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Hormones and Behavior
journal homepage: www.elsevier.com/locate/yhbeh
The cooperative sex: Sexual interactions among female bonobos are linked
to increases in oxytocin, proximity and coalitions
Liza R. Moscovice
a,b,1,⁎
, Martin Surbeck
c,d,1
, Barbara Fruth
e,f
, Gottfried Hohmann
d
,
Adrian V. Jaeggi
b,g
, Tobias Deschner
d
a
Institute of Behavioural Physiology, Leibniz Institute for Farm Animal Biology, Wilhelm-Stahl-Allee 2, D-18196 Dummerstorf, Germany
b
Anthropology Department, Emory University, 1557 Dickey Drive, Atlanta, GA 30322, USA
c
Department of Human Evolutionary Biology, Harvard University, Peabody Museum, 5
th
Floor, 11 Divinity Avenue, Cambridge, MA 02138, USA
d
Primatology Department, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany
e
Natural Sciences and Psychology, Liverpool John Moores University, Byrom Street, Liverpool L3 3AF, United Kingdom
f
Centre for Research and Conservation, Royal Zoological Society of Antwerp, Koningin Astridplein 20-26, 2018 Antwerp, Belgium
g
Institute of Evolutionary Medicine, University of Zurich, Winterthurerstrasse 190, 8057 Zurich, Switzerland
ARTICLE INFO
Keywords:
Pan paniscus
Socio-sexual behavior
Copulations
Genito-genital rubbing
Oxytocin
ABSTRACT
In some species habitual same-sex sexual behavior co-occurs with high levels of intra-sexual alliance formation,
suggesting that these behaviors may be linked. We tested for such a link by comparing behavioral and phy-
siological outcomes of sex with unrelated same- and opposite-sex partners in female bonobos (Pan paniscus).
We analyzed behavioral outcomes following 971 sexual events involving n= 19 female and n= 8 male adult
and sub-adult members of a wild, habituated bonobo community. We additionally collected n= 143 urine
samples before and after sexual interactions to non-invasively measure oxytocin (OT), which modulates female
sexual behavior and facilitates cooperation in other species. The majority of sexual events (65%) consisted of
female same-sex genito-genital rubbing (or GG-rubbing). Female dyads engaged in significantly more sexual
interactions than did inter-sexual dyads, and females were more likely to remain within close proximity to their
partners following GG-rubbing. Females also exhibited greater increases in urinary OT following GG-rubbing
compared with copulations, indicating a physiological basis for increased motivation to cooperate among fe-
males. The frequency of coalitionary support among non-kin was positively predicted by the frequency of sexual
interactions for female as well opposite-sex dyads, although coalitionary support tended to be more frequent
among females. The emergence of habitual same-sex sexual behavior may have been an important step in the
evolution of cooperation outside of kinship and pair-bonds in one of our closest phylogenetic relatives.
1. Introduction
Same-sex sexual behavior, referring to sexual solicitations,
mounting or other genital contact between same-sex partners,
occurs across a wide range of animal taxa under free-ranging
conditions, though with much variation in form and frequency
(reviewed in: Bailey and Zuk, 2009). In many species, same-sex
sexual interactions are rare events that may represent redirected
sexual behavior when suitable opposite-sex partners are absent
(Bailey and Zuk, 2009). However, there are other taxa where a
subset of the population exhibits same-sex preferences even when
viable opposite-sex partners are available (e.g. Japanese
macaques (Macaca fuscata), Vasey and Duckworth, 2006). In rarer
cases, all adult members of one sex exhibit habitual same-sex
sexual interactions that can occur at similar frequencies as oppo-
site-sex sexual interactions (e.g. male bottlenose dolphins (Tur-
siops sp.): Mann, 2006; female bonobos (Pan paniscus): Hohmann
and Fruth, 2000;Idani, 1991;Ryu et al., 2015). The extent of variation
across species in the contexts that elicit same-sex sexual behavior
and how widespread it is within a population suggest that its
functions may be diverse and species-specific.
The adaptive hypotheses that have been proposed to explain
same-sex sexual behavior more generally (reviewed in Bailey and
Zuk, 2009) include: i) Establishing or maintaining cooperative social
https://doi.org/10.1016/j.yhbeh.2019.104581
Received 27 March 2019; Received in revised form 15 July 2019; Accepted 20 August 2019
⁎
Corresponding author at: Institute of Behavioural Physiology, Leibniz Institute for Farm Animal Biology, Wilhelm-Stahl-Allee 2, D-18196 Dummerstorf, Germany.
E-mail addresses: Moscovice@fbn-dummerstorf.de (L.R. Moscovice), Surbeck@eva.mpg.de (M. Surbeck), B.I.Fruth@ljmu.ac.uk (B. Fruth),
Hohmann@eva.mpg.de (G. Hohmann), Adrian.jaeggi@iem.uzh.ch (A.V. Jaeggi), Deschner@eva.mpg.de (T. Deschner).
1
shared first authorship
Hormones and Behavior 116 (2019) 104581
0018-506X/ © 2019 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license
(http://creativecommons.org/licenses/BY/4.0/).
T
relationships (e.g. Japanese macaques (Macaca fuscata), Vasey,
1996); ii) Reducing social conflict, either by reducing social tension,
or as a form of reconciliation following conflict (e.g. bonobos, de
Waal, 1987, 1990); iii) As a form of intra-sexual competition, either
by attracting members of the opposite sex for mating or by pre-
venting members of the same sex from mating (e.g. tropical fish
(Poecilia mexicana), Bierbach et al., 2012)or iv) As a form of prac-
tice for adult sexual behavior (e.g. fruit flies (Drosophila melano-
gaster), Dukas, 2010). The first two hypotheses both suggest a role
of same-sex sexual behavior in promoting cooperative social out-
comes. In dolphins and bonobos, members of the sex that engage
in habitual same-sex sexual behavior are also noteworthy for their
high levels of intra-sexual cooperation among unrelated in-
dividuals (Connor and Krützen, 2015;Furuichi, 2011;Tokuyama and
Furuichi, 2016). This suggests that habitual same-sex sexual inter-
actions may play a role in facilitating additional cooperation in
these species, although the exact mechanisms by which this may
occur remain unclear. Our goals were to test for evidence that
habitual same-sex sexual behavior facilitates cooperative social
outcomes, and to identify mechanisms by which this may occur, in
female bonobos.
