Uniting against a common enemy: Perceived outgroup threat elicits ingroup cohesion in chimpanzees

James Brooks; Ena Onishi; Isabelle R Clark; Manuel Bohn; Shinya Yamamoto

doi:10.1371/journal.pone.0246869

. 2021 Feb 24;16(2):e0246869. doi: 10.1371/journal.pone.0246869

Uniting against a common enemy: Perceived outgroup threat elicits ingroup cohesion in chimpanzees

James Brooks ^1,^2,^*, Ena Onishi ^1,², Isabelle R Clark ³, Manuel Bohn ⁴, Shinya Yamamoto ^1,⁵

Editor: Katie E Slocombe⁶

PMCID: PMC7904213 PMID: 33626062

Abstract

Outgroup threat has been identified as an important driver of ingroup cohesion in humans, but the evolutionary origin of such a relationship is unclear. Chimpanzees (Pan troglodytes) in the wild are notably aggressive towards outgroup members but coordinate complex behaviors with many individuals in group hunting and border patrols. One hypothesis claims that these behaviors evolve alongside one another, where outgroup threat selects for ingroup cohesion and group coordination. To test this hypothesis, 5 groups of chimpanzees (N = 29 individuals) were observed after hearing either pant-hoots of unfamiliar wild chimpanzees or control crow vocalizations both in their typical daily environment and in a context of induced feeding competition. We observed a behavioral pattern that was consistent both with increased stress and vigilance (self-directed behaviors increased, play decreased, rest decreased) and increased ingroup cohesion (interindividual proximity decreased, aggression over food decreased, and play during feeding competition increased). These results support the hypothesis that outgroup threat elicits ingroup tolerance in chimpanzees. This suggests that in chimpanzees, like humans, competition between groups fosters group cohesion.

Introduction

The evolution of intergroup relations is of great importance for theories of both human evolution and animal behavioral ecology. Outgroup threat has long been proposed as a key driver of ingroup cohesion and cooperation and has been emphasized as a potentially significant factor in humans’ great capacity for both cooperation and aggression [1–4], but to date evidence from our closest relatives in controlled experiments is lacking. Competition between groups over resources may incur a high cost during dangerous aggressive encounters but may also result in territorial expansion enhancing group fitness [2, 5]. Outgroup threat, in particular in situations involving limited resources, has therefore been proposed as a context that may simultaneously select for both greater aggression towards outgroup members and greater tolerance towards ingroup members. Under this hypothesis, outgroup threat enhances group cohesion in order to strengthen the group’s competitive ability against intruders [6]. Chimpanzees (Pan troglodytes) are one of humans’ two closest living relatives and engage in both regular intergroup aggression as well as coordinated group-level behaviors such as group hunting [7] and border patrols [8]. Thus, if group level competition has selected for ingroup cohesion and cooperation in humans, proximate cues indicating outgroup threat are predicted to directly stimulate ingroup cohesion in chimpanzees [9].

Some evidence has accumulated that in cooperative breeders with a single breeding pair outgroup conflict solicits ingroup cohesion (e.g. dwarf mongooses (Helogale parvula) [10]; green woodhoopoes (Phoeniculus purpureus) [11, 12]; cichlid fish (Neolamprologus pulcher) [13]), however it is unclear whether this effect generalizes to primates or to species with different social structures. Results from primates on the relation between outgroup competition and ingroup cohesion have so far been mixed. In vervet monkeys (Chlorocebus pygerythrus), individuals participating in intergroup encounters subsequently received more grooming after the encounter ended [14]. In contrast, in capuchin monkeys (Cebus apella) the presence of outgroup visual aggression from adjacent groups increased the frequency of within group aggression, interpreted as a product of higher general social tension [15]. Similarly, simulated intrusion of outgroup individuals led to increased within group aggression in lion-tailed macaques (Macaca silenus) [16] and in the wild Bonnet macaques (Macaca radiata) were more aggressive toward their ingroup following intergroup encounters [17]. These results have been interpreted in part to be caused by increased tension following intergroup encounters, negatively affecting within group social relations [15]. Phylogenetic studies on the relation between outgroup competition and ingroup cohesion have similarly been mixed. One review comparing many primate species, including apes, monkeys, and lemurs, found no effect of intergroup aggression on within group affiliation (measured by absolute grooming frequency and territorial overlap) [18] while another across several Old World monkeys and one New World monkey species found an effect only in females (where affiliation was measured by grooming network density) [19].

Among apes, a recent study found that in mountain gorillas (Gorilla beringei beringei) affiliative interactions among females increased, agonistic interactions among males decreased, and overall time spent resting decreased immediately following intergroup encounters [20]. A previous study found a decrease in fission-fusion dynamics during border patrols and intergroup encounters in wild chimpanzees, potentially indicative of greater ingroup cohesion [21]. Another recent study on the same population found that party size was larger on days and months with territorial activity (direct outgroup encounters or border patrols) and that frequency of ingroup aggression among males was lower on days with territorial activity [6]. The long-term data suggests a directional component where recent territorial activity leads to decreased group modularity and increased party size in the following days while controlling for major ecological factors, however it remains possible that other factors prompted both behaviors and directionality was not assessed for the short-term effects within a given observation day. On the other hand, captive studies have found that during periods of more frequent vocalizations by neighbouring groups chimpanzees display more frequent self-directed behaviour [22] as well as more frequent intragroup agonism and aggression [23, 24]. However, the neighbouring groups included some former groupmates and were in regular visual and auditory contact with one another, making their group affiliation difficult to interpret and raising the possibility that they just demonstrated contagion of arousal and stress from the neighbouring groups, and thus may respond differently to unfamiliar chimpanzee vocalizations.

To date, most direct research on the influence of outgroup threat on ingroup cohesion in primates has come from field and observational studies. Although these studies have revealed important insights into the evolution of intergroup relations, experiments are necessary to complement these studies and directly test the proximate effects of outgroup threat on within group social behavior in controlled conditions. In humans, several experimental studies have emphasized the role of outgroup competition on group coordination in economic games (e.g. [25–27]). Such experiments with non-human primates are lacking and given mixed evidence from observational studies it remains unclear whether this phenomenon is shared with our closest relatives. Using a playback design, a study with wild chimpanzees demonstrated a clear difference in response to vocalizations of familiar compared to unfamiliar individuals but did not measure the effect on social behavior in detail [28]. Another study with captive chimpanzees additionally found a strong increase in vigilance upon hearing outgroup vocalizations compared to crow vocalizations, which was mediated by level of cortisol release, but again did not measure within group social behavior [29]. Such captive experimental designs allow for both highly controlled experimental designs and opportunities for detailed high-resolution behavioural data from several groups and individuals. No studies have measured the direct impact of outgroup cues on ingroup social behavior in a controlled experimental context with great apes, a necessary piece of data to confirm predictions from theory and field experiments about their relation.

Following previous literature validating its effectiveness in chimpanzees, we used a playback design to simulate the presence of outgroup threat [28–30]. Although group relations in captive environments differ from those of wild chimpanzees, experimental studies have proven effective in other species [15, 16] and playbacks have proven to induce vigilance and stress in chimpanzees [29]. Polizzi di Sorrentino et al. [15] argued that simulated intergroup encounters can be analogized to experimental predator presentation, where despite the captive setting individuals are expected to retain innate behavioral tendencies in response to evolutionarily salient stimuli. We compared chimpanzees’ behavior following either outgroup conspecific or control crow vocalizations (following Kutsukake et al. [29]) and then gave semi-monopolizable food to induce feeding competition while recording their behavioral response. If outgroup threat promotes ingroup cohesion, this cohesion may transfer even to times with high within group tension. This would demonstrate the effect is strong enough to withstand additional stress and changes the group’s behaviour in feeding contexts among themselves. To date no direct tests in any species have been conducted on how within group feeding competition is influenced by outgroup threat. We thus designed an experimental protocol to examine the effect of outgroup threat on ingroup social behavior and how it is mediated by feeding competition with captive chimpanzees. We had two alternate hypotheses about the effect of outgroup threat on ingroup social behavior.

