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Animal behaviour
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Sibling competition and hunger increase
allostatic load in spotted hyaenas
Sarah Benhaiem, Heribert Hofer, Martin Dehnhard, Janine Helms
and Marion L. East
Research
Cite this article: Benhaiem S, Hofer H,
Dehnhard M, Helms J, East ML. 2013 Sibling
competition and hunger increase allostatic load
in spotted hyaenas. Biol Lett 9: 20130040.
http://dx.doi.org/10.1098/rsbl.2013.0040
Received: 15 January 2013
Accepted: 4 April 2013
Subject Areas:
behaviour, ecology, evolution
Keywords:
sibling competition, glucocorticoids, allostatic
load, stress, spotted hyaena
Author for correspondence:
Sarah Benhaiem
email: [email protected]
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rsbl.2013.0040 or
via http://rsbl.royalsocietypublishing.org.
Leibniz Institute for Zoo and Wildlife Research (IZW), Alfred-Kowalke-Strasse 17, Berlin 10315, Germany
Allostatis is the process of maintaining homeostatis through behavioural or
physiological responses to challenges, and its cumulative energetic cost
is termed allostatic load. The allostatic load hypothesis predicts that
hunger and the mechanisms that establish and maintain social dominance
should have a strong impact on allostatic load. In spotted hyaenas, dominance between twin siblings emerges during intense early competition for
maternal milk and involves trained winner/loser effects. Conflict over
access to teats declines with age as behavioural dominance conventions
are established. In young litters, the allostatic load of subordinates
measured in terms of faecal glucocorticoid metabolite concentrations
(fGMCs) should be higher than that of dominants. When low milk provisioning threatens survival, hungry subordinates are more assertive,
particularly when competing against a dominant sister. Dominants challenged by assertive subordinates should have allostatic loads and fGMCs
above those of dominants with subordinates that adhere to dominance
conventions. We show that in young litters, subordinates had significantly
higher fGMCs than dominants, and dominant sisters had significantly
higher fGMCs than dominant brothers. When hungry, both dominants
and subordinates had significantly higher fGMCs than when fed. Our
results provide evidence that hunger and sibling competition affect
allostatic load in spotted hyaenas.
1. Introduction
Social status may profoundly affect how animals cope with challenges [1].
Glucocorticoids help maintain allostasis by mobilizing energy reserves and
thus elevated glucocorticoid concentrations indicate allostatic load [2]. Socially
subordinate individuals subject to high-level aggression by dominants
should have higher allostatic loads than dominants, particularly when dominants
restrict their access to food [3]. When hunger threatens their survival, subordinates are more assertive [4–6], thereby probably increasing allostatic load in
dominants [3].
Within-brood/litter dominance can be established during intense early sibling competition [6]. In many bird species, subordinate siblings have higher
glucocorticoid concentrations than dominants [7– 9], particularly when
hungry [7,10]. We present the first study of the impact of intense within-litter
competition [11] on allostatic load in twins of a free-ranging mammal, the
spotted hyaena (Crocuta crocuta). Dominants monopolize maternal milk,
thereby obtaining higher growth rates than their subordinate siblings [5,12].
Insufficient milk provisioning results in early facultative siblicide by enforced
starvation of subordinates [12,13], particularly those competing against a
sister [5,13]. Within-litter dominance is established within three months of
birth through trained winner/loser effects [5]. Littermates exclusively depend
on [12] and intensively compete for [11] highly nutritious milk during their
initial six months of life. Dependence on milk and sibling conflict decline
& 2013 The Author(s) Published by the Royal Society. All rights reserved.
