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Humans excel in cooperative exchanges between unrelated individuals. Although this trait is fundamental to the success of our species, its evolution and mechanisms are poorly understood. Other social mammals also build long-term cooperative relationships between non-kin, and recent evidence shows that oxytocin, a hormone involved in parent-offspring bonding, is likely to facilitate non-kin as well as kin bonds. In a population of wild chimpanzees, we measured urinary oxytocin levels following a rare cooperative event-food sharing. Subjects showed higher urinary oxytocin levels after single food-sharing events compared with other types of social feeding, irrespective of previous social bond levels. Also, urinary oxytocin levels following food sharing were higher than following grooming, another cooperative behaviour. Therefore, food sharing in chimpanzees may play a key role in social bonding under the influence of oxytocin. We propose that food-sharing events co-opt neurobiological mechanisms evolved to support mother-infant bonding during lactation bouts, and may act as facilitators of bonding and cooperation between unrelated individuals via the oxytocinergic system across social mammals.
, 20133096, published 15 January 2014281 2014 Proc. R. Soc. B
Klaus Zuberbühler
Roman M. Wittig, Catherine Crockford, Tobias Deschner, Kevin E. Langergraber, Toni E. Ziegler and
in related and unrelated wild chimpanzees
Food sharing is linked to urinary oxytocin levels and bonding
Supplementary data
"Data Supplement"
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Cite this article: Wittig RM, Crockford C,
Deschner T, Langergraber KE, Ziegler TE,
Zuberbu¨hler K. 2014 Food sharing is linked to
urinary oxytocin levels and bonding in related
and unrelated wild chimpanzees. Proc. R. Soc.
B 281: 20133096.
Received: 26 November 2013
Accepted: 11 December 2013
Subject Areas:
behaviour, physiology
cooperation, food-sharing, bonding
mechanism, chimpanzee, oxytocin,
non-invasive hormone sampling
Authors for correspondence:
Roman M. Wittig
Catherine Crockford
These authors contributed equally to this
Electronic supplementary material is available
at or
Food sharing is linked to urinary oxytocin
levels and bonding in related and
unrelated wild chimpanzees
Roman M. Wittig
, Catherine Crockford
, Tobias Deschner
Kevin E. Langergraber
, Toni E. Ziegler
and Klaus Zuberbu¨hler
School of Psychology, University of St Andrews, St Andrews, UK
Department of Primatology, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany
Budongo Conservation Field Station (BCFS), Masindi, Uganda
Department of Anthropology, Boston University, Boston, MA, USA
Wisconsin National Primate Research Center, Madison, WI, USA
Cognitive Science Centre, University of Neucha
tel, Neucha
tel, Switzerland
Humans excel in cooperative exchanges between unrelated individuals.
Although this trait is fundamental to the success of our species, its evolution
and mechanisms are poorly understood. Other social mammals also build
long-term cooperative relationships between non-kin, and recent evidence
shows that oxytocin, a hormone involved in parentoffspring bonding, is
likely to facilitate non-kin as well as kin bonds. In a population of wild chim-
panzees, we measured urinary oxytocin levels following a rare cooperative
event—food sharing. Subjects showed higher urinary oxytocin levels after
single food-sharing events compared with other types of social feeding, irre-
spective of previous social bond levels. Also, urinary oxytocin levels
following food sharing were higher than following grooming, another coop-
erative behaviour. Therefore, food sharing in chimpanzees may play a key
role in social bonding under the influence of oxytocin. We propose that
food-sharing events co-opt neurobiological mechanisms evolved to support
motherinfant bonding during lactation bouts, and may act as facilitators of
bonding and cooperation between unrelated individuals via the oxytocinergic
system across social mammals.
1. Introduction
The ability to cooperate is seen as crucial to the exceptional biological success of
humans as a species [13]. Sharing food and allo-maternal childcare, among
other behaviours, are common forms of cooperation, which frequently occur
among related and unrelated individuals in huntergatherer and industrialized
societies [ 4,5]. Despite the significance of cooperation as a biological phenom-
enon, its evolution and mechanisms remain poorly understood [3,6]. This is
especially true for cooperation occurring between unrelated individuals in
non-reproductive contexts.
Recent studies show that, in addition to humans, other social mammals
form cooperative relationships between unrelated adults, which can last over
months or years (chimpanzees [7], baboons [8,9] and feral horses [10]).
Crucially, there is evidence that individuals who maintain such cooperative
relationships have more offspring than those who do not [8,1012]. Long-
lasting cooperative relationships have also been referred to as strong social
bonds [813], which are characterized by high rates of cooperative behaviours,
such as grooming and food sharing [813].
Recent evidence suggests that an endocrinological mechanism promoting non-
kin coopera tiv e rela tionships ma y involve the oxytocinergic s y stem [14,15]. In
humans and other social mammals, the hormone oxytocin plays a central role in
facilitating bonding betw een mother and offspring, and between mating partners
[1618]. Physiologically, oxytocin acts in the brain by reducing anxiety and fear
2014 The Author(s) Published by the Royal Society. All rights reserved.
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[19,20], enhancing social memory [1618,21] and activating
neural rew a rd circuits [21]. If exogenously administered, oxyto-
cin enhances cooperativ e behaviour [22,23] between related
animals, and behaviours associated with trust [2426] and
generosity [27] between unrelated humans. When centr ally
administered, oxytocin enhances both affiliation with bonding
partners and av ersion to s trangers in unr ela ted female v oles [14].
Exactly how cooperative bonds are established under the
influence of oxytocin, however, is not well understood
[1618]. In humans, the concentration of plasma oxytocin is
related to the perceived closeness to [28] or support received
by [29] a partner, suggesting a relation between higher oxyto-
cin levels and stronger social bonding. Such a link is also
evident in chimpanzees, where grooming among bonding
partners is associated with higher urinary oxytocin concen-
tration than grooming between non-bonding partners [15].
Additionally, in humans, exogenously administered oxytocin
enhances the encoding of social memory, both of positive [30]
and negative [31] events, suggesting that higher oxytocin
levels improve memorization of social interactions. This is
particularly relevant for the question of how cooperative
relationships are maintained and formed between two part-
ners, especially if the cooperation is based on reciprocation
[32,33]. In sum, higher oxytocin concentrations may be
related to better cooperation via stronger bonding and
better social memory.
Methodologically important is the fact that oxytocin not
onlyacts within the brain, but is also released into the peripheral
circulation before being excreted in urine, although the exact
nature of the relationship between central and peripheral
releases have yet to be clarified [3439]. Significantly, peri-
pheral measures of oxytocin from plasma or urine correlate
positively with psychological and behavioural patterns, such
as aversion reduction in male mice[19], social contact in marmo-
sets [40], lactation in rhesus macaques [41], rates of affiliative
behaviours in pair-bonded tamarins [42] and grooming in
closely bonded chimpanzees [15], indicating that peripheral
oxytocin levels reflect central processing of oxytocin.
In this study, we examine the association of urinary oxy-
tocin levels with food-sharing events between kin and
non-kin. This cooperative behaviour is widespread across the
animal kingdom, with well-documented cases in insects, birds
and mammals [4347]. Food sharing has been defined as the
owner of a food resource allowing others to access it, despite
the fact that it could be monopolized [47]. The benefits of getting
access to food already in somebody else’s possession are self-
evident, but what do the donors gain? Plausible explanations
are that donors benefit through mating advantages [43,44],
maintenance of pair bonds [43], reduction of harassment [47],
or future reciprocation and exchange [48].
In most species, food sharing occurs between kin, such
as parents provisioning their offspring (birds [44], mammals
[45,47,49]), or between mating partners (insects [44], birds
[43], mammals [45,47,50], humans [51]). Food sharing between
unrelated individuals outside the mating context is rare but has
been reported for humans, vampire bats, chimpanzees and
bonobos [13,46,48,49,52]. In chimpanzees and vampire bats,
food sharing typically occurs between individuals that also
engage in other cooperative behaviours at higher rates, such
as grooming and providing coalitionary support [13,49,52
54]. In chimpanzees, it is often discussed in the context of
meat sharing after hunting other primates [50,5256]. Meat is
a high-value, monopolizable resource, which frequently
precipitates fighting and sharing [56]. There is evidence that
males share meat with other males in exchange for receiving
support [54], or with females to receive mating opportunities
[50] (cf. [54]). Additional reasons proposed for meat sharing
are to reinforce cooperative hunting by discriminating against
cheaters [56], or to reduce harassment of begging in order to
allow the donor time to eat [55]. Food sharing in chimpanzees,
however, is not restricted to meat but has also been reported
with non-meat foods, for example honey [52], or large fruits
such as Carica papaya [57] or Treculia africana [52]. For some
food, the access to food is monopolizable and can be shared,
such as when access to stone hammers for cracking Panda
oleosa nuts is limited [52] or when holes in dead trunks of
Raphia farinifera trees are too small for more than one chimpan-
zee to simultaneously access the rotting wood inside [58].
To investigate whether food sharing in chimpanzees is
linked to higher urinary oxytocin levels, we compared subjects’
urinary oxytocin levels after single food-sharing events and
after other types of social feeding without sharing in the
Sonso community of Budongo Forest, Uganda [59]. If urinary
oxytocin levels after food sharing were higher than after
social feeding, this would indicate that food sharing and bond-
ing are closely linked. Given the hypothesized importance
of food sharing for kin and pair bonding [44,46,51], we
examined the relation between urinary oxytocin concen-
trations, relatedness and bondedness. With regard to the
proposed importance of meat sharing in malemale bond-
ing [54] and in the sex-for-meat hypothesis [50], we further
investigated the relationship between urinary oxytocin concen-
trations, meat sharing and the sex of sharers. Finally, to
examine whether different cooperative acts might be associated
with different urinary oxytocin levels, we investigated the
magnitude of the difference in urinary oxytocin levels after
food-sharing events compared with grooming events.