Hypothesis one (social cohesion hypothesis)—Intergroup competition has selected for an association between outgroup threat and ingroup cohesion in chimpanzees, and thus outgroup stimuli will be a proximate driver of increased ingroup cohesion despite increased stress, even during within group competition over resources.

Hypothesis two (generalized stress hypothesis)—Intergroup competition has not selected for an association between outgroup threat and ingroup cohesion in chimpanzees, and thus outgroup stimuli will increase stress and social tension, decreasing affiliative behaviors and increasing within group aggression, especially during within group competition over resources.

The social cohesion hypothesis therefore predicted that despite increased stress and vigilance from the presence of outgroup threat, individuals would become more affiliative and less aggressive within the group. More specifically, we predicted that rest would decrease while self-directed behavior would increase, measures for vigilance and stress respectively, that individuals would spend time in closer proximity to one another and that frequency of social grooming and play (as measures of social affiliation and cohesion) would increase, and finally that frequency of aggression would decrease following presentation of outgroup sounds compared to control. The generalized stress hypothesis, by contrast, predicted a general increase in stress and social tension, resulting in a decrease in rest and increase in self-directed behaviors, as in the social cohesion hypothesis, but that inter-individual distance would increase, that grooming and play would decrease, and that aggression would increase in the outgroup compared to control condition. We predicted that these effects would become stronger in a context of tension induced by feeding competition. The social cohesion hypothesis therefore predicted tension would be released through play rather than aggression following playback of outgroup vocalizations, while the generalized stress hypothesis predicted that tension would be released through aggression rather than play. Due to the likelihood of some habituation, we additionally predicted that for some of the effects found there would be an interaction between trial and condition, where the difference between control and outgroup conditions would become smaller across trials.

Materials and methods

Ethical note

This research was approved by the ethical committee at Wildlife Research Center, Kyoto University (approval number WRC-2019-KS004A). We carefully considered the ethics of this experiment considering it involved increased stress to the chimpanzees. We emphasize that we investigated behaviours found in natural contexts. These natural stressors are impossible to study without some stress. Still, we note both that we observed increased social cohesion among the chimpanzees and that there were no differences in rates of self-directed behaviour in the food phase between conditions, indicating the induced stress was short lived (see results and discussion for more details). The outgroup playback calls thus likely do not represent a major concern to their welfare.

Subjects

Subjects were 29 socially-housed adult captive chimpanzees (17 males and 12 females) in five social groups at Kumamoto Sanctuary of Kyoto University, Japan [31]. Chimpanzees were given various environmental enrichment several times per week in addition to daily meals in the morning and evening with additional food spread across their enclosures. All chimpanzees were socially housed with outdoor access and ad libitum access to water and regular health checks. No animals were food or water deprived at any time and no changes were made to their daily schedules beyond playback of sounds and presentation of feeding enrichment. Animal husbandry and research complied with the international standards in accordance with the recommendation of the Weatherall report “The use of non-human primates in research” and all local guidelines. No changes were made to their housing and caretaking following the conclusion of the experiment.

Fifteen males were housed in a simulated fission-fusion grouping structure in three side-by-side enclosures (measuring 128m², 108.8 m², and 108.8 m²) with visual access to one another and doors connecting them which can be opened or closed. During all data collection for this experiment doors were closed, forming three social groups of five males each. Group composition was the same on all experimental days in their most common grouping arrangement. The remaining two groups each consisted of one male and either four or eight females (in enclosures measuring 269.5m² and 150.1m²), which were kept constant throughout the experiment except for one female who was occasionally housed with another group not involved in this experiment. The majority of the chimpanzees were of the Western chimpanzee subspecies (Pan troglodytes verus), though one male in a single male multi female group was an Eastern (Pan troglodytes schweinfurthii) and Western chimpanzee hybrid, and another female in the same group was a Nigeria-Cameroon chimpanzee (Pan troglodytes ellioti).

Data collection

Data was recorded and live coded by one observer per group. Each group was observed by the same observer across trials. Observers recorded both scan data on individual behavior and interindividual proximity at two-minute intervals as well as all occurrence data on frequency of aggression and play. Behavioral categories recorded during scans included rest (with posture-either lying down or sitting), social grooming (including giving, receiving, or mutual grooming), self-directed behavior (including both self-grooming and self-scratching), eating, and moving. Proximity at each scan was recorded for each dyad into one of four ordered distance categories including in contact, within arm’s reach, <3 meters, and >3 meters (as estimated by the observer) and coded as ordinal data with four levels. The time and individuals involved were recorded for all occurrences of play, aggression (including display, chase, and hit), and copulation. Observers additionally attempted to record instances of vocalizations, but it proved to be too difficult to reliably record all vocalizations and thus was not used in analysis.

Experimental procedure

Four days of experiments were conducted for each group except for one group for which there were only three days of experiments. Experimental days were separated by at least 3-day intervals to reduce the effect of habituation. Two experimental sessions per day were conducted, once in the morning and once in the afternoon, once with outgroup vocalizations (outgroup condition) and once with crow vocalizations (control condition). The order of which condition was in the morning used an ABBA design across trials, with the order counterbalanced between the all male groups and the single-male multi-female groups. The three all male groups were recorded simultaneously and the two single-male multi-female groups were recorded simultaneously due to being within auditory contact of one another. During each session, observers collected data for 30 minutes before any sounds were played to ensure no abnormal events occurred immediately before the experiments. Data was then collected in the playback phase for approximately 30 minutes while stimuli were played. Caretakers were not always able to deliver the food at precisely 30 minutes after the first sounds played, so the actual time of food delivery was within a range of 28–40 minutes after the first sounds. Analysis was restricted to the minimum duration of time between the first sound and food delivery across sessions. Caretakers then provided two bunches of semi-monopolizable feeding enrichment which is regularly given to the apes and data was recorded for another 30 minutes in the “food” phase. Bundles consisted of carton tubes loosely tied together containing primate chow which can be easily extracted and consumed but cannot be eaten all at once. Tubes could easily be removed from bundles, but each bundle could be held easily by a single individual. Each group received two equally sized bundles at the same time at the start of each food phase, in total including one more tube than the number of individuals in the group. Therefore, the three male groups and the single-male multi-female group of five individuals each received two bundles of three tubes each, and the single-male multi-female group of nine individuals received two bundles of five tubes each.

Stimuli

Experimental stimuli consisted of pant-hoots of single adult males unfamiliar to any chimpanzees involved in the experiment including some from both wild settings and other captive facilities. Control stimuli consisted of crow “ka” vocalizations. Twelve different high quality recordings of different individuals for each condition were used in the experiment and each was cut or repeated to create a 15 second stimulus for each recording then normalized to consistent volume. Sounds were played at peak pressure level of 95 dB at 10 meters, consistent with the maximum pressure recorded of pant-hoots by Kutsukake et al. [29]. In any given session of experiments, 4 unique recordings were played in order to increase the salience of the stimuli, again following Kutsukake et al. [29]. Recordings were separated by 1 minute of silence, and all 4 were repeated in the same order with the same intervals 15 minutes after the first recording to keep the stimuli salient for the whole observation period. For each of the first three experimental days all recordings played were completely novel, while the recordings on the fourth day were randomly chosen from those used in the first three. Example recordings can be found in S1 File.

