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Large ‘apex’ predators influence ecosystems in profound ways, by limiting the density of their prey and controlling smaller ‘mesopredators’. The loss of apex predators from much of their range has lead to a global outbreak of mesopredators, a process known as ‘mesopredator release’ that increases predation pressure and diminishes biodiversity. While the classifications apex- and meso-predator are fundamental to current ecological thinking, their definition has remained ambiguous. Trophic cascades theory has shown the importance of predation as a limit to population size for a variety of taxa (top–down control). The largest of predators however are unlikely to be limited in this fashion, and their densities are commonly assumed to be determined by the availability of their prey (bottom–up control). However, bottom–up regulation of apex predators is contradicted by many studies, particularly of non-hunted populations. We offer an alternative view that apex predators are distinguishable by a capacity to limit their own population densities (self-regulation). We tested this idea using a set of life-history traits that could contribute to self-regulation in the Carnivora, and found that an upper limit body mass of 34 kg (corresponding with an average mass of 13–16 kg) marks a transition between extrinsically- and self-regulated carnivores. Small carnivores share fast reproductive rates and development and higher densities. Large carnivores share slow reproductive rates and development, extended parental care, sparsely populated territories, and a propensity towards infanticide, reproductive suppression, alloparental care and cooperative hunting. We discuss how the expression of traits that contribute to self-regulation (e.g. reproductive suppression) depends on social stability, and highlight the importance of studying predator–prey dynamics in the absence of predator persecution. Self-regulation in large carnivores may ensure that the largest and the fiercest do not overexploit their resources.
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EV-1
What is an apex predator?
Arian D. Wallach , Ido Izhaki , Judith D. Toms , William J. Ripple and Uri Shanas
A. D. Wallach (arian.wallach@cdu.edu.au), School of Environment, Charles Darwin Univ., Darwin, Northern Territory, Australia. I. Izhaki,
Dept of Evolutionary and Environmental Biology, Univ. of Haifa, Haifa, Israel. J. D. Toms, Eco-Logic Consulting, Victoria, BC, Canada.
W. J. Ripple, Dept of Forest Ecosystems and Society, Oregon State University, Corvallis, OR, USA. U. Shanas, Dept of Biology and
Environment, Univ. of Haifa - Oranim, Tivon, Israel.
Large ‘ apex predators infl uence ecosystems in profound ways, by limiting the density of their prey and controlling smaller
‘ mesopredators ’ . e loss of apex predators from much of their range has lead to a global outbreak of mesopredators, a
process known as mesopredator release that increases predation pressure and diminishes biodiversity. While the classifi ca-
tions apex- and meso-predator are fundamental to current ecological thinking, their defi nition has remained ambiguous.
Trophic cascades theory has shown the importance of predation as a limit to population size for a variety of taxa (top down
control).  e largest of predators however are unlikely to be limited in this fashion, and their densities are commonly
assumed to be determined by the availability of their prey (bottom up control). However, bottom up regulation of apex
predators is contradicted by many studies, particularly of non-hunted populations. We off er an alternative view that apex
predators are distinguishable by a capacity to limit their own population densities (self-regulation). We tested this idea
using a set of life-history traits that could contribute to self-regulation in the Carnivora, and found that an upper limit
body mass of 34 kg (corresponding with an average mass of 13 16 kg) marks a transition between extrinsically- and self-
regulated carnivores. Small carnivores share fast reproductive rates and development and higher densities. Large carnivores
share slow reproductive rates and development, extended parental care, sparsely populated territories, and a propensity
towards infanticide, reproductive suppression, alloparental care and cooperative hunting . We discuss how the expression
of traits that contribute to self-regulation (e.g. reproductive suppression) depends on social stability, and highlight the
importance of studying predator prey dynamics in the absence of predator persecution. Self-regulation in large carnivores
may ensure that the largest and the fi ercest do not overexploit their resources.
e ecological role of large predators is expressed by their
classifi cation as apex predators ; a term used to denote their
elevated position on the trophic ladder. Apex predators are
primarily known for their role as inhibitors of population
irruptions of prey and smaller predators, an eff ect that
cascades throughout ecological communities and promotes
biodiversity.  e keystone role of apex predators as ecosys-
tem regulators is now fi rmly embedded in ecological theory
(Estes et al. 2011, Ripple et al. 2014). Medium-sized preda-
tors, termed mesopredators , also drive community struc-
ture through a variety of pathways, including predation on
small prey (Roemer et al. 2009). Apex predators limit the
density of mesopredators so that total predation pressure is
contained (Ripple et al. 2014).  e loss of apex predators
removes this inhibiting factor, resulting in mesopredator
release (Crooks and Soul é 1999, Prugh et al. 2009).
