The bigger they come, the harder they fall: Body size and prey abundance influence predator-prey ratios

Abstract

Large carnivores are highly threatened, yet the processes underlying their population declines are still poorly understood and widely debated. We explored how body mass and prey abundance influence carnivore density using data on 199 populations obtained across multiple sites for 11 carnivore species. We found that relative decreases in prey abundance resulted in a five- to sixfold greater decrease in the largest carnivores compared with the smallest species. We discuss a number of possible causes for this inherent vulnerability, but also explore a possible mechanistic link between predator size, energetics and population processes. Our results have important implications for carnivore ecology and conservation, demonstrating that larger species are particularly vulnerable to anthropogenic threats to their environment, especially those which have an adverse affect on the abundance of their prey.

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doi: 10.1098/rsbl.2010.0996
, 312-315 first published online 24 November 20107 2011 Biol. Lett.
Chris Carbone, Nathalie Pettorelli and Philip A. Stephens
prey ratios−abundance influence predator
The bigger they come, the harder they fall: body size and prey
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Population ecology
The bigger they come, the
harder they fall: body size
and prey abundance
influence predator–prey
ratios
Chris Carbone1,*, Nathalie Pettorelli1
and Philip A. Stephens2
1
Institute of Zoology, Zoological Society of London, Regent’s Park,
London NW1 4RY, UK
2
School of Biological and Biomedical Sciences, University of Durham,
South Road, Durham DH1 3LE, UK
*Author for correspondence (chris.carbone@ioz.ac.uk).
Large carnivores are highly threatened, yet the
processes underlying their population declines
are still poorly understood and widely debated.
We explored how body mass and prey abundance
influence carnivore density using data on 199
populations obtained across multiple sites for
11 carnivore species. We found that relative
decreases in prey abundance resulted in a
five- to sixfold greater decrease in the largest
carnivores compared with the smallest species.
We discuss a number of possible causes for this
inherent vulnerability, but also explore a possible
mechanistic link between predator size, ener-
getics and population processes. Our results
have important implications for carnivore ecol-
ogy and conservation, demonstrating that larger
species are particularly vulnerable to anthropo-
genic threats to their environment, especially
those which have an adverse affect on the
abundance of their prey.
Keywords: carnivore ecology; predator–prey
relationships; abundance scaling; climate change;
metabolism
1. INTRODUCTION
It is well recognized that large carnivores are highly
threatened, owing to a combination of environmental
change, biological factors and human pressures [1,2].
However, the main processes underlying global
declines in large carnivores are still widely debated
[3]. Body mass and prey abundance are known to
influence average abundance across mammalian carni-
vores [4]. However, there is also evidence that larger
carnivore species are rarer than expected based on
typical abundance –mass relationships [5,6]. Carni-
vores are extremely wide ranging, with day ranges
two- to threefold that of herbivores of the same size
[7] and, across species, exhibit steeper scaling in day
range and home range [8–10]. This increase in ran-
ging behaviour would influence individual energetic
rates and is consistent with the finding that energetics
may place evolutionary constraints on body size in
predators [11,12]. Ultimately, size and energetics
may be linked with the intrinsic factors identified in a
global analysis of the threat status of mammals [13].
The interplay between the environment, body size
and the intrinsic factors driving this vulnerability
remains poorly understood. Studies that identify
causes of changes in species abundance in relation to
size and ecology have the potential to greatly improve
our understanding of population processes.
In this study, we present an analysis of predator–
prey ratios obtained across multiple sites for 11 species
of carnivores. We focus on a key environmental factor,
food availability (prey abundance), in order to explore
whether large carnivores show a greater population
response to changes in the relative abundance of
their food resources.
2. MATERIAL AND METHODS
To compare carnivore abundance across species in relation to vari-
ation in prey biomass density (enabling a comparison across
different species of carnivores that feed on prey of different sizes
[4,14]), we explored how the logarithm (base 10) of carnivore den-
sity (logN) relates to log carnivore body mass (logM) and log prey
biomass density (logP) for 199 predator– prey population estimates
obtained from 11 species of carnivores (all with six or more
population estimates; table 1; see also the electronic supplementary
material). In our data analysis, we compared the explanatory
power of four different linear combinations of these predictors
using Akaike Information Criterion (AIC) [15,16]. We excluded
data on the population densities of two species, the African wild
dog (Lycaon pictus) and cheetah (Acinonyx jubatus), which are
known to be poorly related to prey availability, owing to competition
with other carnivores [17–20]. Whether or not wild dogs and chee-
tahs are included, our conclusions remain unaffected and the fitted
models remain significant (electronic supplementary material,
table S2); here, however, we focus on the results with wild dogs
and cheetahs omitted.
