Proc. R. Soc. B (2012) 279, 4183–4191
doi:10.1098/rspb.2012.1315
Published online 15 August 2012
Predation risk, stoichiometric plasticity and
ecosystem elemental cycling
Shawn J. Leroux1,†, Dror Hawlena2 and Oswald J. Schmitz3,*
1
Department of Biology, University of Ottawa, Ottawa, Ontario, Canada K1N 6N5
Department of Ecology, Evolution and Behavior, The Alexander Silberman Institute of Life Sciences,
Hebrew University of Jerusalem, Givat Ram, Jerusalem 91904, Israel
3
School of Forestry and Environmental Studies, Yale University, New Haven, CT 06511, USA
2
It is widely held that herbivore growth and production is limited by dietary nitrogen (N) that in turn constrains ecosystem elemental cycling. Yet, emerging evidence suggests that this conception of limitation
may be incomplete, because chronic predation risk heightens herbivore metabolic rate and shifts
demand from N-rich proteins to soluble carbohydrate – carbon (C). Because soluble C can be limiting,
predation risk may cause ecosystem elemental cycling rates and stoichiometric balance to depend on herbivore physiological plasticity. We report on a stoichiometrically explicit ecosystem model that investigates
this problem. The model tracks N, and soluble and recalcitrant C through ecosystem compartments.
We evaluate how soluble plant C influences C and N stocks and flows in the presence and absence of
predation risk. Without risk, herbivores are limited by N and respire excess C so that plant-soluble C
has small effects only on elemental stocks and flows. With predation risk, herbivores are limited by soluble
C and release excess N, so plant-soluble C critically influences ecosystem elemental stocks flows.
Our results emphasize that expressing ecosystem stoichiometric balance using customary C : N ratios
that do not distinguish between soluble and recalcitrant C may not adequately describe limitations on
elemental cycling.
Keywords: carbon cycling; ecosystem functioning; nitrogen cycling; herbivore physiological stress;
predation risk; stoichiometric balance
1. INTRODUCTION
Elemental cycling is a fundamental ecosystem process that
determines rates of primary and secondary production,
food chain length, trophic biomass and species diversity
[1–3]. The classical view of ecosystem functioning holds
that microbial species are the most critical driver of elemental cycling owing to their capacity to convert organic
matter into mineral elements for plant uptake and production, and that plants and animals act as reservoirs that
store and release those elements. Thus, rates of elemental
cycling and hence primary and secondary production are
presumed to be controlled largely by microbial action.
This classic view has been challenged with the rise of ecological stoichiometry [4,5], a more organismal-based field
that aims to understand how elemental cycling and balance
is affected by plant and animal species and their interactions
with each other in ecosystems. Much current stoichiometric
theory holds that elemental cycling within ecosystems is primarily controlled by elemental transfer between plants and
herbivores owing to a mismatch between plant elemental
supply and herbivore elemental demand for maintenance
and production [4–6]. Plant species and parts are characterized by highly variable carbon (C): nitrogen (N):
phosphorus (P) ratios with a relatively high abundance of
low quality tissues, i.e. tissues with high C : N or C : P
* Author for correspondence ([email protected]).
†
Present address: Department of Biology, Memorial University of
Newfoundland, 232 Elizabeth Ave, St John’s, NL, Canada A1B 3X9.
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rspb.2012.1315 or via http://rspb.royalsocietypublishing.org.
Received 7 June 2012
Accepted 23 July 2012
ratios [5,7,8]. Consumers, on the other hand, should regulate body elemental composition within strict, low C : N or
C : P levels—known as homeostasis—to maximize survival,
growth and reproduction [4,9]. This has lead to the widespread idea, at least for terrestrial systems, that C occurs
in excess, whereas N and P are limiting and hence constrain
elemental cycling rates [3–5,10].
Several lines of recent empirical evidence suggest, however, that the above reasoning may give an incomplete
picture of controls over elemental cycling. First, empirical
synthesis shows that there may be considerable intraspecific phenotypic plasticity in consumer body elemental
composition [11,12], meaning that there may not be
strict, homeostatic elemental requirements in many
species. Second, elements do not flow freely, but rather
are bound up with other elements to form macronutrients
such as proteins, lipids and carbohydrates [13,14]. In terrestrial systems especially, plants contain two broad forms
of organic compounds: soluble, aka labile (e.g. soluble glucose, dextrin, sucrose) and recalcitrant (e.g. cellulose
lignin, and fibre from plant support and anti-herbivore
defence tissues). Thus, although those plants have high
overall C content, soluble organic compounds, such as
carbohydrate used to fuel consumer energetic demands,
may be limiting in comparison with the large proportion
of their recalcitrant organic matter content [13–15].
Third, the tendency in ecosystem ecology to focus on transfer just at the plant–herbivore interface means that other
important direct and indirect effects and feedbacks
caused by interactions among species within the broader
food web are not taken into consideration [15–19].
