Forest Systems
26 (2), eR02S, 20 pages (2017)
eISSN: 2171-9845
https://doi.org/10.5424/fs/2017262-11255
Instituto Nacional de Investigación y Tecnología Agraria y Alimentaria O. A., M. P. (INIA)
REVIEW ARTICLE
OPEN ACCESS
Natural regeneration in Iberian pines: A review of dynamic processes
and proposals for management
Rafael Calama1,2, Rubén Manso3, Manuel E. Lucas-Borja4, Josep M. Espelta5, Miriam Piqué6, Felipe Bravo2,7, Carlos del Peso2,7, and
Marta Pardos1,2
1
INIA-CIFOR, Dpt. Silviculture and Forest Management, Ctra A Coruña km 7.5, 28040 Madrid, Spain. 2 iuFOR. Sustainable Forest Management Research Institute INIA-UVa. Avda. Madrid 44, 34004 Palencia, Spain. 3Forestry Comission. Northern Research Station. Roslin Midlothian
EH259SY, UK. 4Castilla-La Mancha University, Technical School of Agricultural and Forestry Engineering, Campus Universitario s/n, 02071
Albacete, Spain. 5CREAF. 08193 Cerdanyola del Vallès (Barcelona), Spain. 6Sustainable Forest Management Unit, CTFC. Ctra. de Sant Llorenç de
Morunys, Km 2, 25280 Solsona (Lleida), Spain. 7Valladolid University, ETS Ingenierías Agrarias, Dept. Producción Vegetal y Recursos Forestales.
Avda. Madrid 44, 34004 Palencia, Spain.
Abstract
Aim of study: Designing adequate silvicultural systems for natural regeneration of a forest species requires sound knowledge of
the underlying ecological subprocesses: flowering and fruiting, seed dispersal and predation, seed germination, seedling emergence
and seedling survival. The main objective of the present work is to carry out a review on the current knowledge about the different
subprocesses governing the regeneration process for the main Iberian Pinus species, in order to propose scientifically based management
schedules.
Area of study: The review focuses on the five main native Pinus species within their most representative areas in the Iberian
Peninsula: Pinus nigra in Cuenca mountains, Pinus sylvestris in Sierra de Guadarrama, Pinus pinaster and Pinus pinea in the Northern
Plateau and Pinus halepensis in Catalonia.
Material and methods: Firstly, currently available information on spatiotemporal dynamics and influential factors is introduced
for each subprocess and species. Secondly, current regeneration strategies are characterized and the main bottlenecks are identified.
Finally, alternative silvicultural practices proposed on the light of the previous information are presented.
Main results: Different climate-mediated bottlenecks have been identified to limit natural regeneration of the Iberian pine species,
with seed predation and initial seedling survival among the most influential. New approaches focusing on more gradual regeneration
fellings, extended rotation periods, prevent big gaps and program fellings on mast years are presented.
Research highlights: Natural regeneration of the studied species exhibit an intermittent temporal pattern, which should be aggravated
under drier scenarios. More flexible management schedules should fulfil these limitations.
Additional keywords: seed production; seed dispersal; seed predation; germination; regeneration fellings.
Authors´ contributions:RC and MP conceived the idea and structure of the article, and gathered all the previous information,
synthetized it and wrote the main corpse of the text; RM, JME, MELB, MP, FB, CDP and MP compiled and prepared information for
the different species and processes, and revised the manuscript.
Citation: Calama R.; Manso R.; Lucas-Borja M. E.; Espelta J. M.; Piqué M.; Bravo F.; Del Peso, C.; Pardos M. (2017). Natural
regeneration in Iberian pines: A review of dynamic processes and proposals for management. Forest Systems, Volume 26, Issue 2,
eR02S. https://doi.org/10.5424/fs/2017262-11255
Received: 19 Feb 2017 Accepted: 07 Jul 2017.
Copyright © 2017 INIA. This is an open access article distributed under the terms of the Creative Commons Attribution (CC-by)
Spain 3.0 License.
Funding: Spanish Program for R+D (Projects RTA-2013-00011-C2.1, AGL-2010-15521, RTA-2007-00044, POII10-0112-7316,
AGL-2011-29701-C02-00, AGL-2014-51964-C2-1-R); EU 7th Framework Program (ARANGE-289437)
Competing interests: The authors have declared that no competing interests exist.
Correspondence should be addressed to Rafael Calama: rcalama@inia.es
Introduction
One of the main aims of sustainable forest
management is to guarantee forest persistence over
time (Nyland, 2002). This general objective implies that
managed stands need to be successfully regenerated.
In Silviculture, natural regeneration is defined as the
renewal of a forest stand by natural seeding, sprouting,
suckering, or by layering seeds that may be deposited
by wind, birds or mammals (Pardos et al., 2005).
The successful regeneration of a forest conforms a
temporal succession of phases that should be effectively
realized: seed production, seed dispersal, seed
predation, germination, emergence, seedling survival
and seedling initial growth. In this way, regeneration
can be considered as a multistage process (Fig. 1)
2
Rafael Calama, Rubén Manso, Manuel E. Lucas-Borja, Josep M. Espelta, Miriam Piqué, Felipe Bravo, et al.
Figure 1. Multistage process of natural regeneration
consisting of underlying consecutive subprocesses that
often can be identified as a series of successive survival
thresholds for potential seedlings (Pukkala & Kolström,
1992; Manso et al., 2014a). The process begins with
the supply of seeds from soil or aerial seedbanks, but
seed supply is commonly highly variable at different
spatial and temporal scales. Across an interval of
several years, several tree species appear to produce
many more small crops than large crops, such process
being known as masting (Kelly, 1994). Once the seed
is available, seed dispersal takes place. Seed dispersal
is thought to enable seeds to escape competition
(with their parents, with other seedlings and/or with
surrounding vegetation) and to colonize favourable
sites (Howe & Smallwood, 1982). Both wind and
animals play important roles in establishing seed banks
in the soil. The density of seeds deposited in a particular
location within a stand is a function of stand stocking
and the spatial arrangement of trees (source), and of
seed production and the capacity for seed dispersal
over long distances (Manso et al., 2012). However,
on heterogeneous environments the spatial pattern of
seed dispersal commonly does not determine the spatial
pattern of established seedlings (Meiners et al., 2002).
In this sense, seed predators are considered to be major
seed mortality agents, structuring recruitment patterns
that will depend in turn on the proportion of seeds
Forest Systems
escaping predation at the source, the mean distance
from the source of dispersed seeds and of predators’
activity, among others (Nathan & Casagrandi, 2004;
Manso et al., 2014b). Frugivore behaviour plays a key
role in plant distribution and demography (Jordano,
1992), ultimately even conditioning species persistence
(Hulme, 1997). Furthermore, differences in hoarding
habits (scatter-hoarding vs larder-hoarding) may impact
seed germination and seedling establishment.
Once the seeds have reached the soil, subsequent
regeneration subprocesses include (i) the germination
of the seeds: defined as the process starting by seed
imbibition and ending with the complete elongation
of the radicle; (ii) seedling emergence, ending with the
complete liberation of the cotyledons; and (iii) seedling
establishment, extending up to the initial phases
of seedling survival. Germination occurrence and
germination timing play an essential role in subsequent
seedling survival (Baskin & Baskin, 2001) and therefore,
in the overall success of natural regeneration (Manso
et al., 2013a,b). In addition, as with seed predation,
germination strongly contributes to reshape recruitment
patterns. The possibility that a seedling emerges and
survives in a given site depends on the metabolic
reserves of the seed. Among the specific characteristics
of plants, seed size has been defined as the most
selective trait, conditioning the spatial and temporal
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Natural regeneration in Iberian pines: A review
pattern of recruitment of the species (e.g. Calama et al.,
2015a). According to the k and r reproductive strategy
(MacArthur & Wilson, 1967) plants must respond to a
trade-off, either producing abundant small-size seeds,
with limited reserves, or producing less large-seed, with
abundant reserves (Westoby et al., 1992). Seedling size
is dependent on seed size during the first weeks until the
true leaves replace the cotyledons as the primary source
of carbohydrates (Greene et al., 1999). In general,
large-seeded species show higher initial growth, but
lower relative growth rate with time and usually occupy
wider geographical ranges (Aizen & Patterson, 1990).