One way to infer potential functions of sexual behavior is by char-
acterizing the social contexts and social configurations in which the
behavior mainly occurs. In several species, same-sex sexual behavior
occurs in contexts that are associated with additional behavioral co-
ordination and cooperation between participants. In female Japanese
macaques, same-sex sexual behavior occurs exclusively within short-
term consortships in which dyads also engage in high levels of co-
ordinated travel, feeding and grooming (Vasey, 2002). In dolphins, si-
multaneous same-sex sexual behavior is frequently observed among
triads of primarily unrelated males and this is also the most frequent
social configuration for cooperative alliances (Mann, 2006). In other
species, same-sex sexual behavior mainly occurs when competition
between participants is high, and it is used to attract opposite sex mates
rather than to strengthen same-sex relationships (e.g. tropical fish
(Poecilia mexicana), Bierbach et al., 2012).
In addition to behavioral data, measures of physiological changes
associated with sexual behavior provide further insights into likely
functions. Of particular interest in the context of cooperation is the
neuropeptide hormone oxytocin (OT), which mediates many aspects of
female sexual, reproductive and social behavior (reviewed in Borrow
and Cameron, 2012). OT is released centrally from hypothalamic nuclei
in response to salient social stimuli, including sexual behavior (rats:
Nyuyki et al., 2011; voles: Ross et al., 2009). Centrally, OT activation in
social brain circuitry results in enhanced social memory, reduced fear
and anxiety and activation of neural reward pathways, all of which are
related to fostering selective social bonds that promote cooperation
(reviewed in Gangestad and Grebe, 2017). OT can also be released
peripherally via the posterior pituitary, facilitating non-invasive mea-
surement (Crockford et al., 2014). In several species, measures of per-
ipheral OT correlate positively with the extent of behavioral co-
ordination and cooperation within selective social relationships, such as
between mothers and offspring (humans: Feldman, 2012), mono-
gamous mates (humans: Grewen et al., 2005;Schneiderman et al.,
2012; cotton-top tamarins (Saguinus oedipus): Snowdon et al., 2010)
and stable alliance partners (chimpanzees (Pan troglodytes):
Crockford et al., 2013). In humans (De Dreu, 2012;Nagasawa et al.,
2009) and chimpanzees (Samuni et al., 2017), there is evidence that the
OT system has been co-opted outside of maternal and reproductive
contexts to facilitate cooperation with a broader range of social partners
(reviewed in Trumble et al., 2015). Based on this combined evidence,
the link between sexual behavior and OT system activation may be
strongest related to sexual behavior that facilitates additional trust and
cooperation, whether this occurs within or outside of monogamous
pair-bonds. We were interested in whether unrelated female bonobos
exhibit increases in peripheral oxytocin associated with sexual
interactions, as this may explain their unusual extent of cooperation.
Bonobos are a particularly promising model for investigating dif-
ferent functions of sexual behavior, given that all adult females engage
in same-sex sexual behavior that occurs at similar or higher rates as
copulations (Hohmann and Fruth, 2000, 2003a;Ryu et al., 2015). In
contrast, same-sex sexual interactions among male bonobos are rela-
tively rare (Fruth and Hohmann, 2006;Kano, 1980;Surbeck et al.,
2017b). Bonobos live in multi-male, multi-female communities char-
acterized by fission-fusion social dynamics, female-biased dispersal and
a promiscuous mating system notable for a relative lack of male coer-
cion and a high degree of female control over sexual partners (Furuichi,
2011;Surbeck and Hohmann, 2013). For female bonobos, their stron-
gest and most cooperative inter-sexual social relationships occur with
their adult sons (Surbeck et al., 2011, 2017a). Females also cooperate
preferentially with other unrelated females within their community in
several contexts, including by sharing monopolizeable foods (Fruth and
Hohmann, 2002;Yamamoto, 2015), co-defending access to food re-
sources (White and Wood, 2007) and participating in coalitionary ag-
gression, which frequently targets males (Nurmi et al., 2018;Surbeck
and Hohmann, 2013;Tokuyama and Furuichi, 2016).
As in all anthropoid primates, female bonobos exhibit extended
sexuality, characterized by sexual proceptivity and receptivity that is
not limited to the fertile period (Wallen and Zehr, 2004). Bonobos also
share with chimpanzees and some old world monkeys ‘exaggerated
sexual swellings’, referring to conspicuous fluctuations in the size,
firmness and color of their perineal sex skin across their menstrual
cycles (Nunn, 1999). However, relative to other primates, their sexual
swellings are less reliable indicators of ovulation (Douglas et al., 2016;
Furuichi, 1987), and they exhibit higher levels of proceptive and re-
ceptive sexual behavior during anovulatory periods, including during
pregnancy and lactational amenorrhea (Furuichi et al., 2014). Thus the
majority of copulations in bonobos are unlikely to serve a reproductive
function. In contrast with evidence in humans (Chapais, 2013) and
other socially-monogamous primates (Snowdon et al., 2010), in bo-
nobos non-reproductive sex between females and males does not appear
to increase pair-bonding or other forms of male investment (Goldstone
et al., 2016;Yamamoto, 2015). Rather, the high frequency of non-
conceptive copulations may help to reduce male harassment and in-
crease paternity confusion, which may contribute to the lack of evi-
dence for infanticide in bonobos (reviewed in Furuichi et al., 2014).
Habitual same-sex sexual behavior among female bonobos primarily
consists of genito-genital rubbing (or GG-rubbing), in which females
embrace ventro-ventrally and use rapid lateral hip movements to rub
their genital swellings together (Hohmann and Fruth, 2000). Females
appear to use GG-rubbing flexibly as a quick and efficient means to
signal trust and social tolerance with a broad range of partners
(Moscovice et al., 2017), which may promote various forms of co-
operation. Previous studies provide indirect evidence that GG-rubbing
may facilitate cooperation by: i) helping recent female immigrants to
initiate social relationships with other young females and with long-
term residents of higher social status (Idani, 1991;Sakamaki et al.,
2015); and by ii) increasing tolerance and reducing tension in poten-
tially tense social contexts, including during fusions when members of a
community reunite after associating in different sub-groups (Moscovice
et al., 2015) and in competitive feeding contexts (de Waal, 1987;
Douglas and Moscovice, 2015;Fruth and Hohmann, 2006;Hohmann
et al., 2009).