Most of the data used in this study were obtained from studies
specifically focused on predator– prey relationships for a single carni-
vore species. Inevitably, the methods used in these studies somewhat
varied. In some instances, data on prey density in one year were com-
pared with predator density estimated in the next; in other instances,
these data might be matched within the same year [4]. In addition,
given the practical difficulties of getting such information, we
found that most data were only available from different locations
and periods across the species’ ranges. Ideally, longitudinal data
(from the same populations across years) should be used; nonethe-
less, we believe that these data have the potential to provide
important insights into predator– prey relationships and a general
understanding of consumer–resource relationships [21].
3. RESULTS
The model including all predictors (logP, logMand the
interaction between them) explained 68 per cent of the
variability in log carnivore densities, enjoying substan-
tially more support than the next best alternative
(DAIC ¼11.24 between this and the next best
model; table 2). This relationship is best described
by a linear model of the form log N¼1.06 2
1.29 logMþ0.33 logPþ0.21 logMlogP(all pre-
dictors are significant with p,0.001 and the full
model is also significant with F
3,195
¼140.9, p,
0.001, r
2
¼0.68). The coefficients confirm that
carnivore densities are negatively affected by body
mass and positively affected by prey availability;
crucially, the significant interaction term shows that
the densities of the larger species of carnivores are dis-
proportionately lower in areas of low prey density.
Intriguingly, the slopes of the predator– prey responses
seem to increase linearly with log carnivore body
mass (figure 1).
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rsbl.2010.0996 or via http://rsbl.royalsocietypublishing.org.
Biol. Lett. (2011) 7, 312–315
doi:10.1098/rsbl.2010.0996
Published online 24 November 2010
Received 23 October 2010
Accepted 3 November 2010 312 This journal is q2010 The Royal Society
on June 10, 2011rsbl.royalsocietypublishing.orgDownloaded from

4. DISCUSSION
Focusing on a common threat, that of declining food
resources [22], this study confronts the important
question of how mammalian carnivores of different
size might respond to differing environmental con-
ditions. Compared with the overall variation across
the dataset, the carnivore mass–prey biomass inter-
action term explains only 2 per cent of the variation;
nevertheless, slopes of the relationship between preda-
tors and prey vary substantially and carnivore mass
explains nearly 80 per cent of the variation in these
slopes (figure 1)—a result of great biological signifi-
cance. A given reduction in prey abundance, leads to
a five- to sixfold greater reduction in the larger
carnivores when compared with the smallest carnivores.
What mechanisms could drive this apparent vulner-
ability? One possibility is that, because large carnivores
consume large prey [12], which themselves may be vul-
nerable to threat processes [13], there may be an
interaction across populations between predator and
prey. However, our analysis of carnivore abundance
controls for prey abundance and so does not support
this argument unless more subtle processes, unrelated
to abundance, are taking place. Alternatively, previous
work has shown that energetic costs may limit body
size in larger carnivores [11]. It is possible that similar
physiological factors influence population processes
as well. Physiologists have long been interested in
metabolic costs under different levels of exercise
[23,24]. Such studies have shown that, at maximum
energy expenditure, large animals have relatively high
metabolic rates [25–27]. Carnivores have larger
home ranges [28–31] and hunt for longer [32,33]in
areas of low prey density or productivity. Building on
earlier physiological arguments, we might expect that
when large carnivores work harder to maintain their
energy budgets under conditions of low prey abun-
dance, this in turn may influence their population
density. If this is the case, predatory species with extre-
mely high hunting costs will be particularly susceptible
to changes in the environment that influence feeding
ecology, because any increase in the time spent hunting
greatly adds to overall energy expenditure [34]. In
energetically stressful situations, both survival and
reproduction are subject to reductions; this situation
could be exacerbated in large carnivores by life-history
attributes that already render them vulnerable to
extinction [35]. Future work on this topic, using
models of predator–prey dynamics to assess the
influence of size and habitat productivity, might be
particularly useful in providing specific testable
predictions [36,37].