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Predator control of elemental cycling
Specific to our case here, herbivores occupy intermediate
levels within food chains and thus must often engage in
behaviours that trade-off plant nutrient consumption
against perceived predation risk to maximize fitness. Such
trade-off behaviour can trigger a cascade of effects that
influence ecosystem functioning [17,20,21]. Perceived predation risk can precipitate such effects, because it induces
chronic stress in herbivore prey to increase the probability
that prey individuals will survive a predator attack [22,23].
Predator-induced physiological stress responses may
affect ecosystem elemental cycling in two ways, especially
if soluble carbohydrate is in limiting supply. It elevates
prey metabolic and respiration rate and accordingly
energy demand, causing herbivores to shift preferences
from N-rich proteins that support production (growth
and reproduction) to carbohydrate – C to fuel the elevated
metabolism and respiration [22 – 24]. Predation risk can
also alter the efficiency and rate of elemental transfer
between trophic levels in ecosystems because C is respired rather than converted to secondary production
[19,22,23,25]. Furthermore, given that the amount of
energy used for production correlates positively with N
demand, and that herbivores have limited ability to
store excess nutrients, stressed herbivores should also
excrete N [23]. Ultimately, prey stressed by predation
risk should increase their body C : N ratio [22,23].
Indeed, a prey body C : N difference of as little as 4 per
cent between risk and risk-free conditions can perturb
below-ground community function enough to alter subsequent organic matter decomposition and nutrient
cycling by 60 – 200%—a large legacy effect of predation
risk [26].
Accordingly, adaptive plasticity in herbivore physiology
and elemental composition owing to the presence and
absence of predation risk may cause important contextdependency in elemental cycling within ecosystems [23],
and perhaps may explain context-dependent effects
in response to other environmental stressors such as
environmental warming [27]. Yet, how such evolutionary
ecological processes at the individual organismal level
scale to whole ecosystem functioning remains altogether
unexplored by analytical tools. To this end, we derive a stoichiometrically explicit food chain model and use this model
to analyse how predation risk may influence ecosystem
elemental cycling through changes in prey physiological
demand for and use of C and N.
Our work contributes to emerging theory aimed at
understanding how species, especially animals, regulate
ecosystem functioning through physiological effects that
determine the nature of their trophic interactions in
food webs [1,2,18,27 –31]. This general class of theory
recognizes that fundamental consumer demands for
elements drive survival, growth and reproduction. But,
since its original conception [1], analytical theory has
been developed using two classes of approach. The first
class [27,29 – 31] explores how variation in the degree of
nutrient limitation and trophic interactions among species
affects the temporal dynamics of consumer population
abundances. The second class [2,18,28] explores how
trophic interactions influence the temporal dynamics of
elemental pool sizes within ecosystem compartments
that have a species designation (e.g. primary producer,
herbivore, carnivore, etc.). Because our interest here is
to develop models of species interactions that inform
Proc. R. Soc. B (2012)
how environmental context influences ecosystem elemental
cycling, we have opted to build on the second class of
approach by infusing mechanistic organismal physiological
considerations into an ecosystem compartment formalism.
We address three general questions: (i) whether the
evolutionary ecology of species interactions can influence
ecosystem functioning [21]; (ii) whether changing
resource quality controls nutrient flows among ecosystem
compartments within the same ecosystem context of
nutrient input and flux [32]; and (iii) whether or not
food-web structure—i.e. presence of top predators
within an ecosystem—influences ecosystem functioning
by inducing changes in the quality (i.e. elemental C : N
contents) of their prey species [4,23,33].
2. MODEL DESCRIPTION
(a) Mechanism for plasticity
Current stoichiometric analyses of ecosystem elemental
cycling hold that foodweb structure does not influence
prey body C : N contents, because prey must maintian
relatively tight homeostatic body C : N ratios to survive
and reproduce [4]. This view, however, assumes that
predator effects on prey are entirely consumptive [33].
However, the mere spectre of predation may elicit fear
responses in prey leading to physiological stress that can
be manifest as increased metabolism and respiration, and
synthesis of heat shock proteins that together elevate maintenance energy demands [22,34–36]. In nutrient-limited
systems, especially those with highly limiting soluble C,
such increased maintenance costs reduce energy-C (i.e. soluble C-based energy) available for growth and reproduction
because of the need to allocate finite resources among the
competing demands of maintenance and production [37].
Hence, to meet heightened maintenance demands, stressed
herbivores should reallocate energy-C from production
to maintenance as well as increase their consumption of
energy-C [22]. The amount of energy-C available for production correlates positively with protein–N demand.