Apex predator ’ , ‘ mesopredator ’ and ‘ mesopredator release ’
are terms that have set the tone for our understanding of
a wide range of ecological processes (Estes et al. 2011). How-
ever, the categorization of predators remains ambiguous.
Within each ecosystem the largest extant predators are often
classed as apex predators even if these same species are con-
sidered typical mesopredators elsewhere. For example, cats
and foxes fall easily into the mesopredator group (Crooks
and Soul é 1999), but as introduced species on islands they
are often the largest mammal present and are therefore
classed as apex predators (Rayner et al. 2007, Bergstrom
et al. 2009, Roemer et al. 2009).  e mesopredator release
concept in itself was developed from the study of the coyote
Canis latrans as an apex predator (Crooks and Soul é 1999), a
species frequently placed in the mesopredator group when
in the presence of wolves Canis lupus (Prugh et al . 2009,
Ripple et al. 2013). Some regions contain a rich guild of
large predators making it diffi cult to determine where to
draw the line between apex- and meso-predators (Prugh
et al. 2009). Indeed, some of the world s iconic apex preda-
tors coexist with larger and fi ercer predators (Palomares and
Caro 1999), and many of the world s largest predators are
now extinct. Is the gray wolf therefore a mesopredator in the
presence of larger carnivores?
Predators of all sizes harass, kill and scare predators
smaller than themselves: tigers dominate wolves (Miquelle
et al. 2005), wolves exclude coyotes (Ripple et al. 2013),
coyotes control foxes (Crooks and Soul é 1999), foxes kill
cats (Glen and Dickman 2005), cats suppress rats (Rayner
et al. 2007), and rats displace mice (Wanless et al. 2007).
© 2015  e Authors. Oikos © 2015 Nordic Society Oikos
Subject Editor: James D. Roth. Editor-in-Chief: Dries Bonte. Accepted 12 December 2014
Oikos 000: 001–009, 2015
doi: 10.1111/oik.01977
EV-2
Predators of all sizes can also induce trophic cascades: pumas
promote tree recruitment by controlling deer (Ripple et al.
2014), sea otters recover kelp forests by eating herbivorous
sea urchins (Estes et al. 2011), cats maintain island produc-
tivity by suppressing rabbits (Bergstrom et al. 2009), plants
benefi t when fi sh reduce dragonfl y predation on pollinating
insects (Knight et al. 2005), and nutrient cycling is infl u-
enced by the stress response of herbivorous grasshoppers to
hunting spiders (Hawlena and Schmitz 2010).
Despite these similarities there appears to be little
functional redundancy between large and small predators.
e loss of the largest of predators has had a dispropor-
tionately disruptive infl uence on ecosystem structure and
function (Ripple et al. 2014); a process coined trophic
downgrading (Estes et al. 2011). Defi ning predator status
comparatively within each system is problematic because
it implies that mesopredators can step into the role of apex
predators as these disappear from the landscape. Studies
suggest the opposite: mesopredators are not eff ective replace-
ments for apex predators (Prugh et al. 2009). Size may in
fact be a reliable predictor of a predator s ecological status,
refl ecting diff erences in evolutionary pressures and adapta-
tion. A mesopredator may therefore remain a mesopreda-
tor even in systems devoid of larger predators, and an apex
predator need not be the single largest.
What then distinguishes apex predators from mesopreda-
tors? One fundamental consequence of size is that large
predators are relatively safe from predation (Promislow and
Harvey 1990). In the absence of an eff ective extrinsic source
of predation, there can be two main mechanisms limit-
ing population growth: 1) the decline in the abundance of
their prey (a bottom up force), and 2) an internal mecha-
nism of self-regulation (a socially mediated force). Although
ecologists have traditionally supported the bottom up view
(Hayward et al. 2007), trophic cascades theory highlights
the role of top down regulation in population dynamics. It
would be surprising if top down forcing infl uences all but
the largest. Indeed, studies frequently fi nd negative rather
than positive correlations between apex predators and their
prey (Estes et al. 2011), hinting that apex predator may not
be bottom up driven. While habitat productivity is not ruled
out as a contributing factor to population density (Carbone
and Gittleman 2002, Jedrzejewski et al. 2007), large preda-
tors may be unique in maintaining their own populations at
sustainable levels.