Understanding the links between physiology, behav-
iour and population phenomena remains one of the
great challenges in ecology [38], and the current back-
drop of declining environmental conditions, climate
change and biodiversity loss makes that challenge par-
ticularly important [39]. Carnivores represent ideal
Table 1. Summary of carnivore density and prey biomass density used in this study, obtained from Carbone & Gittleman [4]
and additional sources (see the electronic supplementary material); see text for details.
species scientific name
ave.
weight
(kg)
no.
populations
carnivore density, N(km
22
)
prey biomass,
P(kg km
22
) range
(min–max)
range
(min–max) slope intercept r
2
least weasel Mustela nivalis 0.14 7 0.52–80.0 0.1615 3.49 0.02 23.9–832.5
arctic fox Alopex lagopus 3.19 14 0.022–0.286 0.2385 0.0268 0.47 1.0 – 2810.9
Canadian
lynx
Lynx canadensis 11.2 28 0.02–0.226 0.4954 0.0047 0.65 16.8–1386.0
European
badger
Meles meles 13.0 9 0.79–8.4 0.3437 12.74 0.73 352.8 –71 400.0
coyote Canis latrans 13.0 19 0.023 – 0.444 0.508 0.0092 0.21 34.5 – 1485.0
wolf Canis lupus 46.0 20 0.005 –0.042 0.6661 0.0003 0.49 89.0–810.5
leopard Panthera pardus 46.5 19 0.005–0.303 0.5079 0.0025 0.51 13.2–41 62.9
spotted
hyena
Crocuta crocuta 58.6 19 0.005–1.842 0.7733 0.0004 0.52 126.0– 17 262.6
lion Panthera leo 142.0 40 0.008 –0.52 0.5854 0.0011 0.66 35.0–14 198.4
tiger Panthera tigris 181.0 16 0.006–0.168 0.7352 0.0002 0.72 171.0–5828.6
polar bear Ursus maritimus 310.0 8 0.003 –0.021 0.8806 00000.9 0.89 41.8– 337.0
Table 2. Models fitted to empirical data on carnivore densities.
fitted model
a
estimated parameters AIC DAIC wr
2
lm(logNlogM)3 2168.22 168.79 0 0.25
lm(logNlogP)3 2156.90 180.10 0 0.20
lm(logNlogMþlog P)4 2325.76 11.24 0 0.66
lm(logNlogMlog P)5 2337.00 0.00 1.00 0.68
a
Model specifications are compatible with R [16] and represent single predictor linear models in the first two cases, a two predictor linear
model in the third case and a model containing both predictors and their interaction in the final case.
Size, abundance and predator–prey ratios C. Carbone et al. 313
Biol. Lett. (2011)
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species for exploring such relationships because, not
only do we know a great deal about their behaviour
and diets [40], but we also have good information on
the abundance and distributions of many of their
prey [4]. We believe that further research exploring
the link between physiology, behaviour and carnivore
population dynamics represents a valuable opportunity
to establish clear relationships, from individual behav-
iour to population processes and macroecological
patterns. This research also has important implications
for the conservation of our largest carnivore species,
which seem especially vulnerable to conditions
influencing the abundance of their prey.
We thank Blaire Van Valkenburgh and Shai Meiri for their
helpful comments on earlier drafts of the manuscript.
1 Cardillo, M., Purvis, A., Sechrest, W., Gittleman, J. L.,
Bielby, J. & Mace, G. M. 2004 Human population den-
sity and extinction risk in the world’s carnivores. PLoS
Biol. 2, e197. (doi:10.1371/journal.pbio.0020197)
2 Van Valkenburgh, B., Wang, X. M. & Damuth, J. 2004
Cope’s rule, hypercarnivory, and extinction in North
American canids. Science 306, 101–104. (doi:10.1126/
science.1102417)
3 Chapron, G., Miquelle, D. G., Lambert, A., Goodrich,
J. M., Legendre, S. & Clobert, J. 2008 The impact on
tigers of poaching versus prey depletion. J. Appl. E co l. 45,
1667–1674. (doi:10.1111/j.1365-2664.2008.01538.x)
4 Carbone, C. & Gittleman, J. L. 2002 A common rule for
the scaling of carnivore density. Science 295, 2273– 2276.
(doi:10.1126/science.1067994)
5 Damuth, J. 1987 Interspecific allometry of population
density in mammals and other animals: the independence
of body mass and population energy-use. Biol. J. Linn.