Analysis

All analysis was done using R version 3.5.3 in RStudio [32]. All models reported below were structured in similar ways: As fixed effects, they included condition (outgroup vs. control), trial (1–4, normalized to a mean of 0 and standard deviation of 1), and their interaction. As random effects, they included random slopes of the fixed effects as well as time since start of the phase (for scan behaviors and proximity, normalized) and time of day (morning or afternoon) within individual (nested within group). The proximity data had the same random slopes within dyad, individual 1, and individual 2, where individual 1 and individual 2 were randomly assigned to include both individuals in the dyad. In all models where possible the bobyqa optimizer [33] was used. In the case of non-convergence, we removed random effects in the following way: first, the random slopes for time of day then time since start of phase, then the nesting of individuals within group, then the random slope of the interaction between condition and trial, then the random slope of trial, then the random slope of condition. This sequence was chosen in order to retain the fixed effects whenever possible prioritizing the effect of condition as this was the main hypothesis to be tested in this study, and time since start of phase included more detail and is expected to have had a higher impact than time of day. The same structured simplification was carried out with singular models and the results below present convergent non-singular models, while the maximal singular models are available in S1 File. For the analyses below, we give the formula of the final converging non-singular model. We additionally checked model stability and collinearity of final models; details can be found in S1 File.

Significance was calculated using chi-squared likelihood ratio test with the drop1 function [34] which uses full—null model comparison for hypothesis testing and an alpha value of 0.05. If the interaction between condition and trial was not significant the model was run again with the interaction term removed. This procedure was followed for all variables of interest in separate models for both the playback and food phases. We additionally calculated odds ratio (OR) estimates and 95% confidence intervals for all significant effects. For interactions, the odds ratio represents the odds of a one unit increase when both variables are present over and above the main effects. For example, if there is an interaction between trial and condition the interaction term represents how much the response changes with every trial in the outgroup condition over and above the change that is due to trial and condition alone.

Proximity

Proximity data was modeled with a cumulative link mixed model (CLMM) via the function clmm from the ordinal package [35]. The proximity data was input as an ordinal measure of 1 (contact), 2 (arm’s reach), 3 (<3m) or 4 (>3m) for each dyad and the CLMM was run on the full data. The final model formula for the playback phase was: proximity ~ trial * condition + (condition*trial|dyad) + (condition*trial|id1) + (condition*trial|id2); and for the food phase was: proximity ~ trial * condition + (condition*trial|group/dyad) + (condition*trial|group/id1) + (condition*trial|group/id2).

Behavior scans

For self-directed behavior, social grooming, and rest, we used generalized linear mixed models (GLMM) with a logit link function, implemented using the function glmer from the package lme4 [34]. The models used the full raw data, where for each individual at each scan, their behaviour was coded as either 0 (not engaged in the behaviour) or 1 (engaged in the behaviour). Another GLMM was run on data restricted to rest data with a 1/0 dependent variable for sitting (1) or lying down (0). For all scan behavior models in both phases the final model formula was: behavior ~ trial * condition + (condition*trial|individual) with the exception of self-directed behaviors in the food phase for which the final model formula was: behavior ~ trial * condition + (condition+trial|individual).

All occurrence behavior

To model the play and aggression data, we also used GLMMs. For each individual, a 1/0 score was given for whether that individual displayed the behavior in question in the observation period. Thus, rather than absolute frequency, the model used the likelihood of individuals displaying the behavior in the whole time window. This was done to ensure one individual playing for several bouts, or aggressing several individuals, was not overrepresented in the data and because it can be difficult to reliably identify when one bout ends and another begins. This resulted in one data point for each individual per phase per condition per trial. Analyses were run on aggression as a whole rather than for each type of aggression due to the relatively small datasets given by separating each type. For all play and aggression models in both phases the final model formula was behavior ~ trial * condition + (1|individual).

Results

Proximity

In the playback phase the proportional odds of a dyad being observed in more distant categories was lower in the outgroup condition than the control condition across trials, indicating chimpanzees were significantly closer together (β = -0.65, SE = 0.20, χ² = 10.81, p = 0.0010; OR = 0.52 (95% CI: 0.36, 0.77); Fig 1). There was no change in proximity in the food phase by condition (χ² = 0.46, p = 0.50).

Fig 1 — Proportion of observations in each proximity category in the outgroup and control conditions. Each dot represents a dyad, blue circles represent the mean for the control condition, and red X’s represent the mean for the outgroup condition. Red and blue bars represent 95% confidence intervals around the mean (based on a non-parametric bootstrap of the data).

Behavior scans

Across trials, individuals spent significantly more time engaged in self-directed behaviors in the outgroup compared to control condition in the playback phase (β = 1.17, SE = 0.44, χ² = 4.84, p = 0.028; OR = 3.21 (95% CI: 1.15, 9.89); Fig 2), but not the food phase (χ² = 0.11, p = 0.74). There was a significant interaction between condition and trial in social grooming in the playback phase (β = -1.44, SE = 0.43, χ² = 9.71, p = 0.0018; OR = 0.24 (95% CI: 0.10, 0.55); Fig 2), where in the first trial individuals engaged in more social grooming in the outgroup condition than control condition but this effect decreased across trials. There was no effect of condition on social grooming in the food phase (χ² = 0.43, p = 0.51). There was additionally a significant interaction between condition and trial in time spent resting in both the playback (β = 0.52, SE = 0.15, χ² = 9.99, p = 0.0016; OR = 1.69 (95% CI: 1.25, 2.36); Fig 2) and food (β = -0.36, SE = 0.11, χ² = 8.22, p = 0.0041; OR = 0.70 (95% CI: 0.55, 0.88); Fig 2) phases. In the playback phase, individuals spent less time resting in the first trials in the outgroup than control condition. In the food phase, this pattern was reversed, and individuals spent more time resting in the first trials of the outgroup than control condition. Within rest, in the playback phase there was a significant interaction between condition and trial on posture (β = -0.32, SE = 0.14, χ² = 4.42, p = 0.036; OR = 0.73 (95% CI: 0.54, 0.98); Fig 2) where individuals in the first trials spent less time lying down in the outgroup compared to control condition but the effect decreased across trials. In the food phase, there was a significant main effect of condition where individuals spent less time lying down in the control condition (β = -0.69, SE = 0.21, χ² = 9.61, p = 0.0019; OR = 0.50 (95% CI: 0.32, 0.76); Fig 2). Although the sample size was too small to directly investigate the effects of group dynamics (such as sex composition), there was considerable variation between groups. A table of results by group can be found in S1 File.

Fig 2 — Social grooming in the playback phase, rest in the playback and food phases, and sitting upright in the playback phase had significant interactions between condition and trial, with the main effect of condition visualized here (graphs depicting trial interactions can be found in S1 File). Each dot represents an individual, blue circles represent the mean for the control condition, and red X’s represent the mean for the outgroup condition. Red and blue bars represent 95% confidence intervals around the mean (based on a non-parametric bootstrap of the data).

All occurrence behaviors

In the playback phase individuals played significantly less in the outgroup condition than the control condition (β = -0.89, SE = 0.44, χ² = 4.37, p = 0.037; OR = 0.41 (95% CI: 0.16, 0.95); Fig 2). In the food phase, individuals played significantly more in the outgroup condition than the control condition (β = 1.15, SE = 0.49, χ² = 6.16, p = 0.013; OR = 3.17 (95% CI: 1.27, 8.72); Fig 2). There was no effect of condition on rate of aggression in the playback phase (χ² = 1.41, p = 0.24), but the rate of aggression was significantly lower in the outgroup compared to control condition in the food phase (β = -1.31, SE = 0.51, χ² = 7.47, p = 0.0063; OR = 0.27 (95% CI: 0.09, 0.70); Fig 2). Copulations were rare and statistics could not be calculated.

