Oikos 126: 497–507, 2017

doi: 10.1111/oik.03967
© 2016 The Authors. Oikos © 2016 Nordic Society Oikos
Subject Editor: Dries Bonte. Editor-in-Chief: Dustin Marshall. Accepted 21 November 2016

Plant life history and above–belowground interactions: missing links

Gerlinde B. De Deyn­
G. B. De Deyn (http://orcid.org/0000-0003-4823-6912) (gerlinde.dedeyn@wur.nl), Dept of Soil Quality, Wageningen Univ., PO Box 47,
NL-6700AA Wageningen, the Netherlands.­

The importance of above–belowground interactions for plant growth and community dynamics became clear in the last
decades, whereas the numerous studies on plant life history improved our knowledge on eco-evolutionary dynamics. How-
ever, surprisingly few studies have linked both research fields despite their potential to increase our mechanistic understand-
ing of how above–belowground interactions are governed. Here I briefly review studies on above–belowground interactions
and plant life history and identify important research gaps. To advance our understanding of ecological strategies and
eco-evolutionary dynamics of plants and their associated organisms it is warranted to elucidate the interconnectivity and
tradeoffs of plant life history traits of growth, defence, reproduction, nutrient cycling and the functional composition of
above- and belowground heterotrophic communities. Using the concept of tradeoffs in growth, reproduction and defence
we can postulate that plants in rich soil grow, reproduce and die fast whilst avoiding above- and belowground antagonists,
whereas plants in poor soil grow slow, live and reproduce longer and invest in above- and belowground mutualists and
defences. However, alternative scenarios are possible and depend on the selection pressure by above- and belowground
mutualists and antagonists during plant ontogeny and via after-life effects. To elucidate missing links between life history
traits and above–belowground interactions, complementary modelling and empirical studies are needed that reveal the cou-
pling between below- and aboveground plant traits of growth, defence and reproduction, their heritability and their cost/
benefit relation. These cost/benefit analyses of defence should span from individuals to future generations, taking feedback
effects via altered biotic communities and resource competition into account. The role of soil fertility in steering plant
life history traits requires explicit testing of trans-generational trait shifts in growth, defence, reproduction, cost/benefit
of associations with mutualists and antagonists and soil feedbacks across plant genotypes/species with distinct life history
traits, grown across soil fertility gradients.

Over the last two decades the coupling between aboveground what is known and unknown. To facilitate integration of
and belowground systems gained considerable interest in above–belowground interactions and plant life history I put
terrestrial ecology. Research on plant life histories has a lon- forward a conceptual model based on current knowledge
ger tradition, and has provided insights in the geographical (Fig. 2), that can be used for in vivo and in silico experi-
distribution of plants with different life histories. Surpris- ments to reveal eco-evolutionary trajectories by plants and
ingly only very few studies have linked above–belowground their associated aboveground and belowground antagonists
interactions and plant life history despite the potential of and mutualists.
the integration of both fields to increase our understand-
ing of eco-evolutionary dynamics. Based on a literature Above–belowground interactions
search in ISI Web of Science using the topic key-words
‘aboveground and belowground interactions’ or ‘above and The vast majority of terrestrial plants are composed of above-
belowground interactions’ mid-June 2016 I retrieved 784 ground and belowground parts which function in highly
articles, whereas the key-words ‘plant life history’ or ‘plant complementing ways. The aboveground plant parts pri-
life histories’ yielded 19 581 articles (Fig. 1). Only 22 articles mary function to acquire solar energy and carbon from the
appeared in both topical groups of articles, indicating that atmosphere, whereas the belowground parts are essential to
both fields have hardly taken note of each other. This low acquire mineral nutrients and water from soil (Fig. 2). As a
representation of articles with both sets of key-words used result plants acquire energy and building blocks that are used
in the title, abstract or key-words provided by the authors, for maintenance and growth, reproduction and defence. Due
may be the use of different jargon in both research fields and to the complementing role of above- and belowground plant
the different time scales they have typically considered. Here parts, plants balance shoot and root biomass in a functional
I briefly review studies on above–belowground interactions equilibrium in response to limitations of energy and nutri-
and their coupling with plant life history strategies to reveal ents (Shipley and Meziane 2002, Weemstra et al. 2016).

497
 Aboveground and Plant life history
belowground interactions
784 22 19 581
Above and belowground
interactions Plant life histories

Figure 1. Number of publications in Web of Science (18 June 2016) with topic ‘plant life history’ or ‘plant life histories’, ‘above and
belowground interactions’ or ‘aboveground and belowground interactions’ and the number of publications that both topic groups (based
on the key-word search) have in common.