2. Material and methods
We analysed 79 urine samples from 26 chimpanzees (females:
10 adults, i.e. more than 15 years of age; three subadults, i.e.
between 10 and 15 years of age; males: six adults, seven suba-
dults; mean sample per chimpanzee + s.d. ¼ 3.0 + 1.97) of the
Sonso community in Budongo Forest, Uganda [59], between Jan-
uary 2009 and July 2010. We collected urine samples if subjects
had engaged in no affiliative behaviours (e.g. grooming or copu-
lation) other than the target behaviour in the hour prior to
urination. This was determined through focal sampling [60] of
subjects or all-occurrence sampling [60] of chimpanzee sub-
groups (or ‘parties’). The Composite Relationship Index (CRI)
and dominance hierarchies were also determined from focal or
all-occurrence sampling conducted between October 2009 and
July 2010 by C.C., R.M.W. and seven experienced field assistants.
Feeding time, food source and party composition were recorded
in 15 min scan samples [60]. Faecal samples for genetic analysis
of kinship were collected throughout the study period.
(a) Behavioural criteria for food sharing
Food sharing occurred when one individual was allowed access to
food in possession of another, in the absence of aggression [47] (see
electronic supplementary material, text S1). This could happen in
one of two ways. Food was passively shared, such that the possessor
allowed another to take the food, or to take over access to the food
supply, in the absence of overt coercion in the form of aggression
or screaming (see electronic supplementary material, video S1).
Alternatively, food was actively shared, such that the possessor Proc. R. Soc. B 281: 20133096
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extended the food towards the receiver and released it in the
absence of aggression (see electronic supplementary material,
video S2). Food-sharing events could thus be single momentary
events, multiple momentary events or protracted events (see elec-
tronic supplementary material, table S1). Food-sharing events
could occur with begging behaviour. Begging definitions were
taken from Gilby [55], with our additions shown in brackets. Beg-
ging was either (i) sitting and staring at the food item (or
possessor), (ii) reaching towards but not touching the food item
or possessor (with or without whimpering), (iii) touching the
food item or possessor, or (iv) placing a hand directly over the pos-
sessor’s mouth. Begging behaviours (iii) and (iv) were considered
to be low and high harassment, respectively [47,55,61].
(b) Long-term cooperation level and composite
relationship index
We assessed the quality of relationships by calculating all-
occurrence rates of the following behaviours over the current and
preceding annual quarters: coalitionary support, food sharing,
grooming, staying in (less than 1 m) proximity and aggression
[62,63]. For all behaviours, each occurrence was recorded as a
single event. From the resulting rates, we calculated the CRI,
a measure of social bond strength [15,64]. The CRI is calculated
over a period of three months and gives socio-positive (given or
received food sharing, coalitionary support, allo-grooming and
resting in less than 1 m proximity) and socio-negative (aggression
given or received) behaviours equal weight:
where SP1 ¼ rate of grooming bouts plus rate of resting in 1 m
proximity, SP2 ¼ rate of food sharing plus rate of coalitionary
support, NP ¼ rate of aggression, i ¼ individual and j ¼ dyad
partner. The index is positive when each individual within a
dyad initiates on average more socio-positive than socio-negative
interactions. ‘Bond partners’ were defined as dyads having a net
socio-positive relationship lasting more than or equal to six
months (at least two consecutive blocks of three months). This
can occur through either a mutual socio-positive relationship
(CRI . 0) during the annual quarter of the experiment and the
preceding quarter, or a large mutual socio-positive relationship
(CRI . 10) during one of the quarters and a socio-neutral or posi-
tive relationship (CRI 0) during the other quarter. According
to this, 1.9% of kin dyads and 1.6% of non-kin dyads reached
bond-partner status.
(c) Urine sampling and oxytocin extraction
Our target behaviours were single food-sharing events or 1 h of
feeding in the presence of chimpanzees without sharing food.
We collected urine samples as described by Crockford et al.
[15]. Specifically, urine was collected 1560 min after the target
behaviour (time window of urinary clearance of oxytocin for pri-
mates [65]). Occasionally, subjects were sampled after engaging
in more than one food-sharing event within the required time
window. In both conditions, samples were not collected if
grooming or copulation also occurred within 60 min prior to uri-
nation, as both of these behaviours are likely to independently
increase urinary oxytocin levels [39]. A volume of 1.1 ml of the
collected urine was pipetted into a cryovial containing 100 ml
of 0.5 N phosphoric acid and stored on ice in a thermo flask.
Solid-phase extraction was conducted later the same day [40].
All samples were then frozen until transported for assaying in
the Assay Services Unit at the NPRC, Madison, WI, using an
enzyme immunoassay kit (Assay Designs, Ann Arbor, MI; cata-
logue no. 901-153). To compensate for variation in urine
concentration, we measured creatinine (crea) levels in each
sample [66] and expressed all oxytocin values as pg mg
We validated the measurement of urinary chimpanzee oxytocin
levels through parallelism and accuracy tests, as described in a
previous paper [15].
(d) Dominance relationships
We collected pant-grunt vocalizations as a unidirectional indicator
of dominance relationships, given by the subordinate to the domi-
nant [53]. We calculated a linear dominance hierarchy for Sonso
chimpanzees on the basis of the pant-grunts using M
AT MAN v. 1.1
(see electronic supplementary material, text S2). Donors and
receivers of shared food were assigned a relative dominance
relationship according to the hierarchy matrix.
(e) Kin relationships
We collected fresh faecal samples, stored and extracted DNA fol-
lowing protocol of [15]. Dyads were classified as kin (n ¼ 11) or
non-kin (n ¼ 10) according to a combination of (i) parentage ana-
lyses based on autosomal microsatellites and (ii) mitochondrial
DNA and Y-chromosome microsatellite haplotype sharing infor-
mation [13,67]. We were able to show that that all kin partners
were either mother offspring (n ¼ 10) or maternal siblings
(n ¼ 1), and none of the non-kin partners were such close
maternal relatives (see electronic supplementary material, text
S3, S4 and table S5).
(f) Statistics
Urinary oxytocin (OT) concentrations were log
-transformed to
fit a normal distribution. Five generalized linear mixed models
(GLMM) were run with maximum-likelihood estimates in SPSS
v. 20, testing the effect of the predictor variables shown in
table 1 on the response variable of log
-transformed urinary
oxytocin levels. In model 1, we compared food-sharing events
with social feeding without food sharing. We tested the effect
of whether food is shared or not and its monopolizability on
the urinary oxytocin concentration after controlling for subjects’
sex and age. Subjects’ identity was included as a random
factor. Model 2 was divided into two separate tests due to
small sample size. Model 2a investigated the variation within
the food-sharing samples with regard to the sharers’ relationship.
We tested the effect of close kinship and bond quality on the
urinary oxytocin concentration after controlling for whether
the subject received the food. Subjects’, partners’ (interaction
partner) and dyads’ identity were included as random factors.
Model 2b examined the variation within the food-sharing samples
with regard to the possible function of meat sharing. We tested the
effect of whether the shared food was meat, and the sex combi-
nation of the sharers, on the urinary oxytocin concentration.
Subjects’, partners’ and dyads’ identity were included as random
factors. Finally, in model 3, we compared urinary oxytocin levels
after food sharing with those after another cooperative behaviour,
grooming (taken from [15]). In model 3a, we tested the effect of
food sharing compared with grooming on the urinary oxytocin
concentrations after controlling for subjects’ sex. Subjects’ identity,
partners’ identity and dyads identity were all included as random
factors. In model 3b, we tested the effect of five different behav-
ioural contexts (food sharing with bond partner, food sharing
with non-bond partner, grooming with a bond partner, grooming
with a non-bond partner and control situations) on the urinary
oxytocin concentrations, while controlling for subjects’ sex.
Subjects’ identity was included as a random factor.
Five outliers (more than 2 s.d.) were excluded from the food-
sharing dataset (three non-sharing and two sharing samples) to
be sure that they were not driving any main effects. Their distri-
bution relative to the main dataset is shown in the electronic
supplementary material (figure S1). We excluded 13 outliers Proc. R. Soc. B 281: 20133096
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(more than 2 s.d.) from the grooming dataset for the compari-
son between grooming and food sharing. Nonetheless, when
we ran the GLMMs with the full dataset, including the outliers,
the results remained remarkably similar to the GLMM results
excluding the outliers (see electronic supplementary material,
tables S2S4). Variables did not exhibit problems of collinearity
[68] (Kendall’s
and Spearman’s r , 0.7 in all cases). As a
check of the overall significance of all predictor variables, we
ran likelihood ratio tests comparing the full model with the
respective null model (comprising only the random effects). We
only considered significant effects of the individual predictors
if the full model explained the variance significantly better
than the null model.
