Download Herbivore-induced resource sequestration in plants: why bother?

Oecologia (2011) 167:1–9
DOI 10.1007/s00442-011-1968-2
CONCEPTS, REVIEWS AND SYNTHESES
Herbivore-induced resource sequestration in plants: why bother?
Colin M. Orians • Alexandra Thorn
Sara Gómez
•
Received: 4 September 2010 / Accepted: 8 March 2011 / Published online: 24 March 2011
Ó Springer-Verlag 2011
Abstract Herbivores can cause numerous changes in
primary plant metabolism. Recent studies using radioisotopes, for example, have found that insect herbivores and
related cues can induce faster export from leaves and roots
and greater partitioning into tissues inaccessible to foraging
herbivores. This process, termed induced resource sequestration, is being proposed as an important response of plants
to cope with herbivory. Here, we review the evidence for
resource sequestration and suggest that associated allocation
and ecological costs may limit the benefit of this response
because resources allocated to storage are not immediately
available to other plant functions or may be consumed by
other enemies. We then present a conceptual model that
describes the conditions under which benefits might outweigh costs of induced resource sequestration. Benefits and
costs are discussed in the context of differences in plant lifehistory traits and biotic and abiotic conditions, and new
testable hypotheses are presented to guide future research.
We predict that intrinsic factors related to life history,
ontogeny and phenology will alter patterns of induced
sequestration. We also predict that induced sequestration
Communicated by Caroline Müller.
C. M. Orians (&) A. Thorn S. Gómez
Department of Biology, Tufts University,
Medford, MA 02155, USA
e-mail: [email protected]
A. Thorn
e-mail: [email protected]
S. Gómez
e-mail: [email protected]
S. Gómez
Department of Biological Sciences,
University of Rhode Island, Kingston, RI 02882, USA
will depend on certain external factors: abiotic conditions,
types of herbivores, and trophic interactions. We hope the
concepts presented here will stimulate more focused
research on the ecological and evolutionary costs and benefits of herbivore-induced resource sequestration.
Keywords Defense Plant–herbivore interactions Storage Tolerance Resource allocation
Introduction
For all organisms, allocation of resources to the primary
functions of growth and reproduction must be balanced
with the various secondary functions required to survive
and deal with abiotic and biotic stresses. Plants rely on
physiological, chemical, biomechanical, and developmental processes to deal with stress. Stresses that vary in time,
such as drought and attack by herbivores, require constant
adjustment and these adjustments are essential to growth
and survival of plants (Mooney and Winner 1991; Karban
and Baldwin 1997; Agrawal and Karban 1999). In response
to herbivory, for example, plants can employ two general
strategies: production of chemical and morphological
defense traits to deter herbivores (‘‘resistance’’), and
mobilization of storage reserves for regrowth and reproduction after leaf loss (‘‘tolerance’’) (Karban and Baldwin
1997). Tolerance mechanisms are often linked to regrowth
processes after a herbivory event (Tschaplinksi and Blake
1989a, b; Tiffin 2000). Less appreciated, however, is the
herbivore-induced change in resource allocation and
physiology that can increase plant tolerance to herbivory
(Schwachtje and Baldwin 2008). This phenomenon, termed
induced resource sequestration, refers to rapid herbivoreinduced changes in resource allocation patterns that result
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in an increase in export of existing or newly acquired
resources from attacked tissues (and/or systemic tissues
with vascular connections) into storage organs. These
resources are thus temporarily sequested (unavailable) for
growth, defense or storage in the tissues from which they
were exported.
Oecologia (2011) 167:1–9
partitioning in wild tobacco extends flowering time and
thereby increases fitness. Given the increasing evidence for
induced sequestration, there is a need to examine the
conditions likely to favor this strategy.
Storage: benefits and costs
Evidence for induced resource sequestration
There is growing evidence that herbivore feeding, herbivore cues and signal molecules associated with herbivory
cause changes in resource export and allocation to storage
tissue (Holland et al. 1996; Schwachtje et al. 2006; Babst
et al. 2008; Kaplan et al. 2008). Holland et al. (1996), for
example, found that feeding by grasshoppers causes 14C to
accumulate in roots. Kaplan et al. (2008) showed a similar
pattern in tobacco roots after folivory by chewing herbivores using 13C. Recent studies have adopted the use of
short-lived radioisotopes (such as 11CO2), which allows
quantification of resource dynamics in vivo and the comparison of allocation patterns before and after treatment.