In ecosystems plants interact with aboveground and da and db). It was also soon recognized that single plants
belowground heterotrophic organisms that acquire their interact with a wide array of aboveground and belowground
nutrients and energy from plants. These organisms acquire antagonists and mutualists during their ontogeny (De Deyn
energy from plants, however in the case of mutualistic asso- and van der Putten 2005). Plant mutualists that directly
ciations like root symbiotic mycorrhizal fungi and N2-fixing interact with plants comprise: mycorrhizal fungi, symbiotic
bacteria plants can benefit from increased uptake of resources N2-fixing bacteria, plant growth-promoting rhizobacteria
belowground (Fig. 2: 1a). The impacts of aboveground and (PGPR), beneficial aboveground endophytes and pollina-
belowground herbivores and pathogens on plant growth tors. Plant antagonists directly interacting with plants are
have long been recognized by ecologists and agronomists. aboveground and belowground herbivores and pathogens. It
However, they were typically investigated separately and has to be noted that plant mutualists require plant resources
studies on the coupling between aboveground and below- too, so that their benefit/cost from a plant fitness perspec-
ground herbivores through plants only started to appear tive depends on environmental conditions of soil nutrient
about thirty years ago (Gange and Brown 1989, Evans 1991, and energy availability, and herbivore and pathogen pressure
Masters and Brown 1992). Since then the number of articles (Vitousek and Howarth 1991, Johnson et al. 1997) (Fig. 2:
on above- and belowground interactions increased markedly, 1a and 1b impact on r relative to m).
especially during the last decade. The first conceptual model Advances in plant physiology studies revealed how above-
to predict above–belowground interaction was presented by ground and belowground organisms interact on individual
Masters et al. (1993) in Oikos. They proposed that root feed- plants through plant physiology and hormonal pathways
ing herbivores stimulate leaf feeding herbivores through a that regulate plant defences (Kaplan et al. 2008, Vos et al.
plant (drought) stress response that increases nutrient flows 2013). The main plant defence pathways are the jasmonic
to leaves (Fig. 2: 2a), whereas shoot herbivores were thought acid (JA) and salicylic acid (SA) pathways, each being
to suppress root feeders by reducing plant carbon allocation induced by and acting against different types of organisms
to roots (Fig. 2: 2b). above- and belowground. Necrotrophic (extracting nutri-
Over the years the simple model of Masters et al. (1993) ents from dead cells) pathogens and chewing insects trig-
was revised by pointing out the need to include non-trophic ger the JA defence pathway, whereas biotrophic (extracting
belowground interactions (Brussaard 1998, Wardle et  al. nutrients from living cells) pathogens and sucking insects
2004), multi-trophic above- and belowground interactions trigger the SA defence pathway (Glazebrook 2005, Howe
(van der Putten et al. 2001, van Dam and Heil 2011), tim- and Jander 2008). These defence pathways enable plants to
ing of above- and belowground herbivory (Blossey and adapt their defence response to the type of antagonist. How-
Hunt-Joshi 2003), and the array of different plant defence ever, both pathways trade off, resulting in increased defence
strategies (Bezemer et  al. 2003, Bezemer and van Dam against specific types of antagonists but increased suscepti-
2005). These defences are generally thought to incur plant bility against others. Root symbiotic mutualists also interact
metabolic costs, associated with the production of aboveg- with the defence pathways that act against plant antagonists
round and belowground plant defence compounds (Fig. 2: (Fig. 2: 1b). As mycorrhizal fungi obtain carbon from plants

498
 D
8 i
Mutualists
s
4 p
sz Seed size
Energy, e
Antagonists r Reproduction sn r
carbon
2c ga
Seed number s
2a 2b Growth a
l
da Defence Da
Biomass ph
Plant 3a 3b
1a JA -- SA ys Death
Above-
growth ic below-
Biomass db Defence al ground
Seed(ling)
survival Db
2a 2b 2c gb
Nutrients, Growth
Antagonists m
water 2d 1b
1a
Mutualists

Antagonists and Mutualists 5

Nutrients 6

Toxins 7

Figure 2. Conceptual model of plant life history traits and their coupling with aboveground and belowground interactions. Plants acquire
energy and carbon aboveground and nutrients and water belowground and distribute nutrients and energy to aboveground and below-
ground plant organs. Plants face tradeoffs in the allocation of energy and nutrients to growth (ga  aboveground growth, gb  belowground
growth), defence (da  aboveground defence, db  belowground defence), reproduction (r) and associations with mutualistic symbionts
(m). The costs and benefits of these mutualists are dependent on benefits of enhanced nutrient uptake (1a) and increased plant defences
(1b) through upregulating the jasmonic acid (JA) defence pathway, which can trade off with reduced defence via the salicyclic acid (SA)
defence pathway. Belowground antagonists suppress plant biomass yet can stimulate aboveground antagonists (2a), whereas aboveground
antagonists generally suppress plant biomass as well as belowground antagonists (2b). Both below- and aboveground antagonists can trigger
plant defence responses which can suppress the antagonists (2c) and potentially also belowground mutualists (2d). The investment in
defence results in impacts on plant biomass as a result of reduced negative impacts of antagonists (3a) and also results in plant material with
specific chemical properties upon plant death (3b). Aboveground reproduction is crucial for ensuring plant fitness, as manifested in seed
numbers (sn) and seed size (sz), and many plant species are dependent on aboveground mutualists for pollination (4). The link between
plant defence and plant reproduction has been demonstrated but is still little explored. Belowground plants stimulate the build-up of
antagonists and mutualists (5) which can reduce (antagonists) or promote (mutualist) plant persistence and establishment of subsequent
generations. As plants die aboveground (Da) and belowground (Db) plant material returns to the soil for decomposition and mineralisation.
The feedback of nutrient (6) and toxin (7) release via plant exudates and litter, together with the feedback effects from plant antagonists and
mutualists (5) determine whether or not seedlings can establish well near parent plants or whether dispersal (8) will be a more favorable
option. Blue arrows: positive effect of mutualists on plant growth, defence and reproduction, red arrows: negative effects primarily gener-
ated by antagonists.