As models 2a and 2b investigated many predictor variablesrela-
tive to the number of cases (n ¼ 33, d.f. ¼ 3ord.f.¼ 5), reduced
power may have led to false negatives (i.e. erroneously non-signifi-
cant effects), as well as some risk of instability in the derived
estimates. Hence, we ran an additional set of univariate GLMMs
with each including only one of the predictor variables at a time
(and the same random effects as in the full model). None of the
predictor variables tested in the univariate models reached signi-
ficance (bond type: F
¼ 0.074, p ¼ 0.787; CRI: F
¼ 0.277,
p ¼ 0.602; kin relationship: F
¼ 0.020, p ¼ 0.888; sharing
direction: F
¼ 0.008, p ¼ 0.931; food category: F
¼ 1.289,
p ¼ 0.264; sex combination: F
¼ 1.200, p ¼ 0.314), which
showed that the lack of significance in models 2a and 2b was
unlikely to be due to power issues.
3. Results
(a) Characteristics of food-sharing events
In 2009, we observed 42 food-sharing events (without overt
aggression occuring during the begging event) in the Sonso
community. Controlling for the overall observation time per
male or female, respectively, males showed an average shar-
ing rate of 0.00187 h
and females showed an average
sharing rate of 0.00176 h
. All food-sharing events sampled
included begging behaviour by the receiver before receiving
food from the donor. While the lower level of harassment
did occur often, the highest level of harassment, the receiver
placing his hand over the mouth of the donor, was never
observed. Urine samples were obtained after 33 food-sharing
and 46 social feeding events. Food items shared were meat
(46%), fruit (30%), rotten wood pith (18%) and honey (6%;
electronic supplementary material, table S1). Two-thirds of
Table 1. Predictor variables tested in the GLMMs. Model 1 refers to the GLMM shown in table 3, which tests sharing and non-sharing samples together (n ¼ 79).
Model 2 refers to the GLMM presented in table 4, using only food-sharing samples (n ¼ 33). Model 3 refers to GLMM presented in table 5, contrasting
food-sharing and grooming samples (n ¼ 182).
model name score definition n
1,3 sex of subject male subject is male 46, 102
female subject is female 33, 80
1 age of subject adult age .15 years 51
subadult age 15 years 28
1 monopolizability
of food
high food clumped in one piece or cluster 37
low many food clusters, but single cluster is defendable by one individual 42
1 food share yes partners share food 33
no partners do not share food 46
2a bond type bond sharers are bond partners 24
non-bond sharers are not bond partners 9
(2a) CRI
continuous mean CRI over two consecutive quarters of the year 33
2a kin relation kin sharers are kin-related 18
non-kin sharers are not kin-related 15
2a sharing direction receiving subject receives food 20
not receiving subject does not receive food 13
2b sex combination FF sharers are both female 10
MF one sharer is male, the other is female 14
MM sharers are both males 9
2b food category meat meat is shared 13
not meat non-meat resource is shared 20
3 behavioural context control resting or social feeding without food sharing 71
groom non-bond grooming with a non-bond partner 34
groom bond grooming with a bond partner 44
food share non-bond sharing food with a non-bond partner 9
food share bond sharing food with a bond partner 24
In a control run of model 2a the continuous variable C omposite Relationship Index (CRI) replaced categorical variable ‘bond type’ in model 2a (see Ma terial and methods). Proc. R. Soc. B 281: 20133096
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all donors were dominant over the receivers (table 2). Among
non-kin food-sharing partners, three quarters of all donors
were dominant. In 25% of the cases, we sampled food sharing
between unrelated males. Less than 10% of the events
sampled involved sharing between non-kin males and
females in a possible meat-for-sex exchange context (table 2).
(b) Link between food sharing and urinary oxytocin
In model 1, we investigated whether urinary oxytocin levels
were higher after food sharing compared with social feeding
events without food sharing. The full model explained the vari-
ation better than the null model (likelihood ratio test:
¼ 20.24,
d.f. ¼ 4, p , 0.002). Urinary oxytocin concentrations after social
feeding events were significantly higher with food sharing than
without (F
¼ 9.623, p ¼ 0.003, table 3 and figure 1; mean
+ s.e. ¼ 1.407 + 0.102 pg mg
crea versus mean
+ s.e. ¼ 0.884 + 0.066 pg mg
crea). P oten-
tially confounding variables, such as the sex or age of the
subjects, or the monopolizability of the food, did not explain a
significant amount of the variance in the urinary oxytocin
levels (table 3).
Model 2 included only the urine samples that followed food-
sharing events to determine what factors were linked to variation
in urinary oxytocin levels during sharing even ts. Neither models
2a or 2b explained the variation better than the null model (lik e-
lihood ra tio test model 2a:
¼ 0.08, d.f. ¼ 3, n.s.; model 2b:
6.24, d.f. ¼ 5, n.s.). The results of model 2a were similar when
exchanging the binary variable of bond quality with the continu-
ous variable of the CRI (likelihood ratio test model:
¼ 0.36,
d.f. ¼ 3, n.s.). Follo wing sharing events, we found no significant
differences in urinary oxytocin levels for any of the predictor vari-
ables (table 4a,b): kin or non-kin sharers (kin: mean log
OT +
s.e. ¼ 1.42 + 0.14 pg mg
OT +
s.e. ¼ 1.39 + 0.15 pg mg
crea), bond or non-bond partners
(bond: mean log
OT + s.e. ¼ 1.42 + 0.11 pg mg
crea; non-
bond: mean log
OT + s.e. ¼ 1.36 + 0.23 pg mg
crea), subject
receiv ed food or not (receive: mean log
OT + s.e. ¼ 1.40 +
0.16 pg mg
crea; not receive: mean log
OT + s.e. ¼ 1.41 +
0.14 pg mg
crea), meat was shared compared with other
foods (meat: mean log
OT + s.e. ¼ 1.55 + 0.18 pg mg
cre a;
other foods: mean log
OT + s.e. ¼ 1.32 + 0.12 pg mg
crea ),
and food was shared between females, males or between both
sexes (FF: mean log
OT + s.e. ¼ 1.36 + 0.11 pg mg
cre a;
M–F: mean log
OT + s.e. ¼ 1.57 + 0.17 pg mg
cr ea; MM:
mean log
OT + s.e. ¼ 1.21 + 0.17 pg mg
crea). Finally , the
interaction of meat and sex combination in sharing dyads was
not significant (table 4b).
(c) Comparison of urinary oxytocin levels following
either food-sharing or grooming events
Model 3a explained the variation better than the null model
(likelihood ratio test model:
¼ 19.11, d.f. ¼ 2, p , 0,001).
Urinary oxytocin levels following food-sharing events (mean
OT + s.e. ¼ 1.41 + 0.10 pg mg
crea) were significantly
higher than following grooming events (mean log
OT +
s.e. ¼ 0.99+ 0.05 pg mg
crea; table 5a and figure 2a). This
result was confirmed when analysing a subset of the data for
a within-subject comparison of urinary oxytocin levels after
sharing food (mean log
OT + s.e. ¼ 1.79+ 0.32 pg mg
crea) and grooming (mean log
OT + s.e. ¼ 1.11+
0.22 pg mg
crea) using only cases when subjects had inter-
acted with the same partner (Wilcoxon exact: n ¼ 9, T
¼ 40,
p ¼ 0.035). We also found that females had marginally signifi-
cantly higher urinary oxytocin levels following food sharing
than males (table 5a).
When examining urinary oxytocin levels in associa-
tion with the type of cooperative behaviour and quality
of the relationship (model 3b), urine collected after food shar-
ing between bond partners showed the highest oxytocin
concentrations (mean log
OT + s.e. ¼ 1.42 + 0.11 pg mg
crea; F
¼ 9.821, p , 0.001). This was not significantly
higher than urinary oxytocin levels collected after food shar-
ing with non-bond partners (mean log
OT + s.e. ¼ 1.36 +
0.23 pg mg
crea) but was significantly higher than urinary
oxytocin levels collected after grooming with bond partners
(mean log
OT + s.e. ¼ 1.13 + 0.07 pg mg
crea). By con-
trast, urine collected after grooming with non-bond
partners (mean log
OT + s.e. ¼ 0.80 + 0.07 pg mg
and after control events (mean log
OT + s.e. ¼ 0.90 +
0.05 pg mg
crea) both showed the lowest urinary oxytocin
levels (table 5b and figure 2b).
4. Discussion
Our results provide empirical evidence that food-sharing
events in chimpanzees are associated with significantly
higher urinary oxytocin levels than non-sharing social feed-
ing events. These effects were independent of the age of the
subject and the monopolizability of the food. In one model,
however, the sex of the subject showed a marginally signifi-
cant effect such that female urinary oxytocin levels, in
contrast to those of males, were higher following food shar-
ing. High urinary oxytocin levels following food sharing
were independent of whether subjects gave or received
food, shared with kin or non-kin, shared with an established
bond partner or not, or shared meat or other food types.
Thus, our results suggest a direct link between food-sharing
events and urinary oxytocin levels.
When comparing current results with results from our
previous study on oxytocin and grooming [15], we found
that urinary oxytocin levels associated with food-sharing
events were significantly higher than those associated with
Table 2. Food-sharing events described with respect to relative dominance
and sex combination of sharing dyads.
dominant donor 10 11 21
mutual food sharing 3 2 5
subordinate donor 5 2 7
F ! F 18 9
F ! C 34 7
C ! F 70 7
C ! C 73 10 Proc. R. Soc. B 281: 20133096
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grooming [15]. The high oxytocin concentrations could indi-
cate that the relatively rare behaviour of food sharing had a
stronger bonding effect compared with the more frequent
grooming behaviour, although this remains to be tested. Fur-
thermore, in contrast to grooming contexts, an existing social
bond with the food-sharing partner was not associated with
higher oxytocin levels, although it should be noted that there
were relatively few food-sharing samples between non-bond
partners. Sobolewski et al. [69] have shown that food sharing
is linked to low urinary testosterone levels in wild male chim-
panzees. As in some species, low testosterone is linked to
nurturance (i.e. behaviours that involve gentle warm contact
with others) [70] and high oxytocin is linked to social bond-
ing [70], and together these results suggest that food
sharing might provide the optimal conditions for social bond-
ing (see [70]). We therefore hypothesize that food sharing
may be a key behaviour for social bonding in chimpanzees.
