
H2O) in Jatropa curcas decrease with drought (Abou Kheira and Atta 2009;
Díaz-López et al. 2012). The highest crop WUE was found in the treatment with the
highest water availability (Abou Kheira and Atta 2009). On the other hand, most other
characteristics, including oilseed quality, do not change with drought treatments, which
indicates that Jatropa curcas can be used to re-vegetate a wide range of arid lands to
exploit its oil without changes in its quality (Abou Kheira and Atta 2009).
Another trait to cope with drought in succulent trees is starch storage during the
rainy season (Fallas-Cedeño et al. 2010). As with water, starch is used seasonally
and not daily in Cochlospermum vitifolium; it is used as a storage reserve for
phenological events such as branch extension, leaf flushing, and reproduction that
take place during the dry season before the onset of rains (Fallas-Cedeño et al.
2010). However, both starch storage and stem succulence are typical traits that
correspond to a drought avoidance strategy.
Stem-Succulent Trees from the Old and New World Tropics 61

Use of Stem-Succulent Trees for Conservation

and Rehabilitation of Degraded Arid Lands

Stem-succulent plants have great potential for use in restoration of degraded lands
due to their exceptional physiological performance and tolerance to drought.
However, little has been done to actually address this hypothesis and determine
whether these traits are enough to promote effective reforestation practices.
One of the few studies that support this hypothesis was performed in South
Africa where Portulacaria afra was found to be a nurse plant playing an important
role in the regeneration dynamics of arid subtropical thicket vegetation (Adie and
Yeaton 2013). This species modifies microhabitats and creates opportunities for
plants that are more susceptible to extreme conditions, which are common in this
ecosystem (Adie and Yeaton 2013). Portulacaria afra clumps comprised approx-
imately 50 % of the studied area and approximately 90 % of tree seedlings were
recorded under its canopy (Adie and Yeaton 2013). Portulacaria afra may simply
provide shade and protection against intense rain events to young seedlings, but a
high soil carbon content has been found under its clumps (Cowling and Mills
2011), which is known to have important effects on soil structure and, possibly, on
the soil microbial community, enhancing the recruitment of other plant species.
More informal than an experiment is the observation that Baobab trees are now
being planted—consciously or unconsciously—in areas where they were not
originally present. Some of these areas are even drier than their native range. This
provides evidence that stem-succulent trees can cope with severe drought periods,
which would be ideal to restore plant communities in arid lands. Furthermore,
Baobabs have multifunctional uses as shade and street trees, for water storage,
shelter and storage, food, wood, fiber, fertilizer, fuel, insecticide, and as an orna-
mental (Wickens and Lowe 2008). Recently, Baobab seed oil and fruit pulp have
been exported to countries outside of Africa, such as Canada, USA and European
countries (Venter and Witkowski 2010). Using them to reforest degraded lands can
have significant positive effects on both the health of the land and the economy of
nearby villages.

Conclusions and Future Directions

In seasonally dry ecosystems, there are predominantly three plant growth forms
with photosynthetic stems, based on morphology, anatomy and physiology of the
stems: sarcocaulescent, retamoid, and cactoid. The sarcocaulescent and retamoid
forms include plant species with a broad biogeographic distribution and many
similar characteristics. Even when the stem does not look green it might have a
layer of chlorenchyma beneath the periderm, which can carry either SNP or SRP
(Ávila et al. 2014). This feature and the possibility to store water in fleshy stems of
sarcocaulescent species, supports the ability to cope with prolonged periods of
water deficit, common in deserts and TDF.
62 E. Ávila-Lovera and E. Ezcurra

There is not a unique hypothesis about the origin of stem succulence, photo-
synthetic bark, or sarcocauls in general. There are multiple hypotheses that cannot
be ruled out because the evolution of the green stem syndrome is polyphyletic, and
all possible models of evolution could have operated independently in different
taxonomically unrelated families.
Ecophysiological performance of different sarcocaulescent species have been
described in tropical countries of the Old and New Worlds. However, more in situ
studies under field conditions that take into account all biotic and abiotic factors
affecting the physiology of adult populations need to be done if we are to use this
information to make decisions about land management and conservation of
endangered species. This effort is underway, but we still need the help of new
physiological ecologists to work on the still unanswered questions.

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Palm Physiology and Distribution
in Response to Global Environmental
Change

Heidi J. Renninger and Nathan G. Phillips

Abstract Palms (Arecaceae) represent one of the oldest surviving monocot fam-
ilies maintaining a presence in tropical rainforest-like biomes throughout history.
Comprising a variety of plant growth forms (arborescent, acaulescent, lianoid),
palms are one of the few monocots that achieve significant heights. In doing so,
they face many of the same environmental and physiological constraints as
dicotyledonous trees including long-distance water transport and longevity making
them an important, but largely missing, component of comparative tree physio-
logical studies. Palms differ from dicot trees in several key ways including lacking
dormancy mechanisms that restrict them to mainly tropical climates. Palms also
lack a vascular cambium and the constant addition of new conduits, and instead,
rely exclusively on vascular bundles for fluid transport and mechanical stability.
The majority of arborescent palm species also possess only one apical meristem
complex from which all new leaf and stem growth originates thereby limiting their
options for leaf positioning and light acquisition. These differences will likely alter
the response of palms to global change compared with dicot species. Temperature
increases have the potential to extend palm distributions to higher elevations and
latitudes, but could negatively affect individual palm carbon balance. Within the
tropics, precipitation has been shown to have the strongest positive effect on palm
species richness and future changes in rainfall patterns will likely alter palm dis-
tributions. Therefore, global change has the potential to alter both palm distribu-
tions and individual physiological functioning, but palms will likely continue to
have a considerable presence in many tropical ecosystems.

H.J. Renninger (&)

Department of Forestry, Mississippi State University,
Box 9681, Mississippi, MS 39762-9601, USA
e-mail: hrenninger@gmail.com
N.G. Phillips
Department of Earth and Environment, Boston University,
685 Commonwealth Avenue, Boston, MA 02215, USA
e-mail: nathan@bu.edu

© Springer International Publishing Switzerland 2016 67

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_4
68 H.J. Renninger and N.G. Phillips

Keywords Agriculture
Architecture
Climate change
Global distribution

Leaf life span

Introduction

Rising atmospheric carbon dioxide (CO2) and temperature are changing the
structure and function of trees (Phillips et al. 2008; Way and Oren 2010) and their
global distributions, including palms (Walther et al. 2007). The unique monopodial
growth form in palms suggests that they may respond to environmental change in
categorically different ways than dicotyledonous trees that display secondary
growth characteristics. Yet little information is available about climate and envi-
ronmental change responses of palms. In addition to their economic and ecological
importance, palms can also provide a broader value in comparative research of tree
physiology, but are absent from some pertinent studies (e.g., Mäkelä and Sievänen
1992; Way and Oren 2010; Stephenson et al. 2014). In this chapter we review
physiological ecology of palms, and assess their potential responses to increased
temperature and [CO2] and altered water availability in the context of global
change.
The palm family (Arecaceae) exhibits a pan-tropical distribution with individual
species found in a wide range of ecosystem types including rainforests, montane
regions, dry forests, savannas and desert oases (Tomlinson 2006). Palms are
monocots and represent one of the oldest extant families in this clade based on
molecular dating (Janssen and Bremer 2004), with the oldest palm fossils found
from the Turonian stage in the Late Cretaceous (Berry 1914; Kvacek and Herman
2004; Harley 2006). There is also evidence that palms have existed throughout the
entire recorded span of the tropical rainforest-like biome (Couvreur et al. 2011;
Baker and Couvreur 2013b) making them a model plant family to study the evo-
lution of tropical rainforests (Couvreur et al. 2011). Palms likely originated in the
northern latitudes on the Laurasian supercontinent and subsequently dispersed to
equatorial South America, Africa and Southeast Asia before the end of the
Cretaceous (Bjorholm et al. 2006; Couvreur et al. 2011; Baker and Couvreur 2013a;
Couvreur and Baker 2013). They were widespread during the Early Eocene
Climatic Optimum where global temperatures were much warmer than today and
boreotropical forests extended well into the northern latitudes (Morley 2000;
Bjorholm et al. 2006). Likewise, palms have shown consistent diversification rates
and low extinction rates throughout their history (Couvreur et al. 2011). Therefore
as a plant family, palms exhibit great resilience as well as evidence of long distance
dispersal and the ability to colonize most areas with suitable climate (Baker and
Couvreur 2012).
Today, the majority of palm species diversity occurs in tropical Asia, with
around 1200 species followed by the Neotropics with about 800 species (Dransfield
et al. 2008). In a study of tree species composition and species richness in the
Palm Physiology and Distribution in Response … 69

Fig. 1 Iriartea deltoidea

(Ruiz & Pav.), the fifth most
abundant tree species in the
Amazon (Ter Steege et al.
2013), growing at Tiputini
Biodiversity Station in eastern
Ecuador

Amazonian rainforest, seven of the 20 most common tree species were palms
(Fig. 1) with the palm family having five times more “hyperdominant” species than
expected by chance and being second only to the Fabaceae in individual tree
abundance throughout the region (Ter Steege et al. 2013). Surprisingly, although
there are about 200 palm species in Madagascar, there are only 65 species in
continental Africa (Dransfield et al. 2008). Research suggests that tropical Asia and
South America have greater species richness due to higher diversification benefit-
ting from plate tectonic activity (Baker and Couvreur 2013a), as opposed to Africa
which has remained relatively isolated from other landmasses since the breakup of
Gondwana (Couvreur and Baker 2013; Couvreur 2014). Historical climate change
and species extinctions may have also played a role in Africa’s shortage of palm
species as well as the current climate because Africa tends to be drier than other
tropical locations (Couvreur and Baker 2013; Couvreur 2014).
Although palms have a dominant presence in the tropics and, in particular tropical
rainforest biomes, they lack dormancy mechanisms and are absent from locations
with extensive freezing temperatures (Tomlinson 2006). Palms exhibit a variety of
growth types including understory shrubs-like forms, vine forms (rattans; Calamus
spp. in the old world tropics and Desmoncus spp. in the Neotropics) and arborescent
tree-like forms. Likewise, palms are one of the few monocot families containing
species that achieve significant heights with the tallest palm being a species that
grows in the Colombian Andes (Ceroxylon quindiuense (Karst.) H. Wendl) and
reaches heights of 60 m (Henderson et al. 1995). Despite arborescent palms being as
70 H.J. Renninger and N.G. Phillips

tall as, or taller than, sympatric dicot trees and displaying long lifespans, they differ
in several key ways that affect their physiological functioning within an ecosystem.
For example, the majority of palm species lack aerial branching and all leaves and
stem growth occurs at a single apical meristem (Tomlinson 1990). This gives palms
little flexibility in terms of their aboveground body plan as opposed to many other
plant types that have a more modular body plan (Tomlinson 2006). Palms also lack
secondary meristems meaning that they do not produce secondary xylem (wood),
secondary phloem or bark tissues and all fluid transport occurs through primary
vascular bundles that are scattered within a matrix of parenchyma cells throughout
the stem. Within tropical ecosystems, these differences could alter the way that
palms respond to climate change compared with other plant types.
This chapter will begin with a discussion of the unique structural and physio-
logical features of palms compared to dicot tree species. Drawing off the literature
and our previous studies, we consider implications of these differences for how
physiological functioning and growth in palms responds to environmental variation.
Next, because palms are a key component of many tropical agricultural systems, we
will review physiological data from these systems and discuss their effect on the
broader landscape. Finally, we consider environmental and physiological con-
straints on palm growth and distribution and the potential for global change to alter
palm abundance and range size.

Key Features of Palms and Physiological Implications

Leaf and Crown Structure

The vast majority of palm species are monopodial (Tomlinson 1961) and, unlike
dicot trees, lack a mechanism for branching. All leaves are successively produced
by one apical meristem complex that, in caulescent species, also produces new stem
tissue associated with each leaf that increases the overall height of the palm. When a
leaf falls, it creates a permanent scar or node on the palm’s trunk leaving a record of
its height growth (Fig. 2). These nodes hold promise for identifying the age of an
individual palm (Oyama 1993) as well as acting as a potential “timescale” in the
aseasonal tropics to determine the age of gaps and forest disturbances
(Martínez-Ramos et al. 1988; Ratsirarson et al. 1996). However, leaf turnover rates
are difficult to predict because they are dependent on environmental variation and
canopy position (Lugo and Rivera Batlle 1987), male versus female individuals in
dioecious species (Ataroff and Schwarzkopf 1992; Cepeda-Cornejo and Dirzo
2010) and ontogeny, increasing with age in some species (Ratsirarson et al. 1996;
Renninger and Phillips 2010) and decreasing in others (De Steven et al. 1987; Lugo
and Rivera Batlle 1987; Renninger and Phillips 2010). Because palm leaves are
produced in a rosette pattern by the apical meristem, new leaves are in a better
position for light interception (Corley 1983) as well as being free of epiphylls
Palm Physiology and Distribution in Response … 71

Fig. 2 Nodal leaf scars on

the stem of the palm Mauritia
flexuosa (L.f.) leave a record
of vertical height growth

(Coley and Kursar 1996) and any other dry deposition compared to older leaves. As
palm leaves age, chlorophyll content (Corley 1983), leaf nitrogen content (Hogan
1988) and stomatal conductance tend to decline (Corley 1983; Hogan 1988).
Because all leaves originate from a single apical meristem in most shrub-like and
arborescent palms, they exhibit a more compact crown with limited options in terms
of canopy architecture compared with dicot trees. This makes leaf area estimations
and scaling of physiological parameters more straightforward for palms (Renninger
et al. 2009; Renninger and Phillips 2010) because crowns are composed of relatively
low numbers of leaves, although individual leaves are some of the largest in the plant
kingdom (Tomlinson 2006). Therefore, construction costs and investment of carbon
and nutrients into a single leaf is higher for palms than dicot trees and a single palm
leaf will experience a variety of light and environmental conditions as it progresses
from a newly formed leaf at the top of its canopy to a lower leaf at the base of its
canopy (Chazdon 1985). There is also evidence that when these large senescent leaves
eventually fall, they affect the understory seedling bank and species composition by
damaging seedlings and covering seeds (Peters et al. 2004; Venceslau Aguiar and
72 H.J. Renninger and N.G. Phillips

Tabarelli 2010). Palms are limited in their options for increasing total leaf areas for
light interception with different species either increasing the number of leaves they
carry and retaining individual leaves longer (Holbrook and Sinclair 1992b; Avalos
and Sylvester 2010; Renninger and Phillips 2010) or increasing the size of individual
leaves (Rich et al. 1995; Renninger and Phillips 2010). Pinnately-compound leaves
appear to have much greater capacity for increases in individual leaf area through
increases in length and three-dimensionality of leaves (Rich et al. 1995) compared
with simple and palmately-compound leaves (Renninger and Phillips 2010).
For palms, there are diminishing returns for increasing light interception capacity
with increasing leaf biomass because new leaves shade older ones (Chazdon 1985)
do to the compact crown structure of palms. However, they do possess some
strategies to deal with their compact crown structure including altering the size,
width and number of leaves they hold, changing the zenith angle of the petiole, and
adjusting the biomass allocations between petioles and the lamina in order to
maximize light capture efficiency in a variety of understory conditions (Chazdon
1985; Takenaka et al. 2001). Nevertheless, leaf support costs were shown to out-
pace increases in leaf and crown size in two understory palms and these costs could
not be completely compensated for by increased leaf longevity (Chazdon 1986).
Despite the constraint to leaf development due to monopodial growth, some tree
palms can adjust leaf demography and biomass allocation under different light
levels inside the forest. For example, leaf life span of Euterpe edulis, a conspicuous
palm in subtropical Atlantic Forests, increases by 100 days with decreasing irra-
diance while the rate of leaf production decreases (Gatti et al. 2011). At higher light
levels, typical of small forest gaps, adjustments in biomass allocation to leaf
components allow E. edulis to reduce self-shading and increase light interception.
At high light, palms allocate more biomass to roots and the plants exhibit small leaf
sizes when leaves are compared using an explicit ontogenetic analysis. Ontogeny
constrains the maximum size that each consecutive leaf could achieve, while
growth irradiance determines the rate of leaf production (Gatti et al. 2011). Thus,
although several studies have been performed on leaf and crown properties of
understory palms, more detailed research on leaf physiology of tall, overstory palms
including light capture efficiency, leaf construction costs, leaf temperatures,
boundary layer conductance and wind resistance compared with tropical dicot trees
is needed to fully understand the implications of a compact crown structure and
large leaf size on global change responses in palms.

Functional Consequences of the Lack of Secondary Growth

As monocots, palms lack a vascular cambium from which secondary growth

originates in woody dicot species. Instead of secondary xylem (wood) and sec-
ondary phloem performing long distance fluid transport, primary xylem and phloem
tissues located within thousands of vascular bundles transport water and photo-
synthetic sugars throughout the palm. Radially, vascular bundles exhibit the lowest
Palm Physiology and Distribution in Response … 73

frequencies in the center of the palm stem and increase in frequency in positions
closer to the stem periphery (Tomlinson 1961; Rich 1987). Longitudinally, vascular
bundles do not remain in the same position within the stem, but instead create a
shallow helix as they travel through the stem center before diverging to the stem
periphery to connect with the leaves (Zimmermann and Tomlinson 1965, 1972;
Zimmermann 1973). In the stem periphery, a vascular bundle splits into elements
that connect to the leaf and elements that continue in a vertical direction moving
back toward the stem center (Zimmermann and Tomlinson 1965). With global
change and anthropogenic activities increasing the occurrence of fire in the tropics
(Goldammer and Price 1998; Cochrane 2003, 2009), the lack of a vascular cam-
bium, the occurrence of both xylem and phloem tissues throughout the stem and the
cluster of leaf bases that insulates the apical meristem may confer palms with
greater fire resistance compared to co-occurring tropical dicot trees (Cochrane
2003). Results are, however, mixed with some studies finding that adult arborescent
palms are relatively resistant to fire-induced mortality (Ratsirarson et al. 1996;
Souza and Martins 2004; Van Nieuwstadt and Sheil 2005), whereas Williams et al.
(1999) found that palms exhibited much lower survival in a wildfire in northern
Australia compared with deciduous and evergreen eucalypt species.
In terms of stem longitudinal and diameter growth, tall palms follow two main
strategies. In many arborescent palms, all diameter growth occurs underground, and
the aboveground stem emerges at its final diameter (Waterhouse et al. 1978). In other
palms, a small diameter, aboveground stem occurs relatively early in development
and continues to increase in diameter until reaching a final size (Fig. 3a, b,
Waterhouse et al. 1978; Alves et al. 2004; Avalos et al. 2005; Avalos and Fernández
Otárola 2010; Avalos and Sylvester 2010). In these palms, stems increase in girth
through increases in the size and space between parenchyma cells (Fig. 3c, d) within
the stem (Waterhouse et al. 1978; Rich 1987). These microscopic changes across the
entire stem can lead to four- to six-fold increases in overall stem diameter
(Waterhouse et al. 1978; Rich et al. 1986; Renninger and Phillips 2010). Recently,
these increases in size and distance between parenchyma cells as well as the helical
path of vascular bundles have also been associated with sustained increases in the
length of the lower stem region in an Amazonian tropical palm species (Renninger
and Phillips 2012). Some palm species that exhibit an aboveground stem in their
early growth stages also possess stilt roots (Fig. 4) which may provide additional
stability to the aboveground stem (Schatz et al. 1985). Therefore, although palms
lack the ability to add new vascular tissue through secondary, radial growth, they still
exhibit a large capacity to alter the structure and functioning of their main stem axis.
Because long distance water transport occurs under negative pressures subjecting
the water in vessels to a metastable state and the possibility for malfunction
(Zimmermann 1983), plants must either efficiently avoid cavitation, replace cavi-
tated vessels with functioning ones, or refill cavitated vessels and reconnect them to
the water transport stream. Without a vascular cambium, palms lack the ability to
replace vessels in their stem or leaves, and therefore need to either avoid cavitation
throughout the lifetime of the palm or refill cavitated vessels. There is evidence that
cavitations occur and are refilled in the petioles of palms on a regular basis (Milburn
74 H.J. Renninger and N.G. Phillips

Fig. 3 Radial stem expansion in the palm Iriartea deltoidea (Ruiz & Pav.) which has a small
diameter, aboveground stem as a sapling (a) that continues to expand until reaching its adult size
(b). Stem expansion occurs through increases in the size of parenchyma cells as well as the
intercellular space between them as seen when comparing a stem cross section from a small
diameter stem (c) and a large diameter stem (d). Scale bars = 0.5 mm

and Davis 1973; Zimmermann and Sperry 1983; Sperry 1986; Renninger and
Phillips 2011) but there is little data on if, and how widespread, cavitations occur in
the stem vessels. Root-generated, positive pressures have been found in palms
(Davis 1961), but likely play a minor role in cavitation refilling (Milburn and Davis
1973). More likely, the overall hydraulic architecture of the palm protects stem
xylem from widespread cavitations. Palms possess hydraulic constrictions between
the stem and subtending leaves because only the tiny protoxylem vessels within
Palm Physiology and Distribution in Response … 75

Fig. 4 Stilt roots in (a) Iriartea deltoidea (Ruiz & Pav.) and (b) Socratea exorrhiza (Mart.) H.
Wendl., the ninth most abundant tree species in the Amazon (Ter Steege et al. 2013)

bundles connect the leaf to the stem (Zimmermann and Tomlinson 1965;
Zimmermann and Sperry 1983). Conductance is highest in the stem tissue, extre-
mely low at the leaf insertion point, and increases distally in the petiole
(Zimmermann and Sperry 1983). This anatomical arrangement provides evidence
that palms conform to the hydraulic segmentation hypothesis (Zimmermann 1983;
Tyree and Ewers 1991; Pivovaroff et al. 2014) in which the integrity of the stem
xylem is protected from the large negative water potentials experienced by the leaf
and petiole xylem (Zimmermann and Sperry 1983). However, empirical evidence for
this hypothesis is lacking, particularly for tall, arborescent palm species that can
reach 60 m in height (e.g. Ceroxylon quindiuense (Karst.) H. Wendl.; Henderson
et al. (1995)) and whose stem xylem in certain species functions for more than
100 years (Tomlinson and Huggett 2012).

Stem and Tissue Longevity

Palms of various species have been found to live for more than a century
(Tomlinson and Huggett 2012), achieving significant heights while lacking a vas-
cular cambium and the radial additions of new vascular tissues. Because palms
continue to use vessels located at their stem bases and produced while they were
younger and smaller in stature, they may be overbuilt hydraulically when young to
accommodate increases in water transport distance as they become older and taller.
An overbuilt hydraulic architecture in young palms and the lack of a vascular
cambium could suggest that long distance water transport may begin to limit
76 H.J. Renninger and N.G. Phillips

stomatal conductance and carbon uptake in tall palms. However leaf-specific

transpiration rates determined from sap flux measurements were found to be similar
between short, young palms and the tallest individuals of a given species
(Renninger et al. 2009; Renninger and Phillips 2010). These results are consistent
with leaf gas exchange measurements which showed no difference in stomatal
conductance or photosynthesis with palm height in subtropical Washingtonia
robusta (H. Wendl), from measurements spanning the full range of palm heights in
this species on sites in two continents (Renninger et al. 2009). Therefore, our
studies have not found a hydraulic limitation to gas exchange (Ryan and Yoder
1997; Ryan et al. 2006) in the tallest individuals of the study species. However, we
did find evidence for sharply reduced leaf epidermal sizes in the tallest palms of
Washingtonia robusta (Renninger et al. 2009), and smaller average frond area, and
smaller total leaf area in taller palms, consistent with a turgor-hydraulic limitation to
palm height (Woodruff et al. 2004) although in two palm species growing in the
humid tropics (Iriartea deltoidea Ruiz & Pav. and Mauritia flexuosa L.f.), the
tallest individuals had the largest leaf areas with similar leaf-specific transpiration
rates as shorter individuals (Renninger and Phillips 2010).
Not only do xylem vessels need to function in water transport throughout the
lifetime of the palm (see Functional consequences of the lack of secondary growth),
but individual phloem tissues and parenchyma cells also remain functional
throughout the 100+ year lifespan of some palm species (Zimmermann 1973;
Bullock and Heath 2006; Tomlinson and Huggett 2012). This condition in palms as
arborescent monocots is particularly novel in the plant kingdom, because in dicot
tree species, phloem transports solutes for one to a few years before its function is
replaced by new phloem tissues produced by the vascular cambium. Likewise,
parenchyma cells in the stems of dicot trees remain functional throughout the
sapwood but become nonfunctional during the transition to heartwood. Therefore,
in many dicot species, stem parenchyma cells remain alive for a few years to several
decades with a few long-lived conifer species exhibiting sapwood longevities
exceeding 100 years (Spicer 2005). Not only do parenchyma cells in palms remain
alive throughout the lifetime of the palm, but they also retain the ability to change
size and wall composition exhibiting cell expansion and cell wall thickening over
extended periods of time (Waterhouse et al. 1978; Rich 1987).
The longevity of the phloem tissues in palm stems deserves increased attention,
however a few studies present data on its structure and functional properties. Using
phloem exudation from developing coconut inflorescences, Milburn and
Zimmermann (1977) measured specific mass transfer rates as high as 70 g h−1 cm−1
and phloem pressures as high as 0.76 MPa which is in agreement with estimates of
phloem osmotic and xylem water potentials. Parthasarathy and Tomlinson (1967)
and Parthasarathy and Klotz (1976) performed anatomical investigations of phloem
in palms and found that, unlike dicot species, sieve plates lack the definitive callose
material that occludes sieve pores during typical phloem senescence, but possess a
small amount of callose material surrounding individual sieve plate pores. They
also found that appreciable amounts of p-protein, a substance that seals phloem
sieve tube cells in the event of large pressure changes, were absent. Therefore, the
Palm Physiology and Distribution in Response … 77

majority of palm phloem tissue appears to lack the dormancy mechanisms seen in
the majority of dicot tree species with the exception of the phloem supporting fallen
palm leaves which become occluded by outgrowths from surrounding parenchyma
cells (Parthasarathy and Tomlinson 1967). It is clear that more research is needed
on the longevity and functioning of palm phloem and parenchyma tissues as well as
their interaction with xylem vessels and the potential for positive stem pressure and
cavitation refilling within palm stems (Renninger and Phillips 2011).

A Higher Proportion of Living Cells in Stems

While dicot trees generally have sapwood containing between 5–25 % living par-
enchyma cells (Spicer and Holbrook 2007), palm stems contain vascular bundles
within a matrix of parenchyma cells that can make up more than 50 % of the
cross-sectional area of the main central portion of the stem (not including par-
enchyma cells located within the vascular bundles themselves; Renninger and
Phillips (2010)). Therefore, palm stems contain a high capacity for stored water and
non-structural carbon reserves within these parenchyma cells that could potentially
increase as palm stems increase in size. However, this may also lead to increased
levels of maintenance respiration in larger palms which could put them at a dis-
advantage compared to co-occurring dicot species. Navarro et al. (2008) found that
autotrophic respiration in coconut (Cocos nucifera L.) palms accounted for about
60 % of total GPP which is slightly higher than an estimate of average autotrophic
respiration of trees from a tropical forest site (50 % from Malhi et al. (1999)). In
terms of foliar respiration, Cavaleri et al. (2008) found that dicot trees and liana
species had higher rates than palms and Henson (2004) found no differences
between maintenance respiration in oil palm (Elaeis guineensis Jacq.) fronds of
differing ages. Per unit stem biomass, maintenance respiration rates were found to
decrease with age (Breure 1988; Henson 2004) being highest near the crown and
decreasing towards the base (Henson and Chang 2000). Nevertheless, total main-
tenance respiration rates increased with palm size due to the accumulation of living
tissues (Henson 2004) and showed a temperature dependence (Henson 2004) which
may increase the respiration costs incurred by palms in a warming climate.
Increased living stem tissue may also mean that stored stem water plays a larger
role in daily and seasonal water relations in palms compared with co-occurring
species. Killmann (1983) found that moisture content increased with stem height in
coconut palms. In some species, palm stems also contain a swollen region with
Fisher et al. (1996) finding this region in the Cuban belly palm (Acrocomia crispa
(Kunth) C. Baker ex. Becc.) to have 89 % moisture content which was higher than
the upper and lower stem regions (62 and 46 % moisture content respectively).
Stem parenchyma tissue has also been found to give up its water relatively freely
having a specific capacitance that was 84 times higher than leaf tissue in Sabal
palmetto (Walt.) Lodd. (Holbrook and Sinclair 1992a). However, this large amount
of stored stem water did not prevent large water deficits in the leaves of Sabal
78 H.J. Renninger and N.G. Phillips

palmetto and stored stem water reserves were only mobilized during periods of high
transpiration due to the large hydraulic constriction at the leaf insertion point
(Holbrook and Sinclair 1992b). Therefore, stored stem water may serve the function
of protecting stem vessels from cavitation under periods of high transpiration and
maintaining leaf turgor during periods of severe drought and stomatal closure
(Holbrook and Sinclair 1992b). Diurnally, transpiration in taller palms showed a
greater reliance on stored water compared with shorter palms (Holbrook and
Sinclair 1992b; Renninger et al. 2009; Renninger and Phillips 2010). Holbrook and
Sinclair (1992b) found that about 35 % of daily water use in Sabal palmetto was
derived from stored stem water with this percentage increasing during a soil dry-
down. In subtropical Washingtonia robusta, stored stem water contributed about
22 % to daily water use in the tallest individuals (Renninger et al. 2009). Even in
the palm Mauritia flexuosa, which grows in permanently inundated swamps and
therefore faces no soil water deficit, stored stem water in the tallest individuals
contributed almost 20 % to daily water use (Renninger and Phillips 2010).
The large proportion of living parenchyma cells within palm stems allows for
storage of significant amounts of non-structural carbon reserves in the form of
starch and sucrose that serve a physiological function as well as making certain
species valuable as an edible food source for indigenous tropical populations (Kahn
1988). Fisher et al. (1996) found that in Cuban belly palms, the largest amounts of
starch were located in the upper trunk region with little to no starch located in the
middle, swollen region and the lower trunk. In coconut palms, non-structural car-
bon was stored mainly as soluble sucrose as opposed to insoluble starch
(Mailet-Serra et al. 2005), the preferred storage form in dicot trees. In coconut
palms, about 60 % of stored non-structural carbon reserves are located in the stem
and about 14 % are found in the leaf petioles with little to no storage in the root
tissues (Mailet-Serra et al. 2005). Petiole carbon reserves appear to act as a buffer
by storing excess photosynthetic carbon in the absence of other sinks and releasing
carbon during periods of high demand and/or low photosynthetic assimilation rates
thereby maintaining vegetative growth over a range of environmental conditions
(Mialet-Serra et al. 2008). In oil palm both glucose and starch are stored in stems
with starch concentrations being highest below the crown and increasing when
assimilation rates are high and decreasing when fruits are being produced (Legros
et al. 2009). The role of the large glucose and sucrose pool in the remainder of the
palm stem remains unknown but could become mobilized under more severe
environmental stressors and disturbances (Mialet-Serra et al. 2008; Legros et al.
2009). While non-structural carbon reserves have been studied in agriculturally
important palm species, they remain largely uncharacterized in the undomesticated
palms occurring widely across the tropics where they potentially represent an
important source of carbon sequestration.
Palm Physiology and Distribution in Response … 79

Stem Biomechanics

A lack of secondary growth also has implications for mechanical stability of palms
as they grow taller and may mean that palms have a predetermined critical height
that is set by the diameter expansion that occurs well before the palm reaches its
maximum stature (Niklas 1992). For dicot trees, wood tissues perform the dual role
of long distance water transport and mechanical stability. Vascular bundles in palms
allocate the role of water transport to large metaxylem vessels and the role of
mechanical stability to fibers, meaning that palms can have a higher hydraulic
efficiency for a given carbon investment compared with dicot trees (Renninger et al.
2013). Palms attain similar heights as co-occurring dicot trees reaching the top of
the canopy in tropical forests. However, palms tend to have larger height to
diameter ratios than dicot trees (Niklas 1994; Niklas et al. 2006) and would be
theoretically unstable if they shared similar material properties (Rich 1986; Rich
et al. 1986; Alves et al. 2004). In addition, palms cannot maintain a constant
slenderness ratio as they grow taller. Due to their lack of secondary growth, they get
proportionally thinner as they increase in height (Niklas 1992). However, palms can
continue to alter the density and stiffness of their tissues as they age. As palms grow
taller, the density, stiffness and strength of the palm base and stem periphery
increases (Fig. 5, Rich 1986, 1987; Rüggeberg et al. 2009) through sustained
thickening and sclerification of fibers (Rich 1986) allowing palms to achieve higher
strength and stiffness values at a given density compared with dicot wood tissues
(Rich 1987). The location of the dense stem material in the lower stem periphery
puts it in an optimal location to withstand the highest mechanical stresses that the
stem experiences (Niklas 1992).

Fig. 5 Decay resistant,

peripheral stem tissue of a
palm containing highly
lignified fibers and
sclerenchyma cells
80 H.J. Renninger and N.G. Phillips

In some species of palms that reach significant heights, the top of the stem
remains flexible allowing the stem to bend without breaking under wind loads (Rich
1987; Winter 1993; Alves et al. 2004; Rüggeberg et al. 2009). The leaf sheaths that
surround the main stem also provide additional mechanical support (Tomlinson
1962; Niklas 1999) against buckling and torsional deformation. Likewise, palm
leaves can reconfigure in the wind, particularly pinnately compound leaves that
exhibit a flexing of the rachis and a rotating of the individual leaflets such that they
form a more compact, aerodynamic structure with less drag (Niklas 1999). Some
palm individuals can grow in the direction of a canopy gap exhibiting a trunk that
diverges significantly from vertical (Fig. 6). The small crown and lack of branching
in palms decreases their mechanical load (Rich et al. 1986) but also means that they
exhibit more dynamic swaying motion in the wind compared to dicot trees whose
sideways motion is dampened by the larger branch mass (James et al. 2006). The
arrangement of vascular bundles within the palm stem also functions in the transfer
of external forces to the ground. The central region of the palm stem contains rigid
vascular bundles within a matrix of pliable parenchyma cells and intercellular air
spaces that perform the function of energy dissipation of external forces (Rüggeberg
et al. 2009). Stress discontinuities between the vascular bundles and the par-
enchyma matrix are avoided by a pattern of decreasing stiffness of fiber cells as they
approach the surrounding parenchyma tissues (Rüggeberg et al. 2008, 2009).
Therefore, a single palm stem has been shown to contain the full range of tissue
density and tensile strength measured across all woody dicot species (Niklas 1992).
These unique mechanical features allow palms to reach significant heights while

Fig. 6 Washingtonia robusta (H. Wendl.) palms growing at the Los Angeles County Arboretum
and Botanic Garden and exhibiting stem axes that diverge significantly from vertical
Palm Physiology and Distribution in Response … 81

withstanding intense wind loads (Winter 1993; Duryea et al. 1996), but may be an
additional limitation to the overall crown size and photosynthetic capacity of a palm
individual.

Palms in Tropical Agricultural Systems

Palms have been cultivated by humans for thousands of years and continue to be an
important component of both subsistence agroforestry systems (Pritchard Miller
and Nair 2006; Clement et al. 2009) and industrialized monoculture plantations
(Chao and Krueger 2007; Fowler et al. 2011). For South American subsistence
cultures, the most useful palms are either tall, have large fruits or large leaflets with
these individuals used for both food and construction (Cámara-Leret et al. 2014). In
terms of more wide-scale cultivation and production, some Amazonian palm spe-
cies like peach palm (Bactris gasipaes Kunth) face challenges due to the shelf life
of its fruits (Clement et al. 2004) while other native palms like açaí palm (Euterpe
oleracea Mart.) are gaining in global popularity (Van Looy et al. 2008).
Increasingly, palm monocultures comprise vast areas of the tropics. Therefore, in
order to better quantify and model fluxes of carbon, water vapor and other green-
house gases across many tropical landscapes, an increased understanding of the
physiological responses of these palm crops to current and future environmental
factors is necessary. Likewise, environmental change may alter the productivity and
profitability of these systems affecting the livelihoods of many in the tropics. In
addition, because of their economic importance, these cultivated palms have been
the most widely studied in terms of physiological functioning and response to
environmental conditions. The following section provides background information
and ecological physiology for the three main palm crops; date palm (Phoenix
dactylifera L.), coconut palm and oil palm.

Date Palm

Palms have been identified as one of the most important plant families in terms of
supplying products for human use (Tregear et al. 2011) and the date palm is thought
to be one of the oldest fruits in cultivation with its usage dating to ancient
Mesopotamia (Chao and Krueger 2007). Date palms differ from many other species
of palms in that they thrive in very hot, dry climates with little rainfall, low humidity
and abundant sunshine. However, they require abundant soil moisture in the rooting
zone (2 m depth) provided from either a shallow water table or constant irrigation
(Chao and Krueger 2007). Date palms continue to be grown in arid areas largely in
the Middle East and North Africa where they play a significant role in the economies
of many countries as well as providing subsistence agriculture for rural desert
populations (Chao and Krueger 2007; El-Juhany 2010). Date palms may also
82 H.J. Renninger and N.G. Phillips

prevent desertification in arid areas (El-Juhany 2010) and can provide shade
allowing understory crops to be grown (Chao and Krueger 2007). Dates are a rich
source of protein, vitamins and mineral salts (El-Juhany 2010) as well as energy with
ripe fruits having sugar concentrations exceeding 80 % (Chao and Krueger 2007).
Likewise, because ripe fruits have low water contents, they can be stored for pro-
longed periods of time under ambient conditions (Chao and Krueger 2007).
Globally, date palm production exceeded 7.5 million Mg in 2012 with 1.1 million ha
in production (FAOSTAT 2014). Egypt, Iran and Saudi Arabia all produced over 1
million Mg of dates in 2012 and Iraq, Iran, Saudi Arabia and Algeria all contain over
100,000 ha of date palms in production (FAOSTAT 2014).
Date palms grow in extreme locations with little rainfall and high radiation,
temperatures and vapor pressure deficits. Of the incoming solar radiation absorbed
by the leaf, 80 % is dissipated through non-photochemical quenching (Sperling
et al. 2014a). Date palms require access to constant soil moisture using about 120 L
of water per day and exhibiting immediate decreases in transpiration if irrigation is
withheld (Sperling et al. 2012). Because consistent irrigation is important for
maintaining crop yield, automated systems including thermal imaging have been
developed to detect water stress in date palms (Cohen et al. 2012). Symbiotic
relationships with arbuscular mycorrhizae have also been found to aid growth of
seedlings during drought conditions (Baslam et al. 2014). Because date palms
require abundant irrigation and freshwater is limited in many locations, saltwater is
frequently used to irrigate palms. Date palms have been identified as salt tolerant,
however high salinity water (EC = 10.5–12 dS m−1) decreases growth and fruit
yields (Tripler et al. 2007, 2011; Sperling et al. 2014a). In a long term study, date
palms irrigated with high salinity water were half as large and their fruit production
was 50 % smaller than palms irrigated with low salinity water (Tripler et al. 2011).
High salinity irrigation does not affect the photosynthetic apparatus but instead
causes decreases in stomatal conductance and water use due to osmotic stress and
more negative soil water potentials (Tripler et al. 2007; Sperling et al. 2014a; b).
Decreased stomatal conductance in palms receiving high salinity irrigation also led
to increased photorespiration rates compared with control palms (Sperling et al.
2014a). Despite effects of drought stress on date palm productivity, increased rain
or humidity with climate change may make certain areas in North Africa and
elsewhere unsuitable for date palm because fruits require dry, hot summers to avoid
cracking and fungal diseases (Shabani et al. 2012). However, other locations
including areas in North and South America may become more suitable for date
palms with climate change (Shabani et al. 2012).

Coconut Palm

Coconut palms likely originated from Southeast Asia (Harries 1978) and are cur-
rently found throughout the humid tropics in areas that receive ample rainfall.
Coconut palms are grown primarily for their fruits which provide products including
Palm Physiology and Distribution in Response … 83

the white endosperm tissue or coconut “flesh”, coconut oil and coconut water from
the immature fruits. Both dwarf and tall varieties are grown for coconut production
with conflicting information about the water use and resistance to drought stress of
each variety (Gomes and Prado 2007). Globally, almost 62 million Mg of coconut
were produced in 2013 with over 12 million ha in cultivation (FAOSTAT 2014).
Asia, by far, has the largest area in production in 2013 with over 9.7 million ha
followed by Africa with almost 1.2 million ha and the Americas with over
600,000 ha (FAOSTAT 2014). Indonesia, the Philippines, and India led coconut
production by country with each producing over 10 million Mg and having over 2
million ha in production in 2013 (FAOSTAT 2014). Well-watered palms are capable
of producing over 90 kg of fruit dry matter per year (Rees 1961), with low light
intensity, drought stress, nutrient deficiencies (Prado et al. 2001; Gomes and Prado
2007) and diseases including lethal yellowing decreasing yield. Lethal yellowing
affects coconut palms throughout the Americas (Maust et al. 2003) and is caused by
a phytoplasma that affects phloem transport (Maust et al. 2003) and leads to
increasing leaf sugar concentrations, decreased root carbohydrate concentrations and
permanent stomatal closure (McDonough and Zimmermann 1979; Eskafi et al.
1986; Leon et al. 1996; Martinez et al. 2000; Maust et al. 2003).
Water use and carbon uptake in coconut palms have been found to respond to
seasonal differences in soil moisture, radiation and vapor pressure deficit.
Well-irrigated dwarf coconut palms in Brazil had evapotranspiration rates ranging
from 2.5 mm day−1 in the rainy season to 3.2 mm day−1 in the hot summer season
(de Azevedo et al. 2006). During the dry summer season in India, evapotranspi-
ration rates averaged 5.5 mm day−1 and were as high as 7 mm day−1 (Rao 1989). In
coconut palm fields (LAI = 3) growing in Vanuatu under ample soil moisture,
evapotranspiration was about 950 mm year−1 with palm transpiration representing
about 68 % of this total and averaging 1.3–2.3 mm day−1 depending on atmospheric
conditions (Roupsard et al. 2006). In locations where rainfall is highly seasonal,
carbon uptake and water use is limited by radiation during the wet season and by
decreased stomatal conductance during the dry season (Prado et al. 2001), although
coconut palms tend to be more water use efficient in the dry season (Rees 1961;
Prado et al. 2001) showing increases in epicuticular wax (Kurup et al. 1993) as well
as sugar and amino acid concentrations in leaves (Kasturi Bai and Rajagopal 2000).
During the dry season, rainfed coconut palms experienced decreased stomatal
conductance due to both soil and atmospheric drought compared to irrigated palms
(Shivashankar et al. 1991; Repellin et al. 1997) that decreased dry matter pro-
duction (Rees 1961) and leaf water potentials by about 0.5 MPa (Rees 1961;
Kasturibai et al. 1988). Prolonged drought has also been found to cause long-lasting
negative effects on the photosynthetic apparatus in coconut palms (Gomes et al.
2008).
84 H.J. Renninger and N.G. Phillips

Oil Palm

Oil palm is native to West Africa (Dufrene and Saugier 1993) and its cultivation has
been steadily increasing globally with over 4 million ha added between 1993 and
2003 and almost 6 million ha added between 2003 and 2013 (FAOSTAT 2014).
Worldwide, over 17 million ha were in production in 2013, with the vast majority
located in Asia (over 12 million ha) and almost exclusively in Indonesia (7 million ha)
and Malaysia (4.5 million ha) followed by Africa with over 3 million ha (with 2
million ha located in Nigeria) and the Americas with over 1 million ha (FAOSTAT
2014). In 2013, over 55 million Mg of palm oil were produced globally (FAOSTAT
2014) and is used as a cooking oil, in a variety of processed foods and other products
and, recently, as a biofuel. In terms of aboveground production of temperate and
tropical forests, oil palm plantations are second only to fertilized Eucalytpus (Dufrene
and Saugier 1993). In Borneo, daytime maximum CO2 uptake was almost two times
higher in an oil palm plantation compared with a nearby rainforest site (Fowler et al.
2011) and, in West Africa, oil palm plantations accumulated almost 3 Mg of carbon
ha−1 yr−1 (Thenkabail et al. 2004). However, the drainage of peatswamp forests in
Southeast Asia for palm oil production leads to large losses of above- and
below-ground carbon as well as the carbon sequestration capacity of further peat
accumulation (Germer and Sauerborn 2007; Koh et al. 2011). Therefore, increasing
yields per unit area, incentivizing smallholder systems and prioritizing conversion of
anthropogenic grasslands should be priorities for future oil palm production (Sayer
et al. 2012).
Although oil palms maintain large leaf areas throughout the year reaching a
maximum LAI over 7 (Gerritsma and Soebagyo 1999) and maximum assimilation
rates of over 14 μmol m−2 s−1 (Legros et al. 2009), they exhibit large stomatal
control over transpiration responding to both soil drought and high vapor pressure
deficits (Smith 1989; Dufrene and Saugier 1993). Even though about 43 % of total
biomass in oil palm plantations is located in the root systems, the ratio of tran-
spiration to potential evapotranspiration decreased from about 0.7 under
well-watered conditions to a minimum of around 0.35 during the dry season
(Dufrene et al. 1992). In a comparison of a rainforest and oil palm plantation site in
Southeast Asia, the oil palm plantation exhibited about twice the net primary
productivity even though both sites had similar LAI of around 6 (Fowler et al.
2011). The oil palm plantation also had larger latent heat fluxes that accounted for a
larger portion of the available energy compared to the rainforest (Fowler et al.
2011). However, the oil palm plantation also exhibited about 25 % higher emissions
of nitrous oxide (N2O) likely due to its fertilization and over five times greater total
volatile organic compound (VOC) emissions than the rainforest site (Fowler et al.
2011). VOC emissions in the oil palm plantation were largely comprised of iso-
prene (Fowler et al. 2011; Misztal et al. 2011) and these emissions were correlated
with sensible heat flux indicating that VOC emissions could increase with tem-
perature increases due to climate change (Misztal et al. 2011). VOCs have the
potential to react with NOx compounds in the atmosphere to form tropospheric
Palm Physiology and Distribution in Response … 85

ozone which has negative effects on human health, crop yields and climate change.
While ozone levels did not differ above the oil palm plantation and an adjacent
rainforest site, increased industrialization in the area and increasing release of NOx
compounds could increase tropospheric ozone to detrimental levels (Hewitt et al.
2009).

Physiology, Growth and Potential Future Distributions

of Palms Under Environmental Change

Environmental Drivers of Palm Distributions

The foreseeable future is one of increasing atmospheric [CO2], increasing tem-

peratures, and an intensified water cycle, albeit with highly variable and uncertain
changes in regional hydrology (Hartmann et al. (2013), pp 201–204). The uncer-
tainty in future regional hydrology, in particular, makes forecasting future palm
responses difficult. Globally, precipitation is one of the most important predictors of
palm species richness followed by modern day temperature and temperature
changes occurring throughout the Quaternary (Kissling et al. 2012). In continental
scale studies of palm species distributions, water availability was the most impor-
tant predictor of palm species richness (Bjorholm et al. 2005; Blach-Overgaard
et al. 2010). For the African continent, the majority of palm species distributions
responded positively to increasing precipitation and peaked in tropical rainforest
climates with a few species preferentially located in low precipitation regimes
(Blach-Overgaard et al. 2010). Again, temperature had little effect but spatial
constraints were significant and may indicate dispersal limitations from historical
refugia (Blach-Overgaard et al. 2010). The low species richness on the African
continent compared to the Neotropics and Southeast Asia may also reflect the
strong climatic changes that pre-date the Quaternary (Kissling et al. 2012). On
islands, palm species richness is most strongly controlled by habitat heterogeneity,
area, and geological origin (Kissling et al. 2012).
For the Neotropics, Bjorholm et al. (2005, 2006) report that annual precipitation,
number of wet days, latitude and soil fertility were identified as strong predictors of
species richness, with temperature and habitat being relatively unimportant.
Svenning et al. (2008) also found that high net diversification and species richness
in palms was associated with decreasing absolute latitude and increasing water and
energy availability with the greatest species richness found in areas that maintained
favorable environments for palm diversification throughout the Cenozoic. Kreft
et al. (2006) found that precipitation and actual evapotranspiration were the
strongest single predictors of palm species richness in addition to latitude whereas
potential evapotranspiration and temperature had relatively low importance. It is
interesting to note that latitude as a predictor was significant even when environ-
mental variables of rainfall and temperature were included in models (Bjorholm
et al. 2005; Kreft et al. 2006; Svenning et al. 2008), which may indicate that energy
86 H.J. Renninger and N.G. Phillips

availability or historical biogeography are also key determinants in palm species

richness. The importance of latitude in neotropical palm species richness may also
be an area effect with the largest land area available to palms located closest to the
Equator due to the geography of the Americas (Chown and Gaston 2000; Svenning
et al. 2008). In a comparison of rare versus more widespread palm species, Kreft
et al. (2006) found that while climatic factors were most strongly associated with
species richness in widespread species, rare species were more strongly predicted
by topographic complexity. Therefore across the Neotropics, the highest palm
species richness occurred in grid cells with >3000 mm of annual precipitation in
both lowland and montane habitats (Kreft et al. 2006). Palm species richness pat-
terns at the subfamily level in the Neotropics also reflects historical dispersal routes
of each group with the Arecoideae being most strongly controlled by modern day
environmental variables reflecting its long presence throughout South and Central
America while Coryphoideae species richness shows strong bias toward North and
Central America due to its northern dispersal route and the Calamoideae exhibits
bias towards South America due to its long history in this region (Bjorholm et al.
2006). Likewise, long-term climate stability appears to be important as regions with
the highest palm species richness have remained wet throughout the climatic
changes occurring in the Pleistocene (Bjorholm et al. 2005).
At more local and regional scales, other environmental and habitat factors pre-
dicting palm species richness and density become significant. In the western
Amazon basin, Vormisto et al. (2004) found that the only environmental determi-
nants of palm species patterns were soil cation concentration and texture while
dispersal limitation also played a role with climatically similar locations exhibiting
significant differences in species composition. Kristiansen et al. (2011) found that
local species diversity in the western Amazon basin was most strongly controlled by
precipitation seasonality while regional species diversity was most strongly con-
trolled by long-term habitat stability. In a study of seven palm species at La Selva
Biological Station, Costa Rica, abundance of tall palm individuals varied with
topography being highest on slope crests and steeper slopes and lowest in areas with
shallow slopes or lowland flat terrain (Clark et al. 1995). This pattern is unrelated to
small palms of each species available for recruitment but could be inversely related
to soil fertility (Clark et al. 1995). Kristiansen et al. (2009) compared factors of palm
species abundance at the local, regional and continental scales across the Neotropics
and found that topographic niche breadth and stem height were the most important
determinants of palm species abundance. Vormisto et al. (2004) also found that tall
palm species tended to have wider geographical ranges which may relate to their
increased dispersal ability (Kristiansen et al. 2009) and more generalized habitat
needs compared with other palm growth forms. Therefore, regionally, climatic
history, environmental factors, terrain and palm-specific characteristics all interact to
determine species composition in a given area.
Topography and hydrology have also been shown to affect palm species richness
and abundance on a regional basis. In Amazonian Ecuador, 17 % of individuals in
terra firme locations were palms compared to almost twice that percentage in
floodplain forests (Fig. 7, Balslev et al. 1987). In Amazonian Brazil, locations with
Palm Physiology and Distribution in Response … 87

Fig. 7 A grouping of Bactris sp. palms growing along the floodplain of an oxbow lake at Tiputini
Biodiversity Station in eastern Ecuador

waterlogged soils had over two times the density of palm individuals compared to
terra firme locations (Peres 1994). However, these waterlogged locations are typ-
ically dominated by only a few species of palms, and therefore, exhibit lower
species richness than terra firme locations (Kahn and Mejia 1990, 1991; Eiserhardt
et al. 2011b). Many permanently inundated swamps in the Amazon basin are
dominated by the palm Mauritia flexuosa (Fig. 8) which has been estimated to have
a population of 1.5 billion stems covering around 3 million hectares across the
region (Ter Steege et al. 2013). Likewise, these waterlogged regions in the tropics
are significant sources of carbon sequestration (Vegas-Vilarrubia et al. 2010) and
their low species richness compared to terra firme forests could make ecological
modeling studies in these palm swamps more tractable.

Potential Effects of Global Change on Palm Distributions

and Individual Physiology

Global increases in temperature have the potential to affect both palm species
distributions as well as individual palm functioning within ecosystems. For indi-
viduals, the large respiration load from the abundance of living parenchyma cells
within stems has the potential to negatively affect carbon balance under warmer
temperatures (Henson 2004). Likewise, increases in temperature may also lead to
increases in atmospheric vapor pressure deficits (VPD). Stomatal conductance in
palms has been shown to be sensitive to increasing VPD (Smith 1989;
Shivashankar et al. 1991; Dufrene and Saugier 1993; Repellin et al. 1997; Prado
et al. 2001; Renninger et al. 2010) leading to greater stomatal closure and poten-
tially limiting carbon gain as a result of increasing temperatures.
88 H.J. Renninger and N.G. Phillips

Fig. 8 Permanently inundated palm swamp in Amazonian Ecuador dominated by Mauritia

flexuosa (L.f.)

In terms of overall palm species distributions, temperature limitations restrict

palms to tropical and warm-temperate latitudes. Eiserhardt et al. (2011a) found that
the ability of either water or energy to predict palm species richness shifted with
latitude within the tropical/subtropical region such that energy became more
important at increasing latitudes. Because palms cannot withstand low freezing
temperatures (Tomlinson 2006), their presence/absence in the fossil record can be
used to track past climates and changes between freezing and non-freezing con-
ditions (Archibald et al. 2014). Notably, of the palm species that extend furthest
into the higher latitudes (Table 1), most belong to a single subfamily, the
Coryphoideae (Morley 2000; Couvreur et al. 2011; Thomas and De Franceschi
2013). These subtropical palms are considered to be relict taxa with low net
diversification rates and are remnants of a time when tropical forests extended into
the boreal zone during the Paleocene-Eocene (Svenning et al. 2008). Cooling
temperatures in the Cenozoic lead to widespread extinction of palms in regions
outside of the tropics (Svenning et al. 2008). Moreover, within this subfamily, most
Palm Physiology and Distribution in Response … 89

Table 1 Selection of palms occurring furthest from the tropics

Subfamily Genus Species Height (m) Leaf form Maximum
latitude
Arecoideae Jubaea chilensis 15 pinnate 36oS
Arecoideae Rhopalostyls sapida 15 pinnate 44oS
Coryphoideae Chamaerops humilis 5 palmate 44oN
Coryphoideae Sabal mexicana 15 costapalmate 30oN
Coryphoideae Sabal minor 2 palmate/ 30oN
costapalmate
Coryphoideae Sabal palmetto 20 costapalmate 34oN
Coryphoideae Trachycarpus fortnuei 10 palmate 46oN
Coryphoideae Washingtonia filifera 15 palmate 35oN
Coryphoideae Washingtonia robusta 22 palmate 35oN

genera occurring at latitudinal extremes are members of the tribe Corypheae.

General characteristics like maximum palm height or leaf type are not consistent
among palms occurring at latitudinal extremes (Table 1). However, a characteristic
common of the Coryphoideae is two or more relatively small diameter vessel
elements per vascular bundle (as opposed to only one or two larger diameter vessel
elements in other subfamilies), and may confer a relatively greater level of freezing
and drought tolerance to members in this subfamily (Thomas and De Franceschi
2013). Certain members of the Coryphoideae have, in recent decades, been
increasing their latitudinal range, including Trachycarpus fortunei (Hook.) H.
Wendl. (Walther et al. 2007), Washingtonia filifera (Lindl.) H. Wendl. (Cornett
1991), Chamaerops humilis L. and species in the genus Sabal (Lockett 2004). How
species within this subfamily are able to withstand occasional freezing conditions
and maintain functionality has not been studied extensively and requires further
attention.
Frost resistance and subzero temperature effects on photosynthesis, survival and
distribution were studied in Euterpe edulis, a tree palm species of the Atlantic
Forest, near the southern limit of the species distribution (Gatti et al. 2008). Euterpe
edulis is absent from forest stands in valley bottoms. Subzero temperatures are
observed in the lowest site, but the medium and higher elevation sites never
experienced absolute minimum temperatures below 0 °C. This palm species can
exhibit substantial supercooling (temperatures can be lowered experimentally down
to the ice nucleation temperature without extracellular ice formation). Ice formation
was observed at about −4 °C, relatively close to the equilibrium freezing temper-
ature, only after an increase in ambient humidity resulted in dew formation, trig-
gering ice seeding on the plant surface (Gatti et al. 2008). Dew formation is
commonly observed in valleys during the mild winter season of the subtropics. This
observation gives further support to the hypothesis that strong infrequent frost
events could be an important environmental factor determining the spatial distri-
bution pattern of palm species in their latitudinal limit of distribution despite the
90 H.J. Renninger and N.G. Phillips

capacity to avoid low subzero temperatures by supercooling. As extremes of cold

continue to move poleward, it seems reasonable to expect that these species may
follow suit, as is occurring, for example, with successfully established and repro-
ducing populations of Trachycarpus fortunei in southern Switzerland (Walther et al.
2007).
While altered regional water availability is inherently difficult to forecast, its
impacts, along with a more predictable regional warming, seem relatively clear on
palm physiology and growth. We understand less about potential impacts of other
global changes, including increased [CO2], nitrogen deposition, changes in local or
regional wind intensity and patterns (Bichet et al. 2012), and the potential inter-
active effects among these environmental factors on palm physiology and growth.
However, it is possible to speculate on how palms may respond to a combination of
changes in the above-mentioned environmental variables, based upon the basic
constraints of the monopodial growth form and associated features described ear-
lier. For example, while research is increasingly showing that trees with secondary
growth show continuous girth growth through old age and large size (Sillett et al.
2010; Stephenson et al. 2014), and that girth growth in old trees may be responding
to global environmental change (Phillips et al. 2008), this primary degree of free-
dom in secondary girth growth is not available to palms, and continuous addition of
stem tissues can only occur primarily along the axial dimension. This creates an
uncertain set of potential costs and benefits to palms given environmental change.
Our research (Renninger et al. 2009; Renninger and Phillips 2010) has demon-
strated that gas exchange in the tallest palms in a species was not hydraulically
limited, so frond carbon uptake could be enhanced with an increase in atmospheric
[CO2]. This is a necessary, if not sufficient, condition for a growth response to
elevated [CO2], and it may be that height growth is ultimately limited by gravity
and its effects on turgor pressure of expanding leaf cells (Woodruff et al. 2004).
Nevertheless, even if elevated [CO2] could promote increased net carbon uptake
and further height growth in palms, it is not clear if benefits of enhanced light
capture of taller palms in closed canopy forests may outweigh costs to mechanical
stability. This mechanical stability may be as much about the impacts of neigh-
boring trees on palm mechanical stability as it is about the intrinsic ability of taller
palms to withstand winds (Zimmerman et al. 1994).
In open-grown conditions, palms have little ability to modify crown form to the
extent that dicotyledonous branching trees can (Mäkelä and Sievänen 1992), and it
is difficult to imagine how a vertical growth response to elevated [CO2] could be of
physiological benefit. Impacts on reproductive structures or respiration components
of palm carbon budgets are even less well known, although research has shown
substantial effects of elevated [CO2] on non-structural carbohydrates and secondary
compounds in palm seedlings, e.g., Ibrahim and Jafaar (2012). Perhaps even more
so than for taller palms in closed-canopy forests, the cost of mechanical stability
may limit increases in open-grown palm height. While there appears to be a global
tendency toward reduced mean winds associated with climate change (Bichet et al.
2012), extreme weather events containing high gusting winds that can contribute to
palm windthrow are expected to increase (Hartmann et al. (2013), pp 216–217).
Palm Physiology and Distribution in Response … 91

In spite of the fundamental difference in growth of palms compared to trees

displaying secondary growth, a fundamental similarity may be that all plants must
grow. To paraphrase Bob Dylan, not growing means dying. Since fronds cannot
live indefinitely, their replacement in arborescent species necessitates stem exten-
sion, and while it appears that frond turnover may slow down with palm age and
size (De Steven et al. 1987; Lugo and Rivera Batlle 1987; Renninger and Phillips
2010), vertical growth is an unavoidable and irreversible condition in the life of an
arborescent palm. On the other hand, vertical growth may cease in trees exhibiting
secondary growth even as girth growth continues. In aging, tall statured forests, and
in an era of environmental change which may under some conditions increase the
growth of both palms and other trees while it simultaneously poses risks to them
(e.g., windthrow), the costs and benefits of constrained girth growth versus vertical
growth, a potentially larger respiration load, and limited options in terms of canopy
form may make for a relatively more precarious future for palms. However, palms,
in one form or another, have been in existence since the late Cretaceous (Berry
1914; Kvacek and Herman 2004; Harley 2006) experiencing both warmer and
colder global climates than the present as well as a strong capacity to compete with
dicot species in the tropics.

Conclusions

Based on the physiological constraints of palms compared with dicot species as

well as studies of palm distributions and species richness patterns at various scales,
water availability and hydrologic factors are of critical importance in explaining
current patterns of palm abundance and richness. Therefore, alterations of precip-
itation patterns and soil moisture regimes with climate change have the potential to
alter palm abundance and species richness in tropical and subtropical forests with
subsequent changes in forest functioning. Palms play an important role in many
tropical ecosystems as a food source for mammals (Wright et al. 2000; Silva and
Tabarelli 2001; Svenning 2001; Fragoso et al. 2003; Galetti et al. 2006) with the
most important seed dispersers in the Neotropics being ungulates, primates and
rodents (Fig. 9, Andreazzi et al. 2009). Fruits from palms were found to be available
throughout the year and during the dry season making them an important food
source for frugivores (Terborgh 1986; De Steven et al. 1987; Peres 1994;
Ratsirarson et al. 1996). In addition, permanently waterlogged tropical locations
tend to be dominated by palms that provide a large resource of nesting habitat for
macaws (Ara sp.) (Bonadie and Bacon 2000; Brightsmith and Bravo 2006). Palms
may also be important for reforestation of disturbed, seasonally dry forests as their
columnar structure prevents colonization by lianas and may facilitate the growth of
late successional tree species (Salm et al. 2005). Therefore, changes in precipitation
patterns and the associated changes in hydrology have the potential to alter palm
distributions in the tropics and could affect the associated ecosystem services that
palms provide. Likewise, increasing temperatures may expand the range of palms to
92 H.J. Renninger and N.G. Phillips

Fig. 9 Spider monkey

(Ateles belzebuth E. Geoffroy)
in the canopy of an Iriartea
deltoidea (Ruiz & Pav.) palm.
These primates are one of the
main seed dispersal agents of
this palm species (Henderson
1990)

higher elevations (Kessler 2000) and higher latitudes provided they are not limited
by dispersal and that their agents of seed dispersal (birds, mammals) are not affected
by human activities. What remains clear is that palms have survived for millions of
years and withstood significant global change providing evidence of their adapt-
ability as a plant family and/or their ability to disperse to their preferred environ-
mental conditions. Their unique anatomical and physiological attributes have
proved successful across the tropics and have allowed them to successfully compete
with woody dicot tree species.

Acknowledgments HJR acknowledges the National Science Foundation East Asia and Pacific
Summer Institute program for support during 2008 (NSF grant OISE – 0813242). NGP and HJR
acknowledge the National Science Foundation for research support (NSF grant IOB #0517521).

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Carbon Allocation and Water Relations
of Lianas Versus Trees

Paula I. Campanello, Eric Manzané, Mariana Villagra,

Yong-Jiang Zhang, Adela M. Panizza, Débora di Francescantonio,
Sabrina A. Rodriguez, Ya-Jun Chen, Louis S. Santiago
and Guillermo Goldstein

Abstract Despite lianas being fundamental components of tropical and subtropical

forest ecosystems throughout the world, the physiological characteristics of this
growth form are not well known. Different behaviors at the seedling stage were
until recently largely unnoticed. In one extreme of a continuum of adaptive traits,
freestanding liana seedlings invest a large proportion of biomass in self-support
tissue while on the other extreme support-seeker seedlings invest more resources in
rapid elongation of slender stems with an efficient hydraulic conductive system.
Adult lianas often have lower wood density and higher specific leaf area than trees
and have most of their leaves deployed at the top of the canopy, experiencing high

P.I. Campanello (&)
M. Villagra
A.M. Panizza
D. di Francescantonio
S.A. Rodriguez

Laboratorio de Ecología Forestal y Ecofisiología, Instituto de Biología Subtropical,
CONICET, FCF, Universidad Nacional de Misiones, Puerto Iguazú, Argentina
e-mail: pcampanello@gmail.com; pcampanello@conicet.gov.ar
M. Villagra
e-mail: marian.villagra@gmail.com
A.M. Panizza
e-mail: adelamariapanizza@gmail.com
D. di Francescantonio
e-mail: debodifra@gmail.com
S.A. Rodriguez
e-mail: sabrinarodriguez78@yahoo.com.ar
E. Manzané
L.S. Santiago
Smithsonian Tropical Research Institute, Balboa, Panama Apartado Postal 0843-03092,
Republic of Panama
e-mail: bioerman@gmail.com
L.S. Santiago
e-mail: santiago@ucr.edu
Y.-J. Zhang
Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA
02138, USA
e-mail: yongjiangz@126.com

© Springer International Publishing Switzerland 2016 103

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_5
104 P.I. Campanello et al.

irradiance and transpirational demands, which requires effective regulation of water

loss to avoid desiccation. Recent studies show that lianas have faster stomatal
responses to increasing vapor pressure deficit (VPD) and exhibit stronger partial
stomatal closure compared to trees. Strong stomatal control and efficient water
transport help lianas maintain leaf water potential (Ψleaf) within a safe hydraulic
range to avoid xylem dysfunction despite their low stem water storage capacity,
which is achieved at a minimum cost in terms of carbon assimilation. Liana col-
onization of tree crowns can significantly reduce tree growth and transpiration with
consequences for carbon and water economy at individual tree and ecosystem
levels.

Keywords Capacitance

Freestanding liana seedlings

Support-seeker liana




seedlings Stomatal conductance Transpiration Long distance water transport

Introduction

Lianas or woody vines are fundamental components of tropical and subtropical

forests. Their importance in forest ecology and functioning has been recently rec-
ognized with increasing studies all around the world, and particularly in tropical
forests, where lianas can contribute up to 35 % of woody plant diversity and 40 %
of stem density (Gerwing and Farias 2000; Chave et al. 2001; Schnitzer and
Bongers 2002, 2011). For more than 30 years, research mainly focused on com-
munity and population-level processes and evaluation of the detrimental conse-
quences that lianas have on trees, rendering a relatively good understanding of their
effect on forest dynamics (Putz 1984a, b; Pinard and Putz 1994; Alvira et al. 2004).
More recently, ecophysiological studies comparing lianas and trees have
enhanced our knowledge of the physiological and morphological behavior of lianas

Y.-J. Zhang
Y.-J. Chen

Key Laboratory of Tropical Forest Ecology, Xishuangbana Tropical Botanical Garden,
Chinese Academy of Sciences, Mengla 666303, Yunnan, China
e-mail: chenyj@xtbg.org.cn
L.S. Santiago
Department of Botany & Plant Sciences, University of California, Riverside, CA 92521, USA
G. Goldstein
Laboratorio de Ecología Funcional, Departamento de Ecología Genética y Evolución,
Instituto IEGEBA (CONICET-UBA), Facultad de Ciencias Exactas y naturales, Universidad
de Buenos Aires, Buenos Aires, Argentina
e-mail: gold@bio.miami.edu; goldstein@ege.fcen.uba.ar
G. Goldstein
Department of Biology, University of Miami, Coral Gables, FL 33146, USA
Carbon Allocation and Water Relations of Lianas Versus Trees 105

(Cai et al. 2008, 2009; Johnson et al. 2013; van der Sande et al. 2013; Santiago
et al. 2015). However their water and carbon economy are still not well known.
Lianas tend to grow rapidly and climb suitable host trees covering most of the
upper canopy where incoming solar radiation is high. Individuals reaching tree
crowns also act as climbing supports, facilitating the access of other lianas to the
upper canopy (Putz 1984a, b; Nabe-Nielsen 2001; Campanello et al. 2007). Lianas
may colonize new gaps delaying gap-phase regeneration processes and the recovery
of a tall mature forest (Schnitzer et al. 2000). They also have detrimental direct
effects on trees, decreasing growth and fecundity and increasing mortality rates
(Nabe-Nielsen et al. 2009; Hegarty and Caballe 1991; Grauel and Putz 2004;
Kainer et al. 2006; Nabe-Nielsen et al. 2009; van der Heijden and Phillips 2009;
Ingwell et al. 2010; Schnitzer and Carson 2010). This positive feedback loop
between disturbance and liana abundance may partially explain increasing liana
abundance and tree infestation in disturbed neotropical Forests (Fig. 1), with pro-
found consequences for biogeochemical cycles (Phillips et al. 2002; Schnitzer and
Bongers 2011; Wright et al. 2004a). In contrast to neotropical forests, liana
abundance in African and Asian tropical forests is stable or even decreasing in some
cases (Schnitzer and Bongers 2011). Global change effects, such as increasing
evaporative demand and CO2 concentration or nitrogen deposition have all been
pointed out as responsible for this pattern (Schnitzer 2015). However, the causes of
increasing liana biomass in neotropical forest remain unknown (Wright et al. 2015).

Fig. 1 Location of study sites around the world examining the abundance change of lianas
through time. Black circles indicate sites where liana abundance or density increased, white circles
indicate sites where liana abundance or density decreased and grey circles indicate no change over
time. Data are from Phillips et al. (2002), Wright et al. (2004a, b, 2015), Wright and Calderón
(2006), Ingwell et al. (2010), Schnitzer et al. (2012), Laurance et al. (2014), Yorke et al. (2013),
Enquist and Enquist (2011), Chave et al. (2008), Caballé and Martin (2001), Bongers and Ewango
(2015), Thomas et al. (2015), Allen et al. (2007), Londré and Schnitzer (2006) and Campanello
et al. (2012)
106 P.I. Campanello et al.

Recognizing functional and morphological differences among lianas is essential

for understanding spatial and temporal patterns of liana abundance. We need to
move from a simplistic perspective in which all lianas conform to a unique
“climbing habit” towards a more mechanistic view in which species are recognized
as having different physiological behaviors and life history traits. Are all liana
species increasing or decreasing in abundance in forests where temporal patterns of
liana change have been documented? Do freestanding versus support-seeking
strategies differ in their colonization ability? Are lianas able to regulate water loss to
avoid desiccation at the top of the canopy where they experience high transpira-
tional demands? To address these and other questions, in this chapter we explore
how different liana species balance their carbon and water economies compared to
trees, as well as the impacts of lianas on their host species.

Liana Seedlings in Tropical Forests

Plant seedlings in general, and liana seedlings in particular, due to their need for using
hosts to climb and reach a reproductive age, are susceptible to high mortality rates.
Liana seedlings vary in how they access host plants, with freestanding seedlings,
which can grow without mechanical support and can remain as small woody plants for
a relatively long period of time, at one end of the spectrum, and support-seeking
seedlings, which reach for a host tree very early in their life cycle at the other end of
the spectrum (Putz 1984a, b; Rowe and Speck 2005; Manzané 2012). Contrasting
seedling forms have important implications for carbon allocation because freestanding
liana seedlings may invest more in mechanical tissues and less in stem and root
extension than support-seekers. This pattern of biomass allocation is comparable to
life-history characteristics described for early—versus late-successional tree seedlings
(Denslow 1980; Swaine and Whitmore 1988; Kitajima 1994). To assess for potential
differences in life history traits of both types of liana seedlings, seeds of eight species
were collected in lowland tropical forests in Panama and were grown in a shade house
(55.70 μmol m−2 s−1 photon flux density, PFD) without any structural support for
12 months. The percentage of the seedlings that bent more than 45° from the upright
position was recorded and used along with other characteristics to determine free-
standing or support seeking behavior (Table 1). After 3 months, seedlings of three of
the liana species started to bend naturally without the presence of any structural
support, and after 12 months of growth, 30–60 % of the individuals of those three
species deviated substantially from the vertical position (Fig. 2). None of the other
seedlings bent after 12 months of growth. The support-seekers had smaller stem cross
sectional area and total leaf area per individual than the freestanding seedlings, but all
species conformed to the same functional relationship between leaf and stem cross
sectional area (Fig. 3). Total leaf surface area per plant was 350 cm2 for the four
support-seekers and 850 cm2 for the four freestanding species.
Carbon Allocation and Water Relations of Lianas Versus Trees 107

Table 1 Species used for the experiments, including species authority name, family and the
hypothesized functional group
Species Family Functional group
Acacia hayesii Benth. Fabaceae SS
Amphilophium crucigerum (L.) L.G. Lohmann Bignoniaceae SS
Serjania atrolineata C. Wright Sapindaceae SS
Machaerium milleflorum Pittier Fabaceae SS
Petrea volubilis L. Verbenaceae F
Cnestidium rufescens Planch. Connaraceae F
Callichlamys latifolia (Rich.) K. Schum. Bignoniaceae F
Tontelea passiflora (Vell.) Lombardi Celastraceae F
SS = support-seekers, F = freestanding. Adapted from Manzané (2012)

Fig. 2 Liana seedling species bending without the presence of any structural support during
12 months of growth in a greenhouse. Species abbreviations are: Cal lat, Callichlamys latifolia;
Amp cru, Amphilophium crucigerum; Aca hay, Acacia hayesii; Mac mil, Machaerium milleflorum;
Ton pas, Tontelea passiflora; Ser atr, Serjania atrolineata; Pet vol, Petrea volubilis and Cne ruf,
Cnestidium rufescens. Each value corresponds to a species mean. Adapted from Manzané (2012)

The support-seekers had higher specific leaf area (leaf area divided by leaf mass;
SLA), suggesting that these leaves had lower construction costs (Poorter et al.
2009), and lower maximum photosynthetic electron transport rate (ETRmax) per leaf
area, than freestanding species (Fig. 4). These differences persist in a mass-based
estimation of ETRmax, indicating that freestanding seedlings with a larger total leaf
surface area and greater photosynthetic capacity per leaf area and mass should
assimilate carbon and accumulate biomass faster than support-seekers.
108 P.I. Campanello et al.

Fig. 3 Relationship between total leaf area and stem cross sectional area for support-seeker and
freestanding liana saplings after 18 months of growing in greenhouse conditions. An exponential
function was fitted to the data, y = 1475.5*(1−exp(−0.0302*x)). Species abbreviations are as in
Fig. 2. Each value corresponds to a species mean. Adapted from Manzané (2012)

Fig. 4 Relationship between specific leaf area (SLA) and maximum electron transport rate
(ETRmax), for support-seeker and freestanding liana saplings. A linear function was fitted to the
data, y = 85.67–0.23x. Species abbreviations are as in Fig. 2. Each value corresponds to a species
mean. Adapted from Manzané (2012)

There appear to be tradeoffs in resource allocation across both liana groups.

Species with freestanding seedlings invest more in self-support tissue as shown by
higher cross sectional stem area than support-seekers, whereas support-seekers
Carbon Allocation and Water Relations of Lianas Versus Trees 109

invest more resources for rapid elongation of comparatively slender stems.

Additionally, freestanding species have a less efficient water transport system than
support-seekers at a comparable age (Manzané 2012). The differences in carbon
allocation may mean that freestanding seedlings remain under forest canopy for
long periods of time and perhaps are more shade tolerant than support-seekers.
Support-seekers, in contrast, may rapidly seek higher light levels by finding suitable
host plants and climbing earlier (Gianoli 2015), and may do so with a relatively low
biomass cost of thin, high SLA leaves with low photosynthetic capacity. This
ecological correlate of the physiological trait differences between support-seekers
and freestanding species needs to be experimentally tested, particularly through
studies exploring ontogenetic changes. For example, support-seekers might com-
pletely change their metabolism after finding a support plant and growing towards
light (Gianoli 2015).
There is currently relatively little data available comparing the physiological
traits of liana and trees seedlings. However, in one recent study, Pasquini et al.
(2015) hypothesized that lianas should be more limited by soil resources than trees
because of their fast growth rates, prevalence in regenerating forest, and affinity for
high-nutrient sites. Using a fully replicated factorial nutrient addition experiment
with nitrogen, phosphorus, and potassium, applied alone and in all combinations for
more than a decade, the authors showed that phosphorus limits the photosynthetic
performance of both trees and lianas in deeply shaded understory habitats, but that
lianas always showed significantly greater ETRmax, photosynthetic quenching, and
saturating light levels across all treatments (Pasquini et al. 2015). There was little
evidence for nutrient-by-growth form interactions, indicating that lianas were not
disproportionately favored in nutrient-rich habitats.

Patterns of Liana Growth and Crown Colonization

Studies on biomechanical properties, morpho-functional traits and biomass allo-

cation could help to understand patterns of spatial distribution of lianas at a local
and global scale as well as trends in liana abundance changes trough time. Some
lianas can develop effective climbing behavior and specialized flexible stems
without highly specialized organs of attachment. This is linked to a high degree of
developmental plasticity in early stages of growth (Menard et al. 2009). The stiffest
stems, those having the highest values of Young’s modulus of elasticity, belong to
saplings and leaning stems. Only when climbing stems are securely anchored to
host trees does the liana develop highly flexible stem properties (low values of
Young’s modulus of elasticity). The change in stiffness during ontogeny is linked to
the development of wood with numerous large vessels and thin-walled fibers
(Menard et al. 2009). Lianas that climb via twining, tendrils or other specialized
attachment organs may not necessarily require developmental plasticity during
ontogeny in terms of biomechanics and stem anatomy.
110 P.I. Campanello et al.

Adult liana species differ in stem anatomical characteristics. For example, if

freestanding liana seedlings conserve their physiological and anatomical charac-
teristics after climbing the host tree, they should have higher wood density and
narrower vessels than support-seeker lianas after reaching the canopy. The vascular
systems of many lianas have specialized tissues that prevent stem breakage, dis-
sipate torsional stress, increment parenchyma storage tissue, and maintain xylem
and phloem transport during stem twisting (Putz and Holbrook 1991). Several
neotropical lianas have stems with xylem cylinders distributed into several stems
that form crowns in the canopy organized into multiple small crowns, while lianas
with a unique xylem cylinder tend to occupy the canopy of the support tree with
only one densely packed crown (Caballé 1993).
This different pattern of crown colonization of lianas associated with different
stem anatomy and the predominance of either freestanding or support-seeking
behavior may partially explain the increase or decrease in liana abundance in
tropical forests around the world. For example, in the tropical forest of Barro
Colorado Island, Panama, almost all of the support-seeking liana species are
increasing in abundance, while freestanding seedlings tend to increase at slower
rates with some species even decreasing in population size (Manzané 2012).
Biomass allocation to leaves and climbing stems should differ among tropical
and subtropical lianas. In a temperate Japanese forest species, lianas that are
abundant in forest edges, allocate a larger proportion of shoot biomass to climbing
stems, whereas liana species growing inside the forest stands allocate relatively
more biomass to leaves (Ichihashi et al. 2010; Ichihashi and Tateno 2011). Both
groups of liana species have different impacts on tree growth. Studies of tropical
lianas focusing on biomass allocation patterns and climbing behavior and the
relationship with their physiological performance are urgently needed.

Carbon and Water Economy of Lianas and Trees

Lianas are considered to be structural parasites because they use the stems of other
plants to reach the forest canopy (Schnitzer and Bongers 2002). As a consequence
of limited allocation to stems, lianas are supposed to have a higher proportion of
photosynthetic biomass per whole plant biomass compared to trees. This allocation
pattern apparently enables them to obtain more resources at faster rates, but this
hypothesis is based on limited data (Santiago et al. 2015). In a subtropical forest in
Argentina, liana species were able to recolonize the canopy of tree species 10 years
after after a cutting treatment was applied (Campanello et al. 2012). Yet, lianas can
lose substantial biomass in reaching the canopy, in part because shoots may fail to
find a host plant or due to the breakage of branches to which they are attached.
Consistent with low mechanical demands, the low density wood in lianas could
help to compensate for large biomass losses during climbing (Putz 1983), as well as
providing a hydraulically efficient xylem. Wood density and saturated water content
is shown in Table 2 for dominant tree species >10 cm diameter and abundant liana
Carbon Allocation and Water Relations of Lianas Versus Trees 111

Table 2 Traits of trees and lianas measured in a subtropical forest in northern Argentina
Species Family SLA WD WSWC
Trees
Ceiba speciosa (A.St.-Hil., A. Bombacaceae 150.7 ± 10.6 0.38 ± 0.02 2.12 ± 0.01
Juss. and Cambess.) Ravenna
Cedrela fissilis Vell. Meliaceae 121.7 ± 4.1 0.46 ± 0.01 1.42 ± 0.00
Cordia trichotoma (Vell.) Borraginaceae 68.5 ± 5.3 0.54 ± 0.02 1.08 ± 0.01
Arráb. Ex Steud.
Cabralea canjearana (Vell.) Meliaceae 141.3 ± 6.9 0.56 ± 0.02 1.18 ± 0.00
Mart.
Ocotea diospyrifolia (Meisn.) Lauraceae 120.0 ± 5.8 0.57 ± 0.01 1.20 ± 0.00
Mez.
Chrysophyllum gonocarpum Sapotaceae 124.4 ± 9.7 0.64 ± 0.02 0.89 ± 0.00
(Mart. and Eichler)Engl.
Balfourodendron riedelianum Rutaceae 127.4 ± 8.0 0.71 ± 0.02 0.72 ± 0.01
(Engl.) Engl.
Lonchocarpus muehlbergianus Fabaceae 137.6 ± 4.9 0.71 ± 0.02 0.78 ± 0.01
Hassl.
Parapiptadenia rigida (Benth.) Fabaceae 126.6 ± 27.2 0.78 ± 0.01 0.62 ± 0.00
Brenan
Holocalyx balansae Micheli Fabaceae 134.4 ± 18.1 0.82 ± 0.01 0.62 ± 0.00
Lianas
Adenocalymma marginatum Bignoniaceae 91.5 ± 2.1 0.44 ± 0.01 1.53 ± 0.07
(Cham.) DC.
Amphilophium paniculatum Bignoniaceae 63.1 ± 4.8
(L.) Kunth
Aristolochia triangularis Aristolochiaceae 44.5 ± 7.6 0.27 ± 0.00 2.70 ± 0.04
Cham.
Schnella microstachya Raddi Fabaceae 57.4 ± 1.2
Condylocarpon isthmicum Apocynaceae 59.4 ± 6.4 0.44 ± 0.00 1.42 ± 0.01
(Vell.) A. DC.
Cratylia intermedia (Hassl.) L. Fabaceae 52.4 ± 5.3
P. Queiroz & R. Monteiro
Dicella nucifera Chodat Malpighiaceae 79.5 ± 8.8
Dioclea violacea Mart. ex Fabaceae 65.4 ± 1.4
Benth.
Forsteronia glabrescens Müll. Apocynaceae 95.1 ± 7.0
Arg.
Fridericia chica (Bonpl.) L.G. Bignoniaceae 56.4 ± 6.3
Lohmann
Fridericia florida (DC.) L.G. Bignoniaceae 84.3 ± 7.3
Lohmann
Gouania sp. Rhamnaceae 50.9 ± 4.2 0.44 ± 0.02 1.39 ± 0.10
Mansoa difficilis (Cham.) Bignoniaceae 81.1 ± 2.7 0.45 ± 0.02 1.56 ± 0.04
Bureau & K. Schum.
(continued)
112 P.I. Campanello et al.

