Behavioural diversity of bonobo prey preference as a potential cultural trait.

The importance of cultural processes to behavioural diversity in our closest living relatives is central to revealing the evolutionary origins of human culture. However, the bonobo is often overlooked as a candidate model. Further, a prominent critique to many examples of proposed animal cultures is premature exclusion of environmental confounds known to shape behavioural phenotypes. We addressed these gaps by investigating variation in prey preference between neighbouring bonobo groups that associate and overlap space use. We find group preference for duiker or anomalure hunting otherwise unexplained by variation in spatial usage, seasonality, or hunting party size, composition, and cohesion. Our findings demonstrate that group-specific behaviours emerge independently of the local ecology, indicating that hunting techniques in bonobos may be culturally transmitted. The tolerant intergroup relations of bonobos offer an ideal context to explore drivers of behavioural phenotypes, the essential investigations for phylogenetic constructs of the evolutionary origins of culture.

Introduction

Humans and other social animals exhibit a diversity of behavioural phenotypes attributed to genetic or social (i.e., cultural) evolutionary processes, and their combination, influenced by the environment (Allen, 2019; van Schaik et al., 2003; Whitehead et al., 2019; Whiten, 2017). While culture is identified as a pivotal selective process in human evolution (Boyd and Richerson, 1995; Whitehead et al., 2019), its relative contribution to shaping the behavioural diversity observed in non-human animals, including our closest living relatives, remains debated. For instance, in comparison to the other great ape species, little is known about potential cultural traits in bonobos (Pan paniscus) (Whiten, 2017), thereby limiting phylogenetic comparisons.

Culture is defined as group-specific behavioural patterns acquired through social learning (Laland and Janik, 2006). There is ample evidence that some foraging techniques are socially learned (e.g., primates [Whiten and van de Waal, 2018; cetaceans [Mann et al., 2012; carnivores [Thornton and Raihani, 2008]) and therefore represent good candidates for cultural traits. However, to distinguish whether social processes contribute to the emergence of behavioural phenotypes, it is essential to quantify ecological variation and account for its influence on behaviour expression, a challenging endeavour in wild settings. Few studies have attempted to limit potential ecological confounders by investigating behavioural diversity between neighbouring groups (Luncz and Boesch, 2014; Pascual-Garrido, 2019; van de Waal, 2018). Nonetheless, in the absence of between-group range overlap, fine-scale ecological variation specific to the locations where behavioural phenotypes are expressed cannot be excluded.

Our closest living relatives, bonobos and chimpanzees, hunt a variety of species across groups and populations (Gilby et al., 2015; Hobaiter et al., 2017; Hohmann and Fruth, 2008; Sakamaki et al., 2016; Samuni et al., 2018; Wakefield et al., 2019). However, it remains unclear whether this diversity is independent of large or even small-scale ecological variation in the distribution of prey species (Hobaiter et al., 2017; Sakamaki et al., 2016). Accounting for potential small-scale local ecological drivers is methodologically challenging in chimpanzees, a territorial species (Mitani et al., 2010; Samuni et al., 2017) where each group predominantly occupies unique non-overlapping areas. In contrast, the tolerant intergroup relations of bonobos (Furuichi, 2020) permit a context in which different behaviours are expressed by individuals of different groups in the same place and at the same time. Here, we investigate variation in bonobo predation patterns of two groups (Ekalakala and Kokoalongo) at the Kokolopori Bonobo Reserve. The groups share an extensive home range overlap (65% kernel overlap; Figure 1,A,B,C) and regular gene flow, thereby reducing ecological and genetic influences as an explanatory variable for intergroup differences in behavioural expressions (van de Waal, 2018). Specifically, we tested whether variation in prey preference between the two bonobo groups is explained by a) environmental variables, such as area usage and seasonality, and/or b) social factors, such as the number of potential hunters, individual association pattterns, and group identity.

Figure 1.

Predation patterns in Kokolopori bonobos.

Hunting locations (Figure 1—source data 1) of the three prey types: (a) anomalure (square), (b) duiker (circle), and (c) squirrel (triangle) in relation to the 95% Kernel usage area of Ekalakala (white polygon with solid border) and Kokoalongo (dark grey polygon with dashed border) and 50% Kernel usage area (Ekalakala in yellow, Kokoalongo in red). The overlapping 95% kernel area between Ekalakala and Kokoalongo is depicted in light grey. Also depicted are (d) the predicted hunt probabilities of the different prey types between Ekalakala and Kokoalongo as obtained from the BR model (Figure 1—source data 2).

