Behavioral Ecology
doi:10.1093/beheco/arr016
Advance Access publication 15 March 2011
Original Article
No risk, no gain: effects of crop raiding and
genetic diversity on body size in male elephants
Patrick I. Chiyo,a,b Phyllis C. Lee,c,d Cynthia J. Moss,d Elizabeth A. Archie,b Julie A. Hollister-Smith,e
and Susan C. Albertsa,f
a
Department of Biology, Duke University, Durham, NC 27708, USA, bDepartment of Biological Sciences,
University of Notre Dame, Notre Dame, IN 46556, USA, cBehavior and Evolution Research Group,
Department of Psychology, University of Stirling, Stirling, FK9 4LA, Scotland, UK, dAmboseli Trust for
Elephants, PO Box 15135, Langata 00509, Nairobi, Kenya, eDivision of Neuroscience, Oregon National
Primate Research Center, Oregon Health and Science University, 505 NW 185th Avenue, Beaverton, OR
97006, USA, and fInstitute for Genome Sciences and Policy, Duke University, Durham NC 27708, USA
Body size is an important influence on the life history of males of polygynous mammals because it is usually highly correlated with
fitness and is under intense selection. In this paper, we investigated the effect of high-risk foraging behavior (crop raiding) and
genetic heterozygosity on male body size in a well-studied population of African elephants. Crop raiding, the foraging on cultivated
food crops by wildlife is one of the main causes of wildlife human conflict and is a major conservation issue for many polygynous
mammals that live in proximity to agriculture or human habitation. Body size was estimated using hind foot size, a measure strongly
correlated with stature and mass. Crop raiding predicted male size in adulthood, with raiders being larger than nonraiders. However,
elephants that became raiders were neither larger nor smaller for age when young. Enhanced growth rates and size among raiders
suggest that taking risks pays off for males. Lastly, genetic heterozygosity had no effect on size for age in male elephants, most likely
because low-heterozygosity males were rare. Risky foraging behavior can evolve as a result of strong sexual selection for large size
and condition-dependent mating success in males. We discuss the implications of these results for managing human–wildlife
conflict. Key words: body size, crop raiding, elephants, growth, growth, human–wildlife conflict, risky foraging. [Behav Ecol
22:552–558 (2011)]
INTRODUCTION
ody size is an important lifehistory–related trait in polygynous mammals, often influencing survival early in life
(Loison et al. 1999), fighting ability, and dominance at maturity and consequently reproductive success (McElligott et al.
2001; Zedrosser et al. 2007). In polygynous mammals, males
generally experience more intense selection for large body
size than females, as a result of intrasexual reproductive competition as well as female preferences for larger males during
mate choice (Poole 1989; Bowyer et al. 2007; Charlton et al.
2007). As a result of this more intense intrasexual competition
among males than among females, there is a larger variance
in reproductive success among males than females (Struhsaker
and Pope 1991; Alberts et al. 2003; Setchell et al. 2005).
In most polygynous species, males have delayed reproductive
maturation compared with females. This delay creates an opportunity for males to invest in growth in order to enhance
their reproductive competitiveness (Whitehead 1994; Post
et al. 1999; Isaac 2006; Field et al. 2007). For example, male
elephants are physiologically capable of siring offspring at 15–
17 years of age (Owen-Smith 1988) but typically do not sire
their first offspring until they are 26–30 years of age (Poole
1989; Hollister-Smith et al. 2007). In spite of strong selection
for large size, male size remains variable even within populations.
Identifying factors that generate this variation is critical for understanding male reproductive success and life-history strategies.
B
Address correspondence to P.I. Chiyo. E-mail: [email protected].
Received 16 June 2011; revised 19 January 2011; accepted 7
February 2011.
The Author 2011. Published by Oxford University Press on behalf of
the International Society for Behavioral Ecology. All rights reserved.
For permissions, please e-mail: [email protected]
In this paper, we investigate the influence of 2 factors on
male size for age in African elephants. One of these factors,
crop raiding (foraging on cultivated food crops by wildlife) is
a major conservation issue for many polygynous mammals
that live in proximity to agriculture or human habitation.