In the current study we investigate behavioral and physiological
outcomes of same-sex sexual behavior in female bonobos in comparison
with outcomes related to sexual interactions with males, the majority of
which are unlikely to result in insemination (Douglas et al., 2016).
While previous studies have sometimes combined intra- and inter-
sexual interactions when examining non-reproductive functions of
sexual behavior more generally (de Waal, 1990;Hohmann et al., 2009),
here we evaluate the evidence for GG-rubbing and copulations sepa-
rately, in order to test for a unique role of habitual same-sex sexual
L.R. Moscovice, et al. Hormones and Behavior 116 (2019) 104581
2
behavior in facilitating female-biased cooperation in bonobos. In this
case, we predict that in potentially competitive contexts in which co-
operation is especially beneficial, i) females will be more likely to en-
gage in GG-rubbing than in copulations (Sex preference hypothesis), ii)
GG-rubbing, but not copulations, will lead to increases in close proxi-
mity between partners (Post-sex behavior hypothesis) and iii) periph-
eral OT concentrations will increase in females following GG-rubbing
but not after copulations (Post-sex physiology hypothesis). Finally, if
female same-sex sexual interactions are associated with increases in
close proximity and oxytocin, then iv) female dyads who have more
frequent sexual interactions will also have more opportunities and
motivation to participate in other forms of cooperation, such as coali-
tionary alliances (Coalitionary support hypothesis). Alternatively, it is
possible that sexual behavior in bonobos helps to maintain cooperative
relationships with a subset of unrelated male and female partners,
analogous to the role of grooming in chimpanzees and other primate
species (Mitani, 2009). In this case, females will exhibit higher fre-
quencies of sexual behavior and greater post-sex maintenance of close
proximity with a subset of unrelated females and males who are more
preferred partners for other forms of affiliation and cooperation.
Changes in uOT concentrations following sexual interactions will be
predicted by the strength of the social relationship between partners,
and the amount of joint coalitionary support among female-female as
well as inter-sexual dyads will be predicted by their frequency of sexual
interactions.
2. Material and methods
We conducted this study on the wild, habituated Bompusa bonobo
community at LuiKotale, Democratic Republic of Congo (DRC)
(Hohmann and Fruth, 2003b) during 1483 observation hours between
January 2013 – May 2014. All research adhered to the legal require-
ments of the DRC and the Institut Congolais pour la Conservation
de la Nature (ICCN). Methods for data and sample collection were
non-invasive and adhered to the American Society of Primatolo-
gists (ASP) Principles for the Ethical Treatment of Non-Human
Primates. The community consisted of between 36 and 40 individuals,
including n= 13 parous, resident females along with their juvenile and
infant offspring, n= 7 mature males estimated to be > 10 years of age
based on body size and dentition, n= 4 natal sub-adults (3 F, 1 M)
between 7 and 8 years of age and n= 3 nulliparous female immigrants
who associated with the community for at least six months during the
study period and were considered as subadults in analyses. Among
adults and sub-adults, close relatives, defined as parents and offspring
(n= 9 dyads) or maternal siblings (n= 6 dyads) were known based on
previous parentage analyses (Moscovice et al., 2017;Surbeck et al.,
2017b). All other adult and sub-adult dyads were classified as non-kin.
We collected behavioral data and urine samples during half-day focal
follows of the thirteen parous females and seven mature males (mean
(x± SD) = 31.5 ( ± 15.1) h per subject). At five-minute intervals we
recorded the behavior of the focal subject and the identity of any social
partners for grooming. At fifteen-minute intervals we recorded the
identity of all partners within close proximity (≤1 m). At 30-min in-
tervals we recorded cumulative party compositions that included all
individuals observed in the previous 29 min. We also recorded all oc-
currences of sexual behavior between focal subjects and other mature
or sub-adult partners, including copulations and any non-penetrative
genital contact. For each independent sexual event (separated by > 1
min or involving a new partner), we recorded the identity of the
partner and additional information when possible on the duration of the
sexual event, the context(s) in which the sexual event occurred and
maintenance of post-sex proximity between former sexual partners
following the sexual interaction. Individuals were considered to remain
within close proximity when they engaged in their next non-sexual
activity (e.g. feeding, resting, traveling) while maintaining a distance of
≤1 m (within arm's reach) of their previous sexual partner. We did not
systematically record the duration of post-sex time in close proximity,
but rather considered the initial decision to remain within close
proximity or not following sex as a sign of social tolerance, as such close
proximity is rare in primates apart from a subset of preferred associates
(Dubuc et al., 2012). We recorded all occurrences of food sharing,
which was defined whenever a possessor shared some part of a pre-
ferred, monopolizeable food item (primarily meat or the large fruits of
Treculia africana or Anonidium mannii) with a bystander, either by
passively allowing a bystander to take pieces of the food, or in rarer
cases by actively transferring part of the food item to a bystander. We
also recorded all occurrences of aggression, which was defined as
charging, chasing and/or contact aggression, including holding, hitting,
or biting, where the intended target was clearly identifiable. Coali-
tionary aggression was recorded whenever two or more individuals
directed any aggressive behaviors in a coordinated fashion against a
third party. In the case of polyadic coalitions, we considered as coali-
tion partners all combinations of dyads that directed aggression to-
wards the same target during an aggressive event.
2.1. Characterizing relationships between individuals
We calculated dyadic Composite Relationship Indices (dyaCRIs)
modified from Crockford et al. (2013) for n= 146 inter-sexual and
n= 156 female dyads, representing all focal subjects with each
other or with sub-adults (excluding male-male dyads since they
were not the focus of analyses). We first determined directional
CRIs (dirCRI) for each individual within a dyad based on: 1) The
proportion of focal scans during which an individual was involved
in common socio-positive behaviors (SPcommon; giving grooming
or staying in close proximity) with each partner, 2) The frequency
with which individuals directed rare socio-positive behaviors
(SPrare; giving support in coalitions or food sharing) to each
partner; and 3) The frequency with which individuals directed ag-
gression to each partner, as a socio-negative (SN) score. The dirCRI
for actor (A
i
) and recipient (B
j
) was calculated as: (SPcommon A
i
B
j
+
SPrare AiBj)/ 2 − SN A
i
B
j
. Each dirCRI was divided by the mean
dirCRI for the given sex class (FF or FM), to correct for differences
in the frequencies of these behaviors across sex-classes. The
dyaCRI was calculated by summing the dirCRIs for partners. Posi-
tive values indicate relationships characterized by net socio-posi-
tive interactions.