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(a)
(b)
50
dom
sub
2
fGMC ng g–1
dom
30
sub
20
10
low
medium
high
young
age category
prey abundance
(c)
old
60
fGMC ng g–1
50
40
30
20
10
0
litter sex composition
Figure 1. Faecal glucocorticoid metabolite concentrations (fGMCs) of siblings in relation to (a) prey abundance, the interactions between (b) within-litter dominance
status (dom, dominant (white); sub, subordinate (grey)) and age category and (c) within-litter dominance status and litter sex composition (CC, all-female;
CF, dominant female and subordinate male; FC, dominant male and subordinate female; FF, all-male). Bars, mean + s.e.m.
after this period and dominance conventions typically operate [5,11]. When hungry, subordinates competing against a
sister are more assertive than subordinates competing against
a brother [5]. For these reasons, we expect allostatic load
measured by faecal glucocorticoid metabolite concentrations
(fGMCs; [14]) to be higher in (i) subordinates than in dominants in litters younger than six months, (ii) dominant
sisters than in dominant brothers and (iii) both dominants
and subordinates when hungry.
2. Material and methods
(a) Study population
We studied three clans in the Serengeti National Park, Tanzania,
between 2007 and 2010, which defended territories with large
fluctuations in prey abundance [15]. These fluctuations profoundly affected maternal milk provisioning. When prey
abundance was high, all mothers nursed their litters daily and
when low only every 1 – 6 days [16], because they undertook
long-distance foraging (‘commuting’) trips (80 – 140 km; [15]).
At medium prey abundance, only mothers of lower social
status commuted [17]. All animals were individually recognized
and monitored at clan communal dens at dawn and dusk [15].
Subordinates were the most submissive siblings [11]. Cubs
were sexed [18], aged [11] and categorized as ‘young’ (less
than six months) or ‘old’ (between six and 24 months). Adults
were older than 24 months.
(b) Faecal glucocorticoid metabolites
Faeces were collected immediately after defaecation, mixed, subsampled and stored frozen as previously described [19]. We
quantified fGMCs as ng g – 1 faeces using a cortisol-3-CMO
enzyme immunoassay validated for spotted hyaenas [19]. Methodological pitfalls [20] associated with the measurement of
fGMCs require careful consideration (see detailed discussion in
the electronic supplementary material).
We measured fGMCs in 175 faecal samples for 77 twins aged
47 – 492 days, including 38 dominants (19 males and 19 females)
and 39 subordinates (20 males and 19 females). These data (see
electronic supplementary material) incorporated paired samples
from both members of 23 young litters: four all-female, six allmale and 13 mixed-sex twins (eight with dominant females
and five with dominant males). To verify that sex differences in
fGMCs were the consequence of sibling competition and not
sex differences in metabolism [20], we compared fGMCs between
29 singleton males and 23 singleton females aged 42 – 467 days
using 132 samples.
(c) Statistics
We used R (R Development Core Team, v. 2.15.0). The
threshold for significance was at 5 per cent, tests were twotailed. Statistics are quoted as mean + s.e.m. We used linear
mixed-effects models (lme4 library) with the reciprocal square
root transformation of fGMCs as the response, and mother
and cub identities as scalar random effects to test whether
fGMCs were affected (i) in twins by prey abundance, the
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fGMC (ng g–1) of dominants
100
80
60
40
3
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sex composition (F3,19 ¼ 3.574, p ¼ 0.035; figure 2). Dominant
females in same-sex (28.3 + 9.5 ng g – 1) and mixed-sex
(70.4 + 37.5 ng g – 1) litters had significantly higher fGMCs
than dominant males in same-sex (14.1 + 3.3 ng g – 1) and
mixed-sex (14.6 + 2.3 ng g – 1) litters. Dominant fGMCs were
not affected by subordinate fGMCs (F1,19 ¼ 1.778, p ¼ 0.20,
model r2 ¼ 0.40).
Among singletons, sex (x2 ¼ 0.738, p ¼ 0.39) and prey
abundance (x2 ¼ 1.01, p ¼ 0.60) did not affect fGMCs.
120
20
litter sex composition
Figure 2. Faecal glucocorticoid metabolite concentrations (fGMCs) of dominants younger than six months in different litter sex compositions (CC, allfemale; CF, dominant female and subordinate male; FC, dominant
male and subordinate female; FF, all-male). Bars, mean + s.e.m.
interaction between within-litter dominance status and age
category and the interaction between within-litter dominance
status and sex composition, and (ii) in singletons by sex and
prey abundance. To assess significance of fixed factors
and interactions, we used log-likelihood ratio tests (x2). To
determine significant differences between prey abundance
levels, we used a post hoc analysis based on a Markov Chain
Monte Carlo (MCMC) simulation (LMERConvenienceFunctions
library, see electronic supplementary material).