Because consumers have limited ability to store excess
nutrients, threshold elemental ratio theory predicts that
reallocation of energy-C from production to maintenance
should cause N to be excreted [22,23,38]. Moreover,
chronically heightened stress hormone levels increase the
breakdown of body proteins to produce glucose, and
hence may exacerbate nitrogen excretion [39] that in turn
should increase herbivore body C : N ratios [22,26].
(b) General model structure
Our stoichiometrically explicit model builds on the general framework of Daufresne & Loreau [28,40]. The
model tracks N, and soluble and recalcitrant forms of C
through explicit compartments within herbivore and primary producer trophic levels, and soil pools (figure 1
and table 1). In real ecosystems, nutrients and elements
also flow through predator and decomposer trophic
levels [1,2,23]. However, as a starting approximation to
motivate explicit thinking about herbivore physiological
plasticity and nutrient cycling, we do not explicitly
model flows through these two trophic levels. Because
we are interested here in the novel pathway of riskinduced plasticity in elemental stoichiometry, we treat
the presence and absence of predators only as a perturbation to elemental flows mediated by herbivore
Predator control of elemental cycling
pbqH + WCH[NH, CSH]
(1 – p)bqH
CSH
(1 – y)aFH
herbivores
NH
qH +
WNH[NH, CSH]
FH
yaFH
(1 – y)aFP
CRP
CSP
yaFP
primary
producers
yaqP
(1 – y)aqP
CR
qP
NP
FP
CS
N
I
gR
gS
soil
nutrient
pools
k
Figure 1. Stoichiometrically explicit model of a terrestrial
herbivore–plant –soil nutrient ecosystem. The model tracks
the pools of nitrogen (N ), soluble carbon (CS) and recalcitrant carbon (CR). Under predation risk, herbivores have
increased metabolism (higher C : N ratio) and therefore,
actively seek plants with higher ratio of soluble carbon (e.g.
sugars). We investigate stoichiometric plasticity in plants
and herbivores by analysing models with and without predation risk and variable quantities of plant-soluble C. Solid
lines are flows of N, dashed lines are flows of CS and
dotted lines are flows of CR. See main text for full model
description and parameter definitions.
physiological stress responses, and thus do not permit predator consumptive effects. Moreover, evidence suggests that
chronic predation risk effects alone can dominate ecosystem functioning despite the occurrence of predator
consumptive effects [17,20,21]. We describe flows through
decomposer pools by recognizing that the rate of microbial
decomposition is often dependent upon the availability
of soluble C in detritus [41]. Specifically, we emulate
decomposition using a function that links the amount
of soluble C released from plants and herbivores to the
soil pool (i.e. microbial activity) to the rate at which N
builds up in the soil pool and is available for plant uptake
(see §2b(i)).
The model couples C and N cycles. The carbon is
separated into two components: a proportion that is soluble
(c; CS) and a proportion that is recalcitrant (1 2 c; CR).
We separate carbon into soluble and recalcitrant components, because these two types of carbon are often
differentially cycled within ecosystems [18,27,42,43]. We
assume that primary producers take up inorganic nitrogen
and produce soluble and recalcitrant carbon from the
photosynthesis of atmospheric carbon (i.e. CO2). The primary producer community combines carbon and nitrogen
into its own biomass and recycles carbon and nitrogen to
the soil pools at a constant CiP : NP ratio, a [28,40]. We
model the primary producer community as homeostatic,
Proc. R. Soc. B (2012)
S. J. Leroux et al.
4185
but we allow for stoichiometric plasticity by modifying
the proportion of plant C that is soluble (c; see §2b(iii)).
Herbivores take up nitrogen and soluble carbon and combine these two elements into their own biomass at a
constant CSH : NH ratio, b [40]. We model herbivores as
homeostatic, but investigate stoichiometric plasticity by
allowing b to vary according to herbivore physiological
state (i.e. not stressed versus stressed, see §2b(iv)). Recalcitrant carbon ingested by herbivores is typically in the form
of indigestible fibre and lignin, which, we assume, based on
analyses of herbivore feeding and nutrition, is egested [7].
Herbivores are assumed to recycle nitrogen through baseline egestion, excretion [44,45] and natural mortality uH
[33,46], and by egestion and excretion through differential
assimilation to maintain homeostasis, WNH[NH, CSH]
[23,47]. Herbivores also recycle soluble carbon (buH) at a
constant CSH : NH ratio, b. A portion ( p) of the recycled
soluble carbon is naturally respired by herbivores; we
assume the remainder (1 2 p) is recycled to the soil-soluble
carbon pool [33,46]. We assume that herbivores also
respire CSH, if in excess, to maintain homeostasis,
WCH[NH, CSH] [48]. Additionally, organic nitrogen (e.g.
predator, decomposer carcasses) is supplied to the system
by assuming a constant and independent source, I [33],
and is lost from the system through a leaching flux, k.
Soluble and recalcitrant carbon is lost from the soil
carbon pools through respiration and leaching (gi) [43].