like biotrophs do, they evolved to suppress the SA pathway large extend dependent on which soil nutrients limit plant
and upregulate the JA pathway of their host plants. This growth most and the type of root mutualist a plant can asso-
finding led to the concept of mycorrhizal induced resistance ciate with (Lambers et al. 2008). In contrast to many above-
(MIR), which states that mycorrhiza increase systemic ground–belowground studies that include belowground
defence against necrotrophic pathogens and chewing herbi- mutualists only few examined impacts on aboveground
vores which concurs with increased susceptibility for sucking mutualists such as pollinators (Pineda et al. 2010) (Fig. 2:
insects and biotrophic pathogens (Pozo and Azcon-Aguilar 4). The few available studies show that these interactions do
2007, Jung et al. 2012). Apart from mycorrhizal fungi plant occur. For example mycorrhizal fungi can increase flower
mutualistic PGPR, rhizobia and fungal endophytes can also numbers, flower visits and pollination (Wolfe et al. 2005),
promote plant growth both by increasing plant nutrient whereas root herbivores can cause opposite effects, largely
availability and through plant defence (Pineda et al. 2010) driven by plant resource allocation constraints (Ghyselen
(Fig. 2: 1a and 1b). et al. 2016) (Fig. 2: 1 and 2 impact on r).
Overall belowground plant mutualists can promote plant
growth in multiple ways (Fig. 2: 1a, 1b), but incur plant Plant life history strategies and belowground
metabolic (Fig. 2: m) and defence associated ecological interactions
cost (Fig. 2: 3a), and in turn respond to plant metabolic
and defence responses to above- and belowground antago- Plant life history theory is central in understanding and
nists (Fig. 2: 2d). The balance between costs and benefit of predicting the occurrence of plants with different traits
belowground mutualist associations (Fig. 2: m vs 3a) is to a within and across ecosystems (Stearns 1976, Grime 1977),

499
 Ruderal Competitor Stress tolerator Plant resource allocation tradeoffs in these different plant
(A) (B) (C) types can be conceptualized as pie charts with growth (g),
r r d reproduction (r) and defence (d) each taking a share but
r d with different distributions between Ruderals, Competitors
g d g g and Stress tolerators which is also associated with different
life-spans and levels of stress and disturbance (Fig. 3: A–C).
Under high disturbance ruderals, which typically grow
(D) (E) (F) and reproduce fast, prevail. Under high resource stress but
r r d d
m r low disturbance stress tolerators proliferate as they are best
d m adapted to such environments by slow growth and invest-
g g g ment in defence and late reproduction. Finally, competitors
are dominant where resources are abundant and disturbance
stress is low, this group invests in rapid growth and resource acqui-
disturbance
sition above- and belowground, yet reproduce slower than
ruderals. The categorical approach of comparing plant strate-
lifespan
gies within and across ecosystems became more quantitative
with the leaf–height–seed (LHS) strategy scheme (Westoby
Figure 3. Conceptual model for the different plant strategies
1998) and plant functional trait approaches (Westoby et al.
Ruderal, Competitor or Stress tolerator (sensu Grime) of the dis-
tribution of plant investment in plant life history traits of growth 2002). These revealed that at a global scale plants appear to
(g), defence (d) and reproduction (r). (A)–(C) indicate energy group along two main axes of trait variation, being the axis
investment distribution not taking root mutualists into account, of the resource economic spectrum which reflects the trait
(D)–(F) show the distribution including allocation to mutualists tradeoff of resource acquisition versus conservation, and the
(m). Ruderals (A, D) are expected to invest most in reproduction axis of plant (organ) size (Diaz et al. 2016). The link between
and not in mutualist, they occur in soil with regular disturbance plant traits and plant life history strategies across ecosystems
and low nutrient stress and live short. Stress tolerators (C, F) are was recently also established, showing that for slow grow-
expected at the other end of the spectrum investing greatly in
ing, long-lived plants with large seeds fitness is mainly deter-
defence and in mutualists, occurring in soil with low disturbance
frequency yet with low mineral nutrient availability and being mined by survival, whereas in fast growing, short-lived plants
long-lived. Competitors (B, E) are expected to invest most in with small seeds fitness is more determined by growth and
growth but also in defence and in mutualists more than ruderals fecundity (Adler et al. 2014). These results are reflected in
do and occur at intermediate levels of disturbance; investing in Fig. 3 with the large allocation to reproduction in Ruderals
root mutualists (m) can partly take the role of enhanced defence (A), large allocation to growth in Competitors (B) and large
and does not need to incur a cost on growth as long as growth allocation to defence in Stress tolerators (C), being associated
limiting plant nutrients are provided in return for plant energy so with a gradient from short to long lifespan.
that energetic costs can be offset.
Soil resources play an important role as environmental
selection filters for plants to establish, reproduce and per-
and over the years many studies on this topic have been pub- sist. However, the coupling between soil nutrients, plant
lished (Fig. 1). Plant life history theory puts forward that traits, litter feedback and plant fitness was only established
plants have limited resources and time to invest in growth, in the 1990s (Berendse 1994). Around this time the role of
reproduction and defence and should balance these to maxi- aboveground herbivores in leaf defence traits with cascad-
mize fitness within the environmental constraints (Bazzaz ing effects on litter decomposition was also demonstrated
et al. 1987, Stearns 1989, Herms and Mattson 1992) (Fig. (Grime et al. 1997). These authors showed that well defended
2: g, r and d). Important plant life history traits are: seed- plants (cf. stress tolerators) experience less herbivory yet
ling survival, growth rate, age of sexual maturity, age of first have more slowly decomposing litter, illustrating indirect
reproduction, plant size, number of seeds, seed size, seed growth–defence tradeoffs (Fig. 2: 3b, 6). Another strat-
dispersal, plant longevity and death. These traits are inter- egy of plants to deal with leaf herbivores is to tolerate her-
related within individual plants (Fig. 2). Plants are to some bivory and regrow the lost tissues (cf. ruderals/competitors)
extend plastic in their traits so that the same plant genotype (Fig. 2: allocation to g versus d), which is possible when
grown in different conditions can differ in resource alloca- belowground nutrients are stored in roots or available in
tion to growth, reproduction and defence. However, at the the soil. For example in grazed grasslands nutrient avail-
basis plant traits are genetically encoded and heritable so that ability can be temporarily increased by aboveground and
life history traits evolve and can differ within and between belowground herbivory via triggering plant root exuda-
species. tion which in turn fuels decomposition and mineraliza-
It is well recognized that environmental abiotic and tion by soil microbes, and by returning excrements to the
biotic conditions act as selection filters on plant establish- soil (Milchunas and Lauenroth 1993, Hamilton and Frank
ment, survival and reproduction, and that thereby the envi- 2001, Bardgett and Wardle 2003). Apart from above- and
ronmental factors select plants with specific traits. Grime belowground herbivores it became increasingly clear that
(1977) conceptualized this selection in his C-S-R triangle root interacting soil-borne microbes also play a key role
of the plant strategy types Competitors, Stress tolerators in plant growth and survival (van der Putten et  al. 1993,
and Ruderals. These plant categories reflect how plants Bever et  al. 1997) and nutrient cycling (Cornelissen et  al.
respond under varying levels of stress and competition due 2001, Lambers et al. 2008). Therefore, to understand plant
to tradeoffs between growth, reproduction and maintenance. life history strategies, above- and belowground interactions