Crop raiding occurs in all elephant populations that border
agricultural areas and is a major source of human–elephant
conflict (Williams et al. 2001). Crop raiding is sex biased and
is undertaken more by males than females (Sukumar and
Gadgil 1988; Chiyo and Cochrane 2005). However, not all
male elephants raid crops even when their home ranges abut
agricultural areas (Sukumar 1995; Williams et al. 2001). Crop
raiding by independent males is initiated after they have dispersed from their maternal families at approximately 14 years
of age (Lee and Moss 1999), and we therefore predicted raiding to affect adult growth and hence size after dispersal. The
second factor we examined is multilocus heterozygosity at
microsatellite loci. Multilocus heterozygosity has been demonstrated to influence infant survival and to correlate with body
size or growth in some species (Coltman et al. 1998; Charpentier
et al. 2006). We therefore expected the effects of heterozygosity
on male body size to occur throughout life.
Crop raiding as a high-risk foraging behavior
Several studies on sexually dimorphic mammals have demonstrated that males seek more abundant, high-quality forage at
the risk of predation, whereas females may sacrifice forage
abundance to minimize predation risk when there is a positive
correlation between food abundance and predation risk (Bleich
et al. 1997; Apollonio et al. 2005; MacFarlane and Coulson 2007;
Hay et al. 2008). The high proportion of males undertaking
Chiyo et al.
•
Body size in male African elephants
high-risk foraging with regard to crop or livestock raiding has
been reported in other species, such as chimpanzees (Wilson
et al. 2007) and lynxes (Odden et al. 2002), respectively. Although male elephants engage in a variety of high-risk foraging tactics more than females, the propensity of individuals to
raid crops is variable (Sukumar 1995). Crop raiding is a highrisk foraging strategy for elephants because crop raiders are
often killed or injured by farmers and sometimes by wildlife
authorities when they are detected raiding (Haigh et al. 1979;
Cheeran et al. 2004; Mpanduji et al. 2004; Obanda et al. 2008).
In the Amboseli elephant population in Southern Kenya, 10%
of raiders were seen with spear injuries during this study
(Chiyo PI, unpublished data). Elephants appear to recognize
these risks. For example, although elephants naturally forage
both during the day and night, foraging on crops invariably
occurs at night (Graham et al. 2009) and particularly during
moonless nights (Barnes et al. 2007), probably to minimize
risks of detection by farmers. On the other hand, crop raiding
offers high nutritional returns compared with foraging on wild
plants (Sukumar 1990; Rode et al. 2006), and raiders can obtain 38% of their daily forage intake in 10% of their foraging
time while raiding crops compared with foraging on wild plants
(Chiyo and Cochrane 2005).
Trading-off safety from predators for forage abundance has
been speculated to provide a nutritional pay off that could accelerate growth or increase body size and consequently reproductive success (Corti and Schackleton 2002; Mooring et al.
2003; Hay et al. 2008). In a species with indeterminate growth
and high energetic costs of sustained growth, such as elephants, sustaining growth rates may be especially critical to
reproductive output. However, no study has demonstrated
a causal relationship between body size and such high-risk
foraging behavior. Here, we test for the effect of high-risk
foraging behavior on body size by specifically examining
whether independent male crop raiders are larger for age
compared with nonraiders and whether males that raid crops
are initially smaller or larger for age.
Microsatellite heterozygosity effects on life-history traits
Multilocus heterozygosity at microsatellite markers has been
shown to be linked to measures of fitness, such as growth
(Liu et al. 2006), infant survival (Da Silva et al. 2006; Cohas
et al. 2009), and reproductive success (Slate et al. 2000;
Zedrosser et al. 2007). These multilocus heterozygosity and
fitness correlations have been shown to result either from locusspecific effects for loci linked to functional genes that influence
fitness and are under balancing selection or from inbreeding
depression associated with genome wide loss in allelic variants
that influence fitness (Hansson et al. 2004; Gage et al. 2006).
Some studies have found positive correlations between microsatellite heterozygosity and growth rates or size for age in vertebrates (Hildner et al. 2003), whereas other studies have found
no correlations between heterozygosity and size or growth rate
(Curik et al. 2003; Overall et al. 2005; Zedrosser et al. 2006).