Depicted from top to bottom. Congo rope squirrel (Funisciurus congicus; 108–113 g) – a diurnal social species that live in small groups. Congo rope squirrel nest in masses of twigs (‘drey’) located in the forks of branches or tree holes (Kingdon et al., 2013). Hunts of squirrels by bonobos appear solitary and opportunistic and are often unobserved, with a few observations suggesting that squirrels are hunted in proximity to their nests. Potentially due to the small size of squirrel prey, squirrel meat is rarely shared except within mother-offspring dyads. Lord Derby’s Anomalure (Anomalurus derbianus; 450–1,100 g) – a nocturnal arboreal species that dens in vertical hollow tree trunks. Adult individuals often nest alone but may occasionally share tree holes with few adults or other species (Kingdon et al., 2013). Bonobos will often climb and inspect tree holes, potentially in the search of anomalure prey. Upon detection, anomalure species usually attempt to escape by gliding from one tree to the other. Therefore, anomalure hunts typically involve several group members that shift between terrestrial and arboreal positions. Anomalure captures are typically accompanied by vocalizations and affiliative interactions (e.g., genital rubbing), and the meat is often shared between several adult individuals. Blue Duiker (Philantomba monticola; 3.9–6.5 kg) – a diurnal monogamous species that forage on the forest floor. After birth, females conceal their calf between tree buttresses for several weeks (Kingdon et al., 2013). Bonobos both actively chase adult duikers or, when detected, opportunistically seize duiker calves from their hiding locations. The only recorded duiker hunt in Ekalakala was the capture of a concealed duiker calf. As with anomalure hunts, the capture of duikers leads to heightened arousal amongst group members, expressed by vocalizations and affiliative gestures, and duiker meat is typically shared. We also once observed three Ekalakala females inspecting an injured adult female Bay duiker (Cephalophus castaneus), the other duiker species frequently hunted by the bonobos, hidden at the exit of a hollow log but they did not attempt to capture it.

Results

Between August 2016 and January 2020, we observed 59 successful captures and consumption of mammals by the bonobos, including anomalure, duiker, and squirrel species (Table 1; Figure 1—figure supplement 1; Video 1). Starting July 2019, we also collected data on unsuccessful hunts, and documented 11 hunt attempts on duiker and anomalure (duiker- NEkalakala = 2, NKokoalongo = 2; anomalure- NEkalakala = 4, NKokoalongo = 3). Overall, we observed all Ekalakala and 84% of Kokoalongo adult group members (100% if considering only individuals that were present for the entire study period) participating in hunts.

Table 1.

Successful hunts in Ekalakala and Kokoalongo between August 2016-Jan 2020.

Group	Anomalure*	Duiker†	Squirrel‡
Ekalakala	31	1	1
Kokoalongo	3	11	12

* Anomalurus derbianus, Anomalurus beecrofti.

† Philantomba monticola, Cephalophus castaneus.

‡ Funisciurus congicus.

Figure 1—figure supplement 1.

Prey species categories hunted by the Kokolopori bonobos.

Depicted from top to bottom. Congo rope squirrel (Funisciurus congicus; 108–113 g) – a diurnal social species that live in small groups. Congo rope squirrel nest in masses of twigs (‘drey’) located in the forks of branches or tree holes (Kingdon et al., 2013). Hunts of squirrels by bonobos appear solitary and opportunistic and are often unobserved, with a few observations suggesting that squirrels are hunted in proximity to their nests. Potentially due to the small size of squirrel prey, squirrel meat is rarely shared except within mother-offspring dyads. Lord Derby’s Anomalure (Anomalurus derbianus; 450–1,100 g) – a nocturnal arboreal species that dens in vertical hollow tree trunks. Adult individuals often nest alone but may occasionally share tree holes with few adults or other species (Kingdon et al., 2013). Bonobos will often climb and inspect tree holes, potentially in the search of anomalure prey. Upon detection, anomalure species usually attempt to escape by gliding from one tree to the other. Therefore, anomalure hunts typically involve several group members that shift between terrestrial and arboreal positions. Anomalure captures are typically accompanied by vocalizations and affiliative interactions (e.g., genital rubbing), and the meat is often shared between several adult individuals. Blue Duiker (Philantomba monticola; 3.9–6.5 kg) – a diurnal monogamous species that forage on the forest floor. After birth, females conceal their calf between tree buttresses for several weeks (Kingdon et al., 2013). Bonobos both actively chase adult duikers or, when detected, opportunistically seize duiker calves from their hiding locations. The only recorded duiker hunt in Ekalakala was the capture of a concealed duiker calf. As with anomalure hunts, the capture of duikers leads to heightened arousal amongst group members, expressed by vocalizations and affiliative gestures, and duiker meat is typically shared. We also once observed three Ekalakala females inspecting an injured adult female Bay duiker (Cephalophus castaneus), the other duiker species frequently hunted by the bonobos, hidden at the exit of a hollow log but they did not attempt to capture it.

Video 1.

Duiker and anomalure hunting by Kokolopori bonobos.