Plant performance depends on the underlying patterns
of resource availabilities. Resources vary spatially and
temporally and species differ in their ability to tolerate
resource scarcity. Thus, more than one resource may
be limiting simultaneously among microsites or at
different times within the same microsite or for different
species grown together (Latham, 1992). Differences in
performance ranking across resource gradients will
result in patterns of seedling abundance that may persist
in the composition of adult trees community.
Natural regeneration has been for long a primary
concern in the forest management of Mediterranean
species. Natural regeneration is commonly unsuccessful
in Mediterranean species for different reasons. Some of
them are directly related to forest management (the use
of silvicultural systems which lead to low densities;
long rotations inducing poor seed crops during the
regeneration period; excessive grazing and uncontrolled
ploughing activities; intensive pruning for providing
fuelwood). Others, however, are related to the species
themselves (the masting habit and lack of synchrony
with regeneration fellings and adequate years for
seedling establishment), to the habitat (soil compaction;
competition with ground vegetation; inadequate
overstorey density and forest fires) or to climate (severe
summer droughts and high summer temperatures that
lead to regeneration failure). Thus, a deep knowledge
of the ecological processes involved in each stage of
regeneration would help to identify the bottlenecks in
natural regeneration, supporting forest planning under
criteria of adaptive silviculture.
The main aim of this work is to thoroughly review the
current state of the knowledge on natural regeneration
of the five main Iberian pine species. We focus on the
most representative areas for these species (Table 1):
Pinus nigra Arn. ssp. salzmannii (Spanish black pine)
in Cuenca mountains, Pinus sylvestris L. (Scots pine) in
Sierra de Guadarrama, Pinus pinaster Ait. (Resin pine)
and Pinus pinea L. (Stone pine) in the Northern Plateau
and Pinus halepensis Mill. (Aleppo pine) in Catalonia.
In a first step, we list the currently observed problems
for the regeneration of the species. Subsequently, we
make a comprehensive review of the state of art of the
different ecological subprocesses involved in natural
regeneration: flowering and fruiting, seed dispersal,
pre and postdispersal seed predation, seed germination,
seedling emergence and initial seedling survival, in
order to identify potential bottlenecks. Finally, we
present recently implemented silvicultural practices,
based on scientific findings, aiming to promote natural
regeneration of the species. We have mainly focused
this review on the processes and factors leading to the
Table 1. Main characteristics of the studied species and regions
Characteristics
P. nigra
P. sylvestris
P. pinea
P. pinaster
P. halepensis
Cuenca Mountains
Sierra Guadarrama
Northern Plateau
Northern Plateau
Catalonia
Involved provinces
Cuenca
Madrid, Segovia
Area occupied by the
species (ha)
259,000
130,000
60,000
124,000
290,000
Altitudinal range (m)
1000 - 1600
1200-1800
600-800
750-850
0-1000
10.7
8.7
12.5
11.9
13.8
Studied region
Average annual
temperatura (ºC)
Annual rainfall (mm)
Valladolid, Segovia Valladolid, Segovia Barcelona, Girona,
Tarragona
700
882
450
430
525
Calcareous
Granites and gneiss
Quartz
Quartz
Calcareous
Sandy-Loam
Sandy-loam
Sands
Sands
Carbonated
materials
Mean water holding
capacity (mm)
30
210
100
100
75
Traditional silvicultural system
Uniform
shelterwood
Uniform
shelterwood
Uniform
shelterwood
Uniform
shelterwood
Diameter selection
cutting
120-150
100
100
80
60-80
Bedrock
Main type of soils
Rotation (years)
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Rafael Calama, Rubén Manso, Manuel E. Lucas-Borja, Josep M. Espelta, Miriam Piqué, Felipe Bravo, et al.
successful initial establishment of the species. Thus we
have deliberately omitted long term seedling and sapling
survival processes as herbivory by large ungulates,
despite the potential importance this process has on
natural regeneration success in both temperate (Putman,
1996) and Mediterranean forests (Zamora et al., 2001).
Natural regeneration in Iberian pines:
Current situation in case study regions
Natural regeneration of Iberian pine stands has been
a major concern for forest managers of the studied
regions since the end of 19th century, when rational
and ecologically-based forest management started to
be applied. In that early time the main effort focused
on homogenising stand composition, increasing forest
standing stock and transforming age-heterogeneous
stands into even-aged ones. However, serious failure
in natural regeneration have also been widely detected
for the different species since then, the issue becoming
dramatically severe over the last decades.
Since the first management plans for P. nigra forests
in Serranía de Cuenca, dated in 1895 (Los Palancares
forest), the commonly proposed silvicultural system for
the species was the uniform shelterwood system, with a
rotation length of 100-120 years and a regeneration period
of 20 years. However, failure in natural regeneration
was detected by the decade of 1920’s (Tiscar et al.,
2011). In a first diagnosis of the main causes leading to
regeneration failure some authors cited: masting habit,
occurrence of consecutive dry summers, excessive
grazing and uncontrolled ploughing activities (Serrada
et al., 1994), soil compaction (Trabaud & Campant,
1991), inadequate overstorey cover and forest fires.
Recent studies (Tíscar et al., 2011) point out to climate
conditions as the main current limitations, being natural
regeneration in a typical dry summer largely threatened.
P. sylvestris is a Eurosiberian species, with the
southern limit of its distribution area in the Mediterranean
mountain environment in Spain. In this region, drought
is considered as the main abiotic factor constraining
the establishment of P. sylvestris in the Mediterranean
environment (Barbeito et al., 2009), unlike in Northern
and Central Europe, where low temperature, biotic
factors (invertebrates, herbivores and pathogens) and
competing vegetation are the main limiting factors. In
Sierra de Guadarrama, some P. sylvestris forests, as
Navafría and Valsaín, have been rationally managed
and successfully regenerated since 1895 and 1899,
respectively. Traditional silvicultural systems in these
forests relied on uniform shelterwood fellings over
a 100 to 120 year rotation period. In Navafría forest
mature stands are completely removed after a 20-years
Forest Systems
regeneration period, followed by soil scarification. The
regeneration period in Valsaín forest is extended to 40
years to assure sufficient natural regeneration, without
any additional intervention (Pardos et al., 2008). The
uniform shelterwood system contrasts with the typical
systems in northern and colder regions, even in Spain,
where the species is successfully regenerated by means
of clearcutting (Montero et al., 2008a).
The establishment of natural P. sylvestris regeneration
in the Spanish Central range shows a great spatial and
temporal variability (Pardos et al., 2008). Mast &
Veblen (1999) suggested that episodes of regeneration
might require a combination of several factors such as a
good seed year, seedbed conditions and the absence of
drought and fire. However, the coincidence of a good
prseed year and the absence of drought is not actually
so common in central Spain, thus resulting in failure
in regeneration. In addition, lack of regeneration has
also been observed in both the timberline and the lower
altitudinal limit, where P. sylvestris is mixed with other
species.
P. pinaster and P. pinea share territory, ecological
conditions and historical management traits within the
Northern Plateau of Spain, where both species occur in
either pure or mixed stands. By the end of 19th century,
the forests of this region exhibited a deplorable state,
mainly due to abusive grazing, defective stocking
volume, intensive pruning for fuelwood purposes and
complete lack of regeneration (Gordo, 1999). Given
these circumstances, the main objective of the foresters
was to transform these depauperated forests into
pure even-aged stands. Clearcutting by strips system,
followed by either lateral seed dispersal (P. pinaster)
or artificial sowing (P. pinea) using local seeds was
the main method used. This method also permitted the
change of species at the stand level depending on the
main product being favoured by management: cones
and nuts (P. pinea) or resin (P. pinaster) (Gordo et al.,
2012a).