Table 2 (continued)
Species Family SLA WD WSWC
Marsdenia macrophylla Apocynaceae 58.4 ± 6.4 0.35 ± 0.01 2.09 ± 0.03
(Humb. & Bonpl. ex Schult.) E.
Fourn.
Mascagnia divaricata (Kunth) Malpighiaceae 49.6 ± 8.5
Nied.
Peltastes peltatus (Vell.) Apocynaceae 47.6 ± 7.9
Woods
Pereskia aculeata Mill. Cactaceae 53.5 ± 1.0
Pisonia aculeata L. Nyctaginaceae 63.9 ± 4.4 0.43 ± 0.01 1.67 ± 0.10
Pristimera celastroides Celastraceae 100.5 ± 5.6 0.46 ± 0.01 1.41 ± 0.04
(Kunth) A.C. Sm.
Tanaecium mutabile (Bureau & Bignoniaceae 70.8 ± 4.7 0.56 ± 0.01 1.11 ± 0.03
K. Schum.) L.G. Lohmann
Tetracera oblongata DC. Dilleniaceae 139.6 0.40 ± 0.01 1.21 ± 0.03
Tynanthus micranthus Corr. Bignoniaceae 75.2 ± 21.3
Méllo ex K. Schum.
Species name, species authority, family, specific leaf area (SLA, cm2 g−1), sapwood density (WD,
g cm−3) and sapwood saturated water content (WSWC, %) are included. Values are means ± SE.
Unpublished information from Panizza et al.

species with stems >2 cm diameter in a subtropical forest in Argentina. Lianas have
on average lower wood density than trees and consequently higher saturated water
content (Fig. 5), a measure of potential maximum amount of stem water storage,

Fig. 5 Relationship between wood saturated water content (WSWC) and wood density for lianas
and trees. An exponential function was fitted to the data, y = 571.89 * exp (−2.94*x). Each value
corresponds to a species mean
Carbon Allocation and Water Relations of Lianas Versus Trees 113

which could contribute to maintain an adequate short-term water balance (Bucci

et al. 2004). Both lianas and trees fit the same negative exponential relationship
between wood saturated water content and wood density as shown in Fig. 5.
Studies of comparative maximum photosynthetic rates of trees and lianas across
a variety of tropical climates have been accumulating throughout the early 2000s
(Wright et al. 2004b; Santiago and Wright 2007; Cai et al. 2009; Zhu and Cao
2009). This data, combined with an expansive global dataset of liana and tree
nutrient concentration and chemistry on more than 7000 tree and liana species from
48 sites now clearly show that lianas have higher foliar concentrations of key
physiological elements such as nitrogen and phosphorus in sites with less than
2500 mm of annual precipitation, but that at greater precipitation or lower tem-
perature this advantage is lost and trees and lianas largely converge in leaf physi-
ology (Asner and Martin 2012). Thus when climate is taken into account,
differences in maximum photosynthetic rates of lianas and trees at drier sites (Cai
et al. 2009; Zhu and Cao 2009, 2010), and lack of differences at wetter sites
(Santiago and Wright 2007), are entirely consistent with global patterns of liana and
tree leaf traits (Santiago et al. 2015). Regardles of differences in net CO2 assimi-
lation between lianas and trees, the apparently higher proportion of photosynthetic
biomass at the whole plant scale for lianas compared to trees, might enable lianas to
grow relatively fast, which could be advantageous for reaching the upper forest
canopy.
Results of studies on subtropical forests in Northern Argentina are beginning to
show patterns similar to other studies on tropical forests (Wright et al. 2004b;
Santiago and Wright 2007; Zhu and Cao 2009); liana species have higher SLA
values than trees (Fig. 6a), consistent with the lower construction costs in lianas
than in trees. Furthermore, ETRmax in trees is higher than lianas in subtropical
forests in Argentina on a leaf area basis (Fig. 6b), but not on a mass basis (Fig. 6c),
consistent with the finding that leaf scale photosynthetic advantages in lianas dis-
appear as annual precipitation increases because mean annual precipitation in the
Argentinean study site is 2000 mm per year with no dry season. Subtropical forests

Fig. 6 Specific leaf area (SLA) (a), maximum electron transport rate (ETRmax) expressed on an
area basis (b) and on a mass basis (c), for lianas and trees. Bars are means + SE. The means were
compared between lianas and trees using a t-test SLA: t = 2.329, P = 0.027; ETRmax area: t = 2.
P = 0.032; ETRmax mass: 0.162, P = 0.872. Unpublished results from Panizza et al.
114 P.I. Campanello et al.

Fig. 7 Relationship between specific leaf area (SLA) and maximum electron transport rate
(ETRmax) for trees and lianas. A regression line was only fitted to liana species, y = 133.64–0.41x.
Each value corresponds to a species mean

in Argentina are geographically and taxonomically linked to seasonally dry forests

(Pennington et al. 2009). In this ecosystem tree species from humid and seasonally
dry forests co-occur, and a similar pattern was recently described for lianas (Malizia
et al. 2015). Interestingly, ETRmax on an area basis was negatively correlated with
SLA for lianas, and for lianas and trees (Fig. 7), but no correlation was found for
trees alone. This relationship for adult lianas in the subtropical forest in Argentina
was also observed for saplings in Panama as described above (Fig. 4), and suggests
that as a given mass of leaf tissue is spread over a smaller area, more photosynthetic
components can be packed into the leaf. According to the leaf economics spectrum,
photosynthetic capacity per unit leaf area is not necessarily expected to be directly
related to SLA (Wright et al. 2004b). But for lianas, higher SLA and likely thinner
leaves with lower construction costs are related to lower photosynthetic capacity per
unit leaf area.

Stomatal Control, Water Transport, and Diurnal Water

Balance in Lianas

Lianas, with most of their leaves on the top of the canopy, experience high tran-
spirational demands at midday, which requires them to effectively regulate water
loss to avoid desiccation. Leaf physiological processes can respond to changes in
soil water availability and vapor pressure deficit (VPD). The temporal scale of
changes in both environmental variables is different, with soil water availability
Carbon Allocation and Water Relations of Lianas Versus Trees 115

changing over the course of several days or weeks while VPD may change strongly
over the course of the day. A decrease in soil water and an increase in VPD may
induce water deficits and constrain carbon assimilation. By regulating the stomatal
aperture, lianas can limit water loss, keeping xylem tension within a safe range and
thus reducing the risks of xylem dysfunction (Brodribb and Holbrook 2003;
Brodribb et al. 2003; Johnson et al. 2011; Zhang et al. 2014). Variation in stomatal
conductance (gs) is mainly governed by stem (Ψstem) and leaf (Ψleaf) water
potentials, VPD, and abscisic acid (Comstock and Mencuccini 1998; Salleo et al.
2000; Brodribb et al. 2003; Bunce 2006; Chapotin et al. 2006). Failure of stomata to
respond quickly to the rapid increases in VPD could result in excessive dehydration
and consequently irreversible hydraulic dysfunction in the vascular system.
Stomatal regulation is thus an important safety valve, especially for canopy plants,
which frequently experience high evaporative demand.
Trees tend to have larger internal stem water storage than lianas, and thus trees
can use water from their stems to replace water loss through transpiration, whereas
lianas rely mostly on soil water (Chen et al. 2015). Exposure to the stressful
environment of the upper canopy does not limit lianas from colonizing the canopy.
Instead, lianas readily thrive and may form a carpet-like leafy layer at the top of the
forest in many tropical and subtropical forests. Lianas typically have wider and
longer vessels than trees and are reported to be hydraulically efficient but vulnerable
to drought induced cavitation (Isnard and Silk 2009; Zhu and Cao 2009; Johnson
et al. 2013; Chen et al. 2015). How lianas balance hydraulic efficiency with safety
and the role of stomatal regulation may be the key to understand the ability of lianas
to aggressively colonize treefall gaps in wet and seasonally dry forests (DeWalt
et al. 2000; Schnitzer 2005; Ledo and Schnitzer 2014).
Leaf and stem water potentials decline in both liana and tree species of a sub-
tropical forest in China during the daytime, with seven of the eight studied species
losing leaf turgor at around midday (Chen et al., unpublished information). Lianas
show a trend of larger disequilibrium between leaf and stem water potential than
tree species during the daytime (Table 3). The difference between minimum stem
and minimum leaf water potential (ΔΨ) is 1.50 MPa for lianas and 0.69 MPa for
trees. Clearly more data is needed to fully evaluate this, but if these differences
between lianas and trees in the driving force for water transport in the terminal
portion of the hydraulic continuum are robust when other species are measured, this
would suggest that lianas have smaller internal stem water storage compared to
trees and that the main source of water for transpiring leaves in lianas is the soil
available water. Trees often have relatively large stem water storage or capacitance
that can be used to replace transpiration water loss, particularly in the morning
(Goldstein et al. 1998). Minimizing the distances between water sources through
stem water storage appears to reduce differences between stem and leaf water
potentials in trees during periods of high evaporative demand.
116 P.I. Campanello et al.

Table 3 Traits of trees and lianas measured in a subtropical forest in China

Species Family Ks SE ΔΨ gs A
Trees
Celtis tetrandra Roxb. Cannabaceae 6.21 0.6 1.19 0.27 17.9
Ficus concinna (Miq.) Miq. Moraceae 3.95 0.7 1.13 0.14 5.8
Harpullia ramiflora Radlk. Sapindaceae 2.20 0.2 0.91 0.11 7.8
Michelia gioi (A. Chev.) Magnoliaceae 0.69 0.2 0.17 0.03 2.5
Sima and H. Yu
Streblus asper Lour. Moraceae 1.86 0.4 0.51 0.16 9.6
Lianas
Celastrus paniculatus Willd. Celastraceae 8.60 1.6 1.39 0.04 4.5
Marsdenia sinensis Hemsl. Apocynaceae 10.53 1.3 1.44 0.07 8.5
Ventilago calyculata Tul. Rhamnaceae 4.80 0.6 1.11 0.15 9.5
Specific hydraulic conductivity (KS ± SE, Kg m−1 s−1 MPa−1), Maximum difference between leaf
and stem water potentials during the day (ΔΨ, MPa), stomatal conductance at midday (gs, mol
H2O m−2 s−1), average daily net CO2 assimilation rates (A, μmol CO2 m−2 s−1). Unpublished
information from Chen et al.

Figure 8 shows the relationship between the maximum daytime differences of

disequilibrium between stem and leaf water potential versus maximum specific
hydraulic conductivity (Ks) for trees and lianas. The difference between stem and
leaf water potentials can be considered as an indirect measure of stem capacitance.
The difference in water potentials was multiplied by two, making the relative index
to range from 0 to 2. If both stem and leaf water potential differences are small (both
water potentials are well coupled) that means that the stem internal water storage is
relatively small. Across tree and liana species, the indirect index of stem capaci-
tance decreases exponentially with increasing Ks. In addition, it has been shown
before that liana stems tend to be narrow, additional evidence of their relatively low
stem water storage. Stomatal regulation is important for lianas not only because
internal stem water storage is relatively small but also because they have a higher
proportion of leaves exposed to the top of the canopy, where the VPD is high (Putz
1983). Lianas might have faster stomatal responses compared to trees and exhibit
stronger partial stomatal closure than trees (Table 3). Lianas might also reach
maximal gs at relatively lower (<1 kPa) VPD than trees, helping them to maximize
carbon assimilation in the morning. Strong stomatal control and efficient water
transport would help lianas maintain Ψleaf within a safe hydraulic range to avoid
xylem dysfunction despite their low stem water storage capacity, which is achieved
at a minimum cost in terms of carbon assimilation. Average daily net CO2
assimilation is 7.5 µmol m−2 s−1 for lianas and 8.7 µmol m−2 s−1 for trees (Table 3).
Carbon Allocation and Water Relations of Lianas Versus Trees 117

Fig. 8 A normalized index of water storage capacity |(2(−Ψleaf–Ψstem))| in MPa as a function of

specific hydraulic conductivity (Ks) for trees (grey circles) and lianas (black circles) from a
tropical forest in SE China. An exponential function was fitted to the data, y = 1.671 e−0.114x. Each
value corresponds to a species mean. Species abbreviations are: Cel pan, Celastrus paniculatus;
Mar sin, Marsdenia sinensis; Ven cal, Ventilago calyculata; Cel tet, Celtis tetrandra; Fic con,
Ficus concinna; Har ram, Harpullia ramiflora; Mic gio, Michelia gioi and Str asp, Streblus asper.
Unpublished information from Chen et al.

Liana Impact on Tree Carbon and Water Economy

Liana colonization of tree crowns was identified early as a limitation for timber
production in tropical forests. Removal of lianas before harvesting is traditionally
used to decrease tree damage during logging operations (Putz and Holbrook 1991;
Vidal et al. 1997; Alvira et al. 2004), and liana biomass in tree crowns reduces
growth rates of canopy trees between harvesting cycles (Putz and Holbrook 1991).
The effect of liana colonization on cumulative stem growth for nine tree species
differing in wood density in a relatively undisturbed subtropical forest in northern
Argentina is shown in Fig. 9. Trees with their canopy covered by more than 50 %
with liana leaves tend to grow slower than trees with little liana infestation.
Liana colonization on tree crowns in a disturbed subtropical forest in Argentina
increased from 69 to 83 % during a 10 years period (Campanello et al. 2012), and is
one of the highest liana abundance increases reported for neotropical forests (van
der Heijden et al. 2008; Ingwell et al. 2010). Taking into account the results shown
in Fig. 9, the potential tree biomass increment lost due to liana colonization should
be of considerable concern. Not all trees are equally affected by lianas. Trees of
118 P.I. Campanello et al.

Fig. 9 Monthly changes of cumulative stem growth from December 2011 to June 2014 of nine
tree species with more than 50 %, and less than 50 % of the crown covered by lianas. The species
studied were: Ceiba speciosa, Cedrela fissilis, Cordia trichotoma, Cabralea canjearana, Ocotea
diospyrifolia, Chrysophyllum gonocarpum, Balfourodendron riedelianum, Parapiptadenia rigida
and Holocalyx balansae. Unpublished information from di Francescantonio et al.

slow growing species are normally severely infested, because older trees provide
more opportunities and time for liana colonization. In addition, tree species with
long branch-free boles and smooth bark are likely to be free of lianas while the
opposite is expected for trees with branched trunks or rough bark (Campbell and
Newbery 1993; Campanello et al. 2007). Liana colonization is a dynamic process
with liana shedding occasionally occurring for some species (Ingwell et al. 2010;
Campanello et al. 2012).
Lianas also have a substantial impact on tree water utilization. In Fig. 10, water
consumption of trees with and without lianas infestation is shown for three species
growing in a subtropical forest. The native forest studied has an average transpi-
ration of 954 mm per year, mostly from trees and palms and only less than 1 % of
this value was due to liana water consumption. Clearly, increasing liana colo-
nization could considerably reduce transpiration with impacts not only on the water
economy and nutrient absorption for individual trees but also with potential con-
sequences at the ecosystem level.
Carbon Allocation and Water Relations of Lianas Versus Trees 119

Fig. 10 Diurnal patterns of volumetric sap flow measured at the base of the main stem for three tree
species with crowns free of lianas (solid line) or colonized by lianas (dashed line) and air saturation
deficit (ASD)(dotted line). (a) Ocotea diospyrifolia is an evergreen species. Measurements were
made in dominant trees without lianas or slightly infested (Diameter 69 and 62 cm respectively);
(b) Cedrela fissilis is a deciduous species. Measurements were made in co-dominant trees without
lianas or slightly infested (Diameter 36 and 31 cm respectively); (c) Balfourodendron riedelianum
is a brevideciduous species. Measurements were made in dominant trees without lianas or severely
infested (Diameter 42 cm). Adapted from Rodriguez (2015)

Concluding Remarks

For more than thirty years, research had mainly focused on the ecological conse-
quences of liana colonization of trees and forest gaps and the subsequent impact on
ecosystem processes. It was not until recently that the differences in physiological
120 P.I. Campanello et al.

behavior between lianas and trees had been addressed. However, lianas are far from
a homogeneous group of species. A comprehensive understanding of liana eco-
physiology is fundamental for interpreting patterns of liana abundance and their
consequences in a changing environment worldwide. In neotropical forests, lianas
are increasing in abundance relative to trees. This increased species richness may
reflect modifications of drivers of global change factors including increased tem-
perature, atmospheric CO2, habitat disturbance, and drought. However, questions
remain as to the specific mechanisms facilitating the liana responses. We hope that
this chapter provides information on specific physiological mechanisms that can
help to explain aspects of the patterns of liana abundance increase as well as to
identify key questions that need to be addressed before we can have a more
comprehensive picture of functional interactions between environmental resource
acquisition, life history traits, and physiology of lianas and host trees in forest
ecosystems.
Liana seedlings fall along a continuum between two extremes represented by
support-seekers and freestanding species, which may, at least partially, relate to the
continuum in life history traits of shade-tolerance versus light requiring responses
of trees. On one side, support-seeking seedlings invest relatively little biomass in
thin leaves with low construction costs and high SLA, but stems grow fast towards
suitable support. On the opposite side, freestanding lianas develop a wider and more
resistant stem, and expand a larger leaf area of more expensive leaves with low
SLA, that appears to enable growth in shaded environments. Both contrasting
climbing strategies appear to characterize species with different growth patterns and
with differential impacts on host trees. The more crown-invasive support-seekers
may respond fast to disturbances with increased growth and canopy expansion.
Photosynthetic capacity and carbon assimilation rates in lianas are greater or
similar compared to trees, depending on climate. However, lianas have stems and
leaves with lower constructions costs than trees and exhibit a comparatively higher
biomass turnover. Despite having low density wood, lianas have lower capacitance
compared to trees because their stems are relatively thin. This limitation is partially
offset by a more efficient water transport system and stronger stomatal control that
allow lianas to cope with high evaporative demands at the top of the canopy. When
colonizing tree crowns, lianas can negatively affect growth rates and transpiration of
their tree hosts, with obvious consequences for the cycling of carbon and water at
the ecosystem level.

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 Part II
Adaptive Responses of Woody Plants
to Particular Tropical Habitats
Flood Tolerant Trees in Seasonally
Inundated Lowland Tropical Floodplains

Pia Parolin, Leandro V. Ferreira, Maria Teresa F. Piedade,

Cátia Nunes da Cunha, Florian Wittmann and Mauricio E. Arias

Abstract This chapter focuses on trees and their responses to flooding in large
fresh water flood-pulsed ecosystems. The regularity and predictability of the flood
pulse has allowed for the development of adaptations by which a large number of
tree species are able to grow in ecosystems subjected to seasonally inundated sites.
By comparing diversity and tree responses in four floodplain ecosystems on dif-
ferent continents, we attempt to improve our understanding of the factors
influencing spatial distribution of plants, diversity of species and adaptations and
thus contribute to our knowledge of tropical wetland ecology. In this way, we hope
to assist in the successful restoration of degraded floodplains and promote the
sustainable use and conservation of these highly valuable ecosystems.

Keywords Anoxic soils
Fresh water flooding
Growth rings
Hypoxia

Waterlogging

P. Parolin (&)
Biocentre Klein Flottbek and Botanical Garden, University of Hamburg,
Mittelweg 177, 20148 Hamburg, Germany
e-mail: pparolin@botanik.uni-hamburg.de
P. Parolin
INRA French National Institute for Agricultural Research,
Univ. Nice Sophia Antipolis, CNRS, UMR 1355-7254
Institut Sophia Agrobiotech, Sophia Antipolis 06903, France
L.V. Ferreira
Museu Paraense Emílio Goeldi, Av. Perimetral 1901,
Bairro Terra Firme, Belém, Pará 66077-530, Brazil
e-mail: lvferreira@museu-goeldi.br
M.T.F. Piedade
INPA, CP 478, Manaus, Amazônia 69011, Brazil
e-mail: maitepp@internext.com.br
C.N. da Cunha
Departamento de Botânica e Ecologia, Universidade Federal de Mato Grosso,
Cuiabá, Mato Grosso, Brazil
e-mail: catianc@ufmt.br

© Springer International Publishing Switzerland 2016 127

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_6
128 P. Parolin et al.

Introduction

Tree physiology is subjected to a particular challenge when it comes to flooded

tropical environments. When roots are waterlogged, or when whole plants are
submerged, species can display a range of responses. Most tropical ecosystems
where plants are subjected to flooding, however, are not well understood, and tree
responses to environmental change can be difficult to comprehend and foresee. The
following chapter focuses on responses and adaptations of tropical trees to different
types of flooding, what we know, where our knowledge is lacking, and what we can
expect regarding climatic and basin wide changes in floodplain ecosystems.
Worldwide, the largest numbers of tree studies in tropical freshwater floodplains are
performed in the Amazon Basin. Thus, we start off with the knowledge we have
about tree physiology and morphology in the Amazon floodplains (Fig. 1), as this is
the flooded ecosystem which to date is best understood. Then we outline infor-
mation about trees in other large floodplains of the world, such as the Okavango
Delta in Africa, the Tonle Sap floodplain of the Mekong River in Asia, and some
other vast wetlands colonized by trees. We try to assess the number of tropical flood
tolerant trees, and we end with some results, which may give insight into the
responses of flood adapted trees to environmental change and increasing frequency
and severity of flooding or drought events.

Responses and Adaptations to Flooding

The responses and adaptations to flooding in tropical environments depend largely

on hydric conditions, including flood duration, depth, seasonality, periodicity and
predictability. So far, a huge variety in responses and adaptations can be found in
Amazonian floodplains, and in other tropical wetlands of the world. All trees
inhabiting these areas are species whose survival and growth is not severely
inhibited by flooding (Gill 1970). Morphological adaptations may be remnants of
pre-adaptations from the non-flooded terra firme species where many floodplain
trees originate (Kubitzki 1989; Wittmann et al. 2013).

F. Wittmann
Department of Biogeochemistry, Max Planck Institute for Limnology,
55020 P.O. Box 3060, Mainz, Germany
e-mail: florian.wittmann@mpic.de
M.E. Arias
Department of Organismic and Evolutionary Biology, 26 Oxford Street, Cambridge, MA
02138, USA
e-mail: mauricio_arias@hks.harvard.edu
Flood Tolerant Trees in Seasonally Inundated Lowland … 129

Fig. 1 Várzea floodplain forest in Caxiuanã (Eastern Amazonia), Brazil (Photos Pia Parolin, June
2014)

Periods of limited growth last only a few weeks, are linked to high water, and
also to periods of strong drought (Parolin et al. 2010). In most trees from
Amazonian floodplains, new leaf flushes, flowering, fruiting and wood growth
occur while they are flooded for several months (Worbes 1986, 1989, 1997; Parolin
et al. 2002; Schöngart et al. 2002).
In the tropics, the aquatic phase occurs in a period in which temperature and
light conditions are optimal for plant growth and development. In contrast to
temperate floodplains where trees often persist in a dormant state, in tropical
floodplains trees grow vigorously during most of the year, including the aquatic
period (Parolin et al. 2004). The regularity of flooding may have enhanced the
evolution of specific traits, which are known from floodplain trees in other tropical
and in temperate regions. As a consequence of regular annual growth reductions,
growth rings are formed in the wood of most flood tolerant tree species (Worbes
1986, 1989; Schöngart et al. 2011).
Constraints imposed on trees by waterlogging and by submergence are clearly
different. Therefore, different types of flooding have different impacts on tree
growth, and it is important to consider flood duration, depth, seasonality, period-
icity, and predictability of the flooded periods if one wants to understand the
ecology and regeneration of the plants inhabiting the ecosystem. Due to the
immense changes of the annual high water levels, trees are seasonally submerged
only in very few ecosystems, including the Amazon and the Tonle Sap floodplain in
the Mekong, where regular differences between high and low water exceed 8 m
every year. Furthermore, whether flooding occurs at periodical intervals as a pre-
dictable flood pulse, as a result of unpredictable rain events or man-made changes,
is fundamental for the evolution of adaptations to withstand flooding (Junk et al.
1989). In the case of unpredictable events, the evolution of adaptations to cope with
flooding stress is far less efficient.
130 P. Parolin et al.

Constraints Imposed by Waterlogging

Adult trees subjected to waterlogging in floodplains have to cope with a lack of

oxygen in the rhizosphere (Crawford 1989). Inundated soils turn hypoxic or anoxic
within a few hours as a result of oxygen consumption by respiring roots and
microorganisms, and insufficient diffusion of oxygen through water (Crawford
1989). Oxygen depletion is accompanied by increased levels of CO2, anaerobic
decomposition of organic matter, increased solubility of mineral substances, and
reduction of the soil redox potential (Joly and Crawford 1982; Kozlowski 1984),
which is followed by accumulation of many potentially toxic compounds, caused
by alterations in the composition of the soil micro flora (Ponnamperuma 1984).

Constraints Imposed by Submergence

Only seldom, will adult trees be fully submerged, but seedlings established on low
levels in the flooding gradient are submerged in a predictable way in the Amazon
floodplains (Parolin 2002). Establishing seedlings are not expected to have a fast
height increase since they cannot escape from submergence of an 8 m water col-
umn. Thus, only species with a high tolerance of submergence can survive in
seasonally inundated sites. They need other physiological and morphological
adaptations than fast growth to resist several weeks to months of submergence,
(Siebel and Blom 1998). Seedlings typically establishing on those sites have sig-
nificantly lower shoot extension than on higher sites (Parolin 2000, 2002). Large
and small seeds produce seedlings with high shoot elongation, enhancing the
chances of non-submergence for the seedlings at high elevations. In igapó high seed
mass compensates for the lack of nutrients of the environment. In nutrient-rich
várzea, the environment supplies nutrients and seeds are smaller, but they may
produce seedlings, which are just as tall as on low nutrient sites (Parolin 2002). It is
assumed that the zonation observed in Amazonian floodplains is very closely linked
to the submergence tolerance and establishment strategy of seedlings, and less to
the tolerance of the adult trees.

Tree Adaptations to Flooding

Different adaptations are found at the level of structural, physiological, and phe-
nological traits (Parolin et al. 2004). These are common to most floodplain trees, of
temperate and tropical regions. Depending on their respective sets of adaptations
and growth strategies, most species are restricted to specific areas with a determined
pattern of flooding and sedimentation, leading to clear vegetation zonations along
the flooding gradients (Wittmann et al. 2004).
Flood Tolerant Trees in Seasonally Inundated Lowland … 131

Fig. 2 Root systems in várzea floodplain forest in Eastern Amazonia, some examples from left to
right: lateral knee roots of Symphonia globulifera; lateral adventitious roots sprouting from the tree
stem of Virola surinamensis; roots of the palm Euterpe oleracea (Photos Pia Parolin, June 2014)

Morphological and anatomical adaptations include the root systems of floodplain

trees (Fig. 2), such as hypertrophy of lenticels, formation of adventitious roots,
plank-buttressing and stilt rooting, development of aerenchyma, and the deposition
of cell wall biopolymers such as suberin and lignin in the root peripheral cell layers
(Schlüter and Furch 1992; Schlüter et al. 1993; Waldhoff et al. 1998; De Simone
et al. 2002a, 2002b; Haase et al. 2003; Parolin et al. 2004). Different types of
aboveground roots—stilt roots, plank buttressing (tabular roots)—are closely
related to flooding duration and habitat dynamics (Wittmann and Parolin 2005) for
Amazonian forests.
Stem-nodulation and nodulated adventitious roots were observed in various
species despite periodical flooding and are assumed to be adaptations that allow
legumes to fix N2 in a flooded environment (James et al. 2001). Radial oxygen
losses are avoided by developing strong suberin deposits in radial and tangential
cell walls of the root hypodermis, starting immediately behind the root tip. This was
found in various species of Amazonian floodplains (De Simone et al. 2003).
The leaves of Amazonian floodplain trees exhibit traits which are generally
considered as xeromorphic (Waldhoff et al. 2002; Parolin et al. 2004). Physiological
adaptations to flooding include changes of decreasing transpiration (Parolin et al.
2004), stomatal closure (Schlüter and Furch 1992), water potential (Scholander and
Perez 1968), leaf chlorophyll (Furch 1984) and nitrogen content, as well as
reductions of leaf size, growth and biomass production (Parolin et al. 2004).
Phenological adaptations in the Amazonian várzea are visible in that leaves are
shed mainly in the flooded period and new leaves are flushed when water recedes.
Flowering peaks at the beginning of the flooded period in igapó, while in várzea the
peak is at highest water levels. The periodic behaviour of vegetative phenology is
determined by the tree’s water status, which is a function of the interaction between
water potential of the environment and the structural and functional state of the tree
(Reich and Borchert 1984; Schöngart et al. 2002).
Dispersal and seedling establishment are also linked to water. The main means
of dispersal are hydro-and ichthyochory, emphasized by a close correlation between
the timing of flooding and fruit maturation (Ziburski 1991; Gottsberger 1978;
132 P. Parolin et al.

Goulding 1980; Moegenburg 2002; Parolin et al. 2002; Piedade et al. 2006; Parolin
et al. 2013). The diaspores show morphological adaptations for dispersal by water,
which enhance floatation, like spongy tissues or large air-filled spaces (Kubitzki and
Ziburski 1994). Seeds germinate very quickly upon emergence (Parolin and Junk
2002).

Responses and Adaptations in Other Large Tropical

Flooded Environments

The patterns described so far for Amazonia may in part be encountered in other
large wetlands of the world. Here, we focus on large tropical flood-pulsed flood-
plains and riverine forests with naturally occurring trees and a clearly predictable
flood pulse (sensu Junk et al. 1989). Many environmental factors are common to all
tropical floodplain forests with a flood pulse that represents a major influence on all
organisms (Junk 1989; Junk et al. 1989) and a dominating stress, which requires a
suite of adaptations for survival (Parolin et al. 2004).
However, there may be striking differences related to the presence or absence of
salt and fire, height and duration of floods, and pressures from surrounding uplands.
Those, which are dominated by grasslands like the African Okavango and Northern
Australian floodplains are subjected to regular fire (Heinl et al. 2004, 2006, 2007;
McGregor et al. 2010), whereas in the forest-dominated floodplains of Amazonia
fire plays no significant role. In the Okavango, the high evapotranspiration causes
increased salinity (Parolin and Wittmann 2010). Also, flooding amplitudes vary
widely between the ecosystems, with about 2–4 m in the Pantanal, Okavango and
Northern Australian, 8 m in the Mekong and 9 m in the Amazon floodplains
(Table 1). This implies that complete submergence of saplings and trees occurs only
in the Mekong and Amazon, posing different constraints for plant life than merely
waterlogging of roots and stems (Parolin 2009).

Table 1 Characteristics of some big flood-pulsed wetlands with natural occurrence of forests
Amazonia Pantanal Okavango Tonle sap
delta
Flood duration where trees 7 months 5 months <1 months 5–10 months
grow
Max flood height on tree 8m 4m Root level 9m
stems
Influence of fire and salt None Fire! Fire + salt! Fire to some
extent
Number of flood-tolerant tree >1000 60 (no 10 47 (very few
species (50 on lowest levels; endemics) endemics)
many endemics)
Density of human population 3, 3–20 1–2 <6 115
(inhabitants per km2)
Flood Tolerant Trees in Seasonally Inundated Lowland … 133

Pantanal

Ecosystem and flooding pattern. The Pantanal is a huge wetland in the centre of
South America, with an extension of 160,000 km2. It has a pronounced monomodal
predictable flood pulse with water levels of maximum 4 m in the sites flooded most
heavily. Flood duration is about 8 months per year. The vegetation is mainly open
grasslands and shrubs, but large forested areas also occur (Fig. 3). The trees are
mostly semi-evergreen, such as Vochysia divergens, which sheds its leaves with the
onset of the dry season or towards the end of the flooded period, and resprouts new
leaves almost immediately thereafter. Only few species, such as those of the genus
Ceiba, are deciduous and remain leafless for 2 months during the flooded phase.
Many species growing on higher levels shed their leaves in the dry period.
Flowering occurs mainly in the leafless period or with the onset of rain in
December, before flooding. Linked to origins in surrounding uplands, the main
dispersal vector for most tree species is wind, but hydrochory may occur. Fruits
mature at high water, and some diaspores are adapted to dispersal by water with air
filled spaces, or to dispersal by fish, with many fish species having a destructive
impact (Galetti et al. 2008).
Diversity of species and functional groups. The Pantanal is highly diverse in
flooded and non-flooded habitats. Different vegetation classifications have been
developed mainly by association with height and period of seasonal inundations
and physical and chemical soil properties (i.e., Prance and Schaller 1982; Ratter
et al. 1988; Zeilhofer and Schessl 1994). Seasonal semi-deciduous forests and
woodlands predominate on well-drained sites, while lower, periodically inundated
floodplains are dominated by open savanna formations interspersed with evergreen
forests (Prance and Schaller 1982).
Periodically inundated forests within the Pantanal are often composed of a few
co-dominant species (Pott and Pott 1994; Oliveira et al. 2014). Pott and Pott (1994)
listed 756 woody plant species in the Pantanal, but less than 20 % of them are
considered tolerant to prolonged floods (Cunha and Junk 2001). On the other hand,
more than 50 % of all tree species are restricted to non-flooded habitats.
Riparian forests, which accompany the main rivers and the secondary
river-channels, are described as the most species-rich inundation forests within the
Pantanal (Pott and Pott 1994; Damasceno-Junior et al. 2005; Wittmann et al. 2008;

Fig. 3 Floodplain forest in the Pantanal near Cuiabá (Photos Pia Parolin, March 2013)
134 P. Parolin et al.

Oliveira et al. 2014). Comparatively high species richness in riparian forests is most
probably traced to high habitat diversity (Wittmann 2012).
There are no endemic floodplain tree species (Pott and Pott 1994; Montes and
San José 1995; Veneklaas et al. 2005). Characteristic morpho-anatomical and/or
physiological adaptations of tree species to flooding, such as they occur in many
species of Amazonian floodplain forests are unknown within tree species of the
Pantanal.
Flooding responses, adaptations and tree distribution. Responses to flooding are
similar for many tropical floodplain species, with many species tolerating prolonged
periods of waterlogging. Leaves are shed in the dry period and only very few
species shed leaves in the high water period, such as species from the
Bombacaceae. The fruit peak occurs at high and at low water, depending on the tree
position in the flooding gradient. Flooding influences the physiology more than
shading in the species of the Pantanal, and consistently higher photosynthesis and
stomatal conductance have been measured under non-flooded conditions (Dalmolin
et al. 2012). The dry period is thus the main growth period.

Okavango

Ecosystem and flooding pattern. The Okavango delta in northwestern Botswana

is fed by the Okavango River which originates in Angola’s western highlands and
forms the world’s largest inland delta. As described in Parolin and Wittmann
(2010), the river discharges about 10 km3 of water onto the delta fan each year,
augmented by about 6 km3 of rainfall, which sustains about 2500 km2 of permanent
wetland and up to 8000 km2 of seasonal wetland. Interaction between this surface
water and the groundwater strongly influences the structure and function of the
wetland ecosystem. Soil pH and mineral content and ground water chemistry play
major roles in the spatial distribution of plant communities. However, Bonyongo
et al. (2000) state that timing and duration of seasonal flooding is the most
important factor determining plant species composition.
Precipitation is low, with 10–320 mm of monthly rainfall. The Okavango delta
experiences seasonal flooding starting toward the north between October and April
and ending in May. In the dry season the floodwaters evaporate leaving salts on the
ground, which leads to a strong influence of salt on the vegetation.
Fire plays a role in this ecosystem (Heinl et al. 2004, 2006, 2007). It is more
frequent in floodplains than on drylands because of greater biomass and fuel load.
Thus, the frequency of fires is determined by flooding frequency.
Diversity of species and functional groups. The floodplains consist mostly of
grasslands with 1250 species (Fig. 4; Ellery and Tacheba 2003), mostly grasses
interspersed with woody plants in the riverine forests. Impeded drainage and high
precipitation in the rainy season lead to temporarily waterlogged soils. No wood-
lands can establish under these conditions, but humid grasslands dominated by
Flood Tolerant Trees in Seasonally Inundated Lowland … 135

Fig. 4 Flooded grasslands in the Okavango delta (Photos Pia Parolin, January 2010)

dwarf-shrubs and small trees exist (Oldeland et al. 2013). Trees only grow in the
Okavango on islands and savannahs that are seldom submerged (Murray-Hudson
et al. 2014). Salt-rich islands are flooded less frequently and are dominated by
acacias, mopane (Colophospermum mopane) and woody shrubs. 43 woody species
occur in the dryland riverine woodland (Ellery and Tacheba 2003), none of which
are endemic (Parolin and Wittmann 2010).
Flooding responses, adaptations and tree distribution. Although seldom floo-
ded, the riparian woodland trees have their roots in the water table (Ellery and
Tacheba 2003). Few woody species are tolerant of flooding and fire. Riparian
woodlands are responsible for much of the water lost from the ecosystem and
deplete ground water by transpiration (Ringrose 2003). Trees ensure that islands of
vegetation function as ‘kidneys’ within the landscape (Ellery and Tacheba 2003).
The riparian trees remain green all year and partly sustain their growth as a result
of groundwater uptake in dry periods. Renewal of leaf growth however is primarily
related to rainfall, not to flood events in the distal Delta (Ringrose 2003). The
Miombo forests are dominated by deciduous tree species which lose their leaves for
a period of some months during the dry season, but deciduousness is not a response
to flooding (Oldeland et al. 2013) Evergreen tree species with microphyllous
compound leaves dominate extensive areas on sandy soils (Oldeland et al. 2013).
Regenerative phenology is unknown, with a high percentage of even-aged stands of
trees indicating that hydrological factors are important for tree regeneration because
they provide spasmodically favorable circumstances for establishment (Hughes
1988). A study of leaf gas exchange of Colophospermum mopane in Northwest
Botswana (Veenendaal et al. 2008) shows differences in physiological and mor-
phological traits between tall and short forms of mopane (Colophospermum
mopane (Kirk ex Benth.) Kirk ex J. Léonard) trees. These differences appeared
attributable to differences in root depth and density between the physiognomic
types (Veenendaal et al. 2008). So far, nothing is published about tree regeneration,
dispersal syndromes, seed germination, seedling growth and physiology, seedling
survival vs mortality, tree growth and productivity, or carbon stocks and seques-
tration. There is clear vegetation zonation due to the hydrological regime
136 P. Parolin et al.

characterized by depth, duration and timing of inundation, and soil and ground-
water salinity (Ellery et al. 1993; Ellery and Tacheba 2003). Vegetation patterns are
governed by prevailing flood regimes and depend on small differences of topog-
raphy (Bonyongo et al. 2000; Oldeland et al. 2013). Trees are particularly important
as they lower the water table beneath islands relative to the surrounding wetlands
and cause a net inward flow of groundwater (McCarthy 2006). On these islands,
broadleaf evergreen riparian trees dominate (Oldeland et al. 2013).
Changes and threats. Changes in the types of vegetation cover, due to both human
and natural causes, have taken place since the first vegetation map was produced in
1971 (Ringrose et al. 2002). In the Southwest, shifts to thorn scrub vegetation
prevail while in the eastern part of the country widespread bush encroachment is
taking place. An increased human population density suggests that these are
anthropogenic agrarian-degradation effects. Wherever broadleaved evergreen trees
are cleared, widespread salinity occurs (Ellery et al. 2000). Projection of future
vegetation changes to about 2050 indicates degeneration of the major vegetation
types due to expected drying of the local climate (Ringrose et al. 2002).

Tonle Sap of the Mekong

Ecosystem and flooding pattern. The Mekong in is one of the world’s longest
rivers with a length of 4,800 km approximately (MRC 2005). Its lower basin
includes extensive floodplains distributed mostly across Central Cambodia,
Southern Vietnam and the Tonle Sap system. It is in this last one where most of the
remaining flooded forests exist, whereas most of the other regions of the Mekong
floodplains have been converted to agriculture. The Tonle Sap River forms a per-
manent lake of 2,600 km2. During the dry season, the water in the Tonle Sap Lake
is only 1–2 m deep. During the wet monsoonal season, it reaches a depth of 9 m
with a water surface of 15,000 km2. Average flood duration through the Tonle Sap
floodplain is 5.4 ± 3.9 months per year (Arias et al. 2013). Fire plays a role in the
Tonle Sap. Most grasslands, which cover about 15 % of the floodplain, have signs
of contemporary fire. However, no quantifications of fire, or knowledge of whether
causes are natural (lighting) or manmade are available.
Diversity of species and functional groups. The Tonle Sap floodplain is covered
with a mosaic of natural, disturbed and agricultural habitats. Typically, most
pristine habitats cover those areas in the lowest and middle portions of the flood-
plain, whereas rice paddies only occur in upper elevations that become flooded for
short periods of time. Among these habitats, swamp shrub lands and forests cover
4,500 km2 (Fig. 5; Arias et al. 2014a). Similar swamp forests are also present along
floodplains of the Mekong and other major rivers in Cambodia. Swamp or gallery
forests originally dominated the dry-season shoreline of Tonle Sap Lake in areas
that are flooded about 9 months per year. The zone that is feasible for forests is
Flood Tolerant Trees in Seasonally Inundated Lowland … 137

Fig. 5 Floodplain forest in the Tonle Sap/Mekong River floodplain (Photos Pia Parolin, July
2010)

about 657 km2 (Arias et al. 2012, 2014b), but tall stands of forest currently cover a
much smaller area.
It is estimated that up to 233 plant species occur in the Tonle Sap floodplain,
with the greatest species density in the swamp shrubs and decreasing both towards
lower and higher elevations (Arias et al. 2013; McDonald et al. 1997). Shrubs reach
a maximum height of 4.4 ± 1.7 m and canopy cover of 58 ± 16 % (Arias et al.
2013). Swamp forests typically have less plant species density (4–8 per 100 m2)
than shrublands, but their canopy is much taller (8–11 m).
Flooding responses, adaptations and tree distribution. Little information is
available on plant distribution and zonation along the Mekong river floodplains. In
the Tonle Sap, the structure and composition of woody vegetation is largely a
function of heterogeneity of soil moisture and seasonal flood dynamics (Arias et al.
2013). Human intervention also plays a key role as rice paddies have been estab-
lished throughout the floodplain. The tallest trees grow closer to the permanent lake
basin. McDonald et al. (1997) attributed the presence of shrub vegetation in this
region to the short period optimal for growth that is restricted to the beginning and
end of the dry season. Most woody species of the floodplain of Tonle Sap are
deciduous, a probable adaptation to the periodic flood pulse. Instead of losing their
leaves in the dry season, these species shed their leaves as a function of light
limitation when submerged as the lake deepens. Flowering and fruit production in
the floodplain trees and shrubs are delayed for several months after the flush of new
leaves. Fruits reach maturity at the time of submergence suggesting that water
movement and fauna may be important dispersal agents. No data on physiological
responses to flooding and morphological adaptations were found.
Changes and threats. Most of the Mekong floodplains are heavily inhabited by
fishermen and rice farmers. While the annual flood cycle of the Mekong provides
resources for these people, it is a fragile balance. The Tonle Sap provides the largest
remaining contiguous wetland in the region. Throughout the dry season burning is
common, with fires used to clear land before ploughing or to facilitate access for
138 P. Parolin et al.

cattle. Roads have permanently delimited the maximum extent of the continuous
flooding. The greatest threat to the hydrological and ecological functioning of the
Tonle Sap is the construction of large dams upstream along the Mekong and its
tributaries (Cochrane et al. 2014). New dams bring hydrologic changes that could
affect flooding regime, habitat distribution, and primary production of the Tonle
Sap floodplain (Arias et al. 2014b).

Australian “Wet-Dry Tropics” of the Northern Territory

Ecosystem and flooding pattern. Floodplain wetlands are uncommon in the

mostly arid continent of Australia. However, an important wetland, the Kakadu
National Park in Northern Australia, extends over 99,000 km2 with 2,900 km2 of
forested wetlands (Lowry and Finlayson 2004; Warfe et al. 2011; Ward et al. 2012).
The annual rainfall is 600–1600 mm spread over 4–7 months. The wet season
(November–December) lasts for 3–4 months (Taylor and Tulloch 1985). Water
flows on a seasonal basis (Finlayson et al. 1990). Northern Australia wetlands are
not contiguous and occur along several small streams. The forests are inundated by
up to 1 m of water during the wet season but are dry at other times (Fig. 6).
Diversity of species and functional groups. Around 55 % of the terrestrial veg-
etation in the Kakadu Region is tropical tall grass savanna, composed of
eucalypt-dominated open forest and woodland with a 1–2 m tall grassy understory
(Finlayson 2005; Warfe et al. 2011; Ward et al. 2012). Closed canopy monsoon
rainforests are restricted to floodplains. Gallery and floodplain forests in monsoonal
northern Australia are mostly sclerophyllous and dominated by five closely related
species of Melaleuca with a tree canopy cover of 10–70 % (Franklin et al. 2007).
Flooding responses, adaptations and tree distribution. Variability due to chan-
ges in the hydrological cycle has resulted in many specific adaptations that enable
the plants to establish and grow (Finlayson et al. 1989; Finlayson 2005). Trees of
the floodplains often have modified bark structures such as the corky bark of
Sesbania formosa and Barringtonia acutangula and the distinctive papery bark of
some melaleucas that possesses internal longitudinal gas-filled passages (Finlayson
2005). The majority of seed dispersal mechanisms involve water even though many

Fig. 6 Floodplain forest in the Kakadu National Park in Northern Australia (Photos Pia Parolin,
July 2014)
Flood Tolerant Trees in Seasonally Inundated Lowland … 139

parts of the floodplains are drier for a longer period than they are wet. Nothing
seems to be published on physiological and morphological adaptations of trees of
the Kakadu National Park. Using a heat-pulse method McJannet (2008) found a
strong relationship between tree size and tree water use and showed that transpi-
ration by M. quinquenervia was unaffected by inundation. This ability to transpire
during flooding may be due to physiological adaptations of this species and to
dynamic root systems that can quickly respond to rising and falling water tables and
dense networks of fine ageotropic roots. Waterlogged Melaleuca quinquenervia
also develops negatively gravitropic roots (Sena Gomes and Kozlowski 1980).
A study by O’Grady et al. (2006) of Corymbia bella and Melaleuca argentea in
riparian zones of Northern Territory, along the Daly River showed that throughout
the dry season predawn leaf water potentials were above −0.5 MPa, indicating that
neither species suffered significant unrelieved water deficit stress during the dry
season. This study demonstrates strong gradients of tree water use within tropical
riparian communities in Northern Australia.
The productivity of the floodplain vegetation changes with the annual cycle.
This is indicated by periodic litterfall from Melaleuca trees. The distribution and
density of trees on at least part of the floodplain was seen to change considerably
between 1975 and 1990 (Finlayson 2005), indicating the dynamic nature of the
wetland environment.
The hydrological cycle has been identified as important in shaping the pattern of
the vegetation in the freshwater wetlands (Finlayson et al. 1989). The duration of
flooding, depth of water and the velocity of water flow are major determinants of
the vegetation composition of the floodplain (Finlayson et al. 1989). The changing
pattern is a function of both the flooding and drying phases of the hydrological
cycle (Finlayson et al. 1989, 1990).
Changes and threats. Fire and invasive plants and animal species have a signif-
icant impact on the extent and distribution of plant species and of the land cover
(Finlayson et al. 1990). Damage to the natural levees that separate freshwater and
saline wetland communities caused by climate change or by feral animals (espe-
cially water buffalo) may also change the vegetation. Notable responses by flood-
plain vegetation have already occurred following the removal of feral buffalo (Skeat
et al. 1996).

Diversity of Flood Tolerant Plants Across Tropical

Floodplains

In tropical floodplains, all plant growth forms are found. Trees, shrubs, vines and
herbs dominate, but a large variety of life history traits is found, including
hemi-epiphytic trees, stem succulent trees, palms and arborescent monocots, or
arborescent tree forms near treeline. A wide range of shade tolerance from rapidly
growing pioneer trees during gap phase regeneration to species that can survive by
140 P. Parolin et al.

growing slowly in deep shade contribute to this diversity. In Amazonian flood-

plains, all functional groups are present, from fast-growing short-lived pioneer trees
to slow-growing millenarians (Schöngart et al. 2011), evergreen and deciduous
species, those which produce large amounts of seeds every year such as Salix and
Cecropia or those which produce some seeds only every four or more years, such as
Aldina latifolia. The large number of adaptations for flooding allows for a partic-
ularly high diversity of species, of growth forms, and of functional traits despite the
strong pressure of flooding.
Despite the mostly unfavourable growth conditions for trees in floodplains, the
number of angiosperm tree species is very high. With 30–150 species in Amazonian
várzea (Balslev et al. 1987; Ayres 1993; Worbes 1997; Wittmann et al. 2002),
species richness is clearly lower than in the adjacent Terra Firme, where 180–300
species ha−1 occur (Klinge and Rodrigues 1968). The overall diversity of species
and life strategies in Pantanal and Amazonian floodplains is lower than in adjacent
non-flooded uplands (Campbell et al. 1986; Balslev et al. 1987). On the other hand,
diversity is still considerable with an estimated (Pott and Pott 1994) total number of
about 756 woody plant species in the Pantanal. The number of species adapted to
long-term flooding is small. A detailed analysis of the distribution of 85 tree species
along the flood gradient in the northern part shows that 45 species are restricted to
permanently dry areas and only 18 species show preference for habitats subject to
extended annual flooding. Twenty-two species tolerate a very broad spectrum of
flooded and dry conditions, a behaviour that is favoured by pluriannual extreme dry
and wet periods (Nunes da Cunha and Junk 2001). If we consider this relationship
representative for the entire Pantanal, 355 species (47 %) would show flood tol-
erance to varying degrees.

Conclusions

What do we know? In the four floodplains we examined, the terrestrial

non-flooded phase is when tree growth is most vigorous. However, many tree
species retain actively flowing phloem sap even during flooding (Waldhoff et al.
2002; Visser et al. 2003) indicating that active sources and sinks for respirable
substrates operate under these conditions. A set of metabolic adaptations are
inevitably required to achieve this. We postulate that for most tree species of
tropical floodplains, the primary morphological strategies in response to flooding
are similar to those of temperate species (Jackson and Armstrong 1999) or in the
well-analyzed tropical Amazonian floodplains (Parolin et al. 2004). In particular,
there must be a development of gas-filled spaces in the roots and stems to allow
diffusion of oxygen from the aerial portions of the plant into the roots.
Morphological adaptations that favour this are hypertrophy of lenticels, formation
of adventitious roots, plank-buttressing and stilt rooting, development of aerench-
yma and the deposition of cell wall biopolymers such as suberin and lignin in the
root peripheral cell layers. The formation of aerial roots may compensate for losses
Flood Tolerant Trees in Seasonally Inundated Lowland … 141

of respiration and function by roots affected by lack of oxygen in the soil. Under
experimental conditions with stable water levels, most species show the potential to
produce adventitious roots. But, in the field, they are seldom found, probably
because their formation is hampered by a rapidly changing water level. Leaves of
tropical forests in general and the Amazonian floodplain forests in particular
commonly have xeromorphic structures (Waldhoff 2003). This attribute contributes
to suppressing water loss at times of low water supply. This can apply to tree
crowns during the aquatic phase and to periods of drought in the terrestrial phase.
The degree of flood tolerance depends, in large part, on the time taken to col-
onize the floodplains.
Morphological adaptations may be remnants of pre-adaptations from
non-flooded upland tree species (Kubitzki 1989), which evolved further, leading
over time to highly adapted species. Thus, the phylogenetic development of
adaptations depends on the age of the ecosystem, and also on the dominant plant
families, which colonized these ecosystems originally. In each of the four
ecosystems, there are large differences in developmental age (Table 1). This implies
different stages of adaptations among the organisms living there. Amazonian and
African floodplains are extremely old, dating at least to the Pleistocene (>12 million
years old), or even earlier. Such ancient landscapes have experienced several
changes in climate and hydrology during the glacial and interglacial periods. In
contrast, the Tonle Sap and the Australian floodplains are much younger and
thought to be no older than 7500 and 4000 years, respectively (Junk et al. 2006).
Where are our major gaps? The data presented here for only a few huge wetlands
is already very rudimentary. Other very large wetlands with forest patches were
completely excluded from our overview, as we do not have any relevant data on
them. For many of the world’s largest wetlands, only basic data on hydrology and
climatology are available with almost no information on plant distribution, tree
adaptations and ecophysiology. It is important to raise attention to such poorly
researched wetlands which are often inaccessible for social and political reasons but
which are threatened by the ever-increasing human population and its need for
water, food, waterways and hydroelectric power (Parolin and Wittmann 2010). The
destruction is so fast that we may never learn of the adaptations underpinning the
success of the tree species in these areas.
Throughout the world, wetland ecosystems are under increasing pressure from
agriculture, urbanization of catchment areas, tourism and recreational activities,
construction of impoundments and changes to hydrology and climate (Parolin and
Wittmann 2010). By comparing diversity and tree responses in four floodplain
ecosystems on different continents, we attempt to improve our understanding of the
factors influencing spatial distribution of plants, diversity of species and adapta-
tions, and thus contribute to our knowledge of tropical wetland ecology. In this
way, we hope to assist in the successful restoration of degraded floodplains and
promote the sustainable use and conservation of these highly valuable ecosystems.
What can we expect regarding climatic changes in floodplain ecosystems?
Predictions suggest a transformation of the Amazon rainforest into cerrado
142 P. Parolin et al.

vegetation (Oyama and Nobre 2003) or the shifting of the moist rainforests in the
Amazon towards semi-deciduous forest types (Malhi et al. 2009). However, models
and predictions often do not consider wetlands and the large percentage of flood-
plain forests which are part of the Amazon basin and have a very important role in
the water cycle of the whole Amazon basin. They form an efficient system for water
retention, recharge the water table, decrease the amplitude of the creeks and rivers
between floods and droughts, and contribute substantially to regional climate by the
high rate of evapotranspiration. These environmental services are of utmost
importance to mitigate the consequences of the changes in rainfall patterns of the
future. All streams and small and large rivers are bordered by floodplain forests that
will, in case the most alarming scenarios come true, form a dense network of
flooded forests in a drier landscape. Floodplains, which by their environmentally
drastic conditions are very resilient, are likely to become even greater hotspots for
biodiversity and very significant biological corridors. Where possible, future studies
should use methods that will allows comparisons to be made with confidence.
Improving our understanding of floodplain functioning will underpin their preser-
vation and effective future management.

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The Physiology of Mangrove Trees
with Changing Climate

Catherine E. Lovelock, Ken W. Krauss, Michael J. Osland,

Ruth Reef and Marilyn C. Ball

Abstract Mangrove forests grow on saline, permanently or periodically flooded

soils of the tropical and subtropical coasts. The tree species that compose the
mangrove are halophytes that have suites of traits that confer differing levels of
tolerance of salinity, aridity, inundation and extremes of temperature. Here we
review how climate change and elevated levels of atmospheric CO2 will influence
mangrove forests. Tolerance of salinity and inundation in mangroves is associated
with the efficient use of water for photosynthetic carbon gain which underpins
anticipated gains in productivity with increasing levels of CO2. We review evidence
of increases in productivity with increasing CO2, finding that enhancements in
growth appear to be similar to trees in non-mangrove habitats and that gains in
productivity with elevated CO2 are likely due to changes in biomass allocation.
High levels of trait plasticity are observed in some mangrove species, which

C.E. Lovelock (&)
R. Reef

School of Biological Sciences, The University of Queensland,
Brisbane St. Lucia, QLD 4072, Australia
e-mail: c.lovelock@uq.edu.au
R. Reef
e-mail: r.reef@uq.edu.au
K.W. Krauss
M.J. Osland
U.S. Geological Survey, Wetland and Aquatic Research Center,
Lafayette, LA 70506, USA
e-mail: kkrauss@usgs.gov
M.J. Osland
e-mail: mosland@usgs.gov
M.C. Ball
Research School of Biology, The Australian National University,
Canberra, ACT, Australia
e-mail: Marilyn.Ball@anu.edu.au

© Springer International Publishing Switzerland 2016 149

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_7
150 C.E. Lovelock et al.

potentially facilitates their responses to climate change. Trait plasticity is associated

with broad tolerance of salinity, aridity, low temperatures and nutrient availability.
Because low temperatures and aridity place strong limits on mangrove growth at the
edge of their current distribution, increasing temperatures over time and changing
rainfall patterns are likely to have an important influence on the distribution of
mangroves. We provide a global analysis based on plant traits and IPCC scenarios
of changing temperature and aridity that indicates substantial global potential for
mangrove expansion.

Keywords Elevated CO2
Flooding
Plasticity
Salinity
Water uptake

Introduction

The trees of mangrove forests have fascinated physiologists for decades. The highly
saline, tidally flooded environments of mangrove forests seem unlikely to support
tree growth, yet mangroves are some of the most productive forests on the planet
(Alongi 2009). Both the number of families and individual species of plants that
have evolved the necessary traits to grow in mangrove habitats has been relatively
small: 70 species in over 40 million years (Ricklefs et al. 2006), reflecting the
complex suite of traits that are required for growth in intertidal environments. The
position of these forests in the landscape, on the ecotone between terrestrial and
marine habitats, also brings high levels of variation in soil conditions that range
over a hierarchy of timescales: daily (e.g., tidal inundation), monthly (e.g., tidal
cycles), annual (e.g. seasonal precipitation) and tens to hundreds of years (e.g., sea
level rise). Such rhythmic and dynamic conditions require the trees that grow in
these intertidal habitats to have high levels of plasticity.
In the present review, we focus on recent insights into the ecophysiological
processes that enable mangrove forests to maintain productivity under both saline
and anoxic soil conditions, how their physiology is limited by temperature and how
these physiological attributes may affect responses of mangrove forests to the
complex environmental changes anticipated under future conditions. Enhancements
in our understanding of the underlying physiological bases of salinity tolerance in
mangroves is important to the development of both salinity tolerant crops and
predictive models for management of the wide range of ecosystem services pro-
vided by mangrove forests under changing environmental and climatic scenarios
(Barbier et al. 2011). However, global climate and atmospheric change do not affect
salinity in isolation. Other key environmental factors, namely atmospheric CO2
concentration, temperature and sea level are also changing with far reaching con-
sequences for the structure, function and distribution of mangrove systems.
The Physiology of Mangrove Trees with Changing Climate 151

Water Uptake in Saline Soils

Mangrove tree species tolerate a wide range of soil salinity (Lugo and Snedaker
1974; Odum et al. 1982; Hutchings and Saenger 1987) (Table 1) and are highly
adapted to salt concentrations in soils that exceed concentrations tolerated by most
other plants (Ball 1988a). However, both low and high salinity can limit mangrove
growth and productivity (Clough and Sim 1989; Lin and Sternberg 1992; Ball
2002). Saline habitats present physiological challenges for plants because their
survival depends on the extraction of almost freshwater from highly saline soils.
The low osmotic potentials of saline soil water make water acquisition and transport
more difficult than in wet, non-saline soils, leading to high carbon costs of water
uptake and transport. These costs are reflected in the typically high water-use
efficiency of mangroves which tends to increase with increases in both the salt
tolerance of the species and the salinity in which the plants are grown (Ball 1988a).
However, such water use characteristics come at the expense of other functions.
Table 2 summarizes the traits associated with salinity tolerance in mangroves and
indicates some of the putative costs associated with salinity tolerance, including
reduced survival in the shade (Ball 2002; Lopez Hoffman et al. 2007), reduced
growth rates (Ball 1988a) or loss of mechanical strength (Santini et al. 2012).
Growth in saline environments necessitates adaptations to maintain the low
tissue water potentials needed to extract water from highly saline soils, and to limit
the loss of extracted water from leaves. To this end, mangrove species can exclude,
accumulate, and excrete salts; none of these are salt tolerance strategies per se,
although each can be related to water uptake and the requirement for water con-
servation (Ball 1988a). Mangroves as a broad group are halophytes with a wide
range of salinity tolerance among species (Krauss and Ball 2013; Reef and
Lovelock 2014) (Table 1). All mangrove species exclude the majority of salt ions
during water absorption by the roots (up to 80–95 %; Scholander et al.1962;
Scholander et al. 1968; Popp et al. 1993). Casparian bands and suberin lamellae
provide barriers to apoplastic water flow through the root endodermis and are well
developed close to the root tip (Lawton et al. 1980). Root traits vary among species.
For example Bruguiera possesses a large root cap, high levels of phenolic deposits
in cells and rapid development of vasculature to prevent salts from entering xylem
vessels through this pathway (Lawton et al. 1981). In contrast Avicennia marina has
a smaller root cap and vascular development is delayed, which may allow greater
salt and water uptake (Fig. 1). Greater development of root apoplastic barriers
among species reduces bypass flow, forcing water through the endodermis and
enhancing efficient salt exclusion (Krishnamurthy et al. 2014). Indeed, concentra-
tion of salts within soils can pose a real dilemma for mangroves; recent stable
isotope studies have shown that mangroves utilize less saline water sources when
freshwater is available (Sternberg and Swart 1987; Ewe et al. 2007; Lambs et al.
2008; Wei et al. 2013). For example, in Florida R. mangle went from using 100 %
shallow soil water in the wet season when that water was fresh to a mix of 55 %
shallow soil water and 45 % deeper groundwater during the dry season when deeper
Table 1 Tolerance of some mangrove species to high salinity, high aridity, and low temperatures
152

Species Relative tolerance Occurrence in extreme climatic conditions

Salinity Aridity Low High Aridity Precipitation Extreme min Monthly mean Monthly mean
temperatures temperatures index (mm/yr) temp (°C) min temp (°C) max temp (°C)
Acrostichum Mid Mid Mid Low Semi-arid 800–1200 0–5 8–12 34–37
aureum
Aegialitis High High Mid Mid Arid <400 0–5 8–12 37–40
annulato
Aegiceras Mid High High Mid Arid <400 −5 to 0 4–8 37–40
comiculatum
Avicennia High High High Mid Arid <400 <−5 4–8 37–40
germinons
Avkennia High High High High Arid <400 <−5 4–8 >40
marina
Bruguiera Mid High High Mid Arid <400 −5 to 0 4–8 37–40
gymnorrtiiza
Bruguiera Low Mid Low Low Semi-arid >1200 0–5 12–16 34–37
sexangula
Ceriops High High Mid Mid Arid <400 0–5 8–12 37–40
australis
Ceriops Low Low Low Mid Dry 800–1200 5–10 12–16 37–40
decandra sub-humid
Ceriops tagal Mid High Mid Mid Arid <400 −5–0 8–12 37–40
Exccecona Low Mid High Mid Semi-arid 400–800 −5 to 0 4–8 37–40
agallocha
Heritiera Mid Mid High Mid Semi-arid 400–800 −5 to 0 8–12 37–40
littoralis
(continued)
C.E. Lovelock et al.
Table 1 (continued)
Species Relative tolerance Occurrence in extreme climatic conditions
Salinity Aridity Low High Aridity Precipitation Extreme min Monthly mean Monthly mean
temperatures temperatures index (mm/yr) temp (°C) min temp (°C) max temp (°C)
Kandelia Mid Low Low Low Dry >1200 5–10 >16 34–37
candel sub-hum
id
Kandelia Low Low High Low Dry >1200 <−5 4–8 34–37
obovata sub-hum
id
Laguncularia Mid High Mid Mid Arid <400 <−5 8–12 37–40
racemosa
Lumnitzera High Low Low Mid Dry 800–1200 0−5 12–16 37–40
littorea sub-humid
Nypa fruticans Low Low Low Low Dry >1200 0−5 12–16 34–37
sub-humid
Osbornia > a Mid Mid Mid Mid Arid <400 0−5 8–12 37–40
octodonata
The Physiology of Mangrove Trees with Changing Climate

Rhizophora Mid Mid Mid Mid Semi-arid 400–800 0−5 8–12 37–40
aptculata
Rhizophora High High Mid Mid Arid <400 <−5 8–12 37–40
mangle
Rhizophora Low High Mid High Arid <400 0−5 8–12 >40
mucronata
Rhizophora High High High Mid Arid <400 −5 to 0 4–8 37–40
stylosa
(continued)
153
Table 1 (continued)
154

Species Relative tolerance Occurrence in extreme climatic conditions

Salinity Aridity Low High Aridity Precipitation Extreme min Monthly mean Monthly mean
temperatures temperatures index (mm/yr) temp (°C) min temp (°C) max temp (°C)
Sonneratia Mid Mid Mid Mid Semi-arid 400–800 0−5 8–12 37–40
alba
Sonneratia Low Low Low Low Dry >1200 5−10 >16 34–37
larceolata sub-humid
Xylocarpus Low Mid Mid Mid Semi-arid 400–800 0−5 8–12 37–40
granatum
Xylocarpus Mid Mid Mid Mid Semi-arid 400–800 0−5 8–12 37–40
moluccensis
Species-specific relative tolerances categories were determined using information in Clough (1992) and Reef and Lovelock (2014) in combination with the
climatic tolerance data presented here. The final four columns provide estimates of the extreme climatic conditions in which a species is present (highest
aridity, lowest precipitation, lowest temperature). Species range data were obtained from Spalding et al. (2010). The aridity index data were obtained from
Zomer et al. (2006). The precipitation and monthly mean, minimum and maximum temperature data were obtained from Hijmans et al. (2005). The extreme
minimum temperature data were obtained from Maurer et al. (2009)
C.E. Lovelock et al.
The Physiology of Mangrove Trees with Changing Climate 155

Table 2 Mangrove plant traits associated with salinity tolerance in mangrove tree species and the
putative costs of the salt tolerance trait
Trait Function Putative costs References
Suberized root cell walls, Ion exclusion Reduced capacity Lawton et al. (1981),
highly developed casparian for water uptake Passioura et al.
strip under fresh water (1992)
conditions;
salinization of soils
High dependence on Ion exclusion Low rates of water Reef et al. (2012)
symplastic water uptake uptake
High salt concentrations in Maintenance of Metabolic/nutrient Takemura et al.
cell vacuoles water potential costs (2000)
in the vacuole
High concentrations of Maintenance of Metabolic/nutrient Popp and Polanía
osmotically compatible water potential costs; reducing (1989), Zimmermann
solutes and ion xylem water flow et al. (1994), but see
exclusion in the Becker et al. (1997)
cytoplasm?
Salt excretion Ion balance; Metabolic Reef and Lovelock
decreased (2014)
VPD/reduced
water loss
Low stomatal conductance Reduced xylem Low rates of Ball (1988a),
tensions transpiration and Sobrado (2000),
(reduced photosynthetic Clough and Sim
potential for carbon gain (1989), Krauss and
cavitation) Allen (2003),
Vandegehuchte et al.
(2014)
Steep leaf angles Thermal Reduced light Ball (1988a),
regulation, capture, reduced Lovelock and Clough
reduced water CO2 diffusion (less (1992)
loss mass transfer—
less air flow)
Reductions in leaf size Thermal Reduced light Ball et al. (1988b)
regulation, capture, increased
reducing water structural
loss construction costs
Abaxial stomata Reduced water Reduced capacity Cheeseman (1994)
loss for CO2 fixation
Leaf succulence Thermal Increased Saenger (1982),
regulation and resistance to CO2 Camilleri and Ribi
maintenance of diffusion, (1983), Wang et al.
ion balance increased structural (2007)
construction costs
Thickened leaf cuticles Reduced water Reduced light Saenger (1982),
loss capture, increased Wang et al. (2007),
structural Naidoo et al. (2011)
construction costs
(continued)
156 C.E. Lovelock et al.

Table 2 (continued)
Trait Function Putative costs References
Leaf pubescence (hairs) Uptake of Metabolic, reduced Reef and Lovelock
atmospheric light capture (2014)
water vapour,
reduced water
loss, thermal
regulation
CO2 uptake of non-leaf Reduced whole Metabolic (nutrient Reef and Lovelock
tissues plant water loss demand imposed (2014)
for carbon gain by chlorophyll and
RUBISCO)
Small vessel size Reduced Low rates of Ewers et al. (2004),
potential for photosynthetic Lovelock et al.
cavitation carbon gain (2006), Stuart et al.
(2007)
Successive cambia Increased Decreased Carlquist (2007),
(Xylem/Phloem/parenchyma capacity to repair mechanical Robert et al. (2011),
bundles) in Avicennia and embolisms strength; Schmitz et al. (2008),
Aegialitis metabolic/nutrient Santini et al. (2012),
costs Yáñez-Espinosa et al.
(2004)
Root growth in patches of Improved water Biomass allocation Ewe et al. (2007),
fresher water balance below ground Wei et al. (2013),
Sternberg and Swart
(1987), Lambs et al.
(2008)

groundwater had lower salinity than shallow soil water (Sternberg and Swart 1987;
Ewe et al. 2007).

Reducing Water Loss Under Saline and Arid Conditions

Once water is transported to the leaves, mangroves are highly efficient in the use of
water during photosynthesis (Farquhar et al. 1982; Sobrado 2000). Mangroves,
which use a C3 photosynthetic pathway, were as much as 35–56 % more efficient in
water use than nearby tropical lowland tree species (Ball 1996) and can even
surpass stand-level water use efficiency of co-occurring C4 grasses in some settings
(Krauss et al. 2014a). Photosynthetic water use efficiency (PWUE) is often reported
as the ratio of leaf photosynthetic CO2 assimilation rate to transpiration rate, while
the intrinsic PWUE is calculated as the ratio of assimilation rate to stomatal con-
ductance of water vapour. These values can be extremely high in mangroves, with
intrinsic PWUE ranging up to 153–212 μmol CO2/mol H2O (Table 3) compared to
40–80 μmol CO2/mol H2O typical in tropical trees, and often increasing with
The Physiology of Mangrove Trees with Changing Climate 157

Fig. 1 Comparative longitudinal sections of representative Bruguiera gymnorrhiza roots (left) and
Avicennia marina roots (right) showing endodermal layers, vascular tissue, and root cap
characteristics (after Lawton et al. 1981). Numbers along the pericycle represent approximate
distance (cm) from root tip
158 C.E. Lovelock et al.

Table 3 Intrinsic photosynthetic water use efficiencies (PWUE) measured in seedlings, saplings,
and trees in mangroves globally (updated from Barr et al. 2009)
Speciesa Life PWUE, intrinsic (mmol Source
stage CO2/mol H2O)
RHST Tree 80–135 Andrews and Muller
(1985)
AVGE, COER Tree 10–100 Smith et al. (1989)
AVGE, LARA, RHMA Seedling 35–90 Pezeshki et al.
(1990)
BRPA, BRGY Tree 40–100 Cheeseman et al.
(1991)
RHMA Tree 40–55 Lin and Sternberg
(1992)
RHMA, LARA Tree 10–30 Martin and
Loeschen (1993)
AVGE Seedling 100–130 Naidoo and von
Willert (1995)
AEAN, AECO Seedling 60–100 Naidoo and von
Willert (1995)
AVGE, LARA, RHMA, Tree 35–40 Snedaker and
COER Araujo (1998)
BRGY, AVMA Tree 50–90 Naidoo et al. (1998)
AECO Tree 43–120 Youssef and
Saenger (1998b)
AVMA Tree 60–80 Sobrado and Ball
(1999)
RHMU, CETA Tree 50–100 Theuri et al. (1999)
AVGE, LARA, RHMA Tree 40–65 Sobrado (2000)
AVGE, LARA, RHMA Seedling 69–153 Krauss et al. (2006)b
AVGE, LARA, RHMA Sapling 51–95 Krauss et al. (2006)b
SOAP, SOCA, KACA, Tree 75–212 Chen et al. (2008)b
AVMA, EXAG
LARA, RHMA Seedling 33–110 Cardona-Olarte
et al. (2013)b
a
RHST = Rhizophora stylosa, AVGE = Avicennia germinans, COER = Conocarpus erectus,
LARA = Laguncularia racemosa, RHMA = Rhizophora mangle, BRPA = Bruguiera parviflora,
BRGY = Bruguiera gymnorrhiza, AEAN = Aegialitis annulata, AECO = Aegiceras corniculatum,
AVMA = Avicennia marina, RHMU = Rhizophora mucronata, CETA = Ceriops tagal,
SOAP = Sonneratia apetala, SOCA = Sonneratia caseolaris, KACA = Kandelia candel,
EXAG = Excoecaria agallocha
b
Actual values obtained from author

incremental addition of salinity (Ball 1988a; Clough and Sim 1989; Smith et al.
1989; Krauss et al. 2008). In a broad survey of 19 different mangrove species in
Australia and Papua New Guinea, Clough and Sim (1989) discovered that intrinsic
PWUE did not drop below 49 μmol CO2/mol H2O for any species by site com-
bination measured in the field, and ranged as high as 195 μmol CO2/mol H2O for
The Physiology of Mangrove Trees with Changing Climate 159

Avicennia marina where sites were highly saline. Changes in PWUE are also
manifest at the stand level; eddy-flux-derived CO2 uptake from a mangrove forest
in south Florida decreased 5 % for each 10 parts per thousand (ppt) increment in
salinity (Barr et al. 2013). High levels of photosynthetic efficiencies in water use of
mangroves are a consequence of structurally imposed limitations on the rates of
water supply to the leaves (Sobrado 2000; Lovelock et al. 2006; Hoa et al. 2009;
Vandegehuchte et al. 2014), as well as tight regulation of water loss at the leaf level
(Ball and Farquhar 1984; Clough and Sim 1989).
High levels of water use efficiency in mangrove tree species are associated with a
range of traits, many of which lead to reductions in the leaf to air vapour pressure
deficit (VPD). These traits include the presence of leaf pubescence (Reef and
Lovelock 2014), the presence of salt on the leaf surface which occurs in salt
secreting species and which may increase the humidity around the leaf (Reef and
Lovelock 2014), and steep leaf orientations and small, thick leaves both of which
affect the thermal balance of leaves (Ball 1988a). The characteristics that minimize
VPD are likely to be particularly important in arid environments. Finally, photo-
synthetic CO2 fixation in non-leaf tissues, which is acquired at lower water costs,
could also be an important aspect of salinity tolerance. In A. marina re-fixation of
respired CO2 by corticular photosynthesis contributed up to 5 % of the CO2fixation
by the plant (Schmitz et al. 2012). CO2 uptake by roots, although not yet studied in
mangroves, has been shown to be significant in other submerged and wetland plants
(Raven et al. 1988; Brix 1990; Rich et al. 2008).

Implications of Physiological and Structural Adaptations

for Function of the Whole Forest

Much ecophysiological research on mangroves has been directed to leaf-level

processes in seedlings, saplings, and occasionally, trees. Saenger (2002) reviews
this literature and concludes that with the combination of ecophysiological strate-
gies (e.g., high leaf-level PWUE) and adaptations for living in saline settings (e.g.,
salt exclusion at the roots, low stomatal conductance), mangrove forests are likely
to be very conservative in water use. Ironically, quantifying the absolute rates of
water use in mangroves has not been the central theme of many research programs;
however, the available data on sap flux indicate that mangrove trees use water at
rates over 3 times less than other forest trees per unit size (Fig. 2a). Individual tree
water use ranged from 0.4–64.1 L H2O/day in mangroves (Hirano et al. 1996;
Muller et al. 2009; Krauss et al. 2007, 2014a; Lambs and Saenger 2011) compared
with 116 ± 16 (SE) L H2O/day from trees in other forest types (Wullschleger et al.
1998). Missing from this analysis are empirical data from large mangrove trees
(>55 cm dbh).
Indeed, scaling ecophysiological processes from leaf to stand in mangroves
provides insight into ecosystem CO2 and H2O fluxes. Lugo et al. (1975) found that
two mangrove forests in Rookery Bay, Florida, USA took up 4.83 and 2.74 g
160 C.E. Lovelock et al.

Fig. 2 a Water use (L/day) versus diameter at breast height (dbh) for individual trees from
non-mangrove ecosystems (Wullschleger et al. 1998) versus data currently available from
mangrove ecosystems. Bars presented for mangroves represent the absolute range of dbh versus
water use values from specific studies (Krauss et al. 2007, 2014a, b; Muller et al. 2009; Lambs and
Saenger 2011). b Stand water use (mm; Krauss et al. 2015) versus net ecosystem exchange (-NEE)
of atmospheric CO2 (g CO2–C/m2; Barr et al. 2010) from a mangrove forest along the Shark River,
Everglades National Park, Florida, USA
The Physiology of Mangrove Trees with Changing Climate 161

C/m2/day through net ecosystem exchange (-NEE) while using 2.57 and 1.57 mm
H2O/day, respectively. Of that transpiration, 95–97 % was associated with the
canopy. Estimation of -NEE of carbon using eddy covariance along the Shark River
in Everglades National Park, Florida was remarkably similar to Lugo et al.’s esti-
mates, ranging from 2–5 g C/m2/day (Barr et al. 2010). This was despite the fact
that trees were nearly 8 m taller and forests had approximately 15 m2/ha greater
basal area along the Shark River than in Rookery Bay. During the same period of
time, estimated water use of the dominant canopy ranged to 4.22 mm H2O/day for
Shark River mangroves, averaging 2.5 mm H2O/day (Krauss et al. 2015; Fig. 2b).
Thus, considering that the mangroves along the Shark River registered among the
highest rates of carbon uptake among 49 forest types in North America (Amiro
et al. 2010), it is truly remarkable that canopy water use was efficient enough in
mangroves to represent only 63 % of regional rainfall and 66 % of ET (Krauss et al.
2015). Inherent to this are month-to-month fluctuations in annual rates of
canopy-level PWUE that require additional study (Fig. 2b).

Elevated CO2 Effects on Water Use

High levels of water use efficiency in mangroves and the increased PWUE with
increasing salinity leads to the expectation that there could be considerable gains in
productivity of mangroves with increasing levels of CO2 in the atmosphere as
stomatal limitations to CO2 uptake are ameliorated. The effects of elevated CO2 on
plant performance have not been studied in mangroves as extensively as in other
forest habitats. Only a handful of experimental studies have been conducted on the
response of mangrove seedlings to elevated CO2. Due to the difficulties posed by
the intertidal habitat, Free-Air Concentration Enrichment of CO2 (FACE) experi-
ments are yet to be conducted in mangroves and thus we have no experimental data
for the effects of elevated CO2 on mature trees. Despite the scarcity of data, it is
becoming apparent that while elevated CO2 has a significant effect on PWUE in
mangroves, the expected alleviation of salinity stress and subsequent improvement
in performance at high salinity does not occur to the extent initially anticipated. The
increase in mangrove seedling growth rates observed in response to elevated CO2
ranged from a 12 to a 47 % increase in growth relative to that under ambient CO2
concentrations (Table 4), which is overlapping with the mean and range recorded
for well watered tropical tree seedlings of different species experiencing similar
elevated CO2 conditions (Cernusak et al. 2011; Krauss et al. 2014b). Studies that
have incorporated a salinity treatment in elevated CO2 experiments in mangroves
conclude that at supra-optimal salinity conditions, elevated CO2 does not signifi-
cantly improve seedling growth, despite a significant improvement to PWUE (Ball
et al. 1997; Reef et al. 2014) and that a fertilization effect is only observed within
the low to mid salinity range. This is likely due to the fact that salinity constrains
tree growth in a manner other than water stress (e.g. ion toxicity).
162 C.E. Lovelock et al.

Table 4 The effects of elevated CO2 on mangrove seedling growth, photosynthetic water use
efficiency (PWUE) and specific leaf area (SLA) presented as the % change relative to values
measured at ambient CO2 concentrations
Species Ambient Elevated % % % Length of Reference
(CO2) (CO2) increase increase increase treatment
ppm ppm in in WUE in SLA (days)
growth
Rhizophora 350 700 47 1.72 NA 408 Farnsworth
mangle et al. (1996)
Rhizophora 340 700 31 15.2 −3 98 Ball et al.
apiculata (1997)
Rhizophora 340 700 21 33.8 7.8 98 Ball (1997)
stylosa
Avicennia 365 720 17 NA −10 540 McKee
germinans (2008)
Avicennia 400 800 22 107 −1.1 132 Reef et al.
germinans (2014)
Avicennia 280 800 12 218 −10 132 Reef et al.
germinans (2014)
In studies that included other factors (salinity, nutrient or humidity treatments) the CO2 response was
averaged over treatments

Mangroves respond to elevated CO2 by reducing stomatal conductance and by

producing leaves with lower stomatal densities (Farnsworth et al. 1996), but overall
productivity of forests may increase. The observed reduction in transpiration rate on
a leaf scale can have an effect on forest water use. However, elevated CO2 can also
lead to higher leaf area to total biomass ratios. In mangroves, increases in leaf area
ratios with increasing [CO2] were observed in most studies (Farnsworth et al. 1996;
Ball et al. 1997; Reef et al. 2014). Furthermore, there appears to be a lowering of
the light compensation point (LCP) of photosynthesis. In A. germinans grown
under elevated CO2 the LCP reduced from 52.3 ± 1.36 µmol m−2 s−1 at (CO2) of
280 ppm to 18.1 ± 9.6 µmol m−2 s−1 at [CO2] of 800 ppm, p = 0.03; R. Reef
unpublished data) suggesting that a positive carbon balance in leaves can be
maintained under shaded conditions at elevated CO2. Declines in specific leaf area
(SLA) were also observed in response to elevated CO2 (Table 4) and in a time series
study of herbarium specimens, SLA declined as CO2 has increased over time in A.
marina (but not for R. stylosa, Reef and Lovelock 2014). These responses to
elevated CO2 could result in increases in leaf level productivity and leaf area index
(LAI) at the stand level with rising CO2 levels. Increases in LAI at the stand level
could offset the reduction in water use by individual leaves and result in enhanced
production, but no overall change to transpiration on larger scales.
An important parameter that can influence the response of mangroves to elevated
CO2 in the field is nutrient availability. Under low nutrient conditions, similar to
those measured in many scrub mangrove forests, seedling biomass did not increase
in response to elevated CO2 (McKee and Rooth 2008). However, when given
higher nutrient concentrations, at levels similar to those measured in soils along
The Physiology of Mangrove Trees with Changing Climate 163

creek banks, elevated CO2 resulted in a significant 23 % increase in total biomass.

Development of nutrient limitations to growth could also be the reason for a
down-regulation of photosynthesis and reduced growth rates under elevated CO2
conditions over time in R. mangle grown in pots (Farnsworth et al. 1996). Nutrient
distributions are not uniform in mangrove forests due in part to their intertidal
nature. Most nutrients are delivered by the tides, thus creating elevation driven
gradients in nutrient availability. Furthermore, differences in nutrient inputs from
rivers and other landward sources, soil salinity, inundation frequency and faunal
activity affect the availability of nutrients (Reef et al. 2010, 2014). The response of
mangroves to elevated CO2 will thus likely be dependent on their position in the
forest and local nutrient conditions.
Finally, in order to understand the effects of elevated CO2 on forest structure and
distribution, competitive interactions must be taken into account. Elevated CO2 can
improve mangrove salinity tolerance within the range of salinities already suitable
for growth (Reef et al. 2014). This shift in the fundamental niche could translate
into a range shift depending on competitive outcomes and could be a contributing
factor in the observed mangrove encroachment into saltmarsh habitats observed at
many locations (Saintilan et al. 2014). In the only experiment to investigate com-
petitive interactions between mangroves and saltmarshes under elevated CO2,
McKee and Rooth (2008) found that elevated CO2 does not improve competitive
outcomes for the mangrove Avicennia germinans when grown in mixed culture
with the saltmarsh species Spartina alterniflora. Although S. alterniflora is a very
fast growing species and may not be representative of many saltmarsh species that
have slower growth rates, this study highlights the difficulties in predicting the
future of mangrove distributions in response to rising CO2 concentrations.

Adaptations to Inundated Soils

Tolerance of periods of inundation by tidal water, flooding and storm surges are
essential for mangrove tree species survival, and differences in species tolerances to
flooding influences their distributions relative to changing hydroperiods with
sea-level rise. Sea level has been relatively stable for the last five thousand years,
but accelerating rates of sea level rise and associated geomorphological adjustments
of the coast (Woodroffe 1990) are likely to result in vegetation transitions that are
linked to inundation tolerance of species. A range of traits are linked to inundation
tolerance (Table 5). Mangroves possess a number of elaborate, aerial root structures
including prop roots (Rhizophora), pneumatophores (Avicennia, Sonneratia), knee
roots (Bruguiera), and cable roots (Xylocarpus, Heritiera), prompting much early
speculation into their role in aerating sub-soil roots and soils. Still, some mangrove
species lack aerial roots (e.g., Excoecaria). Prominent on many of the aerial root
structures and stems are lenticels, or gas exchange pores positioned above the soil
surface. Air diffuses through these pores and via abundant aerenchyma tissues to
belowground root structures facilitating aeration of roots embedded in oxygen-free
164 C.E. Lovelock et al.

Table 5 Plant traits associated with tolerance of inundation in mangrove tree species and their
putative costs
Trait Function Putative cost Reference
Aerial roots Gas transport—air into Allocation of Scholander et al.
with below ground roots biomass to (1955), Youssef and
lenticels non-photosynthetic Saenger (1996),
tissues; respiration Skelton and Allaway
(1996)
Rapid Anchorage of seedlings Reduced allocation to Delgado et al. (2001),
seedling aboveground biomass Balke et al. (2011)
root
extention
Aerenchyma Gas transport and storage; Allocation of Scholander et al.
oxidation of phytotoxic biomass to (1955), Youssef and
substances non-photosynthetic Saenger (1996,
tissues; loss of 1998a, b), Skelton
mechanical strength and Allaway (1996),
Purnobasuki and
Suzuki (2004)
Suberized Limit oxygen leakage Enhance phytotoxic Thibodeau and
root cells into soils; maintain substances Nickerson (1986),
availability of some Youssef and Saenger
essential elements close (1996), Reef et al.
to the root surface (2010)

soils (Scholander et al. 1955; Skelton and Allaway 1996; Allaway et al. 2001). The
structure of mangrove roots facilitates gas exchange (McKee and Mendelssohn
1987; Youssef and Saenger 1996) which in addition to supporting respiration
results in the oxidation of phytotoxic substances within roots (e.g., Fe2+, H2S)
(Armstrong et al. 1992; Youssef and Saenger 1998a), although leakage of O2 into
the rhizosphere may affect the availability of some essential nutrients, particularly
phosphorus which are more available under reduced conditions, and some micro-
bial processes which are also favored under low oxygen concentrations (e.g. ni-
trogen fixation) (Reef et al. 2010) (Table 4). Early rapid root growth and investment
in roots in seedlings are also important for the establishment of seedlings on
exposed tidal flats and thus influences recruitment and forest expansion (Delgado
et al. 2001; Balke et al. 2011).
There are differences among species in the capacity to withstand inundation.
Experiments focused on gas exchange in root systems indicate that A. germinans
and Laguncularia racemosa seedlings suffered a decrease in root oxygen concen-
trations when exposed to experimental hypoxia, while Rhizophora mangle did not
(McKee 1996). McKee (1996) discovered that differences among species in
response to anoxia were attributed to oxygenation of the roots through diffusive O2
fluxes from the shoot, lower root respiration rates in R. mangle than A. germinans or
L. racemosa, and less O2 leakage from R. mangle roots to the surrounding soils.
Oxygen tends to leak from Avicennia roots to a much greater degree than
The Physiology of Mangrove Trees with Changing Climate 165

Rhizophora roots (Thibodeau and Nickerson 1986). In a multi-species comparison,

Avicennia marina and Acanthus ilicifolius had the highest concentrations of aer-
enchyma air space and the lowest diffusional resistance for O2 to soil among eight
mangrove species tested in Hong Kong (Pi et al. 2009) suggesting high levels of
variation among Indo-Pacific species in their capacity to transport oxygen to and
out of roots. Additionally, greater root porosity was found in pneumatophores than
other root types of Sonneratia alba from Okinawa (Purnobasuki and Suzuki 2004)
indicating variation in oxygen transport within root systems among wide-ranging
species. Rates of oxygen leakage from roots not only vary among species but also
with the strength of diffusion gradients between the root and soil (Sorrell and
Armstrong 1994). O2 leakage from the apical tips of Kandelia candel roots was
higher than from the main root walls (Chiu and Chou 1993). Variation in oxygen
leakage was attributed to the structure of the root surface, which is compacted and
lignified in Rhizophora and Aegiceras and thinner with only 3–4 exodermal layers
in Avicennia and Bruguiera (Youssef and Saenger 1996). The differences in
mangrove species in the structure, growth and physiology of roots, including their
ability to transport and retain O2 within their roots, are likely to lead to differences
in species responses to changing inundation regimes and associated hydrological
change with sea level rise. Although many other factors are also likely to influence
the distribution and composition of forests, including the space in the landscape for
landward expansion, human and natural modifications of the coast (Doyle et al.
2010; Traill et al. 2011), underlying differences in species inundation tolerance are
likely to be important.