A limited number of studies have investigated the effects of
multilocus heterozygosity of neutral loci on size for age or
growth in natural free-ranging large mammals, specifically males
(Curik et al. 2003; Charpentier et al. 2006; Zedrosser et al.
2007), but no similar studies have been done on elephants.
Here, we test the hypothesis that elephants with a high microsatellite multilocus genetic heterozygosity are larger for age.
MATERIALS AND METHODS
Study population and age estimation
This study focused on the Amboseli elephant population in
southern Kenya, currently consisting of ;1400 elephants. This
553
population has been studied continuously since 1972 by the
Amboseli Elephant Research Project (Moss 2001; Croze and
Moss 2011). All elephants born to the Amboseli population
are individually known and recognizable from natural tears,
notches, holes, and vein patterns on pinnae, tusk characteristics, natural body marks, and shape. This population is free
ranging and uses an area nearly 8000 km2 of Maasai ranches
(Croze and Moss 2011) surrounding Amboseli National Park
and is connected to elephant populations from Kimana, Tsavo,
and Chyulu in the east and those of Kilimanjaro and Longido
controlled hunting area in the south and southwest (DouglasHamilton et al. 2005; Croze and Moss 2011). All known Amboseli elephants have ages assigned to them; elephants born since
1975 have their ages estimated to within 2 weeks, those born
between 1972 and 1974 have ages estimated to 63 months, and
elephants born between 1969 and 1971 have ages estimated to
within 1 year. Elephants born before 1969 have ages estimated
to within 2–5 years depending on the time difference between
when a mother was last seen without a calf and when she was
first seen with a new born calf. All age estimations are validated
from long-term observations of growth and body shape as well
as tooth ages when dead (Moss 2001).
Estimation of elephant size from footprint measurements
Footprint measurement is a reliable and well-established noninvasive method for determining elephant size (Western et al.
1983). Elephant hind footprint length is highly correlated with
height at the shoulder, accounting for up to 93% of the variance in male elephant height in African elephants (Lee and
Moss 1995) and 94% in Asian elephants (Kanchanapangka
et al. 2007). Footprint length is also highly correlated with
body mass in both species of elephants. In Asian elephants,
forefoot circumference was found to account for 86% of variance in body weight (Kanchanapangka et al. 2007). We estimated the length of the hind foot from measurements of
footprint impressions left on the soil by known individuals.
Specifically, we measured the linear distance perpendicular to
the short foot axis from the outer rear edge of the footprint to
the internal arch of the toe excluding the toenail imprint. For
any given sighting, we took several opportunistic measurements
of footprints whenever the soil substrate allowed delineation
of footprints and whenever we were able to observe footprints
for target individual elephants. We measured 650 footprint
sizes from 302 unique individuals between 1976 and 2007.
These include 120 measurements collected from 36 unique
individuals that we observed to raid crops in 2005–2007. Only
46 unique males measured in 1976/1991 were measured again
in 2005/2007.
Genetic analysis and sample collection
We used 2 sets of genetic data in this paper. First, we used
genotypes of known individuals from recent genetic studies
on this population (See Archie et al. 2007, 2008) for whom we
had footprint measurements (n ¼ 119 males). Second, we
collected fecal samples from 50 known males that were not
previously genotyped for a genetic analysis. From these fecal
samples, we extracted DNA using a QIAamp DNA Stool Mini
Kit (Qiagen, Germantown, MD) following a modified protocol (Archie et al. 2003). All individuals were genotyped at
a minimum of 8 loci and up to 11 loci from previous studies.