In P. pinea, clearcuttings were successfully
maintained up to the end of the decade of 1970’s,
where closer-to-nature regeneration systems where
applied. Based on the experience from other regions
(e.g. Andalusia), uniform shelterwood system
was proposed (Montero et al., 2008b). Under this
scheme, the seeding felling is scheduled when the
stand reaches 100 years, which ideally reduces stand
density up to 60 trees/ha. Two secondary fellings
are usually applied within an interval of 5-15 years,
aiming to completely regenerate the stand in a period
of 20 years at maximum. Cone collection should be
restricted, at least during the initial phases of the
regeneration process. Unfortunately, this system
widely failed throughout the sandiest locations within
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Natural regeneration in Iberian pines: A review
the Northern Plateau, mainly due to incapacity for
disperse seeds on large gaps, seed predation and
summer seedling mortality. As a matter of fact, large
areas remained without regeneration years after the
fellings, exhibiting large highly-exposed gaps where a
deep grass layer was installed instead. Contrastingly,
advanced regeneration occupied unmanaged patches,
leading to non-viable, bad-shaped trees, with low
potential as cone producers. As an alternative, in
those locations with abundant advanced regeneration,
a conversion into uneven-aged stands by means of
group selection system has been successfully applied
(Calama et al., 2005).
P. pinaster was traditionally favoured in the
Northern Plateau up to decade of 1960s, due to the
economic importance of the resin collection. This
production conditioned the whole management
system, resulting in short rotations (80 years) and
regeneration periods (10 years). These short periods,
together with grazing and the keeping of mature resin
producers, which hold low seed production, resulted
in failure of clearcutting methods. Artificial sowing
was therefore widely applied to ensure the stand
homogeneity, even on sites where the species was
not well adapted. Resin price dropped by the mid70s, leading to the successful application of extended
rotation periods (up to 100 years) and uniform
shelterwood systems in a 20-year regeneration
period. Despite this early success, regeneration of the
species is becoming challenging over the last decades
in some areas. Soil conditions, the more frequent
occurrence of extreme droughts and the deepening
of the water table due to the increase of irrigation
practices in neighbouring lands have been suggested
as potential agents behind this failure (Gordo et al.,
2012a).
Finally, P. halepensis represents a singular case
within the Iberian pines. As a species very well
adapted to wildfires, regeneration massively occurs
after an intense forest fire. Strikingly, there are very
few experiences about the success of regeneration
cuttings in P. halepensis. Additionally, the species is a
clear shade-intolerant one and therefore management
guidelines suggest managing it as even aged forests,
by applying clearcutting or uniform shelterwood
system (del Rio et al., 2008). However, in the main
part of P. halepensis forests in Catalonia negative
selection cuttings, focusing only on large trees, have
been commonly applied (Saura & Piqué, 2006). This
has resulted in open forests colonized by understory
species and Quercus sp., while the worst shaped and
genetically depauperated pines stay in the forest,
hence decreasing stand quality, vitality and seed
production. In addition, resulting forest structures
are very vulnerable to forest fires due to the vertical
continuity of vegetation stratums.
Regeneration processes
In this section we present the current state
of the knowledge associated with the different
processes involved in the natural regeneration
for the species, which will permit a subsequent
diagnosis and identification of main bottlenecks for
the regeneration of the species in the studied areas.
At this point it is noteworthy to mention that while
Iberian pines share many common traits – they are
obligate seeders, do not form lasting seed sol banks,
they show masting events… – there are marked
interspecific differences in such features linked
with seed size, dispersal strategies, fire evasion and
drought resistance strategies, pioneering character
Table 2. Main regeneration traits for the five studied species
Regeneration trait
P. nigra
P. sylvestris
P. pinaster
P. pinea
P. halepensis
Seed length (mm)
5-8
3-5
7-9
15-20
5-7
Wing length (mm)
15-20
12-17
30
25
15-20
Seed weight (mg)
15-25
10-15
35-65
600-1000
20-25
Maximum dispersal distance (m)
100-150
100-120
50-60
10
120-150
Seed release
January-May December-March June-August May-June
March-May1
Main dispersal agent
Wind
Wind
Wind
Gravity
Wind
Serotiny
Low
Low
High
Low
Very high
Sexual maturity age (years)
15-40
25-30
10-15
20-25
5
High
Intermediate
Low
Intermediate
Very low
Shade tolerance
Leaf specific conductivity (m /MPa·s)
3.24 E-07
4.98E-07
3.43E-07
2.19 E-07
0.95 E-07
Water use efficiency (‰ δ 13C)
-26.6
-27.0
-24.7
-18.9
-16.1
2
Non-fire associated seed release
1
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Rafael Calama, Rubén Manso, Manuel E. Lucas-Borja, Josep M. Espelta, Miriam Piqué, Felipe Bravo, et al.
and shade tolerance that will define specific natural
regeneration processes (Table 2).
Flowering, fruiting and seed production
The first stage in any regenerative process is
flowering, fruiting and seed production. Although seed
limitation has been reported as a main bottleneck in
natural regeneration of forest species (Muller-Landau et
al., 2002), there still exists a wide gap on the knowledge
on specific topics such as total amount of seeds annually
produced, climate factors affecting fruit and seed
production, initial and final ages for bearing fruits and
masting habit.
P. nigra is assumed to be a masting species, with good
seed crops occurring every 6 years (Alejano et al., 2008),
the minimum seed bearing age being between 15 to 40
years. Existing observations of P. nigra reproductive
ecology may support both the pollination coupling and
the predator satiation hypotheses for masting (LucasBorja et al., 2011). The wind pollination hypothesis
states that wind-pollinated plants obtain reproductive
benefits by synchronizing large flowering efforts,
because it increases the probability of pollination (Smith
et al., 1990). It has been observed that P. nigra produces
higher percentages of empty seeds (unpollinated) in low
flowering years (Tíscar, 2007). Similarly, the predator
satiation hypothesis states that large seed crops are likely
to satiate seed predators, which thus would destroy a
lower percentage of crop (Kelly, 1994). Moreover, seed
production is significantly lower at the altitudinal limit
of the species distribution than in the most favourable
habitat (Lucas-Borja et al., 2012), confirming that pines
under stressed conditions tend to produce solely male
cones or even stop reproducing (Shmida et al., 2000).
Seed production in mast years can be up to 10-fold
greater than that of a non-mast year, with average values
over 70 seeds/m2 on mast years and favourable locations,
and less than 10 seeds/m2 on non-masting years and/
or altitudinal limits (Lucas-Borja et al., 2011, 2012).
Larger values of seed production were identified in high
dense stands. Nevertheless, these values are notably
smaller than those obtained in other non-limiting areas
such as Cazorla (average values of seed dispersal over
600 seeds/m2; Tiscar, 2007). Thus, seed availability is
one of the main factors limiting the natural regeneration.
P. sylvestris in the Central Range of Spain starts
producing a high amount of cone and seeds at 25-30 years
old (in isolated trees) or 40 years old (when growing in
canopy) holding this capacity up to very high ages (Ruiz
de la Torre & Ceballos, 1979; Rojo & Montero, 1996).
According to the classical trade-off theory by Smith &
Fretwell (1974) a small-seeded species like P. sylvestris
will produce a sufficient amount of seeds every year.
Forest Systems
Figure 2. Annual seed production in Pinus sylvestris stands in
Valsaín forest over the altitudinal range of the species. Lines
represent seed production for three different precipitations: half
(dotted thin line), the same (dashed line) and twice (solid thick
line) the mean value for April and May precipitation two years
before cone maturation (PPapr_my_2). Original figure based on
Calama et. al. (2015b).