Body mass may be a good predictor of apex- and
meso-predator status, because it directly infl uences the rate
of extrinsic predation pressure, thus indirectly infl uencing
life-history traits. Across mammals both juvenile and adult
mortality rates increase as body mass declines, and higher
mortality is associated with r-selected life-history vari-
ables (Promislow and Harvey 1990). Among carnivores,
increasing body size is associated with dietary requirements
for larger prey (Carbone et al. 2007) and lower densities
relative to prey biomass (Carbone and Gittleman 2002).
Evolutionary pressures that infl uence body mass may give
rise to similar adaptations in diff erent taxonomic groups,
and the emergence of a self-regulating ecomorph (Flueck
2000).
Most large predator populations are subjected to lethal
control (Ripple et al. 2014) and therefore studies of stable
predator populations are rare. Several recent studies have
pointed to the importance of considering the condition of
social stability in large predators when analyzing predator
prey interactions (Wallach et al. 2009, Cariappa et al. 2011,
Ordiz et al. 2013, Cubaynes et al. 2014). Evidence of social
interactions that may enable self-regulation has emerged from
studies of large predators including bears, large cats, large
canids and large otters (Supplementary material Appendix 1
Table A1).  ese studies off er examples where social interac-
tions, rather than resource availability, drive mortality and
fecundity, limit population density and stability, and infl u-
ence the expression of life history traits that slow population
growth rates (Table 1). Where human-caused mortality is low,
large predators may therefore retain relatively constant popu-
lation densities despite diff erences in resource availability.
Here we investigate the hypothesis that predators above
a certain weight threshold are self-regulating, while smaller
predators require extrinsic regulation by a larger predator
(Fig. 1). We conducted an analysis of life-history traits that
may contribute to self-regulation in the Carnivora (hereaf-
ter carnivores). We selected the carnivores because trophic
cascades eff ects have been consistently demonstrated for
several members of this group (Ripple et al. 2014). We found
that carnivores above a threshold mass have life-history traits
conducive to self-regulation.
Methods
We conducted a review of life-history traits of terrestrial and
semi-terrestrial species, belonging to twelve carnivore fami-
lies, for which suffi cient information was available (n 121,
Supplementary material Appendix 1 Table A2). We selected
eleven variables representing four major life-history traits,
which we considered likely to contribute to self-regulation,
and analyzed them in relation to upper limit body mass
(ULBM) and average body mass (ABM). Data was sourced
from encyclopedias (e.g. Encyclopedia of Life), online
databases (e.g. Carey and Judge 2002, de Magalhaes and
Costa 2009, IUCN), life-history journals (e.g. Mammalian
Species) and other peer-reviewed sources.
Human hunting can have pronounced eff ects on the
expression of life history traits (Haber 1996, Milner et al.
2007) and few populations have escaped this impact (Ripple
et al. 2014). We therefore chose upper limit values for most
variables (Supplementary material Appendix 1 Table A2)
to account for the potential of individuals in undisturbed
Table 1. Evidence that social interactions enable self-regulation in
large carnivores. For each Family we summarize the number of stud-
ies supporting the propositions that social interactions, rather than
resource availability: drive mortality and fecundity (A), limit density
(B), affect population stability (C), and affect the expression of life
history traits that slow population growth rates (D). The proportion
of studies is shown in brackets, with some studies supporting more
than one proposition. Summarized from studies compiled in the
Supplementary material Appendix 1 Table A1.
Proposition Ursidea Felidea Canidea Mustelidea Total
A 8 (89%) 2 (18%) 4 (27%) 3 (60%) 17 (43%)
B 2 (22%) 8 (73%) 7 (47%) 1 (20%) 18 (45%)
C 4 (44%) 3 (27%) 5 (33%) 1 (20%) 13 (33%)
D 7 (78%) 2 (18%) 2 (13%) 0 11 (28%)
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Figure 1. Apex- and meso-predator status are fi xed ecological categories: apex predators are self-regulated and smaller predators are
extrinsically regulated. Antagonistic interactions (dashed arrows) and top down forces (thick arrows) exist within and across both groups,
but the ability to self-regulate (circular arrows) is unique to large predators. Citations for interactions are: 1, 5, 7, 8 Supplementary
material Appendix 1 Table A1; 2 - Murphy et al. 1998; 3, 4, 16, 17 - Palomares and Caro 1999, Gunther and Smith 2004, Jimenez et al.