500
with antagonists and mutualists during and after plant life 6). However, plants from nutrient poor systems invest in
needs to be integrated. We can do so by accounting for their mutualistic mycorrhizal associations to access nutrients from
impact on plant trait selection and its feedback to subsequent organic matter and thereby maintain their fitness in habitats
generations through soil communities and nutrient cycling where plants from nutrient rich systems are not able to estab-
(Wardle et  al. 2004, Ehrenfeld et  al. 2005) (Fig. 2: 5, 6). lish (Berendse 1994, Cornelissen et al. 2001, Lambers et al.
In natural systems habitats of low and high fertility harbour 2008). Moreover, plants with nutrient-poor tissues are more
plants that differ markedly in their life history traits. Plants resistant to herbivore and pathogen attack because they are
from fertile systems grow faster and contain more nutrients less nutritious and because their denser tissues are a stronger
in their plant tissues and litter than plants from nutrient physical barrier. Given these roles of belowground mutualists
poor systems, and this feeds back to subsequent plant growth and the fact that they have been co-evolving with plants and
via fast decomposition and mineralisation in fertile systems plant life-history traits it is warranted to explicitly include
and slow litter decomposition and mineralisation in nutri- them in the equation of plant resource allocation to different
ent-poor systems (Aerts 1999, Wardle et al. 2004) (Fig. 2: life-history traits. I therefore propose Fig. 3D–F as improved

(A) Ruderal strategy

D
8 i
s
sz Seed size p
Energy, e
Antagonists r Reproduction sn r
carbon
Seed number s
ga Growth a
l
Defence Da
Biomass ph
Plant ys Above-
Death
growth ic below-
Seed(ling) Biomass Defence al ground
survival Db
gb
Nutrients, Growth
Antagonists
water

Mutualists

Antagonists 5

Nutrients 6

Toxins 7

(B) Competitor strategy

D
8 i
Mutualists
s
4 p
sz Seed size
Energy, e
Antagonists r Reproduction sn r
carbon
Seed number s
ga Growth a
l
da Defence Da
Biomass ph
Plant JA -- SA ys Above-
Death
growth ic below-
Biomass db Defence al ground
Seed(ling)
survival Db
gb
Nutrients, Growth
Antagonists m
water

Mutualists

Antagonists and Mutualists 5

Nutrients 6

Toxins 7

Figure 4. Conceptual models based on Fig. 2 and 3 showing the expected coupling between plant life-history traits and above- and below-
ground interactions for Ruderals (A), Competitors (B) and Stress tolerators (C). Numbers and symbols have the same meaning as in Fig. 2.