Adaptations to Temperature Thresholds

Variations in temperature affect many processes in mangrove forests ranging from

the fundamental metabolic processes of photosynthesis and respiration (e.g.,
Andrews and Muller 1985; Lovelock 2008) to carbon cycling (Alongi 2009) and
reproductive success (Duke 1990). Temperature regimes greatly influence man-
grove forest composition and structure with extreme temperature events playing an
especially important role in some locations. Increasing global temperatures are
likely to result in changes to growth and distribution patterns of mangrove forests
on the edge of their ranges which are currently limited by low temperatures and in
some locations aridity.
The effects of low temperature on mangrove physiology (Davis 1940; Stuart et al.
2007; Krauss et al. 2008; Ross et al. 2009) and distributions (e.g., West 1977;
Sherrod and McMillan 1985; Woodroffe and Grindrod 1991; de Lange and de Lange
1994; Duke et al. 1998; Saenger 2002) have been widely studied, with recent studies
focused on mangrove recruitment into warm-temperate salt marsh habitats (e.g.,
McKee et al. 2012; Osland et al. 2013; Cavanaugh et al. 2014; Saintilan et al. 2014).
Mangrove species differ in sensitivity to low temperatures (Table 1), but none can
survive the minimum temperatures that occur in cold-temperate climatic zones.
166 C.E. Lovelock et al.

In general, mangrove forest biomass, structural development, and species rich-

ness are higher in wet tropical climatic zones. In colder climatic zones (e.g., sub-
tropical or warm-temperate), low temperature stress typically produces mangrove
trees that are short in stature with a shrub-like architecture (Woodroffe 1985;
Osland et al. 2014a, b). Physiological stress due to low temperatures can be sep-
arated into chilling and freezing stress (Kozlowski and Pallardy 1997; Larcher
2003). Whereas chilling stress occurs at leaf temperatures above freezing (i.e.,
without ice formation), freezing stress occurs at leaf temperatures below freezing
when intra- or extra-cellular ice formation occurs. The physiological effects and
symptoms of freezing/chilling stress in mangrove trees include reduced metabolic
rates, altered membrane structure and permeability (Markley et al. 1982), disrupted
water and nutrient transport (Stuart et al. 2007), partial or complete loss of
aboveground biomass (e.g., Osland et al. 2014a, b), reduced reproductive success
(Duke 1990) and, in extreme cases, mortality (Ross et al. 2009).
Intra- and inter-specific differences in mangrove sensitivity to low temperature
stress greatly influence the structure and composition of mangrove forests. There are
many examples of differential species and life stage responses to low temperature
stress (e.g., Lugo and Patterson-Zucca 1977; Lonard and Judd 1991; Olmsted et al.
1993; Ross et al. 2009; Chen et al. 2010; Pickens and Hester 2011). Climatic origin
greatly influences intraspecific responses to chilling stress with mangrove individ-
uals from colder climates typically being better adapted and more resistant to low
temperatures (Markley et al. 1982; Sherrod and McMillan 1985). Species sensitivity
to low temperature stress can be gauged using species distribution data in combi-
nation with multi-decadal climate data (e.g., Table 1; Quisthoudt et al. 2012; Osland
et al. 2013). For example, whereas some mangrove species are highly sensitive to
chilling stress and are only found in tropical climates (e.g., Bruguiera sexangula,
Sonneratia lanceolata), other species have adaptations that enable them to be
resistant to higher levels of chilling or freezing stress (e.g., A. germinans, A. marina,
Kandelia obovata, Aegiceras corniculatum). Vulnerability to low-temperature
induced xylem cavitation is especially high for mangrove trees due to the low xylem
water potentials required for water transport in highly saline intertidal environments
(Stuart et al. 2007). In a comparison of the most poleward mangrove species in
Australia and the United States, Stuart et al. (2007) highlighted the effects of xylem
embolism and show that species adapted to climates with colder mean annual
minimum temperatures have smaller vessel diameters which enable them to better
avoid embolism; however, narrow vessels also constrain water transport and pro-
ductivity, possibly limiting mangrove forest structural development in these pole-
ward locations. In addition to narrow vessels, variation in membrane properties also
likely enables mangrove individuals and species from colder climates to maintain
membrane fluidity during exposure to low temperatures (Markley et al. 1982).
On some continents, the frequency and intensity of extreme winter events greatly
affect mangroves. For example, near the poleward mangrove limit in China and the
southeastern United States, mean winter temperatures are not as cold as mean
winter temperatures found near the poleward limit of mangroves in Australia or
New Zealand. However, extreme minimum temperature events are more intense in
The Physiology of Mangrove Trees with Changing Climate 167

China and the southeastern United States which can result in sudden leaf loss,
xylem embolism, branch and stem reductions, and, in the most extreme cases, tree
mortality (Davis 1940; Lugo and Patterson-Zucca 1977; West 1977; Lonard and
Judd 1991; Everitt et al. 1996). In these areas, the spatial extent of mangrove forests
expands and contracts in response to the frequency and intensity of extreme winter
events (West 1977; Sherrod and McMillan 1985; Stevens et al. 2006; Giri et al.
2011). In North America, Avicennia germinans is a species that is especially
adapted to and resistant to extreme winter events. In parts of northern coastal
Florida, Louisiana, and the northern coast of Texas, A. germinans individuals often
lose a large portion of their aboveground biomass due to freeze events; however, A.
germinans is capable of vigorous resprouting from the base of stems after
freeze-damage due to the presence of epicormic buds (Lugo and Patterson-Zucca
1977; Tomlinson 1986; Osland et al. 2014a, b). Using data in Table 1 we graph-
ically show the breadth of tolerance of mangrove species in the biogeographic
provinces of the Atlantic and Eastern Pacific Ocean region (Fig. 3a) and the Indian
and Western Pacific Ocean region (Fig. 3b) to temperature extremes and to aridity
and salinity. Those species that are currently documented as expanding in their
range (e.g., A. germinans and A. marina) have the broadest tolerance to low tem-
peratures and to other environmental factors, while species that have restricted
distributions (e.g., the palm Nypa fruticans) are less tolerant of low and high
temperatures, high salinity and aridity.
In contrast, the effects of high temperatures on mangrove trees have not been as
extensively considered. Early research indicates that photosynthesis in tropical
species of Rhizophoraceae is depressed as leaf temperatures exceed 34 °C (e.g.,
Andrews and Muller 1985; Cheeseman et al. 1991). Most of this effect is associated
with the strong stomatal closure required to minimize rates of water loss that can
increase dramatically if leaf temperatures become higher than air temperatures or if
high air temperatures are accompanied by low humidity (i.e. increasing leaf-to-air
VPD). However, more research is required to understand how mangroves, partic-
ularly those in warm tropical climates that may already be close to their thermal
limits, will respond to the projected increases in global temperature of at least 2 °C
in the coming century. Clark (2004) suggested that productivity of tropical

Fig. 3 Spider plots of the overlapping tolerances of mangrove species to high and low
temperature and high and low temperature extremes, salinity and aridity (based on data from
Table 1). a Common species from the Atlantic-East Pacific biogeographic region; b common
species from the Indo-West Pacific region
168 C.E. Lovelock et al.

rainforests could decline with increasing temperature due to increases in respiration

and declining photosynthetic rates (Slot and Winter this volume). As yet there has
been no assessment of this hypothesis in mangrove forests.

Plasticity of Traits Gives Rise to Different Capacity

to Adjust to Climate Change

Plasticity of traits is a key feature of plants that allows them to acclimate to

changing conditions, including climate (Jump and Penuelas 2005). Some mangrove
species occur over broad ranges of environmental conditions and often assume
different forms in different habitats, e.g., scrub and tall fringing forms of R. mangle
in the Caribbean (Feller 1995; Medina et al. 2010) or for A. marina in New Zealand
and southern Australia (Lovelock 2008; Martin et al. 2010) (Fig. 4), displaying high
levels of both physiological and morphological plasticity (Lovelock et al. 2006). In
fact, plasticity in PWUE among and within mangrove species is a primary reason
why water use characteristics in mangroves have not been fully assessed; water use
can depend strongly on site or experimental conditions limiting blanket assessments

Fig. 4 Examples of high levels of morphological plasticity within mangrove tree species. The
upper left and right photos are of tall (15 m), forests fringing water ways and short (<2 m), scrub
forests of Rhizophora mangle, respectively, from Belize. The lower left and right photos are of tall
(5 m), fringing forests and short (<1 m), scrub forests, respectively, in New Zealand
The Physiology of Mangrove Trees with Changing Climate 169

Table 6 Variation in plasticity in growth (height, stem extension, biomass or relative growth rate,
RGR) for mangrove species grown in comparative experiments
Species Parameter Treatment Coefficient Reference
of variation
Ceriops Stem Salinity and 0.21 ± 0.01 (14)a Smith (1988)
australis height competition
Ceriops tagal 0.16 ± 0.02 (10)b
Avicennia Biomass Salinity 0.20 (5) Clough (1984)
marina
Rhizophora 0.17 (5)
stylosa
Sonneratia Stem Salinity 0.14 ± 0.03 (6)a Ball and Pidsley (1995)
alba height
S. lanceolate 0.10 ± 0.02 (4)a
R. stylosa RGR Salinity and 0.14 ± 0.04 (6)b Ball et al. (1998)
humidity
R. apiculate 0.13 ± 0.02 (8)b
A. germinans RGR Salinity and 0.12 ± 0.02 (14)a Ewe S., Lovelock C.E.
nutrient unpublished data
availability
Laguncularia 0.07 ± 0.01 (13)b
racemosa
R. mangle 0.24 ± 0.04 (15)c
Aegiceras Stem Inundation 0.042 ± 0.002 (8)a He et al. (2007)
corniculatum height
A. marina 0.083 ± 0.007 (8)c
Bruguiera 0.078 ± 0.005 (8)
gymnorrhiza bc
R. stylosa 0.067 ± 0.006 (8)b
A. germinans RGR Oxygen around 0.11 (2) McKee (1996)
roots
L. racemose 0.19 (2)
R. mangle 0.24 (2)
A. germinans Stem Nutrient 0.35 ± 0.07 (3)a Lovelock and Feller
extension availability (2003)
L. racemose 0.36 ± 0.04 (3)a
A. marina Stem Nutrient 0.22 ± 0.05 (3)a Lovelock CE, Feller IC
extension availability unpublished
C. australis 0.48 ± 0.10 (3)a
R. stylosa Stem Nutrient 0.21 ± 0.03 (3)a Lovelock CE
extension availability unplublished
C. australis 0.50 ± 0.06 (3)b
(continued)
170 C.E. Lovelock et al.

Table 6 (continued)
Species Parameter Treatment Coefficient Reference
of variation
Lumnitzera 0.19 ± 0.03 (3)a
racemosa
R. stylosa Stem Nutrient 0.15 ± 0.06 (3)a Lovelock CE
extension availability unpublished
C. australis 0.49 ± 0.13 (3)b
Plasticity is represented by the coefficient of variation (based on a mean of means over treatments).
The number of mean values used (N) is in parentheses. The most salt tolerant species is underlined.
Where sufficient data were available differences among species were tested and significant
differences at P < 0.05 are indicated with different letters after the mean

of water conservation in mangroves (see e.g., Becker et al. 1997 vs. Zimmermann
et al. 1994; Krauss et al. 2015). In a comparison of the levels of plasticity in
different traits over variation in fertility in R. mangle, whole plant architectural traits
(e.g. leaf area index, shoot extension and hydraulic properties of stems) had much
higher levels of plasticity than leaf level traits (e.g. photosynthesis, specific leaf
area) (Lovelock et al. 2006). As the most plastic traits are often the ones that
determine overall plant fitness (Agrawal 2001, Poorter and Lambers 1986;
Callaway et al. 2003) this suggests that plasticity in growth rates, canopy devel-
opment and hydraulic function are potentially the most important traits for suc-
cessful dominance of mangrove habitats. A high level of plasticity in belowground
growth is also likely, but as yet remains relatively unexplored (e.g., McKee 1996;
Casteneda Moya et al. 2011; Lang’at et al. 2013). In Table 6 we contrast plasticity
in growth (stem extension, relative growth rate or biomass expressed as a mean
coefficient of variation) for a range of species where contrasts have been made over
variation in treatments. Plasticity in growth varies significantly among mangrove
species and tends to be greater in response to variation in nutrient availability than
to other treatments. Species with the highest plasticity tend to be the most salt
tolerant and widely distributed and may be favored with global climate change. The
fitness cost of high levels of plasticity is difficult to determine, but could be
associated with being inferior competitors; although with few competing species in
mangrove forests (compared to tropical rainforests) there may be few disadvantages
to high levels of plasticity, particularly in the biogeographic province of the Atlantic
and East Pacific Ocean region where species diversity is particularly low.

Conclusions: Change in Distribution and Productivity

of Mangrove Forests

As a group, mangrove species possess many physiological adaptations and life

history characteristics that could enable them to adapt positively to future climate
change. However, the complex interactions between climatic drivers are only just
The Physiology of Mangrove Trees with Changing Climate 171

(a)

(b)

(c)

Fig. 5 The global mangrove distribution (green) overlain on: a predicted change in mean
temperature (IPCC 2007, A1FI scenario); b predicted changes in annual precipitation (IPCC 2007,
A1FI scenario); and c regions where mangrove distribution is sensitive to changes in aridity (red)
or low temperatures (blue)
172 C.E. Lovelock et al.

starting to become clear, and mangrove ecosystem responses to climate change will
be highly context dependent (e.g., Saintilan et al. 2009; McKee et al. 2012). In the
past, the global distribution and spatial extent of mangrove forests has expanded
and contracted in response to changes in sea level, temperature and freshwater
availability (Sherrod and McMillan 1985; Woodroffe and Grindrod 1991; Saintilan
et al. 2014). In the future, climate change is expected to greatly alter the distribu-
tion, composition and ecological properties of mangroves forests and their adjacent
ecosystems (i.e., salt marsh, salt flat, seagrass ecosystems) (Fig. 5). On some
continents (e.g., North America, Northwest Asia, Australia), warmer winter tem-
peratures will likely lead to poleward mangrove forest range expansion and
development at the expense of salt marsh habitat (Osland et al. 2013; Cavanaugh
et al. 2014; Saintilan et al. 2014). The southeastern United States is an area where
the ecological effects of mangrove migration are expected to be especially large due
to the large amount of salt marsh that could be replaced by mangrove forests
(Osland et al. 2013). Moreover, increases in sea level, freshwater availability,
elevated CO2 and human influences including nutrient enrichment will also affect
the productivity, composition and distribution of mangrove forests. In response to
sea level rise, mangrove forests are expected to migrate landward where migration
corridors exist (Doyle et al. 2010; Traill et al. 2011), although landward coastal
wetland migration will be obstructed in some areas by natural and anthropogenic
barriers (e.g., sea walls, hydrologic barriers). Species differences in inundation
tolerance are likely to influence the composition of forests as sea level rise accel-
erates. In arid and semi-arid climatic zones, the abundance and composition of
mangrove forests and other coastal wetland ecosystems will be greatly influenced
by changes in freshwater availability (Smith and Duke 1987; Bucher and Saenger
1994; Saintilan et al. 2009; Semeniuk 2013; Osland et al. 2014a, b). Whereas
increased aridity and/or reductions in freshwater input will likely result in reduced
mangrove coverage and diversity, the converse is also true; in some areas, increased
freshwater inputs, increases in humidity and increases in CO2 could result in
changes in communities, higher mangrove coverage, structural development and
productivity (Reef and Lovelock 2014; Osland et al. 2014a, b).

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Functional Diversity in Tropical High
Elevation Giant Rosettes

Fermín Rada

Abstract Strong daily temperature variations, seasonal soil water availability and
high air evaporative demands play an essential role in adaptive responses of tropical
high elevation mountain plants. Giant rosettes are a perfect example of successful
adaptations to these conditions, representing an important life-form of high elevation
tropical mountains in the Andes, Hawaii and Africa, a well-known case of
convergent evolution. Adaptive radiation resulted in a substantially large number of
giant rosette species in the ‘paramos’, a local name given for tropical alpine Andean
vegetation. Plant functional responses: plant water relations, gas exchange charac-
teristics and freezing resistance in giant rosettes are described in order to understand
their responses to extreme environmental conditions characteristic of high elevation
tropical habitats. Giant rosettes have a large capacitance (water-storage pith) and
strong stomatal control to cope with periods of water deficit, resulting in the
maintenance of high leaf water potentials on a daily and seasonal basis. Maximum
net CO2 assimilation rates are variable among species (3–10 μmol m−2 s−1), all
showing photosynthetic decreases from wet to dry seasons. Giant rosettes rely on
permanent supercooling of the leaves together with insulating structures protecting
stems and apical buds to cope with freezing damage. Even though the general aspect
and plant morphology of giant rosettes is similar across all high elevation tropical
regions, responses to similar selective pressures resulted in different physiological
characteristics in freezing resistance mechanisms, e.g. tolerance versus avoidance,
and thermal balance of the rosette. Giant rosette responses under changing global
environments are also discussed. The emphasis in the description of physiological
and morphological characteristics will be on South American giant rosettes due to
the large number of studies and the large number of species occurring in this region.

Keywords Gas exchange
Leaf pubescence
Stem capacitance
Supercooling

Water relations

F. Rada (&)
Instituto de Ciencias Ambientales y Ecológicas de los Andes Tropicales (ICAE)
Facultad de Ciencias, Universidad de Los Andes, Mérida, Venezuela
e-mail: frada@ula.ve

© Springer International Publishing Switzerland 2016 181

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_8
182 F. Rada

Introduction

Tropical high mountains are characterized by strong daily temperature variations.

Freezing temperatures frequently occur on any night of the year, while high
incoming radiation during the day results in relatively high daytime temperatures at
plant and soil surfaces. Hedberg (1964) characterized these environments as
“summer” during the day and “winter” at night. Daily temperature variations far
exceed seasonal ones (Troll 1968; Sarmiento 1986; Rundel 1994).
The páramos are tropical high Andean ecosystems dominated by tussock
grasses, sclerophyllous shrubs and giant rosettes. In general, this vegetation type is
found above the natural limit of the continuous forest line of the cloud forest
(Monasterio 1979; Smith and Young 1987) from approximately 3000 m up to the
permanent snow line at about 4600 m. This ecosystem occurs in higher altitudinal
regions of Venezuela, Colombia and Ecuador, with minor extensions towards
Panamá and Costa Rica to the north and in Northern Perú to the south between
latitudes 11° N and 8° S (Monasterio 1980; Luteyn 1992). The páramo has been
considered the most floristically diverse and holds the largest number of endemic
species of any mountain ecosystem worldwide (Luteyn 1999).
Intense incoming solar radiation has an impact on the plant and/or soil surface
thermal balance, increasing risks of rapid heating after nighttime frosts. Precipitation
regimes have a wide range of patterns depending on elevation and slope orientation.
In the particular case of the Venezuelan Andes, marked seasonal variations with a
dry season between December and March occurs. Annual precipitation ranges
between 650 mm for the driest to 1800 mm in the more humid Páramos (Sarmiento
1986). In summary, the combination of different environmental conditions of the
high tropical Andes determine thermal and water stresses to which plants are con-
stantly exposed (Fig. 1). Higher daytime incoming radiation and night reirradiation
during the dry season result in a greater minimum-maximum temperature range
generating significant day and nighttime temperature stresses. Increased cloud cover
and fog presence during the wet season dampen day-night temperature extremes
reducing thermal stresses; however infrequent clear skies may produce similar dry
season temperature effects on some occasions. Wet season night temperatures
remain relatively high compared to the dry season. In spite of different seasonal
temperature patterns, tropical alpine environments present small oscillations in
seasonal mean temperatures. In terms of water characteristics, increased cloud cover,
fog and precipitation determine favorable soil water conditions and the low evap-
orative demand during the wet season drastically contrasts with the dry season.
Seasonal water stress may be a key factor in plant adaptations to tropical alpine
climates.
Even though the physiognomy of the vegetation of the tropical Andean moun-
tains may vary between regions, dominant plant species belong to one of the
following growth forms: acaulescent rosettes, cushion plants, tussock grasses,
sclerophyllous shrubs or giant caulescent rosettes (Smith and Young 1987; Azócar
and Rada 2006). The giant rosettes may be considered the result of particular
Functional Diversity in Tropical High Elevation Giant Rosettes 183

Fig. 1 Environmental conditions of the high tropical Andes, which determine persistent thermal
and water stresses for plants. Temperature and water stresses constantly affect plants during the dry
season ( ) and occasionally occur during the wet season ( ) in the presence of unusually
clear skies. See text for a detailed description

adaptations to cold tropical climates. Different genera, consisting of a single stem

supporting a rosette have been described for many tropical high mountain regions:
Coespeletia and Espeletia in the Northern Andes, Senecio, Dendrosenecio and
Lobelia for Equatorial Africa, Argyroxiphium in Hawaii, among others (Cuatrecasas
et al. 1986; Monasterio and Vuillemier 1986; Smith and Young 1987; Bussmann
2006). Giant rosettes have been considered a classical example of convergent
evolution which independently evolved in the different mountain ranges. However,
Antonelli (2009) suggested that giant rosette ‘Lobelioids’ from Eastern Africa and
the Hawaiian Islands are closely related and derived from a single woody African
ancestor. Consequently, parallel evolution among tropical alpine environments
should be further tested.
The Espeletias are considered a typical example of rapid diversification and
adaptive radiation in a relatively recent ecosystem (Monasterio and Sarmiento
1991), a common event in ‘island’ environments (Carlquist 1974) such as the
paramos: high mountain peaks surrounded by lower elevation forests. Berry et al.
(1988) suggest a major role of interspecific hybridization in the adaptive radiation
of these dominant giant rosettes. The Venezuelan Andes display the greatest
184 F. Rada

diversity and number of giant rossette species and is the most probable site of origin
of this functional group (Cuatrecasas et al. 1986). There are approximately 130
species within the former genus Espeletia of which 63 are endemic to the Merida
Cordillera in Venezuela. Cuatrecasas (1976), using morphological attributes, sug-
gested a classification of the genus Espeletia into seven genera included within a
new subtribe, Espeletiinae: Carramboa, Coespeletia, Espeletia, Espeletiopsis,
Libanothamnus, Ruilopezia and Tamania. However, Rauscher (2002) through
phylogenetic studies showed that the Espeletiinae fall within the subtribe
Melampodiinae, and coin instead the term ‘Espeletia complex’ to group these
genera within the larger subtribe Melampodiinae.
The most representative genera of the Northern Andes, Coespeletia and
Espeletia, are characterized by a single stem, which varies in size across species
from a few cm to up to 3 or 4 m, and is covered by a compact, thick layer of dead
attached leaves, termed marcescent leaves, which insulate the stem and water
storage pith from subzero temperatures (Fig. 2a). This stem supports a rosette

Fig. 2 a Coespeletia timotensis at Páramo de Piedras Blancas (4200 m), b Espeletia schultzii
rosette at Páramo de Mucubají (3550 m) and c Ruilopezia atropurpurea rosette at Páramo de San
José (3150 m)
Functional Diversity in Tropical High Elevation Giant Rosettes 185

composed of a dense mass of very pubescent leaves and an apical bud surrounded
by a large number of unexpanded pubescent young leaves (Fig. 2b). The central
pith, made up of parenchymatous tissue, has a large capacity to store water
(Goldstein et al. 1984). Other giant rosettes, for example the Ruilopezias (Fig. 2c),
consist of large rosettes with very large leaves and reduced stems. Leaves are
glabrous on its abaxial surface and pubescent on the adaxial surface.
In this chapter some relevant plant functional traits influencing plant water
relations (how plants cope with water deficits and high evaporative demand con-
ditions), gas exchange (how water availability and temperature conditions affect
stomatal responses, transpirational losses and photosynthetic processes) and
freezing resistance (how plants survive nocturnal subzero temperatures all year
round) in giant rosettes of the Venezuelan Andes is reviewed. A comprehensive
analysis of these functional characteristics will permit us to identify the diversity of
responses and the adaptive significance of the responses in this dominant life-form,
compare these functional characteristics to other Andean plant life-forms and aid in
understanding how rosettes may be affected by global climate change. Information
on giant rosettes from other high tropical mountains is also included in this analysis.

Stem Capacitance and Pith Water Volume Impact

on Water Economy

As a general rule, plant height decreases with increasing altitude (Körner 2003).
However, exceptions exist; Smith (1980) described the paradox of the giant rosettes
of the tropical Andes. These rosettes exhibit different degrees of caulescence, from
sessile plants up to rosettes with stems several meters in height. The tallest giant
rosettes, mainly within the genus Coespeletia, are restricted to the higher paramos
(>3800 m). Espeletia schultzii, species with the widest altitudinal range (2600–
4400 m) in the Andes, increases stem size with altitude (Smith 1980; Meinzer et al.
1985). Meinzer et al. (1985) describe a ten-fold increase in pith volume for E.
schultzii from 2600 to 4200 m. Additionally, leaf area decreases by 50 % at higher
altitudes so that the relative water capacitance, defined by Goldstein et al. (1984) as
the pith volume/leaf area ratio, exponentially increases with elevation. These authors
describe differences along elevational gradients, not only with respect to pith vol-
ume, but in the relationship between transpiring leaf surface and water pith volume
(Fig. 3). This water storage capacity facilitates gas exchange during early morning
hours when low soil temperatures result in high root resistance for water uptake, and
during drought periods. C. timotensis, a species with a large capacitance (Goldstein
et al. 1985a), maintains relatively high and constant leaf water potentials even during
the dry season (Goldstein et al. 1984). These authors suggest that the hydraulic
connections between the pith and the xylem tissue are very efficient allowing this
species to maintain a favorable water status.
186 F. Rada

Fig. 3 Relationship between pith volume/leaf area (PV/LA) and elevation for different Andean
giant rosettes (PV/LA = 0.015e0.0016Altitude, R2 = 0.64). Ruilopezia atropurpurea (Ra), Espeletia
schultzii (Es), E. marcana (Em), E. flocossa (Ef), Coespeletia timotensis (Ct), C. lutescens (Cl), C.
spicata (Cs), C. moritziana (Cm). Data from Goldstein et al. (1984, 1985a), Meinzer et al. (1985),
Navarro (2013)

The role of the insulating marcescent leaves on the water balance of Coespeletia
timotensis was described by Goldstein and Meinzer (1983). Removal of the dead
leaf layer around the stem changed the patterns of stem temperatures, which
affected the plant’s water balance (Smith 1979; Goldstein and Meinzer 1983).
These effects were attributed to impeded water transport through the xylem when
the marsescent leaves were experimentally removed due to embolisms or frost
injury of the exposed pith tissue which occur at night. The role of the marcescent
leaves and their effects on stem and pith temperature will be further discussed. Even
though nutrient relations will not be treated in this chapter, it is necessary to
emphasize the importance of this layer of marcescent leaves on nutrient cycling in
the páramos. A large percentage of the rosette’s biomass remains as standing
necromass in these layers of dead leaves around the stem (Monasterio and
Sarmiento 1991). In a nutrient limited environment such as the paramo, this slowly
decomposing material that surrounds the stem may be considered a key nutrient
reservoir for giant rosettes. With fine roots developing inside the marcescent leaves,
and evidence of the presence of many decomposers, Garay (1981) indicated that
this nutrient pathway which does not include the organic soil is a closed above-
ground nutrient recycling circuit.

The Role of Leaf Pubescence

Different functions have been attributed to leaf pubescence. For hot and arid
environments, this layer reduces light absorption by the leaf lamina resulting in
lower leaf temperatures which in turn lower water losses by transpiration
(Ehleringer 1984). Baruch and Smith (1979) suggest that pubescence in leaves of
Andean giant rosettes may play a similar role as in hot-arid environments.
Functional Diversity in Tropical High Elevation Giant Rosettes 187

Meinzer and Goldstein (1985), on the other hand, find that leaf pubescence affects
the thermal balance of Coespeletia timotensis by increasing the boundary layer
thickness and reducing convective and latent heat transfer, while the effects on
absorption of solar radiation are minor. The resulting effect of the pubescent
boundary layer on energy transfer is a substantial leaf temperature increase during
the daytime. This ability to increase leaf temperature is of adaptive importance in
environments where air temperature is low all year round. The evolution of leaf
pubescence in hot-arid habitats and tropical mountains has occurred in response to
dissimilar selective pressures, even though both environments have high incoming
solar radiation, the daily and seasonal patterns of air temperatures are very different
in hot desserts and in high tropical environments (Meinzer et al. 1994).

Leaf Water Potentials and Seasonal Adjustments

Leaf water potentials of giant rosettes are relatively high, even during the dry
season, suggesting that they do not experience water deficits. Different patterns are
found between the high elevation Coespeletias and Espeletia schultzii and the lower
altitude Ruilopezia atropurpurea and Espeletia marcana (Fig. 4). Minimum leaf
water potentials (Ψmin tlp
L ) were always above leaf water potentials at turgor loss (ΨL )
which means that none of the species loses turgor even under drought conditions.
C. timotensis, the species having the largest capacitance measured within the
Andean giant rosettes (Meinzer and Goldstein 1986), maintains positive and rela-
tively constant leaf water potentials all year round (Goldstein et al. 1984). Rada
et al. (2012) observed lower Ψmin
L and ΨL for Coespeletia moritziana compared to
tlp

other Coespeletia species. Giant rosettes at lower altitudes, R. atropurpurea or

E. marcana, exhibit similar Ψmin L and ΨtlpL compared to the higher elevation

C. spicata C. timotensis C. moritziana E. schultzii R. atropur. E. marcana

0

-0.5
(MPa)

-1

-1.5
L

-2

-2.5

Fig. 4 Mean minimum leaf water potential (Ψmin L , wet (∎) and dry ( ⃞) seasons) and leaf water
potential at the turgor loss point (Ψtlp
L , wet ( ) and dry ( ) seasons) for different Andean giant
rosette species (Goldstein et al. 1984, 1985a, b; Estrada et al. 1991; Rada et al. 1998, 2012;
Navarro 2013). The Coespeletias and Espeletia schultzii (4200 m), Ruilopezia atropurpurea
(3150 m) and Espeletia marcana (3100 m)
188 F. Rada

Coespeletias and Espeletias. C. moritziana (Rada et al. 2012) and R. atropurpurea

(Navarro 2013) are the only species which are able to osmotically adjust from wet
to dry seasons allowing these two species to maintain turgor under the more
stressful dry season conditions. C. moritziana is associated with poorly developed
soils with many fractured rocks and limited water availability. R. atropurpurea
shows the smallest pith volume and relative capacitance of all studied giant rosettes
(Goldstein et al. 1985a; Meinzer and Goldstein 1986).

Seasonal Variations in Gas Exchange Characteristics

The magnitude of leaf stomatal opening and closure, estimated by leaf stomatal
conductance (gs), is regulated by different environmental factors. Among these
environmental drivers of the plant’s water status are soil water availability and
evaporative demand of the air surrounding the rosette leaves. Of all giant rosettes
studied at 4200 m, E. schultzii shows the largest reduction in gs from one season to
the other (67 %) (Table 1). This species, with a smaller capacitance, relies on
stomatal control to maintain positive leaf water potentials during the dry season. C.
timotensis, the species with the largest stem water storage capacity, shows a smaller
seasonal stomatal decrease. C. moritziana exhibits a slight decrease (15 %) in
seasonal stomatal closure from wet to dry season, suggesting that this species, with
the lowest wet season gs, maintains stomata partially opened all year round. This is
probably due to soil conditions and low relative water capacitance described pre-
viously. R. atropurpurea, growing at a lowest elevation, has the highest stomatal
conductances during the wet season, but a large decrease in the dry season (70 %).
In general, low gs observed in Andean giant rosettes explain their relatively low

Table 1 Gas exchange characteristics (leaf stomatal conductance (gs), CO2 assimilation rate (A))
for different giant rosettes of the Venezuelan páramos in wet (WS) and dry (DS) seasons
Species Altitude (m) gs (mmol m−2 s−1) Amax (μmol m−2 s−1)
WS DS WS DS
Coespeletia spicataa 4200 100.3 ± 11.0 60.1 ± 5.3 8.2 ± 0.3 6.5 ± 0.3
Coespeletia timotensisa 4200 89.9 ± 13.2 70.7 ± 6.0 4.2 ± 0.3 2.8 ± 0.7
Coespeletia moritzianab 4200 61.9 ± 7.2 52.3 ± 3.9 8.0 ± 0.3 4.5 ± 0.4
Espeletia schultziic 4200 122.3 ± 22.4 40.4 ± 7.6 2.6 ± 0.2 1.8 ± 0.3
Espeletia schultziic 3550 202.1 ± 26.6 46.8 ± 11.3 3.1 ± 0.2 2.2 ± 0.2
Espeletia floccosad 3550 87 ± 9.1 37 ± 4.3 6.7 ± 0.2 2.5 ± 0.4
Ruilopezia atropurpureae 3150 231.1 ± 56.7 69.9 ± 12.0 9.8 ± 0.6 6.0 ± 0.1
Values are mean maximum ± one standard error
a
Goldstein et al. (1989)
b
Rada et al. (2012)
c
Rada et al. (1998)
d
Unpublished data
e
Navarro (2013)
Functional Diversity in Tropical High Elevation Giant Rosettes 189

transpirational losses (maximum transpirational rates of 3 mmol m−2 s−1)

(Goldstein et al. 1984, 1989; Rada et al. 1998, 2012). The highest transpiration rates
described for Andean giant rosettes correspond to R. atropurpurea,
4 mmol m−2 s−1, during the wet season at a lower elevation (3150 m) (Navarro
2013).
Together with stomatal conductance, the water vapor pressure gradient between
leaf and surrounding air (VPD) determine leaf transpirational losses. Different
authors have described a very close relationship between stomatal conductance and
VPD for Andean rosettes (Goldstein et al. 1989; Rada et al. 1998). The integration
of these adaptive characteristics: large water reservoir in well-developed pith tissues
and a high stomatal control lead to the maintenance of a favorable plant water
balance throughout the year for Andean giant rosettes.
Mean maximum species-specific CO2 assimilation rates for giant rosettes range
from 3–10 μmol m−2 s−1 with an approximate mean of 6 μmol m−2 s−1 (Table 1).
These low rates are comparable to other woody species of the high Andes: Polylepis
sericea, a tree species, exhibits maximum rates of 7 μmol m−2 s−1 and Hypericum
laricifolium, a shrub, exhibits maximum rates of 5 μmol m−2 s−1 (Azócar and Rada
2006). The highest rates were observed in the low elevation species R. atropur-
purea. More importantly, the seasonal decreases in maximum assimilation rates are
consistent with decreasing stomatal conductance.
Optimum temperature for CO2 assimilation decreases with increasing elevation
on altitudinal gradients. E. schultzii has an optimum temperature of 11.5 °C at
2950 m, which decreases to 7.9 °C at 4200 m (Rada et al. 1992). C. moritziana’s
optimum temperature is 10.2 °C at 4200 m (Rada et al. 2012). With respect to
temperature ranges in which CO2 assimilation rates remain positive, E. schultzii’s
low temperature compensation point occurs below 0 °C, while for C. moritziana it
is approximately 3 °C. High temperature compensation points reach 25 °C for both
species at 4200 m. In neither of the two species does air temperature seem to be a
limitation to photosynthesis. Mean leaf temperatures for E. schultzii and C. mor-
itziana were always within the 80 and 90 % of the optimum temperature for
photosynthesis, respectively.

Plant Water Relations and Gas Exchange in Juvenile

Rosettes

Due to the relatively small pith water volumes, stem capacitance does not play a
significant role in the maintenance of a favorable water status in juveniles.
Additionally, environmental conditions at ground level are far more extreme than
those where adult plants inhabit. How do juvenile rosettes survive these harsher
drought conditions near the ground level of high mountain environments? There are
few studies on water relations and gas exchange in juveniles of Andean giant rosette
plants. Low survival rates of seedlings and juveniles indicate that this stage in the
life cycle is the most vulnerable due to the extreme environmental conditions at
190 F. Rada

ground level (Smith 1981; Goldstein et al. 1985a; Estrada and Monasterio 1988;
Guariguata and Azócar 1988). This high mortality is attributed to the inability of
these plants to physiologically respond to drought stress. García-Varela (2000)
indicated that the nurse effect allow juveniles of C. spicata and C. timotensis to
survive associated with adult plants or rocks, both considered favorable microsites.
Orozco (1986) described the water relations of juveniles of three different
Coespeletia species occupying contrasting habitats in the Desert Páramo. C. spicata
occurs in valley bottoms where moisture conditions are more favorable. C.
timotensis survives on slopes where soil water availability is less favorable. Even
though there are no gas exchange studies for this species, high leaf water potentials
in juveniles must be a consequence of strong stomatal closure during daily and/or
seasonal drought periods. C. moritziana juveniles tolerate lower leaf water poten-
tials (−2.3 MPa) and show an important osmotic adjustment from wet to dry season
(Orozco 1986; Rada et al. 2012).
There is only one study which considers CO2 assimilation rates for juveniles of
Andean giant rosettes (Rada et al. 2012). C. moritziana juveniles have mean rates of
5.3 and 3.5 μmol m−2 s−1 for wet and dry seasons, respectively. These rates are
comparable to other Coespeletia species, suggesting that juveniles surviving the
early stages of the life cycle respond in a similar manner to adult rosettes.

Freezing Resistance

Low temperature, and in particular subzero temperatures, is an important factor that

influences a plant’s physiology and performance, and determines, its distribution.
Tropical alpine plants avoid or tolerate ice formation in their tissues at temperatures
below the equilibrium freezing temperatures. Avoidance may occur through the
insulation of organs from surrounding low temperatures. Avoidance may also be
obtained through supercooling, the maintenance of water in a liquid state even
though temperatures may be well below their equilibrium freezing temperatures. In
the case of frost tolerance, ice formation occurs in the extracellular spaces without
damaging their intracellular contents.
Plants from environments where minimum temperatures are not extreme and
only last for a few continuous hours, i.e. tropical mountain plants, rely mainly on
avoidance mechanisms, while those subjected to severe temperatures and longer
duration rely on tolerance (Sakai and Larcher 1987). All Andean giant rosettes
studied to date rely on avoidance mechanisms to survive the conditions of the
tropical Andes.
Functional Diversity in Tropical High Elevation Giant Rosettes 191

Thermal Insulation and Nyctinastic Leaf Folding

Giant rosettes are continuously forming new pubescent leaves from an inner apical
bud (Fig. 2b). At night adult leaves fold in, known as nyctinastic movements, to form
a dense, compact layering protecting the apical bud. Hedberg (1964) described it as
the ‘night bud’ in African giant rosettes. This structure delays heat loss from the bud
towards the surrounding air avoiding freezing of internal water. Smith (1974)
described these leaf nyctinastic movements in the giant Andean rosette Espeletia
schultzii. Rada et al. (1985a) measured differences of up to 6 °C between nighttime
apical bud and air temperatures in Coespeletia timotensis and C. spicata in the high
Andes. Additionally, Ice nucleation and injury temperatures (−5 to −6 °C) for C.
timotensis and C. spicata apical buds, were approximately 8 °C below their mini-
mum measured temperature. Beck et al. (1982) report similar results for two
Afroalpine giant rosettes, Lobelia telekii and Senecio keniodendron.
Stems of most giant rosettes of the genera Espeletia and Coespeletia are covered
with a very dense layer of marcescent leaves (Fig. 2b). The leaves after senescence
remain attached to the stem. This layer acts as a thermal insulator, maintaining
internal stem tissue (e.g. phloem, xylem and pith) temperatures above 0 °C (Smith
1979; Goldstein and Meinzer 1983; Rada et al. 1985a). Minimum stem tempera-
tures remained above 2 °C while air temperature was −3 °C (Rada et al. 1985a).
Freezing of stem tissue never occurred in naturally growing giant rosettes.

Frost Injury and Supercooling

Supercooling functions in environments where minimum freezing temperatures are

not extremely low and only last for a few hours (Beck 1994), as in the high tropical
Andes. This short term supercooling is a risky strategy as ice nucleation experi-
mentally induced in supercooled tissues will immediately result in damage due to
abrupt freezing. This strategy has been described for different life forms of the
Venezuelan high Andes, trees (Rada et al. 1985b; Dulhoste 2010), shrubs (Squeo
et al. 1991) and giant rosettes. Leaves of all giant rosettes studied in the tropical
Andes rely on permanent supercooling (sensu Larcher 1975) in order to survive.
Larcher (1975) and Larcher and Wagner (1976) observed ice nucleation tempera-
tures of −12 °C in leaves of Espeletia semiglobulata. Subsequently, Rada et al.
(1985a) described permanent supercooling capacities of −16 and −14 °C for
Coespeletia spicata and C. timotensis, respectively. Additional research in other
giant rosette species confirmed that temperatures at which ice nucleation began
coincided with that at which injury occurred, therefore indicating that leaves were
not able to resist ice formation in their tissues (Goldstein et al. 1985b; Rada et al.
1987; Cavieres et al. 2000; Dulhoste 2010).
192 F. Rada

The supercooling capacity found in Andean giant rosettes may be explained by:
(a) Sessile leaves which reduce wind effects and buffer ice nucleation, (b) presence
of a hydrophobic pubescent layer on leaves as a barrier for external nucleators,
(c) Small cell sizes and intercellular spaces to reduce the chance of ice crystal
formation in these apoplastic spaces (Goldstein et al. 1985b; Rada et al. 1987).
The water status of a plant is known to affect its supercooling capacity (Burke
et al. 1976; Levitt 1980). Goldstein et al. (1985b) and Rada et al. (1987) explained
how supercooling capacity of Andean giant rosettes increases as ΨL becomes more
negative, with plants from higher altitudes being more sensitive to these changes.
This pattern was observed for a single species, E. schultzii, along a 2600–4200 m
altitudinal gradient, and for a group of species from different altitudes (Rada et al.
1987; Goldstein et al. 1985b). Although this increased supercooling capacity with
decreasing ΨL should not be considered a response, it is of great adaptive value
since minimum air and leaf temperatures occur during the dry season, when plants
exhibit their minimum leaf water potentials.
Supercooling capacity and injury temperatures of giant rosettes are closely
related to elevation (Fig. 5). Species from lower elevations show ice nucleation and
injury temperatures between −5 and −8 °C, with higher elevation species below
−10 °C. Goldstein et al. (1985b) observed decreasing ice nucleation temperatures
with increasing elevation in ten species of the genera Ruilopezia, Espeletia and
Coespeletia. Rada et al. (1987) found similar results for different E. schultzii
populations growing from 2600 to 4200 m in elevation. The decreases in apoplastic
water content and cell size account for the changes in supercooling capacity, with
lower apoplastic water content observed in higher elevation giant rosettes with
higher supercooling capacity.

ALTITUDE (m)
2500 3000 3500 4000 4500
0
-2
TEMPERATURE (°C)

-4
-6
-8
-10
-12
-14
-16

Fig. 5 Relationship between ice nucleation (○) and injury (●) temperatures and altitude for the
different giant rosette species along an elevational gradient. For ice nucleation temperature:
INT = −0.0045(altitude) + 6.26, r2 = 0.78 and for injury temperature: IT = −0.0045(altitude) + 5.85,
r2 = 0.83. Absolute minimum temperature line (——)
Functional Diversity in Tropical High Elevation Giant Rosettes 193

Freezing Avoidance in Juvenile Rosettes

Night re-irradiation from the soil surface determines the low temperatures at ground
level. Plants growing closer to the ground are subjected to more extreme subzero
temperatures compared to taller rosettes which occur further above the ground
level. Adult giant rosettes avoid freezing temperatures through isolating structures
and supercooling. But how do juveniles, growing under a more stressful environ-
ment near the ground, survive freezing temperatures? García-Varela and Rada
(2003) report avoidance mechanisms through permanent supercooling capacity in
juveniles of Coespeletia timotensis and C. spicata (ice nucleation and injury tem-
peratures of −15 °C). A high mortality rate during establishment may also be a
consequence of extreme low nighttime temperatures (Estrada and Monasterio
1988). Established seedlings and juveniles are associated with favorable micro-
habitats such as near adult giant rosettes, rocks or cushion plants (García-Varela
2000; Smith 1981; Pérez 1984, 1989).

Functional Responses of Giant Rosettes Versus Other

Andean Plant Life-Forms

The ability of giant rosettes to maintain turgor is comparable to other tropical

Andean plant life-forms. Trees and shrubs exhibit mean Ψtlp L around −1.8 MPa,
while herbaceous life forms have values between −2.2 and −2.5 MPa (Fig. 6a). If
we consider ΨminL as a measure of tolerance to drought conditions, the giant rosettes
have the most positive values of all life-forms, significantly above the turgor loss
point. General morphological characteristics discussed above and positive mean
leaf water potentials and minimum leaf water potentials which remain above the
turgor loss point indicate that Andean giant rosettes are extremely drought avoidant
species.
Injury in giant rosettes is comparable to trees, shrubs and forbs, while acaulescent
rosettes, grasses and cushion having lower injury temperatures (Fig. 6b). Trees and
giant rosettes rely exclusively on avoidance mechanisms (Rada et al. 1985a, b;
Goldstein et al. 1985b), mainly through supercooling, while grasses (Márquez et al.
2006), acaulescent rosettes and cushion plants (Azócar et al. 1988; Squeo et al. 1991)
tolerate ice formation, and thus cell dehydration, in their leaf tissues. The other two
life-forms, shrubs and forbs, exhibited both avoidance and tolerance mechanisms
(Squeo et al. 1991; Azócar 2006).
194 F. Rada

Fig. 6 a Mean leaf water potential (ΨL) at turgor loss (●) and mean minimum leaf water potential
( ) for different plant life-forms of the Andean tropical mountain. Vertical bars extend up and
down to absolute maximum and minimum leaf water potentials at turgor loss for each of the
life-forms. b Mean injury temperature (●) for different plant life-forms of the Andean tropical
mountain. Vertical bars extend up and down to absolute maximum and minimum injury
temperatures for each of the life-forms. Trees (T), giant rosettes (GR), shrubs (Sh), forbs (F),
acaulescent rosettes (AR), cushions (C), grasses (G)

Functional Responses of Andean Versus Other Tropical

Alpine Giant Rosettes

Important differences are found when functional characteristics of Andean and

other tropical giant rosettes are compared (Table 2). Although injury temperatures
are similar for both Andean and Afroalpine rosettes growing above 3500 m, the
former avoid frost while the latter tolerate extracellular ice formation in their leaf
tissues. African giant rosettes (studied at 4200 m) have a high ice nucleation
temperature while injury occurs at a much lower temperature, typical of plants that
tolerate ice seeding in the extracellular spaces and thus cell dehydration. This
difference in mechanisms highlights two important aspects of giant rosette plant
function. As stated previously, plants rely on avoidance in less extreme environ-
ments compared to tolerant species (Sakai and Larcher 1987) which assumes that
Afroalpine rosettes are adapted to harsher conditions than Andean rosettes. In terms
of water relations, afroalpine rosettes being tolerant to freezing are also tolerant to
drought. Even though daytime mean minimum leaf water potentials of Afroalpine
giant rosettes (Schulze et al. 1985) may be comparable to the lowest minimum leaf
Functional Diversity in Tropical High Elevation Giant Rosettes 195

Table 2 Comparison Functional characteristics Andean Afroalpine

between functional
characteristics of Andeana and INT (°C) −12.8 −5.3
Afroalpine giant rosettes IT(°C) −12.7 −12.3
Ψmin
L (MPa) −1.5 −2.1 (−5.2)b
−2 −1
gs (mmol m s ) 106/44 c
–/130
Amax (μmol m−2 s−1) 7.3/4.3 –/9.5
INT ice nucleation temperature, IT injury temperature, Ψmin L
Minimum leaf water potential, gs mean leaf stomatal
conductance, Amax: maximum CO2 assimilation rate
a
Data correspond to Andean giant rosettes at 4200 m so that they
are comparable to the results presented for afroalpine rosettes
b
Leaf water potential of frozen leaves (−4.4 °C) at night (Beck
et al. 1984)
c
Values for gs and Amax correspond to wet/dry seasons

water potentials reported for Coespeletia moritziana (Rada et al. 2012), Beck et al.
(1984) have observed survival of Afroalpine rosettes down to an absolute minimum
leaf water potential of −5 MPa. This ability to withstand extremely low leaf water
potentials allows Afroalpine rosettes to maintain stomates open during drought
(Table 2). Mean stomatal conductance of Afroalpine giant rosettes during the dry
season is three times higher than Andean giant rosettes during the dry season and is
slightly higher than the mean stomatal conductance of Andean giant rosettes during
the wet season. Consequently, Afroalpine giant rosettes maintain higher CO2
assimilation rates (Schulze et al. 1985; Lüttge et al. 2001) which in turn results in
higher growth rates.
Leaf pubescence affects the thermal balance of Andean giant rosettes by
increasing the boundary layer thickness while light reflectance seems to have a
minor role. This effect on the boundary layer results in an uncoupling of leaves and
air temperatures, with leaves at several degrees above air temperature. Unlike
Andean giant rosettes, the Hawaiian giant rosette Argyroxiphium sandwicense, with
a relatively thin leaf pubescence, has similar leaf and air temperatures under high
incoming solar radiation (Melcher et al. 1994). The leaf pubescence of this species
is highly reflective. The temperature of the apical bud, which is located in the center
of the parabolic rosette, is usually 25 °C higher than air temperatures at midday,
because the incoming solar radiation is focused towards the apical bud. These
authors suggest that this heating effect enhances the rates of physiological processes
and growth rates of developing leaves.
Lipp et al. (1994) and Goldstein et al. (1996) found an interesting case in terms
of freezing resistance adaptations in Argyroxiphium sandwicense. Adult A. sand-
wicense rosettes tolerate freezing, similar to the African counterpart; while seed-
lings avoid freezing of their leaf tissues. Ice nucleation and injury temperatures for
these Hawaiian juvenile rosettes are similar to those of Andean rosette species
(Goldstein et al. 1985b; Rada et al. 1985a; García-Varela and Rada 2003).
196 F. Rada

Giant Rosettes and Climate Change

Mountain ecosystems represent an important source of water and energy, maintain

high endemism due to high altitude isolation and display a high biological diversity
(Beniston 2003). Temperature and precipitation variations along elevational gra-
dients are large, resulting in drastic changes in vegetation types along the slopes of
tropical mountains. This close relationship between climate and environment in
relatively short transitional zones makes them sensitive to any climatic change
(Gosling and Bunting 2007). The combination of a fragile ecosystem and an
amplified climate change illustrates the dramatic effect global change may have on
mountain areas (Buytaert et al. 2010), important hotspots of biodiversity (Myers
et al. 2000).
Global climate change will have a strong impact on water resources. Higher
temperatures are likely to increase evapotranspiration, saturated atmospheric water
vapor content and may result in changes in precipitation patterns and frequency of
extreme events (Bates et al. 2008), mainly in mountain climates under the influence
of continental or Mediterranean regimes (Beniston 2003). There is little agreement
on the effects of climate change on precipitation patterns for mountain ranges (IPCC
2007). The Andes stand out as a region of high projection uncertainty, casting
doubts on the reliability of future predictions. Large errors in the simulation of
precipitation patterns over the Andes result when the model is compared to
observational data (Buytaert et al. 2010).
A first approximation in relation to the response of mountain vegetation to
climate change is that species will migrate upwards. However this hypothesis may
be too simplistic, Walther et al. (2005) recognize that shifts are species-specific and
do not occur as a vegetation ‘front’. Moreover, projections that assume that plant
migration occurs along isotherms overestimate change at the level of vegetation
belts while the effect on single species may be underestimated (Körner 2003). These
differences in species migration rates may be due to their different tolerance ranges,
longevities, survival rates, competition abilities among other varying limiting fac-
tors (Beniston 2003). Migration evidence has not been documented for the Andes
although they have been described for temperate and other tropical mountains
(Chen et al. 2011; Pauli et al. 2012). The predicted upward shifting of plant species
was evidenced as an effect of global warming through an increase in species
richness at mountain summits (Grabherr et al. 1994, 2010; Pauli et al. 1996). These
latter authors also state that the migration of vascular plants was far below the
hypothetical rates of upward movement of temperature isolines indicating an
important time lag between temperature increase and ecological responses. Climate
induced differential migration rates could lead to the formation of new plant
assemblages and result in changes in ecosystem functioning (Root et al. 2003).
Together with migration, plants may respond in two other ways to changes in
climate conditions: through adaptation or local extinction (Thuiller et al. 2008).
How plants will respond depends on their physiological and ecological character-
istics. Studies on plant communities of the tropical Andes suggest that species with
Functional Diversity in Tropical High Elevation Giant Rosettes 197

restricted ranges and those at higher elevations will show a large contraction in their
habitat distribution and perhaps many species will be driven towards extinction
(Cuesta and Becerra 2012). Furthermore, an elevational shift always implies a loss
in habitat size as a consequence of diminishing and more fragmented surface area
with increasing elevation. Therefore high mountain community assemblages are
expected to be modified by increased habitat fragmentation and increased compe-
tition compared to species from lower elevations (Walther et al. 2005).
The paramo may be considered one of the most recently assembled ecosystems
and its presence as a well differentiated and unique ecosystem may be due to:
Altitudinal conditions above 3000 m, geographical location and incoming solar
radiation, specific humidity and precipitation conditions in both horizontal and
vertical gradients, and the central position of the northern Andes along the
Alaska-Patagonia biological corridor permitting an important genetic exchange
between North and South American species. These conditions determine certain
important characteristics of the vegetation: a wide range of adaptability to extreme
conditions of day-night cycles rather than seasonal ones, the fragility to climatic
variations due to the very specialized physiology of most plants and the highest
endemism index compared to any other ecosystem (Castaño-Uribe 2002).
Uncertainty in future projections is the rule for the tropical high Andes.
Temperature is expected to rise over the next century due to anthropogenic activity
(IPCC 2007). Existing projections on temperature shifts are rather consistent and
suggest a 3 ± 1.5 °C rise for the Andes in the next century (Buytaert et al. 2011).
For the last 30 years a 0.34 °C/decade increase has been observed for the northern
Andes (Vuille et al. 2003). Again there are no clear projections in relation to
precipitation patterns. Different reports suggest an approximate 300 mm year−1
increase in a century for Ecuador and most of Colombia, while Northern Colombia
and Venezuela, dominated by trade winds, will show a decreasing rainfall trend
(Buytaert et al. 2011).
Characteristic long life cycles of alpine vegetation represent a greater vulnera-
bility to disturbance in comparison to low elevation plants (Körner 2003). Pioneer
species, with rapid growth rates and production of large amounts of easily dispersed
seeds, may take advantage of climate change by facilitating rapid upward move-
ment (Salick et al. 2009). The extent to which physiological characteristics change
via plasticity or evolution are essential in the projection of the effects of climate
change. If plastic responses and/or evolutionary adjustments do not occur or are
slower than environmental change, plant species will go extinct (Chown et al.
2010).
Resistance to freezing temperatures is a prerequisite for plant survival and
determine to great extent plant distribution at high elevations. Increasing temper-
atures result in an upward displacement of the frost line giving the opportunity to
plants from lower elevations to ascend and occupy sites of established alpine plants.
Under this condition, competition with lower elevation vegetation would seem to
play a more determining role in giant rosette distribution at the pre-páramo
forest/páramo transition zone.
198 F. Rada

Increasing daytime temperatures would not seem to have an important effect on

photosynthetic capacity of giant rosettes. CO2 assimilation in giant rosettes is
maintained at high levels in a wide temperature range. However, higher tempera-
tures will determine higher ambient evaporative demands and lower soil water
availability. Together with projected decreases in precipitation for the Northern
Andes, they may have an effect on water relations and gas exchange of giant
rosettes. Compared to other páramo life-forms, the giant rosettes may be labeled as
extreme drought avoiders. In order to maintain high leaf water potentials a stronger
stomatal control under unfavorable conditions will take place limiting plant phys-
iological activities such as CO2 assimilation and consequently affecting growth.
It is reasonable to assume that species that show similarities in essential func-
tional characteristics will respond in a similar manner to changes in climatic con-
ditions (Diaz and Cabido 1997). As a dominant functional group, all studied giant
rosettes show a narrow range of responses to water stress, suggesting that they may
be susceptible to the changing environmental conditions which in turn result in a
low resilience and a fragile functional stability of the high elevation ecosystems
dominated by giant rosette plants (Azócar et al. 2000).

Acknowledgements Financial support of the author’s research by the Consejo de Desarrollo

Científico, Humanístico, Tecnológico y de las Artes (CDCHTA) of the Universidad de Los Andes,
the Fondo Nacional de Ciencia, Tecnología e Innovación (FONACIT) and the Inter-American
Institute for Global Change Research (IAI) is gratefully acknowledged.

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 Part III
Plant Hydraulics and Water Relations
Physiological Significance of Hydraulic
Segmentation, Nocturnal Transpiration
and Capacitance in Tropical Trees:
Paradigms Revisited

Sandra J. Bucci, Guillermo Goldstein, Fabian G. Scholz

and Frederick C. Meinzer

Abstract Results from water relations and hydraulic architecture studies of trees
from tropical savannas and humid tropical and subtropical forests were reanalyzed
in view of paradigms related to the (i) physiological significance of hydraulic
segmentation across trees with different life history traits and habitats, (ii) deter-
minants of massive tree mortality, (iii) nocturnal transpiration, and (iv) the role of
internal stem water storage. Stems and leaves of tropical and subtropical deciduous
tree species are equally vulnerable to cavitation, whereas leaves of evergreen
species are substantially more vulnerable than stems. Tree species from tropical
ecosystems that do not experience seasonal droughts have stems and leaves with
similar vulnerability to cavitation while trees from tropical ecosystems that expe-
rience seasonal droughts have leaves that are more vulnerable to drought induced
cavitation compared to stems. Strong segmentation (whether hydraulic or
vulnerability) during severe droughts may have an indirect negative impact on tree

S.J. Bucci (&)
F.G. Scholz

Grupo de Estudios Biofísicos y Ecofisiológicos, Facultad de Ciencias Naturales, Universidad
Nacional de la Patagonia San Juan Bosco, Comodoro Rivadavia, Chubut, Argentina
e-mail: sj_bucci@yahoo.com
F.G. Scholz
e-mail: fgscholz@yahoo.com
S.J. Bucci
F.G. Scholz
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET),
Buenos Aires, Argentina
G. Goldstein
Laboratorio de Ecología Funcional, Departamento de Ecología Genética y Evolución,
Instituto IEGEBA (CONICET-UBA), Facultad de Ciencias Exactas y naturales,
Universidad de Buenos Aires, Buenos Aires, Argentina
e-mail: goldstein@ege.fcen.uba.ar; gold@bio.miami.edu
G. Goldstein
Department of Biology, University of Miami, Coral Gables, FL 33146, USA
F.C. Meinzer
USDA Forest Service, Forestry Sciences Laboratory, 3200 SW Jefferson Way, Corvallis,
OR 97331, USA
e-mail: rick.meinzer@oregonstate.edu

© Springer International Publishing Switzerland 2016 205

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_9
206 S.J. Bucci et al.

carbon balance. For example for Sclerolobium paniculatum, a widespread tree

species in neotropical savannas and seasonally dry forests, the decrease in total leaf
surface area per plant (which impact hydraulic architecture) during droughts help to
maintain an adequate water balance but has large physiological costs: trees receive a
lower return in carbon gain from their investment in stem and leaf biomass. Leaf
hydraulic failure and carbon starvation may contribute to the massive,
size-dependent mortality observed in this species. The functional significance of the
widespread phenomenon of nocturnal transpiration in tropical trees is discussed.
One of the most likely functions of nocturnal sap flow in savanna trees growing in
nutrient poor soils appears to be enhanced nutrient acquisition from oligotrophic
soils. Large capacitance plays a central role in the rapid growth patterns of tropical
deciduous tree species facilitating rapid canopy access as these species are less
shade tolerant than evergreen species. Higher growth rates in species with high
capacitance could be achieved by keeping the stomata open for longer periods of
time.

Keywords Carbon starvation
Mortality
Safety margin
Transpiration

Vulnerability to cavitation

Introduction

Physiological traits of tropical trees have been extensively studied for many years.
Although characterization of tree hydraulic architecture was initially conducted on
temperate species (e.g. Zimmermann 1983), it did not take too long for this
approach to be applied for investigating aspects of water relations of woody plants
in tropical ecosystems. The first forest canopy tower crane was erected in Panama in
the early 1990s. Until then, direct observations of transpiration, stomatal behavior
and other physiological attributes in the upper canopy of mature tropical forests
were hampered by difficulty of canopy access. This problem had been partially
overcome by a variety of canopy access systems. Towers have been used to make
observations in the upper canopy of Amazonian forests (e.g. Roberts et al. 1990).
Other access systems include a large canopy-supported raft used in Cameroon
(Koch et al. 1994), but the real breakthrough for assessing the integration of
whole-tree physiological behavior was the use of canopy cranes (e.g. Meinzer et al.
1993). Previously, studies on aspects of the hydraulic architecture of high-elevation
woody giant rosettes in the tropics, and in particular on the role of internal water
storage in the water economy of these woody plants, were done with state of the art
instrumentation by researchers at the Universidad de Los Andes in Venezuela (e.g.
Physiological Significance of Hydraulic Segmentation … 207

Goldstein and Meinzer 1983). Although these arborescent giant rosettes can be
considered functionally as trees, they rarely attain heights greater than 4 m.
Similarly, savanna trees, particularly in South America, are relatively short, and
thus access to their upper crowns does not require tower cranes. The hydraulic
architecture of this type of trees has been extensively investigated in Venezuela and
Brazil for many years, resulting in an important body of knowledge for under-
standing how plant hydraulics, such as stem and leaf hydraulic resistances, stem
capacitance, embolism formation and repair, hydraulic segmentation, and root
morphological patterns in relation to hydraulic lift, influence tree water relations
worldwide (e.g. Bucci et al. 2003, 2004, 2005, 2006, 2008; Goldstein et al. 1984,
1989; Hao et al. 2008; Sarmiento et al. 1985; Meinzer et al. 1999, Scholz et al.
2002, 2006, 2008a, b; Zhang et al. 2009).
In this chapter we focus on some aspects of the water economy and water
relations of tropical trees that are perhaps more controversial. We explore the
validity of some paradigms that are currently being debated. There are two general
questions related to the hydraulic architecture of trees i.e., the assemblage of
structural and functional traits that determine the dynamic patterns of water flow
from roots to leaves that will be discussed. One question is related to hydraulic
segmentation and the other is related to the potential role of hydraulic architecture
traits on the massive mortality of trees. It is assumed that hydraulic segmentation
(differences in the resistance to water flow in roots, stems and leaves according to
Zimmermann 1983) is widespread across tree species. We will assess the extent to
which differences in the degree of hydraulic segmentation among tropical trees are
related to differences in life history traits (e.g. deciduous vs. evergreen) versus
environmental characteristics where the trees occur (e.g. with and without a pro-
nounced dry season). Increasing tree mortality rates as a consequence of more
frequent droughts or an increase in the severity of the droughts has been recently
observed worldwide (Allen et al. 2010). The mechanisms of drought-induced
mortality are not well known. In this chapter we provide evidences of two potential
mechanisms triggering dieback (hydraulic dysfunction and carbon starvation)
mediated by strong hydraulic segmentation for a tropical tree species.
Nocturnal sap flow has been observed predominantly in tropical ecosystems
(Forster 2014), however its functional significance has been little studied. In this
chapter we provide strong evidence that enhanced nutrient uptake by nocturnal
transpiration for plants growing in oligotrophic (nutrient poor) soils are likely to
have an important role in the nutrient balance of some tropical tree species. Finally,
we discuss the key role that internal stem water storage plays in many aspects of
tropical tree functioning, and in particular for helping to maintain high growth rates
in low wood density species (mostly deciduous). The large sapwood capacitance in
deciduous species may also help to avoid catastrophic xylem embolism, and extend
the period which stomata are able to remain open for carbon assimilation diurnally.
208 S.J. Bucci et al.

Hydraulic Segmentation and Vulnerability Segmentation

A widespread paradigm in studies of the water relations of vascular plants is that

hydraulic segmentation prevents cavitation from propagating into less expendable
portions of the water transport system. A key feature of hydraulic segmentation is
that during periods of high evaporative demand over the course of a day or during a
drought period, cavitation is mostly confined to more expendable organs (i.e. leaves
and small branches) in favor of larger organs such as trunks that represent years of
cumulative growth and carbohydrate investments. The range of variation in the
extent and patterns of hydraulic segmentation among tropical trees is not well
known. Another concept related to hydraulic segmentation is vulnerability seg-
mentation. Hydraulic segmentation refers to the differential resistance to water flow
in different parts of woody plant along the root-to-leaf continuum, whereas vul-
nerability segmentation refers to the differential vulnerability to embolism
depending on the organ along the continuum. Implicit in the vulnerability seg-
mentation concept and its relationship to hydraulic segmentation is that leaves are
more vulnerable than branches and trunks. The hydraulic architecture of leaves and
their vulnerability to embolism have only recently been studied intensively (e.g.
Nardini et al. 2001; Broddrib et al. 2003; Sack and Holbrook 2006; Blackman et al.
2010; Johnson et al. 2011; Scoffoni et al. 2014), whereas the vulnerability of stems
and roots to embolism has been studied for several decades (e.g. Tyree and Sperry
1989; Kavanagh et al. 1999; Maherali et al. 2004; Domec et al. 2006). Although
leaves and stems represent consecutive points along a hydraulic continuum, there
are relatively few studies of their hydraulic properties in the same individual (e.g.
Hao et al. 2008; Bucci et al. 2012, 2013).
The extent of hydraulic segmentation is different depending on leaf phenology
(i.e. deciduous versus evergreen species) and depending on seasonal water avail-
ability. A review of studies having simultaneous measurements of vulnerability to
cavitation in stems and leaves suggests that stems and leaves of tropical and sub-
tropical deciduous tree species are equally vulnerable to cavitation as assessed from
Ψ50, species-specific values of leaf or stem water potential inducing 50 % loss of the
maximum leaf or stem hydraulic conductivity (Fig. 1a). Leaves of evergreen species
appear to be substantially more vulnerable than stems, which on average were
1 MPa less vulnerable compared to leaves (Fig. 1a). Tropical tree species from
ecosystems that do not experience pronounced seasonal droughts have stems and
leaves with similar vulnerability to cavitation, whereas trees from ecosystems that
experience seasonal droughts have leaves that are more vulnerable to
drought-induced cavitation than stems (Fig. 1b). In this case, hydraulic segmenta-
tion may help to prevent hydraulic dysfunction of the trunks and stems during mild
droughts. It appears that tree species from aseasonal climates have not been sub-
jected to selective pressures resulting in a highly segmented hydraulic architecture.
Implicit in this assessment of relationships between selective pressures and evo-
lutionary responses is the assumption that there is a cost associated with building
Physiological Significance of Hydraulic Segmentation … 209

(a) 0.0

-0.5

Ψ50 (MPa)
-1.0

-1.5

-2.0 Leaves
Stems
***
-2.5
Dedicuous Evergreen

(b) 0.0

-0.5

-1.0
Ψ50 (MPa)

-1.5

-2.0

-2.5 Leaves
Stems ***
-3.0
Without seasonality With seasonality

Fig. 1 Leaf water potential at 50 % loss of maximum leaf hydraulic conductance (Ψ50, open
columns) and stem water potential at 50 % loss of maximum stem hydraulic conductance (Ψ50,
filled columns) of 26 a deciduous and evergreen tree species from tropical and subtropical
ecosystems and b tree species from ecosystems without rainfall seasonality and with rainfall
seasonality. Significant differences between columns are indicated as ***(p < 0.0001). Information
obtained from Bucci et al. (2008), Hao et al. (2008), Chen et al. (2009), McCulloh et al. (2012),
Johnson et al. (2012), Villagra et al. (2013)

leaves with high resistance to water flow. Across species, regardless if they are
deciduous or evergreen or from seasonal or non-seasonal environments, mean leaf
Ψ50 is similar with values close to −1.25 MPa.

Hydraulic Failure and Carbon Starvation

as Determinants of Mortality

The precise mechanisms and plant traits underlying species-specific vulnerability to

drought-induced mortality are poorly understood but are currently the subject of a
debate and ongoing research (McDowell et al. 2011; Allen et al. 2012; Choat et al.
210 S.J. Bucci et al.

2012; Sala et al. 2012; Hartmann et al. 2013; Plaut et al. 2013). Two non-mutually
exclusive mechanisms have been suggested to explain drought-induced mortality in
trees (McDowell et al. 2008). Species with tight stomatal control to avoid hydraulic
failure (isohydric) have reduced CO2 assimilation during prolonged drought with
negative consequences for their carbon economy, which may eventually lead to
carbon starvation (Sala et al. 2010; Adams et al. 2013). At the other extreme,
anisohydric species, which exhibit loose stomatal control allowing large fluctua-
tions in leaf water potential may be predisposed to hydraulic failure if they operate
with narrow hydraulic safety margins (Bucci et al. 2013). Knowledge of hydraulic
safety margins may be more informative than only documenting xylem water
potentials or xylem vulnerability to embolism because safety margins indicate how
closely a plant operates to the loss of its hydraulic capacity. The safety margin is the
difference between the lowest water potential experienced by plant organs such
leaves and stems, and a reference point at which a given loss of xylem hydraulic
function occurs. The Ψ50 is the most commonly used index of xylem resistance to
embolism, however, this threshold value is not always the best reference point to
compare the susceptibility to irreversible hydraulic failure across species (Scholz
et al. 2014). Gymnosperms generally exhibit wider safety margins than angios-
perms (Meinzer et al. 2009; Choat et al. 2012; Johnson et al. 2012).
A frequently cited paradigm is that the safety margin between leaves and stems
is large enough to avoid any hydraulic dysfunction in the stems during droughts,
assuming that the leaves are more vulnerable to cavitation than stems (vulnerability
segmentation). However, strong segmentation (whether hydraulic or vulnerability)
during severe droughts may have indirectly a negative impact on the tree carbon
balance. An interesting case of dieback has been documented in a tree species
having rapid growth and a relatively shallow root system that occurs in neotropical
savannas and seasonal dry forests in Brazil (Zhang et al. 2009). Massive mortality
in taller trees of Sclerolobium paniculatum appears to be the result of leaf hydraulic
conductance loss due to strong hydraulic segmentation leading to leaf senescence
during periods with low water availability (Zhang et al. 2009). This species is an
evergreen tree species that usually renew the entire leaf crop during the dry season
(the leaf life span is about 14 months). Even though its stems have a wide safety
margin (2.2 MPa or larger depending on tree height) and are well protected by
vulnerable leaves (Fig. 2a), the leaves in the top of the canopy of taller trees have
lower leaf hydraulic conductance (Kleaf) compared to leaves of smaller trees
(Fig. 2b). The threshold of water potential leading to hydraulic dysfunction can be
reached frequently, particularly in leaves of taller trees resulting in leaf senescence
and leaf drop, which decreases the photosynthetic surface for carbon assimilation.
Furthermore, net CO2 assimilation decreases substantially with increasing tree
height (Fig. 2b). Lower Kleaf may result in more negative leaf water potentials at a
given transpiration rate, lower stomatal conductance and lower rates of CO2 dif-
fusion to the sites of carboxylation in the leaf mesophyll. A decline in total leaf
surface area per plant in taller individuals would temporarily help to maintain
adequate water balance, but a substantial decrease in total leaf surface area and
relatively low carbon uptake per unit leaf surface area have a large physiological
Physiological Significance of Hydraulic Segmentation … 211

(a) 3.5

3.0
Leaf Ψ50-Stem Ψ50 (MPa)
2.5

2.0

1.5

1.0

0.5

0.0
<3 3 to 6 6 to 8 >8
Tree height (m)

0.14
(b) 35
K leaf (mmol m MPa )

30 0.12
-1

A (μmol g s )
-1
-1
-2

25 R2 = 0.89 0.10

20 <3m 0.08
3 to 6 m
6 to 8 m
R2 = 0.90
>8m
15 0.06
0 10 20 30 40 50
Dead branches (%)

Fig. 2 a Safety margin between leaf Ψ50 and stem Ψ50 (leaf Ψ50–stem Ψ50) for Sclerolobium
paniculatum trees with different stature and b Leaf hydraulic conductance (black symbols) and net
assimilation rate (open symbols) versus the percentage of S. paniculatum dead branches for trees
with different height. Values are mean ±1SE (n = 4–6 trees for Kleaf and n = 6–14 for a).
Information obtained from Zhang et al. (2009)

cost: larger S. paniculatum trees receive a lower return in carbon gain from their
investment in stem and leaf biomass compared to small trees. Two mechanisms
were apparently responsible for massive mortality in tall S. paniculatum trees: leaf
hydraulic failure and carbon starvation. Leaf hydraulic failure can trigger leaf
senescence and leaf drop, and thus result in a substantial decrease in carbon uptake.
New leaf production would be limited if growth will depend more on the depleted
internal carbohydrate pool stored in permanent tree parts such as roots and/or stems
than on exogenous carbon assimilation. Ultimately, carbon starvation will drive the
taller trees to mortality. No apparent symptoms of herbivore damage was observed,
thus biotic attacks may not play a role in the mortality of S. paniculatum.
212 S.J. Bucci et al.

A similar mass mortality phenomenon associated with strong vulnerability

segmentation has been recently studied (Scholz et al. 2014). Dieback was observed
in South America temperate forests during one of the most severe droughts of the
20th century (1998–1999). During this drought period Nothofagus dombeyi expe-
rienced symptoms of water stress, such as leaf wilting and abscission, before tree
die-back occurred. Even though N. dombeyi stems had a threshold of −6.7 MPa
before reaching nearly complete hydraulic failure (Ψ88), leaf Ψ 88 occurred at a leaf
water potential of only −2 MPa, which probably is reached during extreme episodic
droughts. Massive mortality in N. dombeyi appears to be the result of the total loss
of leaf hydraulic conductance leading to leaf dehydration and leaf drop and ulti-
mately to carbon starvation.
Another proposed mechanism, in addition to hydraulic failure and carbon star-
vation, is cellular metabolism limitation during drought. This hypothesis suggests
that low tissue water potentials during drought may constrain cell metabolism
(Würth et al. 2005; Ryan et al. 2006; Sala and Hoch 2009) thereby preventing the
production and translocation of carbohydrates and secondary metabolites necessary
for plant defense against biotic attacks and herbivory. Of course in addition to
physiological mechanisms, there are other common modes of mortality in tropical
forests that are related to biomechanical factors, and not necessarily to drought,
such as uprooting, trunk snapping, and defoliation due to high winds (Putz et al.
1983; Kraft et al. 2010).

Nocturnal Transpiration

Nocturnal transpiration has been found to occur across many plant species, seasons
and biomes (e.g. Caird et al. 2007; Dawson et al. 2007; Forster 2014). Nocturnal
sap flow in trunks, in general, is the consequence of nocturnal leaf water loss
through open stomata or the recharge of water storage. There is no general
understanding as to how much nocturnal flow (Qn) occurs and whether it is a
significant contribution to total daily sap flow (Q). A recent literature review
assessing the magnitude of Qn as a proportion of Q across seasons, biomes, and
phylogenetic groups found that among 98 species Qn was 12.03 % on average, but
ranging up to 69 % with equatorial and tropical biomes having significantly higher
percentages of Qn than warm temperate biomes (Forster 2014).
There is no consensus concerning the functional significance that nocturnal
water flow may have for trees and ecosystems. Of course, some species may be
incapable of complete stomatal closure at night, which presumably would not
confer an adaptive advantage. Some of the suggested roles of Qn are (1) recharge of
internal water storage, (2) embolism repair, (3) improving nutrient acquisition by
driving bulk flow of soil water to the root surfaces, (4) sustaining carbohydrate
export and other processes driven by dark respiration, particularly in fast
growing-light requiring tree species, (5) and improving oxygen supply to the
sapwood at night which may be necessary to sustain respiration in xylem
Physiological Significance of Hydraulic Segmentation … 213

parenchyma (Bucci et al. 2004; Scholz et al. 2006; Snyder et al. 2008). Regarding
the role of Qn for improving nutrient acquisition it is necessary to mention that for
many ions, it is their mobility and solubility in the soil, rather than the maximal
inflow rate, that determines the rate at which roots can acquire them from the
rhizosphere (Clarkson 1981).
The highest percentage of species with nocturnal water loss has been observed in
tropical regions probably as a consequence of the widespread presence of olig-
otrophic and very nutrient poor soils (Scholz et al. 2006; Forster 2014). Nitrogen or
phosphorus limitations on growth are common in tropical regions, and are partic-
ularly severe in the neotropical savannas of central Brazil (Cerrado) characterized
by well-drained, old oxisols. These soils are not only highly nutrient deficient, and
their pH and cation exchange capacities low, but their aluminum saturation levels
are high, which may affect phosphorylation and reduce availability of calcium and
phosphorus (Furley and Ratter 1988; Haridasan 2000). Moreover, seasonal drought,
high irradiances and high atmospheric evaporative demand are characteristic of
neotropical savannas. Although savanna trees can achieve high transpiration rates
and high stomatal conductances, which could potentially increase nutrient uptake,
hydraulic limitations and the high evaporative demand of the atmosphere during the
daytime, particularly during the dry season, impose strong stomatal control of
transpiration via partial stomatal closure (Meinzer et al. 1999; Bucci et al. 2005,
2008). Thus, imbalances in water uptake and loss during the daytime may sub-
stantially constrain plant capacity to optimize nutrient uptake.
There is evidence that the transpiration stream is largely responsible for sup-
plying mobile soil nutrients (e.g., nitrate) to plant roots. When the nutrients arrives
at the root surface, its transport across the plasma membrane may occur either by
diffusion down an electrochemical potential gradient or mainly by active transport
against an electrochemical potential gradient. For many ions, it is their mobility in
the soil, rather than the maximum inflow rate, that determines the rate at which
roots can acquire them from the rhizosphere (Clarkson 1981). Maintenance of water
flux through the soil–plant–atmosphere continuum via nighttime transpiration could
enhance nutrient supply to plant roots and hence improve the nutrient balance of
savanna trees growing in oligotrophic soils. If this assumption is correct, then lower
rates of nocturnal water loss should be observed in plants growing in
nutrient-deficient soils where nutrient limitations have been relieved. Scholz et al.
(2006) made use of a long-term fertilization experiment in a savanna ecosystem of
Central Brazil in which N, P and N + P nutrients had been added twice a year from
1998 to 2006. Qualea grandiflora, a common savanna tree growing in
non-fertilized plots exhibited relatively high rates of nocturnal sap flow and
stomatal conductance compared with trees in fertilized plots (Fig. 3a, b). The
percent of nocturnal water flow and stomatal conductance compared to total daily
transpiration and stomatal conductance in Q. grandiflora in the non-fertilized plots
were higher than in those in N and P fertilized plots suggesting that long term
fertilization had decreased or completely removed the nutrient limitations of the
oligotophic savanna soils, and that nocturnal transpiration has no longer an adaptive
value.
214 S.J. Bucci et al.

(a) 0.6
C (34%)
0.5 N (21%)

Water use (mmol m-2 s-1)

P (27%)
0.4

0.3

0.2

0.1

(b) 0.0
C (41 %)
250 N (33 %)
P (36%)
gs (mmol m-2 s-1)

200

150

100

50

0
630 830 1130 1430 1730 2030 2330 230 530
Time (h)

Fig. 3 Mean daily courses of a water loss per unit of leaf surface area in terminal branches and
b stomatal conductance, during the dry season, for two trees of Qualea grandiflora in three
treatments: Control (C), Nitrogen (N) added, and Phosphorus (P) added. The gray area indicates
the dark period. Values within parentheses indicate the percent of nocturnal transpiration (a) and
stomatal conductance (b) compared to total daily transpiration and stomatal conductance,
respectively, calculated using the area under the curve. Information obtained from Scholz et al.
(2006)

Total foliar nitrogen content per plant across five savanna tree species was
negatively correlated with nocturnal water use calculated as the percent of total
daily water use (Fig. 4). Total foliar N increased in trees fertilized with N during
5 years, and their nocturnal water use was substantially lower compared to
non-fertilized trees. This functional relationship between N content and nocturnal
water use is also consistent with a putative role of nocturnal transpiration in
improving nutrient acquisition by savanna trees growing in nutrient poor soils.
Other studies have not found evidence of nocturnal transpiration promoting nutrient
uptake in plants (e.g. Howard and Donovan 2007, 2010; Matimati et al. 2014).
However, some of these studies were conducted with short lived species growing in
greenhouses, which constrain the analysis of the adaptive significance of their
results. There is apparently a genetic basis for nighttime transpiration. A study with
Physiological Significance of Hydraulic Segmentation … 215

25
R2 = 0.80

20

N (g crown-1)
15

B. salicifolius (F)
C. brasiliense (F)
10
O. hexasperma (F)
Q. parviflora (F)
S. macrocarpa (F)
B. salicifolius (C)
5 C. brasiliense (C)
O. hexasperma (C)
Q. parviflora (C)
S. macrocarpa (C)
0
0 5 10 15 20 25 30
Nocturnal water use (%)

Fig. 4 Total amount of nitrogen in foliage per tree (N) in relation to nocturnal water use (percent
of daily total water loss) for five savanna woody species. Each point represents the mean
value ± SE of 3–4 trees per species. The line is linear regression fitted to the data: (a) y = 27.7–
0.97x, p < 0.001. Filled symbols are plants in control plots and open symbols are plants in fertilized
plots. Information from Bucci et al. (2006), Scholz et al. (2006) and unpublished data

different accessions of Arabidopsis thaliana indicated that nighttime stomatal

conductance for different accessions of this species were well correlated with their
native habitat vapor pressure deficit (VPD), suggesting lower nighttime stomatal
conductance is favored by natural selection in drier habitats (Christman et al. 2009).
It is likely that in neotropical trees adapted to extremely low soil nutrient avail-
ability, natural selection may have favored maintenance of relatively high nocturnal
sap flow in their native habitats, and that upon removal of nutrient limitation by
long-term fertilization; they can acclimate to their new nutrient status by decreasing
the rate of nocturnal water loss. Furthermore, many neotropical savanna tree species
have deep root systems where abundant water is available, which allow plants to
maintain relatively constant daily minimum leaf water potential regardless of the
duration of the dry season
Recharge of internal water storage at night may occur if water loss by nocturnal
transpiration does not compete strongly with nocturnal recharge. In this case, the
larger fraction of nocturnal water uptake should be directed toward refilling of
internal storage compartments rather than used by transpiring leaves. In the
Brazilian savanna tree species Styrax ferrugineus, sap flow measured near the base
of the trunk continued during the night at rates up to 12 cm−3 h, but substantially
decreased or became negligible when trees were covered to minimize transpiration,
suggesting that a large part of Qn consisted of transpiration rather than recharge of
storage compartments (Fig. 5). Diurnal changes in stem diameter can be used as a
216 S.J. Bucci et al.