The dynamic equations for this ecosystem are defined in
table 1 and represented in figure 1. See the electronic supplementary material, appendix S1 for variable, parameter
as well as function definitions and dimensions.
(i) Nitrogen mineralization
Nitrogen is recycled from the primary producer and herbivore communities in organic form. Nitrogen is mineralized
in proportion to the quantity of soluble carbon (CS) in the
soil carbon pool according to FP ¼ f(CS, N) ¼ aPCSN,
where aP is the nitrogen mineralization rate [43,49–51].
Mineralized (inorganic) nitrogen is then taken up by
plants. Nitrogen mineralization governs soil respiration of
soluble carbon [43]. Specifically, the respiration of CS is a
function of the quantity of soil nitrogen (N) according
to gS ¼ f(CS, N) ¼ qSCSN, where qS is the soil-soluble
carbon respiration rate.
(ii) Herbivore uptake
We assume that herbivore nitrogen uptake follows
simple Lotka–Volterra dynamics FH ¼ aHNPNH, where
aH is the herbivore nutrition rate for N [40]. Specifically,
aH is a proportionality constant relating the amount of
nitrogen taken from plants per unit nitrogen in herbivores
per unit time (the electronic supplementary material,
table S1 and appendix S1). Other models typically describe
herbivore uptake using saturating functions [17,30]. However, those models describe uptake of plant biomass and
assume complete assimilation of elements (i.e. assumes
all elements are soluble or labile), some of which are later
excreted. We instead model elemental assimilation as an
emergent property of the proportion of recalcitrant and soluble C in the diet, and hence differential egestion of C. That
is, reduced soluble N and C assimilation rate per unit plant
matter ingested emerges when recalcitrant C comprises a
high proportion of the herbivore diet.
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Predator control of elemental cycling
Table 1 Stoichiometrically explicit model of a terrestrial herbivore– plant– soil nutrient ecosystem with function and parameter
definitions. See figure 1 for a conceptual diagram of the ecosystem model.
model equations
description
soil nutrients:
dN
¼ I gN þ uP þ uH þ WNH ½NH ; CSH FP ;
dt
dCS
¼ cauP þ bð1 pÞuH gS
dt
dCR
þ ð1 cÞauP þ ð1 cÞaFH gR :
dt
plants:
dNP
¼ F P u P FH ;
dt
dCSP
¼ caFP cauP caFH
dt
dCRP
¼ ð1 cÞaFP ð1 cÞauP ð1 cÞaFH
dt
herbivores:
state variables: Ni, nitrogen stock in trophic level i; CSi, soluble
carbon stock in trophic level i; CRi, recalcitrant carbon stock in
trophic level i
dNH
¼ FH ðuH þ WNH ½NH ; CSH Þ
dt
dCSH
¼ caFH ðbuH þ WCH ½NH ; CSH Þ:
dt
functions: gi, flux of element i lost from soil nutrient pool; ui,
nitrogen flux recycled by trophic level i; WNH[NH, CSH],
herbivore differential assimilation rate of nitrogen; WCH[NH,
CSH], herbivore differential assimilation rate of soluble carbon;
FP, nitrogen flux from the soil nutrient pool to plants; FH,
nitrogen flux from plants to herbivores
function definitions: gN ¼ kN; gS ¼ f(CS, N ) ¼ qSCSN; gR ¼ qRCR;
uP ¼ rPNP; uH ¼ rHNH; FP ¼ aPCSN; FH ¼ aHNPNH;
b ca
WNH [NH ; CSH ] ¼
FH ; WCH [NH ; CSH ] ¼ (ca b)FH
b
parameters: I, independent nitrogen input rate to the soil nutrient
pool; k, nitrogen loss rate from soil nutrient pool; qS, soluble
carbon loss rate from soil nutrient pool; qR, recalcitrant carbon
loss rate from soil nutrient pool; aP, nitrogen mineralization rate;
aH, herbivore nutrition rate; ri, nitrogen-recycling rate of trophic
level i; p, proportion of soluble carbon respired by herbivores; c,
proportion of plant carbon that is soluble; a, CP: NP ratio; b,
CSH: NH ratio
(iii) Plant CSP : CRP : NP regulation
Primary producers exhibit great plasticity in their C : N
ratios [23,38]. We model plants as homeostatic, but investigate stoichiometric plasticity in plants by modifying
the proportion of plant C that is soluble (i.e. c) according
to threshold elemental theory [23,38]. By modifying the
proportion of plant C that is soluble, we emulate diversity
in plant resource quality (i.e. plant CS : N ratio). This
allows us to disentangle the dynamical feedbacks between
trophic interactions (i.e. predation risk and herbivory)
and resource quality and their corresponding effect on ecosystem elemental fluxes. Plant homeostasis implies that
dCSP =dt ¼ caðdNP =dtÞ and dCRP =dt ¼ ð1 cÞa(dNP =
dtÞ. Plant homeostasis is governed by the control of
nutrient uptake [52], and we model this by making the
inflow of CSP and CRP to plants equal to the inflow of NP
multiplied by the plant a.