501
 (C) Stress tolerator strategy
D
8 i
Mutualists
s
4 p
sz Seed size
Energy, e
Antagonists r Reproduction sn r
carbon
Seed number s
ga Growth a
l
da Defence Da
Biomass ph
Plant JA -- SA ys Above-
Death
growth ic below-
Biomass db Defence al ground
Seed(ling)
survival Db
gb
Nutrients, Growth
Antagonists m
water

Mutualists

Mutualists 5

Nutrients 6

Toxins
7

Figure 4. Continued

view of Fig. 3A–C to include belowground mutualists as those listed in Table 1 are available on above–belowground
a component of plant life-history traits. The exact balance interactions and plant life history traits, but apparently these
between allocation to reproduction, growth, defence and did not include ‘plant life history’ as such in their key words,
belowground mutualists depicted in Fig. 3 is indicative and title or abstract. The studies that did include both research
needs quantification. However, based on current literature topics mostly comprised studies on belowground herbivores
it can be expected that ruderals hardly invest in mutualists and root mutualists and their impact on aboveground her-
(Fig. 3D), that competitors invest in mutualists and benefit bivores, plant responses, and in few cases on pollinators and
from improved defence and nutrient returns (Fig. 3E), and seed production (Table 1, Fig. 2: 1a–b, 2a–c, 4). These stud-
that stress tolerators invest most in belowground mutualists ies revealed how belowground interactions invoke changes
and get large returns in terms of nutrient access for growth in aboveground herbivore performance through plant meta-
and much improved defence (Fig. 3F). bolic changes within individual plants, whereas the studies
Defence strategies can be apparent both aboveground and that included several plant species focused on understanding
belowground (van der Putten et  al. 2001). Plant strategies the role of above–belowground interactions in plant species
to deal with belowground antagonists are diverse and range co-existence and succession. These studies (Table 1) illus-
from tolerance and regrowth of lost roots, to root physical trate the role of primary (Fig. 2: 1a, 2a–b) and secondary
and chemical defence, to pathogen escape through clonal (Fig. 2: 2cd) plant metabolites through which belowground
growth and seed dispersal (van der Putten 2003). Short- antagonists and mutualists can suppress or stimulate above-
lived plants tend to escape via seeds or use chemical defences ground antagonists and mutualist and vice versa, as well as
if nutrient and energy availability allow for that (Fig. 4A), tradeoffs in plant growth and defence strategies (Fig. 2: g
whereas long-lived plants protect their roots via dense tissue versus d). Within a system these tradeoffs can differ between
and invest in mutualistic root symbionts which not only help plant species due to specificity/selectivity of antagonists and
with nutrient uptake but also with root defence (Fig. 4C). mutualists and the ability of plants to deal with the prevail-
However, seedlings are generally more sensitive to specific ing abiotic conditions above- and belowground. Therefore
root pathogens and herbivores than adult plants, such that it is required to quantify the benefits plants get from their
seeds need to disperse to escape whereas mature plants are defence strategy in terms of increased net availability of
tolerant or resistant to the these pathogens (Packer and Clay energy and nutrients in relation to pressure of above- and
2000). The optimal mode of defence thus changes with plant belowground antagonists and resource availability, yet very
ontogeny and herbivore and pathogen pressure aboveground few studies have done so (Fig 2: ga and gb versus da and db
(Boege and Marquis 2005) as well as belowground. and longer-term return 3a).
To date it remains hard to predict the coupling between
Coupling between above–belowground interactions above–belowground interactions and plant life history traits.
and life history strategies Nevertheless the concept of plant traits and tradeoffs in the
context of abiotic and biotic selection filters and plant–soil
Only few studies on aboveground and belowground feedbacks offers great potential (Fig. 3, Fig. 4A–C). Such
interactions included an explicit focus on plant life history an integrative approach will also benefit trait based ecology
(Fig. 1). However, it has to be noted that more studies than more generally by helping to identify key environmental

502
Table 1. Studies on aboveground (AG) and belowground (BG) interactions and plant life history (WoS 18 June 2016) according to the specific
interactions and life history trait focus. Plant ID  vegetation or plant species type, AMF  arbuscular mycorrhizal fungi, PGPR  plant growth
promoting rhizo-bacteria, EW  earthworms, LH  life history trait focus.