This is possible because of the rapid decay of 11CO2
(t1/2 = 20.4 min). This approach has been used to document an increase in leaf photosynthate export to stems and/
or roots within hours of treatment with jasmonic acid
(Babst et al. 2005), caterpillar regurgitant (Schwachtje
et al. 2006), or feeding by gypsy moth larvae (Babst et al.
2008). In addition to Babst et al. (2005), other studies have
also used jasmonates to study induced sequestration.
Methyl jasmonate increases photosynthate export from
treated leaves (Gómez et al. 2010) and treatment of roots
with jasmonates causes photosynthate to be diverted away
from the treated roots and into untreated roots (Henkes
et al. 2008). Interestingly, silencing the jasmonate pathway
in wild tobacco does not prevent induced export and partitioning (Schwachtje et al. 2006), suggesting that other
signaling pathways may also be involved.
Changes in resource allocation in response to herbivory
are not limited to photosynthate. For example, Frost and
Hunter (2008) did not observe increased carbon accumulation in storage tissues of oaks following herbivory, but
did observe an increase in nitrogen within these tissues.
When methyl jasmonate is applied to leaves of tomato, it
increases nitrogen (13N) export and partitioning to roots
(Gómez et al. 2010), and when applied to roots of alfalfa it
increases nitrogen storage within the tap root (Meuriot
et al. 2004).
Relatively little is known about the long-term consequences of induced sequestration. Beardmore et al. (2000)
showed that chronic exposure of leaves to methyl jasmonate can increase protein concentrations in storage tissues
in poplar. Schwachtje et al. (2006) found that induced root
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It is well known that constitutive storage represents an
important buffer against abiotic and biotic stresses
(Trumble et al. 1993; Kobe et al. 2010). For example,
drought often triggers a change in the distribution of starch
and sugar reserves and frequently results in greater transport to roots or to young developing leaves (Geiger and
Servaites 1991). Similarly, defoliation is well known to
result in the mobilization of starch reserves to fuel new
plant growth (Tschaplinksi and Blake 1989a, b; Kosola
et al. 2001), and the presence of these storage reserves is a
key factor determining post-defoliation survival (Canham
et al. 1999). The buffering capacity of storage implies that
herbivore-induced storage could be adaptive.
There can be costs of storage. Although studies of wild
and cultivated species have shown that species with higher
rates of storage are more likely to survive stressors such as
shading (Kobe 1997; Myers and Kitajima 2007), drought or
nutrient stress (Shaw et al. 2002; Paula and Pausas 2011),
and defoliation (Anten et al. 2003; Myers and Kitajima
2007), these same studies show that these species grow
more slowly. Induced storage may provide a buffering
mechanism without the long-term growth costs of constitutive storage.
We note that costs may be transient by varying with
plant ontogeny and phenology (Boege and Marquis 2005;
Boege et al. 2007; Orians et al. 2010; Van Dam et al.
2001). In particular, deflection from growth may be most
costly during periods of rapid growth, including periods of
leaf production and fruit maturation. A recent study that
focused on growth–defense tradeoffs in willow illustrates
this concept (Orians et al. 2010). This study found evidence
for a trade-off between allocation to roots and defense in
younger seedlings but a positive correlation in older
seedlings, a result consistent with the observation that
larger plants often grow faster and produce higher concentrations of chemical defenses (e.g., Briggs and Schultz
1990; Orians et al. 2003).
In contrast to the cost of constitutive storage, the costs of
herbivore-induced resource sequestration has received little
attention. It may result in allocation costs (fewer resources
for growth or reproduction), or ecological costs (higher
performance of enemies that consume storage tissues).