Discussion

We observed chimpanzees’ behavioral response to outgroup pant-hoots compared to crow vocalizations. Overall, our results were consistent with the social cohesion hypothesis but not with the generalized stress hypothesis. Indicators of stress and vigilance were higher after hearing vocalizations from unfamiliar chimpanzees compared to crow vocalizations but this did not translate into within group tension. Instead, indicators of affiliation and tolerance were higher in the outgroup vocalization condition compared to control crow vocalization condition. Upon receiving semi-monopolizable food, play was higher and aggression lower in the outgroup compared to control condition, indicating a shift towards prosocial strategies in releasing tension induced by feeding competition. These results suggest that outgroup threat directly induces ingroup cohesion in chimpanzees, and importantly, that this effect translates to feeding contexts with high within group tension.

Consistent with previous studies [28, 29], we found behavioral indicators of vigilance and stress increased. More specifically, in the playback phase there were more self-directed behaviors (self-grooming and self-scratching), less rest, and a lower proportion of lying down in the outgroup vocalization condition compared to control crow vocalization condition. For the latter two this effect decreased for later presentations of the vocalizations, presumably due to habituation to the stimuli (see S1 File). The increase in self-directed behaviors, often interpreted as signals of stress [22, 36], is likely due to chimpanzees finding outgroup sounds more stressful than crow vocalizations, consistent with a previous study documenting a rise in cortisol following outgroup auditory stimuli in many of the same individuals as those involved in this study [29]. The decrease in rest, through its interaction with trial, is consistent with field research on gorillas where rest decreased following intergroup encounters [20], but in this case may simply have been due to a trade-off with the relative increase in other behaviors including self-directed behavior and social grooming. The decrease in proportion of rest lying down (as an interaction with trial) may further be interpreted as a sign of vigilance, where chimpanzees remained alert even while not engaged in other behaviors. In the playback phase, contrary to the social cohesion hypothesis, there was a decrease in play in the outgroup compared to the control crow vocalization condition. One explanation is that this was also indicative of increased vigilance or stress. Taken together, the results of several behavioral measures converge on the result that chimpanzees were more stressed and vigilant when outgroup vocalizations were played, compared to crow vocalizations.

Despite the increase in behavioral indicators of stress and vigilance, this stress was not translated into aggression within the group. Much previous research has linked stress levels to aggression through the response of the hypothalamic, pituitary, adrenal (HPA) axis [37–41]. In our study, however, chimpanzees instead engaged in more affiliative behaviors following the outgroup stimuli compared to the control stimuli. More specifically, individuals moved closer together, indicating that they were spatially more cohesive and tolerant of one another. Further, there was an interaction between condition and trial on social grooming. Chimpanzees engaged in more social grooming in the early trials in the outgroup than control crow vocalization condition, though the difference between conditions decreased across trials, likely due to habituation to the stimuli (see S1 File). These social behaviors indicate that chimpanzees’ tolerance, cohesion, and affiliative behavior increased as a result of hearing outgroup vocalizations.

When chimpanzees were given bundles of semi-monopolizable food following the playback of either outgroup or control sounds, there were substantial differences between conditions. Most notably, there was almost no aggression over food observed following the outgroup sounds, whereas there was significantly more aggression over food in the control condition with crow sounds. Further, chimpanzees were more likely to engage in play with one another upon receiving the food after hearing the outgroup vocalizations than crow vocalizations. These results may suggest a change in strategy used to relieve tension. In the control condition, tension led to aggression and competition over food, whereas in the outgroup condition aggression was inhibited and this tension was instead redirected towards play. Captive bonobos (Pan paniscus) use play to reduce tension during competition [42] and chimpanzees in this experiment likely used a similar strategy. There was no difference in self-directed behavior, social grooming, or inter-individual distance between conditions in the food phase, and only an interaction between trial and condition in amount of rest. This may be due to the tension release which returned behavior to baseline, though could alternatively be due to rapid habituation to silence or to floor effects due to greater time spent eating and relative reduction in other behaviors. Both total rest and proportion of rest sitting upright were opposite to the effects observed in the playback phase, which may be interpreted as higher feeding competition-induced tension in the control condition, increasing vigilance to the ingroup, while in the outgroup condition there was less tension over food resources and individuals rested and laid down more. The effect of condition on behavior during feeding competition was consistent with the social cohesion hypothesis that outgroup threat promotes within group tolerance, indicating that the prosocial effects of outgroup threat directly transfer to situations of resource competition within the group in chimpanzees.

Although we did not playback ingroup pant hoots (due to constant visual contact between all groupmates, as we did not isolate individuals from their group), we consider it unlikely that the measured results were a product of pant-hoots in general for several reasons. First, previous research have found that familiar pant-hoots (from neighbouring groups with regular visual and auditory contact with one another, including former groupmates) is instead associated with higher rates of ingroup aggression in chimpanzees [24]. This opposite result strongly suggests that pant hoots in general do not cause greater ingroup tolerance and cohesion. Second, all individuals in this study heard pant hoots from familiar individuals in every trial both control and experimental throughout the experiment. It is therefore likely that the identity of the callers, rather than the presence of pant-hoots per se, was the most important difference between conditions. Finally, several measures interacted with trial, indicating that the salience of the vocalizations decreased. This result would not be expected if pant-hoots in general, as opposed to vocalizations of unfamiliar individuals, caused the main effects reported here as all individuals have regularly heard pant-hoots throughout their lives and habituation over the four days of the experiment therefore seems doubtful. For these reasons this study implicates perceived outgroup threat as a driver of ingroup cohesion in chimpanzees as has been demonstrated in humans, though future work testing the effect of familiarity and group membership will be important to better understand how chimpanzees perceive and respond to other groups.

While the results of this study are promising, there were some important limitations. First, we were not able to directly compare the effect between males and females due to sample size and the lack of any group with both multiple females and multiple males. Field studies with gorillas and chimpanzees have suggested a possible sex difference in response towards outgroup competition [6, 20], but these possible differences could not be studied here. In wild chimpanzees, coalitions of males are most typically the initiators and participants of intergroup encounters [8], so differences might be expected between groups of differing sex composition. In our sample there was considerable variation between groups (see S1 File). It should be noted that in many measures both the all male and single male multi female groups changed in the same direction but unfortunately we do not have sufficient data to test which grouping factors predicted the direction and size of the effect between groups, nor test the effect of condition on individual groups. Still, these are promising future directions for better understanding the impact of outgroup threat on within group social behavior. The significant variation in response suggests behavioral plasticity and the presence of important but variable social dynamics that strongly alter intergroup response. One social group included a female who was not present during all trials and the all male groups are housed in a simulated fission-fusion environment and had constant visual access to one another. Additionally, some caution should be taken about the generalizability of these findings due to the absence of true outgroup threat in daily lives of these captive chimpanzees and the difference between captive and wild feeding competition. Captive experiments on animals’ response to outgroup cues have been defended as analogous to experiments on predator responses, where the response to evolutionarily salient stimuli produces similar behavioural effects even in the absence of direct experience [15], but it is worthwhile to note that these chimpanzees have not experienced any true intergroup competition in their adult lives (though roughly half were born in the wild where they may have had some experience of intergroup behaviors as infants). Finally, the form of the stimuli, while allowing for controlled, direct tests, were not fully naturalistic as individual pant hoots spaced at 1 minute intervals is not a typical pattern in the wild [43]. We could not directly test whether behaviour following the first pant hoot and fourth in a given day was different, but chimpanzees in the wild are able to differentiate number of outgroup callers [30]. Testing this effect with varying levels of simulated outgroup threat would therefore be a fascinating future direction. Similarly, the form of feeding competition, where caretakers instantaneously gave bundles of food to groups of chimpanzees, is not the same as the kind of competition that wild chimpanzees would experience, but nonetheless creates a situation with elevated within group feeding competition. Despite these limitations, the results from several different behavioral measures converged on a clear effect of outgroup threat on ingroup cohesion.