2.2. Hormone collection, analyses and validations
We collected n= 55 urine samples from n= 13 female subjects
between 15 and 60 min following either GG-rubbing events (n= 35
samples, 2.7 ( ± 1.5) per subject) or copulations (n= 20 samples, 1.5
( ± 1.7) per subject) with seven male and eighteen female partners. We
assumed a clearance time of uOT in bonobos of 15–60 min after se-
cretion, based on a human clearance study (Amico et al., 1987) as well
as several studies in chimpanzees indicating changes in uOT con-
centrations following biologically-relevant social interactions that oc-
curred within this time window (Crockford et al., 2013;Samuni et al.,
2017;Wittig et al., 2014). We included in the analyses n =13 post-sex
samples (1 ( ± 0.70) per subject) following multiple, independent
sexual events (with the same or with different partners), as long as the
events included only one type of sexual interaction (either copulations
or GG-rubbing). Post-copulation urine samples represented mean
( ± SD) = 1.5 ( ± 0.70) copulation events, totalling 20 ( ± 12.8) s of
sexual interactions. Only one post-copulation sample (0.05%) occurred
following copulations with more than one partner. Post-GG-rubbing
samples represented 1.6 ( ± 0.82) GG-rubbing events, totalling 21.5
( ± 19.0) s and 34.3% of samples (n= 12) involved GG-rubbing events
with more than one partner (mean ( ± SD) = 1.44 ( ± 0.66) partners
per sample). We only included post-sex samples when subjects did not
engage in any other direct affiliative or aggressive interactions in the
L.R. Moscovice, et al. Hormones and Behavior 116 (2019) 104581
3
intervening period between the sexual interaction(s) and sample col-
lection. For comparison, we collected n= 88 baseline urine samples
from the same females (6.8 ( ± 5.2) per female) following a period
of > 60 mn during which the subjects were not involved in any direct
affiliative, sexual or aggressive interactions with other adults or sub-
adults. Although samples were often collected in feeding contexts, we
excluded from analyses any post-sex or baseline urine samples that
occurred in food sharing contexts (while feeding on meat or highly
preferred, monopolizeable fruits) due to evidence that food sharing is
associated with elevated oxytocin in other species (e.g. Wittig et al.,
2014). Samples were collected either in plastic bags or on leaves, pi-
petted into cryo vials and kept in a cooled thermos until arrival in
camp, when they were transferred into liquid nitrogen.
Urine samples were transported frozen from the field site to the
Endocrine Laboratory at the Max Planck Institute for Evolutionary
Anthropology, where they were kept frozen at −20 °C until extraction
following a modified protocol from Assay Designs. In brief, thawed
samples were vortexed and centrifuged at 4 °C (5 min, 3000 rpm).
500 μl of urine were loaded on 30 mg Sep-Pak HR-X 1 ml cartridges
(Macherey and Nagel), primed with 1 ml methanol and 1 ml HPLC
water. Samples were washed with a 10% acetonitrile/1% tri-
fluoroacetic-acid solution. Samples were eluted in an 80/20% acet-
onitrile solution. Samples were evaporated with air stream and then
resuspended in 300 μl ethanol in a final precipitation step, in order to
minimize any additional cross-reactivity. Samples were kept at 4 °C for
30 min, then re-evaporated and either frozen overnight or measured
immediately. uOT was measured using an Enzyme Immuno-Assay (EIA,
Assay Designs; catalogue no. ADI-901-153). The assay standard curve
ranged from 15.62 to 1000 pg/ml and assay sensitivity was 15 pg/ml.
Final uOT concentrations were calculated as pg OT per mg creatinine to
compensate for variation in sample concentrations. Inter-assay coeffi-
cients of variation of low- (62.5 pg ml
−1
) and high- (250 pg ml
−1
) value
quality controls were 27.7 and 18.1% respectively (n= 48). Intra-assay
coefficients of variation of low- and high-value quality controls were
9.2% and 6.8% respectively. We performed a series of validations to
confirm that the assay captures the majority of OT and its metabolites
and is suitable for measuring OT secretion in bonobo urine (see also
supplementary data and Fig. S1). Tests of parallelism revealed no dif-
ferences in the slopes between the standard curve and a serial dilution
of pooled bonobo urine spiked with concentrated standard
(10,000 pg ml
−1
) from the ELISA kit (t= 0.724, p= 0.491, n= 6).
Recovery of OT in urine samples spiked with OT standards at three
different concentrations spanning the linear range (4500 pg ml
−1
,
1500 pg ml
−1
, 500 pg ml
−1
) was 87.6 ( ± 16.0)% (n = 6 standard
curve points).
2.3. Statistical analyses
We fit mixed models in R (version 3.5.1, R Core Team, 2018) using
the packages ‘lme4’ (Bates et al., 2014) and ‘glmmADMB’ (Fournier
et al., 2012). To test whether females preferentially engage in sex with
members of the more cooperative sex (Sex preference hypothesis), we
fit a zero-inflated poisson generalized linear mixed model (GLMM),
with the number of times dyads engaged in sexual behavior in feeding
contexts as the response. We included as the predictor an interaction
between the dyadic sex combination and the dyaCRI score, since the
influence of relationship quality on the likelihood of having sex may
differ based on the sex of the partner. However, the interaction term
was not significant (est ± SE = −0.07 ± 0.11, p= 0.48) and was
removed from the final model. We included total dyadic observation
time in the same party as an offset term, subject a and b within the dyad
as random effects, and included random slopes of dyadic sex combi-
nation within subject. To test whether remaining in close proximity
following sexual interactions was predicted by the sex of the partner
(Post-sex behavior hypothesis), we fit a binomial GLMM with the post-
sex distance (≤ 1 m or > 1 m) between individuals as the response.
This model included the subset of n= 333 GG-rubbing events and
n= 122 copulations in feeding contexts for which we also had data on
the distance between individuals during their first post-sex activities.
We again included as the predictor an interaction between dyadic sex
combination and dyaCRI score, but the interaction term was not sig-
nificant (est ± SE = 0.22 ± 0.34, p= 0.53) and was removed from
the final model. We controlled in the model for contexts that occurred
together with feeding and that may have had additional influences on
sexual behavior, including aggression, changes in party composition or
sharing of highly preferred, monopolizeable foods (see Table 2 and
Table S1). We included each subject, the dyad and each feeding bout
(defined as the period of time while located in the same feeding tree, or
in the same food patch if feeding on the ground) as random effects, and
included random slopes of all predictors within subject and dyadic CRI
score within feeding bout.