These included 1 dinucleotide locus (LAFMS02; Nyakaana
and Arctander 1998) and 10 tetranuclotide loci (LaT05,
LaT07, LaT08, LaT13, LaT16, LaT17, LaT18, LaT24, LaT25,
and LaT26; Archie et al. 2003). We used the polymerase chain
reaction (PCR) protocols detailed in Archie et al. (2003) to
amplify DNA from the loci of interest. PCR products were
Behavioral Ecology
554
separated using Applied Biosystems 3730XL DNA Analyzer
and analyzed using Genemapper v.3.7 (Applied Biosystems,
Beverly, MA). Microsatellites alleles were scored using GeneMarker v.1.6. (SoftGenetics State College, PA). For each sample, we ran PCR and genotyping twice if the initial PCR product
was scored as a heterozygote and 3–4 times if it was a homozygote, in order to minimize error associated with spurious alleles
and allelic drop out (Archie et al. 2006). We tested all loci for
Hardy–Weinberg equilibrium and for the presence of null alleles (non amplifying alleles) using CERVUS software (Marshall et al. 1998; Kalinowski et al. 2007; See Table 1). We
calculated a weighted multilocus homozygosity index for
119 male elephants where we had both footprint measurements and genetic data. We used the method of Aparicio
et al. (2006) to calculate homozygosity. We then derived multilocus heterozygosity by subtracting the homozygosity value for
each individual from one.
Identification of crop raiders
Identification of crop raiders was a multistep process (Chiyo
et al. 2011). In the field, we either identified crop raiders by
tracking elephants for several hours following a farm raid or,
when we were not able to track raiders, by collecting their dung
from raided farms. For elephants that we tracked and located,
we could visually identify known members of the Amboseliborn elephant population. In cases, where we were not immediately able to ascertain their identities, we took photos and
later matched these photos with a database of all Amboseliborn males. Dung collected from raided farms was preserved
in 95% ethanol in the field and later brought to the lab at Duke
University. In the lab, we extracted and genotyped DNA from
the dung of these unknown crop raiders that we collected from
raided farms. We genotyped on average 6 loci (LAFMS02,
LaT05, LaT08, LaT13, LaT16, and LaT24) for samples collected
from farms. We then compared the genotypes of crop-raiding
elephants collected over a period of 2 years with genotypes of
586 known male and female elephants.
In order to match genotypes, we had to determine the minimum number of loci required to discriminate between genetic
samples collected from different individuals. We did this by calculating the probability of identity (PI), that is, the probability
that a pair of animals will match at a specified number of loci.
Previous studies have identified a PI threshold of 0.0001 as
sufficient for discriminating between genotypes of different
individuals (Waits et al. 2001; Creel et al. 2003), we therefore
sought to identify the number of loci that would provide
Table 1
An analysis of allele frequency in the Amoseli elephant population
showing that all loci did not differ significantly (as shown in the
column of probability values) from the expected frequency under
the Hardy-Weinberg equilibrium
Locus
Number of
alleles per
locus
Number of
individuals
typed
Observed
frequency
Expected
frequency
P
value
LAF2
LAT5
LAT7
LAT8
LAT13
LAT16
LAT17
LAT18
LAT24
LAT25
LAT26
7
14
20
15
9
10
13
12
11
9
13
575
586
580
586
586
582
575
573
584
556
530
0.722
0.865
0.916
0.851
0.706
0.831
0.857
0.819
0.818
0.817
0.868
0.743
0.857
0.917
0.841
0.717
0.842
0.821
0.827
0.827
0.808
0.874
0.574
0.691
0.261
0.311
0.627
0.272
0.134
0.337
0.128
0.208
0.882
a similar threshold for our study population. We calculated
PI from allele frequency using the formula provided by Waits
et al. (2001). This formula is based on a theoretical expectation of Hardy–Weinberg equilibrium. From calculated PI values, genotyping 4 loci (i.e., PI ¼ 0.00004) was sufficient for
individual identification. We therefore treated 2 genotype
samples as coming from the same individual if 4 or more loci
matched. We also allowed for a mismatch at a maximum of 1
additional locus for matched pairs to account for possible
genotyping error. Using this criterion, we matched similar
genotypes using the CERVUS software (Marshall et al. 1998;
Kalinowski et al. 2007).
Using the fecal genotyping and elephant observations, we
confirmed the identities of 52 Amboseli elephants that were
crop raiders. In combination with population simulations
(Chiyo et al. 2011), we estimated that a total of approximately
84 elephants raid crops in Amboseli, suggesting that there are
likely a few raiders among the elephants we classified as nonraiders (false negatives). We do not expect this to significantly
affect our result because the proportion of unidentified
raiders that might occur in the sample of ‘‘nonraiders’’ was
small relative to true nonraiders (;15%), and any effect of
these false negatives will be to weaken our power to detect the
effect of raiding on size for age.