The results of this study demonstrate that outgroup threat contributed to ingroup cohesion both in standard grouping dynamics and in a context of feeding competition, but there remain several important unanswered questions for future research. Most notably, future studies should investigate what contributes to the intergroup variation that was observed. As noted, comparisons between groups with differing sex ratios, as well as with differing baseline cohesion, will be essential. It will also be interesting to compare types of food given during the induced feeding competition, especially whether the effects differ between high-value, monopolizable food and low-value, non-monopolizable food. Species level comparisons, especially with bonobos, may additionally reveal the extent to which intergroup competition influences within group tolerance [9]. Bonobos are equally closely related to humans as chimpanzees, and while they do sometimes have aggressive intergroup encounters, unlike chimpanzees they do not engage in lethal intergroup aggression in the wild [44, 45] and in fact prefer to share food with strangers in captive experiments [46, 47]. Bonobos have been characterized as more tolerant, including both higher performance on dyadic cooperation tasks in captivity [48] as well as lower intensity aggression in the wild [49], but interestingly do not frequently engage in group-level cooperation such as group hunting and border patrols as do chimpanzees [44]. The same experiment with captive bonobos may reveal species level differences in reaction to outgroup stimuli, which would test the hypothesis that chimpanzees’ behavior in this paradigm, and the association between human cooperation and competition in experimental contexts, is an evolutionary response to strong intergroup competition. It is also worth noting that the majority of chimpanzees in this study, as the majority of captive chimpanzees generally, are of the Western chimpanzee subspecies. In this subspecies females frequently engage in intergroup encounters, unlike in Eastern chimpanzees (Pan trogolodytes) [21], though they display reduced intensity of intergroup encounters overall [50]. Comparisons on the species and subspecies level therefore may prove insightful.

Hormonal mechanisms may further provide a promising future direction. A previous experiment in captive chimpanzees has demonstrated salivary cortisol increases following playback of outgroup vocalizations and correlates with vigilance in response to the stimuli [29], while some human research has found an association between cortisol reactivity and prosocial decision making [51], and thus cortisol release may be a proximate mechanism by which ingroup cohesion is enhanced. Further, oxytocin, a neuropeptide and hormone conserved across mammals, has been strongly implicated in both intergroup behavior and ingroup affiliation in several species [21, 52–58], and may be an important component of the neural and endocrine systems targeted by selection on intergroup behavior [54]. Interestingly, an increase in both cortisol and oxytocin are associated with border patrols in wild chimpanzees, though their release is independent of one another [21, 59]. Future research should measure both baseline oxytocin and cortisol in chimpanzees and bonobos to be compared to one another and to their response in playback experiments. Oxytocin administration in both species, which recently was shown to affect social behaviour differently in bonobos and chimpanzees [60], may further prove to be a promising experimental approach to directly test the hormone’s possible role in the evolution of intergroup behaviors. Interindividual, intergroup, and interspecies comparisons of reactions to outgroup stimuli, baseline social behavior, and the underlying hormonal mechanisms may reveal the evolutionary history and mechanisms by which intergroup aggression and ingroup cooperation have evolved in humans.

In sum, we found across several measures, both in the presence and absence of feeding competition, that perceived outgroup threat directly enhances ingroup cohesion and tolerance in captive chimpanzees. This demonstrates that humans’ greater group cohesion in competitive contexts is shared with chimpanzees, and suggests that intergroup competition in human evolution may have selected for our ability to maintain cooperation and tolerant relations in large groups in the presence of a common enemy. Several questions remain about the precise evolutionary drivers of this behavioral association and the factors which elicit it, but the results of the current study present strong evidence in a controlled experimental context that it is shared with chimpanzees, and that a comparative approach with great apes may prove a promising direction of study in understanding the evolutionary forces that led to humans’ great capacity for group driven behaviors both positive and negative.

Supporting information

S1 File. This file contains all supporting information for this manuscript including: Visualizations of effects by trial, table of result by group, stability and collinearity models results, singular model results, all code used in analyses and figure creation (as well as saved models for proximity), all data, both figures, and two examples each of control and outgroup stimuli used in this experiment.

(ZIP)

Click here for additional data file.^{(56.4MB, zip)}

Acknowledgments

We thank Etsuko Nogami and Yusuke Mori, and the other care staff at Kumamoto Sanctuary for their support during and in preparation for the experiments and for their work caring for the chimpanzees. We also thank Drs. Satoshi Hirata, Naruki Morimura, and Fumihiro Kano for their support in this study. We also thank all the chimpanzees at Kumamoto Sanctuary.

Data Availability

All relevant data are within the paper and its Supporting Information files.

Funding Statement

This research was financially supported by the Leading Graduate Program in Primatology and Wildlife Science of Kyoto University, Grant-in-Aid for Scientific Research (JSPS KAKENHI 17H05862 and 19H00629 and MEXT KAKENHI 19H05736 to SY). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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PLoS One. doi: 10.1371/journal.pone.0246869.r001

Decision Letter 0

Katie E Slocombe

26 Nov 2020

PONE-D-20-33650

Uniting against a common enemy: perceived outgroup threat elicits ingroup cohesion in chimpanzees

PLOS ONE

Dear Dr. Brooks,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Both reviewers have provided thoughtful and detailed comments on the manuscript. I would like to see you respond to each point they raised, but in particular I think the following points are particularly important to attend to: (i) Clarity of the hypotheses - I agree with R2 that the justification for thinking that feeding competition drives the relationship between outgroup confilict and ingroup cohesion is poor and needs changing or better justifying (ii) Methods - much more clarity on how the data collected resulted in the measures entered into statistical models is required - I could not currently replicate your study with the information you have provided, and as R2 points out its hard to assess the statistical models without clarity as to how the measures that enter them were constructed (iii) inter-group differences - I agree with R1 that you would expect differences in groups of different male composition, so this should be explored in the results (iv) Immediate response to 1st playback - please can you explore in the data if there is a difference in terms of the quality of response to the first playback (where numerical odds are in favour of the multimale groups) vs once they have heard all 4 playbacks, or if your sampling methods do not allow this kind of examination, you could suggest this as an avenue for future research.

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Reviewer #1: This paper presents the results of an experiment to test whether hearing the calls of four unfamiliar conspecifics would group-living chimpanzees to increase behaviors associated with ingroup cohesion and group coordination, or to experience generalized stress.

In its favour, the goal of understanding whether competition between groups tends to increase group cohesion is valuable because this relationship is not well studied; the authors’ introductory review made this point effectively. The experiment had an explicit and well-controlled design that was replicated with 5 groups. Results were analysed with careful statistical models, and were useful in clearly being more consistent with the social cohesion hypothesis. The Discussion was generally appropriate.

Against the paper, two important problems need attention.

First, no effect sizes are provided. Fig. 1 suggests that (although P-values were often low) the differences in magnitude were sometimes relatively small. The authors need to provide some indication of how big the effects were.

Second, I saw no indication that analyses took account of possible differences between groups. This is an important issue because different dynamics are expected between single-male, multi-female groups and all-male groups, given that male coalitions are the active force in intergroup interactions among chimpanzees.

Furthermore, given that the effect sizes appear to be rather small, it is important to report how results varied among groups.

Evaluation.

This study is well designed and presented, but it needs some changes before its significance is fully clear.

Additional comments

Introduction. Most captive chimpanzees are a different subspecies (P.t. verus)from many of the wild chimpanzees for which studies were reported. Since Wilson et al. (2012) found less evidence of intense intergroup aggression in verus, the difference should be mentioned.