(iv) Herbivore CSH : HH regulation
Herbivores take up but do not assimilate recalcitrant
carbon (CRP) typically found as fibre and lignin in
plants [7]. Consequently, the recalcitrant carbon taken
up by herbivores is egested with a similar ratio as that
found in plants, a. This implies that herbivores selectively
extract soluble carbon (CSP) and nitrogen (NP) from
plant matter according to the plant ratio, a. Herbivore
homeostasis implies that dCSH =dt ¼b(dNH =dtÞ:
When there is no predation risk, herbivores take up
nitrogen to fuel their growth and maintenance and they
respire the excess CSH taken up in their diet [22]. Consequently, with no predation risk, WNH[NH, CSH] ¼ 0.
Substitution of equations dCSH/dt and dNH/dt with
WNH[NH, CSH] ¼ 0 provides the flux of CSH respired
by herbivores with no predation risk to maintain homeostasis, WCH[NH, CSH] ¼ (ca 2 b)FH. Consequently,
without predation risk, ca . b.
Proc. R. Soc. B (2012)
To investigate the effect of predation risk on ecosystem
function we do not explicitly model the dynamics of predators, we simply modify the CSH : NH ratio of herbivores
such that brisk . bno risk (see §2a). Herbivores usually
maintain homeostasis by differential assimilation, so that
they release the element in surplus contained in the
food they ingest [28,53]. Under predation risk, we
assume that herbivores seek out soluble carbon to fuel
their increased metabolism and therefore excrete excess
NH [22]. Consequently, under predation risk, WCH[NH,
CSH] ¼ 0. Substitution of equations dCSH/dt and dNH/
dt with WCH[NH, CSH] ¼ 0 provides the flux of NH
excreted by herbivores under predation risk to maintain
homeostasis, WNH (NH ; CSH ) ¼ ððb caÞ=bÞF H . Thus,
under predation risk, b . ca.
Empirical evidence suggests that herbivore respiration
( p) is heightened under predation risk (reviewed in
Hawlena & Schmitz [23]). Therefore, we investigate
not only the consequences of differential elemental
uptake by herbivores, but also the effect of increased
herbivore respiration as a secondary mechanism for
herbivore physiological plasticity under predation risk.
Note that models with and without predation risk
respect empirical evidence that plants always have
higher C : N than herbivores, i.e. a . b (5). With predation risk, however, ca , b. ca can be thought of as the
functional C : N ratio of plants or more precisely the
CS : N of plants. Consequently, under predation risk,
the CS : N of herbivores is larger than the CS : N of
plants but the overall C : N of herbivores is lower than
the overall C : N of plants.
(c) Model analysis
We obtained a general solution for our models by setting
the time derivatives to zero and solving the system of
equations in table 1 for non-trivial equilibria. We analysed
Predator control of elemental cycling
nutrient stocks
(i) (a)
1.2
(b)
0.6
(c)
3
0.8
0.4
2
0.4
0.2
1
0
0
0
1.2
0.4
0.6
S. J. Leroux et al.
4187
nutrient stocks
(ii)
0.3
0.4
0.8
0.2
0.4
0.2
0.1
0
0
0.45 0.50 0.55 0.60 0.65 0.70
proportion of plant
C that is soluble
0
0.45 0.50 0.55 0.60 0.65 0.70
proportion of plant
C that is soluble
0.45 0.50 0.55 0.60 0.65 0.70
proportion of plant
C that is soluble
Figure 2. Stocks of nitrogen (circles), soluble carbon (squares) and recalcitrant carbon (triangles) in (a) soils, (b) plants, and
(c) herbivores for an increasing proportion of plant carbon that is soluble (c). Results are for models with predation risk ((i),
b ¼ 0.85) and for models without predation risk ((ii), b ¼ 0.5). Note different scales on y-axis. Other parameter values are
aP ¼ aH ¼ 1.15, I ¼ 0.5, rP ¼ rH ¼ 0.3, qS ¼ qR ¼ k ¼ 0.5, p ¼ 0.5, a ¼ 1.15. Qualitative results are not sensitive to particular
parameter values. See the electronic supplementary material, appendix S3 for analytic results.
3. RESULTS
(a) Effects of plant CS : CR ratio and predation risk
on ecosystem stocks
For 1 . p . 0 and positive values for all other parameters, the ecosystem without predation risk persists if
qS =bð1 pÞ . aP . qS =ca or qS =bð1 pÞ , aP , qS =
ca; whereas the ecosystem with predation risk persists if
qS =cað1 pÞ . aP . qS =ca. The electronic supplementary material, appendix S2 provides the equilibrium
solutions for ecosystem stocks in models with and without
predation risk.