To test for a differentiated physiological response to sexual behavior
according to the sex of the partner (Post-sex physiology hypothesis), we
ran a gaussian LMM in which we paired each subjects' post-GG-rubbing
or post-copulation urine sample with one baseline non-sexual sample
that was collected as close in time to the sexual event as possible (mean
( ± SD) = 5.9 ( ± 8.7) days between paired samples). This provided a
precise measure of short-term changes in uOT associated with each
sexual event. We tested whether uOT concentrations were influenced
by an interaction between type of sample (baseline vs post-sex, re-
presenting relative changes in uOT) and type of sexual event (copula-
tion vs GG-rubbing). We also interacted type of sample with the dyaCRI
score between sexual partners. For one copulation and twelve GG-
rubbing samples that occurred after sexual events with multiple part-
ners of the same sex, we used the largest dyaCRI score from among the
previous partners to represent the maximal strength of social relation-
ships. We controlled in the model for the effect of having sex with more
than one partner and for the time lag from the initiation of the sexual
interaction until sample collection on uOT concentrations. We also
controlled for stage of sexual swelling, since it tended to influence uOT
in a preliminary model testing whether uOT increases following any
sexual event compared to baseline (see supplementary data and Table
S4). We included random effects for subject, feeding bout and to ac-
count for the pairing of each pre- and post-sex sample. We included
random slopes of test predictors within subject. We also conducted
planned comparisons of estimated marginal means (emm) using the
Bonferroni adjustment of p-values in the package “em means” (Lenth,
2018) to compare uOT between post-GG-rubbing and post-copulation
samples, as well as between each type of post-sex sample and baseline.
Although we did not analyze any urine samples that were collected
in food sharing contexts, both post-sex and baseline urine samples were
often collected in feeding contexts, and it is possible that feeding alone
may induce changes in OT (Sabatier et al., 2013). We tested for any
possible effects of feeding on OT by comparing uOT from the subset of
baseline samples that were collected following feeding while alone
(n= 16), feeding with a partner in close proximity (n= 5) or without
any feeding in the previous hour (n= 19 samples). We also tested
whether uOT was higher in samples that occurred following feeding
with GG-rubbing (n= 22) vs feeding without GG-rubbing (n= 21). In
both models we controlled for fluctuations in sexual swelling size and
included random effects of subject and random slopes of swelling and
sampling context (feeding alone, feeding near partner, no feeding)
within subject.
To test whether the amount of joint coalitionary support between
unrelated dyads was predicted by their frequency of sexual interactions
(Coalitionary support hypothesis), we fit a poisson GLMM, with the
number of times each dyad engaged in joint coalitionary aggression as
the response. We included as the predictor an interaction between the
dyadic sex combination (FF vs FM) and the frequency of sexual inter-
actions, since we predicted that the impact of sexual interactions on the
likelihood of additional cooperation would differ based on the sex of
the partner. However, the interaction term was not significant
L.R. Moscovice, et al. Hormones and Behavior 116 (2019) 104581
4
(est ± SE = −0.30 ± 0.52, p= 0.57) and was removed from the final
model. We included dyadic observation time in the same party as an
offset term. We included each subject within the dyad as random ef-
fects, and included random slopes of frequency of sexual interactions
within subject A and dyadic sex combination within subject B.
In all models, continuous predictors were log transformed when
necessary to achieve normal distributions and were also normalized to a
mean of zero and a standard deviation of 1 using a z-transformation. We
confirmed that the models were stable by comparing the estimates
derived from a model based on the full data set with those obtained
from a model with each subject excluded one by one. We also used the
“vif” function in the package “car” (Fox and Weisberg, 2011), to test for
variance inflation and found no evidence for collinearity of the pre-
dictors (max VIF = 1.77). For GLMMs, we confirmed that the models
were not overdispersed (chi-sq = 113.13–431.18, p= 0.13–1, disper-
sion parameters = 0.50–1.09). We used likelihood ratio tests to com-
pare each model to a null model excluding the test predictors and
present results of models that differed significantly from the null model.
Unless otherwise noted, results are presented as mean ( ± SD).
3. Results
We observed n= 971 independent sexual events (0.65 per h) in-
volving the n= 20 focal subjects, either with each other or with the
n= 7 sub-adults. The distribution of sexual interactions among dif-
ferent dyadic sex combinations reflects their different propensities for
cooperation. The majority (65%, n= 627, 0.42 per hour), involved
sexual interactions among n= 105 unrelated female dyads, re-
presenting 70.1% of all unrelated female dyads. All but nine of these
interactions (98.6%) involved GG-rubbing. Ten female sexual interac-
tions between close relatives (one mother-adult daughter and two sister
dyads) were excluded from further analyses. An additional 34% of
events (n= 330, 0.22 per hour) involved inter-sexual interactions
among n= 79 inter-sexual dyads, representing 56.4% of all unrelated
inter-sexual dyads. The majority of these interactions (83.5%) consisted
of copulations. Sexual interactions between males, the dyadic sex
combination with the lowest levels of cooperation, occurred among two
dyads, representing 7.7% of unrelated male dyads and accounted
for < 1% of observations (n= 4, 0.002 per hour). The relative number
of dyads of each sex combination that were observed having sex at least
once during the study period differed significantly from expected (chi-
square = 190.67, df = 2, p< 0.001). This was due to more female-
female dyads and fewer male-male dyads engaging in sexual interac-
tions than predicted, based on their relative frequencies in the com-
munity (see Fig. S2).
The majority of GG-rubbing (n= 513, 91.9%) and copulations
(n= 195, 84.1%) occurred in feeding contexts (see Table S1), where
females frequently form alliances that aggressively exclude males
(Nurmi et al., 2018;Surbeck and Hohmann, 2013), while often feeding
in close proximity or sharing monopolizeable foods with other females
(Douglas and Moscovice, 2015;Yamamoto, 2015). Consistent with the
sex preference hypothesis, female dyads engaged in significantly more
sexual interactions in feeding contexts than did inter-sexual dyads
(GLMM, likelihood ratio text, chi-sq = 23.34, df = 3, p < 0.001,
est. ± SE = 1.10 ± 0.17, p < 0.001, see Table 1 and Table S2). Re-
lationship quality measured by the dyaCRI did not influence dyadic
frequencies of sexual interactions (see Table 1).