Soc. 31, 193–246. (doi:10.1111/j.1095-8312.1987.
tb01990.x)
6 Marquet, P. A. 2002 Of predators, prey and power laws.
Science 295, 2229–2230. (doi:10.1126/science.1070587)
7 Carbone, C., Cowlishaw, G., Isaac, N. J. B. & Rowcliffe,
J. M. 2005 How far do animals go? Determinants of day
range in mammals. Am. Nat. 165, 290 –297.
8 Haskell, J. P., Ritchie, M. E. & Olff, H. 2002 Fractal
geometry predicts varying body size scaling relationships
for mammal and bird home ranges. Nature 418,
527–530. (doi:10.1038/nature00840)
9 Kelt, D. A. & Van Vuren, D. H. 2001 The ecology and
macroecology of mammalian home range area. Am.
Nat. 157, 637–645.
10 Jetz, W., Carbone, C., Fulford, J. & Brown, J. H. 2004
The scaling of animal space use. Science 306, 266 – 268.
(doi:10.1126/science.1102138)
11 Carbone, C., Teacher, A. & Rowcliffe, J. M. 2007
The costs of carnivory. PLoS Biol. 5, e22. (doi:10.1371/
journal.pbio.0050022)
12 Carbone, C., Mace, G. M., Roberts, S. C. & Macdonald,
D. W. 1999 Energetic constraints on the diet of terrestrial
carnivores. Nature 402, 286– 288. (doi:10.1038/46266)
13 Cardillo, M., Mace, G. M., Jones, K. E., Bielby, J.,
Bininda-Emonds, O. R. P., Sechrest, W., Orme,
C. D. L. & Purvis, A. 2005 Multiple causes of high
extinction risk in large mammal species. Science 309,
1239–1241. (doi:10.1126/science.1116030)
14 East, R. 1984 Rainfall, soil nutrient status and biomass
of large African savanna mammals. Afr. J. Ecol. 22,
245–270. (doi:10.1111/j.1365-2028.1984.tb00700.x)
15 Whittingham, M. J., Stephens, P. A., Bradbury, R. B. &
Freckleton, R. P. 2006 Why do we still use stepwise
modelling in ecology and behaviour? J. Anim. Ecol. 75,
1182–1189. (doi:10.1111/j.1365-2656.2006.01141.x)
16 R Development Core Team 2005 R: a language and
environment for statistical computing. Reference index
v. 2.2.1. Vienna, Austria: R Foundation for Statistical
Computing.
17 Durant, S. M. 2000 Predator avoidance, breeding experi-
ence and reproductive success in endangered cheetahs.
Anim. Behav. 60, 121– 130. (doi:10.1006/anbe.2000.1433)
18 Laurenson, M. K. 1995 Dynamics implications of high
offspring mortality for cheetah population dynamics. In
Serengeti II: management, and conservation of an ecosystem
(eds A. C. E. Sinclair & P. Arcese), pp. 385– 399.
Chicago, IL: University of Chicago Press.
19 Creel, S. & Creel, N. M. 1996 Limitation of African
wild dogs by competition with larger carnivores. Conserv.
Biol. 10, 526–538. (doi:10.1046/j.1523-1739.1996.
10020526.x)
20 Kelly, M. J. & Durant, S. M. 2000 Viability of the
Serengeti cheetah population. Conser v. Biol. 14, 786 –797.
(doi:10.1046/j.1523-1739.2000.98329.x)
21 Carbone, C. & Pettorelli, N. 2009 Testing relationships
between energy and vertebrate abundance. Int. J. Ecol.
2009,1–6.(doi:10.1155/2009/496175)
22 Karanth, U. & Stith, B. M. 1999 Prey depletion as a critical
determinant of tiger population viability.InRiding the
tiger: tiger conservation in human-dominated landscapes.
(eds J. Seidensticker, S. Christie & P. Jackson),
pp. 100– 113. Cambridge, UK: Cambridge University
Press.
23 Taylor, C. R., Heglund, N. C. & Maloiy, G. M. 1982 Ener-
getics and mechanics of terrestrial locomotion. I. Metabolic
energy consumption as a function of speed and body size in
birds and mammals. J. Ex p. Biol. 97,1
–21.
24 Fedak, M. A., Heglund, N. C. & Taylor, C. R. 1982
Energetics and mechanics of terrestrial locomotion.
2. Kinetic energy changes of the limbs and body as a
function of speed and body size in birds and mammals.