In an ecosystem without predation risk, variation in
the proportion of soluble versus recalcitrant carbon but
with identical overall C : N ratio leads to minor changes
in soil nutrient pools. An increase in the proportion
of plant C that is soluble produces a slight increase
in the soil and herbivore carbon stocks but no effect on
the soil and plant N stocks (figure 2). Herbivore nitrogen
stocks increase with the CSP : CRP ratio of plants via
Proc. R. Soc. B (2012)
2.0
herbivore stocks
equilibrium conditions for the herbivore–plant– soil
nutrient ecosystem model with and without predation
risk. We investigate the behavioural modifications due to
predation in ecosystems with plants with high and low
relative quantities (i.e. c) of CSP and CRP under a range
of herbivore respiration rates ( p). We investigated the influence of the proportion of soluble carbon c on ecosystem
stocks and fluxes by taking the partial derivative of nutrient
stocks and fluxes with respect to c. Likewise, we investigated the influence of heightened herbivore respiration
rates p under predation risk on ecosystem stocks and
fluxes by taking the partial derivative of nutrient stocks
and fluxes with respect to p. We illustrate our analytical
results for specific parameters in figures 2–4 and the
electronic supplementary material, figures S4a and S5a.
1.5
1.0
0.5
0.65
0.60
op
or
0.55
tha tion
0.50
t i of
ss p
olu lan
ble t C
0.80
pr
0.70
0.50
n
atio
pir
0.60
res
e
r
o
biv rate
her
Figure 3. Herbivore stocks (measured as nitrogen in herbivore trophic level) under predation risk for increasing
proportion of plant C that is soluble (c) and increasing herbivore respiration rate ( p). Parameter values are b ¼ 0.85,
a ¼ 1.15 and all other parameters are as defined in figure 2.
an indirect effect of nitrogen mineralization in soils
which depends on soil-soluble carbon (figure 2 and the
electronic supplementary material, appendix S3).
The role of soluble plant C in driving ecosystem
dynamics dramatically changes when we include herbivore
physiological plasticity under predation risk (figure 2 and
the electronic supplementary material, appendix S3).
Now herbivores become soluble-C limited and they excrete
the excess N from their diets. We predict a large increase in
herbivore N and soluble-C stocks and a corresponding
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Predator control of elemental cycling
(a)
(b)
0.5
(c)
0.5
0.4
0.4
0.3
0.3
0.4
0.2
0.2
0.2
0.1
0.1
recycling flux
1.0
0.8
0.6
0
0.45 0.50 0.55 0.60 0.65 0.70
0
0.45 0.50 0.55 0.60 0.65 0.70
proportion of plant C
that is soluble
proportion of plant C
that is soluble
0
0.45 0.50 0.55 0.60 0.65 0.70
proportion of plant C
that is soluble
Figure 4. (a) Total flux of nitrogen, (b) soluble carbon and (c) recalcitrant carbon recycled to the soil nutrient pools. Results are for
models with predation risk (open symbols, b ¼ 0.85) and without predation risk (filled symbols, b ¼ 0.5). We show results under
predation risk for three levels of herbivore respiration ( p ¼ 0.5 (solid lines), 0.6 (dashed lines), 0.7 (dotted lines)). All other
parameters are as defined in figure 2. See the electronic supplementary material, appendix S3 and S5 for analytical results.
decrease in plant recalcitrant C stocks with an increase in
the proportion of plant C that is soluble. With more plant
C that is soluble, herbivores need to recycle less N to maintain homeostasis. This reduction in herbivore N recycling
leads to stronger regulation of plant nutrient stocks and a
decrease in plant N stocks (figure 2). An increase in
plant-soluble C also leads to a large increase in soluble
and recalcitrant C soil stocks but no effect on the N soil
stock. These results emphasize a potentially important
role of predators for carbon sequestration in ecosystems
dominated by plants with a high proportion of soluble C.
Overall, herbivore N stocks are predicted to be larger in
ecosystems with predation risk than without predation risk
(see the electronic supplementary material, figure S4a and
appendix S4). Herbivore N stocks in ecosystems with and
without predation risk also are larger when there is a higher
proportion of plant C that is soluble (see the electronic
supplementary material, figure S4a and appendix S4).
Plant stocks are not influenced by heightened herbivore
respiration under predation risk but herbivore and soil
nutrient stocks decline under increased herbivore respiration (see the electronic supplementary material, table
S5a and appendix S5). Consequently, the effects of an
increase in the proportion of plant C that is soluble on ecosystem stocks are dampened by heightened herbivore
respiration under predation risk (figure 3 and the electronic
supplementary material, figure S5a and appendix S5).