BG AG
Interaction Plant ID Antagonist Mutualist Antagonist Mutualist LH Ref
Plant–plant prairie – – grazers – plant 1
Plant–plant prairie – AMF – – plant 2
BG–AG Fabacea – AMF caterpillars – caterpillar 3
BG–AG review insects – herbivores – insect, plant 4
BG–AG review herbivores, mycorrhiza, – – plant 5
pathogens PGPR
BG–AG Onagracea – AMF – pollinators plant, seed 6
BG Brassica fly larvae – – – fly larvae 7
BG–AG Fabacea – AMF – nectaries 8
BG–AG Fabacea – – spider mites – spider mite 9
BG–AG review herbivores, mycorrhiza, herbivores, pollinators, plant 10
pathogens PGPR pathogens endophytes
AG Picea – AMF – – plant 11
Plant–plant, AG Carex – – herbivores, leaf fungi – plant 12
BG–AG Fabacea nematode AMF spider mites spider mite 13
BG–AG Fabacea – AMF spider mites – spider mite 14
BG–AG Fabacea – rhizobia spider mites – spider mite 15
BG–AG Asteracea – EW aphids – aphid 16
BG–AG Eschscholzia – – gophers – plant, fruit 17
Plant–plant semi-arid – – – – plant 18
BG–AG Asteracea nematode – locust – plant, seed 19
Plant–plant Poacea salt marsh – – – – plant 20
BG–AG Brassica nematode – trips, spider mites – spider mite 21
BG–AG Brassica nematode – aphids – aphid 22

1) Milchunas and Lauenroth 1993; 2) Hartnett and Wilson 1999; 3) Goverde et al. 2000; 4) Blossey and Hunt-Joshi 2003; 5) van der Putten
2003; 6) Wolfe et al. 2005; 7) van Dam and Raaijmakers 2006; 8) Laird and Addicott 2007; 9) Hoffmann et al. 2009; 10) van der Putten et al.
2009; 11) Camill et al. 2010; 12) Whitlock et al. 2010; 13) Bonte et al. 2010; 14) Nishida et al. 2010; 15) Katayama et al. 2010; 16) Wurst
and Forstreuter 2010; 17) Watts et al. 2011; 18) Pugnaire et al. 2011; 19) de la Peña and Bonte 2014; 20) Crosby et al. 2015; 21) Kammerhofer
et al. 2015; 22) Hol et al. 2016.

selection filters and their dynamics (Shipley et al. 2016). To other trophic levels such as soil fungi (Chagnon et al. 2013,
understand life history traits and tradeoffs from an evolu- Aguilar-Trigueros et al. 2015).
tionary perspective, studies testing the role of intraspecific Pollinators play an important role in life history of
variation in plant defences and their costs and benefits are many plants, yet only few studies have included pollinators
highly relevant, even though the relations between costs in investigations of above–belowground interactions and
and benefits are rarely straightforward (Agrawal 2011). For plant life history (Table 1, Fig. 2: 4). Nevertheless it has
example high constitutive levels of plant chemical defence been shown that belowground mutualists can increase the
against herbivores and pathogens could in principle tradeoff number and size of flowers and pollinator visits and sub-
with reduced benefit from mutualistic root fungi (Fig. 2: sequent seed set and plant fitness (Wolfe et al. 2005). On
2d). One of the few examples testing this idea was per- the other hand root herbivores can constrain the production
formed using Plantago lanceolata and revealed that although of flowers and pollinator visits, but this may not imply pol-
well defended plant genotypes had reduced levels of mycor- len limitation (Ghyselen et al. 2016). More work is needed
rhizal colonisation they still benefitted to the same extent to reveal general patterns in above–belowground interac-
from the mutualistic association as the less defended plant tions from the perspective of interactions with pollinators
genotypes (De Deyn et al. 2009). This raises the question as and plant investments in reproductive organs and tradeoffs
to what the optimal level of colonisation is, both from the with other interactions (Pineda et  al. 2010). It would be
plant and from the AMF perspective, as colonization level interesting to know whether plant species with different
and benefit are not linearly positively related. The fact that modes of reproduction, or with other distinct strategies,
the roots with higher levels of defence compounds were still interact in fundamentally different ways with their above-
colonised by AMF may not be surprising given the long ground and belowground antagonists and mutualists. A
evolutionary history of arbuscular mycorrhizal fungi and recent review of the evolutionary interactions between plant
thereby potentially a larger tolerance to the compounds traits of reproduction and defence shows that the evolution
than pathogenic fungi. We should indeed not forget that of plant defences is affected by the evolution of reproduc-
not only plants but also their antagonists and mutualists tive traits and the other way round (Johnson et al. 2015).
above- and belowground evolve in their life history traits This interconnectedness is due to interrelated plant meta-
in response to their host plants and other biotic and abi- bolic pathways that generate plant floral and defence traits,
otic conditions. Trait-based approaches provide a tool to and the fact that not only pollinators but also herbivores
integrate life history strategies from plants with those from and seed eaters respond to plant reproductive traits. To