Confirming this, during a four-year study (2005 to 2009)
annual seed production was high enough to discard
either source or dispersal seed limitations (Calama et
al., 2015a). Annual seed density mean values ranged
from 150-300 seeds/m2 (Calama et al., 2015b), except
in the lower lands (Fig. 2) where the species occurs in
mixed stands with Quercus pyrenaica Willd. (average
production 36 seeds/m2). A certain masting is to be found
in the species, with about two good crops every seven
years (Montero et al., 2008a), although null crops are
absent (Hilli et al., 2008). In the aforementioned four-year
study, 16-fold average differences between years were
detected, mainly related with the precipitation occurring
in the spring two years before cone maturation (Calama et
al., 2015b). It is worthwhile to mention that the observed
values for P. sylvestris in Central Range are remarkable
if compared with that of the relictic forests of the species
in Andalusia (average annual production 2-20 seeds/m2;
Castro et al., 1999). Seeds from trees in the timberline
stand showed a different interannual variation to those at
mid-altitudes (1400 – 1600 m), where seed production
seems to be maximized. Despite these spatiotemporal
differences, natural regeneration for P. sylvestris seems
not to be limited by the production of seeds, except on the
lower altitudinal limit and/or in years with very low seed
production (Calama et al., 2015a).
Cone and seed production has been largely studied
for P. pinea, given the edible character of the nut. In
this respect, there is a major feature that makes P.
pinea different from all other Iberian pines, as cone
development occurs over a 3-year period, in contrast to
the 2 years of the rest of pines (Calama et al., 2012).
Additionally, P. pinea exhibits a large size seed (over
700 mg ± 200 mg, with 20 mm in length), which
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Natural regeneration in Iberian pines: A review
prevents wind dispersal from occurring. Cone and
seed production is delayed up to an age of 15-20 years,
although it can be anticipated in grafted plantations
(Mutke et al., 2012). On the opposite, trees hold their
productive capacity up to 160-180 years.
Given its large size, and according to the trade-off
theory, we should expect smaller seed crops than in
other species. This was confirmed by the average seed
production of 9.4 seeds/m2 observed over a 5-year
experiment on seed dispersal in P. pinea (Calama et al.,
2015a). However, large differences in cone and seed
production are detected within the study area. Lower
crops are associated with sandy soils with low water
holding capacity (Calama et al., 2012). Low density
stands, where trees can expand their crowns freely,
are more favourable for cone and seed production than
overdense stands (Calama et al., 2011).
Additionally, the species shows a noticeable, climatemediated masting habit, which can result in interannual
20-fold magnitude differences in cone production at
regional level, largely synchronized within the study
area (Calama et al., 2012). The rate of trees not bearing
cones at all in very bad years can reach values close
to 80% (Calama et al., 2016). The occurrence of
favourable climatic conditions during key phenological
stages as bud formation, bud differentiation, conelet
survival through first summer and winter and cone
enlargement determine mast events (Mutke et al., 2005;
Calama et al., 2011). In addition, masting in P. pinea
is secondarily ruled by a three-year delayed resource
depletion effect, resulting in lower than expected cone
production three years after an exceptional bumper crop
(Calama et al., 2016).
Previous findings indicate that the lack of seed
availability could be considered a main limitation for P.
pinea natural regeneration in unfavourable crop years,
especially in overdense stands within low producing
sites. The results of the above mentioned seed dispersal
study came to corroborate this, as regeneration
limitation was related to seed shortage in three out of
the five studied years (2005, 2008 and 2009) (Calama
et al., 2015a).
Contrarily, P. pinaster seed availability has never
been considered a limiting factor within the Northern
Plateau, due to abundant and frequent cone production
and the silviculture approach implemented that always
left a sufficient number of trees in the stands during
the regeneration phase (Gordo et al., 2012a). While
a serotinous species, this trait in P. pinaster is not so
marked in the Northern Plateau as in other regions
(Tapias et al., 2001). However, recent studies have
given exact figures by counting cones on standing
trees and collecting seed from traps (Ruano et al.,
2015), resulting on average values around 7-24
Forest Systems
seeds/m2, though showing large spatial and temporal
availability (3.6 fold magnitude between years). Juez
et al. (2014) found that just a small fraction of mother
trees are responsible for a high proportion of seed
production. Ruano et al. (2015) identified a climatic
control over masting habit in the species, with the
precipitation during the period of secondary growth of
the cones positively affecting cone production. Thus,
water stress may limit seed production in extreme dry
years. Additionally, they identified that following very
intensive regeneration fellings, seed availability could
be a limiting factor.
P. halepensis presents a combination of several
remarkable reproductive attributes related with cone
and seed production that helps explaining the great
colonization potential of this species and its high
resilience to intense fire events (de las Heras et al., 2012).
P. halepensis starts as female the reproductive stage,
prior to the appearance of male structures in secondary
branches and it shows an extremely short juvenile
period, with an early onset of cone and seed production
from 3-5 years of age (Tapias et al., 2001; Espelta et al.,
2008). Annual production of cones is often massive and
quite regular across years (Verkaik & Espelta, 2006)
and part of the crop of mature cones is retained in the
canopy for several years as serotinous (closed) cones
(45–80% according to Thanos & Daskalakou, 2000).
According to these authors, considering both serotinous
and non-serotinous cones, canopy seed bank can reach
values between 115-790 seed/m2, with 10-20% (del Río
et al., 2008) that can be released during summer without
exposure to fire.
In fact, serotiny has probably been one of the most
analysed reproductive attributes of P. halepensis. This
pine is a weak or partial serotinous species as rupture of
serotinous cones is certainly induced by fire, but it may
also occur spontaneously, especially when canopies are
suddenly exposed to high radiation levels (Verkaik &
Espelta, 2006) or after drought episodes (Espelta et al.,
2011). Serotiny degree of P. halepensis decreases with
ageing and tree size, a pattern suggested to be caused
by the costs of maintenance for the plant of these
long-lasting structures competing with younger cones
for resources (e.g. water, in Espelta et al., 2011). In
Spain, a large variability in the degree of serotiny has
been observed among populations across geographical
gradients revealing that serotiny may increase with
stand density and from northern to southern populations
(Moya et al., 2007, 2008; de las Heras et al., 2012).
Recently, studies conducted in common garden
experiments have demonstrated, after controlling for
the effects of tree size, that serotiny has a genetic basis
and it is lower in pines from harsh (dry and cold) sites
compared with mild sites (Martín-Sanz et al., 2016),
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Rafael Calama, Rubén Manso, Manuel E. Lucas-Borja, Josep M. Espelta, Miriam Piqué, Felipe Bravo, et al.
while is more abundant on post-fire stands than on
stands established in fire-free conditions (Ne’eman et
al., 2004).
In spite of the well-known importance of the
occurrence of fire, the abundant production of cones
in P. halepensis ensures a massive availability of seeds
even in the absence of this disturbance (del Río et al.,
2008). Therefore seed availability cannot be considered
a limiting factor for the species, except in very dry
conditions, or when the lapse between two fire events
is shorter than the expected time for younger plants to
reach sexual maturity (del Río et al., 2008; Espelta et
al., 2008).
Seed dispersal
Seed dispersal is a key process in natural regeneration,
determining the arrival of seed to favourable sites for
establishment and the spatial location of the seedlings.
Wind-dispersed seeds are expected to arrive to every
location within the stand, even travelling over long
distances. Contrarily, heavy seeds tend to be clustered
beneath the crown of mother trees, resulting in a
clumper distribution with gaps in those locations where
seeds cannot arrive.
P. nigra, P. sylvestris, P. pinaster and P. halepensis are
species mainly dispersed by wind, a fact that facilitates
its wide distribution, even in low dense stands. P. nigra
disperses seeds from January through May, with a
maximum in March, and seed rain tends to be uniformly
distributed throughout soil, especially on dense stands
(Tiscar, 2007). Literature in P. sylvestris shows that
fifty percent of the seeds remain under the crown, while
other 40% of the seeds are found at distances as long as
2 to 4 times the tree height (Burschel & Huss, 1997).