J. Exp. Biol. 97, 23– 40.
25 Weibel, E. R. & Hoppeler, H. 2005 Exercise-induced
maximal metabolic rate scales with muscle aerobic
capacity. J. Exp. Biol. 208, 1635– 1644. (doi:10.1242/
jeb.01548)
26 Suarez, R. K. & Darveau, C. A. 2005 Multi-level
regulation and metabolic scaling. J. Exp. Biol. 208,
1627–1634. (doi:10.1242/jeb.01503)
0.1
0
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1.0
–1.0 –0.5 0 0.5 1.0 1.5 2.0 2.5 3.0
slope, s, of the relationship between log predator
density and log prey biomass density
lo
g
carnivore bod
y
mass (M, k
g
)
Figure 1. The slope (s) of the predator–prey population
responses plotted against log of carnivore mass (log M,in
kilograms). Steeper slopes are related to a faster rate of
change with changing prey. The best-fit line is s¼0.217 
log Mþ0.245 (r
2
¼0.79).
314 C. Carbone et al. Size, abundance and predator –prey ratios
Biol. Lett. (2011)
on June 10, 2011rsbl.royalsocietypublishing.orgDownloaded from

27 Glazier, D. S. 2009 Activity affects intraspecific body-size
scaling of metabolic rate in ectothermic animals. J. Com p.
Physiol. B: Biochem. Syst. Environ. Physiol. 179,821–828.
28 Creel, S. & Creel, N. M. 2002 The African wild dog:
behavior, ecology, and conservation. Princeton, NJ:
Princeton University Press.
29 Nilsen, E. B., Herfindal, I. & Linnell, J. D. C. 2005 Can
intra-specific variation in carnivore home-range size be
explained using remote-sensing estimates of environ-
mental productivity? Ecoscience 12, 68–75. (doi:10.
2980/i1195-6860-12-1-68.1)
30 Van Orsdol, K. G., Hanby, J. P. & Bygott, J. D. 1985 Eco-
logical correlates of lion social organisation (Panthera leo).
J. Zool. Lond. Ser. A 206, 97–112.
31 Karanth, K. U., Nichols, J. D., Kumar, N. S., Link,
W. A. & Hines, J. E. 2004 Tigers and their prey:
predicting carnivore densities from prey abundance.
Proc. Natl Acad. Sci. USA 101, 4854–4858. (doi:10.
1073/pnas.0306210101)
32 Zalewski, A., Jedrzejewski, W. & Jedrzejewska, B. 2004
Mobility and home range use by pine martens in a
Polish primeval forest. Ecoscience 11, 113– 122.
33 Schmidt, K. 2008 Behavioural and spatial adaptation of
the Eurasian lynx to a decline in prey availability. Acta
Theriol. 53, 1 –16.
34 Gorman, M. L., Mills, M. G., Raath, J. P. & Speakman,
J. R. 1998 High hunting costs make African wild dogs
vulnerable to kleptoparasitism by hyaenas. Nature 391,
479–481. (doi:10.1038/35131)
35 Cardillo, M. 2003 Biological determinants of extinction
risk: why are smaller species less vulnerable? Anim. Con-
serv. 6, 63 –69. (doi:10.1017/S1367943003003093)
36 Dieckmann, U., Marrow, P. & Law, R. 1995 Evolutionary
cycling in predator –prey interactions: population
dynamics and the Red Queen. J. Theoret. Biol. 176,
91–102. (doi:10.1006/jtbi.1995.0179)
37 Abrams, P. A. 2000 The evolution of predator–prey
interactions: theory and evidence. Ann. Rev. Ecol. Syst.
31, 79–105. (doi:10.1146/annurev.ecolsys.31.1.79)
38 Brown, J. H., Gillooly, J. F., Allen, A. P., Savage, V. M. &
West, G. B. 2004 Toward a metabolic theory of ecology.
Ecology 85, 1771–1789. (doi:10.1890/03-9000)
39 Collen, B., Loh, J., Whitmee, S., McRae, L., Amin, R. &
Baillie, J. E. M. 2009 Monitoring change in
vertebrate abundance: the living planet index. Conserv.
Biol. 23, 317–327. (doi:10.1111/j.1523-1739.2008.
01117.x)
40 Gittleman, J. L. 1985 Carnivore body size: ecological and
taxonomic correlates. Oecologia 67, 540–554. (doi:10.
1007/BF00790026)
Size, abundance and predator–prey ratios C. Carbone et al. 315
Biol. Lett. (2011)
on June 10, 2011rsbl.royalsocietypublishing.orgDownloaded from