2008; 6 - Letnic et al. 2011; 9 - Ripple et al. 2013; 10 13 - Crooks and Soul é 1999; 14 - Carlsson et al. 2010; 15 - Glen and Dickman
2005. Artwork by J. Parkhurst.
populations to grow large, mature, form social bonds, hold
territories and provide uninterrupted care for their young.
e relation of life-history traits with ULBM and ABM
showed similar trends (ULBM and ABM values are corre-
lated r 0.97, p 0.0001), and we chose to present ULBM
results because this variable is less likely to be infl uenced by
human activity.
Variables
Reproductive strategy (r/K)
We hypothesized that self-regulating carnivores would
employ a K-strategy (i.e. slow life-history) and invest more
energy in fewer off spring compared to extrinsically-regulated
carnivores. Five variables were assessed for this trait: 1) age
at weaning, 2) age at independence (and dispersal), 3) age
at sexual maturity, 4) lifespan and 5) population reproduc-
tive rate (accounting for reproductive suppression of some
females).
e age at weaning and independence provide measures
of parental care. To account for relative parental investment,
both variables were also analyzed in relation to lifespan and
reproductive rate (e.g. age at independence / lifespan / num-
ber of off spring / year). We modifi ed the reproductive rate
variable to account for social carnivores that limit the repro-
duction of some females (off spring / year / average number
of breeding females in a group / average number of sexually
mature females in a group).
Family planning
e limitation of off spring production below the
species maximum reproductive potential is referred to here
as family planning , and we expected this trait to contribute
to self-regulation. We used two binary variables: 1) female
reproductive suppression and 2) infanticide. Female repro-
ductive suppression occurs in social species in which domi-
nant females exclude other sexually mature females from
breeding, or litters of subordinates are killed or abandoned.
Female territoriality
Territoriality is considered an important mechanism for
spacing individuals or groups and limiting population den-
sity (Cariappa et al. 2011). We focused on females because
territorial males may occupy the home range of several
females and reproduce with all of them (e.g. felids and
bears). We included a binary variable female territoriality
and a continuous subset variable female density .
For the subset of female-territorial carnivores, we recorded
the median female territory size and the average number of
females in a social group to calculate an estimate of female
density (group size / territory size). We used the median value
EV-4
variables were most strongly associated with the fi rst PC
axis (PC1), which is representative of the fast-slow (r-K)
life history continuum.  e piecewise regression identifi ed
a threshold in the relationship between PC1 and ULBM at
33.85 kg (ABM 13 16 kg), with a 95% confi dence inter-
val (CI) between 18.16 63.12 kg (Davies test: p 0.001,
Fig. 2A).  e second PC axis (PC2) was formed by the
socially complex behaviors (e.g. family planning and allo-
parental care) on one side, and high reproductive rates on
the other, with no signifi cant threshold identifi ed. Female
territoriality only appeared as a signifi cant variable in PC3
(Table 2). In no case was a signifi cant threshold detected for
the individual variables included in the PCA.
Across the full carnivore mass range, both PC1 and PC2
were positively correlated with body mass (Pearson s correla-
tion LogULBM: PC1, r 0.73, p 0.001; PC2, r 0.38,
p 0.01). ere was no correlation between PC3 and body
mass (NS). Large carnivores (ULBM 34 kg) had mostly
positive PC1 values (70%) and about half (55%) had positive
PC2 values, refl ecting a K-strategy and a tendency towards
socially complex reproductive behaviors. Small carnivores
(ULBM 34 kg) had predominantly negative PC1 (73%)
and PC2 (69%) values, corresponding with an r-strategy
and more solitary or biparental social groups (Fig. 2B). Both
within and between taxonomic families, large carnivores had
consistently higher PC1 and PC2 values (Fig. 2C). However,
while small carnivore families were clustered together, each
family of large carnivores was distinctly placed along the two
axes (e.g. bears had the highest PC1 values and large canids
had the highest PC2 values).
Female territoriality was ubiquitous and common across
the Carnivora (71% of species), but within the subset of car-
nivores that are female-territorial, female density was nega-
tively correlated with body mass (Spearman s r 0.77,
p 0.001; Fig. 3A) and with PC1 (r 0.41, p 0.01).