Statistical analyses
Our goal was to test the hypothesis that raiders are large for size
as a result of raiding crops. However, our footprint size data
were unbalanced; we had genetic data for some but not all individuals, and we had repeated measurements from a small fraction of individuals taken at irregular intervals. Our ability to
estimate growth rate directly by fitting slopes of age for size for
individual animals was limited because even among animals
with repeated measures we had an average of only 2 measurements per individual. Consequently, we used a linear mixedeffects model framework to determine the effects of raiding
behavior and multilocus heterozygosity on elephant size for
age. Elsewhere, residuals of foot length for age from sexspecific von Bertalanffy growth curve (Lee and Moss 1995)
have been used, but the mixed effects model was used here
because it is an effective formal way to deal with repeated measurements and an unbalanced data set. We carried out these
analyses on log-transformed male age ln(Xi 1 1) and footprint
ln(Yi) data because the relationship between footprint size and
age was nearly asymptotic. We added 1 to each male age (Xi)
because some values for male age were close to zero at the time
of footprint measurement, making it impossible to normalize
data through a log transformation. Multilocus heterozygosity
was also transformed using arcsine transformation.
We ran 2 separate analyses based on male life stages because
we expected crop raiding to affect male size only during a later
life stage (or 16 years and older) and not during an early life
stage (or 10 years and younger). The first analysis included
males 16 years and older because males at this age are independent and spend most of the time away from their mothers
with other males where they may initiate raiding. Sixteen years
of age is also the youngest age an elephant was observed to
raid in Amboseli and follows the mean age at independence
from the natal family in Amboseli (average age is 14 years, and
range is from 8–19 years; Lee and Moss 1999). In a second
analysis, we included only males aged 0–10 years old because
males in this age category are unlikely to raid because they are
still with their natal family and are thus spending most of their
time with their mothers; we found no evidence for raiding by
females in Amboseli (Chiyo et al. 2011).
For each male life stage (0–10 years and 16 years and above),
we first fitted a full mixed-effects model that included
Body size in male African elephants
555
footprint size as a response variable and male age, male raiding status, multilocus heterozygosity, interaction between age
and raiding status, and the interaction between age and heterozygosity as fixed effects. For each model, we used a random
intercept and individual elephant ID as a nesting factor because we had repeated measurements for some elephants. We
then dropped nonsignificant fixed effects from the full model
in a stepwise manner starting with the least significant until
we were left with a model with only significant fixed effects
(Pinheiro and Bates 2004). In all cases in which we used 3 or
more fixed effect factors, age was the only significant fixed
effect for each elephant life stage analysis. As a result, we ran
2 models for each life stage analysis; a model including raiding status and age, and a model including heterozygosity and
age. We fitted these 2 models separately in order to avoid Type
II error because of low statistical power, which could result
from the inclusion of many parameters in the model or from
a reduction in sample size after the elimination of unbalanced
covariate data.
All statistical analyses were carried out in S1, 8.1 (TIBCO
Software Inc, Palo Alto, CA).
RESULTS
Crop-raiding effects on size
Crop raiding had a positive effect on foot size for age for males
16 years and older but not for males 0–10 years (Table 2), such
that males observed to raid crops were larger for age than those
not observed to raid (Figure 1). However, males that became
raiders were not larger for age when young (0–10 years old)
compared with same-aged males that were not subsequently
observed to raid (Figure 1, Table 2). In other words, raiders
became large for age only after they began raiding, suggesting
that raiding affected male body size rather than male body
size determining raiding status.
Microsatellite heterozygosity effects on size
Multilocus heterozygosity had no significant effect on size for
age for males 10 years or younger or males 16 years and older
(Table 2). We did not explore locus-specific effects because of
a lack of a general effect or trend in the predicted direction as
well as the lack of a priori expectations of locus-specific heterozygosity on size for age. The distribution of multilocus
heterozygosity in the Amboseli population was skewed toward
higher values (Figure 2). The mean (6 standard deviation)
heterozygosity for 119 males from this population was (0.8 6
0.147).