Our results are inconsistent with the hypothesis that food
sharing between non-kin is caused by manipulation, particu-
larly through harassment via persistent begging [47,55],
whereby only recipients gain benefits [6,71]. Given that in this
study we found a positive association between urinary oxytocin
levels and food sharing, it seems likely that food sharing is an act
linked with social bonding. We do not exclude the possibility
that harassment avoidance may be a motivation for some
forms of food sharing, nor that bonding can only occur in the
absence of harassment. Indeed, the possibility that food sharing
may serve several functions in chimpanzees seems supported
by several studies [61,72]. Also, it should be noted that in con-
trast to the Gombe field site (Tanzania) where the harassment
avoidance hypothesis was examined [55], in Budongo we only
observed low and not high harassment levels. One important
finding in our study was that both receivers and donors of
food had higher urinary oxytocin levels after food-sharing
Table 3. Variables influencing urinary oxytocin concentrations across both food-sharing and non-food-sharing samples (model 1). Predictor variables and
parameters entered in the models: sex of subject (male, female), age of subject (adult, subadult), monopolizability of food (high, low), food share (yes, no).
n ¼ 79 samples collected either after sharing events (n ¼ 33 urine samples) or after non-sharing events (n ¼ 46 urine samples) from 26 subjects (n ¼ 13
males, n ¼ 13 females). Likelihood ratio test:
¼ 20.24, d.f. ¼ 4, p , 0.001. Response variable: log
oxytocin (pg mg
crea). Random factor: subject ID.
Bold: p , 0.05.
predictor d.f. Fpparameter
sex of subject 1 0.127 0.725 male 20.043 20.357 0.725
age of subject 1 ,0.000 0.989 adult 20.002 20.014 0.989
monopolizability of food 1 1.522 0.221 high 0.171 1.234 0.221
food share 1 9.623 0.003 share 0.427 3.102 0.003
food sharingn =46 n =33
mean residuals ± s.e.
Figure 1. Effect of food sharing versus social feeding without sharing on the
urinary oxytocin concentrations in wild chimpanzees. Residuals are shown +
standard error following model 1 (total of n ¼ 79 samples; 26 subjects;
**p , 0.01).
grooming food sharing
mean residuals ± s.e.
grooming with
control non-bond bond non-bond bond
food share with
mean residuals ± s.e.
n =71 n =34 n =44 n =9 n =24
Figure 2. Effect of (a) food sharing compared with grooming and (b)fivebe-
havioural and social contexts on the urinary oxytocin concentration in wild
chimpanzees. Residuals are shown + standard error following model 3.
Number of samples included in each context are shown beneath each plot
(total n ¼ 182 samples, 34 subjects; *p , 0.05, **p , 0.01, ***p , 0.001). Proc. R. Soc. B 281: 20133096
on January 15, 2014rspb.royalsocietypublishing.orgDownloaded from
compared with non-sharing events, suggesting that both
perceived the interaction positively [70].
(a) Food-sharinglactation hypothesis
Food sharing is often observed in sexual interactions of insects
and birds, with males offering food to females in return for
matings [43,44], as well as in parentoffspring interactions
(e.g. provisioning) [43,45]. In mammals, lactation has been
described as the primary form of food sharing [73], and is
well known to be connected to peripheral and central oxytocin
release in mammals [34,74]. This positive feedback circuitry is
considered a key mechanism for bond formation between
mother and infant [34,75]. In some mammals, maternal care
Table 4. Variables influencing urinary oxytocin concentrations of food-sharing samples only. (a) Model 2a—predictor variables and parameters entered in the
model: bond type (bond, non-bond), kin relationship (kin, non-kin), sex combination (femalefemale, malefemale, male male). Likelihood ratio test:
0.08, d.f. ¼ 3, n.s.. (b) Model 2b—predictor variables and parameters entered in the model: food category (meat, not meat), sharing direction (subject:
receiving, not receiving) sex combination (femalefemale, male female, male male). Likelihood ratio test:
¼ 6.24, d.f. ¼ 5, n.s.; n ¼ 33 samples, 18
subjects. (a,b) Response variable: log
oxytocin (pg mg
crea); random factors: subject ID, partner ID, dyad ID.
predictor d.f. Fpparameter
(a) model 2a
bond type 1 0.059 0.809 bond 0.074 0.244 0.809
kin relationship 1 0.005 0.944 kin 20.020 20.071 0.944
sharing direction 1 0.004 0.951 receiving 20.013 20.062 0.951
(b) model 2b
food category 1 1.940 0.173 meat 0.443 1.055 0.299
sex combination 2 2.371 0.109 FF 0.480 1.171 0.250
MF 0.522 1.274 0.212
food category sex combination 2 0.218 0.805 FF meat
Table 5. Comparison of variables influencing urinary oxytocin concentrations across different behavioural or social contexts. (a) Model 3a—contrasting grooming
and food sharing only. Predictor variables and parameters entered in the model: behavioural context (grooming, food sharing), sex of subject (female, male).
Random factors: subject ID, partner ID, dyad ID. Likelihood ratio test:
¼ 19.11, d.f. ¼ 2, p , 0.001. (b) Model 3b—contrasting behavioural context and
dyads’ bond quality. Predictor variables and parameters entered in the model: behavioural context (control (resting or feeding), grooming with non-bond
partner, grooming with bond partner, food sharing with non-bond partner, food sharing with bond partner), sex of subject (female, male). Random factor:
subject ID. Likelihood ratio test:
¼ 36.47, d.f. ¼ 5, p , 0.001. n ¼ 182 samples, 34 subjects. (a,b) Parameter estimates: the context with 0 was compared
with remaining contexts; parameter estimates of variables in italics were taken from a re-run of the same model with a different order of parameter entry.
Bold: p , 0.05. Response variable: log
oxytocin (pg mg
predictor d.f. Fp parameter
(a) model 3a
behavioural context 1 16.496 <0.001 grooming 2 0.42 2 4.062 <0.001
food sharing 00 0
sex of subject 1 4.193 0.044 female 0.20 2.048 0.044
(b) model 3b
behavioural context 4 9.821 <0.001 control 20.51 24.667 < 0.001
groom non-bond 20.64 25.183 < 0.001
groom bond 20.28 22.403 0.017
food-share non-bond 20.03 20.145 0.885
food-share bond 0 0 0
control 20.48 22.959 0.004
groom non-bond 20.61 23.538 0.001
groom bond 20.25 21.522 0.130
food-share non-bond 0 0 0
sex of subject 1 0.245 0.624 female 0.04 0.494 0.624 Proc. R. Soc. B 281: 20133096
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and provisioning of food, however, aids infant survival beyond
the age of lactation [75]. It is thought that the interface between
oxytocin and the dopaminergic reward system may contribute
to the success of motherinfant and pair-bonding processes
[18,7577]. We therefore posit that food-sharing events
between unrelated adults link into ancient mammalian
neural ‘hardware’ that evolved in the context of lactation-
related oxytocin release. Initially, this mechanism may have
evolved to maintain bonds between mother and offspring
beyond the age of weaning. It may then have evolved further,
promoting bond formation and maintenance in non-kin
cooperative relationships.
(b) Oxytocin circuitry co-opted for non-kin
cooperation hypothesis
What makes food sharing in chimpanzees unusual in the
animal kingdom is that, as well as occurring between kin [52]
and in sexual contexts [50], food sharing also occurs between
non-kin adults in non-sexual contexts [13,15,52,53]. Its occur-
rence is non-random, given that food sharing is more likely
within dyads that engage in high rates of other cooperative
behaviours [7,15,52,78]. Our results, however, suggest that urin-
ary oxytocin levels are not based on prior bonding status of the
sharing dyad, although given that we had relatively few
samples following food sharing with non-bond partners, this
is a tentative result. In addition, urinary oxytocin levels were
high for both donors and receivers of food, suggesting that
food sharing may have a bonding effect between sharers.
This, in conjunction with recent evidence showing similar
levels of urinary oxytocin in both groomers and groomees
[15], leads us to posit the second hypothesis that the oxytocin-
related mechanism associated with food-sharing and grooming
events, although initially evolved to enable kin and sexual
bonds, has, at least in some species, been co-opted to promote
non-kin social bonds in non-sexual contexts. Therefore, such a
hormonal mechanism would enable long-term cooperative
relationships between non-kin to evolve.
As urinary oxytocin had similar levels in both donors
and receivers, both may experience an immediate reward
from sharing, as oxytocin is known to act on areas in the
brain associated with reward and reinforcement [18]. Also, as
oxytocin is thought to act on positive feedback circuits
[16,17,21], sharers may experience a mutual increase in positive
attitude [15,79,80], resulting in the promotion of stronger social
bonds and longer-term benefits of more frequent cooperation
[23,26,80]. Such links between food sharing and long-term
benefits have been described on a behavioural level for chim-
panzees reciprocally sharing meat [7,78], and exchanging
meat for sex [50] or agonistic support [54]. Food sharing may,
in effect, act as a trigger and predictor of cooperative relation-
ships. This link between food sharing and oxytocin found in
chimpanzees may also be relevant for humans [70], where
pro-social behaviour has often been linked to food sharing
and provisioning [46,81,82]. In the end, the word ‘companion’
(Lat.: com [¼with], panis [¼bread]) may be more literal than
previously thought.