This means that between 30 and 75% of the seeds are
found not more than 18 m from the tree (Montero et
al., 2008a). In our specific study area only 20% of
the seeds were released under the crown, while in a
distance of three crown radii the number of dispersed
seeds is similar to that beneath the crown (Calama et al.,
2015b), resulting in a close to uniform distribution of
the seed rain on the soil surface. For P. pinaster median
dispersal distances in the territory varied between 14.1
to 24.5 m, with maximum distances over 54 m (Juez et
al., 2014). Dispersal events are concentrated in only one
period, from June to August, with maximum dispersal
events associated with violent summer storms. Finally,
in P. halepensis spatiotemporal variation of seed rain
reveals dispersal curves with ca. 95% seeds dropping
less than 20 m away from the mother tree, maximum
seed dispersal up to distances of 100-120 m, and
occasional long distance dispersal events spreading 0.2
% of the seeds up to distances over 1 km (Nathan &
Forest Systems
Ne’eman, 2000). Based on the information above, no
limitations associated with seed dispersal are expected
in these species.
Concerning seed dispersal, P. pinea is mainly referred
to as a gravity-dispersed species, due to the morphology
of the large and wingless seeds produced. Manso et
al. (2012) found a strongly aggregate spatial primary
dispersal pattern in a P. pinea stand in the Northern of
Spain, only 1% of the seeds being expected to drop
beyond 2 crown radii. Similar results are due to Masetti
& Mencussini (1991) in their study in Toscana (Italy).
This aggregated pattern of seed dispersal will result
in a clustered distribution of seedlings and samplings
under the influence area of the crown of mature trees,
conforming overdense small patches that will require
further liberation to enhance development (Barbeito et
al., 2008). From a temporal perspective, seed release is
climate-controlled, at least in central Spain locations:
cones break open when mean monthly temperature
reaches a thermal threshold (usually in May), whereas
the subsequent release rate is positively related to
precipitation, taking place from summer until early
fall (Manso et al., 2012), showing a similar temporal
pattern than its conspecific P. pinaster.
Accordingly, low-distance dispersal by gravity
prevent seed arrival into large gaps (radius > 10 m),
thus avoiding natural regeneration in these areas (Fig.
3). Additionally, though dispersal of P. pinea seeds has
been often assumed to be secondarily animal-mediated,
a belief probably linked to the highly nutritional content
of the nuts, this fact has never been clearly confirmed.
In fact, Manso et al. (2014b) did not find any obvious
Figure 3. Seed dispersal limitation index (defined as the rate of
places where no seeds arrive, assuming that there are no limitations in seed source) for Pinus pinea in Northern Plateau as a
function of stand density. Original figure based on Manso et al.
(2012)
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Natural regeneration in Iberian pines: A review
Figure 4. Seasonal variation of seed predation in P. nigra by predator group in typical
Cuenca mountains forest areas in a masting year. Original figure based on Lucas-Borja
et al. (2010)
trace of secondary dispersal by rodents within the
regeneration blocks. The authors detected a minority
seed removing by corvids, though. Although the fate of
these seeds could not be tracked, this can be behind the
occurrence of isolated seedlings growing in the closer
vicinity of managed forests, far beyond the dispersal
distance expected from primary dispersal models.
Pre and post-dispersal seed predation
Pre-dispersal predation by birds (e.g. cornbills),
jays, mammals (e.g. squirrels), or insect pests attacking
cones and seeds in the early stages of maturation can
be responsible for severe seed losses. However, postdispersal seed predation has been reported as a main
limiting factor in many pine species, as the seeds
reaching the soil can be consumed in the ground in
the different seasons of the dissemination period. A
large variety of potential consumers (from insects to
mammals and birds) have been identified, thus resulting
in spatio-temporal heterogeneity in predation due to
factors as abundance of seeds or abundance of predators.
Seed predators can severely reduce the total amount of
seeds available to create a seed bank, but also change
the spatial distribution of seeds after the initial seed rain
(Castro et al., 1999).
For P. nigra in Cuenca mountains three main group
of predators were observed (Lucas-Borja et al., 2010):
ants, birds (Fringilla coelebs L., Parus caeruleus L.,
Parus major L.) and rodents (Apodemus sylvaticus L.,
Mus musculus L.). Predators present different seed
removal rates depending on the season of the year,
with special incidence on winter and lower rates on
Forest Systems
spring, coinciding with the uprising of temperatures
and subsequent lesser activity of rodents (Fig. 4).
Seed predation was related with seed rain patterns
(Lucas-Borja et al., 2016) being lower in the high
seed rain year (11.2±3.7% of removed seeds) than
in the low seed rain years (84.3±6.6% of removed
seeds), a finding in agreement with the predation
satiation hypothesis (Janzen, 1976). For the species,
a good year of recruitment has to be preceded by
a good seed production year, in which case postdispersal seed predation is not as important as in low
seed fall years. In high seed production years, birds
were the most important predators and rodents were
the less important predator group in both typical and
relict forest areas for this species. Due to the high
seed removal percentage by all predator groups, no
conclusion can be obtained in low seed production
years (Lucas-Borja et al., 2010).
Though no specific studies on seed predation
on P. sylvestris in Central Spain have been carried
out, this topic has been widely studied in other
locations of the species. For instance, the great
spotted woodpeckers Dendrocopos major L. is one
of the main predators of seeds in closed cones of
P. sylvestris in central and eastern Europe (Myczko
& Benkman, 2011), while the crossbill (Loxia
curvirostra L.) feeds on ripening seeds in southern
Spain (Castro et al., 1999). Predation pressure
shows an interannual variability that may be related
to temporal variation in cone production (Matias
et al., 2009). Although pre- and post-dispersal
predation can reduce the seed pool of P. sylvestris
to almost 50% (Worthy et al., 2006) or even over
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90% in relict P. sylvestris forests in southern Spain
(Castro et al., 1999), it is unlikely to be a serious
problem for the regeneration of the species in Sierra
de Guadarrama, except in the lower limit, where
seed production is much more scarce.
In the case of P. pinea, it is important to consider
the effect of both pre- and post-dispersal predation.
Pre-dispersal seed predation has only been described
as a serious threat for seed production very recently.
Classical native pests, as Pissodes validirostris Gyll.
or Dioryctria mendacella Staud. have been reported
to produce damage to a limited extent, damaging
about 20% of cones (Calama et al., 2017). Moreover,
in recent years, a North-American invasive seedfeeding bug, Leptoglossus occidentalis Heid.,
has been postulated as the main cause for the dry
cone syndrome, resulting in recent decay in cone
production as well as the rate of filled seeds (Mutke
et al., 2015). In this sense, the rate of damaged seeds
in the Northern Plateau has increased up to 50%
in the recent years, resulting in both economic and
ecological losses. Additionally, it is worthwhile to
notice that this bug species is a conifer-specific pest,
thus the potential damage over other Iberian pines
should not be neglected and the monitoring of its
activity and its effect on seed availability it is highly
recommended.
The size and nutritional value of P. pinea seeds may
not go unnoticed by post-dispersal seed predators.
Manso et al. (2014b) observed that the wood mouse (A.
sylvaticus) was the main predator of seeds of P. pinea
in the Spanish Northern Plateau, being responsible for
more than 80% of seed removal. Secondary agents
for predation were identified as azure-winged mapie
(Cyanopica cyanus Pall.) and common raven (Corvus
corax L.). A. sylvaticus acts exploiting almost all
available seeds during drought-free periods, being
able to consume almost 100% of available seeds
during winter. The favourable summer period for seed
survival is a consequence of both the decreasing rodent
populations due to the effect of drought and the higher
seed availability in summer, when dispersal takes place.
This fact suggests the existence of a dual climate preypredator control, driven by summer conditions and the
climate-mediated masting habit of the species. From a
spatial perspective, predation is slightly higher in the
close vicinity of trees and potential rodent shelters
(Manso et al., 2014b).