L216-226 “Experimental stimuli consisted of pant-hoots of single adult males… In any given session of experiments, 4 unique recordings were played… separated by 1 minute of silence, and all 4 were repeated in the same order with the same intervals 15 minutes after the first recording…”

So in the playback condition, each group heard the calls of 4 different adult males, played back in the same order (with each call separated by 60 seconds of silence). (1) Since this is very artificial, given that free-living chimpanzees tend to produce calls that overlap with each other, the Discussion should briefly acknowledge that the target chimpanzees might have regarded the arrangement as odd. (2) One might expect that the behaviour of the target chimpanzees would change during the playback. After the first call was played, the perception could be that there was an opportunity (for the all-male groups) to conduct an attack. As the number of calls played rose to four, the perceived balance of power would shift in the favour of the playback males. During the first few minutes of the experiment, therefore, one might expect that at least for the all-male groups, the degree of stress would increase. For this reason, I would encourage an analysis that compared responses to the first call with subsequent responses. This is not necessary for the paper to be published, and it may not be possible to do this analysis if there is too little behavioural data in the first minute, but I would at least like to see some acknowledgment of the fact that a single call has a different salience from a collection of calls.

L442 “contributed” (use past tense)

L453 But bonobos do have aggressive intergroup interactions, which should be acknowledged.

L459 Note that these were captive chimpanzees.

Reviewer #2: Review for PONE-D-20-33650

General Comments

This paper experimentally examines the relationship outgroup threat and ingroup cohesion in groups of captive chimpanzees and tests between a social cohesion hypothesis and the alternate generalized stress hypothesis. In the experimental condition, the authors played stranger pant hoots to the chimpanzees and recorded measures of stress, vigilance, affiliation and aggression and compared these behavioral responses to a control condition of playing a crow vocalization. They further examined the behavioral responses to these two conditions after the playback period when the chimpanzees were stressed with a monopolizable food source. The authors found that the chimpanzees increased stress and affiliation in the outgroup condition even during the increased stress of feeding competition providing support for the idea that outgroup threats increase social cohesion. I think this was an interesting experimental paradigm that yielded interesting and compelling results. I have some general comments that I think need to be addressed in a revision followed by some line-by-line comments.

While I think this question is compelling, I found that the authors framed this paper in a confusing way. To me, the social cohesion hypothesis is that chimpanzees when faced with an outgroup threat show increases in within group social cohesion because individuals need to cooperate to defend their territory from this threat. Instead, the authors state the social cohesion hypothesis is that intragroup feeding competition somehow selects for the relationship between outgroup and ingroup competition and cooperation. This sounds a little like an argument from socioecology that if within group feeding competition is too high, then individuals cannot come together to succeed in between group feeding contests. But I don’t think that is the appropriate argument to make here because that has to do with the ability of individuals to even be in a group. Furthermore, I don’t think that the authors are actually testing whether feeding competition selects for the relationship between outgroup threats and ingroup cohesion. Rather I think what is being tested is whether outgroup threat has selected for the relationship between within group affiliation and aggression. This is the comparison between control and the experimental condition in the playback phase. The addition of the feeding competition phase after the playback phase is an additional stressor imposed on the system. I would like to see more explanation in the introduction about why outgroup threats increase group cohesion and think the hypotheses need to be explained better. It would also be helpful to have a better explanation of the predictions in the introduction.

Second, it was a little hard to evaluate the statistical models or really understand the results because there isn’t enough explanation for the metrics that were calculated from the behavioral data. It seems like all of the metrics are some measure of proportion of the scans, but that should be stated explicitly since it might be more appropriate to use the count data with the total number of scans as an offset in these models rather than proportion data. I was also not entirely convinced that there wasn’t a more appropriate way to calculate aggression and play data. This is outlined in more detail below.

Line-by-line comments

Lines 46-50: this seems a bit repetitive with the previous sentences in the introduction.

Lines 56-97: I thought this paragraph could do with some restructuring. First, I think it’s hard to keep track of all of the studies, and maybe it would help to just simplify this without as much detail. I would also have the chimpanzee background be a separate paragraph.

Lines 99-103: While I agree that this question is best investigated experimentally, I am not convinced from these lines that the studies have to be done in captivity, so it’s worth expanding on why that is the case.

Lines 125-130: this is where the idea of the monopolizable food first comes up and it seemed out of place. By introducing it here, it doesn’t seem to have much to do with the stuff in the introduction before this and only starts to fit when you get to the hypotheses. I think the hypotheses should probably be introduced earlier and explained in more detail. But see above about reframing the argument.

Lines 134-142: See above but I disagree that the ingroup feeding competition selects for the relationship between ingroup cohesion and outgroup threat.

Lines 143-157: I think it would be helpful to frame these predictions as stress, vigilance, affiliation and aggression. That way, the authors can specifically describe that self-directed aggression is a proxy for stress, rest is a proxy for vigilance, etc.

Line 146: I think self-directed behavior should decrease.

Lines 164-173: For the 15 males in three groups, how was the composition of these groups determined and were they the same for each trial? Or could the 15 individuals be in different groups from one trial to the other?

Lines 181-183: Are these proximity measures nested? So if individuals are in contact with one another, are they also within 3 meters of one another?

Line 230: Somewhere before you get to the analysis or at the beginning of the analysis section, it would be helpful to know how the data that was collected were turned into metrics that are used in the analysis.

Line 258-262: This is an example of where it would be helpful to know how the data were turned into the metric used here. It’s not totally clear to me whether individual metrics were calculated for each of the four proximity categories.

Lines 273-279: Not clear what the metric is here. Was it some kind of proportion of individuals who exhibited any aggression within the analysis period. I feel like there are a number of ways to calculate aggression including thinking about rates of different kinds of aggression. Displays are quite different than chases and hits which are directed?

Lines 336-338: I’m not sure that this is the place for this but as I was reading this sentence, I thought that a future study or something that could have been done here is to do a control with a non-monopolizable food. That would control for the fact that there might be some excitement or at least an effect of the presence of food.

Lines 356-361: I think it would be helpful in the introduction to explain why play is being used as a measure of social cohesion. It is an affiliative behavior but it’s not one that is often used in metrics of social bonding as is the case for grooming.

Line 441: Also important to note that captive chimps are not facing the same kind of feeding competition and even this kind of simulated feeding competition is not the same.

Line 441: Another factor to consider when thinking about the differences between the groups is the strength of the social bonds within the groups. Some individuals within the groups may have stronger bonds and that might impact certain metrics like grooming, and play.

Figure 2: I think it would be helpful in the text and in this figure to arrange these metrics by categories: stress, vigilance, affiliation and aggression.

**********

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PLoS One. 2021 Feb 24;16(2):e0246869. doi: 10.1371/journal.pone.0246869.r002

Author response to Decision Letter 0

11 Dec 2020

Dear Professor Slocombe,

Thank you for the opportunity to revise our manuscript. We greatly appreciate the comments made by yourself and both reviewers, all of which were valid and extremely useful in revising our manuscript. Below, we have pasted the reviewers’ responses and detailed our responses.

Sincerely,

James Brooks, Ena Onishi, Isabelle R. Clark, Manuel Bohn, and Shinya Yamamoto

Against the paper, two important problems need attention.

Furthermore, given that the effect sizes appear to be rather small, it is important to report how results varied among groups.

Thank you for your fair and valuable evaluation of our manuscript. We have considerably revised the paper to account for yours and the other reviewer’s comments and have addressed each point as below.

Regarding your first major point in need of greater attention, unfortunately there are no standard and agreed upon methods to calculate effect sizes for GLMMs. Still, we recognize the importance of inputting values to allow comparisons of the effect size between studies, and have therefore added odds ratio estimates for each model with significant effects.