We thank Fred Babweteera and our field assistants
Monday Gideon, Jackson Okuti, Sam Adue and Jacob Alio, Anja
Weltring for organizing sample shipments, L. Vigilant, V. Reynolds
and Z. Zommers for providing additional faecal samples, and
Carolyn Rowney for genetic laboratory analyses. The Uganda Wildlife
Authority, the Uganda National Council for Science and Technology,
and the President’s office gave permission to conduct this study.
Funding statement. Financial support was provided by the British Acad-
emy, the Wenner-Gren Foundation for Anthropological Research, the
Leverhulme Trust (Research Leadership Award), the Max Planck
Institute for Evolutionary Anthropology and the Wisconsin National
Primate Research Center (NIH NCRR000167 support of laboratory).
The data of this study are available on request. We acknowledge
the Royal Zoological Society of Scotland for providing core funding
to the Budongo Conservation Field Station.
1. Bowles S. 2006 Group competition, reproductive
levelling, and the evolution of human altruism.
Science 314, 1569 1572. (doi:10.1126/science.
2. Boyd R. 2006 The puzzle of human sociality. Science
315, 15551556. (doi:10.1126/science.1136841)
3. Nowak MA. 2006 Five rules for the evolution of
cooperation. Science 314, 1560 1563. (doi:10.
4. Boyd R, Richerson PJ. 2009 Culture and the
evolution of human cooperation. Phil. Trans. R. Soc.
B 364, 3281 3288. (doi:10.1098/rstb.2009.0134)
5. Hill KR et al. 2011 Co-residence patterns in hunter
gatherer societies show unique human social
structure. Science 331, 1286 1289. (doi:10.1126/
6. Clutton-Brock TH. 2009 Cooperation between non-
kin in animal societies. Nature 462, 5157. (doi:10.
7. Mitani JC. 2009 Male chimpanzees form enduring
and equitable social bonds. Anim. Behav. 77,
633640. (doi:10.1016/j.anbehav.2008.11.021)
8. Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh
AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney
DL. 2009 The benefits of social capital: close social
bonds among female baboons enhance offspring
survival. Proc. R. Soc. B 276, 30993104.
9. Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh
AL, Moscovice LR, Wittig RM, Seyfarth RM, Cheney
DL. 2010 Female chacma baboons form strong,
equitable, and enduring social bonds. Behav.
Ecol. Sociobiol. 64, 17331747. (doi:10.1007/
10. Cameron EZ, Setsaas TH, Linklater WL. 2009 Social
bonds between unrelated females increase
reproductive success in feral horses. Proc. Natl Acad.
Sci. USA 106, 13 85013 853. (doi:10.1073/pnas.
11. Silk JB, Alberts SC, Altmann J. 2003 Social bonds of
female baboons enhance infant survival. Science
302, 12311234. (doi:10.1126/science.1088580)
12. Schu¨lke O, Bhagavatula J, Vigilant L, Ostner J. 2010
Social bonds enhance reproductive success in male
macaques. Curr. Biol. 20, 2207 2210. (doi:10.1016/
13. Langergraber KE, Mitani JC, Vigilant L. 2007 The
limited impact of kinship on cooperation in wild
chimpanzees. Proc. Natl Acad. Sci. USA 104,
77867790. (doi:10.1073/pnas.0611449104)
14. Beery AK, Zucker I. 2010 Oxytocin and same-sex
social behavior in female meadow voles.
Neuroscience 169, 665673. (doi:10.1016/j.
15. Crockford C, Wittig RM, Langergraber KE, Ziegler TE,
Zuberbu¨hler K, Deschner T. 2013 Oxytocin and
social bonding in unrelated chimpanzees.
Proc. R. Soc. B 280, 20122765. (doi:10.
16. Soares MC, Bshary R, Fusani L, Goymann W , Hau M,
K, Oliveira RF . 2010 Hormonal
mechanisms of cooperativ e behaviour. Phil. Tr ans. R. Soc.
B 365, 27372750. (doi:10.1098/rstb.2010.0151)
17. Curley JB, Keverne EB. 2005 Genes, brains and
mammalian social bonds. Trends Ecol. Evol. 20,
561567. (doi:10.1016/j.tree.2005.05.018) Proc. R. Soc. B 281: 20133096
on January 15, 2014rspb.royalsocietypublishing.orgDownloaded from
18. Insel TR. 2010 The challenge of translation in social
neuroscience: a review of oxytocin, vasopressin, and
affiliative behavior. Neuron 25, 768779. (doi:10.
19. Ring RH et al. 2006 Anxiolytic-like activity of
oxytocin in male mice: behavioral and autonomic
evidence, therapeutic implications.
Psychopharmacology 185, 218225. (doi:10.1007/
20. Churchland PS, Winkielman P. 2012 Modulating
social behaviour with oxytocin: how does it work?
What does it mean? Horm. Behav. 61, 392 399.
21. Lim MM, Young LJ. 2006 Neuropeptidergic
regulation of affiliative behavior and social bonding
in animals. Horm. Behav. 50, 506 517. (doi:10.
22. Madden JR, Clutton-Brock TH. 2011 Experimental
peripheral administration of oxytocin elevates a suit
of cooperative behaviours in a wild social mammal.
Proc. R. Soc. B 278, 11891194. (doi:10.1098/rspb.
23. de Dreu CKW, Greer LL, Handgraaf MJ, Shalvi S, Van
Kleef GA, Baas M, Ten Velden FS, Van Dijk E, Feith
SW. 2010 The neuropeptide oxytocin regulates
parochial altruism in intergroup conflict among
humans. Science 328, 1408 1411. (doi:10.
24. Kosfeld M, Heinrichs M, Zak PJ, Fischbacher U, Fehr
E. 2005 Oxytocin increases trust in humans. Nature
435, 673676. (doi:10.1038/nature03701)
25. Baumgartner T, Heinrichs M, Vonlanthen A,
Fischbacher U, Fehr E. 2008 Oxytocin shapes the
neural circuitry of trust and trust adaptation in
humans. Neuron 58, 639 650. (doi:10.1016/j.
26. de Dreu CKW. 2012 Oxytocin modulates the link
between adult attachment through reduced betrayal
aversion. Psychoneuroendocrinology 37, 871880.
27. Zak PJ, Syanton AA, Ahmadi S. 2007 Oxytocin
increases generosity in humans. PLoS ONE 2, e1128.
28. Grewen KM, Girdler SS, Amico J, Light KC. 2005
Effects of partner support on resting oxytocin,
cortisol, norepinephrine, and blood pressure before
and after warm partner contact. Psychosom. Med.
67, 531538. (doi:10.1097/01.psy.0000170341.
29. Light KC, Grewen KM, Amico JA. 2005 More
frequent partner hugs and higher oxytocin levels
are linked to lower blood pressure and heart rate in
premenopausal women. Biol. Psychol. 69, 5 21.
30. Guastella AJ, Mitchell PB, Mathews F. 2008 Oxytocin
enahnces the encoding of positive social memories
in humans. Biol. Psychaitry 64, 256 258. (doi:10.
31. Bartz JA, Zaki J, Ochsner KN, Bolger N, Kolevzon A,
Ludwig N, Lydon JE. 2010 Effects of oxytocin on
recollections of maternal care and closeness. Proc.
Natl Acad. Sci. USA 107, 21 37121 375. (doi:10.
32. Melis AP, Semmann D. 2010 How is human
cooperation different? Phil. Trans. R. Soc. B 365
2674. (doi:10.1098/rstb.2010.0157)
33. Cheney DL. 2011 Extent and limits of cooperation in
animals. Proc. Natl Acad. Sci. USA 108, 10 902
10 909. (doi:10.1073/pnas.1100291108)
34. Ross HE, Young LJ. 2009 Oxytocin and the neural
mechanisms regulating social cognition and
affiliative behavior. Front. Neuroendocrinol. 30,
534547. (doi:10.1016/j.yfrne.2009.05.004)
35. Arletti R, Benelli A, Bertolini A. 1992 Oxytocin
involvement in male and female sexual behaviour.
Annu. NY Acad. Sci. 652, 180 193. (doi:10.1111/j.
36. Caldwell JD, Walk er CH, O’Rourk e ST , Faggin BM, Morris
M, Mason GA. 1996 Analogies between oxytocin
sy s tems of the uterus and brain. Horm.Metabol.Res.28,
6574. (doi:10.10 55/s-20 07-97 9131)
37. Jin D et al. 2007 CD38 is critical for social behaviour
by regulating oxytocin secretion. Nature 446,
4145. (doi:10.1038/nature05526)
38. Ross HE, Cole CD, Smith Y, Neumann ID, Landgraf R,
Murphy AZ, Young LJ. 2009 Characterization of the
oxytocin system regulating affiliative behaviour in
female prairie voles. Neuroscience 162, 892903.