For the within-litter comparison, we used all faeces produced
by both members of the same litter when young, and calculated
mean fGMCs for dominants and subordinates. To increase
robustness, we first used a Wilcoxon signed-rank test (V ) to
check whether subordinates had higher fGMCs than their dominant siblings. We then tested the importance of litter sex
composition on fGMCs of dominants using an ANCOVA with
sex composition as explanatory variable and fGMCs of the subordinate as covariate, as we expected fGMCs of paired siblings
to be positively correlated. fGMCs were transformed using a
reciprocal square root transformation.
Residuals of all models were normally distributed (Lilliefors
test), and variances showed no heterogeneity (residual plots).
3. Results
Overall, siblings had significantly higher fGMCs during low
prey periods (x2 ¼ 7.999, p ¼ 0.018 (figure 1a) post hoc: low
versus medium p(MCMC) ¼ 0.013, low versus high
p(MCMC) ¼ 0.049 and medium versus high p(MCMC) ¼
0.90). When young, subordinates had significantly higher
fGMCs than dominants (x2 ¼ 4.168, p ¼ 0.041; figure 1b).
Dominant females with a subordinate brother had higher
fGMCs than dominants in litters with other sex compositions,
and subordinate males with a dominant brother had lower
fGMCs than subordinates in litters with other sex compositions (x2 ¼ 8.292, p ¼ 0.040; figure 1c).
Within-litter comparison of young individuals revealed
significantly higher fGMCs (V ¼ 64, exact p ¼ 0.023) in subordinates (49.8 + 13.7 ng g – 1) than in dominants (36.2 +
16.4 ng g – 1). fGMCs of young dominants varied with litter
In young twins, subordinates had higher fGMCs than
dominants, and amongst dominants, females had higher
fGMCs than males, particularly when their siblings were
brothers. These results indicate that, as predicted [2,3],
competition for dominance status and access to milk
increased allostatic load.
Experimentally enlarged guinea pig (Cavia aperea) litters
had elevated cortisol concentrations [21]. Our study is the
first to demonstrate an effect of within-litter dominance on
glucocorticoids in a free-ranging mammal. Higher fGMCs
in subordinates than dominants probably resulted from
an increased allostatic load during several months of
competition for and frequent aggressive exclusion from
milk [5,11].
In the Serengeti, when mothers are absent on longdistance commuting trips, litters are not nursed for several
days, requiring cubs to mobilize energy from body reserves
[11 –13]. During periods of low prey abundance with infrequent nursing, twins but not singletons had higher fGMCs
than when they were nursed daily, suggesting that sibling
competition had a stronger effect than hunger on allostatic
load. Furthermore, the fGMCs we report from twins should
be higher than those in populations where long-distance
foraging is absent [22].
Dominants should have a high allostatic load when frequently challenged by subordinates [3]. In spotted hyaena
litters, dominant females are more challenged by hungry
subordinates than dominant males [5], possibly because subordinates with dominant sisters are more at risk of facultative
siblicide than subordinates with dominant brothers [5,13,23].
Accordingly, dominant sisters had nearly four times higher
fGMCs than dominant brothers. Dominant blue-footed
booby (Sula nebouxii) siblings also showed marked increases
in corticosterone concentrations when paired with nonsubmissive chicks [24]. An alternative explanation [20] that
sex-specific metabolism might cause differences in glucocorticoid concentrations is unlikely, because we found no
difference in fGMCs between singleton males and females.
Hence, the higher allostatic load of twin females most likely
resulted from sibling competition.
Our study suggests that sibling competition, its impact
on access to milk and the maternal ‘commuting’ system
are key factors determining allostatic load in spotted
hyaena twins.
We thank COSTECH, TAWIRI and TANAPA for support, A. Francis,
T. Shabani, D. Thierer, K. Wilhelm and M. Andris for assistance,
A. Schwarm, W. Karasov and four referees for constructive comments
and the IZW for financial support.
Biol Lett 9: 20130040
4. Discussion
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