Consistent with the post-sex behavior hypothesis, females were
more likely to remain within close proximity to their partners following
GG-rubbing compared with copulations (56% of GG-rubbing events vs
35% of copulations, GLMM, likelihood ratio test, chi-sq = 8.74, df = 3,
p= 0.03, est. ± SE = 0.72 ± 0.27, p= 0.01, see Fig. 1 and Table 2).
The sex of the partner remained a significant predictor of staying in
close proximity after controlling for sex that occurred in food sharing
contexts, which also increased the likelihood of staying in close proxi-
mity (see Table 2). As in the sex preference model, the measure of
relationship quality did not influence the outcome (see Table 2). To
examine whether this result merely reflects a more general tendency for
females to remain in closer spatial proximity with other females than
with males, we also tested whether GG-rubbing or copulations influ-
enced the likelihood of remaining in close proximity following sex for
the subset of n= 302 events where partners were not in close proximity
before their sexual interaction. Partners who were initially > 1 m apart
were more likely to remain in close proximity after GG-rubbing (n= 93
Table 1
Results of a GLMM predicting the effects of dyadic sex combination (relative to
FM) and Composite Relationship Index (CRI) on frequencies of sex in feeding
contexts (sex preference model). Statistically significant predictors (p< 0.05)
are indicated in bold.
Term est ± SE chi-sq df p value
(Intercept) 0.47 ± 0.17
Test predictors:
Dyadic sex combination (FF) 1.10 ± 0.17 6.27 1 < 0.001
Dyadic CRI 0.02 ± 0.06 0.29 1 0.77
Fig. 1. Influence of different types of sex on the likelihood that partners remain
within arm's reach during their subsequent post-sex activity. Box plots indicate
medians and 25–75% interquartile ranges. The Tukey-style whiskers extend to a
maximum of 1.5 × IQR beyond the box. For full model results see Table 2.
Table 2
Results of a GLMM predicting the effects of dyadic sex combination (relative to
FM) and Composite Relationship Index (CRI) on the likelihood of staying in
close proximity after sex (post-sex behavior model). Statistically significant
predictors (p < 0.05) are indicated in bold.
Term est ± SE chi-sq df p value
(Intercept) −0.76 ± 0.24
Test predictors:
Dyadic sex combination (FF) 0.72 ± 0.27 6.25 1 0.01
Dyadic CRI −0.21 ± 0.14 1.83 1 0.18
Control predictors:
Context: Feed + food sharing
a
1.64 ± 0.57 9.09 3 0.03
Context: Feed + aggression
a
−0.17 ± 0.52
Context: Feed + change in party
a
0.58 ± 0.46
a
Chi-square, df and pvalues refer to comparison with reference category:
Feeding without additional contexts.
L.R. Moscovice, et al. Hormones and Behavior 116 (2019) 104581
5
events (48%) than after copulations (n = 30 events (28%), GLMM,
likelihood ratio test, chi-sq = 4.23, df = 1, p= 0.04, est. ±
SE = 0.71 ± 0.31, p = 0.04, see Table S3), suggesting that GG-rub-
bing is more effective than copulations in establishing proximity.
As expected based on the central role of OT in mediating female
reproductive behavior more generally, female uOT concentrations
tended to be higher following any sexual events (n= 55) compared to
baseline (n= 89 samples, LMM, likelihood ratio test, chi-sq = 3.7,
df = 1, p= 0.05, est. ± SE = 0.31 ± 0.15, p = 0.05, see supplemen-
tary data and Table S4). However, consistent with the post-sex phy-
siology hypothesis, females also exhibited differentiated physiological
responses following different types of sexual interactions (LMM, like-
lihood ratio test, chi-sq = 14.8, df = 7, p = 0.04,
est. ± SE = 0.65 ± 0.30, p = 0.03, see Fig. 2 and Table 3). Planned
comparisons indicated that log uOT concentrations rose significantly
from baseline following GG-rubbing (emm ± SE = 5.45 ± 0.19, vs
4.85 ± 0.21, z = 2.96, adj. p= 0.02), but did not differ from baseline
following copulations (emm ± SE = 4.81 ± 0.27 vs 4.86 ± 0.27,
z = −0.17, adj. p= 0.98). Post-GG-rubbing samples also tended to be
higher than post-copulation samples (z = 2.28, adj. p = 0.05, see Table
S5). Post-sex changes in uOT concentrations were not influenced by the
quality of the relationship with the sexual partner (see Table 3).
Consistent with the prevalence of sexual interactions in feeding
contexts, the majority of post-copulation (75%, n= 15), as well as post-
GG-rubbing (86%, n = 30) urine samples were collected in feeding
contexts, and thus also represent post-feeding samples on one of over
sixteen different food types that were consumed across the sampling
period. An additional 24% (n= 21) of baseline samples were also
collected within an hour following feeding events. We found no dif-
ferences in uOT between baseline samples collected in feeding vs non-
feeding contexts (GLMM, likelihood ratio test, chi-sq = 0.04, df = 2,
p = 0.98). Females had higher uOT concentrations after feeding and
engaging in GG-rubbing, compared with post-feeding samples without
any sexual interactions (likelihood ratio test, chi-square = 10.63,
df = 1, p= 0.001, est. ± SE = 0.95 ± 0.10, p< 0.001, see Table
S6). These combined results suggest that the link between specific
sexual interactions and elevated uOT is independent of feeding beha-
vior.
We observed n= 38 independent coalitions (0.03 per hour), of
which 24% (n = 9) involved more than two coalition partners, and 71%
Fig. 2. Comparison of uOT concentrations (log transformed) between paired baseline and post-sex samples collected within similar time frames. Box plots indicate
medians and 25–75% interquartile ranges. The Tukey-style whiskers extend to a maximum of 1.5 ×IQR beyond the box. For full model results see Table 3.
Table 3
Results of a LMM predicting the effects of dyadic sex combination (relative to
FM) and composite relationship index (CRI) on relative changes in uOT (log
transformed) from pre- to post-sex samples (post-sex physiology model).
Statistically significant predictors (p < 0.05) are indicated in bold.