39. Feldman R. 2012 Oxytocin and social affiliation in
humans. Horm. Behav. 61, 380391. (doi:10.1016/
40. Seltzer LJ, Ziegler TE. 2007 Non-invasive
measurement of small peptides in the common
marmoset (Callithrix jacchus): a radiolabeled
clearance study and endogenous excretion under
varying social conditions. Horm. Behav. 51, 436
442. (doi:10.1016/j.yhbeh.2006.12.012)
41. Maestripieri D, Hoffman CL, Anderson GM, Carter S,
Higley JD. 2009 Mother infant interactions in free-
ranging rhesus macaques: relationships between
physiological and behavioral variables. Physiol.
Behav. 96, 613619. (doi:10.1016/j.physbeh.
42. Snowdon CT, Pieper BA, Boe CY, Cronin KA, Kurian
AV, Ziegler TE. 2010 Variation in oxytocin is related
to variation in affiliative behavior in monogamous,
pairbonded tamarins. Horm. Behav. 58, 614 618.
43. Lack D. 1940 Courtship feeding in birds. Auk 57,
169178. (doi:10.2307/4078744)
44. Vahed K. 1998 The function of nuptial feeding in
insects: a review of empirical studies. Biol. Rev. 73,
4378. (doi:10.1017/S0006323197005112)
45. Brown GR, Almond REA, van Bergen Y. 2004
Begging, stealing, offering: food transfer in non-
human primates. Adv. Study Behav. 34, 265295.
46. Gurven M. 2004 To give and not to give: the
behavioural ecology of human food transfers.
Behav. Brain Sci. 27, 543583. (doi:10.1017/
47. Stevens JR, Gilby IC. 2004 A conceptual framework
for non-kin food sharing: timing and currency
benefits. Anim. Behav.
603614. (doi:10.
48. Jaeggi AV, Stevens JMG, van Schaik CP. 2010
Tolerant food sharing and reciprocity is precluded by
despotism among bonobos but not chimpanzees.
Am. J. Phys. Anthropol. 143, 4151. (doi:10.1002/
49. Carter GG, Wilkinson GS. 2013 Food sharing in
vampire bats: reciprical help predicts donations
more than relatedness or harrassment. Proc. R. Soc.
B 280, 20122573. (doi:10.1098/rspb.2012.2573)
50. Gomes CM, Boesch C. 2009 Wild chimpanzees
exchange meat for sex on a long-term basis.
PLoS ONE 4, e5116. (doi:10.1371/journal.pone.
51. Marlow FW. 2003 A critical provisioning by Hadza
men: implications for pair bonding. Evol. Hum.
Behav. 24, 217 229. (doi:10.1016/S1090-
52. Boesch C, Boesch-Achermann H. 2000 The
chimpanzees of the T
forest. Oxford, UK: Oxford
University Press.
53. Wittig RM, Boesch C. 2003 Food competition and
linear dominance hierarchy among female
chimpanzees of the T¨ National Park.
Int. J. Primatol. 24, 847 867. (doi:10.1023/
54. Mitani JC, Watts DP. 2001 Why do chimpanzees
hunt and share meat? Anim. Behav. 61, 915924.
55. Gilby IC. 2006 Meat sharing among the Gombe
chimpanzees: harassment and reciprocal exchange.
Anim. Behav. 71, 953963. (doi:10.1016/j.anbehav.
56. Boesch C. 1994 Cooperative hunting in wild
chimpanzees. Anim. Behav. 48, 653667.
57. Hockings KJ, Humle T, Anderson JR, Biro D, Sousa C,
Ohashi G, Matsuzawa T. 2007 Chimpanzees share
forbidden fruit. PLoS ONE 2, e886. (doi:10.1371/
58. Reynolds V, Lloyd W, Babweteera F, English CJ. 2009
Decaying Raphia farinifera palm trees provide a
source of sodium for wild chimpanzees in Budongo
forest, Uganda. PLoS ONE 4, e6194. (doi:10.1371/
59. Reynolds V. 2005 The chimpanzees of the Budongo
forest. Oxford, UK: Oxford University Press.
60. Altman J. 1974 Observational study of behavior:
sampling methods. Behavior 49, 227 267. (doi:10.
61. Silk JB, Brosnan SF, Henrich J, Lambeth SP,
Shapiro S. 2013 Chimpanzees share food for
many reasons: the role of kinship, reciprocity, social
bonds and harrasment on food transfers. Anim.
Behav. 85, 941 947. (doi:10.1016/j.anbehav.
62. Wittig RM, Boesch C. 2003 ‘Decision-making’ in conflicts
of wild chimpanzees (Pa n troglodytes): an ex tension to
the relational model. Behav. Ecol. Sociobiol. 54
1504. (doi:10.1007/s00265-003-0654-8)
63. Fraser O, Shino G, Aureli F. 2008 Components
of relationship quality in chimpanzees. Ethology
114, 834843. (doi:10.1111/j.1439-0310.2008.
01527.x) Proc. R. Soc. B 281: 20133096
on January 15, 2014rspb.royalsocietypublishing.orgDownloaded from
64. Crockford C, Wittig RM, Mundry R, Zuberbu¨hler K.
2012 Wild chimpanzees inform ignorant group
members of danger. Curr. Biol. 22, 142 146.
65. Amico JA, Ulbrecht JS, Robinson AG. 1987 Clearance
studies of OT in humans using radioimmunoassay
measurements of the hormone in plasma and urine.
J. Clin. Endocrinol. Metab. 64, 340345. (doi:10.
66. Bahr NI, Palme R, Mo
hle U, Hodges JK, Heistermann
M. 2000 Comparative aspects of the metabolism
and extraction of cortisol in three individual
nonhuman primates. Gen. Comp. Endocrinol. 117,
427438. (doi:10.1006/gcen.1999.7431)
67. Langergraber KE, Mitani JC, Vigilant L. 2009 Kinship
and social bonds in female chimpanzees (Pan
troglodytes). Am. J. Primatol. 71, 840851. (doi:10.
68. Tabachnick BG, Fidell LS. 2007 Using
multivariate statistics, 5th edn. Boston, MA: Allyn
and Bacon.
69. Sobolewski M, Brown J, Mitani J. 2012 Territoriality,
tolerance and testosterone in wild chimpanzees.
Anim. Behav. 84, 14691474. (doi:10.1016/j.
70. Van Anders SM, Goldey KL, Kuo PX. 2011
The steroid peptide theory of social bonds:
Integrating testosterone and peptide responses
for classifying social behavioural contexts.
Psychoneuroendocrinology 36, 1265 1275.
71. Clutton-Brock TH, Parker GA. 1995 Punishment in
animal societies. Nature 373, 209216. (doi:10.
72. Gomes C, Boesch C. 2011 Reciprocity and trades in wild
W est African chimpanzees. Behav. Ecol. Sociobiol. 65,
21832196. (doi:10.1007/s00265-011-1227-x)
73. Hruschka DJ. 2010 Friendship: development, ecology
and evolution of a relationship. Berkeley, CA:
University of California Press.
74. Kendrick KM, Keverne EB, Baldwin BA,
Sharman DF . 1986 Cer ebr ospinal-fluid levels of
acet ylcholinesterase, monoamines and oxytocin during
labor, parturition, vaginocervical s timulat ion, lamb
44, 149 156. (doi:10.1159/000124638)
75. Broad KD, Curley JP, Keverne EB. 2006
Mother-infant bonding and the evolution of social
relationships. Phil. Trans. R. Soc. B 361,
21992214. (doi:10.1098/rstb.2006.1940)
76. Young LJ, Wang Z. 2004 The neurobiology of pair
bonding. Nat. Neurosci. 7, 10481054. (doi:10.
77. Skuse DH, Gallagher L. 2009 Dopaminergic
neuropeptide interactions in the social brain.
Trend Cog. Sci. 13, 2735. (doi:10.1016/j.tics.
78. Wittig RM, Boesch C. 2010 Receiving post-conflict
affiliation from the enemy’s friend reconciles former
opponents. PLoS ONE 5, e13995. (doi:10.1371/
79. de Waal FBM. 2000 Attitudinal reciprocity in food
among brown capuchin monkeys. Anim.
Behav. 60, 253261. (doi:10.1006/anbe.2000.1471)
80. Schino G, Aureli F. 2009 Reciprocal altruism in
primates: partner choice, cognition, and emotions.
Adv. Stud. Behav. 39, 45 69. (doi:10.1016/S0065-
81. Lovejoy CO. 1981 The origin of man. Science 211,
341350. (doi:10.1126/science.211.4480.341)
82. Gurven M, Hill K. 2009 Hunting as subsistence and
mating effort? A re-evaluation of ‘Man the hunter’,
the sexual division of labor and the evolution of the
nuclear family. Curr. Anthropol. 5, 51 74. (doi:10.
1086/595620) Proc. R. Soc. B 281: 20133096
on January 15, 2014rspb.royalsocietypublishing.orgDownloaded from

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... In-group cooperation amongst non-kin, however, is more difficult to explain, especially when benefits are not immediately gained or are gained independently of contribution into the cooperative act. In chimpanzees, similar to humans, unrelated adults frequently cooperate [24], both at the dyadic [25,26] and the group level [27,28]. Grouplevel cooperation in chimpanzees is observed for example in collective hunting events [29][30][31] and territorial defence [24,32,33]. ...
... For example, within-group cohesion (larger association parties and lower tendency of the group to fission) is expected to increase with a reduction in the number of adult group members [99], and stronger within-group cohesion reduces imbalance of power opportunities and hence conflict escalation [39,82]. In turn, social cohesion and bonding promote cooperation [26], including group-level cooperative territorial behaviour (coalitionary attacks and participation in border patrols) [32]. Thus, between-population differences in intergroup lethality could be linked to differences in social dynamics that may impact group-level cooperation. ...