(a) 4

3
D (kPa)
2

0
(b)
50
Sap Flow (cm h )
3 -1

40

30

20

10

0
24 12 24 12 24 12 24 12 24 12 24 12 24 12 24 12
Time (h)

Fig. 5 Daily courses of air saturation deficit (D) and sap flow measured near leaves of one
individual of Styrax ferrugineus. The arrow indicates the moment when the plant was covered
with opaque plastic bags to restrict transpiration. Information from Bucci et al. (2004)

proxy for the dynamics of water movement during utilization and recharge of stem
water (Scholz et al. 2008a). When water is withdrawn from the stem storage, stem
diameter decreases, and when the stem storage is recharged, mainly at night, stem
diameter increases. Based on continuous measurements of stem diameter, stem
water storage tends to recharge faster when nocturnal transpiration is prevented
(Fig. 6), suggesting that nocturnal transpiration and recharge of water storage
compartments act as competing sinks for water taken up by roots. Another com-
peting sink for water taken up by deep roots is hydraulic redistribution (Scholz et al.
2008b), the movement of water from deeper and wetter soil layers to upper and
drier regions of the soil profile via plant roots (Scholz et al. 2002). During hydraulic
redistribution, water taken up by deep roots moves out of shallow roots and into the
upper soil layers instead of moving into the transpiration stream inside the tree. This
can potentially occur when nocturnal transpiration is relatively low and the dry soil
is the stronger sink (Scholz et al. 2008b).
Nocturnal water flow can also contribute to embolism repair. Embolism repair is
unlikely to occur as a consequence of night time water flow alone unless there is an
active mechanism in place for carbohydrate movement into empty conduits
(Johnson et al. 2012). For trees species that cannot avoid embolism formation (see
below), an alternative adaptive response includes the loss and recovery of hydraulic
Physiological Significance of Hydraulic Segmentation … 217

-70

-80 without nocturnal transpiration

Δ Stem diameter (μm)
1.8 μm h-1

-90

-100

with nocturnal transpiration

-0.04 μm h-1
-110
0 1 2 3 4 5 6
Time (h)

Fig. 6 Stem diameter changes from midnight to 6 h for exposed (with nocturnal transpiration,
open symbols) and covered (without nocturnal transpiration, filled symbols) Styrax ferrugineus tree
of Fig. 4. The mean rates of diameter increase or decrease are also shown. Information from Bucci
et al. (2004)

conductivity on a daily basis. This may be an especially common phenomenon in

tropical tree species with high wood density (negligible stem water reservoirs)
(Meinzer et al. 2008a). Apparently for embolism repair to occur, sugars must be
transported into the embolized conduits with water movement following along a
gradient in osmotic potential (Bucci et al. 2003; Johnson et al. 2012). This gradient
in osmotic potential is more likely to occur at night when tension driven gradients
inside the trunks and stems are relatively low.

Capacitance

Wood capacitance seems to be a key functional trait that strongly affects many
aspects of woody plant functioning. There is a strong correlation between sapwood
capacitance and measures of short-term water balance in large trees, including the
operating minimum stem and leaf water potentials and the safety margin (minimum
water potential—water potentials causing catastrophic run-away embolisms)
(Scholz et al. 2007; Oliva Carrasco et al. 2014). These correlations are likely
mediated by interactions between sapwood capacitance, percentage of daily water
use drawn from internal water storages and stomatal regulation of transpiration. The
transient buffering effect of high sapwood capacitance plays a particularly important
role in maintaining tree water balance in species with relatively low wood density
and high growth rates (e.g. Meinzer et al. 2003; Scholz et al. 2007).
218 S.J. Bucci et al.

300
(a) R2 = 0.70 Humid subtropical forest (b) R2 = 0.74
wood density vs Col 22: 0.3084
250 Tropical savanna
Water release (Kg m )

Tropical wet forest

-3

Subtropical cloud forest

200 Wet australian woodland
Dry australian woodland

150

100

50

0
0.3 0.4 0.5 0.6 0.7 0 200 400 600 800
Wood density Sapwood capacitance
-3 -1
(g cm-3 ) (kg m MPa )

Fig. 7 Water released across the stem water potential operating range as a function of a wood
density and b sapwood capacitance for 71 tropical and subtropical tree species. The line in a is the
exponential decay function fitted to the data (y = 2268*exp (−7.3x), p < 0.0001), and in b is the
linear regression fitted to the data (y = 12 + 0.26x, p < 0.0001). Information obtained from Meinzer
et al. (2003, 2004, 2008a, b), Scholz et al. (2007), Zhang et al. (2009), Richards et al. (2014), Oliva
Carrasco et al. (2014)

Species-specific stem water storage and stem capacitance are strongly correlated
with wood density in tropical and subtropical tree species, with lower sapwood
density resulting in larger capacitance (Bucci et al. 2004; Meinzer et al. 2003;
Scholz et al. 2007; Richards et al. 2014; Oliva Carrasco et al. 2014). Figure 7
depicts the relationship between the amounts of water released to the transpiration
stream by the stem storages, across the stem water potential operating range, as a
function of sapwood density. The amount of water released increases exponentially
with decreasing sapwood density (Fig. 7a) across several species from different
tropical and subtropical ecosystems. Similarly, the amount of water released
increased linearly, instead of exponentially, with increasing sapwood capacitance,
which is generally defined as the ratio of change in tissue water volume to changes
in its water potential, indicating the ability of the sapwood to provide water to the
transpiring leaves (Fig. 7b). These relationships reflect species-specific anatomic
differences of the sapwood, perhaps in the fraction lumen:wall of the fibers, which
is one of the determinants of wood density (Chave et al. 2009) and appears to have
an important influence on release of stored water (Richards et al. 2014).
Recently Wolfe and Kursar (2015) determined that water released from water
storages increases during flushing leaves in deciduous species from seasonally dry
tropical forests. Consistent with this finding, sapwood capacitance is significantly
higher in deciduous compared to evergreen tropical tree species (Fig. 8a), which
appears also to play a central role in their rapid growth patterns (Fig. 8b) facilitating
rapid canopy access of the forests as these species are less shade tolerant than
Physiological Significance of Hydraulic Segmentation … 219

Fig. 8 Sapwood capacitance (a) 400

(a) and cumulative growth
rate (b) of deciduous and ***
evergreen species. Values are
mean ±SE from 62 evergreen 300

Sapwood capacitance
and 9 deciduous species for

(Kg m MPa )
sapwood capacitance and 13

-1
evergreen and 5 deciduous
species for cumulative
200

-3
growth. Information obtained
from Meinzer et al. (2003),
Scholz et al. (2007), Zhang
et al. (2009), Richards et al.
(2014), Oliva Carrasco et al. 100
(2014)

(b) 0

**
0.04
Cumulative growth
(cm cm year )
-1

0.03
-1

0.02

0.01

0.00
Evergreen Deciduous

evergreen species. Higher growth rates in species with high capacitance could be
achieved by keeping the stomata open for longer periods of time. For several
tropical and subtropical species, the ratio of crown sap flow in the early afternoon
and the maximum crown sap flow attained during the day (E1300/Emax) increased
asymptotically with the amounts of stored water use determined by comparing the
daily sap flow patterns in the stem base and in the crown of the tree (Fig. 9). The
E1300/Emax ratio reflects the degree of stomatal control of transpirational losses with
higher ratios implying less stringent stomatal control at midday. The asymptotic
relationship suggests that in trees with larger amounts of water in the reservoirs
carbon assimilation can remain relatively high throughout the day.
Several studies have shown that species with high capacitance are more vul-
nerable to vessel cavitation (less negative Ψ50; Meinzer et al. 2008b; Sperry et al.
2008), presumably associated with low wood density. Consistent with this pattern,
220 S.J. Bucci et al.

1.1
R2 = 0.42
1.0

0.9

E 1300 h / Emax
0.8

0.7

0.6

0.5
Subtropical forest
0.4 Neotropical savanna
Tropical forest

0.3
0 10 20 30
Stored water use (%)

Fig. 9 The ratio of branch sap flow measured at 1300 h (E 1300 h) and maximum branch sap flow
(Emax) as a function of stored water use (%) derived from sap flow measured at the stem base and
in the crown of the tree for tree species from subtropical and tropical forests and tropical savannas.
The line is the exponential rise to maximum function fitted to the data (y = 1−exp(−0.13x),
p < 0.05). Information obtained from Goldstein et al. (1998), Meinzer et al. (2003, 2004), Scholz
et al. (2008a, b), Oliva Carrasco et al. (2014)

5
R 2 = 0.41

3
Ψmin - Ψ88 (MPa)

-1 Humid subtropical forest

Tropical savanna
-2
0 20 40 60 80 100 120 140
-3
Water release (kg m )

Fig. 10 Safety margin between minimum stem water potential (Ψmin) and stem water potential at
88 % loss of maximum stem hydraulic conductance (stem Ψ88) (Ψmin–stem Ψ88) as a function of
water release for tropical savanna and subtropical tree species. The line is the linear regression
fitted to the data (y = 0.61 + 0.063x < p = 0.01). Information obtained from Bucci et al. (2008),
Hao et al. (2008), Villagra et al. (2013) and Oliva Carrasco et al. (2014)
Physiological Significance of Hydraulic Segmentation … 221

the safety margin (Ψmin–Ψ88) of tropical and subtropical species increases linearly
with water released into the sapwood (at the operating minimum stem water
potential) (Fig. 10) suggesting a role for stem water storage in preventing embolism
formation by reducing fluctuations in water potential due to water deficits.
Although high wood density and high capacitance are at the end of a trait spectrum
representing a trade-off between avoiding mechanical damage (by biotic or abiotic
agents) and enhanced hydraulic efficiency, high capacity to release water to the
transpiration steam may be a low cost adaptation to avoid water deficits during peak
water use at midday and under seasonal or transient drought periods such as it
occurs in wet subtropical forests.

Conclusions

Most trees species have a relatively short life span of 80–200 years (but see Russo
and Kitajima this volume) in the wet tropics compared to more than a 1000 years in
some temperate zone trees. The results of the unique selective pressures in the
tropics have resulted in a large array of life history traits and in particular a large
array of functional traits related to the water relations of trees. It is not well known if
there are large species specific differences in physiological traits plasticity to
environmental changes. Fast-growing tropical tree species in different light regimes,
for example, are capable of plastic changes in hydraulic architecture, mainly
intrinsic hydraulic conductivity, and increased water-transport efficiency in
response to increases in light availability (Campanello et al. 2008). Slower growing
tree species under similar environments however do not exhibit plastic responses.
More information on the degree of plastic responses and the genetic variability
within species will help to better predict changes in species composition in tropical
ecosystems under different scenarios of global change.
The aspects of tree hydraulic architecture and water transport discussed in this
chapter are relevant for understanding potential tree responses to global climate
change and to the rapid land use changes, in particular deforestation. Multiple
selective pressures may result in species-specific physiological traits that can have
adaptive value under stable environmental regimes. However, under the current
rapid environmental change scenario, a particular trait may become non-adaptive.
The degree of hydraulic segmentation in tropical and subtropical trees varies
depending on their life history characteristics and habitat type. Strong segmentation,
whether it be hydraulic or vulnerability, may help to maintain an adequate water
balance but may also have indirect negative impacts on tree carbon balance during
severe droughts. Two mechanisms can trigger dieback in tree species with strong
vulnerability segmentation: leaf hydraulic failure and carbon starvation. More
research is necessary for assessing the generality of dieback mechanisms in tropical
trees experiencing prolonged drought. Nocturnal water loss and/or nocturnal sap
flow is widespread among many tropical and subtropical tree species. One of the
most likely functions of nocturnal sap flow in savanna or forest trees growing in
222 S.J. Bucci et al.

nutrient poor soils appears to be enhanced nutrient acquisition. Nocturnal water

flow can also contribute to embolism repair. High capacitance appears to play a
central role in the rapid growth of tropical deciduous tree species facilitating rapid
canopy access by keeping the stomata open for longer periods of time, and thus
facilitating carbon assimilation.

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Maintenance of Root Function in Tropical
Woody Species During Droughts:
Hydraulic Redistribution, Refilling
of Embolized Vessels, and Facilitation
Between Plants

F.G. Scholz, S.J. Bucci, F.C. Meinzer and G. Goldstein

Abstract Most woody dominated tropical ecosystems are subjected to drought

periods of different lengths, from few days or weeks in wet forests to several
months in drought deciduous forests and savanna ecosystems. The roots during
these low soil water availability periods may experience hydraulic and metabolic
dysfunctions resulting not only in a substantial decrease in root growth rates, but
also in reduced water and nutrient uptake activity. We discuss three groups of
processes: (1) hydraulic redistribution, (2) refilling of embolized vessels, and
(3) ecological facilitation, which can contribute together or in isolation to contin-
uous root activities despite low soil water availability. Furthermore they can help
avoid physiological uncoupling between above and belowground plant parts and
thus help to preserve the integration of the root, stem and leaf hydraulic continuum
within trees. The two mechanisms for refilling embolized vessels that help repair
the functionality of the water transport system discussed are the transient pressure
imbalance between the xylem and surrounding tissues, and positive root pressures.

F.G. Scholz (&)
S.J. Bucci

Grupo de Estudios Biofísicos y Ecofisiológicos, Facultad de Ciencias Naturales,
Universidad Nacional de la Patagonia San Juan Bosco, 9000 Comodoro Rivadavia,
Chubut, Argentina
e-mail: fgscholz@unpata.edu.ar; fgscholz@yahoo.com
F.G. Scholz
S.J. Bucci
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET),
Buenos Aires, Argentina
F.C. Meinzer
USDA Forest Service, Forestry Sciences Laboratory, 3200 SW Jefferson Way,
Corvallis, OR 97331, USA
G. Goldstein
Laboratorio de Ecología Funcional, Departamento de Ecología Genética y Evolución,
Instituto IEGEBA (CONICET-UBA), Facultad de Ciencias Exactas y naturales,
Universidad de Buenos Aires, Buenos Aires, Argentina
G. Goldstein
Department of Biology, University of Miami, Coral Gables, FL 33146, USA

© Springer International Publishing Switzerland 2016 227

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_10
228 F.G. Scholz et al.

Tree root systems not only obtain water from the soil to compensate for the water
lost through transpiration, but they can also move water from moist to dry layers
within the soil profile along gradients in soil water potential. This process known as
hydraulic lift or hydraulic redistribution provides water for reabsorption by roots of
the same plant or by neighboring individuals with active roots in the soil where
water is released through the process of ecological facilitation.

Keywords Belowground processes
Savanna
Soil
Water uptake
Water

transport

Introduction

Roots not only anchor plants to a substrate but are also the main pathway for water
and nutrient uptake. Knowledge of root distribution and hydraulic determinants of
uptake of available soil resources is critical for understanding the physiology of
trees. However, we know relatively little about roots compared to the aboveground
parts of plants, which reflects in part the inherent difficulties of studying roots in
their natural environment. In some ecosystems, the amount of biomass in tree roots
is higher than 50 % of the total tree biomass (Jackson et al. 1996; Castro and
Kauffman 1998). This is particularly true for some tropical savanna trees that are
exposed to 4–5 months of drought and which sustain a high rate of physiological
and metabolic activity during this period (Sarmiento et al. 1985; Goldstein et al.
1986, 2008; Franco 1998; Franco et al. 2005; Bucci et al. 2006). In addition to root
mass and surface area, access to adequate soil moisture during dry periods depends
on the presence of roots deep enough to tap more abundant water in deeper soil
layers (Scholz et al. 2008). Thus, the metabolic cost involved in maintaining ade-
quate root performance is high, but it is essential for maintaining homeostasis of
whole-tree carbon, nutrient and water economy.
Maximum average rooting depth for tropical deciduous forests (seasonally dry
forests) is 7.3 ± 2.8 m and for tropical evergreen forests is 15.0 ± 5.4 m (Canadell
et al. 1996). This range of rooting depth for tropical evergreen forest is larger than
usually assumed suggesting that trees in wet tropical forests with little or no sea-
sonality in precipitation allocate a substantial fraction of their total biomass to roots.
Length may not translate necessarily to biomass because a long root does not mean
that it is a thick one. However it is likely that due to allometric constraints longer
roots require more energy and biomass investment than shorter roots. It is possible
that the wide range of rooting depth reflects adaptations of some tree species to
climatic anomalies resulting in prolonged droughts. The relatively small amount of
carbon allocated to roots in seasonally dry forests (root:shoot ratio = 0.34; Jackson
et al. 1996) is associated with most tree species in this forest type being
drought-deciduous (Murphy and Lugo 1986). Losing leaves during the dry season
substantially reduces the rate of water loss and prevents water deficits. The main-
tenance of leaves during the dry period would be costly because it requires a large
Maintenance of Root Function in Tropical Woody Species … 229

allocation of carbon to underground biomass. Root systems in savannas are known

to be quite deep, permitting water to be tapped from deep soil layers where water
availability remains high during the dry season (Jackson et al. 1999; Scholz et al.
2008). Although many of the tree species in this type of ecosystem have access to
deep, stable water sources, root architecture differs across species with deciduous
and brevideciduous species having dimorphic root systems with active roots
exploring several soil layers, and evergreen species having monomorphic roots that
tap water from the same soil layer (Scholz et al. 2008). In this chapter we focus on
root hydraulic processes and their consequences for carbon allocation at the
whole-tree level, which contribute to continuous functioning of tropical trees
subjected to diurnal and/or seasonal water deficits.

Xylem Dysfunction and Refilling of Embolized

Conduits in Roots

Properties of the root system are often the primary limitation on water movement
along the soil-to-leaf continuum (Nobel and Cui 1992). Typically, 50 % or more of
the total resistance to water flow occurs below-ground despite the tendency for
xylem conduit diameters to be largest in roots (Passioura 1984). Transpirational
water loss generates tension, which is transmitted through continuous water col-
umns down to the vascular system in the roots, making this portion of the water
transport pathway susceptible to embolism. In roots, loss of functional xylem due to
embolisms reduces whole-plant hydraulic conductance and may partially prevent
water uptake (Linton and Nobel 1999), until the conduits are refilled with water
(Ewers et al. 1997; Johnson et al. 2012). Roots of trees are potentially more vul-
nerable to drought-induced embolism than stems (e.g. Sperry and Saliendra 1994;
Alder et al. 1996). The vessels tend to be larger in roots compared to stems and
leaves (Zimmermann and Potter 1982; Gartner 1995; Pate et al. 1995; Ewers et al.
1997), which may partially explain their greater vulnerability to embolism.
One of the hypothesized mechanisms for refilling embolized conduits in roots
that has been assessed experimentally involves transient pressure imbalance
between the xylem and surrounding tissues. According to this repair mechanism,
embolized conduits are refilled on a daily basis while the surrounding xylem is still
under tension (McCully et al. 1998; Melcher et al. 1998). Bucci and coauthors
(2003) hypothesized that the refilling process in leaf petioles is driven by an
increase in the amount of osmotically active sugars due to starch hydrolysis in cells
surrounding the vascular bundles. This increase in osmotically active solutes drives
water uptake by parenchyma cells resulting in a transient pressure imbalance
because water uptake is mechanically constrained by the petiole cortex. The
development of internal pressure was hypothesized to induce radial movement of
water into embolized vessels. Along the same line of reasoning, Schmitz and
coworkers (2012) showed that leaf-specific hydraulic conductivity of photosyn-
thetic stems in mangroves was lower in covered than in uncovered branches,
230 F.G. Scholz et al.

90

80 PLC morning
PLC afternoon

70

60

PLC (%) 50

40

30

20
-0.15 MPa -1.7 MPa
10
May July August
Month

Fig. 1 Mean diurnal changes in percentage loss of root conductivity (PLC) in four savanna woody
species (Blepharocalyx salicifolius, Byrsonima crassa, Kielmeyera coriaceae and Qualea
parviflora). Closed and open symbols indicate morning predawn and midday measurements
respectively. Values above the x-axis correspond to the maximum (May) and the minimum
(August) soil water potentials at the depth where roots were sampled. Data from Domec et al. (2006)

implicating stem photosynthesis in the maintenance of hydraulic function. Given

the proximity of the sites of exogenous CO2 uptake to the xylem vessels in the
stems, the results of this manipulative experiment suggest that xylary chloroplasts
may play a role in light-dependent repair of embolized xylem vessels.
There is little information on the prevalence of repair of embolized root xylem
conduits in tropical woody species. To our knowledge, daily formation and reversal
of root embolism has only been documented in four Brazilian savanna tree species
(Domec et al. 2006) and may be a more general phenomenon in roots of many
tropical tree species. These diurnal changes in root hydraulic conductivity are
consistent with the diurnal changes in hydraulic conductivity observed in stems and
petioles of temperate trees (Salleo et al. 1996; Zwieniecki and Holbrook 1998).
During the dry season, roots of Brazilian savanna species lose more than 30 % of
their hydraulic conductivity from morning to afternoon (Fig. 1). The results of field
manipulations in roots of the savanna species Blepharocalyx salicifolius were
consistent with the operation of a transient pressure imbalance mechanism proposed
for petioles of savanna species (Bucci et al. 2003), in which the diurnal refilling of
embolized vessels was prevented by incisions in the cortex (Fig. 2). Consequently,
the percent loss of hydraulic conductivity (PLC) in roots with incisions did not
decrease overnight and was significantly higher than PLC observed the previous
morning prior to the experimental treatment (Fig. 2). In contrast, hydraulic function
of control roots was restored overnight. Moreover, Domec et al. (2006) observed a
common relationship between maximum daily stomatal conductance and afternoon
root conductivity over the course of the dry season across the four savanna woody
species studied. Maximum stomatal conductance declined linearly with increasing
Maintenance of Root Function in Tropical Woody Species … 231

70
Control
Longitudinal incisions
60

50
PLC (%)

40

30

20
Morning Afternnoon Next morning
Month

Fig. 2 Diurnal changes in percentage loss of root conductivity (PLC) for control roots (closed
symbols) and for roots with longitudinal phloem incisions (open symbols) in Blepharocalyx
salicifolius during the dry season in a neotropical savanna. Modified from Domec et al. (2006)

afternoon loss of root conductivity, suggesting that daily cycles of embolism and
refilling in roots may be an inherent component of a hydraulic signaling mechanism
that coordinates stomatal behavior and transpiration with fluctuations in liquid
water transport capacity.
Another hypothesized mechanism for refilling embolized conduits in roots,
which has also been assessed experimentally, is root pressure. This mechanism of
embolism reversal appears to be common in bamboos. A survey of root pressure in
53 Asian species of tropical and subtropical bamboo (Wang et al. 2011a) revealed
that all possessed root pressure and in some species root pressure was high enough
to cause guttation of liquid from leaves overnight. Xylem exudates and guttation
fluid have an osmotic pressure greater than root pressure, which can be explained
by the low reflection coefficient of the root endodermis to solutes influx (Wang
et al. 2011a). Root pressure is caused by active extrusion of mineral nutrient ions
into the root xylem, which accumulate and lower the xylem water potential when
transpiration is very low, commonly at night, which drives osmotic uptake of water
from the soil into the root xylem. Root pressure in bamboos thus generates a force,
which refills embolized vessels by pushing water up the stem to the highest leaves.
This is of crucial importance for bamboos because they do not have lateral
meristematic tissues and thus lack the ability to produce new xylem tissue laterally.
Results of a recent study of daily water use strategies of Sinarundinaria nitida, an
abundant subtropical bamboo species, showed that stem hydraulic conductivity did
not decrease during the day whereas the leaf relative water content, leaf hydraulic
and stomatal conductance exhibited a distinct decrease at midday (Yang et al.
2012). Diurnal down-regulation in K(leaf) and stomatal conductance slow down
potential water loss in stems protecting the stem hydraulic pathway from cavitation.
Since K(leaf) did not recover during late afternoon, refilling of bamboo leaf
232 F.G. Scholz et al.

embolisms probably fully depends on nocturnal root pressure. The embolism

refilling mechanism by root pressure could be helpful for the growth and persis-
tence of this giant monocot species (Yang et al. 2012).

Hydraulic Redistribution in Tropical Savanna

and Forest Trees

The root systems of trees not only obtain water from the soil to compensate for the
water lost through transpiration, but also can move water upward from moist to
drier layers within the soil profile along gradients in soil water potentials (Caldwell
et at. 1998). This process, which was initially termed “hydraulic lift”, is also
referred to as hydraulic redistribution because roots can also transport water
downward (e.g. Burgess et al. 1998, 2001) and laterally (e.g. Bauerle et al. 2008).
Reverse sap flow along roots (from the plant to the soil) is an important part of the
hydraulic redistribution process. Hydraulically redistributed water is available for
reabsorption by roots of the same plant or by neighboring plants of the same or
other species that have active roots in the soil layer where water is released. The
magnitude and consequences of hydraulic redistribution are governed by multiple
factors including water potential gradients between various points within the
soil-plant-system, the hydraulic resistances to water flow in the soil, and the spatial
distribution of the roots (Scholz et al. 2008). During the dry season, the upper soil
layers typically have lower water content and thus more negative water potential
compared to deeper soil layers. Hydraulic redistribution driven by differences in
water potential within the soil profile is observed in tropical ecosystems with
seasonal changes in precipitation such as savannas and at the edges of Amazonian
forests. Evergreen trees in the Cerrado of Brazil do not exhibit hydraulic lift
because they have only deep fine roots, however deciduous trees with both shallow
and deep fine roots (dymorphic root systems) can carry out hydraulic lift (Scholz
et al. 2008). Byrsonima crassa is a dominant deciduous savanna species that drops
and expands new leaves during the dry season. Typical of species that can carry out
hydraulic lift during the middle and end of the dry season, the shallow roots of this
species exhibit reverse flow mainly at night (negative values of sap flow in Fig. 3b,
c). At the beginning of the dry season, there are no differences in water potential
between deep and shallow soil layers and thus hydraulic redistribution does not
occur due to a lack of a driving force for passive water movement between roots in
different soil layers (Fig. 3a). However, near the end of the dry season, this species
is nearly leafless and thus the strength of the transpirational sink is relatively small,
allowing reverse sap flow to occur throughout the entire 24-h cycle (Fig. 3c).
Hydraulic redistribution can also be driven by changes in salinity within the soil
as observed in dwarf mangrove ecosystems along the Atlantic coastline (Hao et al.
2009). Tall Rhizophora mangle trees growing along the coastline of Biscayne
National Park in Florida, USA, are continuously flooded and drained by the advance
Maintenance of Root Function in Tropical Woody Species … 233

Beginning of the dry season Middle of the dry season End of the dry season

B. crassa 0.0 MPa (a) B. crassa 0.2 MPa (b) B. crassa 0.8 MPa (c)
20
Sap flow density

Root
15 Root
(g m-2 s-1)

Stem
10
5
0
-5
8 R. mangle 0.8 MPa (d) R. mangle 1.1 MPa (e) R. mangle 1.5 MPa (f)
Sap flow velocity

6
(cm h-1)

-2
24 4 8 12 16 20 24 4 8 12 16 20 24 4 8 12 16 20 24
Time (h)

Fig. 3 a–c Sap flow density of Byrsonima crassa trees in a savanna ecosystem of Central Brazil
on representative days at the beginning of the dry season, at the middle of the dry season and at the
end of dry season, and d–f sap flow velocity of dwarf Rhizophora mangle trees in the inland areas
of the Biscayne National Park, USA. Squares represent the main stem and circles and triangles
represent lateral roots. Negative values of sap flow indicate reverse sap flow when there are
differences in water potential at two soil depths. Values on each panel are (a–c) soil water potential
gradient between 30 and 100 cm depth, and (d–f) soil osmotic potential gradient between 10 and
100 cm depth. Modified from Scholz et al. (2008) and Hao et al. (2009)

and retreat of tides, whereas dwarf R. mangle trees in adjacent inland areas are only
flooded by sea water during occasional high tides. Surface soils in the inland zones
are inundated with seawater during the wet season and gradually dry out during the
dry season, while the source of deeper soil water is fresh water coming from small
rivers or canals. Particularly during the dry season, a large water potential gradient
develops between shallow and deep soil layers, which drives hydraulic redistribution
in dwarf R. mangle at the inland sites. At the end of the wet season (December), the
difference in the osmotic potential of the interstitial soil water (Ψo) between 10 and
100 cm depth is 0.8 MPa (Fig. 3d). During the dry season, the Ψo of the surface soil
becomes more negative due to evaporation but Ψo remains high in deeper soil layers
because of the continuous influx of underground fresh water. At the peak of the dry
season (May) the largest difference in Ψo (c.a. −1.5 MPa) is observed (Fig. 3f).
Reverse sap flow is consistently recorded in prop roots of dwarf R. mangle from the
beginning to the end of the dry season (Fig. 3e, f) and its magnitude increases as Ψo
increases. Reverse sap flow in dwarf trees was found on 93 % of the measurement
days. Most of the reverse sap flow in dwarf R. mangle occurs during the night.
Approximately half of the evergreen forests of the Amazon Basin are subjected
to a 2–3 month dry season with less than 0.5 mm d−1 of precipitation. Hydraulic
234 F.G. Scholz et al.

redistribution by some evergreen eastern Amazonian tree species helps to avoid

water deficits during the short dry season (Oliveira et al. 2005). Although hydraulic
redistribution increases transpiration and plant growth during normal dry seasons,
under extreme droughts during El Niño years, utilization of water sources by deep
roots can eventually reduce dry season transpiration and net primary productivity
during the end of the extended dry season. If soil water storage is not able to sustain
forest transpiration through a long dry season, hydraulic redistribution may enhance
moisture depletion early in the dry season thereby reducing water availability
during the latter portion of the dry period (Wang et al. 2011b). It may appear at a
first sight counterintuitive, but deeply rooted species having fine shallow and deep
roots may be at a disadvantage under a global change scenario with an extended dry
season because of an accelerated depletion of deep water sources. This implies that
hydraulic lift may favor survival of certain tree species at the expense of others,
depending on specific morphological and physiological traits. The shift of the wet
evergreen tropical forests to a different type of forest will depend on the combined
effects of prolonged drought and hydraulic redistribution. However, the nature of
the substrate should also be included in models predicting the future trajectory of
forest composition. At the periphery of the Amazonian forest many species are
drought deciduous not only because of prolonged drought, but also due to high soil
nutrient availability. Under similar climatic conditions, both evergreen forests and
drought deciduous forests can occur depending on soil type. Evergreen-dominated
forests can be found on nutrient poor soils while nutrient rich soils mostly contain
deciduous trees. Consequently, soil nutrient availability has the potential to greatly
improve analyses of plant processes above and beyond climate data (Maire et al.
2015).
Hydraulic redistribution requires seasonal changes in the amount of precipitation
and thus a change in the magnitude of the soil to root water potential gradients from
very small to large gradients from wet to dry seasons, respectively. Alternatively,
besides seasonal changes of precipitation, perpetually arid ecosystems can develop
a vertical soil water potential gradient if there is a shallow water table, with a
capillary fringe above the water table, such as in Southern Arizona and California
along the Colorado River floodplain. Neotropical savannas are characterized by 4-
to 5-month dry seasons. Reverse sap flow from the roots to the soil increases as the
difference in water potential between roots and soil rises at the beginning of the dry
season. The percent loss of hydraulic conductivity in shallow lateral roots from wet
to dry season is species-specific and depends on rates of reverse sap flow (Fig. 4).
Species with lower rates of reverse sap flow exhibit larger hydraulic conductivity
drop during the peak of the dry season. This implies that for each species the
functionality of the roots growing in the upper dry soil layers during the dry season
is a function of the amounts of water discharge around the rhizosphere by hydraulic
redistribution. These results are consistent with the initial suggestion that a
reduction of soil drying rates through hydraulic redistribution would extend fine
root survival and growth (Caldwell et al. 1998). Bauerle et al. (2008) tested this
Maintenance of Root Function in Tropical Woody Species … 235

(a) 90
Wet
R2 = 0.93

(*10 m s MPa )
-1
Dry
80 2

-1
Lp
1

-5
70

(wet to dry season)

Percent loss Lp
0
60 Bc Bs Kc Qp

50

40

30

(b) 20
R2 = 0.90
80

70
(wet to dry season)

60
Percent loss LR

50

40

30

20

10

0
0 50 100 150 200 250 300 350 400
Reverse sap flux density
-2 -1
(kg m day )

Fig. 4 a Percent loss of total root hydraulic conductance (LP) and b percent loss of radial
conductance (LR) from the wet to the dry season in relation to total daily reverse sap flux in lateral
roots of savanna woody species at the peak of the dry season. Values of reverse sap flux are means
(±SE) of three to six roots in different trees. Values of LP and LR are means of three to six different
roots measured during the wet seasons (January 2004) and the dry (August 2004) in different trees.
A linear regression was fitted to each relationship a y = 77 − 0.13x, P = 0.035; b y = 74.5 − 0.17x,
P = 0.05. Symbols are: ( ) Byrsonima crassa, ( ) Kielmeyera coriacea, ( ) Blepharocalyx
salicifolius and ( ) Qualea parviflora. The inset in panel a is Lp in m s−1 MPa−1 measured during
the wet (filled bars) and dry (open bars) for the same species. Modified from Bucci et al. (2008)
and Scholz et al. (2008)
236 F.G. Scholz et al.

1.2
R2 = 0.87
1.0

Normalized reverse sap flow

0.8

0.6

0.4

0.2

B. salicifolius
0.0 B. crassa
K. coriaceae

-0.2
0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6
Water potential gradient soil to root (MPa)

Fig. 5 Normalized total daily reverse sap flow in lateral roots of three savanna woody species in
relation to the water potential gradient between soil and roots for different days from the beginning
to the end of the dry season. Reverse sap flow was normalized respect to the maximum value
reached for a particular root during the dry season. Modified from Scholz et al. (2008)

hypothesis using two Vitis sp. cultivars. Nighttime illumination of plants irrigated
on only one side of the row strongly suppressed hydraulic redistribution. Root water
potentials were twice as negative in plants where hydraulic redistribution was
suppressed than in plants where hydraulic redistribution occurred. A simulation
model developed by Scholz et al. (2010) for neotropical savannas, and validated
with field data, predicted that without hydraulic redistribution, water potential in the
upper soil layers would drop to very low values during the dry season, resulting in
negative effects on tree functioning, dieback of herbaceous plants, and disruption of
the biogeochemical cycles leading to a substantial decrease in rates of soil organic
matter decomposition.
Near the end of the dry season, reverse sap flow in lateral roots of woody
savanna species tends to initially increase sharply but then remain nearly constant
as the root-to-soil water potential gradient increases even further (Fig. 5).
A seasonal decrease in the axial and radial hydraulic conductivity of lateral roots as
the soil dry out could (inset Fig. 5) constitute a compensatory mechanism to limit
losses of water to shallow soil layers via reverse sap flow. The term “rectification”
has been used to describe this process resulting from both physiological and
morphological changes in root characteristics (Nobel and Sanderson 1984). In
addition to rectification, the asymptotic relationship shown in Fig. 5 may be the
result of nocturnal transpiration and recharge of stem internal water storage, which
may compete for internal water resources during the dry season (Scholz et al. 2008).
Maintenance of Root Function in Tropical Woody Species … 237

Facilitation Between Hydraulic Redistributors

and Neighboring Trees

Hydraulically redistributed water may be available for uptake by neighboring

individuals with active roots in the layer to which water is distributed and represents
an example of ecological facilitation (Moreira et al. 2003; Ludwig et al. 2004;
Hawkins et al. 2009; Pang et al. 2012; Sardans and Peñuelas 2013). The effect that
species engaged in hydraulic redistribution have on their neighbors is still unclear.
There are reports of positive, neutral or even negative effects depending on
ecosystem type, plant life form or whether donor and receiver species shared
common ecto- and endomycorrhizal networks (Prieto et al. 2011). A water isotope
labeling experiment conducted with deuterium (2H, D) on tropical savanna trees
from central Brazil was used to answer the question of whether hydraulically lifted
water is utilized by plants neighboring labeled individuals (Moreira et al. 2003).
Uptake of hydraulically redistributed water by neighboring trees was confirmed by
stable isotopic measurements of deuterium (D) in their stem water. A solution
containing 75 % D2O was fed to intact tap roots and stem samples of D-labeled
plants were obtained during the next three consecutive days. All treated plants had
at least two neighbors with stem water showing deuterium abundance above
background, suggesting that roots of those trees were able to obtain water released
into the soil by reverse flow through roots of the treated trees (Fig. 6). However,
there may be other pathways for water transfer between neighboring trees such as
root grafting or mycorrhizal connections. The mycorrhizal pathway seems to be the
most efficient, as twice as much water was transported between donor and receiver
Ponderosa pine trees (Pinus ponderosa) directly via mycorrhizal connections
compared to a non mycorrhizal pathway (Warren et al. 2008). In this study, the rate
of water transport between large trees and seedlings was high (0.16–0.63 m d−1),
which may be an indication that large amounts of water could potentially be
transferred through mycorrhizal networks. Thus, neighbors associated with plants
engaged in hydraulic redistribution could benefit from the extra moisture through
increased survival rates, which could potentially increase their fitness as they may
establish in the community and live long enough to grow and reproduce in sub-
sequent seasons (Schöb 2014).
Belowground competition between East African Acacia trees and grasses may
overwhelm the facilitative effects of hydraulic lift. Prevention of tree-grass inter-
actions through root trenching led to increased soil water content, indicating that
trees took up more water from the upper soil layer than they released through
hydraulic lift (Ludwig et al. 2004). Grasses used hydraulically lifted water provided
by trees, or alternatively they were able to tap deep soil water directly by growing
deep roots when competition with trees occurred. Competition for water resources
may therefore modulate the facilitation effect of hydraulic lift on neighboring
species. Field manipulation experiments, such as those done by Ludwig et al.
(2004) are needed to disentangle facilitation versus competition effects.
238 F.G. Scholz et al.

Fig. 6 Log differences between δD of stem water from plants neighboring treated plants fed with
deuterated water and those of control plants in a Brazilian Neotropical savanna. Three individuals
of two Cerrado tree species were used: Byrsonima crassa (BY) and Blepharocalyx salicifolius
(BL): Background abundance of D in stem samples was collected in individuals of the same
species more than 20 m away from the labeled individuals. The delta (δ) notation is used to
quantify stable isotope as relative ratios. Actual δD values equivalent to those reported on the log
scale are shown on the right axis. Values shown outside the grey area are significantly different
from control values at P < 0.05. From Moreira et al. (2003)

Conclusions

Most woody dominated tropical ecosystems are subjected to drought periods of

different lengths, from few days or weeks to several months. Roots during these low
soil water availability periods may experience hydraulic and metabolic dysfunctions
Maintenance of Root Function in Tropical Woody Species … 239

resulting not only in a substantial decrease in root growth rates, but also in reduced
water and nutrient uptake activity. Maintenance of root functioning is thus key for
the overall tree growth and reproductive performance. Roots constitute one of the
plant segments that are most vulnerable to drought-induced embolism. The vessels
tend to be larger in roots compared to stems and leaves, which may partially explain
their greater vulnerability to embolism. We discussed two of the hypothesized
mechanisms for refilling embolized conduits in roots that have been assessed
experimentally: transient pressure imbalance between the xylem and surrounding
tissues, and positive root pressures. The root systems of trees not only obtain water
from the soil to compensate for the water lost through transpiration, but also can
move water upward from moist to drier layers within the soil profile along gradients
in soil water potentials. This process known as hydraulic lift or hydraulic redis-
tribution can also transport water downward or laterally. Hydraulically redistributed
water is available for reabsorption by roots of the same plant or by neighboring
plants of the same or other species that have active roots in the soil layer where
water is released. The effect that species engaged in hydraulic redistribution have on
their neighbors apparently depends on ecosystem type, plant life form, whether
donor and receiver species share common ecto- and endomycorrhizal networks, and
by the intensity of belowground competition which may overwhelm the facilitative
effects of hydraulic lift.

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Drought Survival Strategies of Tropical
Trees

Louis S. Santiago, Damien Bonal, Mark E. De Guzman

and Eleinis Ávila-Lovera

Abstract Climate change is predicted to increase the occurrence of extreme

droughts, which are associated with elevated mortality rates in tropical trees.
Drought-induced mortality is thought to occur by two main mechanisms: hydraulic
failure or carbon starvation. This chapter focuses on the strategies that plants use to
survive these two drought-induced mortality mechanisms and how these mechanisms
are distributed among the immense diversity of tropical tree species. The traits that
tropical trees may use to survive drought include (1) xylem that is resistant to
drought-induced cavitation, (2) high sapwood capacitance that protects xylem from
critically low water potentials, (3) drought deciduousness, (4) photosynthetic stems
that have the potential to assimilate carbon at greater water-use efficiency than leaves,
(5) deep roots, (6) regulation of gas exchange to reduce leaf water loss or to maintain
photosynthesis at low leaf water potential and (7) when all else fails, low cuticular
conductance from exposed tissues during extended drought. To date, most research
has focused on deciduousness, resistant xylem, soil water, gas exchange behavior and
sapwood capacitance, whereas little is known about the role of photosynthetic stems
or cuticular conductance during extreme extended drought, making these processes a
high priority for a complete understanding of tropical tree physiology during drought.

L.S. Santiago (&)
M.E. De Guzman
E. Ávila-Lovera

Department of Botany & Plant Sciences, University of California,
2150 Batchelor Hall, Riverside, CA 92521, USA
e-mail: santiago@ucr.edu
M.E. De Guzman
e-mail: mark.deguzman@email.ucr.edu
E. Ávila-Lovera
e-mail: eleinis.avilalovera@email.ucr.edu
L.S. Santiago
Smithsonian Tropical Research Institute, Apartado Postal 0843-03092 Balboa
Panama, Republic of Panama
D. Bonal
INRA, UMR EEF—Université de Lorraine/INRA, 54280 Champenoux, France
e-mail: bonal@nancy.inra.fr

© Springer International Publishing Switzerland 2016 243

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_11
244 L.S. Santiago et al.

Introduction

Drought-induced tree mortality has now been documented in forests worldwide

(Allen et al. 2010; Anderegg et al. 2012). With global change, pronounced shifts of
rainfall patterns, as well as increased frequency and severity of extreme droughts
are expected (Field 2014). Even in wet tropical forests, which are some of the
world’s most humid ecosystems, elevated mortality of seedlings and mature trees
associated with drought occurs (Condit et al. 1995; Slik 2004; Engelbrecht et al.
2005, 2006; Comita and Engelbrecht 2009; Phillips et al. 2010; Feeley et al. 2011).
Predicting how tropical forests will respond to increased drought depends on
understanding which species are most susceptible to mortality by drought and
distinguishing these from species that are likely to survive drought and contribute to
future tropical forest composition. This is a grand challenge for ecophysiologists
because tropical forests may contain more than 300 species per hectare, creating a
large amount of data needed to develop predictions of future drought survival and
mortality. Such predictions are critical for understanding how potential mortality of
tropical trees affect carbon cycling and subsequent feedbacks to the climate system
because tropical forests harbor the greatest biodiversity, productivity and terrestrial
carbon stocks of any biome and thus play a disproportionately large role in the
global climate system (Beer et al. 2010; Saatchi et al. 2011). In fact, the largest
uncertainties in modeling how tropical forest carbon pools might alter in response
to climate change are associated with plant physiological responses (Huntingford
et al. 2013).
Much of the study of woody plant susceptibility to water deficit has focused on
the vulnerability of xylem to drought-induced cavitation (Choat et al. 2012; Craine
et al. 2013). Indeed xylem cavitation is a critical step in drought-induced mortality.
However, plants also posses a diversity of features that can buffer xylem from
reaching critical water potentials and prolong survival during drought conditions
(Pivovaroff et al. 2016). The traits that tropical trees use to survive drought include:
(1) xylem that is resistant to drought-induced cavitation, (2) high sapwood capac-
itance that protects xylem from critically low water potentials, (3) drought decid-
uousness, (4) photosynthetic stems that have the potential to assimilate carbon at
greater water-use efficiency than leaves, (5) deep roots, (6) regulation of gas
exchange to reduce leaf water loss or to maintain photosynthesis at low leaf water
potential and (7) when all else fails, low cuticular conductance from exposed tissues
during extended drought (Sperry 2000; Ackerly 2004; Meinzer et al. 2008; Choat
et al. 2012; Ávila et al. 2014). Similar to other ecological strategies, drought sur-
vival strategies thus consist of the presence or absence of drought survival traits
within species and are reflected by particular trait combinations that occur repeat-
edly in unrelated taxa under similar environments (Grime 1974; Chapin 1980;
Westoby et al. 2002). In this chapter, we examine what is known about these traits
in tropical tree species as a framework for understanding drought survival strategies
and predicting which tropical trees may be most susceptible to climate change-type
drought.
Drought Survival Strategies of Tropical Trees 245

During drought, lack of soil water is not the only problem faced by tropical trees.
High temperatures that accompany drought have consequences for photosynthesis,
and respiration, as well as stomatal regulation through the effects of temperature on
atmospheric vapor pressure deficit. Thus, the limitation on carbon assimilation
imposed by drought is also a critical component of drought-induced mortality
mechanisms in woody species. Two physiological mechanisms of woody plant
mortality involving water and carbon have been proposed and provide a useful
conceptual framework (McDowell et al. 2008). The first is the hydraulic failure
hypothesis, which suggests that drought reduces plant water potential such that the
xylem water column cavitates and cessation of water supply to leaves leads to plant
death under conditions of intense, short-term drought (McDowell et al. 2008). The
second is the carbon starvation hypothesis, which suggests that drought causes
stomatal closure and eventually leads to exhaustion of non-structural carbohydrate
reserves and thus leads to plant death under conditions of extended, low-intensity
droughts (McDowell et al. 2008; McDowell and Sevanto 2010). Carbohydrate
exhaustion may furthermore increase vulnerability to pathogens and herbivores,
which may be the ultimate cause of mortality (McDowell et al. 2008). Isohydric
species close stomata early during drought and maintain plant water status at the
expense of declining carbon intake, making them more likely to die of carbon
starvation. In contrast, anisohydric species maintain stomata open further into
drought and maintain carbon intake at the expense of declining plant water status,
making them more likely to die of hydraulic failure. Drought effects on water and
carbon supply also interact in complex ways when limited water supply reduces
carbon uptake, transport, and utilization, or when limited carbon supply reduces
xylem refilling (Salleo et al. 2004; McDowell 2011; McDowell et al. 2013).
Therefore, it is now recognized that both mechanisms are involved and do not act
separately (Hartmann et al. 2015). For example, both hydraulic architecture and
carbon relations have been shown to be important for mortality of tropical tree
seedlings under drought (Kursar et al. 2009; O’Brien et al. 2015).
Most of our understanding of tropical tree mortality during drought is based on
long-term forest census plots that are measured every 3–5 years (Condit et al. 1995;
Condit 1998; Phillips et al. 2010) and on large throughfall reduction experiments
(Nepstad et al. 2002; Fisher et al. 2007). These studies demonstrate that
light-wooded trees tend to suffer higher mortality than dense-wooded trees (Condit
et al. 1995, 1996; Phillips et al. 2010), consistent with the finding that low wood
density is correlated with high vulnerability to xylem cavitation (Hacke et al. 2001).
These studies also demonstrate that small seedlings and large-stature trees are
highly susceptible to mortality by drought (Condit et al. 1995, 1996; Engelbrecht
et al. 2006; Phillips et al. 2010). High seedling susceptibility is consistent with the
relatively small root systems, and thus limited access to water by seedlings. Large
trees may suffer elevated mortality during drought because of exposure to high
temperatures and radiation (Phillips et al. 2010), or due to altered water and carbon
relations in tall trees (Ryan and Yoder 1997; Burgess and Dawson 2007). Yet
within any size class, fine physiological differences and the presence of drought
survival traits should determine mortality during drought. Therefore, this chapter
246 L.S. Santiago et al.

addresses the seven drought survival traits described above in the context of their
occurrence in tropical trees and the particular aspects of physiological regulation
that stave off mortality. We also explore mechanisms of drought recovery as related
to drought survival traits. Although recovery is not strictly a drought survival trait,
there is evidence that the necessity to continue growing and the degree of resource
expenditure during drought largely determine the ability to recover in subsequent
years (Doughty et al. 2015).

Xylem Resistance to Drought-Induced Cavitation

Quantifying the tension under which xylem cavitates and loses the ability to
transport water is a principal approach to characterizing drought resistance in
woody plant species (Tyree and Sperry 1989; Choat et al. 2012). The process of
cavitation during declining water potential is caused by air entry into the xylem
lumen when negative xylem pressure exceeds the surface tension of water at the
border of gas-filled pit membranes (Sperry et al. 1988). Smaller pores in pit
membranes have the benefit of minimizing cavitation risk, but are associated with
smaller xylem vessels and carry the cost of reduced water transport. Vessel size is
also related to wood density, with dense-wooded species generally having smaller
vessels, greater resistance to drought-induced xylem cavitation and lower rates of
water transport (Hacke et al. 2001). Each species has a particular value of tension
under which air begins to enter into xylem vessels and restrict hydraulic conduc-
tivity and thus the ability to transport water to leaves (Choat et al. 2012). Among
species, the tension at which the xylem experiences 50 % loss of conductivity
(PLC) is usually used as a benchmark for comparison (P50; MPa). The P50
parameter is determined by plotting the PLC as a function of plant water potential.
Figure 1 illustrates the trajectory of declining hydraulic conductivity of terminal
stems of two species from Amazonian forest in Paracou, French Guiana, as stem
water potential declines during a dry down under laboratory conditions. The more
vulnerable species, Symphonia globulifera, has among the lowest wood density of
canopy tree species in the Paracou plot, whereas the more resistant species, Licania
alba, is one of the species with the highest wood density found in the Paracou plot
(Fig. 1). Thus the vulnerability curve space between these two end-member species
likely represents the entire range of xylem vulnerability for canopy trees at Paracou.
Data on vulnerability to xylem-induced cavitation on woody plant species from
around the globe have now been assembled into a single analysis (Choat et al. 2012).
This compendium shows that arid systems contain both vulnerable and resistant
species, and that humid systems, such as wet tropical forest, only contain species that
are relatively vulnerable to cavitation. Thus tropical forests represent one of the
world biomes that should be most vulnerable to drought-induced mortality during
extreme drought associated with climate change or El Niño years. However, analysis
of vulnerability curves and comparative P50 does not tell us when the xylem of a
particular species will reach the point of catastrophic hydraulic failure, but rather
Drought Survival Strategies of Tropical Trees 247

100

Loss of conductance (%)

80

60

40

20

0
-7 -6 -5 -4 -3 -2 -1 0
Water potential (MPa)

Fig. 1 Vulnerability curves of upper canopy branches of two tree species from Paracou, French
Guiana. The more resistant species, Licania alba, begins losing water transport capacity at a more
negative water potential than the more vulnerable species, Symphonia globulifera. The arrow
marks the water potential at 50 % loss of hydraulic conductivity (P50) and illustrates the
vulnerability curve space between these two end-member species representing the range of xylem
vulnerability for canopy trees at Paracou (Santiago et al. unpublished data)

what happens when xylem tissue arrives at such dangerous water potentials. For
example, xylem of riparian trees is often very vulnerable to drought-induced cavi-
tation, but it is not likely that these trees will reach critically low water potentials due
to high water availability (Pockman and Sperry 2000; Ackerly 2004). Therefore, the
use of vulnerability curve analysis to predict survival or mortality during drought is
most useful when combined with other drought survival traits.

Sapwood Capacitance

Sapwood capacitance, the stored water in stems that can temporarily supply the
water for transpiration and protect xylem from precipitous drops in water potential
(Bucci, this volume), has recently emerged as one of the most important hydraulic
factors for understanding the actual risk of cavitation (Meinzer et al. 2008; Barnard
et al. 2011). Indeed tropical tree species with high capacitance have been shown to
survive drought even without high cavitation resistance because they are buffered
by stored water and are at lower risk of reaching the xylem tensions that cause
hydraulic failure (Meinzer and Goldstein 1996; Meinzer et al. 2008, 2009; Sperry
et al. 2008). Capacitance is normally determined with a sapwood water release
curve plotted as cumulative water released as a function of sapwood water potential
(Fig. 2). Thus sapwood capacitance reflects the amount of water that can be
mobilized per unit water potential, and together with vulnerability curve analysis
provides keen insight to the functional limits of xylem performance under condi-
tions of declining water potential.
248 L.S. Santiago et al.

Fig. 2 Sapwood water release curve of one upper canopy branch of Hiraea reclinata from Parque
Metropolitano, Panama, showing relationship between sapwood water potential and water
released. Dotted lines indicate value of water potential and water released corresponding to turgor
loss point. Dashed line is a linear regression fit to the initial, nearly linear portion of the curve, the
slope of which is sapwood capacitance in units of kg m−3 MPa−1 (De Guzman, unpublished data)

Drought Deciduousness

Changes in deciduousness are known to occur along the great precipitation gradients
of the tropics (Schimper 1903; Givnish 2002; Santiago et al. 2004). Forests on the
dry side of precipitation gradients commonly have a higher proportion of dry-season
deciduous canopy species that tend to lose their leaves during the dry season when
low soil water availability may limit physiological activity. Dry-season deciduous-
ness is therefore considered to be a characteristic that reduces whole-plant transpi-
ration and respiration, providing an advantage over evergreen phenology in tropical
dry forest, savanna and caatinga vegetation during annual seasonal drought.
However, dry-season deciduousness may also impart an advantage during
supra-annual extreme droughts by providing an ability to maintain dormancy while
minimizing resource expenditure. The cost of this potential drought survival trait
would be suspended carbon income, which could make dry-season deciduous spe-
cies more vulnerable to mortality by carbon starvation.
Within the context of dry-season deciduousness, it is important to distinguish
seasonally deciduous species from normally evergreen species that begin to shed
leaves during extreme drought. Whereas many evergreen species will thin their
canopy throughout a normal dry season (Santiago and Mulkey 2005), with this
behavior continuing into extreme drought situations that extend beyond normal dry
seasons, some evergreen species do not posses the ability to shed leaves and can
experience mortality of entire limbs with crisp, brown leaves still attached to the
plant (Santiago, personal observation). Currently, there is little data to classify
species in terms of leaf shedding beyond the deciduous versus evergreen classifi-
cation scheme based on year-to-year phenology during normal annual dry seasons.
Drought Survival Strategies of Tropical Trees 249

However, the advantage of minimizing water loss and carbon costs of respiration
during drought is consistent with the dominance of dry-season deciduous species in
the most arid regions of the tropics.

Stem Photosynthesis

A close look at the bark of species in arid ecosystems quickly reveals the existence
of green stems (Fig. 3, Ávila-Lovera and Ezcurra, this volume). In many species
that remain leafless for most or part of the year, CO2 fixation by stems represents an
important contribution to whole plant photosynthesis (Pfanz 2008; Saveyn et al.
2010; Steppe et al. 2015). Stem photosynthesis can be classified into two types
based on physiological processes and anatomical characteristics (Ávila et al. 2014):
(1) Stem net photosynthesis (SNP), which includes net CO2 fixation by stems with
stomata in the epidermis and net cortical CO2 fixation in suberized stems, and
(2) Stem recycling photosynthesis (SRP), defined as assimilation of respired CO2 in
suberized stems. Under drought stress, when stomatal closure or leaf shedding (see
above) limit leaf photosynthetic carbon income, stem photosynthesis is expected to
become an increasingly large proportion of total carbon income because it is less
reduced than leaf photosynthesis (Nilsen 1995). It is also thought that stem pho-
tosynthesis can occur at greater water-use efficiency (WUE; carbon gain per unit
water loss) than leaf photosynthesis because of lower rates of water loss during
stem photosynthesis. To evaluate this hypothesis, we assembled the limited data

Fig. 3 Leaves and photosynthetic stems of Parkinsonia praecox from Margarita Island,
Venezuela. Photo by Wilmer Tezara
250 L.S. Santiago et al.

0.25

(µ mol CO2 [mmol H2O] )

-1
0.20

Water use efficiency

0.15

0.10

0.05

0.00
Leaves Stems

Fig. 4 Photosynthetic water use efficiency (mean ± standard error) of leaves and stems of eight
species taken from the literature (Osmond et al. 1987; Comstock and Ehleringer 1988;
Tinoco-Ojanguren 2008; Wittmann and Pfanz 2008). Comparison of means indicates no
statistically significant difference (t = 0.4177; p = 0.6825)

available for WUE of stem and leaf photosynthesis in the same species (Fig. 4). The
results from eight cases (Osmond et al. 1987; Comstock and Ehleringer 1988;
Tinoco-Ojanguren 2008; Wittmann and Pfanz 2008) indicate that whereas WUE
trended higher in stems than leaves, the difference was not statistically significant
(t = 0.4177; p = 0.6825). However, it is important to note that all of the available
data in this limited dataset comes from temperate species, raising the question of
what we will find as similar measurements are undertaken on tropical trees.

Soil Water Access

Belowground processes are notoriously difficult to measure, but access to soil water
as determined by rooting depth or rooting in moist microsites should be a major
determinant of how tropical trees will fare during extreme drought. Matching the
stable isotopic composition of hydrogen (2H, deuterium, D) and oxygen (18O) in
plant sap with water in the soil profile is useful for assessing water sources used by
plants (Allison 1982; Ehleringer and Dawson 1992). In fact, stable isotopic analysis
has revealed patterns that are difficult to observe with any other technique and the
use of labelling approaches provides further tools to estimate soil water extraction
depth (Stahl et al. 2013). For example, in seasonal tropical forest on Barro Colorado
Island in Panama, evergreen tree species take water from deeper soil layers than
deciduous species, suggesting that deep roots allow evergreen species to maintain
their leaves and continue physiological activity during the dry season (Jackson et al.
1995). In some instances, smaller trees have been shown to preferentially tap deeper
water sources relative to larger trees, suggesting that the presence of deep roots in
smaller trees could substantially reduce the risk of mortality during the dry season
Drought Survival Strategies of Tropical Trees 251

(Meinzer et al. 1999). Yet in other instances, smaller trees extract water from 0–2 m
depth and larger trees extract water mainly from deeper layers (Stahl et al. 2013). In
tropical dry forest in Yucatan, Mexico, evergreen trees were also shown to use
deeper water sources compared to deciduous trees, but this difference was only
observed in the earliest successional stage (>10 years), and disappeared in later
successional stages (Hasselquist et al. 2010). Furthermore, Hasselquist et al. (2010)
showed that among deciduous species, larger individuals tapped deeper water
sources, but there was no relationship between tree size and the depth of water
uptake for evergreen species. These results highlight the importance of rapidly
developing deep roots as a strategy to overcome seasonal water limitations for
evergreen tree species.
Although the presence of roots at a particular depth does not necessarily signify
water uptake from that depth, deeper root profiles should promote survival during
drought. In tropical dry forest of Yucatan, Mexico, live fine roots have been
observed near the water table at 9 m (Estrada-Medina et al. 2013). Furthermore, live
fine roots extend to 18 m depth in eastern Amazonian forest (Nepstad et al. 1994;
Trumbore et al. 1995). Therefore, different tropical ecosystems may have very
different sensitivity to drought based on absolute rooting depth of the system rel-
ative to the subterranean water table.

Regulation of Gas Exchange

With the onset of drought, plants are faced with the dilemma of either closing
stomata to minimize water loss at the expense of reduced carbon intake (isohydric
behavior), or opening stomata to maintain carbon intake at the expense of declining
water potential (anisohydric behavior) (McDowell et al. 2008). These two extremes
of stomatal behavior during drought are thought to lead to mortality by carbon
starvation when stomata close, or to hydraulic failure when stomata open. Yet, these
extreme examples may not capture the nuanced behavior of the diversity of tree
species in tropical forest. The available data suggest that there is a wide variability
in the degree of isohydry among tropical trees (Bonal and Guehl 2001). Modeling
exercises based on Bornean tropical forests indicate that under moist conditions,
anisohydric species would have higher productivity than isohydric species, but as
moisture availability decreases, the mortality of anisohydric plants drastically
increases whereas that of isohydric plants remains relatively constant and low
(Kumagai and Porporato 2012). Furthermore, based on a throughfall reduction
experiment in eastern Amazonia, the reduction in modeled sap flow during the dry
season was four times greater than what one would predict based purely on reduced
soil water potential, consistent with isohydric control of leaf water potential (Fisher
et al. 2006). Thus the degree of isohydry measured when water is available may
starkly differ from the degree of isohydry during drought. Additionally, the phe-
nomenon of midday depression, when tropical canopy trees reduce gas exchange
during the heat of midday (Franco and Lüttge 2002), is composed of stomatal and
252 L.S. Santiago et al.

non-stomatal limitations to photosynthesis (Pons and Welschen 2003), highlighting

the fact that the sequence of physiological regulation of gas exchange during
drought necessitates further study.

Cuticular Conductance

When all else fails, restricting water from leaves before they are senesced should be
an important determinant of the trajectory of a tropical tree during drought.
Diffusion of water across the cuticle involves water dissolving in the lipophilic
medium of the cuticle and desorption from the outer surface of the cuticle mem-
brane into the atmosphere (Kerstiens 1996). The principle diffusion barrier is
located in a narrow band near the outer surface of the cuticle and has been called the
limiting skin (Schreiber and Riederer 1996). Thus the overall thickness of the
cuticule is not correlated with water permeability. The term cuticular conductance is
used to describe loss of water vapor under conditions of maximum stomatal closure,
yet when there is uncertainty about the contribution of stomatal conductance to
overall water loss, the term ‘minimum conductance’ (gmin) is often used. Previous
compendiums of gmin clearly demonstrate that there is large variation in this
parameter among species (Kerstiens 1996; Schreiber and Riederer 1996). Figure 5
shows patterns of water loss from upper canopy sun leaves of 13 species of trees
from Amazonian forest in French Guiana (Santiago et al. unpublished data). The
slope of the linear portion of the curve is used to calculate cuticular conductance.
These data indicate that there is large variation among leaves from a single canopy
layer in tropical forest, demonstrating that a greater knowledge of variation in
cuticle conductance among tropical tree species should allow physiologists and
modelers to better simulate drought responses.

100
Water remaining (%)

90

80

70

60
0 50 100 150 200 250
Time (min)

Fig. 5 Evaporative water loss as a function of time for upper canopy excised leaves of 13
Amazonian tree species from Paracou, French Guiana. Measurements were conducted in low
(>20 μmol m−2 s−1 photon flux density) light to maximize stomatal closure
Drought Survival Strategies of Tropical Trees 253

Recovery Mechanisms

Upon alleviation of extended dry periods, the degree of resource expenditure on

growth, defenses, and reproduction during drought are likely to determine
post-drought survival in subsequent years. There is evidence that Amazonian trees
prioritize growth over maintenance and defense during and after drought because
any decrease in growth would give neighboring trees an advantage in terms of
resource acquisition and put that particular individual at a competitive disadvantage
through loss of resources (Franklin et al. 2012; Doughty et al. 2015). Although
there is little empirical data to predict which species expend more on maintenance
and defense during drought, which could improve survival following drought, it is
likely that species normally allocating more to maintenance and defense, late
successional species, are less likely to “overspend” during drought than early
successional species. Beyond carbon allocation, recovery of trees suffering partial
mortality of branches during drought may depend on the ability to re-sprout. This
process has not been explicitly linked to drought recovery in tropical forest, but
databases on sprouting ability exist (Paciorek et al. 2000), and may help develop
predictions of drought survival. Finally, reproductive output during or after drought
has the potential to contribute genes to future generations and could be particularly
important in monocarpic species (Kitajima and Augspurger 1989), or in species that
increase allocation to reproduction following drought due to the increased light
energy absorbed during cloudless drought periods (Wright and van Schaik 1994).

Future Directions

Overall, the framework of drought survival traits presented offers several pathways
forward for developing forecasts of species-specific drought sensitivity for tropical
trees. First, characterizing more tropical tree species in terms of the presence or
absence of drought survival traits will allow us to identify which particular trait
combinations occur under which environmental circumstances, rather than
approaching each species in a completely idiosyncratic manner. Second, where
physiologists can characterize drought survival traits in association with large-scale
studies, such as throughfall exclusion experiments, or watershed studies, progress
can be made linking physiological and ecosystem scales. Third, where experiments
are not available, variation of physiological processes as a function of water
availability can be obtained along natural environmental gradients, thus utilizing
spatial variation as a proxy for temporal climatic variation (Santiago et al. 2004).
Finally, many of the physiological measurements needed to characterize drought
survival strategies among species are exactly the types of data inputs needed for
physiological models that simulate when trees die based on carbon and water
relations (Sperry et al. 1998; Höltta et al. 2006).
254 L.S. Santiago et al.

Acknowledgments The authors thank Christopher Baraloto, Bettina Engelbrecht, Gregory

Goldsmith, Omar Lopez, Yadvinder Malhi, Patrick Meir, John Sperry, Klaus Winter and Joe
Wright for enlightening discussions on the topics presented; Leonor Álvarez-Cansino, Benoît
Burban, Jean-Yves Goret for work together in the field and lab, and the Botany & Plant Sciences
Department of the University of California, Smithsonian Tropical Research Institute, Labex CEBA
(Centre d’Etude de la Biodiversité Amazonienne; Investissement d’Avenir grant from the ANR,
ANR-10-LABX-0025), and the USDA National Institute of Food and Agriculture.

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 Part IV
Nutrient Limitation of Ecophysiological
Processes in Tropical Trees
Nutrient Availability in Tropical Rain
Forests: The Paradigm of Phosphorus
Limitation

James W. Dalling, Katherine Heineman, Omar R. Lopez,

S. Joseph Wright and Benjamin L. Turner

Abstract A long-standing paradigm in tropical ecology is that phosphorus

(P) availability limits the productivity of most lowland forests, with the largest pool
of plant-available P resident in biomass. Evidence that P limits components of
productivity is particularly strong for sites in Panama and the Amazon basin.
Analyses of forest communities in Panama also show that tree species distributions
are strongly affected by P availability at the regional scale, but that their local
distributions in a single site on Barro Colorado Island (BCI) are as frequently
correlated with base cations as with P. Traits associated with species sensitivity to P
availability require more detailed exploration, but appear to show little similarity
with those associated with N limitation in temperate forests. Recent research
indicates that a large fraction of P in tropical forests exists as organic and microbial

J.W. Dalling (&)

Department of Plant Biology, University of Illinois at Urbana-Champaign,
505 S. Goodwin Avenue, Urbana, IL 61801, USA
e-mail: dalling@illinois.edu
J.W. Dalling
O.R. Lopez
Smithsonian Tropical Research Institute, Apartado Postal,
0843-03092 Panama, Republic of Panama
e-mail: olopez@indicasat.org.pa
K. Heineman
Program in Ecology, Evolution and Conservation Biology,
University of Illinois at Urbana-Champaign, 505 S. Goodwin Avenue,
Urbana, IL 61801 USA
e-mail: kheineman@life.illinois.edu
O.R. Lopez
Instituto de Investigaciones Científicas y Servicios de Alta Tecnología,
Apartado Postal, 0843-01103 Ciudad de Saber, Panama, Republic of Panama
S.J. Wright
B.L. Turner
Smithsonian Tropical Research Institute, Apartado Postal,
0843-03092 Balboa, Panama, Republic of Panama
e-mail: WRIGHTJ@si.edu
B.L. Turner
e-mail: TurnerBL@si.edu

© Springer International Publishing Switzerland 2016 261

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_12
262 J.W. Dalling et al.

P in the soil; plant adaptations to access organic P, including the synthesis of

phosphatase enzymes, likely represent critical adaptations to low P environments.
Plants also cope with low P availability through increases in P use-efficiency
resulting from increased retention time of P in biomass and decreased tissue P
concentration. Although foliar P responds strongly to P addition, we show here that
foliar P and N:P are highly variable within communities, and at BCI correlate with
regional species distributional affinity for P. An improved understanding of P
limitation, and in particular the plasticity of responses to P availability, will be
critical to predicting community and ecosystem responses of tropical forests to
climate change.

Keywords Ecosystem nutrient budget

Fertilization experiments
Nutrient



uptake Physiological traits Soil nutrients

Introduction

Humid low elevation tropical forests support among the highest above-ground
biomass and net primary productivity of any ecosystem (Scurlock and Olson 2002;
Houghton 2005). Yet, many tropical forests that have been cleared for agriculture
fail to support crop yields for more than a few years without large fertilizer inputs
(Nye and Greenland 1960; Sanchez et al. 1983; Lal 1986). This apparent paradox
suggested that much of the nutrient reserve of tropical forests is stored in plant
tissue, resulting in critical nutrient limitation once biomass is removed. A synthesis
of datasets on nutrient concentrations in leaves and senescent tissue returning to the
ecosystem as litterfall highlighted phosphorus (P) as the nutrient that most clearly
distinguishes the stoichiometry of tropical from temperate forests, leading to the
paradigm that P availability constrains the productivity of most lowland tropical
forests (Vitousek 1984). Here we review the evidence for this paradigm, high-
lighting the insights gained over the past three decades on the distribution of P in
tropical ecosystems, its availability to plants, adaptations of plants for P acquisition
and use, and evidence that plant growth and forest diversity reflects not only P
supply, but also co-limitation by nitrogen (N) and base cations.

Nutrient Limitation in Tropical Forests

Many tropical soils are strongly weathered, reflecting warm, moist conditions acting
on stable land surfaces that were not directly affected by Quaternary glaciations
(Baillie 1996). These older, well-weathered ‘Oxisol’ (Soil Taxonomy system; Soil
Nutrient Availability in Tropical Rain Forests … 263

Survey Staff 1999) or ‘Ferralsol’ soils (IUSS Working Group WRB 2014) are
characterized by a moderately organically enriched surface horizon, and deep,
relatively uniform yellow-red subsoils, reflecting weathering of clay minerals into
ferric sesquioxides (Baillie 1996). Chemically, these soils are acidic, highly lea-
ched, with a low cation exchange capacity and high aluminum saturation. Beyond
this broad generalization, however, lies a diversity of soil physical properties
(notably influencing drainage patterns and water-holding capacity) and chemical
properties reflecting heterogeneous parent materials, substrate age, and topographic
effects on soil development. Nonetheless, a feature of many soil orders associated
with tropical forests is limited P availability and low total P, resulting from long
periods of leaching and strong adsorption or occlusion of P with iron and alu-
minium oxides (summarized in Table 10.12 in Baillie 1996).
The central importance of P limitation to the productivity of lowland forests
reached prominence after comparisons of litterfall in temperate and tropical forests
(Vitousek 1984). If P is a key limiting nutrient, then plants might be expected either
to function with less of it (reflected in lower tissue P concentrations), or to cycle it
more efficiently (reflected in part in higher resorption efficiency of P as tissues
senesce). Analysis of nutrient concentrations and nutrient ratios in leaf litter is
consistent with both mechanisms. Litterfall from lowland tropical forests, particu-
larly those on older, more weathered soils of the Amazon basin, had low P con-
centrations, whereas tissue N and Ca concentrations were mostly comparable to
temperate forests (Vitousek 1984). This study also highlighted differences in nu-
trient limitation between lowland and montane tropical forests. In montane forests,
P availability can be low, and foliar P generally declines with elevation (Tanner
et al. 1998; Benner et al. 2010). However, N limitation appears to be much more
important in the mountains than in the lowlands, probably due to temperature and
moisture effects on rates of mineralization (e.g. Grubb 1977; Vitousek et al. 1994;
reviewed in Benner et al. 2010).
Fertilization experiments have generally supported the view of P limitation in
lowland forests, and N or N and P limitation in montane forests (reviewed by Sayer
and Banin, this volume, Dalling et al. 2015). However, insights from fertilization
experiments are incomplete with regard to the scale and generality of nutrient
limitation. This is because factorial fertilization experiments are expensive to
establish and therefore restricted in the number of nutrient addition treatments that
can be included, and may take many years to yield clear treatment effects (Sullivan
et al. 2014). Fertilization experiments may therefore miss co-limitation scenarios
that could arise either because productivity in different plant size classes or tissue
types have different and distinct nutrient requirements (as seen in responses to
growth vs. litterfall responses to N, P and K in the Gigante fertilization experiment;
Wright et al. 2011), or because the limited scale and replication of fertilization
experiments precludes analyses of the individual species responses that contribute
to heterogeneous nutrient limitation (Alvarez-Clare et al. 2013; Dalling et al. 2015).
264 J.W. Dalling et al.

Mixed Evidence of Phosphorus Limitation at the Local Scale

If P availability alone governs forest growth and productivity then we would predict
that, at the community level, N:P would be relatively tightly constrained, with
ratios >16 (the Redfield ratio; Koerselman and Mueleman 1996) reflecting selection
for efficient P use. However, evidence from community-wide analyses of foliar N:P
do not support this prediction, with very wide variation in N:P in lowland forests,
but declining N:P with elevation (Fig. 1). In an analysis compiling published
datasets of foliar nutrients from neotropical sites, Townsend et al. (2007) found
limited evidence for environmental control over N:P. Instead, they found large
interspecific variation in N:P among species in lowland forests, suggesting coex-
isting tree species are likely to differ widely in their nutrient requirements (see also
Hättenschwiler et al. 2008; Hedin et al. 2009).
Similarly, analyses of species distributions within large forest dynamics plots
show correlations with a multitude of soil nutrients, with no clear preference for P
(John et al. 2007). For example, at Barro Colorado Island (BCI), Panama, 40 % of

40
Species Mean Foliar N:P

30

20

10

Lowland (BCI) Montane (Fortuna)

Fig. 1 The distribution of species mean foliar N:P ratios for 281 lowland tree species sampled on
Barro Colorado Island (BCI) in the Panama Canal and 91 montane tree species sampled at Fortuna
Forest Reserve in western Panama (800–1300 m a.s.l). The hinges of the boxplot represent the
interquartile range (IQR), and the whiskers extend to the largest and smallest values within
1.5 * IQR. Community mean N:P ratio was significantly higher on BCI (NP = 22.8) than Fortuna
(NP = 19.5; t = 5.65, df = 179.3, P < 0.001). However, variance did not differ significantly between
sites (levene test, F = 2.8; df = 1,370; P = 0.093). The line at N:P = 15 represents the Redfield
Ratio, which is the empirically derived threshold between N and P limitation in terrestrial
ecosystems
Nutrient Availability in Tropical Rain Forests … 265

the 258 most common tree species in the 50 ha forest dynamics plot show a
significant association in their local distribution patterns with at least one principal
component axis representing variation in soil chemical variables (John et al. 2007).
Analysis of individual soil variables shows a relatively even distribution in the
frequency of associations across soil variables (Fig. 2), with as many species
showing significant distributional associations with boron (B), calcium (Ca),
potassium (K), and zinc (Zn) as with P.
The lack of a clear pattern of association between tree species distributions and
soil P could reflect insufficient variability in P availability at the plot level, strong
spatial autocorrelation among soil nutrients, or strong similarity among species in P
requirements. Despite its location on a relatively flat andesite plateau, nutrient
availability within the BCI plot is quite variable. Soil P, extracted using Mehlich III
and analyzed using ICP, ranged from 0.45 to 6.8 mg/kg (10th–90th percentiles).
Although as a group base cations were strongly positively correlated at BCI
(defining the first principal component of soil chemical variation), P concentration
was only weakly correlated with base cations and instead loaded most strongly on a
second principal component axis. Although it might therefore be tempting to
conclude that demographic rates, and therefore distributions of species on BCI are
not primarily differentiated by P requirements, species distributions across the
Panama Canal area forests suggest otherwise.

Fig. 2 Frequency of association of 258 tree species with 12 soils variables measured at 300
locations in the 50 ha forest dynamics plot on Barro Colorado Island, Panama. Positive and
negative associations indicate that species occurred at sites with higher and lower than expected
concentrations (p < 0.05) of that variable based on assessment using the Poisson Cluster Method
(John et al. 2007)
266 J.W. Dalling et al.

Evidence for Phosphorus Limitation at Landscape

and Regional Scales

Analysis of tree communities in 72 forest plots distributed across the 66 km-wide

Isthmus of Panama surrounding BCI has revealed a much stronger imprint of soil P
on species distributions. Condit et al. (2013) examined whether the distribution of
550 tree species in this regional species pool showed distributional associations
with seven environmental variables measured at each plot, and with dry season
moisture availability estimated from a network of rain gauges. This analysis con-
firmed that dry season rainfall was the strongest environmental predictor of tree
distributions, with strong effects on 66 % of species, reflecting a steep gradient in
dry season intensity from the Caribbean to Pacific coasts of Panama. More of a
surprise, however, was that P availability affected nearly as many species (58 %),
revealing a previously unrecognized environmental filter acting on the composition
of these forests. Furthermore, species partitioned a gradient of P availability rela-
tively evenly, with 23 % of species showing affinity for high P and 35 % for low P
soils.
Phosphorus effects on tree community composition may be particularly strong in
central Panama because of the remarkable variation in P availability (resin
extractable P varies from <0.1 to 22.8 mg P kg−1; Condit et al. 2013); comparable
in magnitude to that of the entire lowland tropics (Condit et al. 2013 and references
therein). However, other soil nutrients, notably calcium, were associated with the
distribution of 35 % of tree species, raising the possibility that observed associa-
tions are at least in part driven by other correlated resources. To test whether species
associations reflect differences in growth response to P availability, we have begun
measuring seedling growth rates in a pot experiment manipulating P availability.
Seedlings of fifteen species with contrasting distributions across the Isthmus were
transplanted to a low P soil (0.13 mg kg−1 resin extractable P) and fertilized weekly
with a full nutrient solution either with or without added P. The magnitude of
species growth increase in the P addition treatment was significantly positively
correlated with the degree to which species distributions were skewed towards high
P soils (determined from the Condit et al. (2013) dataset).

Phosphorus Limitation: Links to Functional

and Physiological Traits

Species distributional affinity for P is also likely to be correlated with plant func-
tional traits that potentially impact ecosystem processes. In another pot experiment
exploring how Panamanian tree species respond to P availability, Vargas and Lopez
(unpublished data), found that Hura crepitans, a species with affinity for high P
soils, showed significantly higher leaf specific hydraulic conductance (KL) when
grown under high P conditions, suggesting the potential for P availability to
Nutrient Availability in Tropical Rain Forests … 267

influence ecosystem water balance. Higher KL under high P might be the result of
increased xylem vessel diameter or a by-product of shifts in allocation patterns, and
reduction in wood density (Goldstein et al. 2013).
More broadly, soil P availability is often correlated with foliar P concentration
(Vitousek and Sandford 1983), with effects on decomposition rates and therefore
nutrient cycling (reviewed in Cornwell et al. 2008). While foliar P concentration is
a plastic trait that responds to P fertilization (e.g., Santiago et al. 2012; Mayor et al.
2014), community wide foliar P values may also reflect the wider distribution
patterns of constituent species. We compared foliar N and P concentrations mea-
sured in shade leaves of three individuals of each of 137 species collected on BCI
(Wright and Turner, unpublished data) with species distributional affinity for P from
Condit et al. (2013). Foliar P was significantly positively correlated with distribu-
tional affinity for P (Fig. 3; r = 0.45, p < 0.001), and foliar N:P was significantly

Fig. 3 Relationship between

2.5

foliar N, P, and N:P of shade

Foilar P (mg/g)

leaves of 137 tree species

2.0

collected on Barro Colorado

Island, Panama, and the index
1.5

score of species affinity for P,

based on the distribution of
0.5 1.0

the same species across 72

sites across the Isthmus of
Panama varying in
resin-extractable P. Positive P -1 0 1 2
affinity index scores indicate
that species were associated
40

with sites with high

Foilar N (mg/g)

resin-extractable P
30
20
10

-1 0 1 2
40
Foilar N:P
30
20
10

-1 0 1 2
Species P Affinity
268 J.W. Dalling et al.

negatively correlated (r = –0.38, p < 0.001). Foliar N was not significantly corre-
lated with P affinity (r = 0.17). Interspecific variation in foliar nutrient concentration
may, in turn, be expected to correlate with juvenile and adult growth rates, however
no significant relationships were found between foliar N, P and N:P with sapling
(>1 cm DBH) or juvenile and adult (>10 cm DBH) growth rates of the same 137
species in the BCI 50 ha plot.
Elsewhere, an affinity for low P soils has been found to correlate with a high
P use-efficiency (PUE; a measure of biomass increment per unit P). In Queensland,
Australia, Gleason et al. (2009) found that tree species that were specialists on
P-poor schist-derived soils had twice the PUE of generalist species. High PUE in
turn was related to lower wood P concentrations and to higher retention time of P in
the canopy, but was unrelated to above-ground net primary productivity (sum of
radial growth and litter production). In contrast, along a steeper gradient of soil
P availability spanning the eastern slope of the Andes to the highly weathered and P
impoverished soils of the Guiana Shield, total soil P correlates positively with foliar
P concentration (Fyllas et al. 2009) and wood production, and inversely with wood
density (Mercado et al. 2011; Quesada et al. 2012).

Phosphorus Pools in Soil and Biomass

Much of our understanding of the chemistry of P limitation is based on temperate

chronosequences (Walker and Syers 1976). These studies generally show that given
sufficient time for pedogenesis, a decline in the total P pool size occurs, and is
accompanied by a decline in primary mineral P, and a corresponding increase in the
proportion of the total P occurring in occluded and organic forms. Similar shifts
between inorganic and organic P pools have been observed in the Hawaiian island
chronosequence (Crews et al. 1995), and are likely to be more generally reflected in
wet tropical forests (although no long-term chronosequence has been identified in
species-rich lowland tropical rain forest).
Nonetheless, a traditional view of P cycling in tropical forests holds that the
biological uptake of P is tightly coupled with the deposition of labile P via canopy
litterfall and relies very little on soil organic and inorganic P pools. According to
this hypothesis, nearly all the biologically available P in tropical forests should be
sequestered in plant biomass. This view is supported by the observation that while
intact tropical forests are highly productive, forested land cleared and converted to
pasture is often P-impoverished and frequently abandoned within a few years of
conversion (Serrao et al. 1996). Furthermore, Stark and Jordan (1978) provided
evidence for “direct-cycling” of P by demonstrating that only 0.1 % of
isotopically-labeled P and calcium applied directly soil surface was lost beyond the
root mat in a Venezuelan rainforest, indicating that there should be little chance that
organic P is leached from the ecosystem, or sequestered to iron or aluminum oxides
in the soil.
Nutrient Availability in Tropical Rain Forests … 269

Recent studies, however, provide increasing evidence that soil organic P pools,
which constitute about 25 % of total soil P in tropical forests (Turner and
Engelbrecht 2011), are more dynamic and chemically variable than previously
thought. For example, total soil organic P concentrations decline markedly (up to
25 %) during the dry season (Turner et al. 2015), while Vincent et al. (2010)
showed that organic P contained in DNA and phosphate monoesters declined in
response to experimental litter removal and increased in response to litter addition.
These studies indicate that there are more persistent pools of accessible organic P in
the soil beyond those directly re-assimilated from litter into plant biomass. In broad
terms, the pool of organic P available to plants can be considered to constitute three
groups: (1) recently senesced plant or microbial material, (2) P sequestered in live
microbial biomass and (3) “stable” organic P bound to iron or aluminum oxides.
Soil microbial biomass, characterized by low C:P ratios relative to plant biomass, is
an important P sink in forested ecosystems, and can represent a large fraction of the
total biomass-associated P (Turner et al. 2013). In a lowland tropical forest in
Panama, microbial P was estimated to account for approximately two thirds of the
total soil organic P (Turner et al. 2015). While microbes may compete with vascular
plants for P, microbial sequestration of P prevents the loss of ecosystem P to more
permanent geochemical sinks (Oberson et al. 1997), and facilitates the mineral-
ization of organic P to plant available phosphate (Richardson and Simpson 2011).
A recent detailed ecosystem P budget for sites representing a five-fold range in total
P storage in a Panamanian montane forest reveals that the amount of available P
contained in soil microbial and non microbial pools greatly exceeds the amount of P
sequestered in foliar and woody plant tissues at all sites (Heineman unpublished
data), contrary to the paradigm that labile P is sequestered primarily in plant
biomass.

Acquisition of Organic Phosphorus in Tropical Forests

Adaptations of plants to low P environments may reflect alterations both in P use

efficiency and in the ability to acquire P from less readily available sources. Turner
(2008) suggested that a gradient of biological availability of soil organic P exists,
which is determined by the investment cost to plants of producing an array of
enzymes required to catalyze the hydrolysis and release of phosphate. At one
extreme, plants can take up dissolved phosphate directly from the soil solution or
via mycorrhizas. Simple phosphate monoesters, such as glucose 6-phosphate
however require hydrolysis using phosphomonoesterase enzymes. Phosphate die-
sters, including phospholipids and nucleic acids, require both phosphomonoesterase
and phosphodiesterase enzymes to release phosphate. Finally, inositol hexak-
isphosphates require both solubilization from organic matter or clay minerals and
hydrolysis by phytase enzymes. Turner (2008) further suggested that differences in
the enzymatic capacity of plants confronted with an array of potential P sources
could represent an axis of resource partitioning among plant species.
270 J.W. Dalling et al.