Evidence for allocation costs comes from a study on wild
tobacco (Schwachtje et al. 2006). They found that induction of wild-type plants increased carbon allocation to roots
Oecologia (2011) 167:1–9
(10%) and resulted in smaller plants that exhibited delayed
reproduction. Moreover, a transformed genotype that had
constitutively greater allocation to roots was shorter and
produced fewer reproductive capsules. Interestingly, the
transformed genotype mobilized the root reserves after
elicitation and this resulted in greater flower production
later in the season. Clearly there are costs and potential
benefits of induced sequestration. We expect that costs
might be even larger in other plants since photosynthate
allocation to stems and/or roots has been shown to be as
high as 25% (Babst et al. 2008). Moreover, many studies
have shown that plants grow more slowly and exhibit
reduced fitness after simulated attack (Baldwin et al. 1998;
Zavala et al. 2004; Walls et al. 2005; reviewed by Cipollini
et al. 2003). While this is usually attributed to the cost of
resistance, an increase in induced sequestration could
contribute to this difference.
There are also potential ecological costs (Kaplan et al.
2008). Herbivore-induced resource sequestration and
potential subsequent exudation into the rhizosphere can
alter or create new interactions between plants and other
organisms in the soil (Bardgett et al. 1998; Henry et al.
2008). In some cases, induced allocation changes can lead
to positive interactions by promoting the colonization by
mutualists such as mycorrhizae (Tejeda-Sartorius et al.
2008), but in other cases induced sequestration might incur
ecological costs if it attracts or improves the performance
of consumers of the organs where resources are being
stored. For example, Kaplan et al. (2009) showed that
aboveground herbivory in tobacco resulted in an increased
allocation of carbon to roots and this was linked to an
increase in fecundity of a root nematode.
Conceptual model for resource allocation
While it is apparent that trade-offs often exist understanding the ways in which intrinsic and extrinsic factors
are expected to affect resource allocation requires a
detailed examination of the status of different tissues. In
Fig. 1, we present a conceptual model for possible pathways of resource flow within a plant. In general, mature
source leaves are responsible for the majority of carbon
fixation, and fine roots for the majority of nutrient uptake.
These resources may be allocated locally to growth,
defense, or storage (Blossey and Hunt-Joshi 2003; Karban
and Baldwin 1997), or exported for use elsewhere in the
plant. For a plant in vegetative growth phase that is not
experiencing herbivory, investment in new leaves represents the best assurance of long-term growth, but this may
not be the case when herbivores are present, since these
young leaves are often particularly vulnerable to attack
even when these young leaves are highly defended (e.g.,
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Fig. 1 Conceptual model for resource flows in plants. The labile
resource pool is derived from newly captured pools of carbon and
nutrient pools or from remobilized storage reserves. The labile carbon
pool is generated from photosynthesis, primarily by mature source
leaves. The labile nutrient pool is obtained from roots. The resulting
labile resource pool can then be allocated to support the growth of
sink tissues (roots, leaves, or reproductive tissues), to defense traits,
and to storage tissues. Herbivore-induced export of resources from
leaves or from fine roots (dashed arrows) into stems and storage roots
functions to sequester resources in tissues inaccessible to the
respective herbivores but may incur opportunity costs if resources
allocated for storage limit growth and reproduction or ecological costs
if other enemies specialize on these storage tissues
Nichols-Orians and Schultz 1990). Allocation to stem and
root storage may be increasingly favored as the probability
of continued defoliation increases, but this depends on the
vulnerability of these storage pools to attack by stem and
root herbivores or pathogens (see ecological costs above),
and intrinsic traits of the plant (see Fig. 2 below).
Herbivore-induced resource sequestration: a predictive
framework
We present a fulcrum model that explores conditions that
will tend to favor greater induced sequestration relative to
growth and/or defense (Fig. 2). We note that most plants
simultaneously grow, defend and allocate to storage so our
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Fig. 2 A fulcrum model for
predicting herbivore-induced
sequestration in plants.
Outcomes depend upon the
relative strength of intrinsic and
extrinsic factors. See text for
presentation of specific
predictions
Oecologia (2011) 167:1–9
INTRINSIC FACTORS
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GROWTH AND/OR DEFENSE
INDUCED SEQUESTRATION
FAVORED
FAVORED
Annuals
Perennials
Low storage in leaves
High storage in leaves
High constitutive storage
(in roots/stems)
Low constitutive storage
(in roots/stems)
Developing plants
Mature plants
During leaf flushing
Post-leaf expansion
During seed/fruit production
Prior to seed/fruit production
Low light
High light
High nutrient
Low nutrient
Generalist herbivores
Specialist herbivores
Mobile (specially if small)
Immobile or mobile (if large)
Solitary
Gregarious/outbreaking species
Browsing mammals or
piercing/sucking insects
Leaf chewing insects
High abundance of storage organ
attackers
Low abundance of storage organ
attackers
LIFE
HISTORY
ONTOGENY
PHENOLOGY
EXTRINSIC FACTORS
ABIOTIC
BIOTIC
goal is to highlight conditions that will maximize the extent
of induced resource sequestration. First, we evaluate
intrinsic factors such as life history, ontogeny and phenology. Second, we review extrinsic factors including the
abiotic and biotic environment, including resource availability and attributes of the herbivores themselves.