... The oxytocinergic system is an ancient physiological system highly conserved in mammals, and involved in maternal effects and mother-offspring bonding [139]. Probably co-opted from maternal-offspring bonding and attachment the oxytocinergic system is also known to play a vital role in the formation of pair-bonds and unrelated social bond partners across taxa [25,26,140,141]. The oxytocinergic system is activated during affiliative acts in barbary macaques [142], in food sharing with in-group members in vampire bats [143], and during affiliation, postconflict management and food sharing in chimpanzees [25,26,133,144] potentially playing an essential role in social Phil. ...
Parochial altruism, taking individual costs to benefit the in-group and harm the out-group, has been proposed as one of the mechanisms underlying the human ability of large-scale cooperation. How parochial altruism has evolved remains unclear. In this review paper, we formulate a parochial cooperation model in small-scale groups and examine the model in wild chimpanzees. As suggested for human parochial altruism, we review evidence that the oxytocinergic system and in-group cooperation and cohesion during out-group threat are integral parts of chimpanzee collective action during intergroup competition. We expand this model by suggesting that chimpanzee parochial cooperation is supported by the social structure of chimpanzee groups which enables repeated interaction history and established social ties between co-operators. We discuss in detail the role of the oxytocinergic system in supporting parochial cooperation, a pathway that appears integral already in chimpanzees. The reviewed evidence suggests that prerequisites of human parochial altruism were probably present in the last common ancestor between Pan and Homo . This article is part of the theme issue ‘Intergroup conflict across taxa’.
... Among nonhuman great apes, average TEE = E a because provisioning and food storage are negligible (2,(29)(30)(31). Time spent foraging and distances traveled and climbed per day were compiled from observational studies of wild apes. ...
... To calculate energy budgets of nonhuman great apes, total daily energy expenditure (TEE) was used as a proxy for daily energy acquired from food (kcal/day) under the realistic assumption that energy input and output are approximately equal among nonprovisioned animals in energy balance (2,27). Food sharing and provisioning are very rare among nonhuman apes in the wild, even between mothers and offspring (2,(29)(30)(31), and therefore each individual's average daily food energy acquisition must match their average TEE. A lack of surplus production in other great apes is underscored by the fact that humans exhibit elevated fat deposition compared to chimpanzees and gorillas, and that the fat reserves of orangutans fluctuate in accordance with boom and bust seasonal cycles and supra-annual mast fruiting events (1, 108, 109). ...
Instances of emotion are typically understood as internal mental experiences centering on individuals’ subjective feelings. This conceptualization has been supported by studies of emotion narratives, or the stories people tell about events that they understand as emotions. Yet these studies, and contemporary psychology more generally, often rely on observations of educated Europeans and European-Americans, constraining psychological theory and methods. In this paper, we present observations from an inductive, qualitative analysis of emotion narratives of the Hadza, a community of small-scale hunter-gatherers in Tanzania, and juxtapose them with those drawn from Americans from North Carolina. While North Carolina narratives largely conformed to the assumptions of psychological theory, Hadza narratives foregrounded embodied actions involving social others, focused on the sensory environment and immediate needs, and worked outward from situated events as the motivation for behavior. These observations suggest that subjective feeling and internal mental experience may not be the organizing principle of emotion the world-around. Qualitative analysis of emotion narratives from outside of an American (and western) cultural context has the potential to discover additional diversity in meaning-making, offering a descriptive foundation on which to build a more robust and inclusive science of emotion.
... There were other studies predicting food-sharing behavior beyond food preference, such as the role of hormone levels on food-sharing in non-human primates [31,32]. The hormonal-control possibility of food-sharing may come from the 'oxytocin' explanation [33], where subjects showed higher urinary oxytocin levels after single food-sharing. Unfortunately, the relationship between food-sharing and oxytocin levels was not reliable too [34]. ...
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The current study was designed to predict why human primates often behave unfairly (equity aversion) by not exhibiting equity preference (the ability to equally distribute outcomes 1:1 among participants). Parallel to humans, besides inequity aversion, lab monkeys such as kin of long-tailed macaques (Macaca fascicularis) also demonstrate equity aversion depending on their preference for the outcome (food) type. During the pre-experiment phase, a food-preference test was conducted to determine the most preferred income per individual monkey. Red grapes were the most preferred outcome (100%) when compared to vanilla wafers (0%). The first set of experiments used a 1:1 ratio (equity condition) of grape distribution among six kin-pairs of female long-tailed macaques, and we compared their aversion (Av) versus acceptance (Ac). In the second experiment, we assessed the response to the 0:2 and 1:3 ratio distribution of grapes (inequity condition). A total of 60 trials were conducted for each condition with N = 6 pairs. Our results show aversion to the inequity conditions (1:3 ratios) in long-tailed macaques was not significantly different from aversion to the equity conditions (1:1 ratios). We suggest that the aversion observed in this species was associated with the degree of preference for the outcome (food type) offered rather than the distribution ratio. The subjective preferences for outcome types could bring this species into irrationality; they failed to share foods with an equal ratio of 1:1.
... This suggests that even chimpanzees have an inclination to help others in need without expecting returns. As Mencius suggested, there is evidence that this behavior is linked to neurochemistry of sympathy (Wittig et al. 2014). In other words, it seems that when we rush to help the child falling into a well, we follow an inclination in our primate nature, not merely a habit drilled into us by social conditioning. ...
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Mencius 孟子 is famous for arguing that human nature is good (xingshan 性善). In this article, I offer a reading of Mencius’ argument which can be evaluated in terms of empirical psychology. In this reading, Mencius’ argument begins with three claims: (1) humans naturally have prosocial inclinations, (2) prosocial inclinations can be cultivated into mature forms of virtue, and (3) the growth of prosocial inclinations is more natural than the growth of their alternatives. I also argue that each of these claims is well supported by empirical psychology. The relevant studies demonstrate, for example, that humans’ prosocial inclinations are not merely products of social conditioning or egoistic concerns; that prosocial inclinations can be cultivated by environmental factors and personal effort; that humans—even preverbal infants—have a natural inclination to prefer prosociality over its alternatives; and that growth in prosociality is positively associated with human health. Finally, I suggest we interpret Mencius’ expression “human nature is good” as a rhetorical tool to capture the totality of such empirically minded claims.
... In particular, affiliation among conspecifics is often associated with higher oxytocin levels. For example, studies that use oxytocin levels from blood plasma, urine or saliva as an informative tool on central oxytocin release, have recorded elevated oxytocin following affiliative touch [56][57][58] and cooperative exchange [59][60][61] in mammalian species such as (human) primates and dogs. Also, strongly bonded marmoset monkeys showed synchronized fluctuations of oxytocin over a six-week period [62] (also see [63]). ...
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Across vertebrate species, intergroup conflict confronts individuals with a tension between group interests best served by participation in conflict and personal interest best served by not participating. Here, we identify the neurohormone oxytocin as pivotal to the neurobiological regulation of this tension in distinctly different group-living vertebrates, including fishes, birds, rodents, non-human primates and humans. In the context of intergroup conflict, a review of emerging work on pro-sociality suggests that oxytocin and its fish and birds homologues, isotocin and mesotocin, respectively, can elicit participation in group conflict and aggression. This is because it amplifies (i) concern for the interests of genetically related or culturally similar ‘in-group’ others and (ii) willingness to defend against outside intruders and enemy conspecifics. Across a range of social vertebrates, oxytocin can induce aggressive behaviour to ‘tend-and-defend’ the in-group during intergroup contests. This article is part of the theme issue ‘Intergroup conflict across taxa’.
... Chimpanzees sometimes share meat from carcasses that they control 181,182 and food sharing is associated with elevation of oxytocin which may enhance bonding. 183 Plant foods are rarely shared among adult chimpanzees in the wild, but female chimpanzees regularly share plant foods with their offspring. [185][186][187] If the MRCA formed relatively stable polygynous breeding bonds, as the Ngogo chimpanzees do, sharing and exchange relationships might have been formed with bond partners, and represent a form of joint parental care. ...
Natural selection will favor male care when males have limited alternative mating opportunities, can invest in their own offspring, and when care enhances males' fitness. These conditions are easiest to fulfill in pair‐bonded species, but neither male care nor stable “breeding bonds” that facilitate it are limited to pair‐bonded species. We review evidence of paternal care and extended breeding bonds in owl monkeys, baboons, Assamese macaques, mountain gorillas, and chimpanzees. The data, which span social/mating systems and ecologies, suggest that there are multiple pathways by which conditions conducive to male care can arise. This diversity highlights the difficulty of making inferences about the emergence of male care in early hominins based on single traits visible in the fossil record. We discuss what types of data are most needed and the questions yet to be answered about the evolution of male care and extended breeding bonds in the primate order.