Consistent with the hypothesis that species partition P sources, pools of organic
P differ in composition across a gradient in total soil P (Turner and Engelbrecht
2011) with a higher ratio of phosphomonoesters to phosphodiesters in sites with
higher total P. Nonetheless, to date, little evidence has emerged to suggest that
plants from P impoverished tropical forests differ in their capacity to produce
phosphatase enzymes when compared to those from more P-rich sites. In lower
montane forest at Fortuna, Panama, Steidinger et al. (2015) measured the produc-
tion of phosphomonoesterase and phosphodiesterase of excised roots of arbuscular
mycorrhizal (AM), ectomycorrhizal (EM) and non-mycorrhizal (NM) plant species.
They found only weak evidence for differences in enzymatic activity among these
groups, with no difference in activity between AM and EM taxa but significantly
higher phosphodiesterase activity in the NM taxon. A second experiment with the
same taxa compared growth rates of seedlings infected with mycorrhizas and grown
in acid-washed sand fertilized with inorganic phosphate, glucose phosphate, RNA
and phytate as the sole P source. Again, AM and EM species did not differ in their
response to organic sources of P, but the NM taxon, Roupala montana (Proteaceae)
was the only species capable of exploiting phytate as a P source. At Fortuna EM
and AM taxa, as well as Roupala occur in multiple sites that differ in P availability
(as determined by resin-extractable P and total P). Although the difference in P
source use between Roupala and other taxa suggests P source partitioning could
occur, its ecological significance in tropical forests requires further exploration,
including greater species replication of mycorrhizal groups.
Investment in phosphatase enzymes, however, may explain the abundance of N
fixing legumes, which can account for a large fraction of stems and basal area in
lowland tropical forests (Losos and Leigh 2004) and on occasions form mon-
odominant stands (Connell and Lowman 1989). The dominance of nitrogen fixers
in ecosystems where P is considered to limit forest productivity suggests that
increasing N availability may indirectly impact P acquisition. Houlton et al. (2008)
pointed out that phosphatase production is nitrogen-intensive (up to 15 % N by
mass), and that N2 fixing plants might therefore be able to increase allocation to
phosphatase relative to non-fixers. Evidence generally supports the Houlton
hypothesis, with higher phosphatase activity in soil beneath N2 fixing plants
(Houlton et al. 2008), higher root phosphatase activity (and AM infection) in N2
fixing lowland tropical trees (Nasto et al. 2014), and an increase in the phospho-
monoesterase activity of N2 fixing legumes relative non-fixers with declining soil P
along a chronosequence in Western Australia (Png et al. 2014).

Conclusions and Future Directions

The consequences of P limitation from the individual to the whole community-level

remains a relatively poorly studied aspect of tropical plant ecophysiology and forest
ecology. Just as N availability can limit the productivity of temperate plants under
elevated CO2 (e.g., Long et al. 2004; Norby et al. 2010; but see Drake et al. 2011),
Nutrient Availability in Tropical Rain Forests … 271

chronic P limitation has the potential to constrain the response of tropical forest
plants to rising CO2, particularly if reduced transpiration rates also reduce P uptake
(Cernusak et al. 2011). Despite this, experimental data to explore how CO2 and P
interact to influence the growth of tropical plants remains extremely scarce
(Cernusak et al. 2013). Likewise, an understanding of how tropical forest plants
have adapted to low P environments, either through increases in P-use efficiency or
phosphate-acquisition efficiency, can provide insights into how to manage P inputs
more efficiently in agricultural settings to maximize crop yields while minimizing P
exports from the system (Veneklaas et al. 2012).

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Tree Nutrient Status and Nutrient Cycling
in Tropical Forest—Lessons
from Fertilization Experiments

E.J. Sayer and L.F. Banin

Abstract Highly productive tropical forests often occur on nutrient-poor soils. The
apparent lack of a relationship between tree growth and site fertility has generated
decades of research into which nutrients, if any, limit tropical forest productivity.
This chapter looks at the lessons we have learned from several decades of fertil-
ization experiments, which investigate nutrient limitation by measuring changes in
growth and productivity in response to the addition of specific nutrients. The
enormous diversity of tropical forest ecosystems often confounds attempts to
measure a clear ecosystem response to fertilization because tree species’ nutrient
requirements differ according to life history strategy, adaptation to site fertility, and
the life stage of the individuals under study. Importantly, other limiting resources,
such as light and water, constrain individual responses to nutrient availability,
whereas species interactions such as competition, herbivory, and symbioses can
mask growth responses to nutrient amendments. Finally, fertilization changes the
timing and balance of nutrient inputs to the forest, whereas litter manipulation
studies demonstrate that the combined addition of many different nutrients and
organic carbon minimizes nutrient losses. Most fertilization studies have investi-
gated responses to nitrogen and phosphorus additions but there is still no general
consensus on nutrient limitation in tropical forests. Future experiments will need to
evaluate how the balance of multiple macro- and micronutrients affects tropical
forest growth and ecosystem dynamics.

Keywords Belowground biomass

Ecosystem productivity

Life history




strategy Nitrogen fixation Nutrient limitation Soil chronosequence Tree

growth

E.J. Sayer (&)

Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, England
e-mail: e.sayer@lancaster.ac.uk
L.F. Banin
Centre for Ecology and Hydrology, Bush Estate, Midlothian EH26 0QB, Scotland
e-mail: libanin@ceh.ac.uk

© Springer International Publishing Switzerland 2016 275

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_13
276 E.J. Sayer and L.F. Banin

Nutrient Limitation of Ecosystem Productivity

in Tropical Forests

Tropical forests are the most productive of all terrestrial ecosystems and yet large
areas of tropical forest occur on nutrient-poor soils (Vitousek and Sanford 1986;
Bruijnzeel 1991). Plant communities growing on highly nutrient-limited sites are
likely to be well-adapted to nutrient shortage and large proportions of the nutrients
available to plants are tied up in the living biomass and recycled with plant litter
(e.g. Herrera et al. 1978). The maintenance of such high productivity in tropical
forests on infertile soils can therefore be attributed to highly efficient cycling of
nutrients in organic matter (e.g. Jordan 1985; Cuevas and Medina 1988) and
nutrients from the decomposition of organic matter can make up a large proportion
of the nutrients required for plant growth (Bruijnzeel 1991).
The relative infertility of tropical soils and the highly efficient recycling of
nutrients in tropical forests have given rise to decades of research into which
nutrients, if any, limit productivity in tropical forests (Dalling et al., this volume).
The relationship between soil fertility and net primary productivity in tropical
forests is uncertain; comparative studies have variously demonstrated that above-
ground productivity can be positively (e.g. Quesada et al. 2012), negatively (Proctor
1983) or entirely unrelated to different measures of soil nutrient status (Jordan and
Herrera 1981; Proctor 1983). On the one hand, this may be partly due to the
challenges in quantifying plant-available nutrients in the soil and the ‘efficiency’ of
nutrient cycling in tropical forests (Vitousek 1984; Vitousek and Sanford 1986),
which decouples the simple relationship between soil fertility and plant nutrient
acquisition. On the other hand, differences in biomass allocation and species
composition can confound results in gradient studies; for example, tree growth was
positively related to soil nutrient concentrations in Borneo because of the high
density of a particular canopy emergent at the most fertile sites (Paoli et al. 2008).
Fertilization experiments are a useful tool to resolve some of these issues
because nutrient limitation can be inferred from a change in the rate of an
ecosystem process in response to the addition of a given nutrient (Tanner et al.
1998). Research on the nutrient regulation of plant productivity in the tropics has
focused largely on the macronutrients nitrogen (N) and phosphorus (P). An ade-
quate supply of N is essential for plant growth because it is a building block of
amino acids, enzymes and nucleic acids (Santiago and Goldstein, this volume,
Chap. 14). Phosphorus is also found in nucleic acids and it plays many vital roles in
plants, including energy metabolism. Very few tropical studies have investigated
the effects of fertilization with other plant macronutrients such as potassium (K),
calcium (Ca) or magnesium (Mg), but any nutrient can be said to be ‘limiting’ when
its availability constrains a biological or biochemical process (Tanner et al. 1998).
The concept of limiting nutrients was developed for individual plants or
monoculture crops, whereas community- and ecosystem-level responses are likely
to vary with species composition (Chapin et al. 1986). The high diversity of plants
in tropical forests in particular makes pinpointing nutrient limitation at the
Tree Nutrient Status and Nutrient Cycling in Tropical Forest … 277

ecosystem level especially challenging (Grubb 1989) because not all species are
necessarily limited by the same nutrient, two or more nutrients can be co-limiting
(Tanner et al. 1998), and apparent limitation by one nutrient may actually be
limitation by a different nutrient in disguise, for example when uptake of N is
limited by P-availability (Attiwill and Adams 1993). To complicate matters further,
simultaneous limitation by different types of resources, such as light, water, or
nutrients, is also often the rule (Bloom et al. 1985; Tanner et al. 1998).
During the search for the elusive ‘limiting nutrient’, fertilization experiments
have provided a wealth of valuable information about tropical forest nutrient
cycling, plant growth, and species interactions. In this chapter, we draw on the
results of more than three decades of fertilization studies conducted in tropical
forests to detect patterns in plant responses to altered nutrient supply and identify
considerations and constraints for interpreting experimental results. Most of the
evidence presented here concerns N- and P-dynamics, for which there is a large
body of literature on tropical forests but the same general considerations are likely
to apply to other nutrients.
Nutrients, soil development and the extraordinary case of Hawai’i—
Theoretically, terrestrial ecosystems will experience a shift from N- to P-limitation
over geological time. The primary source of P (and other base cations) in soils is the
weathering of bedrock, so their concentrations decline progressively with soil age
and development, mainly as a result of erosion and leaching (Walker and Syers
1976). In contrast, N accumulates in soil during the course of soil development,
reaching maximum levels in middle-aged soils (Lambers et al. 2008).
Many lowland tropical forest soils are old and highly weathered, particularly
those on ancient Precambrian shield geology, and hence they have low availability
of P, K and other cations (Grubb 1989; Banin et al. 2015). Conversely, tropical
montane forests have low availability and mineralization rates of N (Grubb 1977;
Vitousek 1984). Gradient studies also demonstrate that productivity is related to
foliar P concentrations in lowland forests (Vitousek 1984) and to foliar N in
montane forests (Tanner et al. 1998; Fisher et al. 2013). It is therefore widely
accepted that tropical montane forests are more likely to be N-limited whereas
lowland forests are more likely to be primarily limited by P (Vitousek and Sanford
1986; Tanner et al. 1998).
The Hawai’ian Long Substrate Age Gradient (LSAG) presents a unique oppor-
tunity to test these theories of nutrient availability during soil development in detail.
The gradient comprises a chronosequence of primary forest succession at six sites
ranging from 300 years to 4.1 million years of age; the relative availability of N is
lower at the youngest sites whereas the relative availability of P is lower at the oldest
sites (Crews et al. 1995). The sites along the gradient have comparable elevation,
rainfall, parent material and species composition (Harrington et al. 2001), and the
shift from N- to P-limitation along the gradient is reflected in foliar nutrient con-
centrations (Crews et al. 1995). Factorial +N and +P fertilization treatments at either
end of the gradient have demonstrated N-limitation of forest productivity in the
geologically youngest site and P-limitation at the oldest site (Vitousek and
Farrington 1997). Unfortunately, another exceptional feature of the Hawaiian LSAG
278 E.J. Sayer and L.F. Banin

is that the forest is dominated by a single canopy tree species, and is therefore not
necessarily representative of the highly diverse forests typical elsewhere in the
tropics. Despite this potential limitation for extrapolating results to highly diverse
tropical forests, dominance by only one species (in this case Metrosideros poly-
morpha) makes mechanistic studies possible (Cordell et al. 2001).
The evidence for N-limitation of productivity in tropical montane forests is
strong; fertilization with +N increased tree diameter growth and/or litter production
in Jamaica, Venezuela and Hawaii (reviewed by Tanner et al. 1998), Ecuador
(Homeier et al. 2012), Panama (Adamek et al. 2009) and Peru (Fisher et al. 2013).
In contrast, although the concept of P-limitation in lowland tropical forests is
widely accepted, the collective results of fertilizer studies are far from conclusive.
Aboveground productivity—Large-scale fertilization experiments in lowland
tropical forests have shown no effects of fertilization with +P alone on tree growth
in Borneo (Mirmanto et al. 1999) or Cameroon (Newbery et al. 2002) despite very
low soil P concentrations. After three years of fertilization in mature forest in Costa
Rica, stem growth of small trees doubled with +P additions and a higher percentage
of trees increased basal area in +P treatments than in control plots but there were no
other community-level responses to fertilization with +N or +P (Alvarez-Clare et al.
2013). Tree growth in young and old Mexican dry forests increased with +P, +N
and +NP fertilization; whereas +P and +NP treatments had a greater effect on trunk
growth, only fertilization with +NP enhanced litter production (Campo and
Vazquez-Yanes 2004). Interestingly, wood and leaf biomass of Eucalyptus trees in
a Brazilian plantation were greatly enhanced by fertilization with +K and, to a lesser
extent, sodium (+Na; Epron et al. 2011). Finally, a factorial fertilization experiment
with +N, +P and +K in Panama demonstrated that the addition of each of these
three macronutrients enhanced a different component of forest productivity: stem
growth of saplings was enhanced by the addition of +NK, whereas seedling height
growth increased with +K or +NP fertilization; litterfall increased with +P fertil-
ization, plant investment in fruits and flowers increased with +N, and root biomass
of trees and seedlings decreased in response to fertilization with +K or +NK
(Kaspari et al. 2008; Yavitt et al. 2011; Wright et al. 2011; Santiago et al. 2012).
Belowground responses—It is possible that the variable responses in above-
ground productivity are partly a result of changes in biomass allocation. In theory,
plants adapted to nutrient-poor soils should allocate more biomass to roots to
improve nutrient acquisition (Chapin 1980), whereas plants on fertile sites should
invest a greater proportion of their biomass aboveground. Accordingly, stand-level
root biomass should decrease when nutrient limitation is relieved by fertilization.
On the other hand, fine roots can proliferate into hotspots of nutrient availability in
nutrient-poor soils (St. John 1982), which creates microsites of high root biomass.
This provides an alternative approach to assess the effects of fertilization by mea-
suring root growth into microsites spiked with specific nutrients (Cuevas and
Medina 1988). Using this method, ingrowth cores containing limiting nutrients
represent nutrient hotspots and should therefore have higher root biomass than the
surrounding soil (Raich et al. 1994).
Tree Nutrient Status and Nutrient Cycling in Tropical Forest … 279

A meta-analysis of root biomass responses to fertilization in 45 tropical montane

and 52 lowland tropical forests showed that stand-level root production was
enhanced by +N fertilization in tropical montane forests and by +P fertilization in
lowland tropical forests, and the addition of +NP had a similar effect in both
systems (Yuan and Chen 2012). Nonetheless, decreased root biomass has been
observed in response to fertilization with +K and +NK in Panama (Wright et al.
2011), +P in Costa Rica (Gower 1987), +N in China (Zhu et al. 2013; Mo et al.
2008) and there were variable responses in root biomass and turnover in response to
+N or +P at different sites in Hawai’i (Ostertag 2001).
Similarly, ingrowth core studies demonstrate increased root growth into cores
supplemented with +N or +NP in montane forests (Stewart 2000; Graefe et al.
2010), whereas root proliferation into ingrowth cores has been observed in response
to +N, +P, +K, +NP, +PK and +Ca fertilization in various lowland tropical forests
(Cuevas and Medina 1988; Graefe et al. 2010). These results should be treated with
caution because ingrowth cores are often filled with plant growth media made from
expanded clays, which represent a source of cations such as K, Ca, or Mg (Raich
et al. 1994) and have absorption sites that can interact with added ions (Stewart
2000). In addition, root proliferation into ingrowth cores could represent a response
to greater instant availability of inorganic nutrients compared to the surrounding
soil, rather than a clear indicator of nutrient limitation.
These contrasting and sometimes contradictory results on the nutrient limitation
of above- and belowground productivity at the ecosystem level highlight a number
of considerations for interpreting fertilization experiments. Importantly, stand-level
responses to a sudden increase in nutrient availability are unlikely to be directly
comparable to biomass distribution along natural fertility gradients because adap-
tation of plants to initial soil fertility affects ecosystem responses to fertilization
(Ostertag 2001). Further, the life stage and life history strategies of individual plant
species determine biomass allocation and internal demand for nutrients to a large
extent. Consequently, several nutrient amendment experiments show highly vari-
able responses of different tree species (Alvarez-Clare et al. 2013; Villagra et al.
2013) and size classes of trees (Wright et al. 2011; Alvarez-Clare et al. 2013).
Hence, the interplay of many distinct site- and species characteristics influence the
responses of highly diverse tropical forests to nutrient amendments.

Life-History Strategies and Adaptation to Multiple Limiting

Resources

A large number of experiments have measured seedling responses to nutrient

amendments, which can be conducted on a small scale under controlled conditions.
Studies using multiple species have observed highly variable responses to nutrient
amendments; although the vast majority of species increased biomass in response to
nutrient addition, a much smaller proportion increased relative growth rates
(Lawrence 2003). In general, light-demanding species are more likely to increase
280 E.J. Sayer and L.F. Banin

growth and/or biomass in response to nutrient additions, whereas a larger number of

shade-tolerant species increase foliar N and P concentrations (Lawrence 2003; Cai
et al. 2008; Tripathi and Raghubanshi 2014). These patterns are fairly clear for pot
experiments, whereas field studies with transplanted or naturally occurring seed-
lings have shown fewer or smaller growth and biomass responses to fertilization
(Denslow et al. 1987; Turner et al. 1993). These differences among species and
types of experiments highlight the importance of considering other limiting
resources and their interactions with nutrient availability.
Light limitation in the understorey—Plants adapted to low-resource environ-
ments often have low potential for resource acquisition, invest heavily in defense
and storage, and grow slowly even when resources are increased (e.g. Huante et al.
1995). For seedlings growing in the understorey of tropical forests, light availability
can be more important than nutrient availability. Adaptation to low light levels
often includes greater allocation to leaves, smaller root biomass and low relative
growth rates (Cai et al. 2008). Slow-growing, shade-tolerant species have low
nutrient requirements when light is limiting (Burslem et al. 1996), so they may not
exhibit a strong response to nutrient amendments during the lifetime of an exper-
imental study (Dalling and Tanner 1995). In addition, seedlings grown in low-light
conditions invest primarily in increasing leaf area and leaf longevity while reducing
biomass allocation to roots; this can preclude a rapid or strong growth response to a
sudden increase in nutrient availability (Gunatilleke et al. 1997). Due consideration
of species-specific responses to light conditions is also important for designing
pot-based studies and interpreting their results: whereas some shade-tolerant
understorey species can exhibit a strong positive growth response to nutrient
amendments when light limitation is removed (Burslem et al. 1995), others may
become photo-inhibited under high light conditions (Fetcher et al. 1996).
Changes in growth or biomass in response to nutrient addition are often minimal
or completely absent when seedlings are grown under low-light conditions; instead
a strong increase of nutrient concentrations in foliage (Campo and Dirzo 2003;
Lawrence 2003) and other plant parts (Raaimakers and Lambers 1996) is observed.
Nutrient uptake in excess of requirement is regarded as ‘luxury consumption’ (e.g.
Ostertag 2010; Tripathi and Raghubanshi 2014) but these nutrient stores can enable
rapid growth once plants are no longer constrained by light availability, for example
when a new gap is created by a treefall (Raaimakers and Lambers 1996). Tropical
tree seedlings growing in the understorey are able to respond to very brief increases
in light levels such as sunflecks, so higher foliar concentrations of N, P and K in
particular could allow understorey plants to maximize photosynthesis even when
increased light availability is very sporadic (Pasquini and Santiago 2012). These
trade-offs between nutrient-use strategies and light availability can determine
competitive outcomes along gap-understorey gradients (Cai et al. 2008), because
nutrient storage under low light provides an advantage when the light limitation is
removed, whereas fast growth rates are beneficial for competition under high light
(Raaimakers and Lambers 1996).
Water stress—Many lowland tropical forests experience periods of low rainfall
or drought each year, and there are multiple lines of evidence for important
Tree Nutrient Status and Nutrient Cycling in Tropical Forest … 281

interactions between water and nutrient availability. The relative mobility of dif-
ferent nutrients and the activity of extracellular enzymes vary strongly with soil
water content, which for example affects N mineralization rates and the diffusion of
nutrients to root surfaces (Cavelier et al. 2000; Cernusak et al. 2010). Adaptation to
drought stress can also include greater biomass allocation belowground, which
could make plants more responsive to nutrient additions when water availability is
low or once drought conditions are alleviated. Hence, total root biomass and root
biomass allocation would only decrease in response to increased nutrient supply if
the water supply were adequate (Hall et al. 2003). Despite this, few experiments
report responses of tropical trees or seedlings to nutrient amendments under drought
stress (but see Hall et al. 2003; Burslem et al. 1996).
Nutrient addition can affect the drought resistance of trees by modifying their
hydraulic architecture. Rapid growth in response to fertilization was thought to
increase the risk of drought-induced embolism as a consequence of lower wood
density and larger total leaf surface area, which would result in larger transport
vessels and higher rates of transpiration (Goldstein et al. 2013). Surprisingly, an
experiment with six species of saplings showed the opposite: growth rates and
resistance to drought-induced embolism increased in response to fertilization
because changes in wood anatomy and wood density in response to increased leaf
surface area and transpiration appear to have mitigated the risk of cavitation
(Villagra et al. 2013). Shade-tolerant species in particular were able to increase
growth in response to +N and +P fertilization without increasing their vulnerability
to drought because they have lower specific leaf conductivity than light-demanding
species (Villagra et al. 2013).
Fertilization can reduce transpiration rates in tropical tree seedlings (Winter et al.
2001). An experiment with different species of tree and liana seedlings showed that
water use efficiency was positively related to foliar N and negatively related to
foliar P concentrations (Cernusak et al. 2010). It is possible that increased water-use
efficiency at higher foliar N concentrations decreases transpiration rates, and hence
weakens the pressure gradient that transports solutes to root surfaces by mass flow,
resulting in lower P uptake (Cernusak et al. 2010). These results are intriguing,
because greater water-use efficiency at higher foliar N concentrations may help to
explain why many species of tropical trees and seedlings exhibit luxury con-
sumption and storage of N.

Species Interactions

Tropical tree communities are often strongly affiliated with soil type; particular
species show strong local associations with certain soils because strong competition
excludes species growing in non-optimal habitats (e.g. Russo et al. 2005). Aside
from inter- and intraspecific competition for different resources, plant responses to
altered nutrient supply can modify or be modified by herbivory and symbioses with
mycorrhizal fungi or N-fixing bacteria.
282 E.J. Sayer and L.F. Banin

Mycorrhizal associations—The interplay between soil nutrient availability and

root symbioses is well established. In tropical forests, plants associated with ecto-
and arbuscular mycorrhizal fungi are highly competitive for P (Högberg 1986), so it
is particularly striking that mycorrhizal plants rarely respond to experimental
additions of P (Denslow et al. 1987; Newbery et al. 2002; Burslem et al. 1995),
although the results of some studies suggest that mycorrhizal species may be
limited by K, Ca or Mg (Burslem et al. 1995, 1996; Hall et al. 2003).
Although fertilization with inorganic +N and +P can have a negative (Treseder
and Vitousek 2001) or no effect on mycorrhizal colonization (Turner et al. 1993;
Brearley et al. 2007), mycorrhizas can improve tropical seedling growth by
accessing nutrients directly from decomposing litter (Hodge et al. 2001; Brearley
et al. 2003). Arbuscular mycorrhizal colonization and growth has been associated
with patches of nutrient-rich organic matter in tropical forests (St. John 1982); it is
hence conceivable that mycorrhizas are better adapted to access nutrients in organic
matter and nutrients added as inorganic fertilizers may not have the same effect
(Brearley et al. 2003).
Legumes and N-fixation—Di-nitrogen (N2) fixation by plants can constitute an
important input of N to terrestrial ecosystems when N-availability is low but it is
regarded as a ‘costly’ N-acquisition strategy to plants (Gutschick 1981). The high
prevalence of potentially N-fixing leguminous trees in tropical forests, where N is
not thought to be limiting, has therefore fueled scientific debate about the ecological
and evolutionary advantages of N-fixation (see review by Hedin et al. 2009).
N-fixation requires a sufficient supply of P and could therefore be constrained in
lowland tropical forests (Vitousek and Howarth 1991; Batterman et al. 2013).
Fertilization experiments have contributed evidence to support or refute various
hypotheses about how trade-offs between N and P acquisition or investment may
explain the abundance of N-fixing plants (henceforth: fixers) in lowland tropical
forests. One such theory is that N-fixation occurs in response to low availability of
soil N but is down-regulated when N is abundant (e.g. Hedin et al. 2009; Batterman
et al. 2013), and experiments show that non-legumes respond more strongly to +N
fertilization than legumes when available soil N is low (Tripathi and Raghubanshi
2014). Another theory postulates that N-fixers are able to invest additional N in the
production of extracellular phosphatases to acquire P (Houlton et al. 2008;
Baribault et al. 2012). However, experimental evidence suggests that plants cannot
overcome severe P-limitation by investing N in enzyme production alone
(Batterman et al. 2013) and even N-fixing mycorrhizal species can be poor com-
petitors for P (Högberg 1986).
Herbivory—Herbivory can substantially affect the outcome of fertilization
experiments. Leaves with higher nutrient concentrations and lower investment in
secondary plant compounds or structural carbon are thought to be more susceptible
to herbivore attack (Coley and Barone 1996). Consequently, there are trade-offs
between increasing growth or photosynthetic capacity in response to fertilization
and maintaining defenses against herbivory: firstly, photosynthetic capacity
increases with foliar N concentrations (Evans 1989) but higher foliar N also make
leaves more palatable to herbivores; secondly, rapid growth in response to
Tree Nutrient Status and Nutrient Cycling in Tropical Forest … 283

fertilization may preclude high investment in chemical or structural defenses (Coley

and Barone 1996).
Several experiments have noted that increased herbivory probably masked
growth responses to +N fertilization (Andersen et al. 2010), as well as +P and +K
(Santiago et al. 2012). Herbivore damage was particularly noticeable in pioneer
vegetation (Campo and Dirzo 2003) and fast-growing light-demanding species
(Villagra et al. 2013), which invest fewer resources in structural defenses, as well as
legumes (Campo and Dirzo 2003) and species associated with more fertile soils
(Andersen et al. 2010), which have higher leaf nutrient concentrations. Increased
risk of herbivory may also exert selective pressure against luxury consumption of N
(Ostertag 2010). This risk could be offset by greater investment in plant chemical
defenses but to our knowledge, only a single study has measured increases in
phenolic compounds with addition of specific nutrients and found no consistent
patterns across light-demanding and shade tolerant species (Denslow et al. 1987).

Life Stages

We would expect large growth responses to fertilization in young forests due to the
predominance of fast-growing pioneer vegetation and because tree growth during
the years prior to canopy closure (when light availability is high) is very dependent
on soil nutrient concentrations (Miller 1981). A study of 10-year and 60-year old
stands of secondary tropical dry forest showed that growth rates and litter pro-
duction were higher in the 10-year old forest compared to the 60-year old stand and
greater increases in tree growth and litterfall were also measured in the young forest
in response to fertilization (Campo and Vazquez-Yanes 2004).
Strong responses of secondary forest regrowth to nutrient amendments can also be
attributed to low soil nutrient availability after land-use for pasture or agricultural
crops (Davidson et al. 2004). Accordingly, the productivity of regenerating sec-
ondary tropical forests can increase substantially with fertilization: an 85 % increase
in annual net primary productivity was observed in plots treated with a complete
fertilizer during four years of forest reestablishment (Giardina et al. 2003) and the
rates of tree biomass accumulation in a six-year old forest almost doubled after only
three years of +N and +NP fertilization, although +P fertilization alone had little effect
(Davidson et al. 2004). Similar results were obtained in young dry forest in Mexico,
where trunk growth increased substantially after three years of +N or +P fertilization
and litterfall increased in response to +NP (Campo and Vazquez-Yanes 2004).
By contrast, the effects of nutrient amendments in mature forests are harder to
determine, as they are dominated by slow-growing, shade-tolerant species. Tree
size influences individual- and stand-level responses to nutrient amendments
because large trees are less likely to be light-limited than smaller trees in the
subcanopy (Wright et al. 2011). Species-specific responses of mature tropical trees
to nutrient amendments are also expected but this is difficult to test experimentally
because of the high diversity of tropical forest trees and the relatively low densities
284 E.J. Sayer and L.F. Banin

of individuals of the same species. In addition, disturbance (e.g. gap formation)

creates areas of forest at different stages of regeneration and as a result, nutrient
requirements are likely to be patchy throughout the forest. Seedling experiments are
thought to be useful to address this, because the regeneration phase is most likely to
influence adult abundance and distribution (Grubb 1977). However, seedlings are
subject to very different conditions and constraints than adult trees and hence their
responses may not be representative of later life stages.
A direct comparison of tree and seedling responses to fertilization—We are not
aware of any direct comparisons of the responses of seedlings and adult trees of the
same species to fertilization treatments, but there are legitimate biological reasons
to assume that species’ responses to nutrient additions will vary according to life
stage. We used published data on foliar nutrient concentrations in naturally
occurring seedlings and adult trees in a long-term experiment in Panama to examine
the responses of three common tropical tree species to fertilization with +N, +P, and
+NP (Santiago et al. 2012; Mayor et al. 2013, 2014). The three species included a
small subcanopy tree Heisteria concinna (Standl.), a medium-sized pioneer tree
Alseis blackiana (Hemsl.), and a large canopy tree Tetragastris panamensis (Engl.
Kuntze); all three species have shade-tolerant seedlings that can persist in the
understorey (Santiago et al. 2012).
First, we investigated the relationships between seedling and adult foliar nutri-
ents in control plots. We then calculated the proportional response to experimental
treatments as log response ratios (Eq. 1) to standardize effect size across species and
groups:
RR ¼ lnðRx=RcÞ ð1Þ

where Rx is the measured value of the response variable in a given treatment and Rc is
the corresponding control value (Santiago and Goldstein, this volume); a response
ratio of zero indicates no change in response to a treatment, whereas values greater
than or less than zero represent positive and negative responses, respectively (Hedges
et al. 1999). The effects of fertilization treatment, species and life stage were deter-
mined using linear mixed-effects models in R version 3.1.3. (nlme package; Pinheiro
et al. 2015; Development Core Team R 2014) with block as a random effect.
Significance of each term was determined by comparing nested models using likeli-
hood ratio tests and AICs to check for model improvement (Pinheiro and Bates 2000).
In unfertilized plots, foliar N and N:P ratios were higher in adults than in
seedlings (Fig. 1). Individuals of Alseis had the highest foliar concentrations of both
nutrients and Tetragastris had the lowest. Foliar P concentrations varied little
among species but were higher in seedlings than in adults, especially in individuals
of Tetragastris (Fig. 1).
Although there was no significant overall effect of fertilization with +N, +P or
+NP on foliar N concentrations, the response of Heisteria seedlings was more
positive and more variable than that of adult trees, whereas the other two species
showed no notable response. In contrast, foliar P significantly increased in +P and
+NP treatments (Fig. 2). Although the interaction terms were not significant in the
Tree Nutrient Status and Nutrient Cycling in Tropical Forest … 285

Fig. 1 Boxplots of foliar N

and P concentrations of adult
trees (dark shading) and
seedlings (light shading) of
three common tree species in
the control plots of a
fertilization experiment in
lowland tropical forest in
Panama, Central America;
species are Alseis blackiana,
Heisteria concinna and
Tetragastris Panamensis

Fig. 2 Boxplots of foliar P

concentrations of adult trees
(dark shading) and seedlings
(light shading) of three
common tree species in a
fertilization experiment in
lowland tropical forest in
Panama, Central America,
where +N, +P and +NP are
treatments fertilized with
nitrogen, phosphorus or both
nutrients, respectively;
species names are as given in
Fig. 1

models, the response to fertilization differed slightly among species and life stages:
foliar P varied more amongst seedlings than adult trees and individuals of Heisteria
displayed the strongest response to fertilization (Fig. 2), whereas foliar N:P ratios
tended to decrease in response to +P and +NP fertilization and the fertilization effect
was slightly lower in seedlings than in adult trees, especially in individuals of
Heisteria (Fig. 3).
286 E.J. Sayer and L.F. Banin

Fig. 3 Boxplots of foliar NP

concentrations of adult trees
(dark shading) and seedlings
(light shading) of three
common tree species in a
fertilization experiment in
lowland tropical forest in
Panama, Central America,
where +N, +P and +NP are
treatments fertilized with
nitrogen, phosphorus or both
nutrients, respectively;
species names are as given in
Fig. 1

We demonstrate here that the responses of plants to nutrient amendments also

vary with life stage, at least for these three common tropical tree species. Overall,
seedling responses to a given fertilization treatment were more variable, which
suggests stronger constraints on seedling nutrient uptake and storage, e.g. because
of light limitation (see Sect. Light limitation in the understorey), distinct internal
demands for nutrients, less developed root networks, or because seedlings are
outcompeted by adults (Tanner and Barberis 2007). The foliar nutrient concentra-
tions of adult trees used in our analysis were from canopy leaves, which were fully
exposed to sunlight (Mayor et al. 2014), whereas the seedlings experienced light
levels of only c. 1 % in the understorey (E.J. Sayer, unpublished data). This alone
could account for the large differences between adult trees and seedlings. However,
it is noteworthy that Heisteria displayed the greatest fertilization responses and the
largest differences between seedlings and adult trees, even though subcanopy trees
are often strongly light-limited. This suggests that distinct nutrient demands at
different life stages and by functionally different species may also play a role in
determining foliar nutrient concentrations and the balance of carbon and nutrients.

Litter Manipulation Experiments

Litter manipulation treatments involve the regular removal or addition of the litter
standing crop and fine litterfall (leaves, fruits, flowers and small branches) to disrupt
or enhance the natural forest nutrient cycle (Sayer 2006). Unlike fertilization
experiments, litter manipulation studies do not aim to identify limiting nutrient
Tree Nutrient Status and Nutrient Cycling in Tropical Forest … 287

elements but instead investigate the importance of nutrient cycling via organic
matter (Sayer et al. 2012) and are accordingly discussed separately here. It is
important to note that litter manipulation treatments affect several important soil
properties, such as soil water content, soil temperature, and habitat space for
decomposer organisms (reviewed in Sayer 2006). Furthermore, many of the pre-
viously described constraints and interactions affecting plant responses to nutrient
amendments will also apply to litter manipulation studies.
Although litter addition can also be regarded as a nutrient addition treatment,
two important features distinguish it from fertilization: (1) litter addition treatments
supply multiple nutrients in approximate stoichiometric balance, and (2) nutrients
are added in combination with organic carbon. This second point is important,
because the forest is adapted to cycling nutrients from organic matter and the slow
release of many nutrients from decomposing litter minimizes losses from the system
(Qualls et al. 1991; Sayer et al. 2012). Litter removal treatments have no parallel in
fertilization studies because they effectively disrupt the forests’ natural nutrient
cycle. This disruption allows us to identify different nutrient cycling strategies. For
instance, rapid decreases in the concentrations of N in soil and leaves in response to
litter removal could suggest that decomposing organic matter is the principal source
of N for plant growth (Sayer and Tanner 2010). On the other hand, it also indicates
an inefficient N-cycle, characterized by a lack of mechanisms to mitigate large
losses from the system, such as through retranslocation of nutrients before leaf
abscission.
Although there are now a number of litter manipulation experiments across the
tropics, most have focused on seedling establishment, soil biogeochemistry or
decomposition processes. The few experiments investigating tree responses or
ecosystem productivity have demonstrated rapid responses to litter addition treat-
ments, including increased stem growth of individual tree species (Villalobos-Vega
et al. 2011; see also Sect. The effects of litter manipulation on plant growth.),
increased litterfall (Wood et al. 2009; Sayer and Tanner 2010) and changes in foliar
nutrient concentrations or nutrient return in litterfall (Tutua et al. 2008; Wood et al.
2009; Sayer and Tanner 2010). Litter removal treatments have had little effect on
productivity, possibly because tropical forest adaptation to infertile soils includes
efficient nutrient retention mechanisms. Nonetheless, litter removal affected the
cycling of N and/or K in most experiments with at least four years of treatments
(Tutua et al. 2008; Vasconcelos et al. 2008; Sayer and Tanner 2010), demonstrating
the key role of organic matter in minimizing losses of the more mobile nutrient
elements.
The effects of litter manipulation on plant growth—Tropical tree seedling
responses to litter manipulation have mostly focused on germination, establishment
and survival in the field. Litter addition influences seedling establishment by
forming a physical barrier and providing a favorable habitat and microclimate for
pathogens and herbivores (Sayer 2006), so it is hard to evaluate the effect of
litter-derived nutrients on seedling growth in these experiments. Nevertheless, a
greenhouse experiment showed that litter addition enhanced seedling growth and
biomass via direct uptake of nutrients by mycorrhizal fungi (Brearley et al. 2003).
288 E.J. Sayer and L.F. Banin

Few litter manipulation studies to date are sufficiently long-term to assess the
effects of treatments on the growth of mature tropical trees (but see Villalobos-Vega
et al. 2011). There was no discernable effect of litter manipulation on stand-level
tree growth after 4 years of treatments in a lowland tropical forest in Panama (Sayer
and Tanner 2010), so we used additional data from the same experiment to explore
the individual growth responses of four common tree species to six years of litter
removal (L−) and litter addition (L+) treatments. The focal species were Heisteria
concinna (Standl.) and Tetragastris panamensis (Engl. Kuntze), as described in
Sect. The effects of litter manipulation on plant growth, and Simarouba amara
(Aubl.), a fast-growing tree associated with forest gaps, and Virola sebifera (Aubl.),
a shade-tolerant canopy tree. Experimental treatments began in 2003 and changes in
diameter at breast height (dbh) were recorded using dendrometers from 2004 to
2009; all stems had a dbh between 10 and 40 cm at the start of measurements. We
produced a linear mixed effects model with relative growth rate as the response
variable, treatment and species as fixed effects, and plot and year as random effects.
We used the same model simplification approach as described in Sect. 5.1. and the
model with the best fit included species, treatment and their interaction term.
Species responded very differently to the treatments. Growth rates of Simarouba
and Virola were highest in the L+ and lowest in the L− plots, and this was most
marked in later years (Fig. 4), which suggests that these species have increased
growth in response to the nutrients added with the litter. In contrast, the highest
growth rates of Tetragastris and Heisteria were observed in L− treatments and the
lowest in control plots (Fig. 4); these counterintuitive results could indicate that
these shade-tolerant species are better competitors for fluctuating resources under
disturbed conditions.
Our analyses are restricted to these four species because they were sufficiently
common in the study forest. Nonetheless, these findings demonstrate non-uniform
responses among species to litter and nutrient addition, which perhaps reflect the
complexities of life history traits and competitive interactions that occur in diverse,
mixed-aged natural forests.
Comparing litter manipulation and inorganic fertilization experiments—The
only formal comparison of litter manipulation and fertilization treatments in tropical
forest to date suggests that there are substantial differences in the way nutrients are
cycled, depending on whether they are added as inorganic fertilizers or in organic
material (Sayer et al. 2012). In particular, the dynamics of the most mobile
macronutrients N and K differed substantially between experiments at the same
study site, even though the fertilization and litter treatments added or removed
similar amounts of these nutrients each year. The L+ treatment resulted in much
greater availability of inorganic N in the soil and higher N concentrations in lit-
terfall compared to +N fertilization, whereas K concentrations in litterfall decreased
more in the L− treatments than they increased with +K fertilization (Sayer et al.
2012). Although the P added with litter in the L+ treatment was only c. 12 % of the
amount added in the +P-fertilization treatments, most of the P added as fertilizer
remained in the soil (c. 81 %; Yavitt et al. 2011), whereas increased litterfall in the
Tree Nutrient Status and Nutrient Cycling in Tropical Forest … 289

Fig. 4 Relative growth of three common tree species in a litter manipulation experiment in
lowland tropical forest in Panama, Central America, showing means and standard errors for n = 5
per treatment and species; square symbols denote controls, circles denote litter removal and
triangles denote litter addition; species are Heisteria concinna, Simarouba amara, Tetragastris
panamensis and Virola sebifera

L+ treatment accounted for c. 85 % of the P added with litter (Sayer and Tanner
2010; Sayer et al. 2012).
Changes in root biomass distribution were also revealing: whereas root biomass
in the uppermost soil horizons decreased in +K and +N fertilized plots (Wright et al.
2011; Yavitt et al. 2011), the distribution of fine roots in L+ plots shifted towards
the litter layer and soil surface, probably to take advantage of the greater concen-
tration of nutrients in the forest floor (Sayer 2006). Direct uptake of different
nutrients by roots and mycorrhizal hyphae from decomposing litter has been
demonstrated clearly by experiments using labeled substrates (Stark and Jordan
1978; Brearley et al. 2003) and a large proportion of the nutrients required for
growth may be taken up directly from organic matter on the forest floor (Herrera
et al. 1978). Compounds in litter leachate can also increase the availability of
nutrients to plants, by limiting sorption of P to clay minerals (Schreeg et al. 2013).
Collectively, these results suggest that decomposing litter constitutes an important
source of nutrients for plant growth that needs to be considered in studies of nutrient
cycling and limitation in tropical forests.
290 E.J. Sayer and L.F. Banin

Experimental Limitations

We have demonstrated that differences in life history strategies, species-specific

responses to light conditions, water availability, competition, and mutualistic
associations need to be taken into account when interpreting the responses of plants
to nutrient amendments. The topics we have addressed in this chapter also help us
pinpoint the limitations of fertilizer experiments in tropical forests. To explain some
discrepancies between pot- and field-based studies, we also need to consider
specific ‘pot effects’, the differences in the mobility of nutrient elements, and the
balance and timing of nutrient inputs.
Pot size effects—Although it is certainly possible to use pot experiments to infer
plant performance in the field, the influence of pot size is a well-known issue in
greenhouse studies. The size of the pot not only determines the amount of water and
nutrients available to plants, but the available rooting volume often decides the
duration of the study. The ‘pot-size effect’ is particularly important for fertilization
experiments because the different relative mobilities of nitrate and phosphate ions
cause a shift from P- to N-limitation during the course of the study, which is
determined by the ratio between the soil volume and the length of absorptive roots
(Cornforth 1968; Burslem et al. 1995). The highly mobile nitrate ion is delivered to
the root surface by diffusion or water flow (Ostertag 2010), whereas the relative
immobility of phosphate ions requires roots to forage for P (Yavitt et al. 2011).
Consequently, P is more likely to be limiting at the start of a study when root
biomass is low, and will become increasingly available as roots grow and access
more of the soil in the pot. In contrast, most of the N in the soil is available to plants
at the start of the study and it becomes progressively more limiting during the
experiment as soil N reserves are depleted. The combination of pot size effects and
restricted rooting space could also explain why many fertilization experiments with
potted seedlings have not observed the expected changes in plant root:shoot ratios
in response to nutrient additions.
Balance and timing of nutrient additions—Differences in the mobility and
uptake of nutrient elements also present a problem for field experiments. Substantial
losses of mobile elements can occur as soon as supply exceeds demand, even for a
short period of time (Vitousek et al. 2010). When added as fertilizer, a large
proportion of N in particular can be lost from the system through gas emissions or
leaching, rather than taken up by plants (Sayer et al. 2012). Substantial losses of N
have been measured in long-term fertilization experiments in montane and lowland
tropical forests (Hall and Matson 2003; Koehler et al. 2009; Corre et al. 2010) and
as supply continues to exceed demand, the system becomes increasingly ‘leaky’
(Koehler et al. 2009). In contrast, phosphate is not only immobile in the soil but is
also easily sorbed to clay minerals. Hence, many fertilizer experiments often apply
large amounts of inorganic P to saturate binding sites and increase the availability
of P to plants (Ostertag 2010; Wright et al. 2011). These changes in the ratios of
different nutrients can substantially influence the forest nutrient cycle and outcome
of an experiment.
Tree Nutrient Status and Nutrient Cycling in Tropical Forest … 291

Biological stoichiometry is the balance of energy and nutrient elements in living

systems. The stoichiometry of C:N:P in particular plays a critical role in a large
number of ecosystem properties and processes (Elser et al. 2000 and references
therein). Plant growth rates are thought to be related to the balance of N and P,
because fast-growing organisms require more P to support protein synthesis relative
to N content (termed ‘the growth rate hypothesis’; Elser et al. 2000; Matzek and
Vitousek 2009). In addition, the decomposition of organic matter is strongly con-
strained by the stoichiometric requirements of decomposer organisms, which in turn
influence the dynamics of carbon and nutrients (Manzoni et al. 2010).
The C:N:P ratios of plant tissues are at least partly determined by physiological
constraints and adaptation to nutrient limitation, resulting in a distinct C:N:P ratio
within a given forest ecosystem (McGroddy et al. 2004); pulses of fertilizer
application or large inputs of specific nutrients not only upset this balance but also
alter the timing of nutrient availability, which may be a critical mechanism for
maintaining productivity in nutrient-poor tropical forests (Lodge et al. 1994). The
potential effects of altering the timing and balance of nutrient inputs is summed up
nicely by Newbery et al. (2002): “Forests… are complex, long-lived and highly
interconnected systems in which short-term adjustment responses and time lags are
to be expected. Adding large quantities of fertilizer to such a presumably
near-equilibrium system (in terms of nutrient cycling) is tantamount to a major
disturbance.”

Conclusions

This chapter contributes to the growing body of evidence for multiple nutrient
limitations in tropical forests by demonstrating that plant nutrient demands, and
hence response to fertilization, are strongly influenced by life history strategy, life
stage, water stress, light availability, mutualistic associations, competition and
herbivory, all of which are site- and species-specific.
The interpretation of nutrient amendment experiments also requires due con-
sideration of how different nutrients are transported, stored and cycled. Differential
soil availability and internal demand for nutrients by plants can translate into dis-
tinct uptake strategies for each nutrient (Ostertag 2001), whereas cost-benefit
trade-offs largely determine luxury consumption and storage. The dissimilarities in
the biogeochemistry of N and P, combined with plant life-history strategies and
adaptation to soil nutrient status could even mean that ‘limitation’ and ‘availability’
are qualitatively different for N and P (Harrington et al. 2001; Ostertag 2010).
Plants require at least 17 mineral elements throughout their life cycle (Watanabe
et al. 2007) and several fertilizer experiments and physiological studies have
demonstrated the importance of other nutrients besides N and P in tropical forest
productivity, in particular the macronutrients K and Mg (e.g. Burslem et al. 1995,
1996; Hall et al. 2003; Wright et al. 2011; Santiago et al. 2012). Our understanding
of other macro- and micronutrients in tropical ecosystem processes is much less
292 E.J. Sayer and L.F. Banin

well developed, even though their respective roles in plant physiology and enzyme
production are clear. Tropical soils can contain critically low concentrations of
many micronutrients (Sobrado 2013) but we lack the experiments to evaluate how
this affects tropical forest growth and ecosystem dynamics.
Finally, organic matter plays a crucial role in tropical nutrient cycling, which is
underestimated by studies applying inorganic fertilizers and measuring responses in
the mineral soil. Aside from being a direct source of nutrients for plant growth, the
forest floor helps retain highly mobile elements. Indeed, mineral soil reserves may
contribute less than 10 % to a forest’s annual N cycle and less than 20 % to annual
P cycling (Attiwill and Adams 1993), so nutrients in litter and organic matter may
represent a better measure of site fertility than stocks in the mineral soil (Vitousek
and Sanford 1986; Tanner et al. 1998).
The accumulation and balance of energy and nutrients in plants underpins the
productivity and diversity of ecosystems (Grime 2001). In tropical forests, the high
plant diversity and heterogeneity of the ecosystem make it difficult to assess nutrient
limitation of tropical forest productivity but fertilizer experiments have nevertheless
taught us some valuable lessons about tropical forest nutrient cycling and forest
functioning.

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Is Photosynthesis Nutrient Limited
in Tropical Trees?

Louis S. Santiago and Guillermo Goldstein

Abstract Tropical forests play an enormously important role in the global cycling
of carbon. However, the extent to which nutrients limit the potential for tropical
trees to increase carbon gain as atmospheric carbon dioxide rises, a phenomenon
known as the carbon-concentration feedback, is uncertain. This chapter addresses
our current state of knowledge on nutrient limitation of photosynthesis in tropical
trees, summarizing and synthesizing the results of over 20 studies on photosynthetic
responses to nutrient manipulation experiments. Our results indicate that nutrient
limitation of photosynthesis is widespread, but that contrasting species and
ecosystems vary in their responses, with savannah trees showing the least response
at the leaf scale. Second, although photosynthesis is strongly limited by N in
particular species, N limitation of photosynthesis is modest compared to P limita-
tion of photosynthesis when considering all of the available literature. Finally,
alleviation of nutrient limitation through addition of combined nutrient treatments
produces the strongest photosynthetic responses, highlighting the potentially
complex stroichiometric interactions among elements. The authors discuss several
ways forward for resolving questions regarding the potential and limits of tropical
trees to influence key carbon cycling processes and thus improve our ability to
forecast global responses and feedbacks to climate change.

L.S. Santiago (&)

Department of Botany & Plant Sciences, University of California,
2150 Batchelor Hall, Riverside, CA 92521, USA
e-mail: santiago@ucr.edu
L.S. Santiago
Smithsonian Tropical Research Institute, Ancon, Panama, Republic of Panama
G. Goldstein
Laboratorio de Ecología Funcional, Departamento de Ecología Genética y Evolución,
Instituto IEGEBA (CONICET-UBA), Facultad de Ciencias Exactas y naturales,
Universidad de Buenos Aires, Buenos Aires, Argentina
e-mail: gold@bio.miami.edu
G. Goldstein
Department of Biology, University of Miami, Coral Gables, FL 33146, USA

© Springer International Publishing Switzerland 2016 299

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_14
300 L.S. Santiago and G. Goldstein

Keywords Nitrogen Phosphorus
Potassium Meta-analysis
Fertilization

Atmospheric carbon-dioxide

Introduction

Tropical forests are responsible for approximately one-third of terrestrial gross

primary production (Beer et al. 2010), and are thought to be especially sensitive to
climate change (Phillips et al. 2010), suggesting that their responses to climate
change and feedbacks to the global climate system are likely to be substantial. But
one outstanding question is whether tropical trees can exploit the increasing
atmospheric supply of CO2 through enhanced photosynthetic carbon income (the
concentration-carbon feedback) (Bonan and Levis 2010). Understanding the tra-
jectory of plant photosynthetic responses to increasing CO2 is not straightforward
because nutrient availability has the potential to limit the concentration-carbon
feedback in tropical vegetation such that photosynthesis may not continue to
increase with atmospheric CO2 concentration (Santiago 2015). Predictions are
further complicated by the fact that soil substrates vary greatly in the tropics. For
example, the Amazon lies along a dramatic east–west nutrient availability gradient
(Quesada et al. 2010), and there are often strong changes in nutrient availability
with elevation (Dalling et al., this volume). So how does the formidable diversity of
trees combine with heterogeneity of soil types and elemental availability in the
tropics to limit photosynthetic exploitation of increasing atmospheric CO2? To
address this question, this synthesis focuses on photosynthetic responses of tropical
trees to nutrients and how such information is critical to inform Earth system
models to understand potential climate change feedbacks.
There are multiple ways in which nutrients could mediate the
concentration-carbon feedback. The first is simply that plants increase leaf-level
photosynthetic rates per area with increasing atmospheric CO2 to the degree allowed
by nutrient availability (Bloom et al. 1985; Field and Mooney 1986) (Fig. 1a). The
second is that as atmospheric CO2 increases, plants allocate increased carbon income
to growth such that leaf-level photosynthesis per area remains the same, but the
greater leaf surface area associated with enhanced growth leads to increased pho-
tosynthesis at the whole-plant scale (Poorter and Remkes 1990) (Fig. 1b). A third
scenario is one in which increasing CO2 causes a decrease in stomatal conductance
such that internal CO2 concentration and photosynthetic rate remain the same, but
water use efficiency, defined as photosynthetic carbon gain per unit water loss,
increases (Fig. 1c) (Farquhar and Richards 1984; Cernusak et al. 2007a, b). In all of
these scenarios we expect nutrients to mediate physiological responses to changing
atmospheric CO2 (Raven et al. 2004; Cernusak et al. 2007a, b), such that tropical
trees growing on the most fertile soils would have the greatest increase, or least
reduction in photosynthetic carbon assimilation. All of these potential responses to
atmospheric CO2 could also have larger scale impacts because of the strong bearing
Is Photosynthesis Nutrient Limited in Tropical Trees? 301

Fig. 1 Possible ways for nutrients to mediate responses of tropical plants to increasing CO2

of tropical forests on the global carbon cycle and climate system (Friedlingstein et al.
2006; Bonan and Levis 2010). Yet the only way to determine the extent to which
nutrients limit the carbon-concentration feedback in tropical trees is to determine the
identity of elements that limit photosynthesis and the degree of that limitation.
There are also several valid eco-physiological reasons why tropical woody
species may not show greater photosynthesis on more fertile soils. First, several
studies have now reported increased herbivory following nutrient addition and an
increase in foliar nutrient concentration that appears to make leaves more palatable
to herbivores (Campo and Dirzo 2003; Santiago et al. 2012). In some cases, the
increase in herbivory can be strong enough to mask plant growth responses to
nutrient addition (Andersen et al. 2010). Second, there is evidence that as atmo-
spheric CO2 increases, some plants reduce stomatal conductance such that photo-
synthetic rates remain the same, but water loss goes down and water use efficiency
goes up (Cernusak et al. 2013). Because nutrient availability can interact with plant
regulation of water loss, especially when transpiration rates are linked to uptake of
key elements through mass flow in the transpiration stream (Cramer et al. 2009),
reductions in stomatal conductance with increasing CO2 could reduce nutrient
uptake through mass flow and worsen nutrient limitation of photosynthesis. In other
cases, plants in poor soils have been shown to exhibit greater transpiration rates
than plants in fertile soils and it is thought that the benefit is increased rates of
absorption of nutrients through mass flow (Cramer et al. 2008). In such cases, how
plants in poor versus fertile soils might alter their photosynthetic rates with
changing atmospheric CO2 is unknown. Finally, if increasing atmospheric CO2
concentration indeed increases photosynthetic carbon uptake, at some point a
buildup of carbohydrate products of photosynthesis could lead to down regulation
302 L.S. Santiago and G. Goldstein

of photosynthetic rate in a process known as feedback inhibition (Delucia et al.

1985). Thus careful evaluation of the study design, including plant-animal inter-
actions and other physiological processes such as nutrient allocation to leaves and
interactions with transpiration will increase the depth of interpretation and predic-
tive power of experimental studies.

How Is Nutrient Limitation Studied?

Nutrient limitation of plant productivity and photosynthesis has been studied

through a variety of approaches. Perhaps the most effective has been through
nutrient addition experiments in which responses to fertilization relative to control
treatments are interpreted as limitation by that nutrient, of if there is no response,
the conclusion is that the added nutrient was not limiting (Vitousek 2004). Many of
these are stand-level fertilization experiments consisting of large (40 × 40 m) plots
receiving individual or combined addition of nitrogen (N), phosphorus (P), potas-
sium (K) or micronutrients (Tanner et al. 1992; Vitousek et al. 1993; Mirmanto
et al. 1999; Newbery et al. 2002; Campo and Vázquez-Yanes 2004; Davidson et al.
2004; Bucci et al. 2006; Lu et al. 2010; Wright et al. 2011; Álvarez-Clare et al.
2013; Fisher et al. 2013). Such large experiments are able to evaluate nutrient
limitation at multiple scales including leaf physiological processes, growth and
ecosystem-level processes such as nutrient cycling and litterfall. Yet, because
canopy access poses substantial challenges and because ecosystem science is
usually the focus of these studies, measurements of leaf-scale physiological mea-
surements are only available from five of the known large-scale tropical fertilization
experiments (Cordell et al. 2001; Saraceno 2006; Lu et al. 2007; Pasquini and
Santiago 2012).
Other approaches to manipulating nutrient availability in tropical trees include
litter removal and addition experiments (Sayer and Tanner 2010; Sayer, this vol-
ume) or removal of vegetation to increase nutrient availability of target individuals.
Such process-based nutrient manipulations do not directly reveal the identities of
limiting elements. However, when foliar nutrient responses are included, infor-
mation on the relative importance of key elements can sometimes be determined
(Lewis and Tanner 2000; Barberis and Tanner 2005). At smaller scales, fertilizer
has also been applied directly to individual plants in the field (e.g. Yavitt and
Wright 2008), or in pots (Burslem 1996; Gunatilleke et al. 1997; Lawrence 2003;
Cai et al. 2008). In many cases, such experiments have been successful in deter-
mining which elements limit growth and physiological processes in tropical seed-
lings or saplings.
When stand-scale experimental manipulation of nutrient availability is imprac-
tical, basic questions about plant nutritional effects on physiology have been
approached along environmental gradients that vary in soil nutrient availability
(Vitousek et al. 1992; Santiago et al. 2004; Santiago and Mulkey 2005; Baltzer
et al. 2008; Fyllas et al. 2009). In these in situ studies, by evaluating how foliar
Is Photosynthesis Nutrient Limited in Tropical Trees? 303

nutrient concentration or physiological characteristics vary with soil type it is

possible to generate hypotheses regarding nutrient limitation that can be further
tested experimentally. For example, in Hawaii, the gradual shift from N-limitation
of ecosystem productivity in very young soils to P-limitation of ecosystem pro-
ductivity in very old soils creates opportunities to evaluate the relative importance
of these elements for photosynthesis and growth (Kitayama et al. 1997; Cordell
et al. 2001). In lowland tropical forest in Panama, increasing precipitation leads to
species replacement of dry-season deciduous tree species with evergreen species,
consistent with the idea that evergreeness conserves nutrients by minimizing the
cost of leaf replacement and providing an advantage for evergreen species in wetter
sites with leached soils (Santiago and Mulkey 2005). Even broad ecological pat-
terns, such as in Brazilian savannahs, where patches of closed canopy dry season
deciduous forest appear on calcium-rich outcrops (Haridasan 1992), provide fodder
for new hypotheses and experiments. Thus the interplay between observation and
experiment has continued to be an important process in understanding nutrient
limitation in the tropics.
Direct analysis of foliar ratios of nitrogen-to-phosphorus (N:P) is also considered
a method for inferring relative nutrient limitation of N versus P using the guideline
that N:P ratios below 12 indicate N-limitation, ratios above 16 indicate P-limitation
and values between 12 and 16 indicate co-limitation by N and P (Aerts and Chapin
2000). It is difficult for foliar N:P data alone to establish limitation, yet it seems to
be an excellent measure of relative limitation. Previously, most researchers used the
eco-physiological standard of the youngest mature leaves to study N:P, but recently,
stem, root, and older leaf N:P have been shown to be more responsive indicators of
soil nutrient availability than new leaf N:P, because new leaves appear to act as
nutrient reservoirs during active growth, allowing maintenance of optimal N:P
ratios in recently produced, physiologically active leaves (Schreeg et al. 2014).
Overall, combining soil and plant observational approaches with experiments offer
our greatest potential for unraveling complex interactions between nutrient avail-
ability, increasing atmospheric CO2 and photosynthetic performance in tropical
forests.

The Physiological Basis for Elemental Limitation

of Photosynthesis

The proteins of the Calvin cycle and thylakoids make up the majority of N in
leaves, thus N is known to be a strong determinant of photosynthesis (Field and
Mooney 1986; Wright et al. 2004). Therefore, as leaf N concentration increases
with experimental fertilization (Ostertag 2009; Wright et al. 2011; Pasquini and
Santiago 2012; Santiago et al. 2012), maximum photosynthetic rate is expected to
increase as well. N addition in shade leaves is expected to increase N allocation
toward light harvesting proteins of the thylakoid membrane of the chloroplast,
304 L.S. Santiago and G. Goldstein

including the pigment-protein complexes and components of the electron transport

chain (Evans 1989). In sun leaves, the maximum rate of CO2 assimilation (Amax) is
expected to increase with N addition, but in any case, there should be correspon-
dence between light harvesting and carboxylation because carboxylation capacity
and electron transport are tightly coupled (Wullschleger 1993; Pasquini and
Santiago 2012). The increase in foliar N with fertilization is usually modest, owing
to the metabolic costs of storing N in plant tissue (Ostertag 2009). Thus the
expected enhancement of photosynthesis with N addition should occur over a
relatively small range of leaf N values.
Leaf P is a component of polyphosphates and phospholipids and is necessary for
activity of the Calvin cycle and rubisco regeneration (Marschner 1995). Within the
biochemical reactions of carbon assimilation, activation through phosphorylation is
ubiquitous, highlighting the potential for P to limit or promote rapid photosynthetic
reactions. P addition has been shown to stimulate Amax, but reduce Amax per unit
leaf P (Cordell et al. 2001), because of the ability of leaves to sequester large
amounts of P in vacuoles (Sinclair and Vadez 2002; Ostertag 2009). In most soils of
lowland tropical forests, P is thought to be the most limiting element to productivity
(Dalling, this volume), so understanding P limitation of photosynthesis is funda-
mental for predicting plant responses to climate change.
K+ is the most abundant ion in plant cells and is critical for numerous bio-
chemical functions including osmoregulation, photosynthesis, cell extension,
oxidative phosphorylation and protein activation (Evans and Sorger 1966; Morgan
1984; Marschner 1995; Santiago and Wright 2007). Therefore, K addition has the
potential to increase photosynthesis through efficient biochemistry and stomatal
control, but of the macronutrients, it is the least studied and most rare to find in
fertilization experiments on tropical trees. Currently, there is only one stand-scale
natural forest fertilization study that has incorporated K, and growth of seedlings,
saplings and poles, but not emergent trees, as well as aspects of photosynthesis have
been shown to be limited by K (Wright et al. 2011; Pasquini and Santiago 2012).
K is also unique in that it has no organic phase, so unlike N and P which can be
bound to organic complexes within leaf litter, K leaches quickly (Schreeg et al.
2013), potentially promoting shortages in availability.

Nutrient Addition Studies with Tropical Trees

Of the nutrient addition studies on tropical plants, we have identified 19 studies on

46 species that measured Amax on plants fertilized with N, P, K or a combination of
these and micronutrient elements (Table 1). These include studies on plants in pots
in controlled greenhouse settings, as well as plants in the field, growing in large
stand-level fertilized or control plots. We only included studies that report Amax for
individual species at multiple nutrient levels, but did not consider proxy variables
Is Photosynthesis Nutrient Limited in Tropical Trees? 305

Table 1 Summary of species, locations, experimental details and references for studies involving
responses of maximum photosynthetic rate to nutrient addition in tropical tree species
Location Species Treatment Study type References
Brasília, Brazil Blepharocalyx N, P, field Saraceno (2006)
salicifolius Combined
Brasília, Brazil Caryocar brasiliense N, P, field Saraceno (2006)
Combined
Brasília, Brazil Ouratea hexasperma N, P, field Saraceno (2006)
Combined
Brasília, Brazil Qualea parviflora N, P, field Saraceno (2006)
Combined
Dinghushan, China Cryptocarya chinensis N field Lu et al. (2007)
Dinghushan, China Cryptocarya concinna N field Lu et al. (2007)
Dinghushan, China Randia canthioides N field Lu et al. (2007)
Dinghushan, China Cryptocarya concinna N, P, field Zhu et al. (2014)
Combined
Dinghushan, China Randia canthioides N, P, field Zhu et al. (2014)
Combined
Freetown, Sierra Entandrophragma Combined pot Riddoch et al. (1991)
Leone angolense
Freetown, Sierra Nauclea diderrichii Combined pot Riddoch et al. (1991)
Leone
Fujian, China Eucalyptus dunnii P pot Wu et al. (2014)
Fujian, China Eucalyptus grandis P pot Wu et al. (2014)
Gamboa, Panama Ficus insipida Combined pot Cernusak et al. (2007a,
b)
Gamboa, Panama Platymiscium Combined pot Cernusak et al. (2009)
pinnatum
Gamboa, Panama Swietenia macrophylla Combined pot Cernusak et al. (2009)
Gamboa, Panama Tectona grandis Combined pot Cernusak et al. (2009)
Gigante, Panama Alesis blackiana N, P, K field Pasquini and Santiago
(2012)
Guangzhou, China Acmena N chamber Liu et al. (2012)
acuminatissima
Guangzhou, China Castanopsis hystrix N chamber Liu et al. (2012)
Guangzhou, China Ormosia pinnata N chamber Liu et al. (2012)
Guangzhou, China Schima superba N chamber Liu et al. (2012)
Hawaii, USA Metrosideros N, P, field Cordell et al. (2001)
polymorpha Combined
Queensland, Auranticarpa ilicifolia P pot Bloomfield et al.
Australia (2014)
Queensland, Cryptocarya P pot Bloomfield et al.
Australia triplinervis (2014)
Queensland, Flindersia bourjotiana P pot Bloomfield et al.
Australia (2014)
Queensland, Guioa lasioneura P pot Bloomfield et al.
Australia (2014)
Queensland, Hymenosporum flavum P pot Bloomfield et al.
Australia (2014)
(continued)
306 L.S. Santiago and G. Goldstein

Table 1 (continued)
Location Species Treatment Study type References
Queensland, Neolitsea dealbata P pot Bloomfield et al.
Australia (2014)
Queensland, Syzygium wilsonii P pot Bloomfield et al.
Australia (2014)
Queensland, Flindersia brayleyana Combined pot Thompson et al. (1988)
Australia
Queensland, Argyrodendron Combined pot Thompson et al. (1992)
Australia trifoliolatum
Queensland, Argyrodendron sp Combined pot Thompson et al. (1992)
Australia
Queensland, Flindersia brayleyana Combined pot Thompson et al. (1992)
Australia
Queensland, Toona australis Combined pot Thompson et al. (1992)
Australia
Recife, Brazil Anadenanthera P pot Oliveira et al. (2014)
colubrina
Recife, Brazil Prosopis juliflora P pot Oliveira et al. (2014)
Sabah, Malaysia Dryobalanops Combined field Bungard et al. (2002)
lanceolata
Sabah, Malaysia Shorea johorensis Combined field Bungard et al. (2002)
San Antonio, Costa Cedrela odorata Combined pot Carswell et al. (2000)
Rica
Sao Paulo, Brazil Cariniana legalis Combined pot de Oliveira et al. (2012)
Sao Paulo, Brazil Croton urucurana Combined pot de Oliveira et al. (2012)
Twin Cays, Belize Rhizophora mangle N, P field Lovelock et al. (2006)
Xishuangbanna, Bauhinia aurea N pot Cai et al. (2008)
China
Xishuangbanna, Bauhinia claviflora N pot Cai et al. (2008)
China
Xishuangbanna, Bauhinia monandra N pot Cai et al. (2008)
China
Xishuangbanna, Bauhinia purpurea N pot Cai et al. (2008)
China
Xishuangbanna, Bauhinia tenuiflora N pot Cai et al. (2008)
China
Reference (Oliveira et al. 2014)

related to photosynthetic rate, such as foliar nutrient concentration or specific leaf

area. Whereas most of these studies used simple fertilizer additions, four created
Hoagland or Ingestad solutions to match desired levels of nutrient availability
(Thompson et al. 1988, 1992; Riddoch et al. 1991; Carswell et al. 2000), but in an
attempt to be inclusive we considered all of these studies due to the limited
availability of such information in the literature. Within Table 1, there is also
Is Photosynthesis Nutrient Limited in Tropical Trees? 307

variation in light availability among studies so we used the highest light availability
if there were multiple levels, yet some studies (Lu et al. 2007; Pasquini and
Santiago 2012), were done on understory plants in the field, so very low light
conditions prevailed. Similarly, in studies where multiple levels of nutrient addition
were performed, we utilized treatments with the highest level of nutrient addition
except for the study of Lu et al. (2007), in which the goal of the study was to
simulate N deposition to the point of toxicity. Here, we used the lowest level of
fertilization, which was similar to the high nutrient treatments in other studies. If
multiple time points were given in the paper, we used the latest time point to
represent the values produced under a longer period of experimental treatment.
Finally, we restricted our analysis to woody species and included lianas in addition
to trees, thus three of the Bauhinia species in Table 1 are lianas (B. claviflora, B.
tenuiflora, B. aurea).
Our data show that overall there have been enhancements of Amax with nutrient
addition in tropical trees (Fig. 2). Of the studies on nutrient limitation of Amax in this
synthesis, 22 included control and high N treatments, 21 included control and high
P treatments, and 24 included control and combined elemental treatments of various
kinds, for a total of 67 species × site combinations (Table 1). The raw data shows
that mean Amax trended higher with N, P or combined nutrient addition (Fig. 2).
However, to evaluate the overall effect of nutrient addition on photosynthesis, we
used the ln-transformed response ratio as our main effect size metric: RRx = ln (E/
C), where E is Amax in the enriched or high nutrient treatment, C is Amax in the
un-enriched control or low nutrient treatment (Elser et al. 2007). We then tested
statistically whether RRx for each treatment (RRN, RRP, RRCombined), was signifi-
cantly different from zero. In comparisons across multiple experimental systems
where species, soils and environmental conditions vary considerably, the analysis
of change relative to control is generally considered to be more meaningful than
absolute differences between means (Elser et al. 2007).

Fig. 2 Mean values of 16

Photosynthetic rate (µmol m s )
-1

maximum photosynthetic rate

14
-2

under control versus nutrient Control

addition treatments for Fertilized
12
tropical tree species fertilized
with N, P, or combined 10
nutrient treatments
8

0
N P Combined
Treatment
308 L.S. Santiago and G. Goldstein

0.35

0.30

0.25

RR x 0.20

0.15

0.10

0.05

0.00
+N +P +Combined

Fig. 3 Responses of area-based maximum photosynthetic rate to single enrichment of N, P or to

combined elemental enrichment in tropical woody species. Data are natural-log transformed
response ratios (RRx) in which photosynthesis in the enriched treatment is divided by its value in
the control treatment and then ln-transformed (Elser et al. 2007). For example, a value of 0.5
indicates a value in the manipulated treatment that is approximately 1.6 times its value in the
control. Sample sizes +N (22), +P (21) and +Combined (24). Error bars indicate plus or minus one
standard error

Our synthesis indicates that nutrient limitation of photosynthesis exists across

the woody tropical species studied thus far (Fig. 3). However, the magnitude of the
response varied strongly with the element in question. Across the 22 species × site
combinations for N, photosynthesis trended higher with N addition, but mean RRN
was not significantly different from zero at the 0.05 significance level (p = 0.061 for
t-test of RRN = 0). Mean RRP was significantly different from zero, indicating that
photosynthesis significantly increased with P across the 21 species × site combi-
nations (p = 0.03 for t-test of RRP = 0). Thus our results across studies are consistent
with the idea that P is the most widespread limiting nutrient in tropical forests.
Whereas N produced substantial species-specific responses at some sites, with RRN
values up to 0.50 indicating an increase of approximately 1.6 times its value in the
control, the magnitude of photosynthetic response to N was muted compared to P,
which showed RRP values as high as 0.90 indicating an increase of 2.45 times its
value in the control treatment.
Our data also indicate that the 24 species × site combinations with combined
manipulation of N, P, K or micronutrients produce the greatest response across all
studies (p = 0.0009 for t-test of RRCombined = 0; Fig. 3). RRCombined ranged as high as
0.92 indicating an increase of 2.51 times its value in the control. The highest sig-
nificance in the case of combined nutrient addition leads to one of two possible
conclusions. The first is that synergistic effects of multiple elemental manipulation
has a stronger impact on alleviating nutrient limitation of photosynthesis than single
element manipulation, consistent with the theory of multiple limiting nutrients
(Kaspari et al. 2008). This theory suggests that plants allocate to uptake of limiting
Is Photosynthesis Nutrient Limited in Tropical Trees? 309

resources until all resources simultaneously limit a physiological process such that
addition of any resource increases the rate of that process to the same degree (Bloom
et al. 1985). Alternatively, the greatest response to combined nutrient addition could
result from the fact that manipulating multiple elements leads to a greater chance that
the single most limiting element is included in the study. Overall, the high values for
RRCombined support the idea that the stoichiometric demands of fundamental bio-
chemical processes enable co-limitation by multiple elements (Elser et al. 2007;
Kaspari et al. 2008; Wright et al. 2011; Santiago et al. 2012).
Although our mean RRx values were significantly different from zero or nearly
so in all cases, a closer look at individual species × site combinations reveals that
RRx values were negative in 21 out of 67 cases. Negative RRx values were fairly
distributed across nutrient treatments, with eight negative RRN values, six negative
RRP values, and seven negative RRCombined values. Furthermore, 11 out of the 21
negative RRx values were from a single study, in which 11 out of the 12 RRx values
in the study were negative (Saraceno 2006). The study by Saraceno (2006) is in
many ways unique because it was conducted in Brazilian cerrado sensu stricto
vegetation, an open canopy savannah ecosystem, whereas most of the other studies
include tree species of closed canopy rainforest ecosystems. Cerrado regions are
known for nutrient poor soils that are acidic with a low cation exchange capacity
and high concentrations of aluminum (Furley and Ratter 1988). Additionally, light
availability is likely to be higher in cerrado because of the open canopy and rainfall
is more seasonal than in many closed canopy rainforest ecosystems. Whereas most
rainforest species increase photosynthetic rate with the addition of nutrients, cerrado
trees nearly uniformly decrease photosynthetic rate (Saraceno 2006), and reduce
both nighttime and daytime transpiration with the addition of nutrients (Bucci et al.
2006; Scholz et al. 2007).
Several studies have directly addressed the responses of tropical trees to elevated
atmospheric CO2 by experimentally combining elevated CO2 treatments with
nutrient addition. Application of soil fertilizer substantially accelerated biomass
accumulation of two tropical tree species at elevated CO2, but elevated CO2 had no
significant effect on biomass accumulation in unfertilized communities (Winter
et al. 2001), providing support for nutrient limitation of the concentration-carbon
feedback. However, relatively little data is available on photosynthetic responses to
nutrients at high CO2 (Fig. 4). In one study from southeast China, N fertilization did
not modify the effects of CO2 on photosynthesis (Liu et al. 2012). Yet, in two other
studies from the neotropics, greater combined nutrient availability increased the
magnitude of the response of photosynthesis to elevated CO2 (Carswell et al. 2000;
de Oliveira et al. 2012), providing support for nutrient limitation of the
concentration-carbon feedback. The results of these studies are consistent with the
conclusion that N limitation of photosynthesis in tropical trees is modest
compared to P, and combined nutrient treatments produce the greatest responses
(Fig. 4).
310 L.S. Santiago and G. Goldstein

Fig. 4 Maximum 18

photosynthetic rate (µmol m s )

-2 -1
photosynthetic rate at elevated Elevated CO2 - unfertilized
16 Elevated CO2 - fertilized
CO2 for tropical trees in
control and fertilized 14
treatments 12

Maximum
10
8
6
4
2
0

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Conclusions and Future Directions

We sought to determine whether nutrients limit the concentration-carbon feedback,

the ability of tropical trees to increase rates of photosynthetic carbon gain as
atmospheric CO2 increases. Our evaluation of the available literature indicates
several key patterns. First, nutrient limitation of photosynthesis is widespread in
rainforest trees and appears to manifest itself differently, if at all, in savannah trees.
Second, although photosynthesis is strongly limited by N in particular species, N
limitation of photosynthesis is modest compared to P limitation of photosynthesis
when considering all of the available literature. Finally, alleviation of nutrient
limitation through addition of combined nutrient treatments produces the strongest
photosynthetic responses, highlighting the potentially complex stroichiometric
interactions among elements.
Currently, our predictions for how tropical forest ecosystems will respond to
climate change and how their responses will feedback to the global climate system
are limited by model realism. Several models still represent photosynthesis as
continuously increasing in proportion to atmospheric CO2 (Bonan and Levis 2010),
illustrating the need for improved representation of photosynthesis in Earth system
models (Ali et al. 2015). To build on the current state of knowledge regarding
nutrient limitation of photosynthesis in tropical trees, an expansion of approaches
will be necessary. First, the focus on N and P needs to be broadened to include
other potentially limiting elements. Only one long-term tropical fertilization study
has added K in a factorial design, but it reported substantial K limitation of key
ecosystem processes (Wright et al. 2011). Also, given the diversity of tropical soils,
one wonders if there are other elements beyond N, P, and K that deserve focused
study. Second, better correspondence between large-scale field experiments and key
Is Photosynthesis Nutrient Limited in Tropical Trees? 311

greenhouse experiments designed to test specific mechanisms are needed to pin-

point physiological responses and refine their role in processes at larger scales.
Finally, a greater distinction between nutrient limitation of photosynthetic pro-
ductivity between early and late successional forests is needed to elucidate the
potential carbon sequestration of secondary forest during regeneration. Secondary
forests are becoming a larger proportion of the total tropical land area, and their
rapid growth during early succession has been implicated as a potential major route
for carbon absorption by terrestrial vegetation (Cernusak et al. 2013). This potential
must be determined to improve our predictive power. Overall, understanding the
potential and limits to the key carbon cycling processes of tropical trees will
improve our ability to forecast global responses and feedbacks to climate change.

Acknowledgments We gratefully acknowledge Alex Barron, Sandra Bucci, Walt Carson, Sarah
Pasquini, Jennifer Powers, Fabian Scholz, Jim Sickman, Ben Turner, Peter Vitousek, Klaus Winter,
Joe Wright, and Nina Würzburger for insightful discussions; Xiankai Lu and Keith Bloomfield for
contributing raw data; the Smithsonian Tropical Research Institute and the University of California,
Riverside, for logistical support; and a University of California Faculty Fellowship to Santiago.

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 Part V
Carbon Economy and Allocation
of Tropical Trees and Forests
Facing Shortage or Excessive Light: How
Tropical and Subtropical Trees Adjust
Their Photosynthetic Behavior and Life
History Traits to a Dynamic Forest
Environment

Guillermo Goldstein, Louis S. Santiago, Paula I. Campanello,

Gerardo Avalos, Yong-Jiang Zhang and Mariana Villagra

Abstract Light is critical for plant establishment, growth, and survival in wet
tropical forests. The objective of this chapter is to analyze paradigms of photo-
synthetic performance and life history traits of tropical forest trees to contrasting
light environments across the forest floor, gaps and upper canopy. Physiological
and morphological plasticity as well as genetically fixed adaptive traits are ana-
lyzed, including leaf optical properties and photoprotection from high irradiance.
Photosynthetic adaptations to contrasting light environments of closely related
species are discussed. This approach has the advantage among comparative studies

G. Goldstein (&)
Laboratorio de Ecología Funcional, Departamento de Ecología Genética y Evolución,
Instituto IEGEBA (CONICET-UBA), Facultad de Ciencias Exactas y naturales,
Universidad de Buenos Aires, Buenos Aires, Argentina
e-mail: goldstein@ege.fcen.uba.ar
G. Goldstein
Department of Biology, University of Miami, Coral Gables, FL 33146, USA
L.S. Santiago
Department of Botany & Plant Sciences, University of California,
2150 Batchelor Hall, Riverside, CA 92521, USA
e-mail: santiago@ucr.edu
L.S. Santiago
Smithsonian Tropical Research Institute, Apartado Postal, 0843-03092 Balboa,
Republic of Panama
P.I. Campanello
M. Villagra
Laboratorio de Ecología Forestal y Ecofisiología, Instituto de Biología Subtropical,
CONICET, FCF, Universidad Nacional de Misiones, Posadas, Argentina
e-mail: pcampanello@yahoo.com
M. Villagra
e-mail: marian.villagra@gmail.com

© Springer International Publishing Switzerland 2016 319

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_15
320 G. Goldstein et al.

of adaptations across species in that genetic relationships among species are known.
Species-specific variations in maximum photosynthetic rates, which reflect the
degree of adaptation to growth irradiance, are shown to be gradual, suggesting that
classification into two distinct functional groups in terms of light requirements is
somewhat arbitrary. Trees growing in gaps or in the upper canopy rely strongly on
biochemical mechanisms to dissipate excess energy and to avoid damage to the
light reaction centers and photosystems. Consistent with their high photosynthetic
capacity, light demanding species are capable of plastic changes in hydraulic ar-
chitecture, such as increases in hydraulic conductivity under high irradiance, which
makes them more competitive in open habitats.

Keywords Electron transport rate Hydraulic architecture Leaf pigments






Photoinhibition Photosynthesis Plasticity Shade tolerant trees

Introduction

Light is one of the most important environmental determinants of plant establish-

ment, growth, and survival in wet tropical and subtropical forests (Osunkoya and
Ash 1991; Nicotra et al. 1999). Light varies spatially and temporally in these forests
and consequently trees have developed various adaptations to cope with dynamic
light regimes. Canopy trees are exposed to high irradiance, evaporative demand and
temperature, which can induce nonstomatal limitations to photosynthesis through
the effects of deactivation of photosynthetic enzymes and the reduction of photo-
chemistry (Krause et al. 1995; Ishida et al. 1999; Demmig-Adams and Adams
2006). In the understory of tropical rainforests, light is considered the most limiting
resource, with understory plants often receiving less than 1 % of the ambient light
that reaches the canopy (Björkman and Ludlow 1972; Chazdon and Fetcher 1984).
Forest gaps have a different light regime compared to the upper canopy and the
forest understory (Canham et al. 1990). At a regional scale, a lack of solar radiation
in tropical and subtropical forests during the rainy season appears to limit plant

G. Avalos
Escuela de Biología, Universidad de Costa Rica, San Pedro, San José 11501-2060,
Costa Rica
e-mail: gerardo.avalos@ucr.ac.cr
G. Avalos
The School for Field Studies, Center for Sustainable Development Studies,
100 Cummings Center, Suite 534-G, Beverly, MA 01915-6239, USA
Y.-J. Zhang
Department of Organismic and Evolutionary Biology, 16 Divinity Avenue,
Cambridge, MA 02138, USA
e-mail: yongjiangzhang@oeb.harvard.edu
Facing Shortage or Excessive Light: How Tropical … 321

carbon assimilation and growth due to heavy cloud cover associated with the
Intertropical Convergence Zone (Wright and vanSchaik 1994; Graham et al. 2003).
Light in the forest understory consists of diffuse radiation that is randomly inter-
spersed by short duration light flecks (Chazdon and Fetcher 1984; Canham et al.
1990), and depends on canopy cover at any point in the forest (Fig. 1). Light flecks
occur when movement of leaves in the canopy or changes in the angle of the sun allow
direct light penetration for intermittent periods of time (Lüttge 2008). The diffuse light
in the understory has different spectral characteristics compared to upper canopy light
because certain wavebands are differentially absorbed as light passes through leaves
within the canopy. The red-to-far red ratio (R:FR) ranges from 1.10 in full sun to as
low as 0.10 under an intact forest canopy (Lee 1987). Such changes in R:FR have
profound effects on plant development and growth (e.g. Ballaré et al. 1997). Under
strongly light-limiting conditions of the forest understory, plants are expected to
maximize light capture in the most efficient way by obtaining light resources at the
lowest costs in terms of construction and maintenance (Givnish 1988).
Tropical trees are often classified in terms of succession and light requirements as
early-successional, light demanding, fast growing, pioneer species at one side of the
spectrum and late successional, shade tolerant, slow growing species at the other.
During the establishment stage, light requiring species tend to grow in gaps under
relatively high irradiance levels, whereas shade tolerant species can become estab-
lished in the shaded forest understory. When trees reach the canopy, they are
exposed to environmental conditions very different from where they spend the first
part of their life cycles. Light requiring and shade tolerant species, however, may not
be two completely distinct functional groups (Ellis et al. 2000; Gilbert et al. 2006).
The objective of this chapter is to analyze paradigms regarding physiological
plasticity and adaptation of tropical forest trees to the contrasting light environments

Fig. 1 Vertical fish-eye camera view from the forest floor to the canopy of a lowland tropical
forest in Gigante, Panama (Photograph Sarah Pasquini). The picture shows the low light levels
that plants experience on the forest floor and shows the small openings of the canopy that allow
direct solar radiation to reach the understory of the forest for short periods of time (light flecks)
322 G. Goldstein et al.

provided by the forest understory, treefall gaps, and the upper canopy. A substantial
improvement in the understanding of light responses from tropical trees during the
last two decades, particularly in high light environments, is in part associated with
accessing the upper canopy, often 30–60 m above the forest floor. The first con-
struction tower crane to gain access to the canopy was established in a seasonal dry
tropical forest in Panama in 1990. Since then, other cranes have been established in a
variety of tropical forests around the world.