Most anomalure and duiker hunts occurred within overlapping ranging areas (94% of anomalure and 83% of duiker hunts), compared to only 46% of squirrel hunts (Figure 1,A,B,C). The groups engaged in frequent and prolonged intergroup associations (31% of observation days), and nine of the hunts (five duiker, three anomalure, one squirrel) occurred during intergroup encounters and at times involved between-group meat sharing. Although 45% of the Kokoalongo duiker hunts occurred during encounters, very few to none (mean = 1.4) of the Ekalakala individuals were present during these hunts, and none participated (Supplementary file 1). Due to the cohesiveness of bonobo groups (Hohmann and Fruth, 2002), the conspicuous nature of anomalure and duiker hunting (e.g., distress calls of duikers), and since the acquisition of meat often attracts individuals to hunting areas (Samuni et al., 2018), we are confident that we observed most anomalure and duiker feeding events. However, as the hunting and feeding of squirrel is often quiet and solitary and since hunting is frequently detected only post capture, we are likely to have underestimated this type of hunting.

Kokoalongo bonobos were more likely to capture duiker (estimate = 4.56, CI95% = [1.93, 8.03]; Figure 1D, Table 2) and squirrel species (estimate = 4.99, CI95% = [2.34, 8.21]), and were less likely to capture anomalure species in comparison with Ekalakala. The same pattern persisted during intergroup encounters (once we observed anomalure captured by a Kokoalongo female after a hunt by Ekalakala individuals; Supplementary file 1). We found that prey preferences were independent from potential local spatial and temporal ecological variation. Overall, more than 80% of all hunts occurred in overlapping areas (95% kernel), and neither utilization differences of specific hunt locations (reflecting varying opportunities to encounter prey species) nor potential annual seasonal variation strongly affected phenotypic variation in prey types captured (Table 2). Variation in prey preference can also arise from between-group difference in sizes of female or male association parties, association tendencies amongst party members, or presence of certain specialized hunters. However, the number of adult females or males present during hunts (i.e., available hunters) and the average dyadic association between them had no strong effect on prey outcome (Table 2). Further, we observed 17 different individuals (five males and 12 females) catching prey, encompassing 72% of Ekalakala and 40% of Kokoalongo group members (see Supplementary file 1 for the distributions of catchers). These percentages are likely an underestimation of the overall number of individuals who captured the prey, as their identity was not recorded for 40% of all hunts. Finally, our results are likely independent from genetic variation, as low genetic differentiation is expected (Schubert et al., 2011) mainly due to regular gene flow attributed to female migration between Ekalakala and Kokoalongo.

Table 2.

Bayesian Regression model results of the effect of group identity, number of available hunters and ecological variation on prey species captured (1anomalure and 2Ekalakala as reference categories). 

All numeric predictor variables were standardized to mean = 0 and sd = 1.

Coded level	Term	Estimate	SE	95% CI
Duiker1	Intercept	−3.25	1.04	−5.50,–1.51
	Group (Kokoalongo2)	4.56	1.57	1.93, 8.03
	Available male hunters	0.43	0.77	−1.05, 1.99
	Available female hunters	0.42	0.75	−1.07, 1.90
	Association	−0.77	0.74	−2.30, 0.68
	Usage difference	0.39	0.55	−0.63, 1.52
	Sine of Date	1.24	0.82	−0.33, 2.89
	Cosine of Date	0.00	0.84	−1.68, 1.63
Squirrel1	Intercept	−3.32	1.03	−5.61,–1.52
	Group (Kokoalongo2)	4.99	1.51	2.34, 8.21
	Available male hunters	0.50	0.80	−1.09, 2.11
	Available female hunters	−0.18	0.77	−1.66, 1.30
	Association	−0.61	0.73	−2.06, 0.79
	Usage difference	0.71	0.55	−0.32, 1.89
	Sine of Date	1.03	0.79	−0.47, 2.67
	Cosine of Date	0.36	0.81	−1.21, 1.92

Discussion

We found that bonobo groups that utilize overlapping home ranges and regularly socialize and forage together show group-specific prey acquisition patterns. These group-specific patterns appear independent of genetic and small-scale ecological variation, seasonality, size of hunting parties, or party cohesiveness. The exclusion of these confounders indicates that other drivers of behavioural variation act as mechanisms in prey selection.

Observed differences in prey preferences may arise if different techniques are required to locate and capture them. Duiker and squirrel hunting are either strictly terrestrial (duiker) or arboreal (squirrel) activities, which appear opportunistic and commonly involved a single individual hunter (more so for squirrel hunting). Conversely, anomalure hunting required the engagement of several group members, during which the bonobos employed both terrestrial and arboreal positions. While at this stage it is unclear if hunting techniques in bonobos require time to acquire or involve social learning processes, specialized hunting techniques may be at the basis of the observed group differences.

Prey species preference may additionally reflect differences in prey palatability between groups. Although between-group meat sharing of duiker and anomalure may contradict the idea of group specific meat preference, the costs and benefits associated with hunting relative to begging potentially alter consumption decisions. As hunting behaviour is associated with energetic costs, the benefit of capturing favourable prey may persuade hunt decision making. Conversely, once prey is captured, the costs associated with begging are minimal relative to hunting, thereby largely resetting the cost-to-benefit ratio behind foraging decisions. Thus, while palatability may dictate which prey species to pursue, it is expected to have a lesser impact on begging decisions.