A similar process has been identified in the
conspecific P. pinaster in the Northern Plateau.
Ruano et al. (2014) showed that predation can reduce
seed density up to values below 1 seed/m2, even in
locations where seed rain reached values over 4050 seeds/m2. Although no specific experiment for
Forest Systems
detecting potential predators’ species was carried out,
the authors indicate that together with A. sylvaticus,
C. ciyanus and C. corax, ants should be considered
a potential predator for the seed of P. pinaster. The
authors found a positive correlation among density
of seeds escaping from predation at the end of the
year and total seed rain, thus higher predation rates
occur when the amount of available seed is lower.
Additionally, climate variability influences predator
populations, showing larger rates in autumn-winter
and almost no predation in summer. As for P. pinea,
predation is favoured in the vicinity of stumps and
in denser areas (potential sheltered locations), while
the presence of grasses and needles on the floor hide
seeds and therefore prevents predation (Ruano et al.,
2014).
In P. halepensis, notwithstanding an initial abundance
of seeds, their availability may be reduced by intense
seed predation, especially when no other seed sources
are available (e.g. after a fire event), when seed losses can
reach up to 90%. Rodents have been observed to be the
main predators of P. halepensis seeds, while predation
by ants or birds is considerably lower (Broncano et al.,
2008). Concerning the spatiotemporal patterns of seed
predation, Broncano et al. (2008) showed that predation
by rodents is very high in all situations and seasons.
Germination, emergence and early survival
Seed germination, seedling emergence and early
survival success will define the spatial pattern of
seedling location, and further spatial pattern of adult
plants, redefining the spatial pattern associated with
seed shadow. In this sense, different requirements can
be identified for each process, thus, conditions and
traits beneficial for one developmental process could be
disadvantageous for another.
Stand density, soil preparation, dispersal season and
site conditions had a significant influence on P. nigra
seed germination and initial seedling survival, though
showing conflicting situations for both processes
(Lucas-Borja et al., 2011). The effect of the overstory
can be summarized as positive for seed germination,
with rates reaching values up to 40-60% in denser
stands and below 30% in open stands (Lucas-Borja
et al., 2011). This effect is more evident on drier
and warmer years, where germination and seedling
emergence is also favoured by shrub protection, factor
with no effect on cooler and wetter years. Germination
is also favoured in mid-altitude locations, while largely
restricted in the upper limit area. Site preparation had
a significant influence on seed germination, which was
favoured by scalping, but no effect on seedling survival
at long term (Lucas-Borja et al., 2011).
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Higher light availability (low basal area) promotes
seedling survival, thus a seed germination-seedling
survival conflict can be observed. This conflict is more
patent on wetter years, since the probability of summer
seedling survival in drier and warmer years is very low,
irrespective of crown coverture (Lucas-Borja et al.,
2011). All the results point out that, for P. nigra, annual
climate is the major factor controlling seed germination
and seedling survival, with a secondary control due to
light availability.
Light is a determinant factor for the germination of
P. sylvestris in Central Spain. The optimal radiation
for germination suggested for P. sylvestris is 35% of
full sunlight, thus germination is favoured under the
mid to high shadow conditions that are found when
the group shelterwood system is applied and with
selective cuttings, while is minimized under the large
gaps created after a clearcutting (Calama et al., 2015b).
Apart from the direct limiting effect of radiation on seed
germination, high rates of light are often associated with
the presence of a dense herbal layer which prevents seed
germination and seedling emergence. Under moderate
light levels the presence of this herb layer had a weak
effect on seedling emergence, suggesting that seedlings
and herbs can occupy the same sites (Pardos et al.,
2007). On the contrary, an increase in the light levels
led to a decrease in regeneration performance because
of an increased competition for resources (Módry
et al., 2004). Although P. sylvestris can germinate
in many different types of seedbed (Cañellas et al.,
2004), the litterfall accumulated increases the depth of
Figure 5. Percentage of summer seedling survival in Pinus
pinaster as a function of mean temperature of July and rate of
harvested basal area. Remaining basal area 8.8 m2/ha. Original
figure based on Ruano et al. (2009)
Forest Systems
organic matter and thus improves microsite conditions
for germination (Pardos et al., 2008), except if layer
thickness reach values over 10 cm. This result contrasts
with previous findings for the species in Central Europe
(Hille & den Ouden, 2004), or even in Northern Spain,
where soil scarification is recommended, and reflects
the particular ecological conditions for the species in
the mountains of Southern Europe.
The results from a 3-year (2009 to 2011) study in
Valsaín forest also suggested a climate control that
limits germination at least in the timberline (Calama et
al., 2015b), partly related to the occurrence of spring
frost events and low water availability during summer
(Barbeito et al., 2009). In any case, under the current
climate conditions, germination rates in P. sylvestris are
high, with a great variability between years and sites.
For instance, germination rates recorded in the studied
area were over 70%, the larger rates obtained during
spring and autumn at 1600 m. On the contrary, lower
rates of germination were observed at timberline areas
(Calama et al., 2015b).
Despite high rates of seed germination and seedling
emergence, the regeneration occurs as a temporary pulse
of seedlings, due to seedling mortality that could be close
to 100% after a hot and drought summer (Calama et al.,
2015a). Water availability during the summer seems to be
the key factor driving P. sylvestris regeneration at Sierra
de Guadarrama, similarly to what has been recorded
at its southernmost distribution limit (Matias & Jump,
2014). With respect to light requirements, although in
the Eurosiberian forests P. sylvestris behaves as a light
demanding species, results from different studies in
central Spain, suggest the preference of the species to
moderate light conditions, at least during the early stages
of growth (Pardos et al., 2008; Calama et al., 2015a).
Seedling survival is also threatened after extemporal
cold springs and in highly shaded environments (Calama
et al., 2015b). Mortality in P. sylvestris steadily increases
during the first two years after emergence, but a notable
stabilization in seedling survival is found after three
years (Pardos et al., 2007).
Seed germination in P. pinea is governed by thermal
variables in combination with different degrees of soil
and air humidity. In the field, Manso et al. (2013a,b)
were able to empirically link seed germination of
P. pinea seeds to climatic and stand variables in the
Northern Plateau of Spain. Optimal conditions occur
over few weeks either in autumn (linked with warm
conditions) just after seed dispersal, or in the following
spring (linked with humid conditions). Large interannual
variability in germination rates, conditioned to the
occurrence of this optimal conditions, is observed. Over
a 4 years study, germination rates varied between 9%
and 90%, with two years showing autumn germination
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Figure 6. Mean ± SE relative growth rate (RGR) of Pinus halepensis seedlings in response to light availability (PAR: photosynthetic active radiation). As a shade-intolerant and pioneer
species P. halepensis seedlings exhibit a fast growth response
to an increase in radiation. Conversely, for this species shading
is the main factor constraining seedling recruitment. Based on
Espelta (1996).
events, one year with spring germination events, and
one year with almost no germination at all (Manso et
al., 2013a). Moreover, extremely poor overstory cover
leads to low probabilities of germination. Implications
for natural regeneration in P. pinea are relevant as the
process becomes seriously limited in the absence of
this climatic optimal conditions. Occurrence of cold
fall season prevents germination, thus the remaining
seeds are highly vulnerable to the action of predators
during winter, the season where rodents are more
active. Additionally, if a cold winter is followed by a
dry spring, germination does not occur (e.g. 2008-2009
campaign, germination rate < 9%).