Intrinsic factors
To understand how patterns of resource allocation change
in response to herbivory, it is necessary to characterize the
status of the plant prior to herbivory. This status depends
on a range of factors, but centrally on aspects of plant life
history, plant ontogeny and phenology.
Life history
Plant species diverge greatly in their inherent patterns of
allocation to storage. Many plants constitutively allocate
large amounts of resources to rhizome and root storage.
This is true for cultivated crops such as beets, carrots and
potato, for biennial and perennial wild plants such as Alliaria petiolata (biennial) and Pastinaca sativa (biennial to
perennial; Sosnová and Klimešová 2009), and for species
that have a high capacity for resprouting (Paula and Pausas
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2011). For species with high constitutive storage, the
amount of carbon that can be sequestered during a folivore
attack is likely to be a small fraction of the total storage pool.
Induced carbon sequestration may provide little benefit in
these cases. In contrast, for species with little root storage or
for species that maintain high storage pools in their leaves
during the growing season, induced export is predicted to be
beneficial. In these plants, resources deflected from growth
and into storage during an attack may provide a critical pool of
resources necessary for regrowth.
Although these expectations have not been explicitly
tested, a few studies fit the predictions. Photosynthate
export to roots in the annual Nicotiana attenuata increased
only 10% (Schwachtje et al. 2006). In contrast, induced
sequestration of photosynthate was close to 25% in Populus (Babst et al. 2008), a woody perennial with high
concentrations of starch in its leaves (Babst et al. 2005).
Red oak, however, exhibited no induced sequestration of
photosynthate (Frost and Hunter 2008). Compared to other
species, oaks have a large root system and readily resprout
following cutting (Abrams 2003). The lack of induced
sequestration is consistent with the prediction that induced
sequestration would be low in species with high constitutive storage. Clearly further research explicitly comparing
species with different intrinsic traits is warranted.
Oecologia (2011) 167:1–9
Other life-history traits may also be important. Grime
(2001) classified species as being ruderal (short-lived
weedy species), competitive (long-lived dominant species),
or stress tolerators (species adapted to stressful environments). These differences are likely to influence a plant’s
relative resource allocation to growth, defense and storage.
Rapid growth is a characteristic of ruderal species, and
individuals that do not prioritize growth are likely to be
overgrown, making the opportunity costs of induced storage very high. Only after establishment might we expect
induced sequestration in these species. In contrast, both
competitive and stress tolerant species are expected to
invest significant resources in storage as a way to buffer
against environmental fluctuations (Kobe et al. 2010; Paula
and Pausas 2011). While induced resource sequestration
may be more common in these species, we expect it to be
negatively correlated with constitutive levels of storage as
species with more constitutive storage already have the
capacity to recover from tissue loss.
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(especially in annuals) since reproductive tissues are strong
sinks.
Extrinsic factors
Abiotic
Light and soil nutrient availability have large effects on
patterns of allocation to roots and to storage. In response to
light limitation, both the ratio of roots to shoot (Mooney
and Winner 1991) and the concentration of storage compounds are much lower (Nichols-Orians 1991), suggesting
that induced resource sequestration will be constrained by
light availability. In contrast, root:shoot ratios increase in
response to soil nutrient limitation, and a recent study by
Kobe et al. (2010) showed that investment in non-structural
carbohydrates within roots contributed to this pattern. This
leads us to predict that the capacity for induced sequestration may be greater for plants experiencing low nutrient
conditions.