The ‘impact hunter’ hypothesis (Gilby et al., 2015) could offer an alternative explanation for prey preference variation, proposing that certain individuals encourage social hunts by assuming hunt initiation costs. However, as this hypothesis addresses social hunt occurrence, it could explain the prevalence of social hunts like anomalure but cannot explain why duiker and squirrel hunting (opportunistic and largely solitary) are nearly absent in Ekalakala. Further, we observed many individuals participating in hunts and capturing prey and prey outcome was independent of the number of male or female hunters. Thus, patterns in our data indicate that we indeed document group, instead of individual, tendencies.

In the absence of ecological, genetic, or ingroup social dynamic explanations of prey acquisition, the observed group-specific differences may be cultural. Under this assumption, it is puzzling how such group differences would evolve and persist even when prolonged associations between Ekalakala and Kokoalongo should potentially promote intergroup social learning opportunities. Tolerance, at a degree that facilitates social learning in its various forms, is fundamental in converting innovations into transmitted traditions (Whiten and van de Waal, 2018). To improve ‘learning’ gains, social learners should be selective in the timing of observations and their choice of ‘models’ from whom to learn (Boyd and Richerson, 1995). Although the two groups associate for extended periods their intergroup relations are complex and unpredictable, characterized by a mixture of affiliative and agonistic exchanges, frequent fission-fusions and heightened arousal. Unpredictability of intergroup interactions is thus expected to hamper intergroup learning opportunities of certain skills which may require extensive time and effort to acquire (e.g., hunting techniques). Following group psychology predictions of ingroup bias and favouritism (Brewer, 1993), outgroup members may as well be less appealing ‘models’ for learning. Together, inconsistent intergroup relations and in-group bias may explain how group-specific prey preferences persist despite numerous intergroup learning opportunities. A by-product of divergent hunting techniques is reduced intergroup competition, which is likely adaptive, especially when groups share ranging zones. Thus, group-specific prey preferences in bonobos may have evolved as a form of microlevel niche differentiation that alleviates feeding competition.

Investigating the potential impact of culture on behavioural diversity in non-human animals is challenging due to the difficulties of estimating and accounting for local ecological variation as a driver of behavioural diversity. Challenges may even arise when behavioural variation appears between groups that occupy nearby but non-overlapping ranging areas. Bonobo social groups’ regular overlap in ranging area and tolerant interactions, offer fertile ground in which to explore whether variation in behavioural expressions occurs independently of spatial and temporal use of specific habitat locations. Here, by accounting and largely excluding potential local ecological variation, we provide strong indication for culturally transmitted subsistence hunting techniques in bonobos, informing on the evolution of behavioural diversity.

Materials and methods

Study site and data collection

We investigated behavioural diversity between two fully habituated bonobo groups (Ekalakala and Kokoalongo, followed since 2007) at the Kokolopori Bonobo Reserve, Democratic Republic of Congo (N 0.41716°, E 22.97552°; [Surbeck et al., 2017a]). We conducted full day party follows of the bonobo groups (1102 and 931 observation days in Ekalakala and Kokoalongo, respectively) and documented all occurrence hunting behaviour (here defined as capture of mammalian prey). All prey types were captured across most months, and both during the dry (June-August and December-February) and wet (March-May and September-November) seasons. Hunt participants were almost exclusively adult (>10 years) individuals, and both sexes were observed to participate. Adult group sizes fluctuated during the study between 9–11 adult individuals in Ekalakala and 16–24 adult individuals in Kokoalongo due to several deaths and migration events (Supplementary file 2).

Home range utilization distribution

We recorded data on party locations at one-minute intervals using a GPS (Garmin 62). We constructed home range utilization distributions of the bonobo groups using kernel density estimates (Worton, 1989). The home range (95% kernel) of the two groups between August 2016 and December 2019 was: Ekalakala – 35 km2, Kokoalongo – 40 km2, and the overlapping area encompassed 64% and 66% of the home ranges of Ekalakala and Kokoalongo, respectively.

Habitat structure and spatial distribution of prey species have been used as explanations for variation in hunting behaviours (Hobaiter et al., 2017; Sakamaki et al., 2016). However, as our data originate from two groups with extensive home range overlap, the explanatory power of these drivers is minimized. Nonetheless, we can evaluate intra-range variation in local ecology by accounting for relative home range usage across the groups. To do so, we assigned each hunt with two kernel usage values, one constituting the kernel usage of the group that hunted (hunt group) and the other constituting the kernel usage of the group that did not hunt (other group). We used the values to calculate a score of ‘usage difference’ (i.e., other group - hunt group; ranging between −50 and 86; mean ± sd: 20.19 ± 26.10). Higher scores reflected an area that is more predominantly used by the group that hunted.