Female biomass (female density controlled for standardized
metabolic needs) was also negatively related with body mass
(r 0.48, p 0.001, Fig. 3B), but not with PC1 (NS).
resholds were detected for both density (71.95 kg, 95%
CI 6.67 775.88) and biomass (73.70 kg, 95% CI 4.52
1199.91), but neither threshold was signifi cant (Davies test:
p 0.691 and p 0.913, respectively).
Large carnivores invest more time and a larger portion of
their lifetime in each off spring, relative to small carnivores.
Parental care (age at weaning and independence) and paren-
tal investment (parental care controlled for lifespan and
reproductive rate) were positively correlated with body mass
(parental care: by weaning, r 0.38, p 0.001, by indepen-
dence r 0.52, p 0.001; parental investment: by weaning
r 0.33, p 0.001, by independence r 0.24, p 0.001).
resholds were detected for parental investment (by inde-
pendence: 11.87 kg, 95% CI 3.43 41.02, Davies test:
p 0.1; by weaning 14.0 kg, 95% CI 5.64 34.78, Davies
test: p 0.004), but only the threshold for weaning was
signifi cant (Fig. 4).
Discussion
Life history traits that may infl uence population regulation
diff er between large and small carnivores, lending support
because territory size may vary widely in relation to habitat
conditions. To account for the diff erences in body mass we
calculated an estimate of carnivore biomass by adjusting the
density to standardized metabolic needs (group size / terri-
tory size ABM 0.75 , Gittleman and Harvey 1982). Data
were obtained for 55 (of 69) female-territorial carnivores.
Cooperative behavior
Cooperative behaviors may be features of self-regulating
species and associated with the ability to secure large terri-
tories and large prey (Creel and Macdonald 1995). We used
cooperative hunting, and two forms of cooperative care: 1)
paternal care and 2) alloparental care, as measures of coop-
erative behaviors, all as binary variables. Carnivores were
included in both categories if their social structure was fl ex-
ible and inclusive of both forms (e.g. red fox Vulpes vulpes ,
Cavallini 1996).
Data analysis
We used a principal components (PC) analysis (SPSS 20),
of the eleven variables for which full datasets were available
(n 73 species), to identify groups of strongly interacting
variables (Jolliff e 2002) across the Carnivora and discretely
for each Family and mass group. We compared the main PCs,
and each of the individual variables, with log-transformed
body mass. We then fi t a piecewise regression to identify a
threshold in the relationships (Toms and Lesperance 2003),
using the segmented package in R (Muggeo 2008). Variables
were log-transformed to meet the assumption of constant
variance in residuals. Binary variables were tested using a
piecewise logistic regression (Toms and Lesperance 2003).
We tested the threshold signifi cance using a Davies test
(Davies 1987, Piepho and Ogutu 2003).  e subset variables
female density and female biomass were correlated separately
with the strongest PCs and with body mass. We compared
the relationship between parental care and parental invest-
ment with body mass separately.
Results
e fi rst three PCs cumulatively accounted for 70% of
the variation in the dataset (Table 2). Reproductive strategy
Table 2. Scores of the eleven life-history variables in the top three
models of the principal component analysis (PCA).
Variables
PC1
(33.6%)
PC2
(25%)
PC3
(11.7%)
Lifespan 0.854 0.184 0.091
Age at sexual maturity 0.852 0.190 0.048
Age at weaning 0.814 0.174 0.204
Age at independence 0.770 0.359 0.039
Female reproduction
suppression
0.388 0.800 0.051
Reproductive potential 0.601 0.424 0.152
Paternal care 0.487 0.580 0.238
Alloparental care 0.328 0.824 0.216
Cooperative hunting 0.222 0.513 0.326
Infanticide 0.044 0.631 0.558
Territoriality (female) 0.266 0.163 0.832
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Figure 2. Relationship between the two strongest principal components (PC) and upper limit body mass (ULBM). (A) Relation of PC1 to
log transformed ULBM with the estimated threshold identifi ed at 34 kg (full line), with a 95% confi dence interval of 18 63 kg (dashed
lines). (B) Position of carnivores on the fi rst two PC axes. (C) Position of family and mass groups on the two major axes (average SE),
separated at 34 kg. Blue circles are identifi ed as typical mesocarnivores (ULBM 18 kg), light green circles (in B) denote carnivores that
fall within the lower threshold confi dence zone (ULBM 18 34 kg) and dark green circles are identifi ed as apex carnivores (ULBM 3 4
kg). 1 Canidae, 2 Felidae, 3 Herpestidae, 4 Hyaenidae, 6 Mustelidae, 7 Procyonidae, 8 Ursidae, 9 Ailuridae (red panda,
Ailurus fulgens ), 10 Eupleridae (fossa Cryptoprocta ferox ), 11 Viverridae (common genet, Genetta genetta ).