Ontogeny
Biotic
Herbivore-induced sequestration is also postulated to vary
with plant ontogeny (Fig. 2). Young plants and their young
tissues are particularly prone to attack due to a higher
nitrogen content and less developed physical properties
(McKey 1974; Coley and Barone 1996; Fenner et al. 1999;
Wainhouse et al. 2009). Their small size also makes it
likely that herbivores can rapidly remove most if not all of
the leaf area (e.g., Fritz et al. 2001). This may limit the
benefits of induced sequestration and favor defense and
growth. In contrast, older plants may benefit from induced
export of resources to short-term storage pools prior to
reproduction or to late-season sequestration of resources
for overwintering (perennials only).
Phenology
Both leaf and reproductive phenology are predicted to
influence patterns of induced sequestration (Fig. 2). At leaf
flush, young expanding leaves are generally highly susceptible to herbivores (Coley and Barone 1996), making
rapid maturation a key defensive trait (Aide 1988). We
expect minimal induced sequestration during periods of
leaf expansion; rather, the production of new leaf tissue
and the defense of existing tissue is likely to be particularly
important to both young annuals and first-year perennial
plants as predicted by the Optimal Defense Hypothesis
(McKey 1974; van Dam et al. 1996; de Boer 1999). Once
expanded, induced sequestration rates are predicted to be
higher. We also expect higher rates of induced sequestration prior to reproduction. During seed and fruit maturation, however, we expect minimal induced sequestration
The extent of damage, herbivore specialization, mobility,
feeding guild, and gregariousness are all likely to affect the
likelihood of induced resource sequestration (Fig. 2).
Evolutionarily, species typically consumed by large
browsing mammals, for example, may maintain high constitutive storage and exhibit little induced storage. Insect
herbivores, whose populations fluctuate widely from year
to year, represent a more variable selective pressure
(Hunter 1991), and could select for an induced sequestration response. Even within insect herbivores, the benefits of
induced sequestration are likely to vary and this could lead
to the evolution of specific plant responses (Agrawal 2000).
To date, the evidence for induced sequestration comes from
plant responses to herbivorous insects. Below, we examine
how the extent of damage and characteristics of the herbivorous insect are both likely to affect patterns of resource
sequestration.
Extent of damage Ecologically, under mild or moderate
herbivore defoliation, allocation of storage should be costly
since stored resources are unavailable for investment in
new tissues. A smaller leaf area not only limits growth
rates during herbivory but would also be expected to limit
regrowth potential. In contrast, if leaf area loss eventually
leads to complete defoliation, the growth rate of leaves
during herbivore attack is irrelevant (all leaves are
removed), and the increase in stored carbon pools from
induced storage would be expected to increase the
regrowth potential. Similarly, induced storage during a
mild attack is expected to be beneficial if early season
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herbivory predicts more severe future attack or if late
season defoliation is common for and is predicted by earlyseason herbivory. In particular, if complete defoliation later
in the growing season is likely, induced storage in response
to prior attack would be beneficial. Moreover, since young
tissues are often more vulnerable to subsequent damage
than mature tissues (Denno and McClure 1983; NicholsOrians and Schultz 1990), allocation to new growth could
result in higher total leaf removal. This could shift the
balance to favor storage over continued production of new
leaves.
Specialist versus generalist species We suggest that
induced sequestration may be a more effective strategy
against specialist herbivores than induced chemical
defenses (Fig. 2). Many specialist herbivores have evolved
effective detoxification mechanisms, and even use the toxic
chemicals as feeding or oviposition cues (Macel and Vrieling 2003; Müller-Schärer et al. 2004; Hopkins et al.
2009). The failure of many chemical defenses to deter
specialist herbivores leads to the prediction that induced
sequestration would be prevalent in response to specialists.
In contrast, induced chemical defenses are quite effective
against generalists, and therefore we predict plants to
allocate more resources to defense than to storage when
attacked by generalists.
Sedentary versus mobile species For sessile herbivores,
larvae develop in the tissue on which the adult females
lay their eggs. Unless other ovipositing females are
present, the risk of attack to uninfested leaves is zero.