Term est ± SE chi-sq df p value
Intercept 5.46 ± 0.26
Test predictors:
Sample type(post-sex) :Sex
combination (FF)
⁎
0.65 ± 0.30 4.55 1 0.03
Sample type(post-sex) : Dyadic CRI −0.05 ± 0.14 0.11 1 0.74
Control predictors:
Sample type (post-sex) : > 1 partner
†
0.29 ± 0.34 0.71 1 0.40
Sample type (post-sex) : Time between
event and sample
0.05 ± 0.14 0.16 1 0.69
Swelling score 1
‡
0.73 ± 0.26 8.99 3 0.03
Swelling score 2
‡
0.07 ± 0.25
Swelling score 3
‡
−0.09 ± 0.20
⁎,†,‡
Chi-square, df and p values refer to comparison with reference categories:
*Changes in uOT from baseline to post-sex following sex with males;
†
Changes
in uOT from baseline to post-sex following sex with only one partner,
‡
Relative
to swelling score 4 (most tumescent).
L.R. Moscovice, et al. Hormones and Behavior 116 (2019) 104581
6
(n= 27) included unrelated coalition partners. Consistent with sex
differences in cooperation more generally, the majority of non-kin
coalitions occurred among females (73%, n= 37 dyads), while 24% of
coalitions (n= 12 dyads) involved opposite-sex partners and only 5%
of coalitions occurred among males (n = 2 dyads). Unrelated dyads
who had more sexual interactions also participated in more joint coa-
litionary aggression (GLMM, likelihood ratio test, chi-sq = 12.42,
df = 3, p= 0.006, est. ± SE = 0.66 ± 0.26, p= 0.01, see Fig. 3 and
Table 4). In contrast with predictions from the coalitionary support
hypothesis, this effect was similar for intra- as well as inter-sexual
dyads. However, female dyads tended to engage in more joint coali-
tionary aggression than did inter-sexual dyads (see Fig. 3 and Table 4).
4. Discussion
Results of this study support a link between habitual same-sex
sexual behavior and cooperation and suggest a novel mechanism by
which such sexual behavior may promote additional cooperation in
female bonobos, via oxytocinergic effects. Female preferences for fe-
male over male sexual partners in feeding contexts are reflected in an
increase in close proximity and uOT following same-sex but not oppo-
site-sex sexual interactions. Furthermore, female dyads that have higher
frequencies of sexual interactions also support each other more often in
intra-sexual coalitions, which reinforce female priority of access to
preferred resources (Nurmi et al., 2018) and may reduce male harass-
ment (Tokuyama and Furuichi, 2016). Future efforts will focus on in-
creasing the number of physiological samples to measure changes in
uOT following sexual interactions that co-occur with additional co-
operation, such as coalitionary support or food sharing, in comparison
with sexual interactions without any additional cooperation. This will
help to further clarify the role of oxytocin and sexual interactions in
facilitating cooperation among female bonobos.
Among non-kin, both intra- and inter-sexual dyads who engaged in
more frequent sexual interactions were more likely to engage in joint
coalitionary aggression against third parties. These results are inter-
esting, given that previous investigations considering only female dyads
have failed to find a link between GG-rubbing and coalitionary support
(Moscovice et al., 2017;Tokuyama and Furuichi, 2016). In addition to
including data from inter-sexual dyads, our analysis also differs from a
previous study at this site (Moscovice et al., 2017) in that we included
data from polyadic coalitions, which increased our sample size and
allowed us to test whether dyads who exhibit more sexual behavior also
engage in a greater number of coalitions, rather than merely measuring
coalitionary support as present or absent in dyads. This distinction is
important because effects of socio-positive interactions on associated
oxytocin release and subsequent motivations to cooperate are likely to
be cumulative, becoming stronger in dyads who have more opportu-
nities to engage in emotionally-rewarding sexual interactions (Grewen
et al., 2005).
Planned comparisons of the significant test predictors in the post-sex
physiology model indicate that post-copulation uOT samples did not
consistently differ from baseline. Vagino-cervical stimulation is con-
sidered a potent trigger of OT release in females more generally
(Borrow and Cameron, 2012), but there are also a range of contextual
factors that can influence OT responses to sexual stimuli, including the
intensity of orgasm (humans: Carmichael et al., 1994; rabbits: Todd and
Lightman, 1986), and the extent to which females have control over
their sexual interactions (rats: Nyuyki et al., 2011). Our results suggest
that in bonobos as well, oxytocinergic responses to sexual interactions
are mediated by additional contextual factors.
Behaviorally, there are important distinctions between GG-rubbing
and copulations that may help to explain the differences in underlying
physiology. While copulations among wild bonobos most frequently
occur in a ventro-dorsal position (Furuichi, 1987;Thompson-Handler
et al., 1984, see Fig. S3a), GG-rubbing requires face-to-face contact,
often involving mutual gaze, as well as a high degree of coordination of
body movements to achieve and maintain genital stimulation (see Fig.
S3b). In humans, mutual gaze and behavioral coordination are im-
portant for the formation of various social attachments and increases in
these behaviors are associated with increases in peripheral OT across a
range of relationships, including between mothers and infants
(Feldman, 2012), romantic partners (Grewen et al., 2005;
Schneiderman et al., 2012) and between dog owners and their pets
(Nagasawa et al., 2009). GG-rubbing may thus be an especially effective
means of communicating about trust and motivations to cooperate
(Wrangham, 1993), which may also correspond with increases in per-
ipheral OT. There is also anatomical and behavioral evidence that GG-
rubbing provides direct clitoral stimulation, and is likely to be asso-
ciated with orgasm in female bonobos (Blount, 1990;Dahl, 1985). The
observed increases in uOT specifically in response to GG-rubbing pro-
vides further support for a link between GG-rubbing and orgasm.
We did not directly test whether GG-rubbing contributes to co-
operation by promoting the establishment and maintenance of selective
social relationships (e.g. Idani, 1991) or by reducing social conflict
among partners who may not otherwise be strong associates (e.g. de
Waal, 1987;Moscovice et al., 2017). However, our measure of dyadic
relationship quality, which was weighted to reflect stronger or weaker
social preferences than on average for each sex combination, did not
predict any of the behavioral or physiological outcomes. Thus our re-
sults are more consistent with the ‘reductions in social conflict’ hy-
pothesis to explain how habitual same-sex sexual interactions influence
cooperative outcomes for female bonobos. Same-sex sexual behavior
may reduce social conflict in part by promoting close proximity be-
tween partners, which may lead to additional mutually-beneficial co-
operation such as co-defending access to food (Nurmi et al., 2018). In a
captive study, females faced with a potentially competitive feeding task
Fig. 3. Relationship between dyadic frequency of sexual interactions (log
transformed) and participation in joint coalitionary aggression. The size of the
shapes indicates the number of dyads receiving each score. For full model re-
sults see Table 4.