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Figure 3. Density (A) and biomass (B) of territorial female carni-
vores relative to ULBM.  e giant panda, an outlier, is circled in
(B). Blue circles are identifi ed as typical mesocarnivores (ULBM 1 8
kg), light green circles denote carnivores that fall within the lower
threshold confi dence zone (ULBM 18 34 kg) and dark green cir-
cles are identifi ed as apex carnivores (ULBM 34 kg).
Figure 4. Relationship between parental investment (age at weaning
controlled for lifespan and reproductive rate) and body mass with
the estimated threshold identifi ed at an ULBM of 14 kg (full line),
with a 95% confi dence interval of 6 35 kg (dashed lines).
to the proposition that apex- and meso-predator status are
xed. In this analysis of terrestrial and semi-terrestrial car-
nivores, an ULBM of 18 34 kg (ABM 13 16 kg) marked
a transition between extrinsically regulated meso-carnivores
and self-regulating apex carnivores.  is threshold is similar
to the commonly used ABM of 15 kg to distinguish meso-
carnivores from apex-carnivores (Prugh et al. 2009, Ripple
et al. 2014), but is slightly lower than previous studies that
found a dietary threshold at an ABM of 20 kg (Carbone
et al. 2007). Our analysis also helps clarify the ecological
position of carnivore species whose status is ambivalent (e.g.
coyotes are recognized here as apex predators).
Large carnivores probably self-regulate because they
typically invest more in fewer off spring, suppress the repro-
duction of mature females and commit infanticide ( family
planning ), are socially cooperative and hold sparsely popu-
lated territories (Fig. 2 4). Mesocarnivores on the other
hand are unlikely to self-regulate and are instead adapted to
extrinsic-regulation pressure, as suggested by a higher repro-
ductive rate, lower investment in each off spring, scarcity of
family planning and the potential to attain higher densities.
Diff erences between large and small carnivores persist when
controlling for standardized metabolic needs and group size
(Fig. 3), and for lifespan and reproductive rate (Fig. 4).  ese
life-history traits are often shared more closely within mass
groups than within taxonomic groups (Fig. 2C).
Reproductive strategy, the main contributor to the fi rst
PC axis, was the most important trait defi ning carnivore
status. Extended parental care and heavier investment in each
off spring were particularly characteristic of apex carnivores.
Within apex carnivores K-traits and parental investment
increase relative to body mass at a faster rate than in mesocarni-
vores (Fig. 2A, 4).  us apex carnivores increase their K-traits
as body mass increases but this does not consistently occur in
the mesocarnivore group. Predation pressure on mesocarni-
vores of all sizes may be consistently selecting for r-traits.
Family planning , an important contributor to the
second PC axis, was also characteristic of apex carnivores,
particularly in canids. Infanticide is often associated with
reproductive suppression of sexually mature females, and
65% of carnivores that exclude some females from breeding
perform infanticide. In these species the dominant females
kill the young of the subordinate females in their social
group. Where infanticide is used to restrict the reproduc-
tion of females, it most likely acts to limit the size of social
groups and ultimately population density. Overall, 52%
of carnivores that practice infanticide do not suppress the
reproduction of females. In these cases infanticide occurs
when a rival male displaces the resident breeding male, and
the sire ’ s off spring are killed to gain reproductive advantage
(sexually-selected infanticide). Male-driven infanticide has a
substantial infl uence on population density and demography
of bears and large felids (Supplementary material Appendix
1 Table A1). Male-driven infanticide may in some cases
select for larger groups. In banded mongoose, reproductive
suppression is selected against because pup survival increases
when more females in each group reproduce due to male
infanticide (Cant 2000).
Female reproductive suppression is clearly an important
regulation mechanism in social carnivores, occurring in most
large canids (88 100%) and large hyenas (67%) (Supple-
mentary material Appendix 1 Table A2). It may however
also function indirectly in solitary predators. For example,
Ordiz et al. (2008) found that an adult female brown bear
was less likely to produce cubs if her nearest neighbor already
had cubs.  ey argued that this could be considered a form
of reproductive suppression, probably caused by resource
competition among female bears living close to each other.