Moreover, it is not uncommon for these sedentary species
to aggregate (Whitham 1983; Orians and Björkman
2009). We therefore predict that damage by sedentary
herbivores will favor export of resources from the
attacked leaves (Fig. 2), although the opposite pattern
may be observed if herbivores are able to hormonally
manipulate the plant (Giron et al. 2007). Indeed, high
densities of leaf miners are known to trigger early leaf
abscission (Bultman and Faeth 1986). In contrast, mobile
herbivores often move between leaves. We therefore
expect mobile herbivores to induce export both locally
and systemically, as has been observed for gypsy moths
on Populus (Babst et al. 2008).
Gregarious versus solitary species We predict that the
ability to rapidly sequester resources into storage organs
may be an essential response to gregarious herbivores
(Fig. 2). In fact, the propensity to aggregate is the one
factor repeatedly associated with insect species that commonly reach outbreak densities and cause extensive defoliation (Nothnagle and Schultz 1987; Larsson et al. 1993;
reviewed by Hunter 1991). Moreover, gregarious species
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Oecologia (2011) 167:1–9
are often the most frequently observed herbivores on their
host plants (Björkman et al. 2000; Carson and Root 2000;
Dalin 2006). Solitary species, in contrast, are less likely to
become numerically dominant and often exhibit conspecific avoidance and even experience higher mortality rates
when aggregated (Jones 1987; Eber 2004). This will tend to
limit the magnitude of damage, unless individual herbivores are large (e.g., later instars of some insect species
such as Manduca sexta). Induced sequestration may be
critical to regrowth following attack by gregarious species
whereas for solitary species it would more likely represent
an opportunity cost.
Feeding guild To date, studies documenting induced
sequestration have used leaf-chewing herbivores as models, either by releasing herbivores on the plants, inducing
them with regurgitants/salivary cues, or by treating plants
with jasmonates. To our knowledge, no studies have
examined the effects of mammalian browsers or piercing/
sucking insects such as aphids, whiteflies, adelgids and
scale insects. Several lines of evidence suggest that induced
sequestration will be limited in response to both. Browsers
can rapidly defoliate an entire plant and thus there would
be little time to respond. Although piercing/sucking insects
do not cause defoliation, we still expect little induced
sequestration. By feeding directly from the phloem, they
cause less tissue damage, and thus tend to cause little or no
induction (Walling 2000, 2008). Some even silence plant
defense responses (Walling 2008). Still other piercing/
sucking insect species are able to hormonally manipulate
the plant and thus actually increase sink strength within the
attacked tissues (Giordanengo et al. 2010).
Communities of attackers: from aboveground to belowground The adaptive value of induced sequestration of
carbohydrates in the roots and stems depends on the
security of this pool of storage reserves (Fig. 2). Despite
the benefits that resource sequestration can confer to plants
in response to herbivory, exporting resources to storage
organs can have far-reaching consequences that may not
always have a positive effect on plant performance. Plants
are simultaneously attacked above- and belowground by a
myriad of herbivores and pathogens (Masters et al. 1993;
Van der Putten et al. 2001; Blossey and Hunt-Joshi 2003;
Dicke 2009; Kaplan et al. 2009). Therefore, the presence of
root attackers could represent a major cost to export of
material from the leaves by providing additional resources
to root herbivores and pathogens (Kaplan et al. 2008).
Similarly, stem-borers could also exploit the sequestered
resources. Thus, the success of exporting aboveground
resources into stems or roots as a strategy to safeguard
valuable resources will depend on the herbivore/pathogen
pressure on those tissues.
Oecologia (2011) 167:1–9
Conclusions
There is increasing evidence showing that plants increase
their allocation to storage tissues in response to herbivory.
All else being equal, however, allocation to storage represents an allocation cost since investment in new growth
would increase plant size and ultimately reproductive
potential. Yet certain conditions are more or less likely to
favor such a strategy. We have argued that greater attention
to the ecological context is needed before testing when and
where induced sequestration is likely to be common and to
evaluate its adaptive value. In Fig. 2, we have outlined
several conditions predicted to favor induced sequestration
and other conditions that make such a strategy less likely.
The balance of these forces is expected to determine the
magnitude of induced storage in a given species or population. We hope this paper stimulates further research into
the benefits, costs and mechanisms of this phenomenon.
Acknowledgments We thank the anonymous reviewers for their
valuable comments on the manuscript. The project was supported by
the National Research Initiative (or the Agriculture and Food
Research Initiative) of the USDA National Institute of Food and
Agriculture, grant number # 2007-35302-18351.
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