Association patterns

We recorded the cumulative adult party composition at 30 min intervals and marked individuals observed during the hunt scan as potential hunters. Whenever a party composition scan collected either immediately before or during a hunt included individuals of both groups (representing between-group spatial proximity), that hunt was marked as occurring during an intergroup encounter. This approach categorized two hunts as intergroup hunts although members of only one group were present, but accounts for the likelihood that the other group is nearby.

We used these party scans to calculate dyadic association values for each dyad and year, using the following equation: SRI = PAB/(PA + PB - PAB) (Surbeck et al., 2017b). PA and PB represent the number of scans A or B were present, and PAB represents the number of scans both A and B were present. For every hunt, we then calculated the average dyadic association of the hunting party as a proxy of group social cohesion, which may affect the likelihood to capture prey.

Statistical analysis

We applied a Bayesian Regression model with prey type as a categorical response and logit link function to examine the influence of environmental (area usage and seasonality) and social (group identity, presence of potential hunters, and social cohesion) factors on prey preference expression. We fitted the model in R (version 3.6.1 [R Development Core Team, 2016]) using the function brm of the R package ‘brms’ (Bürkner, 2017) and weakly informative t-distributed priors (Lemoine, 2019). As predictors, we included the following environmental factors: a) ‘usage difference’ score as described above, and b) a seasonal temporal term, by including the sine and cosine of the Julian dates of the hunts converted into a continuous circular variable (Stolwijk et al., 1999). The sine and cosine predictors allow for the modelling of a wave like periodic pattern of peaks and valleys, thereby representing potential seasonal oscillations in hunt dates. Additionally, we included the following social factors: a) group identity of the individual who caught the prey, b) female and male party sizes (mean ± sd: Ekalakala - 7.19 ± 1.47; Kokoalongo – 7.05 ± 3.62; encounter - 13 ± 7.4), and c) average dyadic associations of hunt party mean ± sd: Ekalakala - 0.51 ± 0.09; Kokoalongo – 0.34 ± 0.13; encounter – 0.26 ± 0.14). Note, if dietary requirements alone were to dictate hunting patterns, then we would expect a random distribution (reflecting prey species encounter probabilities) of the different prey species captured within groups instead of group-specific patterns.

We ran 2000 iterations over four MCMC chains, with a ‘warm-up’ period of 1000 iterations per chain leading to 4000 usable posterior samples (Bürkner, 2017). Visual inspection of all MCMC results revealed satisfactory Rhat values (<1.01; [Gelman et al., 2013]), no divergent transitions after warmup, and stationarity and convergence to a common target, suggesting that our results are stable. We report the estimate (mean of the posterior distribution) and the 95% credible intervals (CI95%) indicating the strength of the effects. For estimate comparability and to ease model convergence, we standardized all numeric variables to mean = 0 and sd = 1. Our model did not suffer from issues of collinearity, evaluated using Variance Inflation Factors (Field et al., 2012) with the R package ‘car’ (Fox et al., 2020). The data reported in this paper are available as Source data 1.

In the interests of transparency, eLife publishes the most substantive revision requests and the accompanying author responses.

Acceptance summary:

The present paper is important because it reports behavioural variation between two overlapping groups of some of our closest relatives: bonobos. The authors provide a very interesting potential cultural trait in a relatively under-reported domain, predatory behaviour. Moreover, this research is able to provide compelling evidence of this behavioural variation due to the large overlap in the two groups territories, which convincingly sets aside the alternative explanation of ecological foundations for the observed variation.

Decision letter after peer review:

Thank you for submitting your article "Behavioural diversity of bonobo prey preference as a potential cultural trait" for consideration by eLife. Your article has been reviewed by three peer reviewers, including Erica Van de Waal as the Reviewing Editor and Reviewer #1, and the evaluation has been overseen by Detlef Weigel as the Senior Editor.

The reviewers have discussed the reviews with one another and the Reviewing Editor has drafted this decision to help you prepare a revised submission.

We would like to draw your attention to changes in our revision policy that we have made in response to COVID-19 (https://elifesciences.org/articles/57162). Specifically, when editors judge that a submitted work as a whole belongs in eLife but that some conclusions require a modest amount of additional new data, as they do with your paper, we are asking that the manuscript be revised to either limit claims to those supported by data in hand, or to explicitly state that the relevant conclusions require additional supporting data.

Our expectation is that the authors will eventually carry out the additional experiments and report on how they affect the relevant conclusions either in a preprint on bioRxiv or medRxiv, or if appropriate, as a Research Advance in eLife, either of which would be linked to the original paper.

Summary:

This is a very interesting report of apparent hunting differences in terms of prey preference in two neighbouring/overlapping bonobo groups. The paper is well-written and clear, as are the figures, and the methods and statistical analyses are rigorous, such that the authors' principal conclusions are well supported. While all reviewers enjoyed reading the article and were generally positive about the data (particularly in that they address the 'ecological' argument usually brought up by animal culture critics), some of the claims seem too strong and should be better substantiated by data presented directly in the main text.