The Paradigm of Forest Gap Dynamics

Regeneration of trees in rainforests tends to occur when treefall gaps initiate a

canopy opening. These gaps, where most of the incoming light is direct solar
radiation, are filled with previously suppressed or newly arriving seedlings and
saplings. This process may have important effects on forest structure, composition,
and dynamics (Whitmore 1975; Hartshorn 1978; Runkle 1981; Brokaw 1985). In
fact, mature forests have been described as shifting mosaics of different-sized
patches at contrasting stages of gap closure (Watt 1947; Whitmore 1975; Oldeman
1978; Bormann and Likens 1979). In addition to higher light availability, tropical
forest treefall gaps are also less humid, hotter, and usually have greater soil nutrient
and water availability than surrounding forest understory (Vitousek and Denslow
1986; Pearcy 1987; Meinzer et al. 1995). Gap formation has been suggested to play
a major role in maintaining tree diversity in species-rich tropical and subtropical
forests because it provides habitat heterogeneity that can be partitioned by species
with contrasting light demands (Denslow 1980). However, Hubbell et al. (1999)
found that species richness of seedlings was greater in gaps than in forest under-
story, but species richness per stem was similar in gaps and in non-gap sites
suggesting that gap phase regeneration does not fully explain species richness of the
forest. Species richness is divided by the number of stems because stem density in
gaps is substantially higher than stem density in the forest understory.
Some plant species can be used as “biological clocks” to estimate the temporal
dynamics of gap openings (Zalamea et al. 2012). This is important because treefall
gaps tend to close fast and a few years after gap formation it can be difficult to
recognize where and when the gap opening occurred. Astrocaryum mexicanun is an
understory palm species that endures tree falls when gaps are formed. The palm
bends under falling trees, but rapidly recovers vertical growth. Based on the
age-constant rate of stem elongation, the vertical stems of the palm were used to
determine the age of the gap opening (Martinez-Ramos et al. 1988). Using this
morphological feature of the palm, it was estimated that the turnover rate of gap
openings in a Mexican wet tropical forest is about 47 years, providing evidence that
gap openings and thus the release of suppressed seedling and saplings of forest trees
occur frequently in time, and spatially at short distances within the forest. Species of
the genus Cecropia can also be used to date previous disturbances or gap formation
in tropical forest because the scars of fallen leaves, inflorescences and branches
Facing Shortage or Excessive Light: How Tropical … 323

remain visible along the trunk. The high annual periodicity in branching and
alternation of long and short nodes make it possible to distinguish fast and slow
growth periods, allowing the gap history of particular sites to be quantified
(Zalamea et al. 2008).
In tropical and subtropical forests, growth of particular plant groups can alter the
gap phase regeneration process. For example, in some disturbed forest, native
bamboos that are present in the understory can colonize treefall gaps and inhibit tree
regeneration, preventing recovery of disturbed forests (Campanello et al. 2007).
There is also evidence that lianas can send treefall gaps on an alternate successional
pathway, whereby gap-phase regeneration is dominated by lianas and stalled in a
low leaf area index canopy state for many years (Schnitzer et al. 2000).

Developmental Plasticity of Physiological

and Morphological Traits Under
Contrasting Light Regimes

Tropical and subtropical plants or plant parts, such as leaves, have the ability to
adjust their morphology and physiology to a particular light environment. For
example, there are substantial differences between sun exposed and shade exposed
leaves, and it is well documented that leaves developed in the sun are smaller,
thicker, have more layers of palisade cells, and have higher photosynthetic and
respiration rates than shade leaves (Pearcy 1987; Vogelmann et al. 1996). Optical
properties such as reflectance, absorptance, transmittance, and pigment composition
of leaves also change depending on the growing light environment (Poorter et al.
2000). At the crown level, crown architecture, including branching patterns and
degree of self-shading, as well as allometry, including key ratios such as
height-to-diameter, and supporting-to-non-supporting tissue mass, can also change
depending on light regime (Hallé et al. 1978; Kohyama and Hotta 1990; King 1991;
Kitajima 1996; Valladares 1999; Valladares et al. 2000).
Tropical and subtropical tree species have developed species-specific morpho-
logical and physiological characteristics enabling them to optimize the capture of
scarce solar radiation in the dynamic light environment of wet forests. Plants
growing in the forest understory assimilate up to 80 % of their carbon uptake during
short duration high intensity light flecks (Chazdon 1988). Responses to low light
therefore involve rapid photosynthetic induction in response to sudden increases in
light (Chazdon and Pearcy 1986; Montgomery and Givnish 2008). Maximizing
carbon gain during light flecks depends on the photosynthetic induction response
once a leaf is illuminated and on the ability to continue photosynthetic activity
immediately after a light fleck strikes a leaf (post-illumination CO2 assimilation)
(Sharkey et al. 1986; Valladares et al. 1997; Montgomery and Givnish 2008;
Santiago and Dawson 2014). Maximizing carbon gain also depends on the ability to
maintain induction during diffuse-light periods, which is affected by light regime
324 G. Goldstein et al.

and overhead canopy structure. Frequent light flecks will enhance carbon gain
because photosynthetic induction is a function of Calvin cycle enzymes and
build-up of metabolite pools (Sassenrath-Cole et al. 1994).
Drastic changes in solar radiation produced by a gap opening in a forest can
subject understory plants to substantial changes in physiological performance. The
success of the trees under the new light conditions will depend on their phenotypic
plasticity. Light requiring species grow fast and use substantial amounts of light
resources before the gap is closed. Therefore these tree species depend on physi-
ological and morphological attributes enhancing light capture and carbon assimi-
lation. Phenotypic plasticity varies greatly among different species. Generally, high
light requiring trees exhibit larger differences in photosynthetic rates and specific
leaf area between high irradiance and low irradiance growing conditions compared
to shade tolerant species (Fig. 2). In this figure B. densiflora and C. fissillis are light
demanding while L. leucanthus and B. ridelianum are more shade tolerant species.

60
* Amax 10%
Amax 45%
Amax (µmol CO2 m-2 s-1)

45 **
**

30

15

0
* ***
400 ***
**
* ***
g )
-1

300
2
SLA (cm

200

100

0
B. densiflora C. trichotoma L. leucanthus
C. fissilis C. americana B. riedelianum

Fig. 2 Maximum assimilation rate (Amax, n = 3) in the upper panel and specific leaf area (SLA,
n = 6–10 depending on species) in the bottom panel for saplings of six tree species, differing in their
tolerance to the shade, growing under 10 and 45 % growth irradiances (black and gray bars,
respectively). Bars indicate the mean + SE. Values of Amax were obtained from light response curves
with an infrared gas analyzer (CIRAS I, PPSystems). T-tests were performed to assess differences
between growth irradiances within each species (in the case of Amax values obtained from an
asymptotic exponential regression of light response curves were compared). Significant differences at
*P < 0.05 %, ** P < 0.01 *, and *** P < 0.005 are indicated. From Campanello et al. (2011)
Facing Shortage or Excessive Light: How Tropical … 325

Are Shade Tolerant and Light Demanding Tree Species

Two Distinct Functional Groups?

In contrast to acclimation, which occurs within the lifetime of one individual, adaptation
represents gradual genetic change over several generations that result in new fixed
characteristics (Lambers et al. 1998). With regard to photosynthetic adaptations to light
environments, the traits that characterize adaptation to high or low light tend to be
similar to the traits that characterize acclimation to high or low light described above.
Thus tropical and subtropical tree species adapted to high light tend to exhibit relatively
small and thick leaves with high rates of photosynthesis and respiration, whereas trees
adapted to low light tend to exhibit opposite traits. The capacity to survive long periods
under deep shade involves trade-offs in which increased physiological performance
under shade results in a pattern of resource use that favors growth and survival under
limited light, but at the cost of partially restricting capacity to respond to sudden light
increases, and specifically, to grow and survive under high light conditions (Kitajima
1994; Wright et al. 2010). Many types of tropical trees, including light demanding
species, can spend relatively long periods of time under shade, but to complete their
regeneration trajectory they must survive the lack of light on the forest floor, at least
temporarily. Most pioneer tree species can only regenerate in open conditions, such as
large gaps and forest edges, but many can survive variable periods under deep shade
(Popma and Bongers 1988; Clark and Clark 1992). Long-lived pioneers are finally
excluded from the gap phase regeneration process due to shade conditions prevalent in
late successional stages, and are replaced by long-lived tree species that started
regeneration as shade-tolerants (Gómez-Pompa and Vázquez-Yanes 1981).
Regardless of the physiological and morphological adjustments that the leaves of
each species experience under different light environments, species-specific dif-
ferences can be observed even when they are growing under similar environmental
conditions. Maximum photosynthetic rates of leaves exposed to full sun in the
canopy can reflect their light requirements because species-specific differences in
photosynthetic performance are maintained even if measurements are done under
the same environmental conditions. Figure 3 depicts photosynthetic rates of twenty
one species of tropical trees accessible from the canopy crane in San Lorenzo,
Panama (Santiago and Wright 2007), ranked in order of maximum mass-based
photosynthetic rate and classified into shade tolerant or light demanding species
according to Santiago (2010). The data show that classification into shade tolerant
and light demanding species approximates the order of rates, with only one shade
tolerant species having a rate greater than any light demanding species (Fig. 3).
Additionally, across all species, light demanding species as a group had signifi-
cantly greater maximum rates of photosynthesis than shade tolerant species
(t = 4.90; P < 0.0001). Yet, a close view of the differences among species also
demonstrates that species fall along a continuum, and except for the much higher
rates in Ochroma and Cecropia, there are no major jumps in the rates across
species. Similarly, among trees in a subtropical forest in Argentina, species with
higher light requirements also tend to have elevated maximum electron transport
326 G. Goldstein et al.

Fig. 3 Mean maximum photosynthetic rate (Amax) per unit mass (±1 SE) of tree species measured
at the Fort Sherman Canopy Crane, San Lorenzo, Panama, and categorized into shade tolerant
(canopy) or light demanding (pioneer) species according to Santiago (2010) and Santiago and
Wright (2007). Species are ranked in order of increasing values from left to right. The two far right
bars represent the means (±1 SE) of all shade tolerant and light demanding species; means are
significantly different (t = 4.90; P < 0.0001)

+ Machaerium stipitatum
Balfourodendron riedelianum
Allophylus edulis
Inga uruguensis
Lonchocarpus leucanthus
Shade tolerance

Cordia americana
Maclura tinctorea
Cedrela fissilis
Luhea divaricata
Chorisia speciosa
Cordia trichotoma
Peltophorum dubium
Cecropia pachystachya
Bastardiopsis densiflora
Trema micrantha
Solanum granulosum-leprosum
Bauhinia forficata
-
0 25 50 75 100 125 150 175 200 225 250 275 300
ETR max (µmol m -2 s -1 )

Fig. 4 Maximum electron transport rate (ETRmax) estimated from light response curves obtained in
tree saplings of 17 canopy species growing in the field at 100 % irradiance. Species are ranked according
to their shade tolerance. Bars are means + 1SE, n = 4 per species from Campanello et al. (2011)

rates of photosystem II (ETRmax) compared to shade tolerant tree species (Fig. 4).
Again, it is notable that species-specific variation in ETRmax is gradual, ranging
from 75 to 225 μmol m−2 s−1, suggesting that any classification of these species into
two distinct functional groups regarding light adaptations would be arbitrary.
Facing Shortage or Excessive Light: How Tropical … 327

Photosynthetic Adaptations to Contrasting Light

Environments of Closely Related Species

Photosynthetic adaptations to light have rarely been studied in large numbers of

closely related taxa (Robichaux and Pearcy 1980, 1984; Lei and Lechowicz 1997),
and even less so for plants whose distributions along light gradients have been
quantified and whose phylogenetic relationships to each other are known (Givnish
et al. 2004; Santiago and Kim 2009). A study on static photosynthetic light
responses of 11 Lobelia species provides support for predictions of physiological
performance based on economic theory under different growth irradiance (Givnish
et al. 2004). Among Hawaiian lobelias, maximum photosynthetic rate per unit area
increases with average photosynthetic photon flux density (PPFD), as do dark
respiration rates. Species growing under high light environments exhibit high res-
piration rates and therefore require more light to achieve a zero net rate of carbon
uptake and reach maximum photosynthetic rates compared to species growing in
darker habitats (Givnish et al. 2004). Yet, species growing under low light envi-
ronments also achieve higher photosynthetic rates at high PPFD, however the
maximum rates are not as high as species from open habitats. These results suggest
an “adaptive cross-over” in photosynthetic light response, in which shade tolerant
species outperform light requiring species at low light levels with low respiration,
whereas light requiring species have higher photosynthetic performance at high
light levels.
It is interesting that the instantaneous light compensation points (the PPFD at
which net CO2 assimilation is zero) in the Givnish et al. (2004) study range,
depending on the species, from 0.1 to 1.2 % of full sunlight, which is much lower
than the ecological or whole plant compensation points of 1.1–29 % of maximum
incoming solar radiation. Ecological compensation points take into account night-
time leaf respiration, leaf construction costs amortized over leaf lifetimes, and
allocation to non-leaf tissue, assuming identical rates of turnover for leaf and non
leaf tissue (Givnish 1988; Givnish et al. 2004). The ecological compensation points
are substantially closer to the lower limits of PPFD actually experienced by the
lobelia species growing along a gradient of different light conditions, suggesting
that the ecological compensation point can better explain the distribution of plants
under different light conditions than the more traditional instantaneous leaf com-
pensation points obtained from light response curves.

Adjustment in Leaf Optical Properties in Response

to Changes in Light Conditions

Leaves of shade adapted tropical tree species have higher specific leaf area, syn-
thesize less chlorophyll per unit area and use less chlorophyll for capturing the same
amount of PPFD compared with leaves of high light requiring tree species (Lee
328 G. Goldstein et al.

1986). The leaf anatomical properties correlated with increased photosynthetic

efficiency are palisade cells with equal dimension having more chloroplasts on their
abaxial surfaces. This dense layer of chloroplasts maximizes light capture effi-
ciency. The leaves of high light requiring trees have columnar palisade cells making
the chloroplast less efficient in PPFD absorption, but allowing light to reach
chloroplasts in the spongy mesophlyll (Lee 1986).
Leaf accumulation of anthocyanins is also commonly regarded as a photopro-
tection mechanism under high irradiance. Anthocyanins can strongly absorb
blue-green light (Harborne 1988; Barnes et al. 2000). The presence of anthocyanins
in leaves can function as a ‘sunscreen’ to reduce the photons captured by chloro-
phylls (Smillie and Hetherington 1999; Feild et al. 2001; Gould et al. 2002;
Oberbauer and Starr 2002; Gould 2004; Hughes et al. 2005; Hughes and Smith
2007). Anthocyanins are commonly produced during leaf expansion, especially in
tropical plants, and appear to protect expanding leaves from photo-damage when
the photosynthetic apparatus is not fully developed (Zhang et al. 2013b). In addition
to photoprotection, anthocyanins may also function to backscatter light for under-
story plants under light-limiting conditions. Anthocyanins are prevalent on abaxial
leaf surfaces of mature leaves in some understory plants of light requiring tropical
tree species. Lee (1986) hypothesized that the anthocyanin rich cell layers located in
the abaxial leaf surfaces can backscatter transmitted light back to the chloroplasts of
shade adapted tree species growing in the forest understory.

Photoinhibition and Photoprotection of Tropical Canopy

Trees Exposed to High Irradiances

Excessive light energy can cause transient reduction in the photosystem II (PSII)
efficiency and may consequently limit CO2 assimilation in sun-exposed leaves of
the upper canopy, which may have an impact on plant growth. At midday, the
reduction in photosynthetic rate due to midday decline in stomatal conductance that
most species experience (Tenhunen et al. 1987; Zhang et al. 2013a), and high
temperatures can induce a decline in enzyme activity, subjecting canopy leaves to
excessive light energy. Photoinhibition may result in a decline in photosynthetic
rates when leaves are exposed to high light levels that exceed their photon
requirements for photosynthesis. Excessive light can place considerable stress on
the leaf and result in damage to the photosynthetic apparatus. In plants that have
been exposed to high light, the efficiency of photosynthesis decreases because of an
increase in the number of photons absorbed per molecule of CO2 assimilated. This
decline in the quantum yield of PSII can cause both short- and long-term reductions
in CO2 assimilation depending on the extent of the photoprotective recovery and
repair processes (Krause 1988). Among species growing under different light
conditions, species restricted to high light habitats exhibit a higher capacity to
Facing Shortage or Excessive Light: How Tropical … 329

tolerate and recover from light stress than shade tolerant species (e.g. Kamaluddin
and Grace 1992; Johnson et al. 1993).
Shade tolerant trees, however, growing in small size gaps where light levels are
intermediate between full sun and full shade, can avoid reductions in photosynthetic
rates when exposed to high light levels. Acclimation capacity to respond to high
light may be a requirement of shade tolerant plants that need to efficiently utilize
short periods of high light levels in the forest understory or in small gap openings.
Shade tolerant species growing in small gaps of subtropical wet forest in NE
Argentina are less photoinhibited and recover faster than higher light requiring
species (Villagra 2012). For example, shade tolerant Balfourodendron riedelianum
and Euterpe edulis growing in small gaps recovered 90 % of their maximum PS II
efficiency, measured as Fv/Fm (the ratio of fluorescence under the measuring light
and under a light saturation pulse) (Fig. 5). The light requiring tree species Cedrela
fissilis and Maclura tinctoria growing under similar light regimes, on the other hand
only recovered 80 % of their maximum Fv/Fm. It does appear that shade tolerant
tree species growing at intermediate light levels inside the forest have the capacity
to dissipate excess light and to utilize incoming radiation for photosynthesis instead
of undergoing strong photoinactivation and/or downregulation of the PSII, which
might reduce carbon gain.
Some plants avoid absorbing excess radiation through leaf movements, leaf
folding, chloroplast re-orientation and increased reflectance. In particular, light
requiring canopy tree species in subtropical forests can fold their leaves when
exposed to high light (Huang et al. 2012). Leaf folding reduces light absorptance
and consequently helps to reduce the potential damage of PSII. Most plants,
however, rely strongly on biochemical mechanisms to dissipate excess energy and
to avoid damage to photosystems (Bilger and Björkman 1990; Johnson et al. 1993;
Fetene et al. 1997; Demmig-Adams 1998). One of the principal means of photo-
protection occurs through xanthophyll-cycle-dependent energy dissipation under
high light. Photoprotective mechanisms are critical for individuals growing in
sun-exposed sites and for shaded individuals during intense light flecks. Depending
on the species and the habitat of origin, such plants use only 10–50 % of peak
irradiance for photosynthesis (Demmig-Adams and Adams 1996).
Despite the potential negative effects of excess light, considerable inactivation of
PSII in some species can occur under high light conditions without a significant
effect on carbon assimilation. Under high light conditions, the energy absorbed
exceeds the downstream capacity to use that energy (Lee et al. 1999; Kornyeyev
et al. 2006, Adams et al. 2007). Dipterocarpus retusus is one of the tallest tropical
tree species in the world reaching up to 72 m in height in SW China. The leaves of
this species exhibit photosynthetic depression at midmorning in the upper canopy,
and are able to reduce photochemistry and increase heat dissipation during the dry
season (Zhang et al. 2009). Photorespiration in this species plays an important role
330 G. Goldstein et al.

Fig. 5 The Fv/Fm ratios of five subtropical saplings during dark-acclimation (Maximum
efficiency of PSII) and after exposure to saturating light levels (a) and the percentage Fv/Fm dark
recovery (b) after 30 min (bars are means (n = 3)). Fv/Fm of dark-adapted leaves was measured
three times at 5 min intervals after which a saturating beam of actinic light (2,000 μmol m−2 s−1)
was applied for 20 min (dashed line). Recovery of Fv/Fm was measured at a photon flux density of
20 μmol m−2 s−1 over a 30 min period. Different letters indicate significant differences among
species (LSD-Fisher, P < 0.05). Abbreviations are: Ee, Euterpe edulis; Br, Balfourodendron
riedelianum; Ca, Cordia americana; Mt, Maclura tinctoria; Cf, Cedrela fissilis; and Pd,
Peltophorum dubium. Adapted from Villagra (2012)

in photoprotection. The sustained photosynthetic depression in the uppermost-

canopy leaves of these giant trees could be a protective response to prevent
excessive water loss and to avoid catastrophic leaf hydraulic dysfunction without a
large negative effect on photosynthetic gas exchange (Zhang et al. 2009).
Facing Shortage or Excessive Light: How Tropical … 331

Coordination Between Photosynthetic Capacity

and Water-Transport Efficiency in Tree Species
Growing at Different Irradiances

The ability of plants to allocate resources among functions in a coordinated manner

can determine competitive success in a tropical forest where substantial and
unpredictable changes in light environments occur as a result of the opening and
closure of canopy gaps. High water-transport capacity should allow maintenance of
high leaf water potentials, stomatal conductance and consequently support high
photosynthetic carbon assimilation rates (Santiago et al. 2004), especially in
environments with high evaporative demand and solar radiation as commonly
found in canopy openings. A large investment in an efficient water transport system
in the understory of the forest would be non-adaptive as the light levels and
evaporative demand conditions are relatively low and the size of the trees is small.
Dominant subtropical tree species in northern Argentina exhibit different degrees
of coordination between photosynthetic capacity and water transport efficiency
depending on their light requirements. Slow growing shade tolerant species exhibit
lower maximum electron transport rate (ETR) than fast growing species. A positive
correlation between ETRmax and maximum leaf hydraulic conductivity has been
observed in high light requiring species growing at different light levels such as
Cedrela fissilis, Patagonula Americana and Cordia trichotoma: they increase both
ETRmax and hydraulic conductivity with increased growth irradiance (Fig. 6). This
coordinated change in photosynthesis and hydraulic conductivity suggests that the

140

120
ETRmax (µmol m s )
-2 -1

100

80

60

40

2
20 r = 0.81

0.0 0.5 1.0 1.5 2.0 2.5 3.0 3.5

K L (kg s-1 m -1 MPa-1 x 10 -4 )

Fig. 6 Maximum electron transport rate of PSII (ETRmax) versus leaf specific hydraulic
conductivity (KL). A linear regression was fitted to the data. Symbols represent mean values ± SE
for KL and maximum electron transport rates obtained from light response curves for each species
and light treatment. Irradiances of 10, 30, 40 and 65 % of full sun are indicated by black, dark
gray, light gray and open symbols respecievely. Species are Balfourodendron riedelianum
(Triangle down), Cedrela fissilis (circle), Cordia trichotoma (square), Lonchocarpus leucanthus
(diamond) and Patagonula Americana (triangle up). Adapted from Campanello et al. (2008)
332 G. Goldstein et al.

high light requiring species are capable of plastic changes in hydraulic architecture
and water transport efficiency in response to increases in light availability resulting
from the formation of canopy gaps which makes them more competitive in open
habitats. In contrast, the hydraulic conductivity of slower-growing and more shade
tolerant species such as Balfourodendron riedelianum and Lonchocarpus leucan-
thus does not increase with increasing growth irradiance (Fig. 6).

Summary

Irradiance is extremely variable in forest ecosystems with large spatial and temporal
changes, particularly in tropical and subtropical forests. A very low percentage of
the incoming irradiance reaches the forest floor, consisting of diffuse radiation that
is randomly punctuated by short duration light flecks. Consequently understory
plants face a shortage of light energy. Understory plants maximize light capture in
the most efficient way, i.e., at the lowest costs in terms of construction and main-
tenance resulting in relatively low photosynthetic capacity. High light demanding
species, on the other hand, exhibit high photosynthetic capacity. Even though
carbon assimilation increases asymptotically with increasing PPFD, excessive light
can result in photoinhibition of the photosynthetic process. Canopy leaves may
avoid absorbing excess radiation through leaf movements, leaf folding, chloroplast
re-orientation and increased reflectance. Most tree species, however, rely strongly
on biochemical mechanisms to dissipate excess energy and to avoid damage to the
photosystems. Maximum photosynthetic rate per unit area increases with changes in
light growing conditions, from shaded understory to gaps and upper canopy trees,
consistent with increases in dark respiration, leaf mass and photosynthetic capacity
per unit area. High water-transport capacity allows maintenance of high carbon
assimilation in environments with high evaporative demand and solar radiation,
commonly found in canopy openings and in the upper canopy. The ecological
compensation point better predicts the distribution of species along gradients in
light growing condition than the instantaneous photosynthetic points obtained from
traditional light response curves with leaves. Shade adapted and light requiring tree
species from tropical and subtropical rainforests tend to have contrasting life history
traits and leaf photosynthetic characteristics. Most of the species, however fall on
intermediate places along a continuum of light adaptations.

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Carbon Economy of Subtropical Forests

Yong-Jiang Zhang, Piedad M. Cristiano, Yong-Fei Zhang,

Paula I. Campanello, Zheng-Hong Tan, Yi-Ping Zhang,
Kun-Fang Cao and Guillermo Goldstein

Abstract Compared to tropical and temperate forests, subtropical forests have

received little attention in physiological and ecological studies until now, and the
contribution of this ecosystem type to the global carbon cycle has not been fully
assessed. In this chapter we discuss results on the carbon balance of subtropical
forests at different spatial and temporal scales, analyze the potential limitation of
seasonal low temperatures and water deficits on physiological processes of sub-
tropical trees, and characterize the uniqueness of subtropical forest ecosystems in
terms of carbon economy. Results from multiple techniques and scales were
included in the carbon balance assessment. The largest two regions with subtropical
forests are located in Asia and South America. The net ecosystem carbon gain of

Y.-J. Zhang (&)

Department of Organismic and Evolutionary Biology, Harvard University,
Cambridge, MA 02138, USA
e-mail: yongjiangzhang@oeb.harvard.edu
P.M. Cristiano
Laboratorio de Ecología Funcional, Departamento de Ecología Genética y Evolución,
Instituto IEGEBA (CONICET-UBA), Facultad de Ciencias Exactas y Naturales, Universidad
de Buenos Aires, Buenos Aires, Argentina
e-mail: piedad@ege.fcen.uba.ar
Y.-F. Zhang
Department of Geological Sciences, John A. and Katherine G. Jackson School
of Geosciences, University of Texas at Austin, Austin, Texas, USA
e-mail: yongfei@utexas.edu
P.I. Campanello
Laboratorio de Ecología Forestal y Ecofisiología, Instituto de Biología Subtropical,
CONICET, FCF, Universidad Nacional de Misiones, Posadas, Argentina
e-mail: pcampanello@yahoo.com
Z.-H. Tan
Y.-P. Zhang
Key Laboratory of Tropical Forest Ecology, Xishuangbanna Tropical Botanical Garden,
Chinese Academy of Sciences, Mengla, Yunnan 666303, China
e-mail: yipingzh@xtbg.ac.cn

© Springer International Publishing Switzerland 2016 337

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_16
338 Y.-J. Zhang et al.

subtropical forests in these two regions, which have annual precipitations larger
than 800 mm, is probably neither strongly limited by soil water availability nor by
seasonal low temperatures. Relatively low evapotranspiration in the winter/dry
season and high soil water-holding capacity help maintain good water availability
for trees in most subtropical forests. High solar radiation, light penetration and low
ecosystem respiration in winter may compensate for the negative effects of low
temperatures on gross photosynthesis. Therefore, subtropical forests in many areas
can assimilate carbon in excess of respiration throughout the year and they are,
probably, among the largest terrestrial carbon sinks across terrestrial ecosystems
worldwide. In addition, because leaf and ecosystem respiration respond to tem-
perature changes to a larger extent compared to ecosystem carbon assimilation, a
negative relationship between net ecosystem carbon gain and mean annual tem-
perature was found in Asian subtropical and tropical forests. This relationship
suggests that global warming may weaken the carbon sink strength of these forest
ecosystems. These results indicate the important contribution of subtropical forests
to the global carbon cycle and the potentially negative response of these forests to
global warming. We hope this information will promote additional physiological
and ecological research and conservation in subtropical forests.

Keywords Carbon sink
Climate change
Evapotranspiration
Respiration

Water deficit

Introduction

Compared to tropical and temperate forests, the ecological processes of subtropical

forests and the physiology of subtropical trees are less-studied. The largest two
regions with subtropical forests are located in China and Argentina, with some
forests also occurring in North America, Africa and Australia (Fig. 1). In general,
subtropical forests have received relatively little attention in terms of physiological

K.-F. Cao
State Key Laboratory for Conservation and Utilization of Subtropical Agro-Bioresources,
and College of Forestry, Guangxi University, Nanning 530004, China
e-mail: caokf@xtbg.ac.cn
G. Goldstein
Laboratorio de Ecología Funcional, Departamento de Ecología Genética y Evolución,
Instituto IEGEBA (CONICET-UBA), Facultad de Ciencias Exactas y naturales, Universidad
de Buenos Aires, Buenos Aires, Argentina
e-mail: gold@bio.miami.edu; goldstein@ege.fcen.uba.ar
G. Goldstein
Department of Biology, University of Miami, Coral Gables, FL 33146, USA
Carbon Economy of Subtropical Forests 339

Fig. 1 A world forest cover map. Global forest cover derived from MODIS (Moderate Resolution
Imaging Spectroradiometer) with a yearly temporal resolution and a spatial resolution of 0.05°.
Product type vegetation type data (MOD12C1) for 2010. The subtropical zones are indicated

and ecological research until recently (Tan et al. 2012; Zhang et al. 2013b; Cristiano
et al. 2014; Yu et al. 2014). Different from the ‘tropics’ that are clearly defined by
diurnal air temperature variations being substantially larger than seasonal temper-
ature changes, the Subtropical region is not a well-defined area. Subtropical climatic
regimes also occur at high elevations within the tropics. A large portion of the
world’s deserts are also located within the subtropics due to the development of
the subtropical ridge, which is a significant belt of high pressure situated around 30°
latitude in the Northern or Southern Hemisphere. While the limits of subtropical
zones toward the equator (23.4o latitude) are widely accepted, the poleward limits
of the subtropics are controversial and lack a universal agreement; latitudes around
30o–35o, and even 40o have been used to define the northern and southern limits of
the subtropics (Corlett 2013). Unfortunately, the subtropics have been considered
by some authors as a transition zone between the tropical and temperate zones and
not as a distinct climatic zone. In previous studies related to carbon stocks and net
primary productivity (NPP) of worldwide forests, the subtropical forests were often
included together with temperate forests (Pan et al. 2011, 2013).
Subtropical forests have unique ecological characteristics compared to tropical
and temperate forests. Regardless of the latitudinal limits, subtropical climates are
those characterized by seasonal air temperature ranges being relatively similar to
diurnal temperature changes. Compared to typical tropical rainforests with little
climatic seasonality and year-round high temperatures, subtropical forests have mild
winters (Tan et al. 2012; Zhang et al. 2013a; Cristiano et al. 2014) (Fig. 2), which
potentially negatively affect leaf photosynthetic performance (Zhang et al. 2013a)
340 Y.-J. Zhang et al.

500 35 500 35
(a) Xishuangbanna (e) Iguazú
(Marginal tropics) 30 30
400 400 Rainfall
25 Temperature 25
300 20 300 20

200 15 200 15
10 10
100 100
5 5
0 0 0 0
(b) Dinghushan (f) Río Pilcomayo
Month
30 30
400 400
25 25
300 20 300 20

200 15 200 15
Temperature (oC)

Temperature (oC)
10 Rainfall (mm) 10
100 100
Rainfall (mm)

5 5
0 0 0 0
(c) Ailaoshan (g) Pampa del Indio
30 30
400 400
25 25
300 20 300 20

200 15 200 15
10 10
100 100
5 5
0 0 0 0
(d) Maoershan (h) El Rey
30 30
400 400
25 25
300 20 300 20

200 15 200 15
10 10
100 100
5 5
0 0 0 0
J F M A M J J A S O N D J F M A M J J A S O N D
Month

Fig. 2 Seasonal dynamics in average air temperature and precipitation of subtropical forests and a
forest in the marginal Asian tropics (Xishuangbanna). Circles are monthly average air
temperatures; bars are average monthly precipitation. Xishuangbanna data from Xishuangbanna
Tropical Rainforest Ecosystem Station, China. Ailaoshan data from Ailaoshan Station for
Subtropical Forest Ecosystem Studies, China and (Qiu and Xie 1998). Dinghushan data from
Huang et al. (2011), and Maoershan data from Bai et al. (2010). Iguazú, Río Pilcomayo, Pampa del
Indio and El Rey data from Meteorological Stations in Argentina (Cristiano et al. 2014; Cristiano
unpublished data)
Carbon Economy of Subtropical Forests 341

and ecosystem carbon gain. However, there is some evidence that mild winters have
little impact on tree growth, as depicted by high Normalized Difference Vegetation
Index (NDVI) values observed throughout the year, and by high ecosystem net
carbon assimilations measured during winters on subtropical forests (Tan et al. 2012;
Cristiano et al. 2014). Further, plant species composition and leaf and flower phe-
nology of subtropical forests tend to be more similar to tropical forests compared to
temperate forests (Qiu and Xie 1998).
Subtropical forests are a strong carbon sink potentially contributing greatly to
global forest carbon sequestration. A few recent studies have suggested that these
forests assimilate carbon all-year-round with high canopy photosynthetic rates and
high ecosystem carbon sequestration (Tan et al. 2011, 2012; Cristiano et al. 2014;
Yu et al. 2014). For instance, an old-growth subtropical forest in Ailaoshan,
Southwest (SW) China is the largest carbon sink (*9 t ha−1 year−1; estimated by
eddy covariance method) among all Asian ecosystems studied so far, including
tropical, subtropical, and temperate forests, croplands, wetlands, and grasslands
(Chen et al. 2013). Further, because the subtropics are geographically in the tran-
sition zone between tropical and temperate zones, understanding the ecological and
physiological mechanisms controlling the carbon sink strength of subtropical for-
ests could provide some hints for predicting the future of temperate forests during
global warming.
Despite the potentially important role of subtropical forests in the global carbon
cycle, their carbon economy and the controlling environmental, ecological, and
physiological factors are poorly-understood, and have attracted little attention until
now. In this chapter, we summarize published results on leaf and ecosystem level
carbon exchange of subtropical forests (Table 1 and those in Chen et al. 2013),
analyze the limiting effects of water and temperature on carbon economy of sub-
tropical forests, and assess the potential for subtropical forests to be among the
largest terrestrial carbon sinks across all terrestrial ecosystems. Here we focus on

Table 1 Major subtropical forest ecosystems in Southern China and Northern Argentina,
including a tropical forest at the northern limit of the Asian tropics, used in this chapter, and their
location, elevation, mean annual temperatures (MAT), and mean annual precipitation (MAP)
Forest name Latitude Longitude Elevation (m) MAT (°C) MAP (mm)
China
Xishuangbanna (Marginal tropics) 21° 41′ N 101° 25′ E 570 21.7 1560
Dinghushan 23° 10′ N 112° 32′ E 240 21.0 1956
Ailaoshan 24° 32′ N 101° 01′ E 2460 11.3 1931
Maoershan 25º 50′ N 101º 49′ E 1500 10.8 2510
Argentina
Iguazú 26° 25′ S 54° 37′ W 193 21.0 2000
Río Pilcomayo 25° 10′ S 58° 90′ W 57 22.6 1260
Pampa del Indio 26° 15′ S 60° 00′ W 80 21.5 827
El Rey 24° 40′ S 64° 40′ W 1500 19.5 1251
342 Y.-J. Zhang et al.

Asian and South American subtropical forests because they account for the largest
proportion of worldwide subtropical forests (Fig. 1). Although the poleward lim-
its for subtropical forests could vary depending on regional geography (e.g. ele-
vation) and climate (Zhang 1989; Ni and Song 1997), here we adopted the
poleward limits of 30.0° as this is the most conventional and convenient definition
(Corlett 2013).

Water Limitation of Carbon Economy

Does water availability limit carbon gain of subtropical forests? Since many sub-
tropical forests are characterized by a seasonal decrease in monthly precipitation
(Fig. 2), seasonal water deficits could be a limiting factor for ecosystem carbon
gain. Water deficits negatively affect leaf photosynthesis through lowering stomatal
conductance and by limiting CO2 supply to the Calvin Cycle (Flexas et al. 2001).
At a global scale, ecosystem net primary productivity (NPP) is positively correlated
with annual precipitation across different terrestrial ecosystems (Lieth 1975;
Michaletz et al. 2014). The most humid south American subtropical forests showed
year-round high precipitation with no apparent dry season, thus canopy photo-
synthesis and ecosystem carbon assimilation of these subtropical forests in South
America is probably not substantially influenced by seasonal water deficits
(Cristiano et al. 2014). These humid subtropical forests are located in northeastern
Argentina (Misiones Province) and also along the eastern slopes of the Andes
Mountains in northwestern Argentina, a region locally known as Las Yungas. Both
areas are rainy, humid, and have mild winters, with some eastern slope Andean
subtropical forests having a dry season with substantial fog (El Rey). Between these
two humid forests, there are large regions with seasonally humid subtropical forests
(also known as humid Chaco) and dry subtropical forests (also known as arid
Chaco). We have included in this chapter information on the humid subtropical
forests and the seasonally dry subtropical forests (Fig. 2 right panels). Arid Chaco is
not included in the current analysis because it has regular frosts during the winter
and its annual precipitation is lower than 800 mm. Arid Chaco also has strong
floristic affinities with temperate ecosystems, while seasonally humid Chaco has
strong floristic affinities with neotropical forests (Pennington et al. 2000).
Influenced by the Asian summer monsoon (the East Asian Monsoon and Indian
Monsoon), the Asian subtropics are characterized by a warm and wet summer and a
cold and dry winter. During the dry season, precipitation of the Asian subtropical
forests can be low (Dinghushan, Ailaoshan, and Moershan, Fig. 2). For example,
Ailaoshan has 6 months with rainfall <100 mm (Fig. 2c). No evidence of water
deficits, however, has been found in the dry season in high elevation subtropical
forests in Southwest China (Ailaoshan, see Table 1). The dry season predawn leaf
water potentials of all 10 tree species studied are close to zero, ranging from −0.07
to −0.16 MPa (Zhang et al. 2013a). Further, even during a once-in-a century
regional drought event (*half year without rains; 2009–2010), trees in the
Carbon Economy of Subtropical Forests 343

Ailaoshan subtropical forest showed no symptoms of drought stress and still

maintained predawn leaf water potential very close to zero (Qi et al. 2012, 2013).
Indeed, the soil layers where the roots are mainly distributed were able to maintain
high water availability (soil water potential >−0.5 MPa) during the driest period of
the 2009–2010 drought event. High capacity of the Ailsoshan subtropical forest in
buffering rainfall shortages has been attributed to its high soil water-holding
capacity, which is distinctly higher than that of some plantations, shrub lands, and
secondary forests in this region (Qi et al. 2012). Although it is still unknown
whether other subtropical forests have high soil water-holding capacity and can
effectively buffer the effects of seasonal rainfall shortages, it is very likely that water
availability is not a strong limiting factor on net ecosystem carbon exchange
(NEE) of most Asian and Argentinean subtropical forests.
Limited impact of seasonal rainfall shortage on NEE of subtropical forests is
supported by the seasonal dynamics in NDVI of these forests. The NDVI is a
spectral index that estimates the amount of green biomass and thus is related to the
rate of ecosystem net CO2 assimilation level and net productivity. Satellite-based
NDVI (or the enhanced vegetation index, EVI) has been used to assess canopy
carbon exchange (Cristiano et al. 2014) and predict forest NPP or NEE (Xiao et al.
2004; Campos et al. 2013). The NDVI of some Asian subtropical forests in the
driest months (e.g. December to April for Ailaoshan, September to November for
Maoershan, Fig. 2) is higher than that of the rainy season (Fig. 3a). The most humid
Argentinean subtropical forest (Iguazú, 2000 mm annual precipitation) exhibits a
constantly high NDVI pattern while the other three subtropical forests of Northern
Argentina with seasonal declines in precipitation exhibit only small declines in
NDVI during the winter/dry season (Fig. 3b). The decrease could be the result of
lower temperature effects on photosynthesis, decrease in leaf area index during this
period, and/or drought effects on plant metabolism. Notably, the dry season coin-
cides with the winter in both the Asian and Argentinean subtropics. Since evapo-
transpiration is positively correlated with air temperature (Kosa 2009, and Fig. 4),
winter evapotranspiration is much lower than that of the summer for subtropical
forests (Fig. 4a). The winter/dry season evapotranspiration of four Argentinian
subtropical forests is only about 23–53 % of that of the summer/wet season
(Fig. 4a). Lower winter ecosystem evapotranspiration could help in water conser-
vation during the winter/dry season, and thus partially compensate for the negative
effects of rainfall shortages on tree carbon assimilation.

Is Seasonal Low Temperature a Limiting Factor?

Is the carbon gain of subtropical forests limited by seasonal low temperatures? The
answer is yes and no. Compared to typical temperate forests with strong seasonal
changes in air temperatures, winter is generally mild and the seasonality of tem-
perature or NDVI is weaker (Fig. 5). Trees in subtropical forests are exposed to
344 Y.-J. Zhang et al.

Fig. 3 MODIS NDVI 1.0

seasonal dynamics (a)
(Normalized Difference 0.9
Vegetation Index) of
subtropical forests and a
0.8
tropical forest at the marginal
tropics (Xishuangbanna).
Error bars represent standard 0.7
errors of the values.
Xishuangbanna, Ailaoshan, 0.6
Maoershan data from Zhang Xishuangbanna
and Zhang (unpublished 0.5 Ailaoshan
data). Iguazú data from Maoershan
NDVI
Cristiano et al. (2014). Río 0.4
Pilcomayo, Pampa del Indio
(b)
and El Rey data from 0.9
Cristiano (unpublished data)
0.8

0.7

0.6
Iguazú
Río Pilcomayo
0.5 Pampa del Indio
El Rey
0.4
JAN
FEB
MAR
APR
MAY
JUN
JUL
AUG
SEP
OCT
NOV
DEC
Month

mild seasonal low temperatures, which can negatively affect leaf photosynthesis in
several ways. Low temperatures can directly inhibit photosynthetic enzyme activ-
ities (Holaday et al. 1992; Kingston Smith et al. 1997), increase the probability of
photoinhibition (Levitt 1980; Allen and Ort 2001; Huang et al. 2010), reduce
stomatal conductance (Allen and Ort 2001; Zhang et al. 2014), and increase car-
bohydrate concentration (high sink effect) in leaves consequently inhibiting pho-
tosynthesis (Azcon-Bieto 1983). In forests with subzero temperatures, freeze-thaw
cycles could cause xylem embolism (blocking of xylem conduits by air bubbles)
(Davis et al. 1999) slowing down water transport and consequently limiting pho-
tosynthesis (Taneda and Tateno 2005). Based on field measurements, leaf net
photosynthetic rates of well-irrigated trees and shrubs at the northern limit of Asian
tropics declined 28–44 % in the cool season, and that of trees from three warm
subtropical forests declined by 20–30 % (Table 2). The winter decline in leaf net
photosynthetic rate could be as high as 81 % in cold subtropical forests such as that
in Maoershan, China, which has an average air temperature of 0 °C in the coldest
month (elevation 1500 m; Table 2).
Carbon Economy of Subtropical Forests 345

Fig. 4 a Monthly average 8

evapotranspiration estimated (a)

Evapotranspiration (mm day )

using the MODIS product

-1
Iguazú
MOD16A2, for four 6 Río Pilcomayo
subtropical forests in Pampa del Indio
Argentina, and b monthly El Rey
average evapotranspiration in
relation to mean monthly air 4
temperature. The relationship
between evapotranspiration
and air temperature was fitted 2
by a linear regression. Data
from Cristiano et al.
(unpublished data) 0

JAN
FEB
MAR
APR
MAY
JUN
JUL
AUG
SEP
OCT
NOV
DEC
Month

8
(b)
Evapotranspiration (mm day )
-1

6 2
R = 0.73 (P < 0.001)

0
10 15 20 25 30
Temperature (oC)

The negative effects of seasonal low temperatures on ecosystem carbon gain

coincide with a decrease in total leaf surface area during the winter. The leaf area
index (LAI) of an Asian and a South American subtropical forest declined signif-
icantly in winter (Fig. 6). The winter decline in LAI is mainly the result of leaf drop
of winter-deciduous trees (Cristiano et al. 2014). The subtropical forests in South
America and Asia are evergreen dominated forests mixed with some deciduous tree
species (occasionally dominated by deciduous species) (Bai et al. 2010; Chen et al.
2013; Zhang et al. 2013b; Cristiano et al. 2014).
Subtropical forests have ecosystem and leaf level mechanisms to compensate for
the negative effects of seasonal low temperatures on leaf photosynthesis. First of all,
although leaf drop of deciduous trees decreases total leaf surface area, it can
increase the light penetration through the canopy and increase the light interception
of lower canopy leaves, sub-canopy trees, as well as understory saplings and shrubs
(Miyazawa and Kikuzawa 2005; Cristiano et al. 2014). Second, increased leaf
346 Y.-J. Zhang et al.

0.8

0.6
NDVI

0.4
N. subtropical forests
N. temperate forests
S. subtropical forests
0.2 Tropical forests

MAY

SEP
FEB

MAR

APR
JAN

AUG

NOV
JUL

OCT

DEC
JUN
Month

Fig. 5 Seasonal dynamics in MODIS NDVI (Normalized Difference Vegetation Index) of forests
of different climatic zones. Forests were identified according to MODIS vegetation type data
(Moderate Resolution Imaging Spectroradiometer; product type vegetation type data (MOD12C1)
for 2010). Data from Zhang and Zhang (unpublished data)

Table 2 Summer and winter leaf net photosynthetic rates of trees from a marginal tropical forest
(Xishuangbanna) and three subtropical forests (Dinghushan, Ailaoshan, Maoershan) in Southern
China. Values are means ±SEs
Leaf net photosynthetic Percent decline (%)
rate (μmol m−2 s−1)
Summer Winter
Xishuangbanna (native species, n = 3) 12.6 ± 1.4 7.3 ± 2.1 44
Xishuangbanna (introduced species, n = 9) 9.7 ± 1.0 7.2 ± 1.6 28
Dinghushan (native species, n = 4) 8.0 ± 0.1 6.4 ± 0.4 20
Ailaoshan (native species, n = 10) 11.4 ± 0.4 7.9 ± 0.3 30
Maoershan (native species, n = 4) 10.0 ± 0.5 1.9 ± 0.3 81
Data source Xishuangbanna (Zhang et al. 2014), Dinghushan (Zhang and Ding 1996), Ailaoshan
(Zhang 2012; Zhang et al. 2013a), Maoershan (Bai et al. 2010)

chlorophyll concentrations of trees could partially compensate for the negative

effects of low temperatures on LAI and leaf photosynthetic capacity as observed in
a South American subtropical forest (Cristiano et al. 2014). Third, in the case of
Asian subtropical forests, solar radiation is higher and sunshine duration is longer in
autumn and winter seasons compared to summer owing to less frequent rain and fog
events, which can also compensate for the negative effects of seasonal low tem-
peratures on photosynthesis (Zhang et al. 2013b). Lastly, in humid subtropical
forests in Argentina, winter daytime temperatures are within the range of optimum
temperature for CO2 assimilation of trees (Goldstein, unpublished information).
Carbon Economy of Subtropical Forests 347

Fig. 6 Seasonal dynamics in 10.0

leaf area index (LAI) of two (a)

Field measured leaf area index

subtropical forests. a Field
8.0
measured LAI in summer and
winter of Ailaoshan and Summer
Iguazú subtropical forests. 6.0 Winter

(m m )
-2
b Average monthly
MODIS LAI of Iguazú. Data

2
4.0
source; Ailaoshan data from
Qi et al. (2013), Iguazú data
from Cristiano et al. (2014) 2.0

0.0
Ailaoshan Iguazú
Forest

7.0
(b) Iguazú
6.5
MODIS leaf area index

6.0
(m m )
-2

5.5
2

5.0

4.5

4.0
MAY
MAR

SEP
FEB

APR

AUG

NOV
OCT

DEC
JAN

JUN
JUL

Month

To summarize, the leaf photosynthesis and gross ecosystem carbon exchange

(GEE) of subtropical forests are negatively affected by seasonal low temperatures,
but subtropical forests have many tree and ecosystem level adaptations to
compensate for low temperature effects. Then the question is to what extent trees
and ecosystems can maintain net carbon gain during winters. The trees in the high
elevation Ailaoshan subtropical forest (SW China), where average monthly winter
temperature drops to 5 °C, maintained considerably high winter carbon assimilation
rates (5.4–8.8 mol m−2 s−1) and the estimated winter carbon gain (by photosynthetic
light response curves and PPFD dynamics) accounts for *30 % of the yearly net
carbon gain of the evergreen broadleaf tree species (Zhang 2012; Zhang et al.
2013b). Indeed, substantial winter carbon gain by the evergreen broadleaf trees,
which is the dominant growth form in these forests, helps them to maintain high net
yearly carbon gain compared to deciduous species. Interestingly, a deciduous
species extends the leaf senescence process to facilitate photosynthetic carbon
assimilation during part of the winter period (Zhang et al. 2013b), possibly as a
348 Y.-J. Zhang et al.

Fig. 7 Seasonal dynamics in 6

net ecosystem CO2 (a)
assimilation of two Asian
4
subtropical forests and one
forest located at the northern
limit of the Asian tropics. 2
Data for Ailaoshan and
Dinghushan subtropical
0
forests are from Tan et al.
(2012), and data for

Monthly average net ecosystem

CO2 assimilation (µ mol m-2 s -1)
Xishuangbanna -2
tropical-subtropical forest are Xishuangbanna
Ailaoshan
from Zhang et al. (2010).
Error bars are standard errors -4

JAN
FEB
MAR
APR
MAY
JUN
JUL
AUG
SEP
OCT
NOV
DEC
of the values in each month
6
(b)
4

-2
Dinghushan

-4
JAN
FEB
MAR
APR
MAY
JUN
JUL
AUG
SEP
OCT
NOV
Month DEC

result of the selective pressures favoring year round carbon assimilation. At the
ecosystem level, some subtropical forests can maintain high winter NEE compa-
rable to that of the summer season (Tan et al. 2011, 2012) (Fig. 7). The NEE of
the Ailaoshan subtropical forest is constantly high throughout the year (Fig. 7a),
while the NEE of the Dinghushan subtropical forest is even higher in winter than in
summer (Fig. 7b).

Why Are Subtropical Forests Among the Largest

Carbon Sinks?

High year-round leaf photosynthesis and net ecosystem carbon exchange or carbon
gains (NEE) (Fig. 7) suggest that subtropical forests are large carbon sinks. This
prediction has been supported by eddy covariance data. At least in Asia, NEE of
subtropical forests are among the highest of Asian ecosystems and are generally
Carbon Economy of Subtropical Forests 349

higher than that for tropical and temperate forests (Fig. 8) (Chen et al. 2013; Yu
et al. 2014). In general, NEE of Asian forests increases with latitude from 0 to 28°
N and declines as latitude further increases from 28° N (Fig. 8a). Therefore the
maximum NEE of Asian forests is achieved in the subtropical zone (indicated as the
shaded area of Fig. 8a).
Different responses of respiration and photosynthesis to temperature may explain
the high carbon sink strength of subtropical forests. Plant tissue and soil respiration
are very sensitive to changes in temperature (Atkin and Tjoelker 2003; Cavaleri
et al. 2008; Tan et al. 2012; Slot et al. 2013). Across Asian tropical and subtropical
forests, both gross ecosystem carbon exchange (GEE) and net ecosystem respiration
increase exponentially with increasing mean annual temperature (MAT; Fig. 9).
However, ecosystem respiration increases at a faster rate with increasing MAT than
GEE, resulting in a negative relationship between NEE as a function of increasing
MAT (Fig. 9). The relationship between NEE and MAT is well-described by a
linear regression; NEE decreases as MAT increases and approaches zero at a MAT
of 25.8 °C (Fig. 9). Above this temperature threshold the forests are sources (rather
than sinks) of the main greenhouse gas (CO2). This pattern is also supported by

Fig. 8 Net annual ecosystem 1200

carbon gains of Asian forests (a)
Net ecosystem carbon gain

1000
in relation to latitude (a) and R2 = 0.47
mean annual temperature (b). 800 (P < 0.001)
(g C m -2 year -1)

Data from Tan et al. (2012)

600
and Chen et al. (2013). All
forest types were included. 400
The solid black lines indicate
200
Gaussian equations fitted to
the data; y = a + b × e−0.5 [(x 0
−c)/d]^2
. The blue and red
-200
break lines are 95 % Subtropical zone
confidence bands and 95 % -400
0 10 20 30 40 50 60 70
prediction bands,
o
respectively. The shaded area Latitude ( N)
in (a) indicates the subtropical
zone 1200
(b)
Net ecosystem carbon gain

1000
R2 = 0.44
800 (P < 0.001)
(g C m -2 year -1)

600

400

200

-200

-400
-10 0 10 20 30
Mean annual temperature (oC)
350 Y.-J. Zhang et al.

Gross ecosystem carbon gain

Net ecosystem carbon gain
Ecosystem respiration
5000
Ecosystem carbon exchange

4000
(g C m-2 year-1)

3000
Sink
Source
2000

1000

-1000
10 15 20 25 30
Mean annual temperature (oC)

Fig. 9 Gross ecosystem carbon gain, net ecosystem carbon gain, and ecosystem respiration of
Asian subtropical and tropical forests in relation to mean annual temperature (MAT). Data from
Tan et al. (2012) and Chen et al. (2013). Subtropical forests include Ailaoshan, Dinghushan,
Chilanshan, Qianyanzhou, and Huitong. Tropical forests include Pasoh, Lambir, Sakaerat, Mae
Klong, and Xishuangbanna. Solid symbols are gross ecosystem carbon gain; grey circles are net
ecosystem carbon gain; open circles are ecosystem respiration. The relationships between gross
ecosystem carbon gain and MAT, and between ecosystem respiration and MAT were fitted with
exponential regressions. The relationship between net ecosystem carbon gain and MAT was fitted
with a linear regression

field measurements in Ailaoshan. Low temperatures in winter caused a 30 %

decline in leaf photosynthetic rate of trees in Ailaoshan (Table 2), but at the same
time resulted in a 62.9, 38.1 and 46.6 % decline in leaf, stem and soil respiration,
respectively (Table 3). Higher declines in tree and soil respiration than photosyn-
thesis contribute to the high winter carbon sequestration of the Ailaoshan sub-
tropical forest. In addition, the young forest ages and high nitrogen deposition are

Table 3 Summer and winter Respiration rate Percent decline

respiration of a subtropical (μmol m−2 s−1) (%)
forest on Mount. Ailaoshan,
Summer Winter
Southwest China
Leaf dark 1.03 0.38 62.9
respiration
Tree trunk 0.85 0.53 38.1
respiration
Soil respiration 4.37 2.33 46.6
Data source leaf respiration data from Zhang (2012), tree trunk
respiration data from Hu (2010), and soil respiration data from
Tan et al. (2012)
Carbon Economy of Subtropical Forests 351

also factors contributing to the high NEE of the Asian subtropical forests (Yu et al.
2014). Compared to Asian tropical and temperate forests, Asian subtropical forests
are generally younger and show significantly higher nitrogen deposition, both of
which are positively related with forest net productivity (Yu et al. 2014).
In contrast to the Asian subtropical forests that have constantly high NEE
throughout the year (Tan et al. 2012), a forest at the northern limit of the Asian
tropics (Xishugangbanna) is a carbon sink in the cool season, but a carbon source
during the warm season (Zhang et al. 2010) (Fig. 7), resulting in its lower annual
net carbon gain (168.83 g C m−2 year−1) compared to the subtropical forest in the
same region (Ailaoshan; 976.15 g C m−2 year−1). Indeed, Xishugangbanna has
higher NDVI than Ailaoshan does in all seasons (Fig. 3a). It also has higher annual
GEE (2342.67 g C m−2 year−1) than Ailaoshan has (1848.33 g C m−2 year−1).
However, high warm season temperatures result in a much higher annual ecosystem
respiration in Xishuangbanna (2173.83 g C m−2 year−1) than in Ailaoshan
(871.68 g C m−2 year−1) (Zhang et al. 2010), which weakens its carbon sink
strength. Therefore, respiration is the main factor determining the strength of carbon
sinks of the Asian subtropical and tropical forests.
A global data synthesis has shown that the net ecosystem primary productivity
(NPP) estimated by forest inventory (including stem, root and foliage growth) is
positively correlated with MAT (Michaletz et al. 2014). It is possible that the forest
inventory method has not taken the soil carbon stock into account, whose respi-
ration accounts for a large proportion of the forest respiration and it is a very
sensitive process which increases substantially as temperature increases (Tan et al.
2012). The forest inventory method may underestimate the carbon sink strength of
the subtropical forests, e.g., the NPP of Ailaoshan subtropical forest estimated by
forest inventory is 3–4 t ha−1 year−1 less than the NEE estimated by eddy
covariance (Tan et al. 2011). More mechanistic studies are needed to address these
differences and to better understand processes that are responsible for the
differences.

Potential Responses of Subtropical Forests to Warming

Warming may weaken the carbon sink strength of subtropical forests. In the Asian
tropics and subtropics, forest net carbon exchange or carbon gain (NEE) is nega-
tively correlated with mean annual temperature (MAT; Fig. 9). Therefore, predicted
global warming in the future (IPCC 2007) probably will reduce the net carbon
sequestration strength of the subtropical forests. Since the ecosystem respiration
dominates the forest NEE responses to MAT, higher increases in ecosystem res-
piration than in carbon assimilation will weaken the carbon sink strength and even
turn the carbon sinks into sources (Fig. 9). According to the temperature response of
respiration and carbon assimilation or GEE, the optimum MATs for NEE are
between 11 and 15 °C, and further increase in MAT above 25.8 °C will turn the
forests from carbon sinks to sources (Fig. 9). Although NEE of a forest can
352 Y.-J. Zhang et al.

acclimate to changes in temperature (Yuan et al. 2011), the NEE of the forests used
for NEE versus MAT analysis in this chapter are values of trees acclimated to the
temperature regimes at each specific location. Thus the negative relationship
between NEE and MAT found in Asian subtropical and tropical forests (Fig. 9)
suggests that the temperature related decline has a strong potential to affect the
carbon sink strength of these forests.
These predictions are consistent with tree growth studies in Australian sub-
tropical and temperate forests. The optimum MAT for growth of Australian sub-
tropical and temperate eucalyptus forests is around 11 °C. Because the current
MAT of most Australian eucalyptus forests is above 11 °C, it is predicted that
warming will decrease their growth and carbon sink strength (Bowman et al. 2014).
It is possible that global warming may shift the temperate forests bordering the
subtropics into subtropical forests and turn them into substantial carbon sinks. In
addition, it is still unknown whether potentially positive effects of increased
atmospheric CO2 concentration and nitrogen deposition related to anthropogenic
climate change would be able to compensate for the negative effects of warming on
ecosystem net carbon gain.

Final Remarks

By analyzing the current results on carbon balance of subtropical forests, we hope

to provide a better assessment on the potentially large contribution of subtropical
forests to the global carbon cycle. We acknowledge that leaf, tree and ecosystem
level mechanistic studies have only been conducted in a few forests of the sub-
tropical region, preventing us from getting a comprehensive carbon economy map
for all subtropical forest ecosystems. With the information obtained so far, how-
ever, we can conclude that high photosynthesis and carbon sequestration and rel-
atively low respiration explain why subtropical forests are among the largest
terrestrial carbon sinks of the world. A higher sensitivity of respiration than pho-
tosynthesis to low temperatures contributes to their high carbon sink strength
throughout the year. Therefore, the subtropical forests may highly impact the global
carbon cycle, calling for global attention on subtropical forests and indicating the
importance of preserving these ecosystems for their buffering power of industrial
carbon emissions.

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The Ecophysiology of Leaf Lifespan
in Tropical Forests: Adaptive and Plastic
Responses to Environmental
Heterogeneity

Sabrina E. Russo and Kaoru Kitajima

Abstract Leaf lifespan, the time from leaf expansion to shedding, exhibits wide
variation and is a key integrator of relationships with photosynthetic rate, leaf mass
per area (LMA), and leaf nitrogen among coexisting tropical tree species. We
present a hierarchical view of sources of variation in leaf lifespan in tropical forests,
emphasizing the importance of substantial within-species variation, which has
rarely been addressed. Interspecific variation in leaf lifespan is positively correlated
with LMA, varying from short-lived, low-LMA leaves to long-lived, high-LMA
leaves of species associated with resource-rich versus resource-depleted habitats,
respectively. Phenotypic responses of leaf lifespan and LMA to light show
counter-gradient variation: with acclimation to shade, leaf lifespan increases, and
LMA decreases, but both increase with adaptation to shade. In contrast, phenotypic
responses to soil fertility are predicted to show co-gradient variation: both leaf
lifespan and LMA increase with declining fertility both inter- and intraspecifically.
We present new data analyses supporting these predictions, but the interactive
effects of light and soil resources can produce complex phenotypic responses.
Future studies of leaf lifespan should devote more attention to within-species
variation to better quantify and explain how leaf lifespan is central to trade-offs
generating the contrasting ecological strategies of tropical tree species.

S.E. Russo (&)

School of Biological Sciences, University of Nebraska, Lincoln, USA
e-mail: srusso2@unl.edu
K. Kitajima
Graduate School of Agriculture, Kyoto University, Kyoto, Japan
e-mail: kaoruk@kais.kyoto-u.ac.jp
K. Kitajima
Smithsonian Tropical Research Institute, Balboa, Panama

© Springer International Publishing Switzerland 2016 357

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_17
358 S.E. Russo and K. Kitajima

Introduction

Leaf lifespan, the duration of time between when a leaf is first expanded and when
it is senesced from the plant, differs greatly among species, among individual
plants, and also among leaves on a plant (Chabot and Hicks 1982). Since the leaf is
the principal photosynthetic organ of higher plants, its lifespan determines how
long it will return photosynthetically fixed carbon to the plant (Kikuzawa and
Lechowicz 2011). Plant growth and survival are critically dependent upon cumu-
lative net photosynthetic carbon gain, which in turn depends strongly not only on
insolation, but also on the availability of nutrients, especially nitrogen, and water in
soil (Field 1983). Thus, leaf lifespan and nutrient allocation patterns are function-
ally linked (Ackerly and Bazzaz 1995; Hikosaka 2005), making leaf lifespan a
critically important trait mediating the carbon and nutrient economies of plants that
ultimately translate into fitness variation in relation to environmental heterogeneity.
Leaf lifespan is one axis of variation in the worldwide leaf economic spectrum
(WLES), which describes a spectrum of coordinated leaf functional trait variation
ranging from fast-growing species that produce short-lived, structurally inexpensive
leaves with high nutrient concentrations and high photosynthetic productivity to
slow-growing species that produce longer-lived, structurally expensive leaves that
have lower nutrient concentrations and photosynthetic rates (Reich et al. 1991, 1992,
1997; Wright et al. 2004). Recent analyses of leaf lifespan using increasingly larger
databases tend to focus on site and species-level means, neglecting large
within-species variation, even though it can be substantial (Westoby et al. 2002). As a
result, our knowledge of within-species variation in leaf lifespan in relation to dif-
ferences in resource availability and other plant functional traits, at both the indi-
vidual and leaf-levels, is comparatively rudimentary. The ability of a plant to respond
to environmental shifts through acclimation will in part dictate responses to climate
change, as well as determine patterns of species distribution along environmental
gradients (e.g., Vanderwel et al. 2015). Furthermore, an integrated understanding of
how multiple sources of natural selection operate on leaf lifespan in relation to the
evolution of diverse plant ecological strategies (Donovan et al. 2011) requires
quantitative estimates of how leaf lifespans change with environmental variation.
In this review, we seek to call attention to within-species variation in leaf
lifespan, some of which can be understood as optimal plastic responses. We focus
on tropical forests, where tree species display a wide range of leaf lifespans,
including very long-lived leaves. First, we present a hierarchical view of the sources
of variation in leaf lifespan and the dynamic underlying physiological mechanisms
that influence how lifespan affects a plant’s carbon and nutrient economies. Then,
we discuss within-versus among-species variation in leaf lifespan and leaf mass per
area (LMA) that can be related to variation in light availability and soil fertility
from the perspective of theories on optimal leaf lifespan. We show that the direction
and strength of the relationship of leaf lifespan with LMA differ among versus
within-species, depending on the type of environmental factors considered. In the
last section, we discuss knowledge gaps and research questions that are worth
The Ecophysiology of Leaf Lifespan in Tropical Forests … 359

pursuing toward a more mechanistic understanding of leaf lifespan in the carbon

and nutrient economies of the whole-tree.

Theories of Optimal Leaf Lifespan

Cost-benefit theories of leaf lifespan have a long history (e.g., Chabot and Hicks
1982). Here, we limit our review to the essential ideas needed for understanding the
key elements of optimization of leaf function that have resulted in the global
diversity and distribution of leaf lifespans and leaf habits. The fundamental question
addressed by optimal leaf lifespan models is, for how long should a tree retain its
leaves in a given environment? The optimal answer depends on the costs of leaf
construction and maintenance, as well as costs associated with leaf turnover, versus
the benefits that the leaf provides, namely photosynthetically fixed carbon and
nutrient storage. Table 1 summarizes potential key costs and benefits, which will be
described throughout this chapter. The cost of leaf construction is the total cost of
acquiring all energy and materials required to build a leaf and its supporting organs
(e.g., stem), as well as the cost of the maintaining molecules that make up the leaf
(e.g., respiration). However, given the difficulty of assessing some of these costs,
what is generally quantified is a minimum leaf construction cost, estimated as the
total chemical bonding energy in organic molecules multiplied with a factor for
biosynthetic pathway costs (Williams et al. 1987; Poorter et al. 2006). Per unit dry
mass, this minimum biosynthetic cost of leaf construction may not differ much
among species (Griffin 1994). Hence, leaf construction cost per unit area is
approximated by LMA, and leaves with higher LMA require either fast photo-
synthetic rates or long lifespan to pay back construction costs and generate a net
carbon gain.
Since the target of natural selection is individuals, optimization of carbon gain
relative to carbon and nutrient costs must be considered at the whole-plant level,
even though ecophysiological analyses, including many that we review here, often
treat leaves as the unit of study. Leaves are expensive to manufacture: large
amounts of limited resources such as nitrogen and phosphorus, as well as carbon to
construct systems for structural support, vascular transport, and belowground
resource uptake, must be allocated for their construction (Givnish 1988; Williams
et al. 1989; Kikuzawa and Ackerly 1999; Reich et al. 2009). Thus, how many
leaves a plant should maintain at a given time reflects a dynamic optimization of
maximizing benefit, i.e., photosynthetic income, relative to costs of carbon and
nutrient allocation for construction and maintenance. It is dynamic, because as a
plant produces new leaves or is overtopped by neighbors, old leaves become shaded
and less productive (e.g., Mooney et al. 1981). Moreover, aging results in the
decrease of net photosynthesis per unit area and photosynthetic nitrogen use effi-
ciency (PNUE) (Field and Mooney 1983; Sobrado 1994; Kitajima et al. 1997b,
2002). In addition, the cost of making and keeping a leaf is not fixed, as it is
influenced by variation in structural and chemical defense (McKey 1974;
360 S.E. Russo and K. Kitajima

Table 1 Potential trade-offs that are relevant for cost-benefit models of leaf lifespan
Property Benefit Cost
Slower leaf ⦁ Leaf construction costs are infrequently ⦁ Leaf area of tree does not always
turnover incurred maximize light interception
⦁ Nutrient resorption and translocation costs are ⦁ Slower height and crown growth
infrequently incurred rate limit competitive ability
⦁ Nutrient and carbon losses are minimized, ⦁ Slower leaf turnover delays the
and leaves may store nutrients and response to spatio-temporal
carbohydrates, contributing to better nutrient fluctuations of light
retention and nutrient use efficiency ⦁ Lost opportunity cost due to less
⦁ Cost of allocation to roots for uptake of optimal allocation to maximize
belowground resources is reduced the compounding interest of
⦁ Slower development of self-shading enables photosynthetic production
leaf to remain near its maximal productivity
for longer time period
Slower Amax ⦁ Lower nutrient demands alleviate need for ⦁ Slower rate of return of
extensive belowground investment photosynthetic carbon requires
⦁ Slower transpiration rates reduce need for longer lifespan to repay initial
extensive water uptake carbon construction cost
⦁ Photosynthetic machinery requires less ⦁ Plants fail to benefit from
maintenance respiration compounded interest associated
with high Amax
Greater ⦁ Durability is enhanced through greater ⦁ Larger construction cost per unit
investment resistance to damage agents, such as physical leaf area means longer payback
in defense forces and natural enemies time
⦁ Functional deterioration with leaf age may be
slower via slower accumulation of damage to
the leaf
The benefits and costs at the plant level of three key properties associated with extending leaf lifespan for
evergreen tropical species are summarized. Abbreviations: Amax, maximum rate of photosynthesis at the
leaf level

Coley 1983), lost-opportunity costs of not allocating nutrients to newer leaves or

non-leaf tissues (Harper 1989; Westoby et al. 2000), and costs of stem and root
tissues to support leaves (Kikuzawa and Ackerly 1999; Givnish 2002). Thus,
dynamic optimization of leaf lifespan involves processes operating at both the leaf
and whole-plant levels, and it is adaptive for plants to adjust leaf phenotype and
lifespan to acclimate to spatio-temporal variation in the environment and resource
availability (Ackerly and Bazzaz 1995).

Sources of Variation in Leaf Lifespan

Here, we present a hierarchical view of the total phenotypic variation in leaf

lifespan across all individuals, which can be partitioned into mechanisms operating
at different levels of organization (Fig. 1).
The Ecophysiology of Leaf Lifespan in Tropical Forests … 361

Frequency distribution of leaf

lifespans in a Panamanian
Number of leaves

forest community

Leaf lifespan (days) Partitioning of leaf lifespan variance

Total community-level variance
Species Interspecific Intraspecific Unexplained
Abundances

Between-individual variance
Genotype Environment Genotype x Unexplained
Environment
Interaction

Within-individual variance
Ontogeny Environment Ontogeny x Unexplained
Environment
Interaction

Fig. 1 Conceptual diagram of how the total variation in leaf lifespan within a forest community is
hierarchically partitioned among different sources of variation at different levels of biological
organization (lower portion), along with an example of leaf-level variation in estimates of leaf
lifespan of seedlings across 58 species in a Panamanian forest community (upper portion). The
part of the histogram in darker green indicates data for one species, Virola surinamensis
(Myristicaceae), demonstrating substantial within-species variation in leaf lifespan, some of which
reflects plasticity in response to light. Different species in a community contribute disparate
amounts to the total variance of the community, depending on their intraspecific variation

Interspecific Variation

The covariation of leaf lifespan with other leaf functional traits defines key axes in
the WLES describing interspecific variation in species ecological strategies (Reich
et al. 1991, 1992, 1997; Wright et al. 2004). Tropical tree species vary enormously
in their leaf lifespans, from pioneer species that exchange leaves within several
weeks (e.g., Heliocarpus appendiculatus, Ackerly and Bazzaz 1995) to shade
tolerant species that retain leaves over multiple years (e.g., 25 years reported for
Araucaria by Molisch (1928), cited by Chabot and Hicks (1982); 12 years reported
for a dicot tree sapling in Panama, pers. comm., P.D. Coley). Although phyloge-
netic history can constrain evolutionary changes, it is widely accepted that
362 S.E. Russo and K. Kitajima

interspecific variation in leaf lifespan, and the shape of the WLES axes, arise
through natural selection (Donovan et al. 2011), which has produced a diversity of
convergent solutions, even within a given tropical forest community (e.g., Reich
et al. 1991). Overall, we can interpret the trait syndromes associated with leaf
lifespan as being evolutionary answers to optimization problems posed by complex,
interacting trade-offs related to the carbon and nutrient economies of plants and
their consequences for fitness in heterogeneous environments.
One of the widely-reported patterns from tropical forest tree communities is that
species with shorter leaf lifespans tend to have faster maximum rates of photo-
synthesis and higher leaf nitrogen concentrations per unit leaf mass (Williams et al.
1989; Reich et al. 1991, 1992, 1997; Wright et al. 2004). They also generally
occupy more productive habitats that can support the faster growth rates that make
such a strategy advantageous, such as moist soils with high nutrient availability and
irradiance. Since rapid shoot growth also causes self-shading, decreasing the
insolation and productivity of older leaves (Hikosaka 1996; Ackerly 1999; Yamada
et al. 2000), the rate of decline in photosynthetic rate with leaf age tends to be faster
for species with shorter-lived leaves (Kitajima et al. 1997a, b, 2002). In such
productive environments, greater whole-plant photosynthetic income may be
gained by reallocating nutrients in aging leaves to support production of new leaves
and rapid height growth (Field 1983; deJong 1995; Hikosaka 2005; Marty et al.
2010), and there would be little to gain by investing in structural durability beyond
the minimal need to achieve the short optimal leaf lifespan.
Conversely, long-lived leaves with high LMA are generally found on
slower-growing tree species that persist in less productive habitats, such as
nutrient-depleted, well-drained soils or the shaded understory, where diurnal pho-
tosynthetic carbon gain is constrained by light, nutrient, or water availability.
Longer leaf lifespan is advantageous because it prolongs the time over which such
high carbon construction costs can be recouped (Chabot and Hicks 1982; Poorter
et al. 2006). Moreover, in these habitats, allocation of limited resources to roots
may constrain allocation to leaf construction (Bryant et al. 1983; Poorter et al.
2012), and leaves may have lower nutrient concentrations per unit mass (Reich
et al. 1991, 1992, 1997; Wright et al. 2004). Longer lifespans are also selected
because they reduce the nutrient loss associated with leaf turnover, and thus
increase the whole-plant retention time of expensive-to-acquire nutrients (Monk
1966; Small 1972; Chapin 1980; Aerts and de Caluwe 1994). Likewise, defense
(often carbon-based structural and chemical defenses, rather than nitrogen-based
chemical defense, on infertile soils; Bryant et al. 1983) to avoid damage and pre-
mature leaf loss from herbivory or other hazards should also be favored (Janzen
1974; McKey 1979; Coley and Barone 1996).
In summary, variation among species in leaf lifespan should be viewed as an
important part of the functional variation underlying the interspecific trade-off
between growth and survival rates, which represents plant species’ ecological
strategies spanning fast growth and low survival to slow growth and high survival
The Ecophysiology of Leaf Lifespan in Tropical Forests … 363

(Kitajima 1994; Kobe 1999; Hubbell 2001; Kitajima and Myers 2008; Russo et al.
2008). Indeed, interspecific variation in leaf lifespan is positively correlated with
survival rate in shade for seedlings and saplings in neotropical forests (Poorter and
Bongers 2006; Kitajima and Poorter 2010; Kitajima et al. 2013) and saplings in
Bornean rain forests (Russo, unpub. data).

Intraspecific Variation

Many studies, including those cited above, focus on interspecific variation, com-
paring mean or median lifespan of species, ignoring large variation within species
(Fig. 1). Tree species with evergreen leaf habits should have evolved the capacity to
produce leaves with varying lifespans, given that leaf structural and biochemical
traits show such ecological plasticity (Valladares et al. 2007) and that plasticity in
leaf lifespan enables trees to respond to environmental changes to maintain positive
net carbon gain. The total variance within a population of a phenotypic trait such as
leaf lifespan can be partitioned into four sources, plus unexplained variance
(Fig. 1): (1) variation attributable to genes, (2) variation attributable to the envi-
ronment, (3) variation attributable to ontogeny, (4) variation attributable to
genotype-by-environment interaction (genetic variation for phenotypic plasticity).
Within-species variation in leaf lifespan may arise because the genotypes in the
population differ in their leaf lifespan, and the relative proportion of these geno-
types may differ among populations. Environmental heterogeneity can also be a
significant source of variation in leaf lifespan both between habitat types and
between microenvironments within a habitat due to differences in forest canopy
structure, microtopography, or tree-size, which all influence access to above- and
belowground resources (Weiner 1990). Even individual leaves and branches on a
tree experience contrasting environments. In seasonally dry tropical forests, leaves
produced in the early wet season function for a longer time under lower light
availability of the cloudy rainy season, whereas those produced prior to the dry
season can achieve higher productivity under a brighter sky, but are limited in
maximum leaf lifespan due to dry-season deciduousness (Kitajima et al. 1997a).
The shapes of leaf survival curves, which show the proportion of leaves remaining
versus leaf age, demonstrate that leaf-level variation in lifespan can be substantial,
even within a species (Fig. 2). When most leaves have similar lifespans, the survival
curve shows low mortality before declining dramatically, which coincides with a
short phase of synchronous senescence (Fig. 2a). Alternatively, the survival curve
can decline more gradually, indicating steady mortality from early to late leaf ages,
which reflects greater variation leaf lifespan among individual leaves (Fig. 2b).
Phenotypic plasticity is the capacity of a genotype to produce different pheno-
types in different environments (Sultan 1995). It is considered by some to be a trait
under selection that is favored when the environment is highly and unpredictably
variable (Via and Lande 1985) or when it enables a plant to take maximal
364 S.E. Russo and K. Kitajima

(a)

Portion of leaves surviving, S(t)

(b)

Sun leaves
Shade leaves

Time (days)

Fig. 2 Examples from two Panamanian tree species to demonstrate how the shapes of leaf
survivorship curves differ between environments and species. Panels show Kaplan-Meier estimates
of the survival function for sun leaves in the canopy (red) and shade leaves in the understory
(blue). In the case of Bombacopsis sessilis (Bombacaceae) (a), sun and shade leaves show similar
magnitudes of leaf-level variation in leaf lifespan across contrasting light environments, but for
Virola surinamensis (Myristicaceae) (b), the survival function is steeper for shade than for sun
leaves, indicating less variance in observed leaf lifespans among individual leaves in the former

advantage of ephemeral pulses of resources, and so faster-growing species are

thought to have greater plasticity (Bazzaz 1979; Lambers and Poorter 1992;
Valladares et al. 2000). Quantifying phenotypic plasticity at the individual level is
challenging because genetic clones are rarely available for wild tree species, hence,
environmentally induced phenotypic variation in leaf lifespan is measured at the
population level using maternal siblings grown in contrasting environments. Even
so, studies of plasticity in leaf lifespan of tropical species are rare (Ackerly and
Bazzaz 1995; Kitajima et al. 2013). However, they still yield insights because even
though the variation due to genotype and genetic variance for phenotypic plasticity
are unknown, total phenotypic variation can be partitioned into what is explained by
the environment versus all other sources (Whitman and Agrawal 2009).
Ontogenetic plasticity, in which the phenotype depends on an individual’s
developmental stage, also contributes to within-species variation. The tissue density
and toughness of the leaf lamina increase from saplings to adults in tropical trees
(Kitajima and Poorter 2010), and in a Malaysian forest, Osada et al. (2001) found
that more sunlit leaves at taller heights within tree crowns had shorter lifespans
relative to more shaded leaves at shorter heights. Because the environment changes
The Ecophysiology of Leaf Lifespan in Tropical Forests … 365

dramatically with tree size in closed canopy tropical forests, the proportion of this
variation due to purely environmental versus developmental influences is unknown.

Leaf Structure and Nitrogen: Key Aspects of Leaf

Construction Cost and Lifespan

LMA and nitrogen concentrations vary with leaf lifespan among species, as
described in the WLES, and also plastically within species (Ackerly and Bazzaz
1995). It is overly simplistic to consider LMA only as a measure of structural
defense or to assume that a fixed proportion of nitrogen resides only in the car-
boxylation enzymes. It is therefore important to consider a leaf as a heterogeneous
structure (Terashima et al. 2011). In mesic tropical forests, trees with needle-shaped
leaves are rare. A common design that simultaneously allows for efficient harvest of
light energy under a shaded canopy while enabling CO2 uptake is for a plant to have
multiple layers of thin and flat leaf blades arranged in its crown (Horn 1971; Halle
et al. 1978; Hikosaka 2005). The leaf blade is a complex structure consisting of
photosynthetic and vascular cells sandwiched between cuticles that provide pro-
tection from desiccation and physical damage. Within the leaf blade, metabolically
active molecules reside in cells surrounded by cell walls of different thickness and
mechanical properties (Onoda et al. 2015). There are many sources of structural and
mechanical variation in the leaf blade that contribute to its toughness and density,
two correlates of leaf lifespan (Coley 1983; Kitajima and Poorter 2010; Westbrook
et al. 2011; Kitajima et al. 2012).
When a plant should shed a leaf is a function of nutrient, as well as carbon balance
(Field 1983; Aerts and Chapin 2000). Shorter leaf lifespan should be favored when
the cost of acquiring nutrients is low, whereas the reverse is true in nutrient-depleted
soils, and only by accounting for the cost of nutrient acquisition can models accu-
rately predict an evergreen leaf habit in highly seasonal, nutrient-limited, boreal
environments (Givnish 2002). Consistent with these predictions, in an Argentine
subtropical forest, leaf lifespans of seedlings of five tree species grown in high-light
gaps declined with N and P fertilization, although some only marginally so (Villagra
et al. 2013). Similar results were seen by Cordell et al. (2001) for Metrosideros
polymorpha (Myrtaceae), but only on N-limited substrates. On P-limited substrates,
fertilization with N and P had no effect on leaf lifespan. Thus, the effects of nutrient
limitation on leaf lifespan are likely to depend upon the nutrient in question.
In some leaf lifespan models that consider costs and benefits only in terms of
carbon, the predicted optimal time of leaf shedding is the time at which the leaf can
no longer off-set its own carbon costs of maintenance respiration (Monsi and Saeki
2005; translated from Monsi and Saeki 1953). Consideration of optimum nitrogen
allocation strategy in the plant canopy, however, is critical (Hirose 2005). For
example, Oikawa et al. (2006) showed that this prediction is met for an herb when it
was grown under high nitrogen availability, but that under low nitrogen availability,
366 S.E. Russo and K. Kitajima

leaves were shed despite still having positive net carbon gain. When nitrogen
availability limits the maximum leaf area within the plant canopy, the effects of leaf
area index and self-shading are less pronounced, such that the oldest leaves at lower
positions may be receiving sufficient light to allow C-gain to remain positive up
until the time of leaf shedding (Ackerly and Bazzaz 1995). To maximize net carbon
gain over all leaves in an entire, heterogeneously illuminated plant canopy, nitrogen
should be allocated so that the most sun-lit leaves contain the greatest photosyn-
thetic nitrogen concentrations, and such differential nitrogen allocation is expected
to be more pronounced in species with a steep self-shading gradient (Hikosaka
2005; Hirose 2005). In a tropical forest canopy, Cecropia species with a low leaf
area index (<1) had a shallower nitrogen gradient compared to species with greater
LAI and self-shading (Kitajima et al. 2002, 2005). Thus, there are complicated
interactions between insolation at the top of the crown and soil nutrient availability
that influence LAI and the steepness of the self-shading gradient, which together
affect differential nitrogen allocation among leaves and leaf lifespan. Moreover,
how these processes interact to affect whole-plant C-gain is likely to vary among
species with different ecological strategies.
One of the most commonly used, but deceptively simple, ecological measures of
leaf structure is LMA (Osnas et al. 2013). However, LMA is a complex trait that
can be decomposed into lamina thickness and density, which play different func-
tional roles (Witkowski and Lamont 1991; Poorter et al. 2009). Sun-exposed leaves
have multiple layers of elongated palisade mesophyll cells for more thorough
absorption of high irradiance, resulting in greater lamina thickness and high LMA
(Goldstein et al. this volume; Givnish 1988; Terashima et al. 2011). Greater LMA
of sun leaves compared to shade leaves also involves change in the abundance of
thick-walled vascular cells to meet high transpirational water demand and conse-
quent increases in tissue density (Poorter et al. 2009). In contrast to these sun-shade
acclimation responses, adaptation to high versus low-light habitats exhibit different
directional responses: the leaves of light-demanding tree species have lower LMA
than those of shade-tolerant tree species (Kitajima 1994; Walters and Reich 1999;
Rozendaal et al. 2006; Markesteijn et al. 2007). This interspecific trend in LMA can
be understood as adaptation to resource-limited environments, such as the shaded
forest understory or infertile soils, in which longer time is required for paying back
leaf construction cost (Mooney and Gulmon 1982; Williams et al. 1989).

Selection for Leaf Lifespan—What Is the Role of Defense?