DISCUSSION
Our results indicate that foraging behavior such as raiding
crops with a high risk of injury or mortality can lead to gains
in body size. Although we cannot unambiguously identify the
causal link between body size and crop raiding (and we did
not explicitly model interactions because of the unbalance
measurements we had for raiders), the fact that our data indicated that raiders were not largefor age before they began
raiding suggests that crop raiding caused males to be large for
age. This observation supports our hypothesis that high-risk
foraging has an energetic pay off and suggests that the relative
dearth of females among crop raiders relates to the fact that
males, the sex experiencing high variance in reproductive
success (Poole 1989), are more likely to take on these mortality risks in order to obtain the energy and growth payoff. An
enhanced size for age as a result of crop raiding is likely to
confer reproductive benefits to male elephants for 2 reasons.
First, their age at the onset of musth, the physiological state
of heightened sexual and aggressive behavior, will be younger
for larger males resulting in a longer breeding lifespan (Lee
et al. 2011). Male elephants experience delayed siring of offspring (Hollister-Smith et al. 2007) that extends many years
Coefficient
(SE)
df
P value
2.856
0.291
20.012
3.141
0.219
0.028
(0.016)
(0.010)
(0.022)
(0.025)
(0.008)
(0.008)
29
29
101
236
236
195
,0.001
,0.001
0.604
,0.001
,0.001
,0.001
2.910
0.274
20.015
3.145
0.218
0.007
(0.052)
(0.019)
(0.041)
(0.033)
(0.010)
(0.014)
11
11
26
154
154
97
,0.001
,0.001
0.721
,0.001
,0.001
0.646
Crop-raiding effects:
On males
0–10 years
Intercept
Age
Raiding status
On males
Intercept
161 years
Age
Raiding status
Heterozygosity effects:
On males
Intercept
0–10 years
Age
Heterozygosity
On males
Intercept
161 years
Age
Heterozygosity
The coefficients indicated for age and intercept represent the
baseline coefficient for non crop-raiding males, and the coefficient
for raiding status represents an additional effect of raiding on size.
Elephant ID is incorporated into the model as a random intercept.
Male age (11) in years and foot size in centimeters were transformed
into the natural logarithm, and we used arcsine transformation for
heterozygoszity. We used a random intercept for all the models
displayed. SE, standard error; df, degrees of freedom.
3.7
Model: fixed
effects
Ln of foot size in centimeters
Covariate
4.0
Table 2
Coefficients for the effect of crop-raiding status and genetic
heterozygosity on foot size for age in male elephants presented
separately for males 0–10 years old, before individuals that became
raiders initiated raiding and 16 and more years of age after they
initiate raiding
3.9
•
3.8
Chiyo et al.
2.8
3.0
3.2
3.4
3.6
3.8
4.0
Ln of age+1 in years
Figure 1
Effect of crop raiding on size for age in males 161 years of age
showing that both raiders (solid line) and nonraiders (dashed line)
have the same slope (see Age and Intercept in Table 2) but different
intercepts (see raiding status in Table 2). Size is presented as a logtransformed measure of footprint size (see main text). Data for
raiders are shown as solid diamonds, whereas data for nonraiders are
shown as open circles.
Behavioral Ecology
60
0
20
40
Frequency
80
100
120
556
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1.0
Heterozygosity
Figure 2
Distribution of mean multilocus heterozygosity using microsatellites
in male Amboseli elephants, showing that multilocus heterozygosity
was generally high in this population. Heterozygosity was calculated
as 1-(HL, homozygosity by loci) estimated using the method of
Aparicio, et al. (2006).
past their maturation in reproductive physiology (Owen-Smith
1988). The delay in siring by young reproductively mature
males due to intense competition from older males provides
an opportunity for an extended period of investment in growth
and size in young males.
Second, annual reproductive performance is positively correlated with musth duration (Poole 1989; Hollister-Smith et al.