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understand and predict evolutionary trajectories between Conclusions
pollinators, herbivores and belowground mutualists it is
warranted to reveal the genes underlying mutualist symbi- Terrestrial plants intrinsically couple aboveground and
ont associations, plant reproductive traits and plant defence belowground ecosystem components through their above-
traits and investigate their molecular (intragenomic) ground and belowground organs which function in a coor-
coevolution. dinated way (Fig. 2). The abiotic environment determines
It is well established that plants and their mutualistic the maximal availability of energy, water and nutrients,
root symbionts and antagonists can co-evolve (Mytton whereas the biotic environment sets the scene for the actual
1975, Thrall et al. 2006). Saprotrophic soil microbes on the plant availability of these resources in space and time. Plant
other hand have long thought to be non-specific given the life history traits capture how plants allocate their energy
large diversity and redundancy of microbial species with and nutrients to growth, defence and reproduction, and
respect to litter decomposition. However, in recent years ideally also to belowground mutualists (Fig. 3). For a long
for example work with Populus angustifolia showed that dif- time studies of plant life history traits focussed on above-
ferent plant genotypes can select different associated soil ground traits and considered belowground interactions
microbial communities in a heritable way (Schweitzer et al. merely from the perspective of abiotic resources (Reich
2008). Moreover, these plant genotype specific soil com- 2014). However, it is now recognised that both the soil
munities feed back to promote seedling survival and growth and aboveground biotic environment also act as major
of these genotypes despite reduced nitrogen availability selection filters on plant life history traits (Fig. 2: 1, 2,
(Pregitzer et al. 2010) (Fig. 2: 5, 6). Further empirical and 3a), and in turn that these traits alter the soil abiotic and
modeling work revealed that interactions between plants biotic environment through plant–soil feedbacks (Fig. 2:
and soil communities can generally lead to evolution of 3b, 5–7) which can lead to eco-evolutionary dynamics. To
plant traits through niche construction, provided gene flow increase our understanding of eco-evolutionary dynamics
and selection pressure are large enough (Schweitzer et  al. of plant life history traits, plant community dynamics and
2014). These findings illustrate potential evolutionary tra- ecosystem functioning a key challenge is to include above-
jectories resulting from plant–soil feedbacks. However, they and belowground biotic interactions in trait-based ecology.
also illustrate the need to identify the biotic components This will require revealing the selection pressure invoked
of negative and positive feedbacks, their interaction with by plant antagonists and mutualists in a community con-
the abiotic environment, and the tradeoffs in the underly- text across abiotic environmental gradients, during plant
ing plant traits in a community context (Van Nuland et al. growth and reproduction and through abiotic and biotic
2016) (Fig. 2: 5–7). legacy effects in soil.
Plant life history strategies are determined by environ- Studies on aboveground–belowground interactions on
mental constraints of energy availability aboveground and individual plants revealed how belowground mutualists and
soil nutrient and water availability and pH belowground. antagonists affect aboveground antagonists (and the other
These properties can vary greatly at large spatial scale and way round) through plant defence mechanisms and allo-
result in biomes composed of plant species with particular cation of primary and secondary plant metabolites. These
life history traits (Fig. 3). Within communities the avail- mechanisms result in increased or decreased plant protec-
ability of energy and soil resources for individual plants is tion against aboveground antagonists, depending on the
strongly affected by the presence of plants competing for mode of action and sequence of arrival of belowground and
these same resources, so that also species within an ecosys- aboveground mutualists and antagonists (Jung et al. 2012,
tem can differ in their allocation patters resembling differ- Vos et al. 2013, Poelman and Kessler 2016). To date many
ences between ruderals, competitors and stress tolerators unknowns remain with respect to the mechanisms and
(Fig. 3) albeit in more subtle ways. Recent work demon- heritability of plant defences induced by plant antagonists
strated that plant community context can drive plant trait and mutualists (van Dam and Heil 2011), as well as with
evolution such that progeny of plants selected in plant respect to the interconnectedness between traits of defence
species mixtures have increased interspecific trait comple- and reproduction (Johnson et  al. 2015). Nevertheless,
mentarity as compared to progeny of individuals selected the complexity of the interactions can be reduced by
in monocultures (Zuppinger-Dingley et  al. 2014). The identifying and focussing on keystone antagonists and
enhanced investment in complementary growth strategies mutualists and their impacts on plant fitness (Agrawal 2011,
however may come at a cost of reduced tolerance or resis- van Dam and Heil 2011, Poelman and Kessler 2016). This
tance to herbivores and diseases (Zuppinger-Dingley et al. requires an integrative approach which combines mecha-
2016). On the other hand plant species mixtures can buf- nistic studies with a holistic perspective in ecologically rel-
fer against the build-up of soil-borne antagonist whilst at evant settings (van Dam and Heil 2011, Cortois and De
the same time retaining beneficial mutualists (Cortois et al. Deyn 2012). In this context it is important to realise that
2016). This indicates that the tradeoff of reduced defence of belowground mutualists perform multiple functions which
progeny selected in species mixtures would be strong when can change during plant ontogeny, whereas antagonists can
growing in monoculture but much less so when growing in provide indirect benefits, so that evaluating costs and ben-
species mixtures where investing in growth is more advan- efits of the association under different environmental con-
tageous. These findings are not only relevant for natural ditions requires long-term investigations in a community
systems but also suggests potential benefits for agricultural context.
systems through breeding for combinability between species Trait-based ecology and the resource economic spec-
or genotypes. trum promoted a more generic understanding of the