Revisions for this paper:

We ask the authors to revise their paper following the comments here below. If the authors can address our concerns, we agree that the paper should be published in eLife, but the claims on culture should be toned down in line with what the data show.

1) Reviewer 3 has in particular a strong concern regarding the duiker data, which he fails to understand with the way data are presented in the manuscript at the moment (the raw data do not appear to be in mat sup either). This is crucial, because what the authors present as 'cultural differences' may also be just one group having a certain preference for a given prey (anomalures: whether this in itself is enough to claim cultural differences can be debated, enough for some authors, and not for others). In addition, there is no evidence at present that this group difference results from social learning.

2) Group composition (Sex differences and ID of hunters): we disagree with authority arguments of the type "because we do not expect it to have a difference on prey acquisition". Where does this come from, especially as it is well documented in the literature that there are sex differences regarding hunting in bonobos, which is often assumed to be female-led? It seems like it would be an important factor, in fact even more so for the identity of the main 'driver' of the hunt (or the Gilby 'impact hunter'). The results for the catcher also suggest that sex would have been a good factor to include in the analysis. What if females have a preference for anomalures and males for duikers? If there are more females in group A than group B, this can lead to apparent cultural differences because a given sex dominates the hunt in one group compared to the other. The authors need to provide more data to address this. In particular, it would be great to have a table that at least shows the different IDs of the 'catchers', as there is already a sex bias appearing with females more likely to catch the prey than males (which group do they belong to? Are the sex split between the two communities?). This will possibly already address the issue of personal preferences.

General comment for the Discussion: you found that the smaller group was mainly capturing anomalures, could it be not explained by the fact that smaller group are more cohesive and coordinated? Even if you checked for party size could you control for the composition of the party size? If in the larger group individuals are less bonded and stay more in the same party without successful anomalure hunters they might be less likely to hunt them? Whereas in the smaller group the individuals might be spending more time with all other group members?

3) Intergroup hunts: There is a lack of clarity on which hunt was an intergroup hunt in Table 1 and it is particularly concerning regarding the duiker hunt data. Out of 59 successful hunts, 9 were considered intergroup hunts. If 5 of the successful duiker hunts (as in, including meat sharing) involve members of both groups, why are they classified as 1 Ekalakala and 11 Kokoalongo hunts? Is it because the 'catcher' is from one of the groups only? But then if the ones who consume the food are from both groups, it's hard to argue that there would be 'culinary' cultural differences between the two groups (at best, the cultural difference is in the likelihood to engage in a certain type of hunting for a given prey). Thus shouldn't these hunts be taken out from the group analysis? The authors only state that 'the same pattern persisted during intergroup encounters'. The problem then is that whether these particular hunts are shared between both groups or removed, the possible duiker difference probably becomes minimal and largely irrelevant for lack of data. If that is the case, based on the remaining data, the authors can probably identify a strong preference in one group (Ekalakala for anomalure), but it gets harder to argue for cultural differences (particularly because there is no evidence provided for social learning processes).

4) Culture/social learning claims: The Discussion starts with the authors saying that the "findings demonstrate that social processes….". That is not true. The Materials and methods and Results do not actually test for any type of social influence or social learning on hunting. This sentence should thus be modified and in general, the discussion on specific kinds of social learning mechanism (emulation etc…) toned down or removed because there is nothing in the manuscript that can help with this question. It would be really nice to see (pending confirmation), that one community is more opportunistic in their hunting (duiker + squirrel) compared to the other that seems to go more collectively. However, the authors cannot take evidence for social learning for collective hunting from the literature (here, findings in dolphin hunting and a more general review in primates including foraging) as evidence for their own findings, which are quite distinct, starting with the study species. The authors' finding is that there is a clear difference in terms of (at least one) prey preference between two neighbouring/overlapping bonobo groups. Whether this is cultural can then be discussed in light of what the authors have shown (e.g. no effect of ecology). Hence it would be more correct to say: we have observed this difference, can it be cultural? In contrast, the last two paragraphs are good to keep, once the assumption that the difference is cultural is met.

5) Unsuccessful hunts: you need to clarify your hypothesis about the unsuccessful hunts. Is the argument about the unsuccessful hunts (Discussion, second paragraph) really valid if it is based on only 6 months of data (compared to the hunt count that spans several years)? Also, while reading the Results, it seemed that it was the entire dataset for unsuccessful hunts; but that does not seem to be the case in fact. It should probably be introduced differently to avoid confusion then. In general, this specific paragraph in the Discussion needs to be reworked as well if it aims to address the possible "Gilby argument". It can only be properly addressed by offering a list of IDs that shows diversity in individual hunters/catchers, and not by making group pattern remarks.

Revisions expected in follow-up work:

You need to add a table (for the hunts where you were able to record the identity of all participants) with the list of the different individuals that have been observed hunting on all three types of prey in both group, with their individual characteristics (such as age, sex, rank, relatedness of participants), and if the hunt with successful or not.