2007), and the duration of musth is dependent on condition
and body size as well as age of individual males. Males with
access to reliable, easily digested, and high energy human
crops experience longer musth episodes while those with limited energy are less likely to experience musth (Poole 1989;
Sukumar 2003). Larger males may also have increased reproductive success because they are preferred by females as mates
(Moss 1983; Poole 1989; Hollister-Smith et al. 2007).
Microsatellite heterozygosity has been shown to be positively
correlated with fitness traits in many populations, but in this
study, mean individual heterozygosity of microsatellites loci
was not correlated with size. Correlations between heterozygosity of neutral markers and fitness traits, such as size and growth
rate are weak or absent in outbred populations and stronger
in inbred populations (Rowe and Beebee 2001; Hildner et al.
2003; Overall et al. 2005). The lack of a relationship between
multilocus heterozygosity and size for age in the Amboseli
elephant population may simply reflect the high heterozygosity and extensive outbreeding in this population. This outbreeding is a consequence of inbreeding avoidance (Archie
et al. 2007) and extensive gene flow between Amboseli and
adjacent elephant populations.
Our findings on the sex-specific nature of high-risk behavior
and the consequences of such behavior to gains in body size may
generalize to other sexually dimorphic species with high reproductive variance because high-risk foraging is widespread
among males of many sexually dimorphic species. Examples include fallow deer, (Apollonio et al. 2005) roe deer (Mysterud
et al. 1999), moose (Miquelle et al. 1992), elk (Winnie and
Creel 2007), Dall’s sheep (Corti and Schackleton 2002), bighorn sheep (Berger 1991; Mooring et al. 2003), mountain
sheep (Bleich et al. 1997), and African buffalo (Hay et al.
2008). The prevalence of additional physiological traits in species exhibiting this behavior such as condition-dependent mating strategies (musth and rut) and prolonged growth in males
suggests that these traits are related to the evolution of highrisk foraging behavior in males of sexually dimorphic species.
Our findings also relate to the fact that high-risk foraging
behavior such as crop raiding is a major cause of wildlife–
human conflict. Wildlife–human conflict is a major conservation issue for many polygynous mammals like primates and
carnivores that live in proximity to agriculture or livestock
(Bunnefeld et al. 2006; Wilson et al. 2007; Hazzah et al.
2009). Because these findings suggest that crop raiding or
livestock killing by wildlife is a male life-history tactic commonly observed in polygynous mammals, conflict will likely
be a recurring problem in most wildlife populations found
in proximity to humans. Managing such conflict will require
measures that separate agriculture or livestock from conservation areas through use of wildlife barriers (Hoare 1995). It will
also require land use practices that are compatible with wildlife conservation in proximity to protected areas through zoning (Linnell et al. 2005; Woodroffe et al. 2005). Alternatively,
coexistence between wildlife and humans can also be encouraged by use of measures that increase public tolerance for the
damage caused by wildlife (Woodroffe et al. 2005). On the
other hand, approaches that directly target males such as control shooting are likely to have limited effect in reducing conflict (e.g., Hoare 2001) and will negatively influence the
evolution of body size in these populations. Because high-risk
foragers grow large, culling of males for purposes of reducing
conflict is likely to eliminate individuals that are larger and
reproductively competitive. Evolutionary consequences of selective killing have been demonstrated elsewhere. For example, hunting pressure has been demonstrated to decrease
body size and horn size of male bighorn sheep (Coltman
et al. 2003) and to increase the incidence of tusklessness in
African and Asian elephants (Jachmann et al. 1995).
FUNDING
US Fish and Wildlife Service (grant number AFE-0314/
6-G085) and the National Science Foundation (grant number
IBN0091612) to S.C.A. Further support was provided by the
Amboseli Trust for Elephants.
We thank the Office of the President of the Government of Kenya for
permission to conduct this research through Ministry of Education,
department of Science and Technology permit number 13/001/35C
225. We also thank Kenya Wildlife Services and Amboseli National
Park staff for their hospitality and collaboration during the study.
Finally, we thank Norah Njiraini, Katito Sayialel, and Soila Sayialel
for their invaluable knowledge on elephant identification and for
their support in the field.
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