Regarding your second major point, we unfortunately do not have the data to fully explore this possibility fairly. While we strongly agree that differences might be expected and this will be an extremely important direction of future study, at this time we are unable to statistically answer with confidence whether such a difference exists. Still, we have expanded considerably on this point in the discussion, both in the limitations (lines 451-461) and future directions (lines 492-493) paragraphs. We additionally add the point that the response did indeed vary quite a bit between groups, there was not an obvious difference in direction between the all male and single male multi female groups, but that this variation will be a worthwhile point of future study (line 458).

Evaluation.

This study is well designed and presented, but it needs some changes before its significance is fully clear.

Additional comments

Thank you for pointing this out, we have made note of this in the methods (lines 188-192) as well as the discussion (lines 508-513), added that in this subspecies females are more likely to participate in intergroup encounters, suggesting subspecies comparisons in addition to species comparisons as a future direction.

This is an important point we have now added to the manuscript in lines 476-480. We now explicitly mention that the vocalizations’ presentation style is not fully naturalistic, but do provide a test of the hypotheses nonetheless. We also have added your idea as a future direction (lines 480-482) while noting that in this study we do not have enough data to compare changes across the playback phase, this is a fascinating future project. We hope new experiments will be able to examine how the effect observed here relates to assessment of numerical strength of outgroup parties. This is a promising and interesting direction we hope to examine in the future.

L442 “contributed” (use past tense)

Changed, thank you for your attention to detail.

L453 But bonobos do have aggressive intergroup interactions, which should be acknowledged.

We have added this point, thank you for pointing out the need for this clarification (line 501-504).

L459 Note that these were captive chimpanzees.

Added.

Thank you again for your very helpful review of our paper and noting the areas we can improve. We appreciate your advice and thanks to your comments believe our paper is much improved.

Reviewer #2: Review for PONE-D-20-33650

General Comments

Thank you for your review of our manuscript. We fully agree with you on all points, and recognize our manuscript made our main hypothesis unnecessarily confusing in the introduction. As you note, our experiment was aimed to test whether intergroup competition has selected for the relation between ingroup cohesion and perceived outgroup threat. Our food phase was included, as you highlight, to test whether this effect transfers to a time with high ingroup tension where within group affiliation may break down in favour of aggression. We did not mean to imply that ingroup feeding competition was the selection pressure responsible, but that ingroup feeding competition is a prime instance where the effects of outgroup threat may be expected to be prominent and measurable on within group behaviour due to the added social tension. We have changed this discussion to better reflect out motivation and hypotheses (lines 129-132, 138-146, 147-153). We have also briefly expanded on why outgroup threat may increase ingroup cohesion (such as through increasing group defence against intruders) in the introduction as in lines 48-50.

We have also added more detail to each of our statistical models. More specifically, in the analysis section of the methods, for each type of model we now include sentence clarifying the datasets that were included. We now mention all models were run on raw data. For that reason, offset terms were not necessary as the same number of scans were included in each condition. Regarding the play and aggression data, we have also added more reasoning (lines 302-307) and discuss these in regards to your other points below.

Line-by-line comments

Lines 46-50: this seems a bit repetitive with the previous sentences in the introduction.

We have removed this sentence.

While we think it is important to include all of these studies, as the literature on this subject is relatively underdeveloped and all of the previous studies with non-human animals can be described in the space of a few paragraphs, we agree this paragraph was too long and difficult to read. For that reason, we have separated the great ape background into a separate paragraph while retaining the information in the prior paragraph.

We have made this sentence less strong (line 101-103) and have added a brief sentence about the benefits of such experiments taking place in captivity (lines 113-115), namely the amount of experimental control and relative ease of consistent high-resolution observational data.

As we mentioned earlier we have rewritten this part to make our point clearer, which we agree was not well stated in the first draft. We instead bring this in as a secondary prediction, where outgroup threat promotes ingroup cohesion, and this then transfers and is especially noticeable in situations with ingroup tension (induced by feeding competition) as in lines 129-132 and 138-146.

Lines 134-142: See above but I disagree that the ingroup feeding competition selects for the relationship between ingroup cohesion and outgroup threat.

Thank you for this suggestion, we agree this makes it easier for readers to quickly understand the predictions from multiple behavioural measures.

Line 146: I think self-directed behavior should decrease.

In both our hypotheses, self-directed behaviour increased, and rest decreased, based on Kutsukake et al.’s (2012) study where cortisol and vigilance rose. While we used different measures, following his study we predicted that stress and vigilance would rise, but that it would be dealt with and its effect on social relations would be different between the conditions.

We have clarified this point, that we used the same composition on each day, which was simply the grouping composition that is already most frequent for these chimpanzees (lines 184-185).

Lines 181-183: Are these proximity measures nested? So if individuals are in contact with one another, are they also within 3 meters of one another?

Following your main point earlier, we added more detail to the statistical methods, and clarified that the proximity measures were on an ordinal scale of four levels (lines 280-282). A CLMM can then takes raw ordinal data and measures the likelihood of changing from one category to another.

We have added this information at the beginning of the analysis sections for each type of data.

As mentioned, we used all the proximity data together in a CLMM rather than running analyses on each of the four proximity categories, we made this point clearer in lines 280-282.

We have added details to this metric, where for each individual in each phase of each condition of each trial, there is a simple 1/0 metric of whether they displayed the given behaviour (lines 290-292, 305-306). This was done because separating bouts was not considered reliable and gives a more robust metric. While we then were not able to compare the different forms of aggression, which we agree are quite different, because of smaller sample sizes and floor effects of any one given form of aggression, we feel confident that these measures are valid and replicable.

Thank you for this suggestion, we agree this is a very interesting question for future research and have added this to the future directions on lines 493-493.

Relating to your earlier comment, we have clarified how each measure relates to the more general predictions of the group cohesion hypothesis (lines 149-154). We now state more clearly that we take play as another measure of affiliation, and while as you note it is not typically used as a metric of social bonding in the same way, we take it as another useful short term measure of positive social relations because it shows spontaneous affiliative social behaviour with other group members.

Line 441: Also important to note that captive chimps are not facing the same kind of feeding competition and even this kind of simulated feeding competition is not the same.

This is a good point we have added to the paragraph on limitations (lines 482-485).

We strongly agree and think this will be an important and insightful future direction for this line of research. Baseline social relations and their impact on the observed correlation between ingroup cohesion and outgroup threat will be a fascinating future project. We have added this suggestion to lines 492-493.

Figure 2: I think it would be helpful in the text and in this figure to arrange these metrics by categories: stress, vigilance, affiliation and aggression.

Thank you for this suggestion, we have added this to the figure exactly as you suggest and agree in makes the graph more readily understandable by readers at first glance.

Thank you again very much for all your comments and suggestions which we believe have made our manuscript significantly stronger.

Attachment

Submitted filename: RevResponse20201202.docx

Click here for additional data file.^{(25.4KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0246869.r003

Decision Letter 1

Katie E Slocombe

13 Jan 2021

PONE-D-20-33650R1

Uniting against a common enemy: perceived outgroup threat elicits ingroup cohesion in chimpanzees

PLOS ONE

Dear Dr. Brooks,

==============================

Thank you for your thorough and thoughtful revision of your manuscript. I think you did an excellent job of addressing the reviewer’s comments and this is shaping up to be a great paper. Careful reading of your revision have yielded a few more areas I would like you to address. All line numbers refer to the track changed version of the manuscript.

Interactions. Whilst your predictions exclusively deal with main effects of condition, many of your models reveal significant interactions. Whilst you are careful to describe the pattern of interaction between trial and condition in the text you don’t provide any illustration of these effects (Figure 2 which is cited represents main effects only).