504
coupling between plant life history traits and tradeoffs Future directions
in relation to the abiotic environment, with species from
rich environments growing and reproducing fast and spe- To reveal if plant species with different life history strategies
cies from poor environments growing slow yet living long interact in fundamentally different ways with aboveground
and reproducing later in life (Reich 2014, Adler et  al. and belowground antagonists it is warranted to experi-
2014, Diaz et al. 2016). These strategies result from plant mentally test how the soil communities and aboveground
tradeoffs in growth, reproduction and defence, with slow communities develop across plant species with different life
growing plants generally being less nutritious and bet- history strategies over time, and what their impact is on the
ter defended against generalist herbivores and pathogens fitness of following generations. These trajectories should be
(Fig. 3). This in turn feeds back in slow nutrient cycling tested across the plant species in soils of different levels of
due to the production of nutrient poor litter. Moreover, fertility and of different starting densities of mutualists and
above- and belowground antagonists and mutualists act antagonists.
as a prime selection filter on plant traits, by selective sup- Field observations within ecotypes (grassland, forest, ...)
pression of herbivore and disease prone plants and selective on soils of the same texture class (clay/silt/sand) and across
promotion of plants that associate with beneficial mutual- a gradient of different levels of soil fertility should inform
ist symbionts. Therefore, an integrative approach of plant about the composition of plant species and their life history
life history and above–belowground interactions is needed traits, as well as on the composition of belowground and
to advance our mechanistic understanding of the cou- aboveground communities of mutualists and antagonists.
pling between plant traits, eco-evolutionary dynamics and Such surveys can then reveal co-occurrence patterns of life
ecosystem functioning (Fig. 2). history strategies and above- and belowground communities,
Recent work shows that root traits play a key role in and can provide the backdrop to set-up controlled experi-
plant–soil interactions and that the aboveground plant ments with relevant starting densities and compositions of
resource economic spectrum is not mirrored belowground, soil biota and soil fertility.
such that explicit inclusion of root traits and their associ- To capture the eco-evolutionary dynamics between
ated symbionts in trait-based ecology is warranted (Weem- plant life history traits and belowground and aboveground
stra et al. 2016, Cortois et al. 2016) (Fig. 2: gb, db, m, Db). mutualists and antagonists, plant selection experiments
Plant–soil feedbacks are generated through nutrient cycling using a range of plant genotypes that span the intraspecific
(Baxendale et  al. 2014) (Fig. 2: 6), by phytotoxic effects variation in life history traits are warranted. The impact of
(Fig. 2: 7), and via soil mutualists and antagonists (Cor- belowground antagonists and mutualists on the selection
tois et al. 2016) (Fig. 2: 5), yet in natural systems it is hard of aboveground plant traits can then be tested by the selec-
to separate these effects as they interact (Cortois and De tive inclusion or exclusion of belowground mutualists and/
Deyn 2012). A next major step forward will therefore be to or antagonists and quantification of the change in plant life
understand how plant traits of nutrient cycling and those of history traits of growth, defence and reproduction over mul-
defence against antagonists and of associations with mutu- tiple generations. Ideally such experiments should be per-
alists belowground (Ke et  al. 2015) and aboveground are formed in outdoor field settings in which plants planted in
interrelated. An integrative trait-based approach of aboveg- mesocosms with different soil community treatments can
round and belowground plant resource acquisition, defence be exposed to, or protected from, interactions with above-
and reproduction that includes keystone interactions with ground antagonists and mutualists. Earlier work using
antagonists and mutualists will not only advance our under- selective exclusion of aboveground herbivores showed eco-
standing of plant life histories, it can also strengthen the evolutionary impacts of aboveground herbivores on plant
field of trait-based ecology by revealing selection filters and life history traits of defence and competitive ability (Agrawal
explicitly including intraspecific variation (Shipley et  al. et al. 2012). Such studies demonstrate the value of combin-
2016). Conceptually I would like to translate Fig. 3 into a ing local experimental treatments with relevant field settings
more flexible representation of plant allocation and life his- and should be extended to include belowground interactions
tory traits, taking the flows of energy and nutrients in the and their selection on plant life history traits over multiple
context of above–belowground interactions as well as soil generations taking into account soil feedbacks via the plant
feedbacks into account. Starting with the relatively simple selection on soil communities of mutualists and antagonists
Ruderals (Fig. 3AD) this would translate into plants grow- and soil abiotic changes in terms of organic matter returns.
ing fast and investing primarily in reproduction, whilst at The tools available to move forward are several which
the same time building-up belowground antagonists thereby are to be used in a complementing way. Advancements in
promoting seed dispersal to increase fitness (Fig. 4A). Spe- molecular microbial and plant ecology, genomics and bio-
cies with more Competitor life-history strategies primar- informatics enable tracking changes in biological systems at
ily invest in growth (Fig. 3BE), yet have more complex unprecedented scale from plant genes to plant metabolites
interactions as also associations with mutualists and plant and soil microbial communities in all its diversity. However,
defence come into play (Fig. 4B). It is expect that plant–soil the most detailed knowledge we have on plant allocation to
feedbacks operate especially via nutrient returns as well as growth, defence and reproduction and their interaction with
via mutualistic and antagonistic soil communities. Finally aboveground and belowground antagonists and mutualist is
Stress tolerator type plants invest mostly in defence and so on a few fast growing model plant species. The challenge now
in longevity (Fig. 3CF), relying heavily on belowground is to expand this knowledge to other plant types and to com-
mutualists for resource acquisition in mature plants as well bine the short-term and longer-term (including feed-back)
as in their offspring (Fig. 4C). impacts of plant life history traits in a community context,

505
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