Summary:

This is a very interesting report of apparent hunting differences in terms of prey preference in two neighbouring/overlapping bonobo groups. The paper is well-written and clear, as are the figures, and the methods and statistical analyses are rigorous, such that the authors' principal conclusions are well supported. While all reviewers enjoyed reading the article and were generally positive about the data (particularly in that they address the 'ecological' argument usually brought up by animal culture critics), some of the claims seem too strong and should be better substantiated by data presented directly in the main text.

We thank the anonymous reviewers, Reviewing Editor Erica Van de Waal, and Senior Editor Delef Weigel for their valuable and constructive comments which have helped to improve our manuscript. We have addressed all their comments by incorporating additional predictors into the model (i.e., the number of males or female party members, association patterns of party members), adding tables, figure supplement, and video, and by toning down cultural claims.

Revisions for this paper:

We ask the authors to revise their paper following the comments here below. If the authors can address our concerns, we agree that the paper should be published in eLife, but the claims on culture should be toned down in line with what the data show.

1) Reviewer 3 has in particular a strong concern regarding the duiker data, which he fails to understand with the way data are presented in the manuscript at the moment (the raw data do not appear to be in mat sup either). This is crucial, because what the authors present as 'cultural differences' may also be just one group having a certain preference for a given prey (anomalures: whether this in itself is enough to claim cultural differences can be debated, enough for some authors, and not for others). In addition, there is no evidence at present that this group difference results from social learning.

This is a valuable point which we failed to clarify in the initial submission. As suggested, we have added a table of all documented successful hunts (Supplementary file 1), together with information of party composition by group, and when available, the identity and sex of the individual who captured the prey and the identity of individuals that participated in the hunt. We also provide more information on duiker hunts in the manuscript and toned-down discussions of social learning.

2) Group composition (Sex differences and ID of hunters): we disagree with authority arguments of the type "because we do not expect it to have a difference on prey acquisition". Where does this come from, especially as it is well documented in the literature that there are sex differences regarding hunting in bonobos, which is often assumed to be female-led? It seems like it would be an important factor, in fact even more so for the identity of the main 'driver' of the hunt (or the Gilby 'impact hunter'). The results for the catcher also suggest that sex would have been a good factor to include in the analysis. What if females have a preference for anomalures and males for duikers? If there are more females in group A than group B, this can lead to apparent cultural differences because a given sex dominates the hunt in one group compared to the other. The authors need to provide more data to address this. In particular, it would be great to have a table that at least shows the different IDs of the 'catchers', as there is already a sex bias appearing with females more likely to catch the prey than males (which group do they belong to? Are the sex split between the two communities?). This will possibly already address the issue of personal preferences.

The reviewers are correct to suggest that sex differences may drive prey acquisition patterns, which may explain group specific prey preference. We have now incorporated additional information on the group identity and sex of the individuals that captured the prey within the main text and as supplementary tables (Supplementary files 1-2). Further, to account for potential sex-differences in prey acquisition in the statistical analysis, we now include the number of available hunters as two separate covariate predictors, the number of male or female party members. Neither of the two predictors showed a clear effect on the response nor altered the overall model results.

General comment for the Discussion: you found that the smaller group was mainly capturing anomalures, could it be not explained by the fact that smaller group are more cohesive and coordinated? Even if you checked for party size could you control for the composition of the party size? If in the larger group individuals are less bonded and stay more in the same party without successful anomalure hunters they might be less likely to hunt them? Whereas in the smaller group the individuals might be spending more time with all other group members?

This is a nice suggestion. To account for the idea that social cohesion may drive hunt success of different species, we have incorporated into the model the average dyadic association values of hunt party members (i.e., adult individuals present during the hunt). The average dyadic association value serves as a proxy for social cohesion, such that higher values represent parties of individuals that associate more frequently overall. By including this predictor, we are accounting for some of the variation in prey type that can potentially be explained by social familiarity (see Results).

3) Intergroup hunts: There is a lack of clarity on which hunt was an intergroup hunt in Table 1 and it is particularly concerning regarding the duiker hunt data. Out of 59 successful hunts, 9 were considered intergroup hunts. If 5 of the successful duiker hunts (as in, including meat sharing) involve members of both groups, why are they classified as 1 Ekalakala and 11 Kokoalongo hunts? Is it because the 'catcher' is from one of the groups only? But then if the ones who consume the food are from both groups, it's hard to argue that there would be 'culinary' cultural differences between the two groups (at best, the cultural difference is in the likelihood to engage in a certain type of hunting for a given prey). Thus shouldn't these hunts be taken out from the group analysis? The authors only state that 'the same pattern persisted during intergroup encounters'. The problem then is that whether these particular hunts are shared between both groups or removed, the possible duiker difference probably becomes minimal and largely irrelevant for lack of data. If that is the case, based on the remaining data, the authors can probably identify a strong preference in one group (Ekalakala for anomalure), but it gets harder to argue for cultural differences (particularly because there is no evidence provided for social learning processes).