I would like you to:

produce figures of graphing trial and condition for each of the significant interactions and include them in the supplementary and cite them in the main text;
Include some reference to habituation across trials and an interaction with trial being expected in the predictions section of the introduction – so making it clear that either a main effect of condition or an interaction with trial and condition, where the effect of condition decreases with trial would be supportive of the hypothesis (so that Figure 2 can legitimately say the effect is ‘consistent’ with the hypothesis even when it represents an interaction with trial).
Be explicit in the figure 2 legend that the measures which produced significant interactions are graphed here as main effects of condition and refer the reader to the new figures in the supplementary if they wish to see the interactions graphed.
I am unsure of how to interpret an oddsratio for an interaction – could help the reader to understand what it means?

Ethical concerns. Some readers may find the increase in stress the experimental procedure induced ethically questionable. I think it would be good to highlight in the discussion that investigation of a natural event which induces stress (intergroup encounters) is impossible without elevating stress levels, but as there was no difference in stress behaviours in the feeding context, the induced stress effects appeared to be shortlived (30 minutes), and therefore do not represent a substantial welfare issue.
In response to R1, you now state in the discussion there was considerable group variation. Please provide some data to demonstrate this in the supplementary (maybe figures showing the effect of condition by group?) and add a short section in the results to introduce this. Group doesn’t make it as a factor in most of your final models, so currently you don’t provide any evidence to support your claim of group variation, and it would be good for the interested reader to be able to look at the variation.

L471-3 I’m not quite clear what the point you are trying to make here – what part of the results could these factors account for (unless its clear what they might explain, saying they are unlikely to explain it doesn’t make much sense!).

L512 – insert ‘they’ between ‘chimpanzees’ and ‘do’.

Finally there are no copy editors for PLOS One, so please proof read your revision carefully before resubmission.

==============================

Please submit your revised manuscript by Feb 27 2021 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at [email protected]. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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We look forward to receiving your revised manuscript.

Kind regards,

Katie E. Slocombe, Ph.D

Academic Editor

PLOS ONE

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PLoS One. 2021 Feb 24;16(2):e0246869. doi: 10.1371/journal.pone.0246869.r004

Author response to Decision Letter 1

18 Jan 2021

Dear Professor Slocombe,

Thank you very much for your feedback and the chance to resubmit. We agree will all your suggestions, and have made the relevant changes to the manuscript and have added the requested figures to supplementary information. We additionally revised minor grammar and formatting points, and added a citation to a recently published study validating oxytocin administration affects social behaviour in bonobos and chimpanzees (Brooks et al. 2021). We have pasted your comments below with specific response in blue. Thank you for your consideration of our manuscript.

Sincerely,

James Brooks, Ena Onishi, Isabelle R. Clark, Manuel Bohn, and Shinya Yamamoto

1. Interactions. Whilst your predictions exclusively deal with main effects of condition, many of your models reveal significant interactions. Whilst you are careful to describe the pattern of interaction between trial and condition in the text you don’t provide any illustration of these effects (Figure 2 which is cited represents main effects only).

This is an important point. We have now made new visualizations for all of the effects for which the interaction was significant in order to clarify for the readers exactly how the effect changed across trials. These can be found in the supporting information zip file.

I would like you to:

i. produce figures of graphing trial and condition for each of the significant interactions and include them in the supplementary and cite them in the main text;

We have added these to the supporting information and refer to them on lines 367-369 400-401, and 425-426.

ii. Include some reference to habituation across trials and an interaction with trial being expected in the predictions section of the introduction – so making it clear that either a main effect of condition or an interaction with trial and condition, where the effect of condition decreases with trial would be supportive of the hypothesis (so that Figure 2 can legitimately say the effect is ‘consistent’ with the hypothesis even when it represents an interaction with trial).

We have added mention of this aspect of our hypotheses on lines 163-166.

iii. Be explicit in the figure 2 legend that the measures which produced significant interactions are graphed here as main effects of condition and refer the reader to the new figures in the supplementary if they wish to see the interactions graphed.

We have added this information (lines 367-369).

iv. I am unsure of how to interpret an oddsratio for an interaction – could help the reader to understand what it means?

Thank you for pointing this out, odds ratios are less straightforward to interpret with interactions and we have described this on lines 289-293.

2. Ethical concerns. Some readers may find the increase in stress the experimental procedure induced ethically questionable. I think it would be good to highlight in the discussion that investigation of a natural event which induces stress (intergroup encounters) is impossible without elevating stress levels, but as there was no difference in stress behaviours in the feeding context, the induced stress effects appeared to be shortlived (30 minutes), and therefore do not represent a substantial welfare issue.

Thank you for mentioning this point, we have added these details into the methods in the subsection “Ethical note” in order to give readers a clearer understanding of our ethical thinking (lines 171-178).

3. In response to R1, you now state in the discussion there was considerable group variation. Please provide some data to demonstrate this in the supplementary (maybe figures showing the effect of condition by group?) and add a short section in the results to introduce this. Group doesn’t make it as a factor in most of your final models, so currently you don’t provide any evidence to support your claim of group variation, and it would be good for the interested reader to be able to look at the variation.

Although we do not have sufficient data to include group type as a factor in our models, we recognize the importance of this and have added to the supporting information a table which include values for each group and measure to demonstrate the variation, and added mention of this to the manuscript in lines 360-363 and 479.

We have taken out this sentence. We had no specific predictions regarding how it could account for any part of our results, but mentioned it simply to clarify potential sources of variation. As you note it made the paragraph more confusing and we removed this sentence. Thank you for your suggestion.

L512 – insert ‘they’ between ‘chimpanzees’ and ‘do’.

Done

Thank you again for your careful consideration and advice on our manuscript.

Attachment

Submitted filename: editorreply_rev2.docx

Click here for additional data file.^{(18.9KB, docx)}

PLoS One. doi: 10.1371/journal.pone.0246869.r005

Decision Letter 2

Katie E Slocombe

28 Jan 2021

Uniting against a common enemy: perceived outgroup threat elicits ingroup cohesion in chimpanzees

PONE-D-20-33650R2

Dear Dr. Brooks,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Kind regards,

Katie E. Slocombe, Ph.D

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

Thank you for carefully addressing all the points I raised - looking forward to seeing this published! Congratulations!

Reviewers' comments:

PLoS One. doi: 10.1371/journal.pone.0246869.r006

Acceptance letter

Katie E Slocombe

1 Feb 2021

PONE-D-20-33650R2

Uniting against a common enemy: perceived outgroup threat elicits ingroup cohesion in chimpanzees

Dear Dr. Brooks:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact [email protected].

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Thank you for submitting your work to PLOS ONE and supporting open access.

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on behalf of

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Academic Editor

PLOS ONE

Associated Data

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Data Availability Statement

All relevant data are within the paper and its Supporting Information files.

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PERMALINK

Uniting against a common enemy: Perceived outgroup threat elicits ingroup cohesion in chimpanzees

James Brooks

Ena Onishi

Isabelle R Clark

Manuel Bohn

Shinya Yamamoto

Roles

Abstract

Introduction

Materials and methods

Ethical note

Subjects

Data collection

Experimental procedure

Stimuli

Analysis

Proximity

Behavior scans

All occurrence behavior

Results

Proximity

Fig 1. Proximity in the playback phase.

Behavior scans

Fig 2. Behaviors in the playback and food phases.

All occurrence behaviors

Discussion

Supporting information

Acknowledgments

Data Availability

Funding Statement

References

Decision Letter 0

Katie E Slocombe

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Author response to Decision Letter 0

Decision Letter 1

Katie E Slocombe

Roles

Author response to Decision Letter 1

Decision Letter 2

Katie E Slocombe

Roles

Acceptance letter

Katie E Slocombe

Roles

Associated Data

Supplementary Materials

Data Availability Statement

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