If leaf lifespan is merely a function of how quickly a leaf wears out under the
bombardment of attacks from herbivores and physical stresses, it may be reasonable
to hypothesize a positive association between defense and leaf lifespan. But, a
casual walk in a tropical forest reveals many “holey” leaves that exhibit extensive
damage (e.g., 11-year old leaves in a Bornean rain forest Fig. 3). Coley (1983)
evaluated saplings of 46 tropical tree species in Panama under a standardized
The Ecophysiology of Leaf Lifespan in Tropical Forests … 367

Fig. 3 Portraits of leaves that are greater than 11 years old on saplings of five tree species in the
mixed dipterocarp forest of Lambir Hills National Park, Borneo, a Polyalthia sarawakensis
(Annonaceae), b Syzygium cf. grande (Myrtaceae), c Shorea laxa (Dipterocarpaceae), d Knema
galleata (Myristicaceae), e Dipterocarpus globosus (Dipterocarpaceae)

environment of treefall gaps to examine which leaf traits best explain differences in
herbivory of young and mature leaves, leaf lifespan, and inherent differences in
growth rates. The results show that interspecific variation in herbivory rates of
young leaves is not explainable by most putative defense traits except for
368 S.E. Russo and K. Kitajima

toughness. In contrast, differences between species in herbivory rates of mature

leaves, although they are overall much lower than in young leaves, can be explained
by toughness, cellulose contents, and pubescence, but not by carbon-based chem-
ical defense of tannins and phenols. Similar results are reported for 24 species from
the same Panamanian forest in Kitajima et al. (2012), in which leaf toughness is
measured as fracture toughness and work-to-shear, along with their material bases.
Interestingly, these putative structural and mechanical defenses explain species
differences in leaf lifespan and growth rates better than herbivory rate does. Thus,
there is a paradox. Leaf lifespan, rather than herbivory, is associated with leaf
functional traits associated with physical defense. But, a cafeteria experiment with a
generalist herbivore has shown a clear negative correlation between toughness and
herbivory rate (r = −0.78), which were as strong as positive correlations of
toughness with leaf lifespan (r = 0.88) and sapling survival rate (r = 0.78) (Kitajima
and Poorter 2010). Perhaps, specialist herbivores are responsible for herbivory in
the field, but they may be influenced differently by different chemical defenses,
such that comparison of a broad range of species does not reveal significant
association between herbivory and putative leaf defense traits.
Recent comparative studies also shed light on how LMA is linked to leaf
structural properties through evolution and acclimation. In comparative analysis of
subcanopy leaves of 197 species, Westbrook et al. (2011) asked, “what makes
leaves tough?” from an evolutionary perspective, using structural equation models
with phylogenetic independent contrasts. The results showed lamina density and
cellulose per unit dry mass as two alternative paths to evolutionarily increase leaf
fracture toughness, which was greater for species with high survival in shade. Their
results also suggested that lamina thickness evolved independently of density and
cellulose per unit mass. Perhaps, fracture toughness and its material bases should be
viewed as the physical robustness necessary to set the upper limit for maximum
lifespan. For a given leaf, realized leaf lifespan, however, may be shorter than this
potential maximum. Even if a leaf is built to last for five years, it is perhaps not
adaptive for a sapling to keep it that long. Particularly when a canopy opening
forms, it may be more beneficial to senesce old leaves, translocate nitrogen and
phosphorus to new leaves at higher and sunnier positions, and thereby extend the
main stem.
For a given leaf, LMA is a product of lamina thickness and tissue density (dry
mass per volume). Both lamina thickness and density may have plastic responses to
light and nutrient availability as described in later sections with respect to LMA.
Higher light availability in treefall gaps is associated with thicker, denser, and
tougher leaves, but leaf lifespan is shorter, and herbivory is more common in gap
seedlings than in understory seedlings (Kitajima et al. 2012). Hence, it is overly
simplistic to interpret LMA as a putative structural defense trait. For interspecific
variation, the tissue-density aspect of LMA enhances leaf lifespan, but the lamina
thickness appears to be of lesser importance. For intraspecific variation associated
with sun-shade gradients, leaf lifespan may decrease while LMA increases from
shade to sun. Such counter-gradient variation (Lusk et al. 2008) is also found for
putative chemical defense as well (Coley 1993); for temperate tree saplings, Shure
The Ecophysiology of Leaf Lifespan in Tropical Forests … 369

and Wilson (1993) found that within species, acclimation to larger gap size (i.e.,
more light) resulted in higher tannin concentrations, but among species, higher
tannin was associated with adaptation to shade.

Empirical Tests of Conceptual Models for Acclimation

and Adaptation to Varying Resources

As discussed above, acclimation to variable light availability versus adaptive spe-

cialization to contrasting irradiance habitats may exhibit different relationships of
leaf lifespan with LMA and other leaf functional traits. The interaction of nitrogen
and light availability is also key to understanding the optimization of leaf lifespan.
Unfortunately, much less is known about how acclimation and adaptation exhibit
co-variation of leaf lifespan and LMA within and among species in relation to soil
fertility variation in tropical forests. In this section, we first present conceptual
predictions of covariation of leaf lifespan and LMA (Fig. 4). We then test them with
empirical data on plasticity of species specialized to habitats with contrasting
resource availabilities, using data on leaves from Panama (seedlings grown under
contrasting light environments) and Borneo (seedlings grown under contrasting
light and soil environments). Our goal is to interpret these patterns in adaptive
ecological plasticity with respect to the resource economic strategies of tree species.

Acclimation Versus Adaptation to Light Availability:

Counter-Gradient Variation

As discussed in the previous section, the among-species correlation in leaf lifespan

and LMA is positive (WLES), whereas plastic covariation within species is nega-
tive. Such counter-gradient variation is summarized graphically for light (Fig. 4a):
acclimation to shade causes a decrease in LMA (Arrows 1 and 3 in Fig. 4a) and an
increase in lifespan (Arrows 2 and 4 in Fig. 4a) within species, whereas between
species, longer leaf lifespan is associated with higher LMA (positive slope of across
species in the same light environment). This conceptual model is similar to the one
by Lusk et al. (2008), but our model is more explicit about variation in the accli-
mation response of each species, depending on its resource economic strategy.
More specifically, we predict that the degree of plasticity in leaf lifespan is greater,
but that of LMA is smaller, for species with longer maximum leaf lifespan (shal-
lower slopes for the gray arrows representing plastic covariance toward the
right-hand side of Fig. 4a). For species under selection to have rapid leaf turnover in
a resource-rich environment, it may be infeasible to reduce leaf lifespan beyond a
370 S.E. Russo and K. Kitajima

(a)

Increasing LMA
High light
Low light
Increasing Leaf Lifespan

(b)
Increasing LMA

Less fertile
More fertile
Increasing Leaf Lifespan

Fig. 4 Conceptual models of how leaf mass per area (LMA) covaries with leaf lifespan across and
within species in terms of phenotypic responses to a contrasting light regimes (open symbols high
light, closed symbols low light) and b contrasting soil types (open symbols fertile, closed symbols
infertile). Each pair of circles connected by a solid gray line corresponds to an individual species
and its phenotypic reaction norm. The interspecific relationship of LMA versus lifespan in a given
environment is shown as dotted or broken lines: in high or low light (short and long-dash,
respectively) and in more or less fertile soil types (long and short-dash, respectively). Small circled
numbers indicate directional changes in LMA and lifespan, and the mechanisms involved for each
are described in the main text

certain minimum, due to ever-increasing costs associated with leaf-turnover, even

though they may exhibit a high degree of plasticity in LMA under higher light
availability. At the other end of the LMA-lifespan spectrum, species selected to
have structural defense to enable longer leaf lifespans have more latitude for plastic
lifespan responses, which may result in greater shifts in response to light envi-
ronment. There is also likely to be an upper limit on LMA, since light attenuates
within thick mesophyll layers, and severely decreased lamina area may reduce
photosynthetic surface area. Thus, the degrees of plasticity in LMA and leaf
lifespan may differ across species with different ecological strategies, influencing
the slope of the interspecific LMA-lifespan relationship (Fig. 4a).
The Ecophysiology of Leaf Lifespan in Tropical Forests … 371

(a)

(b)

Fig. 5 a Interspecific variation and plasticity of leaf lifespan and LMA across seedlings of 41
Panamanian tropical tree species. Seedlings were grown from seeds in common gardens in treefall
gaps (red, open circles) or understory common gardens or shade house (0.8 % of total daily PPFD
in both; blue, closed circles). Each solid line connecting two data points from a given species
shows the direction of phenotypic co-variation in LMA and leaf lifespan. The dotted and broken
lines indicate the interspecific relationship. Species with estimates of median leaf lifespan
exceeding 1300 days were not included, nor were species that were raised or could survive only in
one of the environments. See Kitajima et al. (2013) for further details. b Relationship between
plasticity in LMA and leaf lifespan derived from the data shown in (a), with the 95 % confidence
ellipse in red. The plasticity index was calculated as the difference in trait values between
contrasting light environments divided by the geometric mean of those values

We tested these predictions using data on the LMA and leaf lifespans of seed-
lings from 41 Panamanian tree species that were experimentally grown in replicated
common gardens in gaps and shaded understory. These species represent a range of
shade-tolerance strategies, from light-demanding pioneers to shade tolerant
late-successional species (Kitajima et al. 2012, 2013). Overall, the results shown in
372 S.E. Russo and K. Kitajima

Fig. 5a support the conceptual model predictions (Fig. 4a). Within-species, accli-
mation to shade involved an increase of leaf lifespan and decrease of LMA (neg-
ative correlation). Among species, longer leaf lifespans were associated with
increased LMA under each standardized light environment (positive correlation).
Also, light-demanding species with short leaf lifespan exhibited large degrees of
plasticity in LMA, but relatively smaller changes in leaf lifespan between the two
light environments. Consistent with our conceptual model, plasticity in LMA
declined with increasing plasticity in leaf lifespan (r = –0.491, P = 0.001; Fig. 5b).

Acclimation Versus Adaptation to Soil Resource

Availability: Co-gradient Variation

Among and within tropical forests, soil properties vary greatly in terms of avail-
ability of mineral nutrients, such as nitrogen and phosphorous, and water, even
under the same climate (Ashton 2015). Co-variation of leaf lifespan and LMA in
relation to natural soil gradients is widely demonstrated both in temperate and
tropical ecosystems (e.g., Cordell et al. 2001; Wright et al. 2002), although in many
such studies, variation due to acclimation versus adaptation are confounded. While
we recognize that different types of belowground resources may produce varying
responses (e.g., low-rainfall vs. low-nutrient sites, Wright et al. 2002; nitrogen vs.
phosphorus, Cordell et al. 2001), here we develop a general conceptual model for
inter- and intraspecific variation in leaf lifespan and LMA due to soil fertility.
Variation in soil fertility is expected to produce co-gradient variation (Fig. 4b),
unlike the case for insolation (Fig. 4a), since lower soil fertility should be associated
with increases in both LMA (Arrows 1 and 3 in Fig. 4b) and leaf lifespan (Arrows 2
and 4 in Fig. 4b) both within and between species. Species with contrasting soil
associations across fertility gradients experience and are presumably adapted to
different soil nutrient and moisture regimes, and so we expect them to differ in
LMA and leaf lifespan plasticity, causing the slope of the interspecific
LMA-lifespan relationship to vary across soil habitat types, analogous to
light-related patterns.
Patterns of within-species variation in leaf lifespan with soil fertility, however,
can be quite inconsistent across studies, often with apparently non-adaptive phe-
notypic responses, such as reduced leaf lifespan in less fertile soils (Aerts and
Caluwe 1995; Richardson et al. 2010; Pornon et al. 2011). Pornon et al. (2011)
proposed a conceptual model to explain these counter-intuitive soil-related
responses, in which they consider that sink activity due to growth accesses
endogenous, more than exogenous, nitrogen when soil nitrogen is very low,
accelerating leaf senescence (Marty et al. 2009; Pornon et al. 2011). However, this
logic only makes sense if a plant species does not sufficiently down-regulate sink
activity in resource-depleted environments via regulation of leaf production and
growth rates, which would reduce demand for nitrogen in the first place. Although
The Ecophysiology of Leaf Lifespan in Tropical Forests … 373

height competition is less intense in nutrient-depleted soils, down regulation of

height growth may not be an evolutionarily stable strategy in some circumstances
(Anten 2005). There is ample evidence that growth rates vary depending on
resource availability, but there are likely to be limits to the amount by which a
species can adjust inherent variation in growth rate (sensu Lambers and Poorter
1992).

Interactions of Light and Soil Resource Availability

on Leaf Lifespan Variation

Both light and soil resources vary in time and space, and in the forest understory,
they are often interdependent (Coomes and Grubb 2000; Russo et al. 2012), and so
it makes sense to examine their interactive effects on acclimation of LMA and leaf
lifespan. We examined these patterns using data from seedlings of 13 Bornean tree
species that were reciprocally transplanted into contrasting light and soil environ-
ments in forest experimental plots. Leaf lifespan was estimated on seedlings of each
species sown on clay and sandy loam soils in gaps and understory. All study species
are shade tolerant, but differ in soil specialization, ranging from species associated
with nutrient-depleted, well-drained sandy loam soil, to clay soil with greater
nutrient concentrations and water-holding capacity, and generalist species associ-
ated with both soil types (Davies et al. 2005). Moreover, the sandy loam specialists
have slower diameter growth and higher survival rates compared to clay specialists
(Russo et al. 2005).
The patterns among the Bornean species across light and soil treatments (Fig. 6)
were considerably more complex than the pattern due to insolation alone (Fig. 5).
As predicted by our conceptual models (Fig. 4), the results show counter-gradient
variation for acclimation versus adaptation of LMA and leaf lifespan with light
environment, and co-gradient variation with contrasting soil environments.
However, the direction and magnitude of plasticity of both traits depended on the
soil and light environment, as well as the species’ soil specialization. Among
species, increases in leaf lifespan were associated with increases in LMA, and,
consistent with our conceptual model, the slopes of these relationships depended
upon the environment. Within-species, acclimation to shade produced an increase
in leaf lifespan and a decrease in LMA (negative slopes of the black lines in Fig. 6a,
b). These relationships were most consistently seen on sandy loam (Fig. 6b), which
exhibited counter-gradient selection and resembled patterns for the Panamanian
species (Fig. 5a). On the more fertile clay (Fig. 6a), LMA decreased for all species
with acclimation to shade, as expected. However, leaf lifespan on clay showed
variable patterns with acclimation to shade, increasing or showing little change, as
expected for clay specialists, but counterintuitively decreasing for sandy loam
374 S.E. Russo and K. Kitajima

specialists and generalists. One explanation is that the sandy loam specialist
seedlings may have accelerated leaf senescence in order to reduce carbohydrate
consumption (Sevanto et al. 2014), since the understory on clay is shadier than the
understory on their home sandy loam soil to which they are presumably adapted
(Russo et al. 2012).
Within-species, acclimation from sandy loam to clay produced a decrease in leaf
lifespan and either little change or a decrease in LMA (Fig. 6c, d), co-gradient
variation that is most consistently seen in the low light understory (Fig. 6d). In gaps,
however, patterns were complex, with some species exhibiting counter-gradient
selection or little change in leaf lifespan across contrasting soils (Fig. 6c). These
disparate responses could be related to whether species are N or P-limited. On a
P-limited substrate, Cordell et al. (2001) found no change in the leaf lifespan of M.
polymorpha in response to fertilization with N, P, or their combination, in contrast
to an N-limited substrate, on which leaf lifespan declined with fertilization.
Although responses of individual species varied, at a given LMA, leaf lifespan was
always longer for seedlings in low light especially on sandy loam (Fig. 6a, b).
However, at a given LMA, leaf lifespan was on average longer for seedlings on
sandy loam than on clay soil only in low light (Fig. 6d); in high light, leaf lifespan
 The Ecophysiology of Leaf Lifespan in Tropical Forests … 375

b Fig. 6 Interspecific variation and plasticity of leaf lifespan and LMA of seedlings of 13 tropical,
shade-tolerant tree species in the Dipterocarpaceae specializing on sandy loam soil, clay soil, or
neither (generalists). Seedlings were grown from newly germinated seeds in a field reciprocal
transplant experiment in plots in Bornean forest (Lambir Hills National Park, Malaysia) located on
sandy loam (purple, open circles) or clay (green, closed circles) and in treefall gaps (red, open
circles) or shaded understory (blue, closed circles). Responses in the four environmental regimes
are in each panel, comparing plots in high versus low light (a and b) or sandy loam versus clay
(c and d), holding either soil or light environment constant, respectively. The two data points for
each species are connected by a black line showing the phenotypic reaction norm, with the dashing
pattern indicating soil specialization (solid, generalist; long dash, clay specialist; dot-dash, sandy
loam specialist). Colored dotted and broken lines (colors correspond to the symbol colors for the
different environments) indicate the interspecific relationship of LMA with the 25th quantile of leaf
lifespan within each soil or light environment. LMA was determined for all true leaves at
approximately 1.5 years after seeds were sown. Species’ 25th quantile leaf lifespan was
determined for marked true leaves for up to 1200 days. The 25th quantile of lifespan was used
because the median lifespan could not be estimated for all species based on the study duration
(3.25 years) and long leaf lifespans. Study species are shade-tolerant and either canopy or
emergent tree species. Congeneric species of contrasting soil associations include the following:
sandy loam specialists, Dryobalanops aromatica, Hopea beccariana, Dipterocarpus globosus,
Shorea beccariana, Shorea laxa, Vatica nitens; clay specialists, Dryobalanops lanceolata, Hopea
dryobalanoides, Dipterocarpus palembanicus, Shorea macrophylla, Shorea xanthophylla; and
generalists, Anisoptera grossivenia and Dipterocarpus acutangulus. Soil associations are based on
Poisson cluster model analyses in Davies et al. (2005; see also Russo et al. 2005), with stems of
specialists being significantly aggregated on that soil type and generalists showing no significant
aggregation due to soil type

at a given LMA was shorter for seedlings on sandy loam than on clay (Fig. 6c).
This unexpected response resembles findings from Reich et al. (1999) and Wright
et al. (2002) in relation to water availability: at a given LMA, species associated
with lower rainfall sites had shorter leaf lifespan than those at wetter sites. For these
Bornean species, the LMA required to achieve a given lifespan is higher on sandy
loam, potentially owing to lower soil moisture (Russo et al. 2010). Higher LMA
may confer better tolerance to low soil water potentials experienced at low-rainfall
sites or well drained soils (Niinemets 2001; Wright et al. 2002). Thus, soil-related
plasticity in leaf lifespan when light is not limiting may depend upon the particular
belowground resource in question, as well as variation among species in which
resource is most limiting to growth.
As with the results from Panama, plasticity in LMA and leaf lifespan were
negatively correlated (r = −0.56, p < 0.001; Fig. 7). However, on the
resource-depleted habitats, the mean plasticity index for leaf lifespan (sandy loam:
0.50 and low light 0.45) was on overage two to four-fold higher than that for LMA
(sandy loam: 0.26 and low light 0.11), whereas in the more productive environ-
ments, the mean plasticity indices for leaf lifespan and LMA were more comparable
(lifespan, 0.15 and 0.20, and LMA, 0.19 and 0.14, for clay and high light,
respectively), suggesting that in resource-depleted habitats leaf lifespan may be
extended by means other than increasing LMA.
376 S.E. Russo and K. Kitajima

Fig. 7 Relationship between

plasticity in leaf mass per area
(LMA) and leaf lifespan for
the data shown in Fig. 6. The
plasticity index was
calculated as the difference in
trait values between
contrasting soil or light
environments (with the other
factor held constant) divided
by the geometric mean of
those values

Towards a More Mechanistic Understanding of Leaf

Lifespan—What Remains Unknown?

Leaf lifespan is central to the carbon and nutrient economies of trees, with direct
and indirect links to individual growth and survival. Yet, even very basic infor-
mation about leaf lifespan in tropical trees is still lacking. Here, we highlight some
important knowledge gaps impeding a more mechanistic understanding of the role
of leaf lifespan in whole-tree carbon and nutrient dynamics of tropical species.

How Long Is the Longest Leaf Lifespan among

Tropical Broad-leaved Species?

Although there are several methods for estimating leaf lifespan (see Kikuzawa and
Lechowicz 2011, Chap. 1 for a review) accurate estimates of the distribution of leaf
lifespans for evergreen tropical tree species are difficult to obtain. Estimates of leaf
lifespan are improved when the data are not censored, i.e., when lifespan of all
leaves are followed from their birth to death (Dungan et al. 2003). But data col-
lection campaigns over long time periods for a sufficient number of leaves are
logistically challenging, especially for slow-growing species in aseasonal or
resource-poor tropical environments. Leaf lifespans of shade-tolerant juveniles in
tropical moist forests can be typically five or more years (e.g., Kursar and Coley
1993; King 1994). In saplings of shade-tolerant tree species in an ever-wet Bornean
rain forest growing on nutrient-depleted soils, for 14 out of 31 species, even the
The Ecophysiology of Leaf Lifespan in Tropical Forests … 377

25th percentile of the leaf lifespan distribution was not well estimated after
6.5 years of censuses, suggesting that leaf lifespans of these species may routinely
exceed 10 years (Russo, unpub. data; Fig. 3). Thus, many published leaf lifespans
for evergreen tropical species may not only fail to encompass the full range of
within- and between-tree variation, but they may also be underestimates.

Why Are Seemingly Unproductive Leaves Retained?

Juvenile trees of shade tolerant species in closed-canopy tropical forest often sur-
vive for long periods of time under deep shade. Given the aged appearance of their
often self-shaded leaves, which themselves are frequently covered with lichens and
epiphylls (Fig. 3), it is hard to imagine that such leaves are contributing signifi-
cantly to the tree’s carbon economy. So, why are they retained? These leaves may
have such low respiratory maintenance costs that they can still achieve positive net
carbon balance, in which case, there may be little advantage to senescing the leaf,
particularly if the new leaf would not intercept appreciably more insolation as is the
case for shaded juveniles. New and young leaves are more likely to be attacked by
herbivores (Coley 1983; Coley et al. 2005), and thus replacing old leaves could
present a significant risk of resource drain. It is also possible that these leaves are
retained because they function to store nutrients, for example, nitrogen in disused
proteins, that will be used to produce a flush of new leaves when the growing
environment improves. Carbon and nitrogen isotope labelling studies (e.g., Pornon
and Lamaze 2007) hold promise for identifying the sources of nitrogen used to form
new leaves and the leaf-level photosynthesis-respiration balance of older leaves.

Are Leaves Senesced When Leaf Photosynthetic Function

Declines to Zero?

How rapidly photosynthetic rates and PNUE decline with leaf age is a key
parameter in theoretical models of optimal leaf lifespan because it strongly influ-
ences photosynthetic productivity through the lifetime of the leaf (Kikuzawa 1991,
1995; Ackerly 1999; Escudero and Mediavilla 2003). At least three classes of
mechanism likely cause the decline in function with leaf age: self-shading,
age-related deterioration per se, and withdrawal of nitrogen from the lamina. With
the exception of a few studies (Kitajima et al. 1997b, 2002), how much variation in
the age-related decline in leaf function exists among and within tropical tree species,
and the environmental controls over this process, remain largely unmeasured.
Estimation of decline-rate functions can be accomplished with either a
chronosequence approach, in which leaf position substitutes for exact leaf age, or
with a repeated-measurements approach, in which photosynthetic parameters are
378 S.E. Russo and K. Kitajima

repeatedly estimated on the same leaf over its lifetime (Kitajima et al. 2002; Osada
et al. 2015). The chronosequence approach is less labor intensive, but it ignores
within-plant and within-species variation the leaf lifespan or decline-rate function,
which can be substantial, as discussed earlier. This results in substantial bias in
estimating functional decline rate with leaf age, and mismatch of empirical data to
theoretical predictions of leaf lifespan as to whether leaves are senesced when
photosynthetic function declines to zero (Osada et al. 2015). Importantly, the bias
worsens as the leaf-level variance in lifespan increases. Given the substantial
variation in survival time among individual leaves within-species and even within
plants (Figs. 1 and 2), we call attention to the importance of considering variance in
age-related changes in leaf function and demography in future tests of optimal leaf
lifespan models with empirical data.

Models of Leaf Lifespan—What Are the Key Trade-Offs?

The internal dynamics of carbon and nutrients in trees are complex, are determined
by multiple functional traits, and often involve latent physiological and biochemical
processes. As a result, the mechanisms by which leaf lifespan affects these
dynamics are difficult to quantify with empirical studies. Models of leaf-lifespan
that only consider leaf-level processes cannot account for key processes affecting
leaf lifespan that are operating at the whole-tree level. Many optimal leaf lifespan
models differ in fundamental ways in terms of which mechanisms and physiological
processes they incorporate. As a result, each is more appropriate in some ecological
contexts than in others. For example, the whole-tree model of Givnish (2002)
includes a parameter controlling the fractional carbon allocation to leaves versus
roots, and not accounting for this yields predictions of the distribution of deciduous
versus evergreen leaf habits in seasonal environments that do not match those found
in nature. Somewhat paradoxically, simpler models that do not explicitly consider
whole-plant nutrient allocation strategies, in contrast, can also give rough approx-
imation of the prevalence of deciduous versus evergreen habits (Kikuzawa et al.
2013). Although there is no complete consensus as to what are the critical
parameters that explain leaf lifespan variation from an ecophysiological perspec-
tive, there is a general recognition that trade-offs in resource allocation strategies are
key to mechanistic understanding. In Table 1, we summarize some of the critical
leaf-level and whole-tree trade-offs in function that mechanistic models of leaf
lifespan should capture. Whether we want to explain global variation in leaf habit or
the biological mechanisms governing leaf lifespan variation in a forest community
in relation to resource availability, dynamic resource allocation models that
incorporate these major physiological processes and that accurately capture these
critical trade-offs are needed. Development of such models is particularly exciting
in species-rich and functionally diverse tropical tree communities.
The Ecophysiology of Leaf Lifespan in Tropical Forests … 379

Acknowledgements Bornean and Panamanian leaf trait data were collected under the US
National Science Foundation (NSF) award DEB-0919136 to SER and IBN-0093033 to KK,
respectively. The manuscript preparation was initiated while SER was supported by a Short-term
Fellowship (S-14181) from the Japanese Society for Promotion of Science.

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The Effects of Rising Temperature
on the Ecophysiology of Tropical
Forest Trees

Martijn Slot and Klaus Winter

Abstract The response of tropical trees to rising temperatures represents a key

uncertainty that limits our ability to predict biosphere-atmosphere feedbacks in a
warming world. We review the current understanding of temperature effects on the
ecophysiology of tropical trees from organelle to biome level, where we distinguish
between short-term responses, acclimation, and adaptation. We present new data on
short-term temperature responses of photosynthesis and dark respiration, and
temperature acclimation of photosynthesis. We also compare new field and
laboratory-obtained photosynthesis-temperature response data. We identify several
priority study areas. (1) Acclimation: We need to better understand photosynthetic
acclimation, for example to determine whether the adjustment of the thermal
optimum of photosynthesis (TOpt) is consistently negated by a decrease in photo-
synthesis at TOpt, as we observed. (2) Growth: Whereas tropical seedlings may
grow better with warming, canopy trees reportedly grow worse; we do not currently
know what explains these contrasting temperature effects. (3) Reproduction:
Tropical trees may be close to reproductive temperature thresholds, as heat sterility
in crops occurs in the upper 30 °C range. Nonetheless, the temperature sensitivity of
tropical tree reproduction is virtually unstudied. (4) Mortality: How does
heat-induced atmospheric drought (high leaf-to-air vapor pressure deficit) affect
tropical tree mortality? (5) Stomatal behavior: What is the specific role of tem-
perature in the induction of midday-stomtal closure on sunny days? Better
knowledge in these areas will improve our ability to predict carbon fluxes in
tropical forests experiencing ongoing warming.

M. Slot (&)
K. Winter

Smithsonian Tropical Research Institute, Apartado 0843-03092,
Balboa, Ancón, Republic of Panama
e-mail: SlotM@si.edu; martijnslot78@gmail.com

© Springer International Publishing Switzerland 2016 385

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_18
386 M. Slot and K. Winter

Introduction

Tropical forests cover only 15 % of the planet’s terrestrial surface (Pan et al. 2013),
yet they account for more than one-third of its net primary productivity
(NPP) (Saugier et al. 2001) and two-thirds of its plant biomass (Pan et al. 2013).
Given this disproportionally large contribution to the global carbon cycle, it is
important that we increase our understanding of the effects of global warming on
tropical forest trees. Recent analyses have suggested that global variation in tem-
perature and precipitation have no direct effect on global patterns of NPP after
accounting for stand age and biomass (Michaletz et al. 2014), but this does not
mean that changes in climatic variables will not affect NPP within a given biome.
The coming decades will see ongoing warming in tropical regions, leading to
unprecedented temperature regimes (Diffenbaugh and Scherer 2011) that currently
do not support closed-canopy forests (Wright et al. 2009). Tropical regions have
previously experienced warming—most notably leading up to the Paleocene-
Eocene Thermal Maximum (*56 million years ago) when temperatures rose by 3–
5 °C—but even the most rapid of such historical warming events took place over
thousands to tens of thousands of years, timescales during which gradual changes in
species composition, adaptive responses, and speciation are possible (Jaramillo
et al. 2010). Current warming, on the other hand, occurs over the lifetime of
individual trees, necessitating a high degree of thermal plasticity to maintain
long-term growth and survival.
Warming effects on the physiology of woody plants have been studied primarily
in mid- and high-latitiude ecosystems. Many of these effects are expected to be
broadly generalizable, given the universal effects of temperature on enzyme
kinetics, and the common principles of the biochemical pathways of both photo-
synthesis and mitochondrial respiration, the key drivers of terrestrial
biosphere-atmosphere carbon exchange. However, there are several important dif-
ferences between tropical and higher latitude ecosystems that might differentially
affect plant responses to climate warming.
First, seasonal temperature fluctuations are minimal in the tropics, and such
thermally stable conditions may not favor evolution of the capacity to acclimate to
temperature changes (Janzen 1967; Cunningham and Read 2003). If tropical spe-
cies have limited thermal plasticity, current warming may be highly detrimental to
their performance. Second, for most of the past 2.6 million years tropical regions
have experienced lower temperatures than today. Natural selection under such
conditions would not have favored heat-protective traits (Corlett 2011). Temperate
and boreal climates have also been cooler over this period, but current warming is
more likely to expose tropical vegetation to temperatures near the thermal limit of
photosynthesis than higher latitude vegetation. Indeed, tropical forests might be
close to their thermal optimum already (Doughty and Goulden 2008; but see Lloyd
and Farquhar 2008). Third, warming does not lengthen the growing season in the
tropics as it does at higher latitutes (Menzel and Fabian 1999; Menzel et al. 2006).
The Effects of Rising Temperature on the Ecophysiology … 387

This means that a longer growing period will not compensate for any negative effect
of temperature on carbon uptake in the tropics. Given the above three points,
temperature relationships of tropical trees deserve special attention.
Here we review the current understanding of the effects of elevated temperature
on the ecophysiology of tropical trees and forests. We present new data on
instantaneous effects and growth-temperature effects on seedling gas exchange; we
compare laboratory-based measurements with in situ measurements of temperature
effects on foliar physiology; we review experimental, observational, and modeling
studies; and we identify areas of study that should be prioritized to improve our
ability to predict carbon fluxes in gradually warming tropical forests. We will focus
on temperature responses at the ecophysiological level, emphasizing the effects of
warming in the non-damaging temperature range. For information on molecular
responses to heat stress we refer readers to several reviews on this subject that have
been published in the past decade (e.g., Wahid et al. 2007; Allakhverdiev et al.
2008; Ashraf and Harris 2013). Our primary concern here is the effect that warming
has on tropical lowlands, which are currently the warmest ecosystems that support
closed-canopy forests (Wright et al. 2009). The *15 % of tropical forests that are
montane are beyond the scope of this chapter.
We distinguish between different temporal scales at which temperature may
affect tropical trees, and between the organizational scales at which these temper-
ature response processes operate (Table 1). We will start our review at the organelle
and leaf level—with a strong focus on photosynthesis and respiration—then work
our way up through the whole-tree level out to stand-, ecosystem-, and biome-level
temperature effects. Along the way we go from a highly mechanistic understanding
of organelle- and leaf-level processes—based on foundational work on temperate
species and backed up by a large body of experimental work—to more speculation
as we attempt to predict temperature effects at higher organizational scales and over
longer time periods for which no experimental work exists to date.

Leaf-Level Temperature Effects

Photosynthesis

Net photosynthesis (ANet) increases with short-term warming before reaching a

maximum CO2 assimilation rate (AOpt) at optimum temperature (TOpt), beyond
which net CO2 uptake rates decline and eventually drop to zero at the upper CO2
compensation point (Box 1). We will first discuss the short-term temperature
response over non-harmful, reversible temperature ranges. After briefly addressing
heat damage, we discuss temperature responses at timescales over which accli-
mation may occur.
Table 1 Temperature responses (+ and − indicate the direction of change) across organizational and temporal scales
388

Biophysical response Acclimation Adaptation Adaptation/Species Species turnover/

turnover speciation
Organizational Biome Possible temperature/drought-induced
scale collapse of closed-canopy forest
If closed canopy forest is lost: big changes
in rainfall patterns, climate feedbacks; risk
of runaway warming
Ecosystem + Mineralization in soils could + Isoprene Savanna or desert species may take over
benefit tree growth in nitrogen emissionh If closed canopy forest is lost: big changes
limited ecosystems − NPP/GPP in hydraulics, rainfall patterns, climate
− NPP/GPP ratioa ratioa feedbacks; risk of runaway warming
Tree + Respiration of all organs − Respiratory capacity of all Possible If closed canopy forest is lost: increased
(however: root and bulk stem organs; species-specific change in abundance of savanna or desert species that
temperatures are well buffered interactions with mycorrhizae biomass are better adapted to drought
and do not track instantaneous may either strengthen or allocation and
air temperature changes) weaken the acclimation leaf display
− Pollen viability responseb + Leaf cooling
− Reproductive efficiency traits for
− Stem diameter growth of adapted
canopy trees species
Seedling/sapling growth + Isoprene
unaffected emissionh
Leaf Photosynthesis peaks near local + TOpt of photosynthesis + Heat
mean temperature and then Constructive adjustment: tolerance
declines + AOpt tolerance
+ Respiration Detractive adjustment: − Low-
+ Isoprene emission − AOpt temperature
+ Monoterpene emission − Respiratory capacity tolerance
+ Isoprene emission + Isoprene
Change in morphology, e.g. emissionh
− leaf mass per areac Respiration
+ Mesophyll conductanced homeostatic
with
pre-warming
M. Slot and K. Winter

(continued)
Table 1 (continued)
Biophysical response Acclimation Adaptation Adaptation/Species Species turnover/
turnover speciation
Sub-leaf/Organelle + Monoterpene synthesis + Heat tolerance of If closed canopy forests are converted into
+ Protein turnover photosynthetic machinery savanna/desert ecosystems: increased
+ Membrane fluidity + Thermostability of Rubsico abundance of C4 and CAM species
+ Photorespiration activase or different isoforms
− Electron transport rate being expressede,f
− CO2 solubility + Electron transport capacity
+ Membrane rigidity Change in
membrane composition (e.g.,
increased ratio of saturated to
unsaturated fatty acids)g
Instantaneous Days-months Years-decades Decades-decennia Decennia-Millenia
Temporal scale
Ecosystem and biome-level predictions for long timescales are speculative
a
Zhang et al. (2014), bFahey et al. (2015), cCheesman and Winter (2013b), dMakino et al. (1994), eSalvucci and Crafts-Brander (2004), fWang et al. (2010), gMurakami et al. (2000), hSharkey
and Monson (2014)
The Effects of Rising Temperature on the Ecophysiology …
389
390 M. Slot and K. Winter

Direct Effects: CO2 Fixation

At a given light level, photosynthesis is limited by one of three factors: (1) the
capacity of ribulose 1,5-bisphosphate carboxylase/oxygenase (Rubisco) to car-
boxylate ribulose bisphosphate (RuBP) (Rubisco-limited, or RuBP-carboxylation-
limited photosynthesis); (2) the capacity to regenerate RuBP through the Calvin
cycle and the thylakoid reactions (RuBP-regeneration-limited photosynthesis); or
(3) the capacity for triose phosphate use (TPU) through starch and sucrose syn-
thesis, where low TPU limits the regeneration of inorganic phosphate necessary for
photophosphorylation (TPU-limited photosynthesis) (Harley and Sharkey 1991;
von Caemmerer 2000). At light levels that saturate photosynthesis, RuBP-
regeneration capacity generally reflects the maximum electron transport capacity
(Jmax), whereas the rate of RuBP-carboxylation-limited photosynthesis represents
the maxium capacity for Rubisco carboxylase activity (VCmax). TPU limitation at
current atmospheric CO2 concentrations only occurs at low temperatures (Sage and
Kubien 2007), and is expected to have minimal impact on photosynthesis in low-
land tropical forest trees (but see Ellsworth et al. 2015 for potential TPU limitation
driven by foliar phosphorus limitation). At current ambient CO2 concentrations,
RuBP-caboxylation limitation is common at intermediate temperatures, whereas
RuPB-regeneration can become limiting at high temperatures (Sage and Kubien
2007). High temperature can also impede Rubisco functioning through its effect on
Rubsico activase, the enzyme that promotes the dissociation of inhibitory sugar
phosphates from the active site of Rubisco, thereby activating it (Portis 2003).
Rubisco activase has lower heat tolerance than Rubisco itself, so high-temperature
impairment of Rubisco activity may represent reduced activation of Rubsico, rather
than reduced functioning of activated Rubisco (Salvucci and Crafts-Brandner
2004).
Rubsico can not only carboxylate RuBP, it can also oxygenate it, leading to
photorespiration, a process that results in loss rather than gain of CO2.
Photorespiration, although associated with reduced carbon gain, appears to play a
beneficial role under high temperatures by maintaining electron flow and preventing
photo-oxidation (Osmond and Björkman 1972; Kozaki and Takeba 1996), and by
providing a substrate for the synthesis of isoprene (Jardine et al. 2014), a volatile
organic compound believed to be associated with thermoprotection of photosyn-
thesis (see “Volatile organic compounds and thermoprotection”). Increasing tem-
perature promotes photorespiration in two ways. First, the solubility of CO2
decreases more strongly with temperature than that of O2, so proportionally more
O2 can reach the active sites of Rubisco and stimulate RuBP oxygenation. Second,
the relative specificity of Rubisco for CO2 compared to O2 decreases with
increasing temperature, so at higher temperatures, higher CO2 concentrations are
needed to achieve a given RuBP-carboxylation rate (von Caemmerer and Quick
2000).
Under current ambient CO2 concentrations, photosynthesis is controlled by TPU
capacity at low temperature (<*20 °C for the tropical species Ipomoea batatas (L.)
Lam. (sweet potato; Sage and Kubien 2007). At intermediate temperatures RuBP
The Effects of Rising Temperature on the Ecophysiology … 391

carboxylation becomes the rate-limiting step. With further warming (>*32 °C for I.
batatas) increased photorespiration reduces photosynthetic efficiency, and the
electron transport processes of RuBP regeneration become limiting. Ultimately, at
temperatures exceeding the thermal tolerance of Rubisco activase, Rubsico activa-
tion may become limiting. Increasing CO2 concentrations will reduce photorespi-
ration, thus increasing the rates of both RuBP-regeneration-limited photosynthesis
and RuBP-caboxylation-limited photosynthesis, without affecting TPU-limited
photosynthesis. RuBP-caboxylation-limited photosynthesis is more strongly stim-
ulated by CO2 than RuBP-regeneration limited photosynthesis. Consequently, at
higher CO2, there is a shift in what controls net photosynthesis at a given temper-
ature, with control exerted by TPU extending to higher temperatures than at low
CO2, and RuBP regeneration starting to limit photosynthesis at lower temperatures,
resulting in a reduced or disappearing role of RuBP-caboxylation-limitation in
constraining net photosynthesis (Sage and Kubien 2007). In other words, at elevated
CO2, Jmax exerts stronger control over the temperature response of photosynthesis
than VCmax. The remainder of our discussion will focus primarily on temperature
effects at current ambient CO2 concentration (*400 ppm).
Figure 1a illustrates how temperature affects net CO2 assimilation at 21 % versus
2 % O2—i.e., with and without photorespiration—in two early-successional tropical
tree species, Ochroma pyramidale (Cav. ex Lam.) Urb. and Ficus insipida Willd.,
and in the late-successional species Calophyllum longifolium Willd. Because
photorespiration is proportionally higher at higher temperatures (Slot et al. 2016),
TOpt of net photosynthesis is higher at 2 % O2, similar to what has been observed
under elevated CO2 (e.g., Berry and Björkman 1980). C. longifolium has the lowest
rates of photosynthesis regardless of temperature, consistent with its conservative
growth strategy. O. pyramidale and F. insipida, in contrast, are fast growing species
with higher TOpt and AOpt values. They germinate in forest gaps where irradiance
levels as well as temperatures are higher than in the understory where C. longi-
folium typically regenerates.

Direct Effects: Thermodamage

One of the most temperature-sensitive components of plants is photosystem II

(PSII), a protein complex located in the thylakoid membrane of the chloroplast.
PSII efficiency can be readily determined using chlorophyll a-fluorescence tech-
niques (e.g., Krause and Weis 1991). Thermodamage assessment from chlorophyll
fluorescence measurements correlates well with classical analysis of post-heating
necrosis (Krause et al. 2010, 2013). The critical temperature for irreparable leaf
damage is about 52 or 53 °C, depending on whether thermal damage is determined
in the dark or in the light (Krause et al. 2015). Such temperatures are only a few
degrees above leaf temperatures that already occur occassionally in situ in
sun-exposed leaves of tropical forest trees (Krause et al. 2010; Fig. 2). There is
some variation across species in reported thermotolerance, but this may in part
392 M. Slot and K. Winter

Fig. 1 Temperature response curves of net photosynthesis under photorespiratory (21 % O2,
dashed lines, closed symbols), and non-photorespiratory conditions (2 % O2, solid lines, open
symbols) a, and dark respiration b of recently fully expanded leaves of Calophyllum longifolium
(circles), Ficus insipida (triangles), and Ochroma pyramidale (squares) seedlings grown outdoors
under full natural radiation in Panama (mean annual temperature 27 °C). Arrows indicate increases
in TOpt and AOpt with removal of photorespiration. Non-photorespiratory conditions were created
by mixing air entering the cuvette with nitrogen gas at a 1:9.5 ratio. After passing the mixture
through soda lime, CO2 was added to generate a CO2 concentration of 400 ppm. Measurements
were made on attached leaves (n = 3–6) in a temperature-controlled Walz cuvette (Walz GmbH,
Eiffeltrich, Germany) attached to an LI-6252 infrared gas analyzer (Licor). Photosynthesis curves


were fit as: net photosynthesis ¼ b  ðTLeaf  TMin Þ  1  ecðTLeaf TMax Þ . TMin and TMax are the
hypothetical low- and high-temperature CO2 compensation points, and b and c are constants. All
four variables were estimated using a non-linear solver function. Respiration fits are 3rd order
polynomials. For clarity only means are shown in a; in b means ± 1 SEM are shown. Modified
after Slot et al. (2016)

reflect differences in methodology used to assess thermotolerance. In a study

comparing tropical and temperate rainforest tree species in Australia, the leaf
temperature at which irreversible damage occurred was independent of growth
temperature and biome of origin (Cunningham and Read 2006), suggesting minimal
acclimation and phylogeographic predisposition to thermal damage.
The Effects of Rising Temperature on the Ecophysiology … 393

Fig. 2 Comparison of field and laboratory based measurements of net photosynthesis versus leaf
temperature (TLeaf) of Ficus insipida a, and the frequency distribution of daytime TLeaf for this
species in the field b based on 1 month (Jan–Feb, dry season) of continuous monitoring of 6 leaves
with thermocouple wires touching the abaxial surfaces. The inset in a shows the temperature
response of stomatal conductance (GS). Lab measurements were made as described in Fig. 1. Field
measurements were made with an LI-6400 (Licor) between 8 a.m. and noon on a typical dry
season day. The leaves of the *30 m tall study tree were accessed using a canopy crane. The
response curve of field-based measurements is overlaid on the frequency distribution of TLeaf in
b to illustrate the fact that TOpt occurs at the most frequently occurring TLeaf. Error bars represent
1 SEM (n = 4–6). Modified after Slot et al. (2016)

Indirect Effects: CO2 Fixation

Photosynthetic carbon uptake may also be affected by temperature via leaf-to-air

vapor pressure deficit (VPD). Warm air can accomodate more water vapor than cool
air, so at a given absolute moisture content of the air, VPD increases with leaf
temperature, potentially causing stomatal closure. It is very difficult with standard
gas-exchange equipment to keep VPD constant over a large range of leaf temper-
atures. One study that appears to have successfully controlled for VPD reported TOpt
values of 28–29 °C for two rainforest tree species in Costa Rica measured in situ
(Vargas and Cordero 2013), values that are comparable to those reported in Fig. 1, in
which VPD was not controlled. These observations also roughly correspond to
394 M. Slot and K. Winter

decreasing ANet values at temperatures >30 °C that Doughty and Goulden (2008)
observed on three species measured in situ in the Brazilian Amazon, and with
observations of Cheesman and Winter (2013a) of decreasing ANet when TLeaf was
>27–30 °C in three tropical tree species grown in controlled-environment chambers
in Panama. Whereas Vargas and Cordero (2013) maintained VPD < 2.0 kPa at leaf
temperatures above TOpt, VPD in the experiment depicted in Fig. 1 increased from
about 2.0 kPa at TOpt to 8.0 kPa at the upper CO2 compensation point. Nonetheless,
these two studies show similar decreases in net photosynthesis at temperatures above
*30 °C. Insufficient data on VPD-controlled temperature responses of ANet of
tropical trees complicate the interpretation of the role of VPD-induced stomatal
closure in determining TOpt and photosynthetic decline above TOpt.
In upper-canopy tree leaves of tropical forest canopies, the combination of high
temperature, high irradiance and high VPD can lead to pronounced midday
depressions of stomatal conductance and CO2 uptake (e.g., Zotz et al. 1995;
Cernusak et al. 2013; Goldstein et al. this volume, Santiago et al. this volume).
Figure 2 shows changes in net CO2 uptake of F. insipida leaves measured in situ in
the upper-canopy of a tropical forest in Panama as photosynthetic photon flux
density (PPFD), temperature and VPD all increase from morning to noon on a
sunny day. Compared to laboratory-measured seedling leaves (see Fig. 1 for
methods), AOpt of canopy leaves was much higher because these leaves were
acclimated to higher PPFD and had higher leaf mass per area. TOpt was also higher
in the field, probably owing to generally higher leaf temperatures in situ. Whereas
stomatal conducantance and photosynthesis in the field decreased to zero when leaf
temperatures reached 45 °C, in the laboratory net photosynthesis remained positive
up to 50 °C and conductance—after a marked decrease between 30 and 45 °C—
started to increase above 45 °C (Fig. 2). This re-opening of stomata at high tem-
peratures in the laboratory was also observed for O. pyramidale and C. longifolium
(Slot et al. 2016). Nonetheless, in exposed canopy leaves, high heat load caused by
high solar radiation can become so stressful that photosynthetic carbon uptake may
take place mainly during morning hours. During the course of the day depicted in
Fig. 2a, 50 % of the time leaf temperatures exceeded TOpt of F. insipida (Fig. 2b),
stomata were partially closed, and ANet was reduced. Depending on leaf orientation,
the extent to which midday depression occurs may vary considerably, even between
neighboring leaves, or within leaves if they are undulated (e.g., Cecropia; K.
Winter, unpublished data). The variability in leaf-level irradiance and leaf tem-
perature makes stomatal conductance particularly challenging to model and predict
with high spatial and temporal resolution. Given the frequent occurrence of midday
stomatal reductions in tropical trees on sunny days, further understanding of this
phenomenon is warranted to better predict global carbon fluxes in a warming world.

Acclimation

Thermal acclimation is a biochemical, physiological, or morphological adjustment

by individual plants in response to a change in the temperature regime, which
The Effects of Rising Temperature on the Ecophysiology … 395

results in an alteration in the short-term response to temperature (Smith and Dukes

2013). Thermal acclimation of photosynthesis commonly leads to a shift of the
thermal optimum of photosynthesis towards the new growth temperature (Box 1).
This shift results from a change in relative contribution of RuBP carboxylation and
RuBP regeneration in controlling net photosynthesis. The optimum temperature of
RuBP regeneration is higher than that of RuBP carboxylation (Kirschbaum and
Farquhar 1984; Hikosaka et al. 2006). Warm-acclimated plants tend to have a lower
Jmax/VCmax ratio than cool-grown control plants (e.g., Bernacchi et al. 2003). When
Jmax/VCmax is low, RuBP regeneration—with its relatively high TOpt— exerts
greater control over net photosynthesis than when Jmax/VCmax is high in cool-grown
plants, and as a result TOpt of net photosynthesis is higher in warm-acclimated
plants (Hikosaka et al. 2006). If the Jmax/VCmax ratio is not reduced by high tem-
perature, TOpt may still increase if the activation energy of VCmax increases more
with growth temperature than that of Jmax (Hikosaka et al. 2006).
Consistent with thermal acclimation, TOpt of C. longifolium seedlings grown in
controlled-environment chambers increased with growth temperature (Fig. 3), but

Fig. 3 The optimal temperature of photosynthesis (TOpt) (a), and net photosynthesis at TOpt (AOpt)
(b) plotted against growth temperature of Calopyllum longifolium seedlings (mean ± 1 SEM).
Seedlings were grown in individual pots (2.8 l) in commercial potting soil in growth cabinets
(Environmental Growth Chambers, Chagrin Falls, OH, USA) at day/night temperatures of 25/19,
30/24, 35/29, 35/29 + elevated RH, and 39/33 °C. Plants from the 39/33 °C did not have enough
live leaves for photosynthesis measurements (see Fig. 4). Net photosynthesis was measured with
an LI-6400 (Licor) at 20, 25, 30, 35, and 40 °C on one leaf per seedling (n = 6/treatment) after
equilibration for at least 45 min in growth cabinets set to the target temperature. TOpt was
calculated as described in the caption of Fig. 1. In one 35/29 °C cabinet relative humidity was
increased to *90 % (as opposed to *45 %) by maintaining a pot of water near boiling point in the
cabinet during the light period
396 M. Slot and K. Winter

there is a limit to this adjustment. Plants grown at 25/19 °C (day/night) and 30/24 °C
had TOpt values close to their daytime growth temperature, whereas plants grown at
35/29 °C had a TOpt of 30 °C, suggesting that, at least for this late-successional
species, 30 °C represents the maximum TOpt at current CO2 concentrations. While
TOpt shifted towards the growth temperature, AOpt decreased with increasing growth
temperature. Way and Yamori (2014) call this detractive adjustment to warming, as
opposed to constructive adjustment (see Box 1). The exception to this pattern was the
35/29 °C treatment associated with elevated relative humidity (*90 % as opposed to
*45 %), for which both TOpt and AOpt were highest among all treatments. This may
indicate that part of the decrease in AOpt relative to growth temperature resulted from
temperature effects on VPD, with higher stomatal conductance being maintained
when plants were grown at elevated relative humidity.
Kositsup et al. (2009) grew Hevea brasiliensis Müll. Arg. seedlings at 18 and
28 °C and also found that TOpt adjusted to growth temperature. They further
observed that ANet, VCmax and Jmax all increased with increased growth tempera-
ture, suggesting constructive acclimation. However, 18 °C is probably sub-optimal
for lowland tropical species such as H. brasiliensis, and the observed adjustments
may indicate that 28 °C is closer to the optimum temperature for this species, rather
than indicate strong constructive thermal acclimation. Doughty (2011) warmed
leaves of trees and lianas (woody vines) in the Brazilian Amazon and found no
acclimation of ANet. The decrease in photosynthesis with warming was assigned to
leaf damage caused by occasionally very high leaf temperatures of experimentally
warmed leaves during sunny spells. Similarly, C. longifolium plants grown in
controlled-environment chambers at 39/33 °C (day/night) showed severe leaf
damage and photosynthesis could not be measured (Fig. 4).
Dusenge et al. (2015) reported that VCmax was similar between leaves of trees
from two tropical rainforest sites in Rwanda differing in temperature regime,

Fig. 4 The effect of growth temperature on total biomass (mean ± 1 SEM of 6 seedlings per
treatment) and biomass allocation in Calophyllum longifolium seedlings, with photographs of
representative plants of each treatment at final harvest
The Effects of Rising Temperature on the Ecophysiology … 397

whereas Jmax was significantly lower at the warmer site, resulting in a reduced Jmax/
VCmax, in line with observations on temperate species. The physiological plasticity
notwithstanding, ANet was reduced at the warmer site compared to the cool site,
suggesting detractive adjustment, similar to observations on C. longifolium (Fig. 3).
We still know little about the thermal acclimation potential of VCmax and Jmax of
lowland tropical species, and to date no study has compared the acclimation
potential of VCmax and Jmax of tropical and temperate tree species. Such experi-
mental studies are needed to better predict the effect of long-term warming on the
photosynthetic properties of tropical forest vegetation.

Adaptation

There is at least one comparative study that points to fundamental differences in the
physiological properties of species adapted to temperate versus tropical conditions.
Cunningham and Read (2002) reported higher TOpt values for tropical than tem-
perate species at a given growth temperature. Furthermore, the temperature
response curve for temperate species was wider, i.e., temperate species had pho-
tosynthesis rates of >80 % of AOpt over a larger temperature range. These results are
consistent with the absence of strong selection for a broad temperature range of
photosynthesis for tropical species. We found that TOpt of tropical species is lower
than growth temperature when growth temperatures exceed *30 °C (Fig. 3). The
narrower curves of tropical species and the apparent limit to increasing AOpt,
despite a small increase in TOpt, suggest that significant warming in the tropics may
cause a decline in photosynthetic carbon uptake.

Dark Respiration

Temperature Response

About 30 % of the carbon fixed by tropical forests through photosynthesis is

released back into the atmosphere by foliar respiration (Chambers et al. 2004; Malhi
2012). Respiration is vital for plant growth and survival, supporting biosynthesis,
cellular maintenance and repair, but from a carbon-balance perspective respiration
represents a loss.
In the short term, dark respiration increases with temperature, peaks with a
TOpt > 50 °C, and then steeply declines. The initial increase is often assumed to be
exponential, and can be expressed as a Q10 value—the proportional increase in
respiration with 10 °C warming (Box 1). The general assumption is that respiration
rates double for every 10 °C warming, resulting in a Q10 of 2.0, although in reality a
wide range of Q10 values—from *1.4 to 4.2— has been reported (Atkin et al.
2005, and references therein). Leaf respiration of tropical forest species is at least as
sensitive to short-term temperature increase as that of temperate species, with Q10
398 M. Slot and K. Winter

Box 1. Photosynthesis and respiration are highly sensitive to temperature, but the effects depend
on the timescale of exposure. Long term warming (e.g., weeks to months) may modify the
short-term response through acclimation, i.e., the biochemical, or structural adjustment by
individual plants in response to a new temperature regime
The Effects of Rising Temperature on the Ecophysiology … 399

values ranging from 1.5 to 4.1 (Meir et al. 2001; Cavaleri et al. 2008; Slot et al.
2013, 2014b), and averaging above 2.0 (Slot et al. 2013, 2014b). Figure 1b shows
respiration-temperature response curves for leaves of C. longifolium, F. insipida,
and O. pyramidale. Notably, the response-curves (n = 3–6) are not exponential.
Over a relatively narrow temperature range it is difficult to distinguish different
shapes of temperature response curves, but the examples in Fig. 1b cover a range of
*25 °C, and an exponential curve is clearly not an appropriate approximation. We
do not know whether the data shown in Fig. 1b reflect a uniquely tropical phe-
nomenon, but a recent study with Oryza sativa L. (rice) reported similarly linear
temperature responses of respiration over a *14 °C range (Peraudeau et al. 2015).
In contrast, measurements over a broad temperature range on the temperate
Eucalyptus pauciflora suggest a good exponential fit up to critical temperatures
around 50 °C (O’Sullivan et al. 2013), whereas Hüve et al. (2012) showed con-
siderable variation in the shape of the response curve over a *25 °C range across
three temperate herbs. Modeling temperature responses using an exponential Q10 or
Arrhenius-type fit when a linear fit better describes the actual response could lead to
overestimation of respiration rates at high temperatures. Future research will need to
assess how widely distributed the non-exponential temperature responses of dark
respiration are among tropical species.

Acclimation

Nighttime temperatures increase more rapidly than daytime temperatures (e.g.,

Easterling et al. 1997), potentially leading to increased respiration costs in tropical
forest systems. However, acclimation of respiration might mitigate this. Respiration at
a given temperature is generally decreased in warm-acclimated plants compared to
control plants, either through down-regulation of respiratory capacity at all tempera-
tures, or because the short-term temperature sensitivity in warm-acclimated plants is
reduced, leading to lower rates at intermediate to high temperatures (Atkin and Tjoelker
2003; see Box 1). Recently, we showed that upper-canopy leaves of tropical canopy
trees and lianas acclimate to nighttime warming (Slot et al. 2014a). Acclimation has
also been shown in seedlings of tropical tree species grown under different temperature
regimes in controlled-environment chambers and open-top chambers (Cheesman and
Winter 2013b). In fact, when accounting for the degree and duration of warming there
is no indication that tropical species differ from species from other biomes in their
capacity for thermal acclimation of respiration (Slot and Kitajima 2015).
At the whole-plant level, respiratory acclimation can be affected by interactions
with mycorrhizal symbionts (Atkin et al. 2009). The only study to date that has
addressed these interactions for tropical tree species indicated a strong
species-specific effect of mycorrhizal colonization of roots on acclimation of
whole-plant respiration to nighttime warming (Fahey et al. 2016). The host
species-specific nature of the effects of mycorrhizae may complicate generalizations
of acclimation trends in vegetation models, and calls for more research into the
mechanisms behind these interactions.
400 M. Slot and K. Winter

Adaptation

Respiration rates at ambient temperature vary considerably across biomes, with

rates increasing twofold from the Arctic to the tropics (Atkin et al. 2015). This
doubling over a *20 °C range in growing season temperature represents a con-
siderable deviation from the much steeper instantaneous temperature response.
Respiration standardized to 25 °C is threefold lower in the tropics than in the Arctic
(Atkin et al. 2015), suggesting significant downregulation of respiratory capacity in
warm-adapted species. These global patterns may reflect adaptation to different
climates, but model simulations by Vanderwel et al. (2015) show that accounting
for acclimation to local temperature regimes produces very similar patterns in
simulated respiration across global temperature gradients. Given that the capacity
for acclimation is common across the globe (Slot and Kitajima 2015) and sufficient
to explain global patterns, it appears that there may not have been further selective
pressure leading to adaptive temperature responses of respiration.

Volatile Organic Compounds and Thermoprotection

Volatile organic compounds (VOC) can contribute significantly to the carbon

emissions from forests. The most common VOCs are isoprenes and monoterpenes,
and the emission of both increases with short-term warming in the tropics (Keller and
Lerdau 1999; Bracho-Nuñez et al. 2013). Isoprene emission is hypothesized to
protect photosynthesis from short, high-temperature episodes (Sharkey and Yeh
2001; Sasaki et al. 2007) by helping stabilize thylakoid membranes (Velikova et al.
2011), quenching reactive oxygen species (Velikova et al. 2012; Jardine et al. 2013,
2014), and/or increasing heat dissipation (Sasaki et al. 2007; Pollastri et al. 2014). In
the short term (minutes to hours), isoprene emission increases exponentially with
temperature, both in temperate (Sharkey and Monson 2014) and tropical trees (Keller
and Lerdau 1999), but above 38–40 °C emissions may decrease (Tingey et al. 1979;
Alves et al. 2014; Jardine et al. 2013, 2014). TOpt of isoprene emission is *10 °C
higher than TOpt of net photosynthesis. Consequently, at high temperatures isoprene
synthesis requires carbon sources other than recent photosynthates. Photorespiration
may provide such an alternative source at temperatures exceeding TOpt of photo-
synthesis (Jardine et al. 2014). Controlled-environment studies with temperate spe-
cies have shown that plants acclimated to higher growth temperature have a higher
capacity for isoprene release than plants grown at moderate temperatures (Tingey
et al. 1979; Monson et al. 1992), but there is currently no evidence to suggest that
warm-adapted tropical species have higher emission rates than temperate species.
Despite its potential importance in thermoprotection, isoprene emission does not
occur in all plants. It only occurs in perennial plants with C3 photosynthesis (Loreto
and Fineschi 2015), but without a clear phylogenetic distribution, due in part to
frequent loss and secondary acquisition of the trait (Monson et al. 2013). In the
tropics isoprene emission is equally common in deciduous and evergreen plants,
The Effects of Rising Temperature on the Ecophysiology … 401

whereas emission is comparatively rare in temperate evergreens (Loreto and

Fineschi 2015). Tambunan et al. (2006) studied isoprene emission in 42 tropical
tree species and reported high rates in 4 species, very low rates (<10 µg g−1 h−1) in
28 species, and non-detectable rates in 10 species. Of the 51 tropical tree and lianas
studied by Keller and Lerdau (1999), only 15 emitted isoprene at detectable rates.
Even for the latter species, the total contribution of emission of isoprene to the
carbon balance was relatively small, with an overall mean rate of 24 nmol m−2 s−1
(*65 µg g−1 h−1 at mean leaf mass per area of 90 g m−2) at 30 °C and PPFD of
1000 µmol m−2 s−1, which is *500 times lower than the mean photosynthesis rate.
It is likely that long-term warming will increase rates of isoprene emission from
leaves of isoprene-emitting species (Sharkey and Monson 2014), but given the
thermoprotective role these emissions appear to play, the loss of isoprene carbon is
probably more than compensated for by the maintenance or recovery of photo-
synthetic functioning during episodic heat.

Whole-Plant Temperature Effects

Biomass Accumulation

Two meta-analyses suggest that plant growth decreases with warming when starting
temperatures are already high (Way and Oren 2010; Lin et al. 2010); in both studies
tropical species were underrepresented. Figure 4 shows the effect of combined day
and nighttime warming on growth of C. longifolium. Growth was optimal at 35/29 °
C (day/night), i.e., at temperatures well above those in its natural habitat in the
forest understory. Several studies show that nighttime warming stimulates growth
in seedlings of tropical tree species (Esmail and Oelbermann 2011; Cheesman and
Winter 2013a, b). These seedling responses contrast with results obtained for
tropical canopy trees, which suggest a negative correlation between nighttime
temperature and tree growth (Clark et al. 2003, 2010, 2013; Vlam et al. 2014;
Anderegg et al. 2015a). A recent study on Eucalyptus species across a temperature
gradient in Australia reported that, compared to small trees, big trees show a dis-
proportionally strong decline in growth with increasing mean annual temperature
(Prior and Bowman 2014). Perhaps ontogenetic differences in temperature sensi-
tivity govern the contrasting temperature effects on tropical canopy trees and
seedlings. Leaf area ratio (leaf area divided by total plant mass) decreases with
ontogeny, so canopy trees have proportionally less photosynthetic material with
which to support the maintenance of non-photosynthetic tissue than seedlings. If the
capacity for thermal acclimation of root and stem respiration is smaller than that of
leaf respiration, then warming would increase the respiration load in canopy trees
more strongly than in seedlings. There is no indication that acclimation of root
respiration is lower than that of leaf respiration in temperate species (Loveys et al.
2003), but little is known about thermal acclimation of root and stem respiration in
the tropics beyond the observation by Fahey et al (2016) that acclimation of
whole-plant- and root respiration varied greatly among species.
402 M. Slot and K. Winter

In in situ studies of growth-temperature relationships—using latitudinal or ele-

vational temperature gradients, or inter-annual trends in temperature—temperature
is one of multiple factors that change, and patterns of biological response cannot be
assigned to temperature differences alone. Controlled-environment chambers, on
the other hand, enable the isolated study of temperature effects. However, in
controlled-environment studies with potted seedlings, soil temperature may track
changes in air temperature more closely than in the field, and soil warming itself
may increase growth (Königer and Winter 1993; Holtum and Winter 2014). Forest
soils are thermally very stable, so soil processes may explain at least part of the
observed contrasting responses of seedlings and canopy trees to nighttime warming.
Soil warming may increase nutrient mineralization rates (Jarvis and Linder 2000),
thereby stimulating growth. However, we found that nighttime warming stimulated
growth of O. pyramidale seedlings equally in fertilized and non-fertilized soils (Slot
and Winter unpublished data). Altered source-sink relationships (Pilkington et al.
2015) may provide an alternative, though not yet tested explanation for the
observed responses.

Mortality

A quantitative trait locus (QTL) for thermotolerance has been identified for the
comparatively heat-tolerant Oryza glaberrima Steud. (African rice), the overex-
pression of which in O. sativa L., Arabidopsis thaliana L., and Festuca arundi-
nacea Schreb., significantly reduced their mortality following a 12 day 38/35 °C
treatment (Li et al. 2015). The QTL is associated with degradation of cytotoxic
denatured proteins that accumulate during heat exposure, suggesting an important
role for the proteins encoded by the QTL in mitigating warming-induced cell death
and plant mortality. Several other factors may play a role in warming-induced
mortality. For example, increased rates of respiration and decreased rates of pho-
tosynthesis could lead to carbon starvation. Atmospheric drought caused by
temperature-induced increase in VPD may also kill plants. It is hard to disentangle
drought and temperature effects, as soil moisture availability may prevent
warming-induced carbon starvation by enabling transpirational leaf cooling and
maintenance of a positive carbon balance during heat events (Bauweraerts et al.
2014), and carbon reserves in the form of soluble carbohydrates may prevent
drought-induced hydraulic failure (O’Brien et al. 2014). Drought is a common
agent of mortality in the tropics (e.g., Condit et al. 1995; Allen et al. 2010), subject
of observational (e.g., Condit et al. 1995; Phillips et al. 2010) and experimental
studies (e.g., Slot and Poorter 2007; Nepstad et al. 2007), but atmospheric drought,
such as occurs during warming, is much less studied (Breshears et al. 2013).
In the C. longifolium study depicted in Fig. 4, daytime temperature of 39 °C and
relative humidity of *29 % was lethal for most seedlings. We do not know
The Effects of Rising Temperature on the Ecophysiology … 403

whether the well-watered seedlings died from cytotoxicity, carbon starvation, or

hydraulic failure, but the fact that TOpt and AOpt at 35/29 °C were higher under
elevated relative humidity (Fig. 3), shows that atmospheric drought can negatively
impact the maintenance of a positive carbon balance, and potentially survival.
Tropical sapling mesocosms grown outdoors in Panama, with daytime warming of
*5 °C did not negatively impact biomass accumulation and photosynthetic traits as
long as plants had access to soil water (Slot and Winter unpublished data), further
highlighting the interconnected nature of heat and drought as agents of plant
mortality.
Elevated CO2 improves both the carbon balance and water use efficiency of
plants, but a recent greenhouse study on Eucalyptus radiata A.Cunn. ex DC sug-
gests that negative effects of elevated temperature on drought-induced mortality are
not alleviated by elevated CO2, despite higher leaf-level water use efficiency in the
high CO2 treatment (Duan et al. 2014). Thus, drought-induced mortality may occur
in parts of the tropics where warming is accompanied by decreased precipitation
(Olivares et al. 2015). Furthermore, abiotic climatic changes are likely to interact
with biotic sources of mortality such as insect outbreaks (Anderegg et al. 2015b).
For example, warming can affect phytochemistry and the feeding efficiency of
invertebrate herbivores (Jamieson et al. 2015), potentially leading to increased leaf
loss and plant mortality.

Reproduction

There have not been any detailed experimental studies on how rising temperatures
affect reproduction of tropical vegetation, although the reproductive phase is one of
the most temperature-sensitive parts of the lifecycle of plants. Pollen production,
pollen viability and pollen tube growth all decrease with warming in a range of crop
species (Sage et al. 2015, and references therein). There is considerable variation in
temperature sensitivity across genotypes and species, but no clear relationship
between ambient growth environment and thermal sensitivity (Prasad et al. 2006).
Pollen viability of the tropical tree Mangifera indica L. (mango) decreases above
33 °C (Issarakraisila and Considine 1994), which is not an unusually high tem-
perature in the tropics. Many tropical species flower for only short periods and risk
reproductive failure if flowering coincides with anomalously high temperatures.
Surprisingly, flower production correlated positively with temperature both sea-
sonally and interannually in tropical forests in Panama and Puerto Rico (Pau et al.
2013). Increased flower production could compensate for decreased pollen viability
but detailed study is required to better understand temperature effects on tropical
tree reproduction and to disentangle direct warming effects on plant fertility, and
warming effects on reproductive allocation.
Temperature may also affect reproduction through its effect on pollinators. For
example, fig-pollinating wasps—which develop inside developing figs—die at
404 M. Slot and K. Winter

temperatures only a few degrees above current ambient temperatures (Patiño et al.
1994). Transpirational cooling helps maintain fruit temperatures in non-lethal
ranges, but further warming could have major negative consequences for fig
reproduction.
Exposure to high temperature is necessary to break physical dormancy of seeds
of many species. This is especially common for species that form seed banks, as the
high temperature is associated with high light conditions favorable for seedling
establishment of these early-successional species. More intense heatwaves (Meehl
and Tebaldi 2004) could potentially trigger germination under conditions not
favorable for seedling establishment, leading to mortality. The potential effects of
climate change on the seed ecology of tropical forest trees is not well understood
(Walck et al. 2011).

Stand-, Ecosystem-, and Biome-Level Temperature Effects

An important aspect of tropical forests is their very high species diversity. All trees
ultimately use—and often directly compete for—the same resources, and species
coexistence is at least in part maintained by niche specialization along resource
gradients (e.g., Kitajima and Poorter 2008; Condit et al. 2013). This means that
climate warming may shift the competitive balance within a forest community if
rising temperature differentially affects mortality and reproduction across species.
For example, warming may increase soil mineralization rates in the tropics (Salinas
et al. 2011). Tropical tree species vary widely in their phosphorus affinity (Condit
et al. 2013), and temperature-induced changes in nutrient availability potentially
contribute to shifts in species composition. This may result in reduced diversity, or
a change in the dominant species and functional types associated with a particular
nutrient regime. Climate-induced changes in species composition will affect forest
growth (Coomes et al. 2014). Systematic changes in growth rates of trees may also
cause turnover rates in tropical forests to increase (Phillips and Gentry 1994).
Nevertheless, changes in tree growth rates and turnover do not necessarily change
ecosystem carbon storage if the size structure of trees within the ecosystem is
maintained (Körner 2009).
Tropical ecosystems have lower ratios of NPP over gross primary productivity
(GPP) than most higher latitude ecosystems (Zhang et al. 2009, 2014). Furthermore,
rising temperatures decrease the NPP/GPP ecosystem carbon use efficiency (Zhang
et al. 2014) suggesting that, despite observed thermal acclimation capacity at the
leaf level, warming causes ecosystem-level respiration cost to increase. Soil res-
piration is a major component of ecosystem respiration, and soil respiration rates in
tropical forests are higher than in any other ecosystem in the world (Raich and
Schlesinger 1992). The capacity of tropical soil respiration to acclimate to higher
temperatures is unknown.
The Effects of Rising Temperature on the Ecophysiology … 405

Concluding Remarks

Because most research on temperature effects on the ecophysiology of plants has

been done on non-tropical species, much is still to be discovered about how tropical
trees will respond to climate change. We have a fairly sound understanding of
general principles of temperature responses at the organelle and leaf level (Table 1),
but we do not know whether tropical trees differ systematically from non-tropical
species in how warming affects leaf and whole-plant performance. For example,
more research is needed to establish the generality of detractive acclimation of
photosynthesis in tropical species, as observed in C. longifolium (Fig. 3). We have
shown that the commonly assumed exponential increase of respiration with tem-
perature may not apply to tropical leaves over wide temperature ranges, a finding
that requires further confirmation. At this point, we can only speculate on the whole
tree-level effects of warming, apart from noting that warming is associated with
atmospheric drought and may affect reproduction. At the stand level, warming may
exacerbate midday reductions in stomatal conductance. A better mechanistic
understanding of the causes and consequences of midday stomatal closure will
improve our ability to translate understanding based on individual leaf responses to
stand-level photosynthesis simulations.
In the decades to come the tropics will experience further increases in atmo-
spheric CO2 concentrations and warming, and significant alterations in the timing
and amount of rainfall (Diffenbaugh and Scherer 2011; Mora et al. 2013). The
vulnerability of tropical forests to climate change is under much debate (e.g., Clark
2004; Lloyd and Farquhar 2008, Lewis et al. 2009; Booth et al. 2012; Randerson
2013). Because of the large contribution of tropical forests to the global carbon
cycle, a better understanding of how these forests respond to climate change drivers
will improve our ability to predict future climate and biogeochemical cycling at the
global scale (Booth et al. 2012; Huntingford et al. 2013; Piao et al. 2013).
Information on thermal acclimation of photosynthetic parameters VCmax and JMax
will be crucial to improve predictive models De Kauwe et al. (2016). We can learn a
lot about plant-temperature interactions from elevation gradients in the tropics
(e.g., Malhi et al. 2010), but these gradients do not reveal how plants at the
high-temperature end of the gradient will respond to further warming, and that is
precisely the key in determining the fate of tropical lowland forests in a warming
world. As global warming generates novel climate regimes in tropical latitutes,
maintenance of current forest structure requires processes of thermal acclimation to
occur in conjuction with adjustments to changing precipitation regimes (Mora et al.
2013)—and possibly changes in cloud cover—under gradually rising ambient CO2
concentrations and increasing atmospheric deposition of nutrients (Hietz et al. 2011).
Clearly, in situ warming experiments of entire forest segments are needed to better
assess the effects of rising temperatures on tropical vegetation (Cavaleri et al. 2015).

Acknowledgements This work was supported by the Smithsonian Tropical Research Institute.
M.S. was recipient of a CTFS-Forest-GEO postdoctoral fellowship. Milton Garcia assisted with
in situ canopy measurements.
406 M. Slot and K. Winter

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Tree Biomechanics with Special Reference
to Tropical Trees

Karl J. Niklas

Abstract All structures, whether engineered or natural, must obey the same
physical laws and processes. Trees are particularly susceptible to these laws and
processes because they are structures, composed mostly of wood, that begin and
end their lives in the same location, which can experience dramatic changes in
abiotic and biotic conditions (e.g., rainfall and epiphyte loads, respectively). The
biomechanical behavior of trees is reviewed by presenting and discussing a few
equations, with a particular emphasis on the effects of wind on branches, trunks,
and roots. Limited space precludes a detailed review of these equations. Therefore,
some basic references are listed to provide the necessary details. An important point
is that unlike engineered objects and the engineering theory that deals with them,
trees are growing biological entities that violate many of the assumptions of
engineering theory. Consequently, the equations presented here provide only a first
order approximation of how trees will respond to static (self) and dynamic (wind)
loadings. Understanding the limits of these equations, therefore, is a critical first
lesson in dealing with the biomechanical behavior of trees, regardless of whether
they grow in tropical, temperate, or desert conditions. In the final analysis, every
tree will ultimately fail. The challenge is to anticipate when and how.

Keywords Biomechanics Buckling

Dynamic loading
Maximum height

Static loading Trees Wind

Introduction

The goal of this chapter is to provide an overview of the basic physical principles
and phenomena that influence the mechanical behavior of trees. This overview
revolves around eight biomechanical features that hold true for all trees, regardless

K.J. Niklas (&)

Plant Biology Section, School of Integrative Plant
Science Cornell University, Ithaca, NY 14853, USA
e-mail: kjn2@cornell.edu

© Springer International Publishing Switzerland 2016 413

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_19
414 K.J. Niklas

of their habitat: (1) trees sustain two general categories of mechanical forces (static
loads and dynamic loads), (2) these forces are additive (stresses as well as strains
are additive), (3) static loads increase slowly over time as trees increase in size and
as epiphytes, if any, increase in number or size (therefore, tree growth patterns can
compensate for these increasing loads), (4) dynamic loads can change dramatically
over short periods of time (these loads are unpredictable and therefore potentially
dangerous), (5) trees generally fail as a result of dynamic loads, (6) plant tissues
resist bending more than twisting (eccentric loadings are potentially dangerous),
(7) young parts of woody plants are more flexible than older parts, and (8) be-
lowground growth generally does not keep pace with aboveground growth. Each of
these claims will be explored in the following sections.
However, before exploring these topics, it is important to emphasize that trees
grow and respond to their mechanical environment. This may seem trivial, but it is a
vital fact. Fluid and mechanical engineering makes a number of assumptions that
are consistently violated by anything that grows organically. For example, engi-
neering theory by and large assumes that a structure is composed of materials that
are homogeneous and elastic in behavior. No animal or plant tissue is homogeneous
and every tissue is viscoelastic. Engineering practice deals with structures that are
fabricated to meet specific specifications for a particular work-place environment.
Natural selection has no agenda. Perhaps most important is the fact that an engi-
neered structure cannot heal itself and cannot change its size, with the exception of
corrosion. Every organism has the capacity to replace damaged parts and every
organism changes size as it grows, reproduces, and ultimately dies. Trees grow in
response to their local environment in ways that cannot be modeled easily nor
comprehended fully. Engineering theory also typically deals with small deflections,
whereas trees often experience extremely large deflections. For these reasons, many
of the assumptions made in engineering theory and practice are naïve in the context
of tree biology. Consequently, the principles presented in this chapter can provide,
at best only guidance when predicting the mechanical behavior of trees.
As noted, the concepts presented in this chapter pertain generally to all trees,
regardless of whether they grow in the tropics, deserts, or in temperate ecosystems.
However, tropical trees flourish under some conditions that would seem to set them
apart. For example, many tropical trees have buttressed root systems that have been
interpreted to function as anchorage stabilizers in moist or soft soils. Tropical trees
tend to have greater epiphyte loads than trees growing in most other types of
ecosystems. They can also have large liana loads that additionally entangle the
branches of neighboring trees in ways that can affect dynamic dampening.
Likewise, arboreal animals and large fruits often distinguish tropical trees, which
suggests greater canopy dynamics and seasonal variations in self-loading compared
to trees in other ecosystems. Finally, dense stands of trees growing in low latitudes
often experience limited light availability during the early and late daylight hours.
These and other features seem to set tropical tree biomechanics apart from tree
biomechanics in general. Nevertheless, with few exceptions, as for example but-
tressed root systems, which present a unique morphological and biomechanical
context, these and other differences are a matter of degree and not of kind. For
Tree Biomechanics with Special Reference to Tropical Trees 415

example, the deflection of a cantilevered uniformly loaded beam, which can be used
to model tree branches, depends on the load per unit length (see Eq. 15), regardless
of whether the load is solely due to self-loading or involves additional loads
resulting from epiphytes.
Finally, space precludes giving the derivations for the equations presented here.
The derivations of these equations are provided by Niklas (1992) and Niklas and
Spatz (2012), and in additional literature, which is cited as required.

Static and Dynamic Loadings

In biomechanics, any internally or externally applied force is referred to as a load.

There are two general types of loads—static loads and dynamic loads, denoted as Ps
and Pd, respectively. Static loads (also called self-loads) are the result of gravity
acting on the aboveground parts of a plant. They are the product of mass m and the
acceleration of gravity g:
Ps ¼ mg: ð1Þ

Although the numerical value of g differs as a function of altitude, this variation is

irrelevant to dealing with tree mechanics. The conventional standard is
g = 9.80665 m/s2.
Dynamic loads are externally applied forces such as the pressure exerted by
wind, the collision of stems or leaves with other stems or leaves, or the activities of
animals in a canopy. The most pervasive dynamic load is wind pressure, which
produces a drag force, denoted as Df. This force is the product of air density ρ, wind
speed U squared, projected (sail) area Sp, and a dimensionless parameter called the
drag coefficient CD:

Df ¼ 0:5 q U 2 Sp CD ð2Þ

CD is often assumed to be a constant for computational ease. However, it is not a

constant for plants because leaves and stems reorient with respect to oncoming
wind and thus reduce the numerical value of this “constant” (Vogel 1981). This
reorientation also typically reduces Sp. Consequently, under some conditions, the
drag force exerted by wind can be reduced even if wind speed increases. This
phenomenology and the loss of leaves, twigs, and branches in strong winds can
increase the safety factor of a tree (Niklas and Spatz 2000).
Mechanical loads are additive. Therefore, the total load experienced by a tree Pt
is given by the formula

Pt ¼ Ps þ Df ¼ mg þ 0:5 q U 2 Sp CD : ð3Þ

Because loads are vectors (i.e., they have direction and magnitude), Eq. 3 is a vector
equation.
416 K.J. Niklas

Fig. 1 The drag force exerted on a vertical cylinder (with a radius of 0.03 m and a length of 1.5 m)
subjected to different uniform wind speeds. It is important to note that vertical wind speed profiles
are never uniform. Under natural conditions ambient wind speeds increase from zero at
ground-level to their maximum with increasing distance from ground level

With the aid of a few simplifying assumptions, Eqs. 1–3 can be used to evaluate
whether static or dynamic loads contribute most to the total load. Consider a vertical
cylinder with a radius of 0.03 m and a length (height) of 1.5 m subjected to a
uniform wind speed of 11 m/s. Assuming that it is composed of wood with a
density of 844 kg/m3 (which is the average density of green conifer and angiosperm
wood; see Niklas and Spatz 2010), Eq. 1 shows that the static load equals π
(0.03 m)2 × 1.5 m × 844 kg/m3 × 9.80665 m/s2 ≈ 35.09 kg m s−2 or 35.09 N. With
an ambient temperature of 20 °C, the density of air is 1.2041 kg/m2. Assuming that
the drag coefficient is approximately 1.0, Eq. 2 shows that the drag load equals
0.5 × 1.2041 kg/m3 × (11 m/s)2 × 0.06 m × 1.5 m × 1.0 ≈ 6.56 kg m s−2 or 6.56 N.
Consequently, the drag load exerted on this hypothetical cylinder by air moving at
11 m/s is a small component of the total load. This situation changes as the ambient
wind speed increases because the drag force scales as the square of wind speed
(Fig. 1).
However, as we will see, what really matters are the stresses that develop at the
base of the column when subjected to its own compressive load and to the stresses
developed by the wind-induced drag. These stresses can be easily calculated, but
this requires an understanding of other concepts and other formulas (see
Concluding Remarks), which need to be presented first.

Stresses, Strains, and the Elastic and Shear Moduli

A load produces stresses and strains. A stress equals a load P divided by the area
A over which the load is applied, i.e., stress is a force per unit area and thus has
units of kg m−1 s−2 or N/m2. There are three kinds of stresses: compressional
stresses, tensile stresses, and shear stresses (denoted as σ–, σ+, and τ, respectively):
Tree Biomechanics with Special Reference to Tropical Trees 417

r ; r þ ; and s ¼ P=A: ð4Þ

These stresses result when a material is subjected to pure compression, pure

tension, or pure shear. They also result when a material is bent or twisted (Fig. 2).
A strain is a dimensionless measure of deformation. It is typically expressed as a
decimal fraction or as a percentage, e.g., 0.01 or 1 %. Strains can be measured in
different ways. For example, the Cauchy strain ε (also called the engineering strain)
is the change in a reference dimension ΔL divided by the original non-deformed
dimension Lo:

e ¼ DL=Lo ¼ ðLLo Þ=Lo : ð5Þ

The true strain εtrue (also called the logarithmic or Henchy strain) is calculated by
integrating the incremental Cauchy strain:

etrue ¼ ln ð1 þ eÞ: ð6Þ

For small strains (<5 %), Eqs. 5 and 6 yield similar results. For large strains, true
strains should be used. Regardless of which equation is employed, it is always
prudent to report how strains are calculated.

Fig. 2 Transverse and longitudinal distributions of tensile, compressive, and shear stresses (σ+,
σ–, and τ, respectively) in a circular solid cylinder fixed at its base and subjected to bending and
twisting. The magnitudes of each stress are denoted by the stippled lines in each figure. Note that
σ+ and σ– reach their local maximum intensities at the surface of each transection and achieve their
overall maximum the base of the cylinder, and that the bending shear stresses (τb) achieve their
local maximum intensities at the center of each transection and achieve their overall maximum the
base of the cylinder. In contrast, torsional shear stresses (τt) reach their local maximum intensities
at the surface of the cylinder and their overall maximum at the free end
418 K.J. Niklas

Fig. 3 Diagram of shear strains γ developing in a small volume of an isotropic material. The shear
strain equals the deformation in the direction that parallels the direction of the shearing force
divided by the distance over which the shearing force acts. In this illustration the direction of the
shearing force is in the x–axis and the distance over which it acts is the height of the volume, which
is z. Therefore, the shear strain γ equals Δx/z, which in turn equals the tangent of Θ (see Eq. 7)

Shear strains γ are more complicated. Referring to Fig. 3, the shear strain equals
the deformation in the direction that parallels the direction of the shearing force
Δx divided by the distance over which the shearing force acts z:

c ¼ Dx=z ¼ tan H: ð7Þ

Equation 7 is convenient and simple. However, it is not appropriate when shearing

forces produce substantial gradients of deformation within a structure. In this case,
the shear strain must be calculated in its differential form:

c ¼@x=@z: ð8Þ

The ability of a material to resist a load is measured by its elastic modulus

E (also called Young’s modulus) and its shear modulus G, which are given by the
quotient of the appropriate stress and its corresponding strain:

E ¼ r=e ð9Þ

and

G ¼ s=c: ð10Þ

Experimentally, these moduli are calculated by measuring the slope of the linear
portion of bivariate plots of stress versus strain (Fig. 4).
Most materials are less capable of coping with shearing than with compression
or tension because, for most materials, G ≪ E. This fact does not imply that
materials will fail more easily in shearing than in bending. It simply means that
most materials shear more easily. The delamination of wood subjected to bending
looks like a shearing failure, but it is not. It reflects the fact that upon bending wood
Tree Biomechanics with Special Reference to Tropical Trees 419

Fig. 4 A hypothetical bivariate plot of the increasing magnitudes of the stresses and strains (σ and
ε, respectively) developing within a sample of a material subjected to either tension, compression,
or bending. The slope of the linear portion of the stress versus strain plot equals the elastic
modulus E. In this example, non-linear behavior is denoted by the dashed lines, which are
curvilinear

fails more easily in the longitudinal direction than in the radial direction. It is worth
noting further that engineering theory typically deals with what is called pure
tension and pure compression (that is, compression and tension without shearing).
However, this hardly ever happens in reality. Shearing always occurs in one form or
another when a material is bent, compressed, or pulled. The fact that G ≪ E does
help to explain why less force is required to twist a material than to bend it.
However, it is important to draw a sharp distinction between a material and a
structure. A structure can fail in a variety of ways depending upon the type and
direction of loading. Indeed, as we will see, tall and slender structures can bend
gracefully or catastrophically (see Buckling).