(b) Effects of plant CS : CR ratio and predation risk
on ecosystem elemental fluxes
In an ecosystem without predation risk, whole ecosystem elemental fluxes are N ¼ uP þ uH, CS ¼ cauP þ
(1 2 p)buH þ WCH[NH, CSH], CR ¼ (1 2 c)auP þ (1 2
c)aFH. Without predation risk, ecosystem fluxes of N, soluble C and recalcitrant C increase monotonically with an
increase in the proportion of plant C that is soluble
(figure 4 and the electronic supplementary material,
appendix S3).
In an ecosystem with predation risk, whole ecosystem
elemental fluxes are N ¼ uP þ uH þ WNH[NH, CSH],
CS ¼ cauP þ (1 2 p)buH and CR ¼ (1 2 c)auP þ (1 2
c)aFH. Now, ecosystem fluxes of N increase significantly
with an increase in the proportion of plant C that is
soluble, whereas ecosystem fluxes of soluble C and recalcitrant C show more modest increases. Fluxes of nitrogen
Proc. R. Soc. B (2012)
and carbon decline with increased herbivore respiration
under predation risk (see the electronic supplementary
material, table S5b and appendix S5), because the negative relationship between percentage soluble C and
respiration rate (figure 3) means that increased respiration
can dampen any increase in ecosystem fluxes due to
higher availability of soluble plant-C (figure 4 and the
electronic supplementary material, appendix S5).
4. DISCUSSION
A fundamental assumption of ecological stoichiometry is
that C reflects all carbohydrate-based energy. As a result,
the majority of ecological models, even stoichiometrically
explicit ones, do not distinguish between different carbohydrate-C sources [5]. This is in spite of substantial
variation in the molecular structure of those compounds
(e.g. glucose versus hemicelluloses), and hence in a
consumer’s ability to use them. Moreover, growing
empirical evidence demonstrates that disregarding variation in digestibility of different organic compounds
may mask important ecosystem dynamics. We included
a simple representation of this variation in a consumer’s
ability to use different organic compounds by modelling
soluble and recalcitrant C as separate pools (figure 1).
Changes in the relative quantity of soluble versus recalcitrant C in plants influence mineralization, recycling and
photosynthesis in our model. In an ecosystem with
predation risk, plant-soluble C influences herbivore
differential assimilation which has cascading effects on
ecosystem elemental stocks and fluxes (figures 2 and 4).
Specifically, an increase in the proportion of plant C
that is soluble leads to a large increase in herbivore and
soil nutrient stocks and whole ecosystem elemental
fluxes in ecosystems with predation risk. However, this
increase in ecosystem stocks and fluxes is dampened if
herbivores experience heightened respiration owing to
predation risk (figures 3 and 4). In ecosystems without
risk, an increase in the proportion of plant C that is soluble leads to relatively modest increases in ecosystem
stocks and fluxes (figures 2 and 4). The positive effect
of an increase in the proportion of plant C that is soluble
occurs, because herbivore nitrogen stocks increase with
the CSP : CRP ratio of plants via an indirect effect of nitrogen mineralization in soils that depends on soil-soluble
Predator control of elemental cycling
carbon (figure 2). This is consistent with an established
body of literature that demonstrates N availability and
not C-energy is driving ecosystem processes and properties in ecosystems comprised of soil, plant and herbivore
trophic compartments but without considerations of predation or predation risk [5]. Collectively, these results
answer our three initial questions in the affirmative,
namely that (i) the evolutionary ecology of species interactions (i.e. adaptive physiological response to stress)
can influence ecosystem functioning by changing;
(ii) the way resource quality controls nutrient flows
among ecosystem compartments of an ecosystem, and
that such effects do depend on (iii) food-web structure, in
particular, the presence of top predators within an ecosystem influences ecosystem functioning by inducing changes
in the quality (i.e. elemental C : N contents) of their prey.
This shows further that consumer-mediated recycling can
be a key mechanism determining the nature of cascading
trophic effects within ecosystems [26,33,44,54].
Our results demonstrate the need for caution in interpreting findings that are based on the commonly used
C : N ratio. This index is based on the assumption that
N is the limiting element in consumer diets and hence
that lower C : N ratio reflects a better diet. This does
not consider physiological and resource choice plasticity
in herbivores under predation risk and that soluble
carbon can be a limiting nutrient in ecosystems. Moreover, in some cases, herbivores may be chronically
limited by non-protein energy and the impaired performance owing to this limitation forces them to ingest a
surplus of N in which case high dietary N again does
not reflect higher dietary quality [55,56]. Thus, our
model highlights the diverse effects of energy-C limitation
on ecosystem function and shows that a simplistic index
that does not distinguish between soluble and recalcitrant
C may not be adequate to reflect the structure and
dynamics of ecosystems.