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Cryptoprocta ferox , the largest member of the Eupleridae
and Madagascar s largest carnivore, shares traits with apex
carnivores (Fig. 2C).  e threshold mass is also likely to be
much higher in the pinnipeds whose large body mass is an
adaptation to their marine habitat where they are sub-
jected to predation from even larger predators. Secondly,
the threshold mass identifi ed can also be infl uenced by
the traits investigated and by sample size. Here, parental
investment showed a threshold at a lower position (14 kg)
than the eleven variables combined in PC1 (ULBM 34
kg), possibly due to the larger sample size of the former,
and the absence of many medium-sized carnivores in the
latter. Lastly, it remains unclear whether habitat size infl u-
ences predator status and self-regulation. Several islands
are too small to support large carnivores but do contain
medium-sized carnivores, which our analysis suggests are
mesopredators. Whether plasticity in the expression and
evolution of life-history traits can enable mesopredators
to self-regulate and function as apex predators on small
islands remains unknown.
e ecological roles of large carnivores vary greatly, and
only some function ecologically as apex predators . Large
carnivores that are primarily vegetarian will have ecological
eff ects that diff er from those that are carnivorous. Despite
this, self-regulation within large predators may provide a
distinct ecological function. For example, apex carnivores
are less likely to become invasive . A notable case is the
contrasting ecologies of the red fox and the dingo Canis dingo ,
two canids that migrated to Australia.  e fox, a mesopreda-
tor, correlates positively with resource availability, and in the
absence of regulation by dingoes reaches high densities and
can drive the extinction of their prey. By contrast the dingo,
an apex predator, forms stable population densities across a
wide productivity gradient when socially stable, and contrib-
utes signifi cantly to the preservation of Australia s biodiver-
sity (Wallach et al . 2009, Letnic et al. 2011).
Identifying whether predators are primarily self- or
extrinsically- regulated requires long-term studies of socially
stable populations. Human persecution of predators is
a major infl uence not only on their numbers, but also on
their social structure (Haber 1996, Wallach et al . 2009,
Ordiz et al. 2013). In turn, social stability determines preda-
tor prey dynamics, and the relative importance of bottom
up and top down forces driving population size.
Infl uence of social stability on life-history
e expression of self-regulation in apex carnivores stems
from social interactions, and is therefore subject to the
condition of social stability. Reproductive strategy (r/k)
variables are responsive to conditions of population density,
demographics and stability. In apex carnivore populations
subjected to human hunting, age at sexual maturity (and
primipatry) declines, reproductive rate increases, parental
care shortens and demography skews towards juveniles. In
non-exploited populations of large canids, off spring often
remain within their natal group for several years, delaying
primipatry and reducing litter production (Haber 1996).
Social stability generally acts to promote the expression
of K-traits by slowing down population turnover rates
(Supplementary material Appendix 1 Table A1).
In apex carnivores, female territoriality contributes
to self-regulation by maintaining low densities (Fig. 3,
Supplementary material Appendix 1 Table A1), but on its
own territoriality is not a signifi cant predictor of predator
status (Table 2). Territoriality is unlikely to contribute to
self-regulation if territories shrink in response to increased
densities, as has been observed in several small carnivore
populations (Cavallini 1996, Benson et al. 2006). Flexibility
in territorial behavior is probably advantageous for smaller
carnivores that have to adjust their space use in relation to
the threat of larger carnivores (Cavallini 1996), while terri-
torial stability is important for large predatory carnivores to
buff er patchy or variable resources and for protection from
dangerous conspecifi cs (Supplementary material Appendix 1
Table A1).
Cooperative behaviors were more pronounced in large
carnivores (Table 2).  e predisposition for cooperative
hunting is in line with a tendency towards hypercarnivory
in large carnivores (Carbone et al. 2007). While cooperative
hunting of large prey is not unique to large carnivores (some
ant species hunt prey thousands of times their size, Dejean
et al. 2010), nor is it obligate (not all large carnivores are
carnivorous), the most complex forms of cooperative hunting
have been observed primarily in large carnivores (MacNulty
et al. 2009, Bailey et al. 2013).
Alloparental care was more common in the large
carnivore group, and was associated with family planning in
the second PC (Fig. 2B). In large social carnivores therefore,
the association of alloparental care with female reproductive
suppression and infanticide provides a high carer:off spring
ratio. Paternal rearing, on the other hand, was affi liated
with an r-strategy and with small carnivores in the fi rst PC
(Fig. 2B). In both solitary and biparental carnivores, female
breeding is unrestricted. An r-strategy without family plan-
ning is a condition conducive to high reproductive output
and is more common in mesocarnivores: 48% of small carni-
vores versus 7% of large carnivores have negative PC1 values
and are solitary or biparental.
e results of our study were robust despite the high
level of noise in the dataset.  e quality of life history
knowledge varies between species and traits: research eff ort
is biased towards a small number of carnivores (Ripple et al.