Previous research has found that oxytocin (OT) is associated with intergroup behaviour in humans as well as wild chimpanzees, and that exogenous OT affects Pan social attention. The two Pan species, bonobos and chimpanzees, differ drastically from one another in their intensity of intergroup competition, with lethal intergroup aggression often led by males in chimpanzees and more tolerant associations often centered around females in bonobos. However, it remains unclear how exogenous OT changes the two species' responses to ingroup and outgroup individuals. In this study, after intranasal administration of nebulized OT or placebo control, chimpanzees and bonobos viewed image pairs of ingroup and outgroup conspecifics while their eye movements were tracked with an eye-tracker. Although the overall effect of OT was small, we found that OT shifted bonobos' and chimpanzees' attention to outgroup images of the sex primarily involved in intergroup encounters in each species. Specifically, OT selectively shifted attention towards outgroup photos of female conspecifics in bonobos, and those of outgroup male conspecifics in chimpanzees. This suggests that OT generally promotes outgroup attention in both bonobos and chimpanzees but this effect is restricted to the sex most relevant in intergroup relations. These results suggest that, although OT may have a generally conserved role in hominid intergroup behaviour, it may act in species-relevant ways under the influence of their socio-ecological backgrounds.
Behavioral plasticity refers to changes occurring due to external influences on an organism, including adaptation, learning, memory and enduring influences from early life experience. There are 2 types of behavioral plasticity: “developmental”, which refers to gene/environment interactions affecting a phenotype, and “activational” which refers to innate physiology and can involve structural physiological changes of the body. In this review, we focus on feeding behavior, and studies involving neuropeptides that influence behavioral plasticity - primarily opioids, orexin, neuropeptide Y, and oxytocin. In each section of the review, we include examples of behavioral plasticity as it relates to actions of these neuropeptides. It can be concluded from this review that eating behavior is influenced by a number of external factors, including time of day, type of food available, energy balance state, and stressors. The reviewed work underscores that environmental factors play a critical role in feeding behavior and energy balance, but changes in eating behavior also result from a multitude of non-environmental factors, such that there can be no single mechanism or variable that can explain ingestive behavior.
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Oxytocin has become a popular analyte in behavioral endocrinology in recent years, due in part to its roles in social behavior, stress physiology, and cognition. Urine samples have the advantage of being non-invasive and minimally disruptive to collect, allowing for oxytocin measurements even in some wild populations. However, methods for urinary oxytocin immunoassay have not been sufficiently optimized and rigorously assessed for their potential limitations. Using samples from oxytocin knockout (KO) and wildtype (WT) mice, we find evidence of considerable interference in unextracted urine samples, with similar distributions of measured oxytocin in both genotypes. Importantly, although this interference can be reduced by a reversed-phase solid-phase extraction (SPE), this common approach is not sufficient for eliminating false-positive signal on three immunoassay kits. To better understand the source of the observed interference, we conducted epitope mapping of the Arbor Assays antibody and assessed its cross-reactivity with known, biologically active fragments of oxytocin. We found considerable cross-reactivity (0.5-52% by-molarity) for three fragments of oxytocin that share the core epitope, with more cross-reactivity for longer fragments. Given the presence of some cross-reactivity for even the tripeptide MIF-1, it is likely that many small protein metabolites might be sufficiently similar to the epitope that at high concentrations they interfere with immunoassays. We present a new mixed-mode cation-exchange SPE method that minimizes interference—with knockout samples measuring below the assay's limit of detection—while effectively retaining oxytocin from the urine of wildtype mice. This method demonstrates good parallelism and spike recovery across multiple species (mice, dogs, sifakas, humans). Our results suggest that immunoassays of urine samples may be particularly susceptible to interference, even when using common extraction protocols, but that this interference can be successfully managed using a novel mixed-mode cation exchange extraction.
An ongoing debate in animal behaviour research is whether food calls function to cooperatively inform others or provide the caller with competitive advantages. When feeding, chimpanzees, Pan troglodytes, produce two types of call: context-specific, close-range ‘rough grunts’ and context-general, long-range ‘pant hoots’. We investigated this dual signalling behaviour by wild male chimpanzees that were either actively joining others or passively being joined in food trees, considering the effects of the audience composition and the type of food encountered. For arriving individuals, we found that pant hoot production was best explained by the absence of socially important individuals (i.e. social bond partners and/or high-ranking males), suggesting that callers were cooperatively informing them about food availability, probably to strengthen social relationships. In contrast, rough grunts were mostly produced by low-ranking individuals, suggesting they were part of competitive interactions to avoid aggression. For individuals already in a tree, we found that both rough grunt and pant hoot production were most common in low-ranking individuals reacting to the arrival of high-ranking males and there was no significant effect of the presence, or absence, of social bond partners. We discuss these patterns and conclude that, when chimpanzees enter a food tree, their vocal behaviour functions to mediate both cooperative and competitive interactions.
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The role of men in hunter‐gatherer societies has been subject to vigorous debate over the past 15 years. The proposal that men hunt wild game as a form of status signaling or “showing off” to provide reproductive benefits to the hunter challenges the traditional view that men hunt to provision their families. Two broad assumptions underlie the signaling view: (1) hunting is a poor means of obtaining food, and (2) hunted game is a public good shared widely with others and without expectation of future reciprocation. If hunters lack the ability to direct food shares and obtain subsequent benefits contingent on redistribution, then the ubiquitous observations of male hunting and universal pair‐bonding cannot be explained from a perspective that emphasizes kin provisioning and a division of labor. Here we show that there is little empirical support for the view that men hunt for signaling benefits alone. The ethnographic record depicts a more complex relationship between food sharing patterns, subsistence strategies, mating, and the sexual division of labor. We present a framework incorporating trade‐offs between mating and subsistence strategies in an economic bargaining context that contributes to understanding men’s and women’s roles in hunter‐gatherer societies.
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Many animal species, from arthropods to apes, share food. This paper presents a new framework that categorizes nonkin food sharing according to two axes: (1) the interval between sharing and receiving the benefits of sharing, and (2) the currency units in which benefits accrue to the sharer (especially food versus nonfood). Sharers can obtain immediate benefits from increased foraging efficiency, predation avoidance, mate provisioning, or manipulative mutualism. Reciprocity, trade, status enhancement and group augmentation can delay benefits. When benefits are delayed or when food is exchanged for nonfood benefits, maintaining sharing can become more difficult because animals face discounting and currency conversion problems. Explanations that involve delayed or nonfood benefits may require specialized adaptations to account for timing and currency-exchange problems. The immediate, selfish fitness benefits that a sharer may gain through by-product or manipulative mutualism, however, apply to various food-sharing situations across many species and may provide a simpler, more general explanation of sharing.
Chimpanzees have never been more threatened with extinction than they are today. This book focuses on one chimpanzee group, the Sonso community, living in a tropical rain forest, the Budongo Forest in western Uganda. The book builds up a detailed picture of the forest environment of these apes, their social and behavioural adaptations, and the range of threats they face at the present time. The facts presented in the book summarize the author's own work and that of the many students and colleagues who have worked with the Budongo Forest Project, which the author founded, over the years from 1990 to the present day. Comparisons are made with other chimpanzee field studies. A picture is built up to show the Sonso community living in a complex environment to which it has adapted well. The diet, culture, social behaviour, and social organization of the chimpanzees are described in detail. Focus then shifts to the various dangers they face in the modern context of increasing pressure from local hunters who put snares in the forest, and from a local agribusiness which threatens to engulf the forest. A careful appraisal of the future for these animals is made, ending with a note of hope for their survival if the national organizations that exist to protect them can become more effective.
Friends-they are generous and cooperative with each other in ways that appear to defy standard evolutionary expectations, frequently sacrificing for one another without concern for past behaviors or future consequences. In this fascinating multidisciplinary study, Daniel J. Hruschka synthesizes an array of cross-cultural, experimental, and ethnographic data to understand the broad meaning of friendship, how it develops, how it interfaces with kinship and romantic relationships, and how it differs from place to place. Hruschka argues that friendship is a special form of reciprocal altruism based not on tit-for-tat accounting or forward-looking rationality, but rather on mutual goodwill that is built up along the way in human relationships.
Political scientists have documented the many ways in which trust influences attitudes and behaviors that are important for the legitimacy and stability of democratic political systems. They have also explored the social, economic, and political factors that tend to increase levels of trust in others, in political figures, and in government. Neuroeconomic studies have shown that the neuroactive hormone oxytocin, a peptide that plays a key role in social attachment and affiliation in non-human mammals, is associated with trust and reciprocity in humans (e.g., Kosfeld et al., Nature 435:673–676, 2005; Zak et al., Horm Beh 48:522–527, 2005). While oxytocin has been linked to indicators of interpersonal trust, we do not know if it extends to trust in government actors and institutions. In order to explore these relationships, we conducted an experiment in which subjects were randomly assigned to receive a placebo or 40 IU of oxytocin administered intranasally. We show that manipulating oxytocin increases individuals’ interpersonal trust. It also has effects on trust in political figures and in government, though only for certain partisan groups and for those low in levels of interpersonal trust.
Although testosterone (T) has well known organizational and activational effects on aggression, the relationship between the two is not always clear. The challenge hypothesis addresses this problem by proposing that T will affect aggression only in fitness-enhancing situations. One way to test the challenge hypothesis is to examine the relationship between T and different types of aggression. Chimpanzees, Pan troglodytes, show aggressive behaviours in several contexts and provide an opportunity for such a test. Here we show that urinary T influences a form of male chimpanzee reproductive aggression, territorial boundary patrols. In contrast, T does not affect predatory behaviour, a form of aggression that has no immediate link to male reproduction. While these results are consistent with the challenge hypothesis, our results indicate that male chimpanzees experience a significant drop in urinary T during hunts. Additional analyses reveal that males who share meat with others display this decrease. The reason for this decrement is unclear, but we hypothesize that the relative lack of aggression that results from voluntary sharing episodes and the tolerance engendered by such acts may be contributory factors.