Table 4
Results of a GLMM measuring how the number of sexual interactions between
partners (corrected for observation time), and the sex of the partner impact on
the amount of coalitionary support between partners. Statistically significant
predictors (p < 0.05) are indicated in bold.
Term est ± SE chi-sq df p value
Intercept −2.9 ± 0.50
Number of sexual interactions 0.66 ± 0.26 7.12 1 0.01
Dyadic sex combination (FF) 0.82 ± 0.50 2.71 1 0.10
L.R. Moscovice, et al. Hormones and Behavior 116 (2019) 104581
7
exhibited increases in same-sex but not opposite-sex sexual behavior
and then shared access to a monopolizeable food exclusively with other
females (Hohmann et al., 2009). These females also exhibited decreases
in concentrations of the stress hormone cortisol during the feeding task,
suggesting a possible physiological link between increased GG-rubbing
and reductions in social tension.
Among chimpanzees, same-sex sexual interactions are sometimes
observed in socially-tense situations, especially among males (e.g.
Romero et al., 2011). However, such behavior is infrequent in com-
parison to the frequencies observed among female bonobos (reviewed
in Gruber and Clay, 2016). Chimpanzees do engage in frequent social
grooming and exhibit selective increases in uOT following grooming,
but in this case increases in uOT concentrations are predicted by the
strength of the dyadic social relationship, and not by the sex of the
grooming partner (Crockford et al., 2013). While these results appear to
contrast with our findings, they make sense in light of the differences in
social dynamics between these two close phylogenetic relatives
(Surbeck et al., 2017a). In chimpanzees cooperation is mainly dyadic
and is largely predicted by the strength and stability of grooming re-
lationships between kin and a subset of non-kin bond partners (re-
viewed in Mitani, 2009). In contrast in bonobos cooperation occurs
among a wide range of primarily female social partners (Moscovice
et al., 2017;Yamamoto, 2015), is frequently polyadic (Nurmi et al.,
2018;Tokuyama and Furuichi, 2016) and is not linked to measures of
association and grooming (Moscovice et al., 2017;Tokuyama and
Furuichi, 2016). Thus, in both Pan species, individuals exhibit selective
changes in uOT following socio-positive interactions with partners who
are more likely to cooperate in other contexts.
5. Conclusions
Although same-sex sexual interactions have been reported across a
wide range of animal taxa (Bailey and Zuk, 2009), they occur as fre-
quently as opposite-sex sexual interactions in only a few species and sex
combinations, including male dolphins and female bonobos. In humans,
cross-culturally and historically a proportion of the population engages
in habitual or exclusive same-sex sexual interactions (reviewed in
Kirkpatrick, 2000;Sommer and Lowe, 2018). Research on the evolution
of non-reproductive sexual behavior in humans often emphasizes its
role in maintaining stable opposite-sex pair bonds that improve access
to resources for females and paternity certainty for males (Chapais,
2013;Gangestad and Grebe, 2017). However, the alliance theory of
homosexual behavior (Kirkpatrick, 2000;Muscarella, 2005) emphasizes
the importance of stable same-sex alliances that are often reinforced
through sexual interactions in providing benefits such as social support,
resource sharing and mutual defense (Kirkpatrick, 2000;Sommer and
Lowe, 2018). Comparative evidence suggests that this theory may also
be relevant for explaining the evolution of habitual same-sex sexual
behavior in species such as dolphins and bonobos that share with hu-
mans complex fission-fusion social systems, high levels of social cog-
nition and extensive cooperation outside of kinship.
In contrast with evidence in humans and dolphins, in bonobos fe-
males do not restrict same-sex sexual interactions to a subset of pre-
ferred partners (Hohmann and Fruth, 2000;Moscovice et al., 2017).
Rather, females use sexual interactions flexibly to signal social toler-
ance and promote close proximity with a wide range of female partners.
Female sexual interactions are associated with OT release that may
facilitate additional female-biased cooperation. These results provide a
novel example of the co-option of the oxytocinergic system outside of
kinship and selective pair bonds to facilitate flexible cooperation in a
close phylogenetic relative of humans.
CRediT authorship contribution statement
Liza R. Moscovice: Conceptualization, Methodology, Investigation,
Formal Analysis, Writing - original draft, Funding Acquisition. Martin
Surbeck: Conceptualization, Methodology, Investigation, Writing - re-
view & editing, Funding Acquisition. Barbara Fruth: Writing - review &
editing, Funding Acquisition. Gottfried Hohmann: Conceptualization,
Methodology, Writing - review & editing, Funding Acquisition.Adrian
V. Jaeggi: Writing - review & editing, Funding Acquisition. Tobias
Deschner: Conceptualization, Methodology, Writing - review & editing,
Resources, Funding Acquisition.
Declaration of competing interest
None.
Acknowledgements
This research was supported by the Max Planck Society and by
additional funding from the Leakey Foundation, the Wenner-Gren
Foundation (grant no. 8450 to L.R.M and grant no. 8914 to M.S.), the
National Geographic Society (GEFNE119-14 to M.S.) and the
VolkswagenStiftung (Grant No. 86048 to L.R.M.). In addition, L.R.M.
was supported by Emory University and M.S. was supported by the
SNSF. We thank the Institut Congolais pour la Conservation de la
Nature (ICCN) for permission to work in the Democratic Republic of
Congo, and the people of the village of Lompole for granting access to
their forest. Laura Martinéz-Inigo, Pamela Heidi Douglas, Lucas
Goldstone, Max Kölbl and Luis Férnandez assisted with field data and
sample collection. Vera Schmeling and Roisin Murtagh provided im-
portant assistance in sample analysis and in validation of the EIA.
Franka Simea Schaebs and Verena Behringer provided helpful input on
laboratory methods. Frieder Hadlich provided help with figures. We
thank Kim Wallen and two anonymous reviewers for their helpful
feedback that led to several improvements to the original manuscript.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.yhbeh.2019.104581.
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