Studies carried out in the Northern Plateau show
that seedling mortality of P. pinea occurs as a result
of a combination of low water potential and negative
assimilation rates (Calama et al., 2015c). These
circumstances usually take place during the summer
season, with older seedlings being able to better thrive
due to carbon reserves stored in previous favourable
seasons. This picture matches up with the empirical
evidence found in the same area, where the vast majority
of emerged seedlings perished in the first two years
after emergence, except if optimal summer conditions
occurs. Interestingly, winter frost does not significantly
affect seedling survival (Pardos et al., 2014). From a
spatial perspective, optimisation of the carbon balance
and survival is attained when seedlings are placed in
mid-shaded locations, which are those locations more
Forest Systems
favourable for germination. This is in full accordance
with the findings of Awada et al. (2003), which reveal
that P. pinea seedlings can actually tolerate some
degree of shading in the initial stages of development.
The same observations show that individuals emerging
in autumn and closer to adult trees are more likely to
survive than seedlings from spring cohorts and isolate
individuals (Manso et al., 2014a).
Seed germination for P. pinaster in the Northern
Plateau seems not to be a limiting factor, with this
provenance showing larger germination rates in
response to drought than Atlantic provenances (Núñez
et al., 2013), and positive response to thermal shocks
(Herrero et al., 2004). Concerning germination rates on
field conditions, Ruano et al. (2009) observed, over an
18 months experiment, a significant effect of remaining
basal area on germination rates. Higher germination
rates (around 60%) were found at remaining basal area
of 6.6 m2/ha (25% of reduction) on harvest operations.
Surprisingly, values of germination rate about 40% were
obtained both in non-harvested as well as on clearcut
areas. Germination occurs in either fall or spring season,
seasonality that could explain the observed little effect
of summer rainfall on germination rate.
Seedling establishment and survival processes in
P. pinaster are closely related to seed germination,
thus more favorable sites for germination are those
more favorable for survival. However, initial seedling
survival is largely threatened by water stress during
the summer (Fig. 5), as well as interactions with other
factors. In particular, mid-shaded conditions, the
presence of shrubs acting as nurse plants (RodríguezGarcía et al., 2011) and needle soil cover (del Peso et
al., 2012) facilitate P. pinaster germination, emergence
and initial survival.
Unless severe predation or topographic constraints
limit seed availability, germination of P. halepensis
seeds and early survival is often successful and occurs
at high rates (80%) under contrasting environmental
conditions: i.e. from closed (10% full sunlight) to
open (80% full sunlight) canopy cover. In this sense,
while shading favours earlier germination (Broncano
et al., 1998), previous studies in Southern France have
reported complete lack of regeneration in very dense
stands (Prévosto et al., 2012). Germination is favoured in
exposed mineral seedbeds while thick layers of organic
matter may limit this process (Broncano et al., 2008).
As a light-demanding and drought-tolerant species, once
established, seedlings are able to tolerate high levels of
radiation exposure (Fig. 6) and moderate water stress
(Eugenio et al., 2006). Indeed, these are environmental
conditions particularly occurring after intense standreplacing wildfires and therefore, in this situation,
regeneration is often successful (de las Heras et al., 2012),
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Natural regeneration in Iberian pines: A review
Figure 7. Influence of the different subprocesses on the success of natural regeneration for each
pine species.
with densities of young seedlings varying from 0.1 up to
10 seedlings/m2 (Rodrigo et al., 2004). The fact that P.
halepensis shows similar environmental conditions for
both germination and initial seedling establishment, as
well as a wide plastic response, confirm the lack of a
seed-seedling conflict in this species (Broncano et al.,
1998). Thus, the lack of natural recruitment in some
cases could be associated with the absence of effective
dispersal. Interestingly, in contrast with the myriad of
studies in Spain that have analysed the regeneration
of P. halepensis forests after stand-replacing wildfires
and that claimed for the high resilience of this species
to these disturbance, the regeneration in the absence
of fire has been seldom explored (Beltrán et al., 2011),
and this is a main constrain to predict the dynamics of
undisturbed forests (but see Zavala et al., 2000, 2011)
and their response to global challenges.
Main bottlenecks and threats for natural regeneration in Iberian pines
Findings from the previous section allow us to
identify the main bottlenecks for natural regeneration in
Iberian pines (Fig. 7), and give insight into the potential
threats for the future.
Seed production can be a key limiting factor in nonmast years for masting species such as P. nigra and
P. pinea, especially in the ecological limits of their
distribution. For the rest of species, even though some
interannual variability in cone and seed production
is observed, seed availability seems sufficient except
under very limiting environments (e.g. at lower
altitudinal limits for P. sylvestris, or in very dry years).
Forest Systems
Little is known about the process of non-fire-associated
ripening of serotine and non-serotine cones in P.
halepensis, though the total amount of seeds produced
and dispersed even in non-fire events seems sufficient.
Given the climate control over masting on pine species,
limitation due to seed availability could be a limiting
factor for regeneration of pines under future climate
scenarios.
Concerning seed dispersal, the only species severely
affected by ineffective dispersal seems to be P. pinea,
which is the unique species showing a main gravity
dispersal process. Low current densities of mature P.
pinea stands-associated with a common silvicultural
practice applied in the territory during the 20th century
to promote cone production-resulted in large gaps that
cannot be occupied by the seeds. The postulated animal
mediated seed dispersal in the species seems not to be
sufficient to fill these gaps, thus resulting in a patched
and clumped distribution of seeds under the crowns of
adult trees.
Seed predation is a key limiting factor for the main
part of the species, especially on low seed years. In this
sense, masting can be considered a regeneration strategy
to deal with this, by satiating predator populations
on mast years and starving them on non-mast years,
according to the postulated predator-satiation theory
(Salisbury, 1942; Janzen, 1976). At within-year
temporal levels, we detect a delay among the season
of seed fall and the maximum activity of predators
(mainly rodents), which would allow seeds to escape
predation if favourable conditions for germination are
attained. On the contrary, complete losses of seed crop
can be found on unfavourable years for many of the
studied species.
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Seed germination and seedling emergence is
mediated by both environmental control and soil
conditions where seed arrives. Seed germination is
mainly regulated by temperature, water availability
and light. Freezing temperatures can limit autumn
germination in P. pinea, as well as germination of P.
sylvestris and P. nigra on their altitudinal limits. Dry
years can result in lack of spring germination for all the
species. With respect to light, germination is generally
favoured under mid-shaded environments, except
in P. halepensis, whose germinative ability remains
high under a wide range of cover conditions. Finally,
for the small seeded species, as P. nigra, P. sylvestris
and P. halepensis, the presence of a dense herbal
layer limiting the access of seeds to mineral soil can
prevent seed germination and seedling emergence. In
this sense, light exerts a multiple control, since in very
open stands the presence of herbs and competitors is
enhanced, while soil water content is minimized. On
the opposite, in very dense stands the presence of a very
thick litter layer together with low light availability
could be detrimental to emergence and survival (Sayer,
2006).
Shortage in water during the first summer seasons
together with excessive light irradiance seems to
be the key factors impairing seedling survival in
all the studied pine species, except, once more, in
P. halepensis, which shows large rates of survival
even at high exposures. The rest of species require
initial shading for seedling survival, and initial
survival is more likely in the close vicinity of parent
trees, or even under the presence of shrubs acting
as nurse plants. Nevertheless, as seedlings grow,
different degrees of tolerance are identified among
species. In this sense, and according to their low
shade tolerance, P. halepensis seedlings require
earlier liberation (Scarascia-Mugnozza & Schirone,
1984), followed by P. pinea and P. pinaster (Ruano
et al., 2009; Manso et al., 2014a). On the opposite
side, P. sylvestris and P. nigra are the species whose
seedlings can survive longer periods under the shade
of parent trees (Calama et al., 2015b; Lucas-Borja
et al., 2016).
The main bottlenecks identified for all the species
in the studied areas are climate-mediated. This
means that it is very likely to have unfavorable
conditions for one or several of these processes
in a given year, thus favorable conditions for the
regeneration of the species occur within a lapse of
years. Under changing climate scenarios we should
expect, in general, more unfavorable conditions
for seed production, seed germination and seedling
initial survival. On the other hand, processes as
autumn-winter germination can be favored by
Forest Systems
increasing temperatures, which could also affect
the population dynamics of predators as rodents.