Per the reviewers’ comment, we understand that there was unclarity regarding definitions of intergroup encounters, the group identity associated with the hunt, and the overall duiker hunt data in initial submission.

Hunts were classified as Ekalakala or Kokoalongo depending on the identity of the individuals that participated in the hunt, and in cases when both groups participated, the identity of the individual that caught the prey defined the group identity (see Discussion).

We defined a hunt as occurring during an intergroup encounter whenever individuals of both groups were observed in the same party, either during the hunt scan or during the immediate scan prior to the hunt. This was done to account for the high likelihood that the other group is nearby when observed in temporal and spatial vicinity to the hunt. We have added the intergroup encounter definition in the Results. By this approach, two of the nine hunts defined as intergroup encounters included only Kokoalongo individuals (two duiker hunts). We believe that this definition is reliable as in one of the two cases, an Ekalakala female immediately joined the Kokoalongo party once duiker distress calls were heard after the successful capture, and received a share of the meat (Supplementary file 1).

Although, as the reviewer pointed out, 45% of Kokoalongo duiker hunts occurred during intergroup encounters, the average number of Ekalakala individuals present during these hunts was 1.4 and none of them participated in the hunt. Further, while Kokoalongo individuals are frequently observed to hunt adult duikers (Video 1), the only duiker hunt observed in Ekalakala involved the capture of a duiker calf from its hiding place (involving a different hunting technique than what is needed for adult duikers). We have added this information in the main text (Results) and in the legend of the additional figure (Figure 1—figure supplement 1). Taken together, we argue that the duiker data is meaningful for the observed between-group prey difference.

The reviewers also suggest that between group meat sharing observations likely refute ‘culinary’ differences between the groups. However, here we argue that prey palatability differences may still be at the basis of the observed group differences because the costs associated with hunting for meat are very different (higher) than the costs associated with begging for meat. While palatability differences may dictate hunting decisions so to maximize the cost-to-benefit ratio, once prey is already captured the costs associated with access to meat are minimized. In sum, bonobos might not initiate a hunt on a less preferred prey due to hunt costs but will beg for the meat when others have caught it. We have added this as part of the Discussion.

4) Culture/social learning claims: The Discussion starts with the authors saying that the "findings demonstrate that social processes….". That is not true. The Materials and methods and Results do not actually test for any type of social influence or social learning on hunting. This sentence should thus be modified and in general, the discussion on specific kinds of social learning mechanism (emulation etc…) toned down or removed because there is nothing in the manuscript that can help with this question. It would be really nice to see (pending confirmation), that one community is more opportunistic in their hunting (duiker + squirrel) compared to the other that seems to go more collectively. However, the authors cannot take evidence for social learning for collective hunting from the literature (here, findings in dolphin hunting and a more general review in primates including foraging) as evidence for their own findings, which are quite distinct, starting with the study species. The authors' finding is that there is a clear difference in terms of (at least one) prey preference between two neighbouring/overlapping bonobo groups. Whether this is cultural can then be discussed in light of what the authors have shown (e.g. no effect of ecology). Hence it would be more correct to say: we have observed this difference, can it be cultural? In contrast, the last two paragraphs are good to keep, once the assumption that the difference is cultural is met.

We followed the reviewers’ comment and modified claims of cultural transmission or discussion of social learning and further emphasize our findings regarding the lack of ecological effects.

5) Unsuccessful hunts: you need to clarify your hypothesis about the unsuccessful hunts. Is the argument about the unsuccessful hunts (Discussion, second paragraph) really valid if it is based on only 6 months of data (compared to the hunt count that spans several years)? Also, while reading the results, it seemed that it was the entire dataset for unsuccessful hunts; but that does not seem to be the case in fact. It should probably be introduced differently to avoid confusion then. In general, this specific paragraph in the Discussion needs to be reworked as well if it aims to address the possible "Gilby argument". It can only be properly addressed by offering a list of IDs that shows diversity in individual hunters/catchers, and not by making group pattern remarks.

Successful hunts have only been recorded starting July 2019, when LS initiated field work in Kokolopori. Thus, we unfortunately only have preliminary data regarding unsuccessful hunts. We have reworded the sentence to clarify this “Starting July 2019 we also collected data on unsuccessful hunts”. We have also decided to remove this section from the Discussion, as we agree with the reviewer that the results are preliminary and sample size is low.

Revisions expected in follow-up work:

You need to add a table (for the hunts where you were able to record the identity of all participants) with the list of the different individuals that have been observed hunting on all three types of prey in both group, with their individual characteristics (such as age, sex, rank, relatedness of participants), and if the hunt with successful or not.

We have added two tables (Supplementary files 1-2). One table includes the identities of all individuals per group with information on their sex and age categories (Supplementary file 2), and a second table with information of all successful hunt cases, including the identity of individuals present during the hunt by group membership, and when available the identity and sex of the individual who caught the prey and of those that participated in the hunt (Supplementary file 1).