We modelled non-consumptive effects of predation as
a cost function in which physiological adjustment to
escape predation increases respiration and metabolic
demands for soluble-C and consequently alters herbivore
nutrient (elemental) balance. To maintain homeostasis
herbivores may shift their diet to match these new requirements. As a result, under predation risk, herbivores
actively use a food source richer in soluble C, and this
food source can support larger herbivore biomass [22].
This leads to the counterintuitive result that predation
risk can actually increase herbivores biomass (figure 2
and the electronic supplementary material, figure S4a).
However, if the physiological stress of predation risk
leads to higher herbivore respiration, the magnitude of
increase in herbivore biomass will also be reduced (figure
3 and the electronic supplementary material, figure S5a
and appendix S5). Similarly, consumptive effects of predators, which we have not included in our model, can
regulate herbivore populations and dampen the positive
effect of predation risk and herbivore physiological plasticity on herbivore biomass (S. J. Leroux, D. Hawlena
and O. J. Schmitz 2012, unpublished results).
An increase in soluble carbon in plants also has an
additional indirect positive feedback on herbivore biomass, because predation risk is predicted to increase
nitrogen-recycling flux and hence the productivity
that can ultimately support larger herbivore biomass
Proc. R. Soc. B (2012)
S. J. Leroux et al.
4189
(figures 2 and 4). Indeed, this predicted effect of predation risk on N cycling has been observed in field
experiments involving a hunting spider predator, a dominant grasshopper herbivore and a variety of grasses and
forbs, where treatments in which the grasshoppers faced
predation risk had soil N-cycling rates that were double
that of risk-free conditions [57]. This intriguing result
emphasizes the need for more empirical research to test
whether elemental feedbacks between above- and belowground processes, and herbivore biomass-C, are indeed
mediated by a key mechanism in which herbivore
response to predation risk is manifest as a trade-off
between availability of environmental-soluble carbon for
energy offset by heightened respiration (figure 3). Our
model also treats nitrogen mineralization as a simple
linear donor control function of soil-soluble C and N
but future work should investigate the effect of more
complex mineralization functions on ecosystem function.
The effect of perceived predation risk is larger in
environments in which a lower proportion of the plant
carbon is invested in structural compounds (figures 2–4).
Consequently, we predict more dramatic effects of predation risk on ecosystem function in aquatic environments
in which plants have much lower proportions of structural
compounds (i.e. recalcitrant carbohydrates such as cellulose and lignin). Similarly, our model predicts dramatic
consequences of predation risk in terrestrial systems
characterized by plants with lower proportions of structural
compounds (e.g. grassland) relative to the effect of predation risk expected in ecosystem characterized by woody
plants (e.g. temperate forest).
Systems with low proportions of structural carbohydrates may also be most prone to the biggest changes
in ecosystem function as a result of predator extirpation.
We predict that loss of apex predators in these systems
will lead to reductions in nitrogen and soluble carbon
fluxes with potential cascading effects on food-web
structure (i.e. lower herbivore biomass).
The kinds of effects we describe may not apply solely
to cases of perceived predation risk. Indeed, animals
show similar physiological responses when facing other
life-threatening stressors such as drought, competition
and environmental warming, because the physiological
machinery driving the stress responses are evolutionarily
conserved across many taxa [23]. We therefore expect
that the physiological effects that modify the animal
trophic function described here are generalizable to
other contexts in which animals must adjust their body
elemental balance to maximize fitness [27].
5. SUMMARY
We derived a stoichiometrically explicit ecosystem model to
investigate the interaction of predation risk, herbivore physiological plasticity and plant quality on biogeochemical
cycling and food-web dynamics. Our analysis contributes
towards increased appreciation [33,44,45,58,59] that
consumers among several trophic levels in ecosystems can
be critically important in driving elemental cycling within
ecosystems. Foraging plasticity can alter the ratio of
elements contained within their body as well as ratios
of elements cycled and stored throughout the ecosystem
[22,23,60]. We show that predators can exert important
indirect control over the elemental content and supply of
4190
S. J. Leroux et al.
Predator control of elemental cycling
detritus inputs to the soil. The attributes of detrital quality
determine the rate at which microbes perform ecosystem
processes such as decomposition and mineralization [26].
Predictions of this theory are also consistent with
results of experiments examining the linkages among predation risk, herbivore metabolism and body C : N ratio,
and C and N mineralization rates in the soil [26,57].
Thus, our theory helps to increase our understanding of
the way plasticity in herbivore organismal physiology in
response to predation risk can explain context-dependency
in ecosystem functioning.
We thank M. Cherif, J. Marleau and the anonymous
reviewers for comments. The work was supported by a
postdoctoral research fellowship from NSERC (Canada) to
S.J.L., a postdoctoral fellowship from funds from the Yale
School of Forestry and Environmental Studies to D.H. and
NSF grant (no. DEB 0816504) to O.J.S.
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