In any case, natural regeneration of the species in
the studied areas would surely continue to exhibit
an intermittent temporal pattern, which should be
aggravated under drier scenarios.
Managing natural regeneration in Iberian pines
Based on the previous findings, new proposal
for managing forests in order to attain the natural
regeneration have been proposed for the species in the
studied areas.
In the case of P. nigra it has been proposed (Lucas–
Borja et al., 2016) an extension of both the rotation
and the regeneration periods up to 150 and 30 years,
respectively, in order to ensure the occurrence of
favorable conditions permitting successful natural
regeneration. In addition, less intense and more gradual
and continuous regeneration fellings should be applied.
These fellings should be programmed following a mast
year, and applied in combination with soil treatments
(i.e. scalping) oriented to prevent soil compaction and
to favour soil humus. Shrubs cover might have an
important role regarding natural regeneration. In drier
years, shrub cover should be promoted since seedling
emergence has been enhanced under moderate light
(about 25 m2/ha) and shrubs protection. However,
in wetter years, forest managers should promote P.
nigra regeneration by clearing shrubs after seedling
emergence to increase light availability and to avoid
shrub competition. Overall, the natural regeneration of
P. nigra has to go through conflicting situations between
conditions suitable for seedling emergence (medium
basal area interval, shrub cover) and conditions suitable
for seedling survival (outside shrub cover without basal
area influence), these effects being modulated by the
climate of a given year, seed predation and site quality.
These issues make many of these recommendations
difficult to be implemented in the field.
Similar, but even more flexible schedules are
proposed for P. sylvestris in the Central Range
(Cabrera & Donés, 2010). Uniform shelterwood
system is being now replaced by a more gradual group
regeneration system, where the shelterwood fellings
are gradually applied on small patches and trees are
harvested through several fellings. In this way, natural
regeneration establishes progressively under the older
trees canopy during a 40 years regeneration period
and a 140 years rotation length, with some seed trees
still remaining after the last cutting. For example, in
Valsaín forest, the aim is to gradually substitute the
August 2017 • Volume 26 • Issue 2 • eR02S
15
Natural regeneration in Iberian pines: A review
old stand by a thicket stand with 250 trees per ha. This
initial density will decrease by natural mortality and
harvesting operations. Under these proposed practices,
P. sylvestris stands would naturally turn to semiregular
or multi-aged structures, making the stand more
vulnerable to fire. It is important to note the adaption
of the silviculture to the peculiarities of the different
stands, with important restrictions to the harvesting
operations in those stands that hold protected species
as the European black vulture (Aegypius monachus L.).
The main innovative proposal in managing natural
regeneration in P. pinea (Gordo et al., 2012b) is that in
order to ensure seed arrival into gaps, thinning schedules
should target to densities about 125-150 stems/ha at the
beginning of regeneration fellings. This means that less
intensive and more gradual thinnings should be applied
during the whole cycle. Early thinning operations are also
recommended in order to favor initial lateral expansion
of the crowns, facilitating seed arrival into the gaps. A
second concern is related to the need of initial shading
conditions to favor seed germination and seedling
survival, especially under more severe climate scenarios.
Intense uniform shelterwood system should be replaced
by more gradual fellings. An initial single preparatoryseeding felling, reducing stand density up to 80-100
stems/ha, is recommended. With this cutting we aim to
remove dominated, co-dominant and dominant trees in a
bad state, with inadequate stem form, malformed crown
and low cone production. The remaining trees will act as
seed trees, also providing initial shelter for the recently
emerged seedlings. Simultaneously, it may be necessary
to eliminate the understory vegetation and nonviable
advanced regeneration. Once a sufficient number of
viable seedlings had been already established beneath
the crown cover of the seed trees (after 5-10 years), a
secondary felling should be applied, aiming to release
the most promising regeneration patches. Subsequent
removal cuttings should aim to gradually uncover the
new cohort of regenerated trees. These removal cuttings
should elapse a maximum of 5 years, to prevent the
negative effect due to competition or damage from
harvested mature trees on the young saplings. At the end
of the period, 5-10 extra mature trees per ha are to be
retained.
The regulation of light through operational forestry
practices influences significantly the germination,
survival and growth of the P. pinaster. Shelterwood
method applied by light interventions (reduction of
basal area between 25 and 50 % at maximum) favors
the seed germination generating seedlings protected
by residual trees. In this way, seedlings will grow
to generate stands compatible with the provision of
ecosystem services (resin and wood), while obtaining
other environmental services. A reduction of 50% of the
Forest Systems
basal area should be applied when economic conditions
restrict operations, thus larger amount of wood must
be removed to make feasible the intervention. As for
other Mediterranean pines, the role of tree canopy
protection will be more important as the climatic
conditions become more stressful (especially extreme
dry and hot summers). When an adequate amount of
viable seedlings is obtained (after regeneration felling
or taking advantaging of advance regeneration) a final
felling should be applied to avoid damages to new crop
trees. In some special cases, a reduced number of trees
from the previous cohort can remain in the stand to
enhance biodiversity values.
The management proposals for natural regeneration
of P. halepensis on absence of fire should aim to mimic
small perturbations (Prévosto et al., 2012). Beltrán
et al. (2011) propose even-aged structures following
shelterwood regeneration system with 80-150 years
rotation. The authors suggest the application of
shelterwood method in two phases: seeding cutting and
final cutting. Moreover, they propose optionally the
regeneration by clearcutting with reserves, retaining
uniformly spaced ca. 50 trees/ha after the clearcut.
In addition, they point out the importance of some
treatments to help regeneration: clearing, with the
partial or total removal of the understory vegetation
(Serrada, 2003) and slash management to facilitate
the germination of the seeds and establishment of the
saplings. Soil preparation techniques as scarification
and even prescribed burning are also recommended to
favor the contact of the seeds with the mineral soil and
to promote regeneration of P. halepensis stands after
cutting (Prévosto & Ripert, 2008).
Conclusions
Many different bottlenecks have been identified to
limit natural regeneration of the Iberian pine species,
except for P. halepensis. The main part of the limiting
subprocesses are climate-mediated, thus joint occurrence
of favourable conditions for natural regeneration occurs
on intermittent events. Under changing climate scenarios
we expect an increase of the time lapse between
two successful regeneration events. Consequently,
new silvicultural schemes aimed to promote natural
regeneration should rely on taking profit of all the
successful regeneration events, favouring advanced
regeneration, ensuring mid-shaded optimal conditions
for seed germination and seedling survival, preventing
the creation of big gaps, and programing fellings in
those mast years where abundance of seeds allow
predator satiation. Intensive clearcutting and uniform
shelterwood systems are mainly substituted by more
August 2017 • Volume 26 • Issue 2 • eR02S
16
Rafael Calama, Rubén Manso, Manuel E. Lucas-Borja, Josep M. Espelta, Miriam Piqué, Felipe Bravo, et al.
flexible schedules, including group shelterwood systems.
This would result in stand age structures closer to that of
semiregular forest, which mimics the natural dynamics of
regeneration of the species, but could be more vulnerable
to forest fires, a main risk in Mediterranean forests.
Acknowledgements
Author wish to thank all the persons and institutions
involved in the installation, maintenance and monitoring
of the different trials, mainly: G. Madrigal, M. Conde,
E. Garriga, F. J. Gordo, Ayto. El Portillo and Servicio
Territorial de Medio Ambiente de Valladolid (P. pinea);
A. Bachiller, I. Cañellas, J. Donés and Centro de
Montes de Valsaín (P. sylvestris); J.A. García Abarca
and J. L. Serrano Cuenca (P. nigra); Oficina Técnica
de Prevención Municipal de Incendios Forestales de la
Diputación de Barcelona-OTPMIF (P. halepensis); I.
Ruano, E. Rodríguez-García, C. Ordóñez, and Servicio
Territorial de Medio Ambiente de Segovia (P. pinaster).
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