2014); much data are derived from captive animals; and data
sourced from wild populations may be equally biased due
to anthropogenic eff ects (Milner et al. 2007). Additionally,
life-history traits vary with habitat conditions (Carbone and
Gittleman 2002, Jedrzejewski et al. 2007). While these biases
are unlikely to be confounding in this study, we do expect
that advances in life history studies of wild populations with
minimal anthropogenic eff ects (particularly predator control)
will help clarify the mechanisms regulating population size.
Our analysis identifi ed a threshold at approximately 34
kg (ULBM), but there are several reasons not to consider
this weight overly prescriptive. Firstly, the threshold mass
that diff erentiates apex- from meso-predators is likely to vary
between taxonomic groups. In this study the threshold mass
was strongly infl uenced by three families that contributed the
highest number of species: the canids, felids and mustelids.
Defi ning a threshold mass at the Order level was necessary
in order to obtain a suffi cient sample size, but it may obscure
diff erences between families. For example, the 12 kg fossa
EV-8
health (Wallach et al. 2009, Ordiz et al . 2013). Carnivores
subjected to hunting undergo markedly diff erent popula-
tion dynamics.  ere are few studies that have investigated
how the loss of individual animals infl uences populations,
and fewer still that have determined the drivers of popula-
tion density in protected populations. We are only recently
beginning to appreciate the profound importance of large
carnivores for the health of ecosystems. Apex predators may
keep the proverbial balance of nature not only by limit-
ing the populations of those they hunt, but also by limiting
themselves. Whether humanity can achieve a similar feat is
an important question to consider.
Are we apex primates?
Our earliest ancestors were prey species most likely top down
regulated by large carnivores (Rose and Marshall 1996), but
we have evolved into the fi ercest predator on the planet,
free of extrinsic top down regulation and are arguably apex
predators in our own right. In the words of Louis C. K. we
got out of the food chain (Oh My God, HBO, 2013). And
yet, after surpassing a population size of 7 billion in 2012,
triggering a sixth mass extinction and severely depleting
non-renewable resources, one would hesitate to argue that
humans are self-regulating. Current human society appears
to be a classic case of mesopredator release, destined to end
in a Malthusian collapse (Ehrlich and Ehrlich 2013). How-
ever, when we consider that self-regulation in apex carnivores
is dependent upon a state of social stability, we can refl ect
upon our own condition as that of a socially disrupted apex
primate. And social instability can be redressed.
Acknowledgements We thank A. O Neill, D. Grossman, B. Purcell
and S. Carroll for helpful discussions on the manuscript s concept,
and Subject Editor J. Roth for constructive comments on an
earlier version of this work. We are grateful to J. Parkhurst for the
artwork.
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Appendix 1.
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Principal component analysis has often been dealt with in textbooks as a special case of factor analysis, and this tendency has been continued by many computer packages which treat PCA as one option in a program for factor analysis—see Appendix A2. This view is misguided since PCA and factor analysis, as usually defined, are really quite distinct techniques. The confusion may have arisen, in part, because of Hotelling’s (1933) original paper, in which principal components were introduced in the context of providing a small number of ‘more fundamental’ variables which determine the values of the p original variables. This is very much in the spirit of the factor model introduced in Section 7.1, although Girschick (1936) indicates that there were soon criticisms of Hotelling’s method of PCs, as being inappropriate for factor analysis. Further confusion results from the fact that practitioners of ‘factor analysis’ do not always have the same definition of the technique (see Jackson, 1981). The definition adopted in this chapter is, however, fairly standard.
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Suppose that the distribution of a random variable representing the outcome of an experiment depends on two parameters xi and theta and that one wishes to test the hypothesis xi = 0 against the alternative xi > 0. If the distribution does not depend on theta when xi = 0, standard asymptotic methods such as likelihood ratio testing or C(α) testing are not directly applicable. However, these methods may, under appropriate conditions, be used to reduce the problem to one involving inference from a Gaussian process. This simplified problem is examined and a test which may be derived as a likelihood ratio test or from the union-intersection principle is introduced. Approximate expressions for the significance level and power are obtained.
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