The Role of Geometry

Although the ability to resist loads depends on the physical properties of a material
or structure, it also depends on size, shape, and geometry (note that shape and
geometry are not the same thing). Specifically, the ability to resist bending is
quantified as the product of the elastic modulus E and the second moment of area
denoted by I, which is called flexural stiffness. In a similar manner, the ability to
resist twisting is quantified as the product of the shear modulus G and the polar
moment of area J, which is called the torsional stiffness:
420 K.J. Niklas

Flexural stiffness ¼ EI ð11Þ

Torsional stiffness ¼ GJ ð12Þ

Formulas for I and J for different geometries are easily obtained from the literature.
A few are provided in Fig. 5. The second moment of area and the polar moment of
area quantify how the cross sectional geometry, shape, and size of an object con-
tribute to the ability of the object to resist mechanical forces. For a circular cross
section, I = π r4/4 and J = π r4/2, where r is radius. Notice that, in this particular
case, J = 2I, and, second, both I and J increase dramatically as r increases.
Although, J is twice the numerical value of I, the ability of a material or structure to
resist twisting is still much less than the ability to resist bending because, as noted,
the shear modulus G of virtually every material is many times lower than that of the

Fig. 5 Equations for computing the second moments of area (I) and the polar moments of area
(J) of beams, columns, etc. characterized by different transverse geometries and shapes. Note that
in each case J > I. Also note that, with the exception of the circular cross section, the numerical
values of J and I depend on the plane of bending (i.e., the neutral plane), which is denoted in each
figure by n – – – – n. The importance of the plane of bending is shown here by comparing the
formulas for the two elliptical cross sections, which have different (orthogonal) orientations with
respect to the neutral plane
Tree Biomechanics with Special Reference to Tropical Trees 421

elastic modulus E. For example, for structural steel, G = 79 and E = 200 GN/m2,
whereas, for Douglas Fir (Pseudotsuga menziesii) wood at a density of 625 kg/m3,
G = 0.68 and E = 8.3 GN/m2.
A third feature is also important. With the exception of a circular cross section,
the numerical value of I depends on the plane of bending. Consider the formulas for
the second moment of area of a beam with an elliptical cross section (see Fig. 5).
When the major axis of the ellipse is oriented in the vertical direction, I = πa3b/4.
However, when the minor axis is oriented in the vertical direction, I = πab3/4.
Consequently, the same object can resist bending differently depending on its
orientation or the direction of an applied force. This phenomenon is evident when
the cross sections of cantilevered branches or leaf petioles are inspected. Many of
these structures have an elliptical cross section in which the major axis is oriented
vertically. This orientation helps a branch or petiole to resist the pull of gravity, but
it permits sideways deflection in the wind.

Bending and Twisting of Cantilevered Beams (Branches)

We are now in a position to consider bending and twisting moments. A moment,

denoted as M, is the product of an applied load and the lever arm over which the
force acts. This is illustrated for a cantilevered beam of length L fixed at one end
and loaded at its free end (Fig. 6a). Assuming that the beam is uniform in its cross
sectional area and homogenous in its composition, the bending moment at any point
x from its fixed end given by the formula

M ¼ PðLxÞ: ð13Þ

Thus, the bending moment increases linearly from the point-loaded free end toward
the base of the beam where x = 0. The maximum deflection δmax of such a beam
occurs at the free end. It is given by the formula

dmax ¼ PL3 =3EI: ð14Þ

In the case of a uniformly loaded beam, the maximum deflection is given by the
formula

dmax ¼ wL4 =8EI; ð15Þ

where w is the weight of the beam per unit length.

The situation with torsion is more complex. Consider a condition called pure
shear in which a beam is twisted but not bent. Referring to Fig. 6b, the angle of
twist θ results in strains γ that decrease toward the fixed end, and the circular arc
between two points A and B has a length equal to Lγ and rθ, where r and L are the
422 K.J. Niklas

Fig. 6 Diagrams of horizontally cantilevered beams (fixed at one end and free at the other)
subjected to bending (a) and to twisting (b). a The displacement of a beam (with length
L subjected to a point-load P at the free end) from the vertical (δ) increases along the distance
x from the fixed end toward the free end and reaches its maximum (δmax) the free end of the beam
(P). Likewise, the maximum bending moment (Mmax) occurs at the fixed end of the beam where
x = 0 (see Eqs. 13–14). b The material elements in a beam (with length L subjected to a clockwise
torque T) located along line a will be displaced along the dashed line b. The magnitude of the
displacement (the strain) of these material elements (γ) increases from the fixed end toward the free
end. Note that angle of twist θ is equal to the strain γ (see Eqs. 16–17)

radius and the length of the beam, respectively. Assuming that the beam is
homogeneous and elastic and that the distortions are not excessive, the relationships
among the shear stress τ just beneath the surface of the beam, the shear strain γ, the
shear modulus G, and the geometry of the beam (r and L) are given by the formula

s=h ¼ Gðr=LÞ: ð16Þ

The total torque T experienced by the beam is given by the formula

T ¼ GJ ðh=LÞ: ð17Þ
Tree Biomechanics with Special Reference to Tropical Trees 423

Buckling

Bending can result in buckling. This phenomenon results from the addition of a
load that exceeds the maximum load that a column can sustain. Once this critical
load is reached, the column undergoes mechanical instability that can lead to
mechanical failure. Two forms of failure are possible, compressive (crushing)
failure or buckling. Which of these occurs depends on the ratio of a column’s radius
r to its length L. The value of the quotient that characterizes the transition from one
mode of failure to the other is given by the equation

1=2
r=L ¼ ð4=pÞ rcomp =E ; ð18Þ

where σcomp is the maximum compressive stress a material (such as wood) can
sustain. Equation 18 shows that very short and thick columns will undergo com-
pressive failure, whereas tall and thin columns are more likely to bend under the
applied load.
The load exerted on a tree trunk increases annually due to the addition of new
leaves and branches and the loading condition of the trunk can be stylized as a point
load at the top of a vertical column. The girth of a tree trunk also increases as a
result of the annual addition of wood. However, different trees attain different r/L as
they get older as a result of species-specific differences (e.g., Populus versus
Quercus) and differences in local growing conditions (e.g., shaded habitats versus
sunny habitats). Although it is conceivable that a trunk might undergo compressive
(crushing) failure, a far more common response to applied loads is bending (Fig. 7).
Assuming that a slender trunk has a solid cross section, the critical load is given by
the formula

Pcrit ¼ p2 EI=ð2LÞ2 ; ð19Þ

where L is the length (height) of the column. The equation describes what is called
Euler buckling in honor of the great mathematician Leonhard Euler (1707–1783)
who derived it. Euler’s equation shows that the elasticity of the material (wood)
used to construct a column (trunk) determines the load bearing capacity of the
column. It also shows that the critical load is directly proportional to the second
moment of area of the column. Thus, the load bearing capacity of the column can be
increased by using a material with a higher elastic modulus, or by maximizing the
second moment of area. In general, denser materials such as woods have higher
elastic moduli, but a denser material contributes more weight per unit volume,
which decreases the critical load because of increased self-loading.
An alternative to increasing the elastic modulus of a column is to distribute the
material as far from the principal axis of the cross section as possible without
incurring local buckling. This can be seen by dividing the critical load of a hollow
column by the critical load of a solid column with the same material and the same
424 K.J. Niklas

Fig. 7 Diagrams illustrating Euler (long-wave) buckling and Bazier (short-wave) buckling in a
slender vertical thin-walled tube subjected to a point-load (P, which equals the point-mass m times
the acceleration of gravity g) at the tube’s free end. In each case the original undeformed tube and
point-mass are indicated by dashed outlines. In Euler buckling, the column deflects under the
point-load and the displacement along the horizontal plane (Δx) increases along the length of the
column (L). In Brazier buckling, the tube deflects from the vertical (not shown) and its circular
cross sections gradually ovalize until catastrophic failure occurs at a confined location (indicated
by short arrow)

outside diameter, i.e., Pcrit=hollow/Pcrit=solid = [π2EI/(2L)2]hollow/[π2EI/(2L)2]solid = 1

−(Di/Do)4, where Di is the internal diameter and Do is the external diameter. As Di
increases, Pcrit=hollow/Pcrit=solid increases. Although this helps to explain why a
tubular section is much more efficient than a solid section for the construction of a
column, this tactic has limits because very thin tubes are susceptible to a phe-
nomenon called Brazier buckling. This mode of failure, which is also called
short-wave buckling, results when a bending load causes a cross section to ovalize.
As the load increases, the ovalization of the cross section increases and eventually
results in catastrophic localized crimping (Fig. 7). Hollow stems and leaves are
susceptible to this mode of failure. It should be noted that Euler buckling and
Brazier buckling are interrelated because a tall slender hollow column starts to
undergo Euler buckling before it experiences Brazier buckling. The critical bending
moment for this case is given by the equation


Mcrit ¼ 0:99E ro t2 =ð1m2 Þ1=2 ; ð20Þ

where ro is the outside radius, t is the thickness of the hollow column, and ν is the
Poisson ratio, i.e., the negative quotient of the transverse and the axial strains a
Tree Biomechanics with Special Reference to Tropical Trees 425

material experiences. The equation holds true provided that ro > 10 t and that the
column is composed of an isotropic material (i.e., a material that mechanically
responds the same regardless of the direction a load is applied). Whether a hollow
trunk or branch undergoes compressive failure or Brazier buckling failure depends
on many factors, including wall thickness, outside diameter, and length (a detailed
treatment is provided by Spatz and Niklas 2013).

The Critical (Maximum) Buckling Height

Euler’s formula for the critical buckling load (see Eq. 19) provides a way to
calculate the critical height to which a column can be elevated before it begins to
bend under it’s own weight. This calculation begins by noting that the critical load
Pcrit has to be some fraction or multiple γ of the weight of a column. The weight of
a column equals the column’s density times the acceleration of gravity times its
volume. The weight of an untapered circular cylinder with radius r and length
L equals ρgπr2L. Therefore, the critical buckling load equals γρgπr2L. Inserting this
expression into Euler’s formula gives

cqgpr 2 L ¼ p2 EI=ð2LÞ2 : ð21Þ

Solving for the critical buckling length Lcrit, we obtain

Lcrit ¼ ½p2 EI=ð4cqgr 2 1=3 : ð22Þ

Since the column is circular, I = πr4/4 (see Fig. 5). Inserting this expression into
Eq. 22 gives

Lcrit ¼ ðp2 =16cÞ1=3 ðE=qgÞ1=3 r 2=3 ; ð23aÞ

or

Lcrit  ð0:85=c1=3 ÞðE=qgÞ1=3 r 2=3 : ð23bÞ

Unfortunately, we do not know the precise numerical value of γ. However, more

sophisticated mathematics gives us the following relationships for columnar and
conical stems:

Columnar stems Lcrit ¼ 0:79ðE=qgÞ1=3 D2=3 : ð24aÞ

Conical stems Lcrit ¼ 1:25ðE=qgÞ1=3 D2=3 ; ð24bÞ

where D is basal stem diameter. Notice that a conical (tapered) trunk provides for
greater maximum height than does a cylindrical (untapered) trunk.
426 K.J. Niklas

However, the extent to which these formulas can be used to estimate the extent
to which a tree has reached its maximum height becomes problematic, particularly
when we examine the assumptions underlying Eq. 24a, b. Tree canopies are never
completely symmetrical, trunks are never perfect cylinders or cones, and they
almost always experience lateral loads due to moving air. For these and other
reasons, Eq. 24a always over-estimates maximum tree height, which may help to
explain why empirical observations indicate that trees growing in open habitats
almost never reach their critical buckling heights. In contrast, trees growing in
habitats sheltered from the wind, particularly, in dense stands, can approach their
critical buckling heights in part because they are sheltered from wind by their
neighbors and because they do not experience a phenomenon called wind-induced
thigmomorphogenesis (see next section).
Before leaving the topic of critical buckling height, it is worth noting that the
geometry of a tree and the material properties of a tree are equally important when
considering safety factor analyses. This is no better illustrated than by the detailed
study of six baobab (Adansonia) tree species by Chapotin et al. (2006). Despite the
considerable girth with respect to the height of mature specimens, which might give
the impression that these trees have very high factors of safety, Chapotin et al.
(2006) report that safety factors based on estimated elastic buckling heights are
rather low. Baobab trees are no more overbuilt than the majority of temperate or
tropical trees. This feature is the result of baobab wood, which has a low elastic
modulus owing to its high water content and parenchymatic volume fraction
(Chapotin et al. 2006). It is also worthy noting that the elastic modulus of baobab
wood can change as a function of the withdrawal of water, since the elastic modulus
of this wood decreases with water content. This opens up the curious possibility that
the second moment of area of the trunk and the elastic modulus of its wood are
inversely correlated and thus possibly compensatory and altered by the addition or
removal of water. In this context, it is interesting to return to Eq. (11), which shows
that a stem’s ability to resist bending depends on E and on I such that “fat but weak”
can be just as affective as “slender and strong”.

Thigmomorphogenesis

During their lifetimes, trees are constantly subjected to mechanical stresses

resulting from the effects of bending and swaying under the influence of wind.
Various workers have subjected woody as well as nonwoody plants to continuous
swaying by mechanical devices and have found that, in general, the stems of woody
plants tend to take on an elliptical cross section with the major axis aligned parallel
to the major axis of the ellipse as a result of the differential growth of the vascular
cambium (Knight 1811). Inspection of Fig. 5 reveals that a change from a circular
cross section to an elliptical cross section results in a change in the second moment
of area such that an elliptical cross section contributes more to the ability of a stem
to resist bending if the major axis of the ellipse is aligned in the direction of the
Tree Biomechanics with Special Reference to Tropical Trees 427

applied load. Jacobs (1954) provided additional insights on the affects of bending
and swaying by guying the trunk of young Monterey pine trees (Pinus radiata) with
wires approximately 20 ft (≈6.1 m) above ground so that trunks would sway above
the attachment points of the wires but remain unperturbed below. The portion of the
trunks above the guy wires was observed to grow in girth more rapidly that the
portion of the restrained trunks. When the wires were removed, the lower portions
of the trunks grew in girth at the same pace as the portions of trunks that were
permitted to sway. These experiments indicate that wind-induced swaying stimu-
lates the activity of the vascular cambium and results in thicker stems.
Experiments with nonwoody plants indicate that mechanical perturbation pro-
duces similar results. Mechanically stimulated stems grow more rapidly in girth and
less rapidly in length compared to stems that are not permitted to move. In addition,
mechanical tests reveal that the tissues of mechanically perturbed stems have lower
elastic moduli compared to tissues that are not perturbed. Collectively these
experiments indicate that mechanical stimulation increases the second moment of
area but decreases the elastic modulus of stem tissues. These responses increase the
contribution of geometry to bending and twisting but decrease the contribution
made by the mechanical properties of tissues, presumably so that stems deflect more
easily in the wind and thus reduce their projected area toward the oncoming wind.
This phenomenology is an example of thigmomorphogenesis, a term that refers
to any growth response to mechanical perturbation (for a mechanistic review, see
Telewski 2006). It is most often studied in terms of the changes in morphology or
anatomy attending the application of external forces such as loading.
Thigmomorphogenesis has been reported for over 80 % of all the species examined
(Jaffe 1973). More recently, it has been studied in terms of the molecular events
preceding changes in shape and size. Braam and Davis (1990) have shown that ten
to twenty minutes after mechanical stimulation by handling, rain, or wind, the
mRNA levels of mouse-ear cress (Arabidopsis) increase up to a hundredfold. Four
touch-induced (TCH) genes are involved. These genes encode for calmodulin,
suggesting that calcium ions are required for the transduction of mechanical signals,
thereby enabling plants to sense and respond to dynamic as well as self-imposed
mechanical forces.

Trunk-Root Interactions and Damping

The growth and development of woody roots are known to respond to chronic
dynamic perturbations with a predictable directional component by adaptively
altering cross-sectional morphology, patterns of wood deposition, and even the
mechanical properties of tissues. The data reported from a number of case studies
confirm that woody roots have the capacity to alter important physical and geo-
metrical properties that are adaptive to stress and strain conditions (e.g., Knight
1811; Coutts 1983, 1986; Ennos 1993, 1994; Stokes et al. 1995, 1996; Niklas
1999).
428 K.J. Niklas

Dynamic loadings typically actuate roots to bend and twist. Typically, the roots
on the windward side of the tree will bend upward and the roots on the leeward side
will bend downward as a result of the rotational pivoting of the trunk caused by the
wind (Fig. 8). Roots oriented at an angle with respect to the direction of the
oncoming wind will twist as well as bend to varying degrees. This bending and
twisting can also cause the more distant parts of the root system to be pulled toward
the base of the trunk. Gusts of wind coming in different directions can cause the
root system to oscillate such that the direction of bending and twisting will change,
e.g., root surfaces experiencing compression will experience tension and the
direction of torsion will be reversed. Significant and sudden changes in the direction
and magnitude of the wind force (drag) can result in root-wood fatigue-failure,
some of which may not be visible until uproot occurs.
The extent to which roots bend and twist depends on many factors other than the
force of the force and the strength of root-wood. For example, soil depth, com-
paction, and hydration can contribute to the ability of roots to resist bending,
twisting and pulling by virtue of providing counteracting compressive forces near
the trunk-root crown and by providing counteracting shearing or suction forces
along the surfaces of more distal parts of the root system. Other important factors
are (1) the general morphology of the root system, which influences how stresses
are distributed along the length and breadth of individual roots (e.g., Crook and
Ennos 1996; Stokes and Mattheck 1996; Crook et al. 1997), (2) the morphology
and size of the tree canopy, which influences how drag forces are transmitted to the
root system (Ennos 1993; Edelin and Atger 1994; Vogel 1996), and (3) soil-type
and weather conditions, which influences the extent to which roots can remain
anchored and the duration and magnitudes of wind-induced dynamic loadings (e.g.,
Casada et al. 1980; Marshall and Holmes 1988).
An important aspect of the transfer of energy from the wind to a tree, or to any
large plant, is the damping of oscillations. Damping causes a decrease in the
amplitudes of free oscillations and thus reduces the danger of a resonance catas-
trophe in dynamic winds. Oscillation and oscillation damping in trees have been
widely studied (see Mayhead 1973; Milne 1991; Peltola et al. 1993; Moore and
Maguire 2004; Jonsson et al. 2007). If friction among different trees, or among
different branches, and dissipative mechanisms in the root-soil system are set aside,
there are two principal sources of damping: fluid damping and viscous damping
within the material. Fluid damping (dissipation of energy to the surrounding
medium) depends on the square of the velocity of the object’s movement relative to
the surrounding medium. With estimates of the effective projected area and the drag
coefficient (see Eq. 2), fluid damping can be calculated by iteration of the loss of
energy during each cycle of the oscillation. Viscous damping in the material
(conversion of mechanical energy into heat) is linearly related to the velocity of
relative movements between adjoining branches or systems of branches that move
in consort with one another. It can be determined in loading-unloading experiments
by measuring the loss of energy in a hysteresis loop. In order to relate these
measurements to a real tree, measurements should be performed using green wood,
since the water in wood plays a pivotal role in viscous damping.
Tree Biomechanics with Special Reference to Tropical Trees 429

Fig. 8 Synoptic diagram of self-loading resulting from individual branches and the total
above-ground mass of a tree (a), dynamic loading resulting from wind drag (b), and trunk-root
interactions under conditions of wind-induced drag forces (c). a Self-loading for an individual
branch with mass mbranch results in a bending moment MB whose magnitude depends on tangent of
the branch angle ϕ. In the simplest case, MB = g mbranch L sin ϕ, where L is the length of the branch.
Since sin ϕ = 1.0 when ϕ = 90º, a horizontally oriented branch achieves the maximum bending
moment (which occurs at its base). The maximum self load and the maximum bending moment,
however, occur at the base of the trunk, which experiences the maximum compressive stresses,
which is equal to the product of the acceleration of gravity and the total aboveground mass divided
by the area of the base of the trunk, i.e., σ– = g mtotal/A = PS/A. b A pictorial of a tree subjected to
dynamic loading as a result of wind-pressure. U = wind speed. The drag force experienced by the
tree canopy (with a projected area of Sp) is given by Eq. 2. The maximum bending moment MB
occurs at the trunk-root junction. MB equals the drag force times the height of the tree. Mechanical
stability requires a rotational (counter) moment MR such that MR ≥ MB. Flexure of the windward
and leeward root system results in compression and tension within the root systems (see c).
c Diagram of root-system flexure experiencing a wind-induced torque. Roots on the windward side
bend upward and experience tensile stresses and compression stresses on their upper and lower
surfaces (σ+ and σ–, respectively); more distal roots also experience tensile stresses as they are
pulled toward the base of the trunk. Roots on the leeward side bend downward and experience
compressive stresses and tensile stresses on their lower and upper surfaces (σ+ and σ–,
respectively); more distal roots also experience tensile stresses as they are pulled toward the base
of the trunk. Root flexure can be reduced if compacted soil resists root displacements and provides
compression on the upper surfaces of upwind roots and compression on the lower surfaces of
downwind roots (denoted by upward and downward pointing arrows)
430 K.J. Niklas

In complex structures such as trees, certain processes can enhance damping.

In gusty winds, branches do not necessarily sway in line or in phase with their
subtending stems. Rather, they can perform independent movements relative to one
another. In this way, energy is distributed among branches and twigs and is dis-
sipated more effectively than in a structure too stiff to allow relative movements
between its elements. This phenomenon, which is referred to as structural damping
(Niklas 1992), is not a different mode of damping. It merely emphasizes the
enhancement of overall damping by the relative movements of structural elements
(branches and twigs), which affect both fluid and viscous damping—processes that
are most effective in the periphery of the tree canopy. Structural damping can be
caused by the loose coupling mass (termed mass damping; James 2003) or by the
distribution of mechanical energy through resonance phenomena within the tree
(see James et al. 2006; Spatz et al. 2007), a phenomenon well known in the
engineering sciences (Holmes 2001). As shown for a Douglas fir, a tree can react to
dynamic wind loads like a system of coupled damped oscillators. This concept has
been confirmed theoretically by Rodriguez et al. (2008). The interaction between
the different elements leads to a higher damping ratio, and additionally to less strain
on the stem as compared with a structure with much stiffer side branches. Multiple
resonance damping is therefore essential for the survival of trees and other large
plants growing in windy environments. An interesting but as poorly understood
topic is the effect of epiphytes and lianas on the damping of the canopies of tropical
trees. In theory, the eccentric loads created by epiphytes and the potential for lianas
to entangle branches can increase damping ratios and produce coupled damped
oscillators.

Buttressed Root Systems

As noted in the introduction, tropical trees manifest features that can set them apart
from trees growing in other ecosystems. One of these features is the formation of
buttressed root systems (Richards 1952). Various theories have been proposed to
account for the formation of these triangular flanges joining the roots to the lower
portions of trunks. Black and Harper (1979) suggested that buttresses prevent lianas
from climbing trees, a hypothesis that was disproved by Boom and Mori (1982).
Senn (1923) and Richards (1952) suggested that buttresses provide mechanical
support, a hypothesis that has been supported by indirect observations that corre-
lated tree development with environmental conditions (e.g., Richter 1984; Lewis
1988). For example, buttresses rarely if at all develop on the trunks of trees with
well developed tap roots (e.g., Francis 1924; Corner 1988), whereas buttressing is
correlated with emergent canopy trees (Richards 1952; Smith 1972) and with
species growing in shallow waterlogged or weak silty soils (Richards 1952). An
additional correlation that tends to support the biomechanical hypothesis is that
Tree Biomechanics with Special Reference to Tropical Trees 431

buttresses on the upwind sides of trunks tend to be more well developed and
extensive that those growing on the leeward sides of trunks (Senn 1923; Baker
1973; Lewis 1988; Warren et al. 1988). Perhaps for these and other reasons,
Henwood (1973) proposed that buttresses act as tensile elements. Along similar
lines, Mattheck (1991, 1993) noted that buttresses are often associated with
bayonet-like sinker roots (Jenik 1978; Baillie and Mamit 1983) and suggested that
sinker roots in tandem with buttresses provide a robust mechanism to resist wind
throw (Fig. 9a).
The biomechanics of sinker roots attached to buttresses was examined in a
seminal study provided by Crook et al. (1997) who investigated the anchorage
mechanics of the buttressed root systems of Aglaia and Nephelium and compared it
with the anchorage mechanics of the non-buttressed trunks of Mallotus. Using
winches to simulate wind throw and strain gauges, Crook et al. (1997) exerted
bending forces sufficient to rotate the root systems of trees and noted the following:
(1) all trees failed in their root systems (and not by trunk failure), (2) despite dif-
ferences among the species used in the study, windward buttressed laterals with our
without sinker roots either pulled out of the ground or delaminated, while leeward
buttresses pushed into the ground and broke near or at their ends (Fig. 9b–c),
(3) buttresses with sinker roots resisted simulated wind throw better than those
without sinker roots, and (4), in the non-buttressed root system, upwind roots
extended in tension, uprooted, but rarely broke, leeward roots buckled appreciably,
and taproots bent and compressed the leeward soil profile that often produced an
upwind crevice (Fig. 9d).
Some of the results reported by Crook et al. (1997) are in disagreement with the
Mattheck model (Fig. 9a). For example, the majority of buttresses examined in the
study lacked sinker roots. Likewise, the Mattheck model posits that buttresses
strengthen anchorage by preventing delamination at the junction of windward roots
and the trunk, whereas windward buttresses with sinker roots delaminated rather
than uprooted in the Crook et al. (1997) study. Nevertheless, trees with buttressed
root systems had almost twice the anchorage strength as similar sized trees lacking
buttressed systems, and leeward and windward buttresses appear to function in
compression and tension, respectively.
The question as to why some species regularly produce buttressed root systems
while others do not remains unanswered. It is possible that wood density may play a
part in this, because tree species with higher wood densities may have thinner
trunks and thinner roots that may be insufficient to provide anchorage when indi-
vidual trees reach threshold critical heights. The scaling of stem and root diameters
with respect to growth in height is likely to be another factor, because thicker stems
and roots can compensate for lower wood densities or greater heights by virtue of
magnifying second moments of areas. Clearly, many factors conspire to cope with
anchorage requirements and each species “solves” these requirements using a
multi-factorial approach based on its unique combination of functional traits.
432 K.J. Niklas
 Tree Biomechanics with Special Reference to Tropical Trees 433

b Fig. 9 Biomechanical behavior of buttressed root systems. a Mattheck’s (1991, 1993) model for
the distribution of mechanical forces running from sinker roots through buttresses. As the trunk is
bent by wind (with speed U), the bending force is transmitted to upwind sinker roots that resist
upward forces, whereas leeward roots and buttresses resist downward forces. Compare with Fig. 8.
b–d Trunk, buttress, and sinker root displacements resulting from mechanical simulations of wind
throw. Adapted from Crook et al. (1997). b Displacements of buttressed trunks without sinker
roots at two different rotation centers (indicated by black circles). c Displacements of buttressed
trunks with sinker roots at two different rotation centers (indicated by black circles).
d Displacements of an unbuttressed trunk with superficial roots subjected to modest and large
bending forces (left and right, respectively). For details, see text

Concluding Remarks

This chapter began with a treatment of the static and dynamic loadings experienced
by a vertical cylinder with a radius of 0.03 m and a length (height) of 1.5 m
subjected to a uniform wind speed of 11 m/s. It was noted that these loads are far
less important than the stresses they produce. The treatment of biomechanical
principles that followed allows us to calculate these stresses. As noted, the drag
force exerted by a uniform wind speed of 11 m/s was 6.56 kg m s−2 or 6.56 N. The
bending moment MB resulting from this force equals the force times the length of
the column, or 6.56 N × 1.5 m = 9.84 Nm. The maximum stress at the perimeter at
the base of this column is given by the formula σmax = 4 MB/π r3 = [4 (9.84 Nm)]/[π
(0.03 m)3] = 4.64 × 105 N/m2. The compressive stress σcomp across the base of the
column resulting from static loading is the mass of the column times the acceler-
ation of gravity divided by the cross sectional area of the column. With a density of
844 kg/m3, we see that σcomp = (ρ πr2 L g)/(π r2) = g ρ L = (9.806 m/s2) (844 kg/m3)
(1.5 m) = 1.24 × 105 kg m−1 s−2 or 1.24 × 105 N/m2. Thus, the stresses produced by
even a modest wind speed are more than 3.5 times the stresses produced by the
static loading of the column.
This comparison shows that tree biomechanics is an extremely complex subject
because much of what we think we know depends on the questions we ask and how
we use equations to answer them. In addition, there are many aspects that are poorly
understood, e.g., viscoelastic nonlinear behavior and the effects of lianas on damping.
Thus, predicting the mechanical behavior of any particular tree poses many chal-
lenges because each tree has its own individual characteristics that reflect its par-
ticular genetic composition and growth responses to its particular habitat. The tropics
is a huge and diverse ecosystem consisting of many different types of habitats.
Likewise, the behavior of a tree observed at any particular time cannot be used to
predict the behavior of the same tree a few years hence because trees grow in size and
produce new branches and roots and loose branches and roots over the course of their
lifetime. Nevertheless, the concepts and equations reviewed here provide some
guidance in evaluating the potential mechanical behavior of trees. They provide
boundary conditions as to what is possible and what is highly unlikely. However, in
the final analysis, predicting the mechanical behavior of any tree requires experience
and prudent judgment, attributes that thus far have eluded mathematical description.
434 K.J. Niklas

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 Part VI
Ecophysiological Processes at Different
Temporal Scales
Tree Rings in the Tropics: Insights
into the Ecology and Climate Sensitivity
of Tropical Trees

Roel J.W. Brienen, Jochen Schöngart and Pieter A. Zuidema

Abstract Tree-ring studies provide important contributions to understanding the

climate sensitivity of tropical trees and the effects of global change on tropical
forests. This chapter reviews recent advances in tropical tree-ring research. In
tropical lowlands, tree ring formation is mainly driven by seasonal variation in
precipitation or flooding, and not in temperature. Annual ring formation has now
been confirmed for 230 tropical tree species across continents and climate zones.
Tree-ring studies indicate that lifespans of tropical tree species average c. 200 years
and only few species live >500 years; these values are considerably lower than
those based on indirect age estimates. Size-age trajectories show large and persis-
tent growth variation among trees of the same species, due to variation in light,
water and nutrient availability. Climate-growth analyses suggest that tropical tree
growth is moderately sensitive to rainfall (dry years reduce growth) and temperature
(hot years reduce growth). Tree-ring studies can assist in evaluating the effects of
gradual changes in climatic conditions on tree growth and physiology but this
requires that sampling biases are dealt with and ontogenetic changes are disen-
tangled from temporal changes. This remains challenging, but studies have reported
increases in intrinsic water use efficiency based on δ13C measurements in tree rings,
most likely due to increasing atmospheric CO2. We conclude that tree-ring studies
offer important insights to global change effects on tropical trees and will
increasingly do so as new techniques become available and research efforts
intensify.

R.J.W. Brienen (&)

School of Geography, Leeds University, Woodhouse Lane, Leeds LS2 9JT, UK
e-mail: r.brienen@leeds.ac.uk
J. Schöngart
Instituto Nacional de Pesquisas da Amazônia (INPA), Av. André Araújo 2936,
P.O. Box 478, Manaus, AM 69011-970, Brazil
P.A. Zuidema
Forest Ecology and Forest Management, Centre for Ecosystems,
Wageningen University, P.O. Box 47, 6700 AA Wageningen, The Netherlands

© Springer International Publishing Switzerland 2016 439

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5_20
440 R.J.W. Brienen et al.

Introduction

Tropical trees are an important element of the global biosphere. Tropical forests and
woody savannas cover 12–15 % of the Earth’s terrestrial surface (FAO 2006), and
host more than 40,000 tree species (Slik et al. 2015), they store about 60 % of total
global forest biomass (Pan et al. 2011), and play a significant role in the water,
carbon and nutrient cycles of the earth (Bonan 2008; Spracklen et al. 2012). Given
these important roles, it is essential to understand how tropical forests respond to
changing climatic conditions. This requires information about the climate sensi-
tivity of tropical trees and the long-term dynamics of tropical forests. For instance,
to project the effects of future climate change, it is pertinent to obtain insights into
the responses of tropical trees to variation in climate and CO2 (Zuidema et al.
2013), while long-term information on tree ages and forest disturbance history are
important to infer residence times of carbon in forests as well as the interactive
effects of disturbance and climate change on forest dynamics (Babst et al. 2014;
Gebrekirstos et al. 2014).
Tree ring analysis (or dendrochronology) can importantly contribute to the study
of tropical forest responses to changing climate. However, in the tropics it has
lagged behind studies in temperate and boreal trees, where tree rings provided
detailed insights into tree growth and functioning, and trees’ responses to past
climate (Fritts 1976; Speer 2010). While the occurrence of clearly defined annual
rings in tropical trees is less common than in temperate trees, a substantial number
of tropical species is known to form annual rings. One of the first documented
observations on tree rings in a tropical tree species was by Brandis in 1856, who
noticed that Teak (Tectona grandis) in Indonesia produced distinct rings which he
assumed to be formed in response to an annually recurring dry season. This was
confirmed in 1881 by Gamble by counting rings on plantation trees with known
age, and much later by the publication of the first tropical tree ring chronology on
Teak from Java by Berlage (1931). The research field of tropical dendrochronology
has made some important advances since then. Two workshops specifically dedi-
cated to this research field (1980 and 1989) summarized the advances and con-
cluded that it has been clearly demonstrated that many tropical tree species in
regions with seasonality in rainfall or flooding form distinct annual rings (Bormann
and Berlyn 1981; Baas 1989). In 2002, Worbes evaluated 139 species from
neotropical floodplains and terra firme, showing the occurrence of growth bands in
at least a third of the listed species. In the last decade the number of species with
proven annual rings has increased strongly (Zuidema et al. 2012) due to increased
research efforts throughout the tropics. Despite these recent advances, even today
the Berlage teak chronology (1514–1929) published in 1931 remains one of the
longest tree ring chronologies in the tropics. The apparent lack of success in
reconstructing long climate sensitive ring width chronologies, as witnessed for
example in the paucity of tropical chronologies in the International Tree Ring
Database (Grissino-Mayer and Fritts 1997), highlights undeniable problems in
detecting tree rings for a large number of species, but is also partially due to
Tree Rings in the Tropics: Insights into the Ecology … 441

insufficient efforts, and long-standing skepticism towards the occurrence of ring

formation in tropical trees.
In this chapter, we present important findings obtained in tropical tree ring
research relevant to the general theme of this book, the adaptation of tropical trees
to changing climate. We first describe the different mechanisms of tree ring for-
mation in tropical trees, relate this to tree phenology, and provide an overview of
tropical tree species with proven annual rings. The following sections present
results on ages, growth patterns and regeneration strategies of tropical trees, and a
review of the sensitivity of tropical trees to inter-annual variation in climate and
long-term tree responses to CO2 increase. We end with a section on insights from
isotope techniques and a summary of our main conclusions.
In our review, we included all studies from tropical latitudes (i.e., between 23.4°
North and South) thus including both wet forests and savannas, very wet and dry
areas, and flooded and non-flooded areas. We excluded studies in mountain systems
(>1500 m a.s.l), and mangroves, where environmental conditions and cues are very
different.

Tree Ring Formation in the Tropics

Tree-ring boundaries are formed when cambium cells in tree trunks are dormant. In
mid- and high-latitude regions, the principal trigger behind cambial dormancy and
the formation of anatomically distinct tree rings is seasonal variation in day length
hours and temperature (Fritts 1976). In the tropics, there is no (or very limited)
seasonality in these climatic variables. This notion was the basis for the long-held
belief that tropical trees show relative constant growth throughout the year and
would not form annual rings (cf. Lieberman and Lieberman 1985; Whitmore 1998).
Nevertheless, many tropical trees do show annually recurring phenological patterns
(van Schaik et al. 1993), which may slow down cambial activity or induce complete
cambial dormancy, and result in an anatomically distinct layer of wood i.e., a tree
ring boundary. Seasonality in leaf phenology in tropical trees is thought to be an
adaptation to variation in external (abiotic) stress. Rainfall seasonality is by far the
most common stressor for tropical trees (Worbes 1995, 1999). Over large areas of
the tropics, especially further away from the equator, evapotranspiration exceeds
rainfall for at least several weeks per year. This causes seasonal water-stress
especially for shallow rooted species in dry sites (Borchert 1994), and may result in
complete leaf shedding (deciduous), or exchange of leaves within a very short
period (brevi-deciduous). When trees are leafless, cambial activity stops, and a
distinct layer of wood is formed. While this behavior is most likely a plastic or
evolutionary adaptation to reduce leaf cover during periods of prolonged water
stress, the actual trigger to which trees respond may be different. For instance, in
some deciduous species of seasonally dry forests, it has been observed that trees
drop their leaves before water stress has developed and that bud break often occurs
before the onset of the wet season and is triggered by variation in day length
442 R.J.W. Brienen et al.

(Rivera et al. 2002; Elliott et al. 2006). Another abiotic stress factor leading to the
formation of annual rings is seasonal flooding. During flooding, anoxic conditions
of the roots induce leaf fall, cambial dormancy and the formation of annual rings in
many tree species (Worbes 1985; Schöngart et al. 2002).
Whether trees form annually distinct rings depends both on the species-specific
physiology and wood anatomy, but also on exogenous factors like the seasonality
of the rainfall or flooding. Trees showing strictly annual cycles of leaf fall and
flushes are more likely to form annual rings, and the percentage of species with
annual rings is expected to be higher in sites with strong annually recurring sea-
sonality (Borchert 1999). Several studies demonstrated the importance of season-
ality in environmental conditions by showing that some species may form clear
annual rings in seasonal sites, but lack rings in very wet sites with low precipitation
seasonality or in very dry sites with highly irregular precipitation (Geiger 1915;
Coster 1927; Borchert 1999; Pearson et al. 2011). Hence, tree ring formation can be
strictly annual, bi-annual (Jacoby 1989; Gourlay 1995) or irregular with false
(non-annual) rings occurring every few years (Wils et al. 2011). Formation of
annual rings can also differ between life stages with clear and annual rings in the
adult phases, but absent, vague, or non-annual rings formed during the juvenile
phases (Dünisch et al. 2002; Brienen and Zuidema 2005; Soliz-Gamboa et al.
2011). These issues call for cautious interpretation of tree-ring measurements in
new species or in the same species at different sites.
A global dicot wood anatomy database with 5663 anatomical descriptions,
indicates that ca. 23 % of the tropical woody dicots present distinct growth
boundaries, somewhat lower than the global average of 34 % and the 76 % in
temperate regions in the northern hemisphere (Wheeler et al. 2007). Considering
the very high diversity of tropical tree species (Slik et al. 2015) and the propor-
tionally low number of studied species, this lower occurrence of tree rings in the
tropics still yields a potentially very large number of species forming anatomically
distinct ring boundaries. As anatomic records do not indicate whether rings are
formed annually, we provide a review of 130 studies on tree rings in tropical trees
(see also Zuidema et al. 2012; Schöngart 2013) for which annual formation of tree
rings has been verified using various methods (e.g. cambial marking, climate cor-
relations, bomb-peak dating, trees of known age, etc., see Worbes 1995). This
review shows that 230 different tropical tree species from 46 different families form
annual rings (see summary Table 1). These studies cover all continents and climates
(see Fig. 1), and also include some very wet sites (4000 mm annual precipitation)
with limited seasonality in rainfall (Fichtler et al. 2003; Groenendijk et al. 2014).
The majority of the studies however, are located in zones away from the equator
that have at least one distinct dry season (cf. Fig. 1).
The existence of growth rings is closely related to the wood anatomical structure,
and therefore—at least partially—genetically determined (Wheeler et al. 2007, but
see; Fichtler and Worbes 2012). Variation in wood anatomy of tropical trees that
defines ring boundaries is distinctly different from temperate northern hemisphere
woods (Worbes 1995), thus requiring a separate classification. A useful and widely
used anatomical classification of growth ring boundaries in tropical woods is that of
Tree Rings in the Tropics: Insights into the Ecology … 443

Table 1 Summary table of Vegetation type # studies

literature review of 130
studies showing the number Wet forest 76
of species with annual rings Moist forest 117
per vegetation type, the Dry forest 18
top-five species used for tree Open savannah and desert 15
ring studies, and top five
Floodplain 21
families with ring forming
species Top five species used in the tropics
Tectona grandis
Terminalia superba
Cedrela odorata
Triplochiton scleroxylon
Macrolobium acaciifolium
Top five families with ring forming species # species
Fabaceae 95
Meliaceae 17
Malvaceae 11
Bignoniaceae 7
Combretaceae 7
A total of 230 species with annual formation of tree rings was
found. The annual character of rings in these studies was verified
using various methods (e.g. cambial marking, climate
correlations, bomb-peak dating, trees of known age, etc.).
A comprehensive list of these studies can be found in Zuidema
et al. (2012) and Schöngart (2013). Studies in mountain systems
(>1500 m a.s.l) or mangroves are excluded from this review

2000

1500

1000

500

Fig. 1 Map with locations of tree-ring studies in the tropics. The background color shows the
precipitation in the driest quarter (data: WorldClim, Hijmans et al. 2005) with blue areas marking
areas that receive more than 300 mm during the driest quarter

Coster (1927) adopted by Worbes (1995, 2002). It distinguishes four different types
of growth zones: (1) density variations; (2) marginal parenchyma bands; (3) repeated
patterns of alternating parenchyma and fibre bands; (4) variations in vessel distri-
bution and/or vessel size (i.e., ring-porosity) (Fig. 2). As currently no large-scale
classification of wood anatomy of growth zones exists for tropical tree species, it is
444 R.J.W. Brienen et al.

hard to make generalizations about relations between wood anatomy or the occur-
rence of growth zones and taxonomy. Nevertheless, the top families with
ring-forming species are Fabaceae, Meliaceae and Malvaceae (see Table 1). Growth
zones in Fabaceae and Meliaceae often show marginal parenchyma bands (Worbes
1989; Groenendijk et al. 2014), while alternating parenchyma and fibre bands are a
common feature in Lecythidaceae, Sapotaceae, and Moraceae (Worbes 1989).
Density variations and vessel size variation can occur in concurrence with the pre-
vious features, or delineate an annual growth zone by itself. The best example of a
“ring-porous” species with wide vessels delineating the start of a new ring, is Teak
(Tectona grandis), one of the most widely used tropical species for climate recon-
struction in the tropics (cf. Fig. 2f). Examples of families with species with variations
in wood-density include Annonaceae, Lauraceae and Euphorbiaceae (Worbes 1989).
Despite the advances in tropical tree ring analysis, tropical trees commonly
present problems in the form of vague growth boundaries, false rings (Fig. 2h) and
wedging rings (Fig. 2i) or discontinuous (locally absent) rings (Fig. 2g). For those
interested in performing tree-ring studies in the tropics, please refer to Stahle (1999)
and Worbes (1995, 2002) for practical guidance.

Inferences from Trees Rings on Tree Longevity, Growth

Patterns and Regeneration

Tree rings allow detailed reconstruction of growth curves for individual trees over
the full length of their life, thereby providing profound ecological insights that
cannot be obtained using for example relative short-term growth measurements. We
will highlight a few important ecological inferences that have been made from
growth rings of tropical trees.
Tree rings provide accurate information on tree ages. The question of how old
tropical trees become has occupied scientists for a long time, and has been the
subject of fierce scientific debate. Ages in trees can be measured directly only by
means of radiocarbon dating or tree ring analysis (Martinez-Ramos and
Alvarez-Buylla 1998). Some radiocarbon dating methods revealed ages for tropical
trees in excess of 1000 years (Chambers et al. 1998; Vieira et al. 2005), but given
the controversy on these reported ages (Martinez-Ramos and Alvarez-Buylla 1998,
1999; Worbes and Junk 1999) and the focus of this chapter, we here report on the
outcome of ages obtained by tree ring analysis only.
Figure 3 shows the range of maximum observed ages for 71 tropical tree species.
These results provide an indication of tree longevities, although it should be noted
that in most cases, the purpose was not to sample the largest individuals of the study
species. The mean of the maximum observed age across all tropical tree species is
208 years (median = 200 years). In line with the high diversity in life-history
strategies among tropical trees, ages vary from a few decades for pioneer species
(Schöngart 2008; Brienen et al. 2009; Vlam 2014) to several centuries. Taxodium
mucronatum trees show the highest longevity reaching ages of more than 1500 years
Tree Rings in the Tropics: Insights into the Ecology … 445

(a) (b)

(c) (d)

(e) (f)

(g) (h)

(i) (j)

Fig. 2 Wood anatomical features of tropical tree rings showing the most common ring boundaries
(panels a–f) and some common problems encountered in tree ring studies (g–j). Growth direction
in panels a–f is from left to right. Filled white triangles indicate annual growth boundaries; open
triangles in panel h indicate false rings

in swamp forests in central Mexico (Stahle et al. 2012). However, such long-lived
conifers can be regarded an exception, as most broadleaved trees in lowland areas are
substantially younger. The oldest broadleaved tree with confirmed ages in excess of
1000 years using a combination of tree rings and radiocarbon dating are Baobab
trees from Africa (Robertson et al. 2006; Patrut et al. 2007), while few studies report
ages over 500 years old (Fichtler et al. 2003; Borgaonkar et al. 2010). This outcome
446 R.J.W. Brienen et al.

Fig. 3 Histogram of
observed maximum ages of
71 tropical tree species by use
of counting of annual tree
rings

of the studies reviewed here are close to estimates of tree longevity derived from
growth rates from rainforests of central Amazon (median of 296 years, Laurance
et al. 2004) and Costa Rica (mean of 230 years from 10 cm DBH, Lieberman et al.
1985), and shows that life-spans of broadleaf tropical tree species are not different
from those of temperate broadleaf tree species (cf. Loehle 1988). However, the
results contrast with life-spans of several millennia for trees (mainly gymnosperms)
growing in extreme environments (Brown 1996). Reliable estimates of tree
longevities are an important basis for calculations of carbon residence times.
Reconstructions of age-size relationships show a large variation both within
(Fig. 4a, b) and between species (Fig. 4d–f). Within species several magnitudes of
variation in ages exist between trees of a similar size, even at the youngest stages.
For example, within the same population the ages of Cedrela odorata trees of
10 cm in diameter range from 9 to 75 years (cf. Fig. 4a), and a similar magnitude of
variation exists among Macrolobium acaciifolium trees from floodplain forests (cf.
Fig. 4b). Hence, young juvenile trees may be as old as large canopy trees. Such
large variation in growth rates between trees of the same species seems very
common in tropical trees (Worbes et al. 2003; López et al. 2013; Groenendijk et al.
2014), reaffirming that size is a poor predictor for tree age. This variation between
trees arises due to differences between individuals in light and water availability,
and soil fertility (Schöngart et al. 2005; Baker and Bunyavejchewin 2006; Brienen
et al. 2010a). The relative importance of these factors may vary between sites and
species. Comparison of two Cedrela populations showed that in moist forest with a
relatively dark understory, variation in juvenile growth was mainly governed by
fluctuations in light availability, while at a dry site spatial variation in water
availability was more important (Brienen et al. 2010a). In the Amazonian floodplain
species M. acaciifolium the effect of differences in nutrient availability seemed to
dominate variation in growth rates, with much slower growth in the nutrient poor,
black-water floodplains (Igapó), compared to the nutrient rich white-water flood-
plains (Várzea) (Schöngart et al. 2005). Remarkably, this growth variation is
associated with tree longevities, with slow growers at the nutrient poor sites
Tree Rings in the Tropics: Insights into the Ecology … 447

140
(a) Cedrela odorata ,Terra firme Moist forest
(b) Macrolobium acaciifolium , Floodplain
120 (1750 mm) Várzea, nutrient rich Igapó, nutrient poor
100
80
60
40
20 Dry forest (1100 mm)

0
0 50 100 150 200 250 0 50 100 150 200 250 300 350 400 450

(c) Moist to wet tropical forest (1750-4000 mm precipitation) (d) Central Amazonian floodplain forests

0 50 100 150 200 250 300 350

(e) Seasonally dry tropical forest (1470-1530 mm precipitation) (f) Dry forest-savanna mosaic (1200 mm precipitation)

Fig. 4 Growth trajectories of tropical trees derived from tree ring analysis. Panels a–b show
trajectories of individual trees for Cedrela odorata from two terra firme forests (Bolivia and
Mexico; Brienen et al. 2010a) and for Macrolobium acaciifolium from Brazilian floodplains
(Schöngart et al. 2005). Panels c–f show mean trajectories for different species from (c) moist to
wet tropical forests (6 spp. northern Bolivia; Brienen and Zuidema 2006); 4 spp. Cameroon
(Groenendijk et al. 2014), d Central Amazonian Várzea floodplain forests (14 spp.; Schöngart
2008), e seasonally dry tropical forests (5 spp. southern Bolivia; van der Sleen 2014), 5
spp. Thailand; (Vlam 2014), and f dry forest-savannah mosaics (6 spp. west Africa, Schöngart
et al. 2006)

attaining much higher ages (i.e., 403 years) compared fast growers at the richer sites
(i.e., 157 years). Such trade-offs between growth and longevity have been observed
in temperate trees (Bigler and Veblen 2009) and may have important implications
for future responses of forests to increased levels of CO2 and temperature (cf.
Bugmann and Bigler 2011).
Comparison of mean age-size relationships between species shows a comparable
variation to that observed within a species (Fig. 4c–f) indicating that microsite and
stochastic difference between individual trees may be as important as its taxonomy
in shaping growth trajectories. Mean age of similarly-sized trees varies by a factor
of four to five across species and across vegetation types (wet to dry terra firme and
floodplain forests and savannas).
A final contribution of tree ages to tropical forest ecology is in evaluating
changes in forest dynamics and reconstructing past disturbances. Distinct peaks in
the age distribution of light-demanding tree species may indicate periods of dis-
turbances if these have resulted in elevated recruitment rates of these species (Baker
448 R.J.W. Brienen et al.

et al. 2005; Vlam et al. 2014b). The spatial configuration of tree ages of such
light-demanding species may provide important additional information on the
extent of these disturbances (Middendorp et al. 2013). Another indication of
changes in forest dynamics can be obtained from the analysis of ‘releases’, periods
of elevated growth rates, which can be caused by increased light levels. In forests
where tree mortality is gradually increasing over time, more gaps are formed, which
may lead to an increase in the incidence of such growth releases. The interpretation
of the causes of growth releases is not straightforward though, as individuals and
species may strongly differ in responses to gap formation (Brienen and Zuidema
2006; Soliz‐Gamboa et al. 2012) and releases may be induced by climatic vari-
ability (Brienen et al. 2010a; Vlam 2014). So far, the few analyses of release
frequency for tropical tree species have shown no or minor shifts in the rate of
releases during the last century, suggesting that gap dynamics have remained rather
stable over the last century (Rozendaal et al. 2011; Vlam 2014). It should be noted
however, that retrospective tree ring studies miss a significant and possibly
non-random proportion of the original historical tree population (Landis and Peart
2005; Rozendaal et al. 2010), which may lead to biases in reconstructions of
historical growth rates and release frequencies (Brienen et al. 2012a).

Climate Sensitivity of Tree Rings

Temperature, water-availability, and incoming solar radiation all affect tree growth.
The responses of tropical trees to these controls may be complex and non-linear,
and may vary across species and ecosystems. Tree ring analysis is an ideal tool to
evaluate growth responses to climatic fluctuations, as it yields long series of growth
rates at annual resolution. Here we review growth responses of tropical trees to
climatic variation based on 45 studies reporting climate growth relations (Table 2).
The studies generally adopt standard dendrochronological techniques (Speer 2010)
to develop a climate sensitive tree-ring chronology. A chronology is a time series of
averaged growth for individuals that shows comparable growth fluctuations

Table 2 Summary table of the climate-growth relationships for different vegetation types
(excluding floodplains)
Vegetation type Correlation ring n Correlation ring n
width-rainfall, mean (max) width-temperature, mean (min)
Wet forest 0.49 (0.75) 6 – –
(>2000 mm)
Moist forest (1000– 0.44 (0.66) 39 −0.44 (−0.6) 8
1500 mm)
Dry forest 0.57 (0.89) 7 −0.42 (−0.57) 5
(<1000 mm)
Open savannah 0.49 (0.65) 7 −0.3 (−0.40) 2
Tree Rings in the Tropics: Insights into the Ecology … 449

(a)

(b)

(c)

(d)

(e) (f) (g)

Fig. 5 Example of time series of growth (a, b), leaf intercellular CO2 derived from tree ring
carbon isotopes (c), and tree ring oxygen isotopes (d) for a dry forest tree species, Mimosa
acatholoba from southern Mexico. Panels e, f, and g show the relationship of the ring width and
isotope derived data to external variables. Growth and internal CO2 (derived from δ13C in tree
rings) are most strongly related to annual rainfall, while oxygen isotopes related strongly to
variation in isotopes in rainfall from a distant station in San Salvador and was also negatively
correlated to local precipitation (r = −0.72). All relations are significant at p < 0.001. Data-sources
Brienen et al. (2010a, 2011, 2013)

(cf. Fig. 5a). It should be noted that a straightforward comparison of the results of
climate-growth relations is hampered by variation in the selection of trees to be
included, the procedures to remove ontogenetic trends from the growth data, the
length of the growth series and the statistical analyses applied.
450 R.J.W. Brienen et al.

Our analysis shows that annual variation in tropical tree growth is often asso-
ciated with fluctuations in precipitation: in nearly 60 species, growth rates increased
with rainfall (Table 2). This sensitivity to rainfall fluctuations was similar for dry,
moist and wet forests (Table 2), although one would expect a higher sensitivity in
drier forest sites. The lack of a clear relation of growth responses with underlying
climate is at least partially due to methodological differences across studies, but also
due to differences between species in their sensitivity to rainfall fluctuations, even
when they occur in the same area (e.g., Schöngart et al. 2006; Mendivelso et al.
2013; Vlam et al. 2014a). In addition, some species are more susceptible to rainfall
during the dry period, others to the wet period or transitional periods. And finally,
species may also show growth responses to rainfall during the previous growing
season (year). Such lagged responses are common, especially in strictly deciduous
species (e.g., Teak; Buckley et al. 2007, and several Meliaceae; Dünisch et al. 2003;
Brienen and Zuidema 2005; Heinrich et al. 2008; Vlam et al. 2014a), and may be
due to use of stored reserves at the beginning of the rainy season to support wood
formation (Dünisch and Puls 2003; Ohashi et al. 2009). These strong differences in
sensitivity to rainfall reflect species’ differences in stem water storage, phenology,
rooting depth and use of reserves (Borchert 1994; Meinzer et al. 1999).
The strongest responses to precipitation are observed in dry sites in northern
Columbia and Peru and in southern Mexico, where >60 % of variation in ring width
is explained by year-to-year variation in rainfall totals (Rodríguez et al. 2005;
Brienen et al. 2010b; Ramírez and del Valle 2011, 2012). In these dry to very dry
sites (50–900 mm annual precipitation), rainfall can be extremely variable among
years (partially due to ENSO), resulting in a strong control of precipitation on
growth (see Fig. 5e). Despite these exceptions, the overall effect of precipitation on
growth is relatively weak (mean correlation, r, across all species is 0.47, cf.
Table 2), suggesting that rainfall fluctuations have a limited impact on tree growth.
However, reserve storage in trees has a buffering effect and may reduce annual
fluctuations in tree growth. Work in a dry tropical forest shows that trees may be
relatively tolerant to annual fluctuations in rainfall, but sensitive to multi-annual
droughts (Mendivelso et al. 2014).
Temperature negatively affects growth in tropical trees (cf. Table 2), but the
number of studies reporting temperature growth relations is much lower than those
reporting precipitation influences. This is at least partially because fewer studies
included temperature explicitly in their climate growth relations, but also due to
lower responsiveness of tropical tree growth to temperature fluctuations. Especially,
in dry forests and savannas temperature influences were weaker than the influence
of rainfall, and in some cases temperature influences simply resulted from
co-linearity between inter-annual variation in rainfall and temperature (cf. Brienen
et al. 2010b). Several studies in moist forests show temperature effects that are of
comparable or slightly higher in magnitude compared to effects of precipitation
(Buckley et al. 2007; López and Villalba 2011; Ramírez and del Valle 2012;
Locosselli et al. 2013; Vlam et al. 2014a). These results along with findings of
temperature influences on tree growth from repeated tree diameter measurements in
several tropical forests (Clark et al. 2010; Dong et al. 2012) clearly show negative
Tree Rings in the Tropics: Insights into the Ecology … 451

influences of inter-annual variation in temperature on tropical tree growth. This

response is opposite to observed temperature responses of tree rings in cold cli-
mates (Fritts 1976), and consistent with negative effects of temperature on photo-
synthesis at high temperatures, above 30 °C (Doughty and Goulden 2008) and with
effects of temperature on respiration and evaporative demand (Lloyd and Farquhar
2008).
While there is a large uncertainty in climate models with regard to rainfall
predictions, there is a high degree of certainty for warming to occur throughout the
tropics (Stocker et al. 2013). This predicted warming may negatively affect tree
growth in the decades to come, but results of temperature sensitivity of tropical tree
growth based on annual fluctuations in temperature cannot be easily translated into
growth responses to a gradual rise in temperature, given possible acclimation of
photosynthesis and respiration to gradual temperature changes (Lloyd and Farquhar
2008). Also, the negative temperature effects may be offset by increases in atmo-
spheric CO2 (Lloyd and Farquhar 2008). In all, our analysis indicates that tropical
tree growth is moderately to highly sensitive to rainfall fluctuations and less so to
temperature variation. Sensitivities to climatic fluctuations are highly
species-specific, which may contribute to an overall resilience of diverse tropical
forests to increased climatic variability in rainfall and temperature.

Global Change and Tropical Tree Growth

Future global climatic and atmospheric changes may affect the physiology and
growth of tropical tree species in various ways. Major atmospheric and climatic
drivers affecting tree growth include rising CO2 levels, rising temperature, changes
in precipitation regimes and frequency of droughts, and increased atmospheric
deposition of nutrients. Tree-ring studies and analyses of stable isotopes in tree rings
can be used to quantify the effects of past climatic and atmospheric changes on tree
growth (Zuidema et al. 2013), and evaluate the performance of Earth system models
and improve their projections (Babst et al. 2014). Most importantly, the effects of
rising CO2 levels on tree physiology and growth (CO2 fertilization) can be studied
using stable carbon isotopes (13C) from tree rings and by changes in tree-ring width.
Analyses of carbon isotope ratios (δ13C) in tree rings over periods of time during
which atmospheric CO2 levels have increased can be used to evaluate changes in the
intrinsic water use efficiency (iWUE), the ratio of carbon fixed (photosynthesis) to
water lost (stomatal conductance) (McCarroll and Loader 2004). In addition, stable
oxygen isotopes (18O) could potentially be used to infer changes in water fluxes
(e.g. evapotranspiration from forests, Brienen et al. 2012a, b), and stable nitrogen
isotopes (15N) can be used to evaluate changes in nitrogen cycling (Hietz et al.
2011).
There are several advantages of using tree-ring analyses for studying global
change effects on tropical forests, compared to analyses based on plots: tree rings
cover longer periods of time, they yield growth rates at annual time resolution and
452 R.J.W. Brienen et al.

additional measurements (stable isotopes, anatomy) can be obtained from tree rings
(Zuidema et al. 2013; Babst et al. 2014). On the other hand, limitations of tree-ring
analysis include that it cannot be conducted for full tree communities, and that it
requires well-trained researchers and more sophisticated materials. In addition,
there are a number of methodological issues (Brienen et al. 2012a) that need to be
accounted for in tree-ring analysis. First, sampling issues arise due to the fact that
alive trees sampled in tree-ring studies may be (and are likely) a non-random subset
of the population, which may affect the outcome of analyses of growth trends over
time (Briffa and Melvin 2011; Brienen et al. 2012a). Dealing with these biases
requires the sampling of trees of all sizes (Brienen et al. 2012a; Nehrbass‐Ahles
et al. 2014). Some biases cannot be prevented by adjusting sampling schemes in the
field, and need to be assessed by additional statistical analyses (Groenendijk et al.
2015) or simulations (Vlam 2014). Second, analyses of trends require that temporal
trends in growth, isotope values or derived variables (e.g., iWUE) are separated
from those occurring over the size range (or age range) of trees. Third, age dis-
tributions and recruitment waves of tree species may also affect the outcome of
analyses of trends (Vlam 2014). There is a need for critical methodological eval-
uations and the development of statistical and simulation tools to evaluate the
robustness of trends detected based on tree-ring analyses (Briffa and Melvin 2011;
Brienen et al. 2012a; Vlam 2014; Peters et al. 2015). We therefore call for a
cautious interpretation of published trends in growth, iWUE or isotope values for
which such robustness checks are lacking.
So far, trends in iWUE and tree-ring width have been evaluated for a small
number of tropical tree species. In several of these studies the abovementioned
methodological issues have not been (sufficiently) taken care of, potentially
affecting the sign and strength of trends in iWUE or growth. For instance, a number
of studies on trends in iWUE over time have not or insufficiently separated the
strong ontogenetic trend in iWUE from that occurring over time due to CO2 rise
(Hietz et al. 2005; Nock et al. 2010; Brienen et al. 2011; Locosselli et al. 2013).
A recent study on 12 tree species across three tropical regions (Van der Sleen
et al. 2014) evaluated trends in iWUE for fixed diameter categories (8 and 27 cm
diameter), thus explicitly accounting for ontogenetic changes, and revealed a
30–35 % increase in iWUE over the last 150 years. A study on several Amazonian
species used the same approach to account for ontogenetic growth patterns and
reported increased growth rates for small individuals but not for large trees
(Rozendaal et al. 2010). These trends however may be confounded by differences
in survival of fast and slow growing trees (Brienen et al. 2012a). In a study on three
Thai species, decreasing growth trends were found (Nock et al. 2010) which may
partially have been generated by ontogenetic patterns and by effects of forest dis-
turbances. And finally, in the abovementioned pan-tropical study (Van der Sleen
et al. 2014) no growth increases were observed for 12 species over the past 100–
150 years. While these studies have explicitly addressed or discussed the effect of
several of the abovementioned biases, the reported trends may nonetheless have
been affected by forest disturbance and absence of tree regeneration (cf. Vlam
2014), and other biases (cf. Groenendijk et al. 2015).
Tree Rings in the Tropics: Insights into the Ecology … 453

In all, tree-ring studies in the tropics revealed (modest) increases in iWUE that
can be associated with the historical rise in atmospheric CO2 levels. So far, the
contribution of tree-ring and isotope analyses to generating insights on responses of
tropical trees to global change has been small, in part due to the abovementioned
methodological issues (biases), but also a limited research effort in the tropics.
Nevertheless, this contribution can potentially be substantial if sampling designs
and statistical analyses are appropriate, biases are taken into consideration and
results are interpreted cautiously.

Advances in Stable Isotope Measurements in Tropical

Tree Rings

Analysis of stable isotopes (δ18O, δ13C) is increasingly being used in tropical tree
rings. Such measurements provide additional information: carbon isotopes mainly
provide a measure for plant physiology (i.e., the magnitude of isotope discrimi-
nation is related to the ratio between carbon fixed per water lost; McCarroll and
Loader 2004), while oxygen isotopes reflect variation in isotopic composition of the
source water, tree transpiration rates and relative humidity (Sternberg 2009). In the
section below, we will outline some recent advances on applications of isotope
analysis in tropical tree rings, and the main insights obtained.
Carbon isotopes in tree rings provide a good drought signal in sites where
moisture stress is limiting growth (Gebrekirstos et al. 2009; Fichtler et al. 2010;
Brienen et al. 2011; Schollaen et al. 2013). During dry years stomatal aperture
decreases, leading to reduced influx of CO2 into leaf intercellular spaces, and thus a
lower intercellular [CO2] (ci) and lower isotope discrimination (Δ). An example of
the effect of precipitation on intercellular CO2 concentrations (derived from carbon
isotopes in tree rings) for a dry forest species from southern Mexico is shown in
Fig. 5f. At sites where trees experience less drought stress, the dominant factor
controlling tree ring δ13C may be the photosynthetic rate affected by irradiance (cf.
McCarroll and Loader 2004). In line with this, a study on a moist tropical tree species
comparing δ13C in tree rings before and after gap formation shows a positive rela-
tionship between δ13C and growth, thus suggesting variation in growth was most
strongly driven by temporal changes in light availability (van der Sleen et al. 2014).
These studies show the potential for carbon isotope measurements in tree rings to
help interpret the causes of temporal growth rate variation in tropical trees.
Oxygen isotopes in tree rings reflect variation in source water δ18O and plant
physiological effects like leaf water enrichment due to transpiration (Sternberg
2009). Correlations of inter-annual variation in tree ring δ18O of tropical trees with
precipitation δ18O, suggest that plant physiological effects are not very pronounced
and that tree rings in these species mainly record source water influences (Brienen
et al. 2012b, 2013; Schollaen et al. 2013). Figure 5g shows the relationship between
tree ring δ18O from southern Mexico and precipitation δ18O from San Salvador (ca.
700 km away). This shows that variation in source water δ18O (even from distant
454 R.J.W. Brienen et al.

stations) explains more than 60 % of the variation in tree ring δ18O, but the degree
to which source water controls tree ring δ18O may vary between sites and species.
Variation in source water δ18O depends on local precipitation intensity (i.e., the
amount effect, cf. Dansgaard 1964), the origin of the water source, and rainout
processes during water vapour transport. For which of these processes tree ring
δ18O provides a proxy, depends on the location and geography of the site. In the
western Amazon, δ18O in tree rings proved to be a strong indicator of total
basin-wide precipitation and river discharge (Brienen et al. 2012b), while tree ring
δ18O at other (less continental) sites shows good correlations with more regional
precipitation amounts (Poussart and Schrag 2005; Xu et al. 2011; Brienen et al.
2013; Schollaen et al. 2013).
Recent technical developments in isotope techniques allow for very precise
dissection of small wood at high resolution (e.g., Schollaen et al. 2013). This has
permitted the detection of annual cycles in species that lack anatomically distinct
rings, which could subsequently be used to infer growth rates, determine tree ages,
or relate the isotope or growth signals to climate (Poussart et al. 2004; Anchukaitis
and Evans 2010; Schollaen et al. 2013; Xu et al. 2014). In addition, high-resolution
isotope series of δ13C has provided insights into differences between evergreen and
deciduous species in allocation of photosynthates to reserves versus wood (Ohashi
et al. 2009; Gulbranson and Ryberg 2013), and high-resolution oxygen isotopes
may allow for more detailed seasonal reconstructions of historical rainfall regimes.
For instance, it may allow studying differences in dry versus wet season precipi-
tation (Schollaen et al. 2013), and can be used to detect short-term climate events
caused by the El Niño-Southern Oscillation (ENSO) (Evans and Schrag 2004;
Anchukaitis and Evans 2010) or tropical cyclones (Li et al. 2011).
Finally, a few other useful techniques include the measurement of wood density
using gamma radiation, X-ray or high-frequency densitometry (Schinker et al.
2003; De Ridder et al. 2010). High-resolution densitometry measurements could
greatly assist ring boundaries detection, for those species presenting growth
boundaries defined by density variation (cf. Fig. 2d, e), and density variations
themselves may contain climate information. For example, Worbes et al. (1995)
found a significant relationship between density variations and the length of the
terrestrial phase in floodplains of Central Amazonia.

Conclusions

While the study of tropical tree rings started over a century ago, most advances in
this field have been made during recent decades. Important insights arising from
these recent tropical tree-ring studies in relation to the theme of this book include:
• Tree-ring analyses of 71 tropical species shows that tree longevity is shorter than
often believed (mean longevity ca. 200 years), suggesting relatively fast rates of
turnover and carbon cycling in tropical biomes.
Tree Rings in the Tropics: Insights into the Ecology … 455

• Individual tropical trees show incredibly strong and persistent variation in

long-term growth rates, resulting in a fourfold variation in the ages of similarly
sized trees. Interestingly, this intraspecific growth variation exceeds the
long-term growth variation between species.
• A review of the climate sensitivity of tropical trees shows that annual growth of
tropical tree species is more sensitive to fluctuations in rainfall than temperature.
While informative for tree sensitivity to climatic fluctuations, these results
cannot be directly used to predict growth responses to long-term and gradual
changes in temperature or rainfall.
• Long-term trends in water use and growth can be obtained from measurements
of stable isotopes and tree-ring width, but such analyses need to take sampling
biases and other methodological issues into account. So far, few long-term
studies have revealed evidence for century-long increases in intrinsic water use
efficiency of several tropical tree species. These results indicate that tropical tree
physiology is changing, most likely due to rising CO2.
• Combined studies on tree ring width and stable isotopes are promising to gain
new insights into the response of tropical vegetation to climate change, validate
coupled climate-vegetation models and diagnose large–scale changes in the
climate system.

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Index

A Borneo, 84, 276, 367

Acclimation, 16, 325, 330, 357, 358, 366, 369, Brazil, 49, 83, 86, 129, 210, 213, 232, 233, 305
372, 373, 385, 392, 394, 396, 397, 399, Buckling, 80, 419, 423–426
401, 404, 405, 451 Buttress, 131, 140, 433
Adaptation, 6, 10, 15, 16, 18, 21, 29–31,
34–36, 128–132, 134, 135, 137–141, 151, C
159, 163, 165, 183, 221, 228, 262, 269, δ13C (carbon stable isotope composition), 31,
279–281, 291, 320, 321, 325, 327, 347, 36, 59, 451, 453
366, 369, 372, 385, 400, 441 C3, 7, 21, 32, 34, 36, 37, 156, 400
Adventitious roots, 4, 131 C4, 32, 156
Aerial root, 4, 5, 19, 140, 163 Calcium, 213, 265, 266, 268, 427
Africa, 45, 46, 49, 52, 60, 61, 338, 445 California, 46, 49, 58, 254
Agriculture, 46, 81, 136, 141, 262 Calvin cycle, 303, 324, 390
Amazonia, 39, 59, 69, 81, 86, 129, 131, 132, Canopy regeneration, 21
140, 141, 232, 234, 251 Capacitance, 77, 115, 120, 185, 188, 189, 207,
Andes, 40, 69, 182, 183, 185, 190, 191, 217, 218, 221, 243, 244, 247
196–198, 206, 268, 342 Carbon sink, 78, 338, 341, 348, 351, 352
Anisohydric, 210, 245, 251 Carbon starvation, 207, 210–212, 243, 245,
Anoxic soils, 150 251, 402
Anthocyanin, 35, 328 Caulescent, 70, 182
Arbuscular mycorrhizae, 82 Cavitation, 9, 73, 78, 115, 166, 208, 210, 219,
Architecture, 5, 7, 71, 75, 166, 206, 207, 221, 231, 243, 244, 246, 247
229, 245, 281, 320, 332 Cellulose, 368
Argentina, 51, 53, 110, 113, 117, 325, 329, Cerrado, 141, 213, 232, 238, 309
331, 340–342, 346 Chile, 45, 51, 52
Atmospheric carbon-dioxide, 68 China, 5, 115, 167, 279, 305, 338, 340–342,
Australia, 17, 49, 73, 132, 138, 141, 158, 166, 344, 347, 350
268, 305, 338, 392 Chlorophyll, 31, 71, 131, 327, 346
Chlorophyll fluorescence, 391
B Climate Change, 38, 46, 69, 82, 91, 139, 168,
Barro Colorado Island, 110, 250, 264, 265 170, 243, 246, 299, 300, 310, 352, 405, 455
Belowground biomass, 170 Climate change-type drought, 244
Belowground processes, 164, 250 CO2, 9, 14, 16, 30, 34, 36, 38, 48, 57, 84, 90,
Biomass, 16, 26, 36, 60, 72, 105, 109, 110, 113, 116, 130, 156, 159, 161, 162, 172,
117, 134, 162, 166, 169, 170, 228, 229, 188, 189, 195, 210, 230, 249, 271, 300,
261, 268, 276, 278–281, 289, 309, 343, 304, 309, 323, 328, 342, 343, 346, 348,
401, 440 352, 365, 390, 391, 394, 403, 440, 451, 452
Biomechanics, 109, 414, 431 Colombia, 40, 69, 197

© Springer International Publishing Switzerland 2016 463

G. Goldstein and L.S. Santiago (eds.), Tropical Tree Physiology,
Tree Physiology 6, DOI 10.1007/978-3-319-27422-5
464 Index

Concentration-carbon feedback, 105, 300, 309, G

310 Gas exchange, 9, 10, 48, 76, 90, 135, 164, 185,
Conservation, 7, 8, 28, 39, 61, 141, 170, 338, 188, 190, 243, 251, 330, 387
343 Global distribution, 68, 172
Conservative water use, 9, 15, 60 Growth ring, 129, 442
Costa Rica, 28, 37, 58, 59, 86, 182, 278, 393 Guiana Shield, 268
Crassulacean Acid Metabolism (CAM), 29, 48
Cuticular conductance, 31, 35, 243, 244, 252 H
Hawaii, 183, 278, 303
D Hemiepiphyte, 4, 7, 18
Deciduous, 46, 48, 49, 51, 58, 59, 119, 133, Hemiepiphytic Ficus, 6, 8–10, 21
137, 142, 207, 209, 219, 222, 228, 229, Hemiepiphytism, 6, 15
234, 248, 250, 303, 345, 347, 378, 441, 454 Herbivory, 212, 275, 282, 283, 301, 367, 368
Decomposition, 32, 38, 130, 236, 267, 276, Heteroblastic, 34, 35
291 Homoblastic, 35
Defense, 212, 253, 282, 359, 360, 362, 366, Hong Kong, 6, 165
368 Hydraulic architecture, 7, 74, 206–208, 221,
Dendrochronology, 440 245, 281, 332
Deuterium (2H), 237, 250 Hydraulic conductance, 8, 9, 14, 210, 212, 229,
Drought tolerance, 8, 10, 15, 60, 89 235, 266
Dry forest, 17, 29, 45–47, 68, 114, 210, 228, Hydraulic conductivity, 7, 8, 9, 59, 116, 117,
248, 251, 278, 283, 441, 453 208, 221, 230, 231, 234, 236, 246, 247, 331
Dynamic load, 414, 415 Hydraulic failure, 11, 15, 209–212, 221, 243,
245, 247, 402
E Hydraulic lift, 207, 232, 237, 239
Ecosystem nutrient budget, 26 Hydraulic redistribution, 216, 232, 234, 237,
Ecosystem productivity, 151, 172, 287, 303 239
El Niño, 234, 246 Hydraulic resistance, 207, 232
Electron transport capacity (Jmax), 390, 391, Hydraulic segmentation, 75, 207, 208, 221
396, 405 Hydrenchyma, 31, 35
Electron transport rate (ETR), 57, 326, 331 Hydrochory, 133
Elevated CO2, 36, 161–163, 172, 270, 309, Hypoxia, 164
391, 403
Embolism, 166, 186, 207, 208, 210, 216, 217, I
222, 229, 231, 232, 281, 344 Ichthyochory, 131
Epiphytes, 4, 7, 26, 28–30, 32, 36–40, 430 Igapó, 130, 131, 446
Evapotranspiration, 83–85, 142, 196, 338, 343, Iguazú, 340, 343
345, 441, 451 India, 6, 83
Internal CO2concentration (Ci), 57, 300, 453
F Isohydric, 210, 245, 251
Facilitation, 237 Isoprene, 84, 390, 400
Fertilization, 37, 84, 161, 213, 215, 263, 267, Isotopic composition, 36, 59, 250, 453
275, 276, 278, 279, 281–286, 288, 302,
307, 365 K
Fertilization experiments, 213, 263, 277, 279, Kakadu National Park, 138, 139
288, 290, 304
Fine root, 186, 232, 234, 251, 289 L
Flexural stiffness, 419 Lamina thickness, 72, 366, 368
Flooding, 21, 128–131, 133–135, 138–140, Leaf economic spectrum, 114, 358
163, 439, 442 Leaf life span, 72, 210
Fracture toughness, 188, 368 Leaf pigments, 323
Freestanding liana seedlings, 106, 110 Leaf mass per area (LMA), 10, 11, 357, 358,
French Guiana, 246, 247 370, 401
Fresh water flooding, 252 Leaf pubescence, 159, 186, 195
Index 465

Lenticel, 48, 131, 163 O

Life history strategy, 6, 106, 170, 275, 291 Okavango Delta, 128, 135
Lifespan, 18, 70, 76, 357–366, 368–370, Ontogenetic changes, 109, 439, 452
372–376, 378, 439 Oxygen isotope (δ18O), 451, 453, 454
Life span of trees, 221
Light-demanding tree, 21, 366, 447 P
Light fleck, 321, 323, 332 Panama, 4, 27–29, 38, 50, 51, 106, 114, 206,
Lignin, 131, 140 250, 261, 264, 266, 269, 278, 284, 303,
Litterfall, 37, 139, 262, 263, 268, 278, 286, 305, 325, 326, 361, 369, 392, 394
288, 302 Pantanal, 132, 133, 140
Litter manipulation, 275, 286–289 Paracou, 246, 247, 252
Long distance water transport, 73, 75, 79 Paraguay, 49
Long Substrate Age Gradient, 277 Páramo, 182, 184, 186, 188, 197
Peru, 278
M Phloem, 53, 72, 76, 83, 110, 140, 191, 231
Macronutrient, 276, 278, 291, 304 Phosphate, 269, 270, 290, 390
Madagascar, 46, 49–51, 60, 69 Phosphodiesters, 270
Mangrove, 150, 151, 156, 158–160, 163–167, Phospholipids, 269, 304
170, 232, 441, 443 Phosphomonoesters, 270
Marcescent, 184, 186, 191 Phosphorus, 38, 109, 164, 213, 214, 261, 262,
Maximum height, 137, 425 266, 268, 269, 275, 276, 302, 359, 390
Maximum photosynthetic rate (Amax), 113, Photo-oxidation, 390
195, 303, 304, 307, 308, 310, 324–327 Photoinhibition, 32, 328, 332, 344
Mekong delta, 128, 129, 132, 136–138 Photon flux density, 29, 106, 327, 330, 394
Mesophyll, 210, 366 Photorespiration, 82, 329, 390–392
Meta-analysis, 279 Photosynthesis, 7, 9, 29, 32, 36, 48, 57, 59, 76,
Mexico, 29, 46, 49, 50, 251, 283, 450 134, 162, 167, 230, 243, 244, 249, 252,
Micronutrient, 275, 291, 302, 308 280, 299–304, 308–310, 325, 329, 331,
Mineralization, 263, 269, 281, 404 338, 343, 344, 346, 349, 352, 385, 386,
Minimum conductance (gmin), 252 390, 393–395, 397, 400, 405, 451
Miombo forests, 135 Photosynthetic Bark, 45, 48, 49, 62
Monopodial, 68, 70, 90 Photosynthetic nitrogen use efficiency (PNUE),
Mortality, 73, 105, 135, 166, 190, 193, 207, 11, 359, 377
209, 211, 212, 243–246, 248, 253, 363, Photosynthetic phosphorus use efficiency
402–404, 448 (PPUE), 14
Mycorrhizal fungi, 34, 281 Photosystem II (PSII), 60, 326, 328, 391
Physiological traits, 4, 11, 16, 21, 59, 109, 221,
N 234, 266
Nebulophyte, 32 Phytase enzymes, 269
Necromass, 186 Plasticity, 6, 16, 21, 59, 109, 168, 170, 197,
New Zealand, 166, 168 221, 262, 319, 323, 324, 361, 363, 364,
Nitrate, 213, 290 369–373, 376, 397
Nitrogen, 14, 34, 38, 71, 90, 109, 131, 213, Pneumatophore, 163
214, 262, 275, 286, 350, 357, 359, 362, Poikilohydric, 35
365, 366, 369, 372, 451 Potassium, 109, 265, 276, 302
Nitrogen fixation, 164 Primary hemiepiphyte, 4
Nocturnal transpiration, 207, 212, 214–217, Puerto Rico, 37, 38, 50, 59, 403
236 Puna, 52
Nucleic acids, 269, 276
Nutrient limitation, 37, 163, 213, 262, 263, R
275–279, 291, 299, 301–303, 308–311, 365 Respiration, 57, 77, 87, 91, 164, 168, 212, 245,
Nutrient uptake, 29, 37, 207, 213, 214, 239, 249, 323, 327, 332, 338, 349–352, 359,
280, 301 365, 385, 397, 399, 401, 404, 451
Nutrient use efficiency, 360 Response ratio, 284, 307, 308
466 Index

Retamoid, 48, 52, 53, 56, 61 T

Ribulose 1,5-bisphosphate Tap root, 237, 430
carboxylase/oxygenase (Rubisco), 156, 390 Thermal optimum, 385, 386, 395
Ribulose bisphosphate (RuBP), 390, 395 Thylakoid, 303, 390, 400
Rosette, 32, 37, 70, 182, 184, 185, 187–189, Torsional stiffness, 419
191–196, 198, 206 Trade-off, 14, 221, 280, 282, 325, 357, 360,
Rubisco carboxylase activity (VCmax), 390 362, 378, 447
Transpiration, 35, 48, 58–60, 76, 78, 82, 84,
S 115, 118, 135, 161, 186, 206, 213, 214,
Safety margin, 10, 210, 211, 217 218, 231, 234, 239, 247, 248, 271, 281,
Salinity, 82, 132, 136, 150–152, 159, 162, 163, 302, 453
232 Tree growth, 135, 150, 239, 275, 276, 278,
Sap flow, 58, 60, 119, 207, 213, 219, 220, 341, 401, 439, 448, 450, 451
232–234, 236, 251 Tree ring, 439–442, 444, 448, 451, 453, 455
Sapwood, 8, 76, 77, 112, 212, 217–219, 221, Trichomes, 26, 30, 34
243, 244, 247, 248 Triose phosphate, 390
Sarcocaulescent, 48–50, 61
Savanna, 55, 68, 133, 138, 207, 210, 213, 215, U
220, 228, 230–232, 236, 238, 248, 450 Understory, 6, 15, 21, 36, 69, 72, 109, 138,
Sclerophylly, 36 307, 320–322, 324, 329, 332, 345, 366,
Secondary hemiepiphyte, 4 373–375, 446
Shade tolerant tree, 21, 326, 329 United States, 166, 172
Shear modulus, 418, 420, 422
Soil, 4, 9, 26, 29, 30, 37, 57, 61, 78, 82–86, 91, V
114, 115, 130, 134, 136, 150, 151, 156, Vapor pressure difference, 385, 393
163, 165, 182, 188, 193, 207, 213, 216, Vapor pressure deficit, 57, 82–84, 114, 215,
228, 231–234, 236, 237, 239, 243, 250, 245, 385, 393
251, 262, 264, 266–270, 275–279, Várzea, 130, 131, 140, 446
281–283, 287, 288, 290–292, 300, 301, Vascular bundles, 53, 70, 72, 77, 79, 80, 229
303, 309, 310, 338, 343, 350, 357, 362, Velamen, 30, 31
366, 370, 372–375, 402, 403, 428, 446 Venezuela, 6, 46, 182, 197, 206, 278
Soil chronosequence, 268, 277 Vietnam, 136
Soil nutrients, 213, 265, 266 Vulnerability curve, 246, 247
Specific leaf area (SLA), 60, 107, 108, 114, Vulnerability to cavitation, 208
162, 170, 306, 324, 327
Stable isotopes, 34, 151, 238, 451, 453, 455 W
Starch, 60, 78, 229, 390 Water deficit, 7, 15, 35, 57, 58, 61, 77, 115,
Static load, 414–416 185, 221, 234, 244, 337, 342
Stem capacitance, 116, 185, 189, 207, 218 Water potential, 7, 12, 75, 82, 115, 116,
Stem photosynthesis, 57, 230, 249 131, 151, 155, 185, 187, 190, 193–195,
Stoichiometry, 262, 291 209, 210, 215, 218, 220, 231–234,
Stomata, 7, 9, 11, 31, 35, 48, 49, 57, 115, 188, 236, 239, 243, 244, 246, 247, 251,
207, 212, 222, 245, 249, 394 342, 375
Stomatal conductance (gs), 7, 9, 10, 12–14, 36, Water relations, 40, 77, 185, 189, 206, 221,
60, 76, 82, 87, 115, 116, 134, 155, 159, 253
188, 189, 195, 213–215, 230, 231, 252, Water transport, 8, 11, 73, 115, 166, 208, 237,
300, 301, 331, 342, 394, 405, 451 246, 247, 331, 344
Strain, 16, 414, 416–418, 421, 422, 427 Water uptake, 30, 58, 151, 155, 185, 213, 229,
Stress, 10, 12, 30, 35, 80, 82, 83, 110, 132, 251, 360
161, 166, 182, 198, 212, 249, 280, 328, Water use efficiency, 9, 36, 48, 156, 161, 162,
343, 387, 416–418, 427, 433, 441, 453 250, 281, 300, 301, 403, 451, 455
Succulence, 26, 31, 32, 35, 53, 58, 60, 62, 155 Waterlogging, 129, 134
Supercooling, 89, 190–192 Wind, 26, 72, 80, 81, 90, 133, 192, 212, 413,
Support-seeker liana seedlings, 110 415, 416, 426–428, 431, 433
Index 467

Wood density, 58, 110, 112, 207, 217, 218, Y

221, 245, 246, 267, 281, 454 Yucatan, 250

X
Xylem, 8, 9, 15, 53, 70, 72, 74–76, 110, 115,
151, 185, 191, 210, 212, 229, 231, 239,
243–247, 267