Publications

2024
Rachna Reddy, Liran Samuni, Veronika Staedele, Linda Vigilant, and Martin Surbeck. 2024. “Maternal conflict intervention is more frequent in chimpanzee compared to bonobo development.” Animal Behaviour, 208, Pp. 127-136. Publisher's VersionAbstract
One way mammalian mothers support offspring is by intervening on their behalf when they receive conspecific aggression. Maternal intervention protects offspring and facilitates mother–offspring rank correlation in several female-philopatric species. We tested the hypothesis that maternal intervention during development similarly facilitates mother–offspring rank correlation in one of our two male-philopatric closest living relatives: bonobos, Pan paniscus, for whom male ranks have been described as matrifocal but mechanisms of status transmission are unclear. We predicted mothers would intervene at higher rates in bonobos compared to chimpanzees, Pan troglodytes, where sons earn adult ranks independently. We expected this difference would be especially pronounced for sons as they reached reproductive age (∼8 years) and when aggressors were adult males, which female bonobos, but not female chimpanzees, often dominate. However, for both sons and daughters of all ages (0.5–16 years) and against aggressors of varying age and sex, bonobo mothers in Kokolopori, DRC (N = 22 pairs, 210 conflicts) intervened less frequently than did chimpanzee mothers at Ngogo, Uganda (N = 66 pairs, 221 conflicts), doing so in 8% versus 49% of all conflicts. These differences persisted regardless of the severity of aggression offspring received and the distress they demonstrated. Our results provide no support for our hypothesis that conflict intervention facilitates mother–son rank correlation in bonobos. Nor are patterns explained by additional alternative hypotheses related to species variation in costs of retaliation, quality of female–female relationships or infanticide risk. We introduce two new hypotheses: (1) that success in aggressive competition is less important for male bonobos than for male chimpanzees and (2) proclivities for support are heightened in chimpanzees compared to bonobos because of increased ingroup protectiveness in chimpanzees. The latter hypothesis arises from our unexpected, preliminary observation that nonmother bonobo bystanders intervened less often than nonmother chimpanzee bystanders during these events.
Liran Samuni, Erin Wessling, and Martin Surbeck. 2024. “Rethinking peace from a bonobo perspective.” Behavioral and Brain Sciences, 47, Pp. e27. Publisher's VersionAbstract
Reconstructing pathways to human peace can be hampered by superficial evaluations of similar processes in nonhuman species. A deeper understanding of bonobo social systems allows us to reevaluate the preconditions for peace to gain a greater insight on the evolutionary timescale of peace emergence.
2023
Maud Mouginot, Leveda Cheng, Michael L. Wilson, Joseph T. Feldblum, Veronika Städele, Emily E. Wroblewski, Linda Vigilant, Beatrice H. Hahn, Yingying Li, Yingying Li, Anne E. Pusey, and Martin Surbeck. 6/26/2023. “Reproductive inequality among males in the genus Pan.” Philosophical Transactions of the Royal Society B: Biological Sciences, 378, 1883. Publisher's VersionAbstract
Reproductive inequality, or reproductive skew, drives natural selection, but has been difficult to assess, particularly for males in species with promiscuous mating and slow life histories, such as bonobos (Pan paniscus) and chimpanzees (Pan troglodytes). Although bonobos are often portrayed as more egalitarian than chimpanzees, genetic studies have found high male reproductive skew in bonobos. Here, we discuss mechanisms likely to affect male reproductive skew in Pan, then re-examine skew patterns using paternity data from published work and new data from the Kokolopori Bonobo Reserve, Democratic Republic of Congo and Gombe National Park, Tanzania. Using the multinomial index (M), we found considerable overlap in skew between the species, but the highest skew occurred among bonobos. Additionally, for two of three bonobo communities, but no chimpanzee communities, the highest ranking male had greater siring success than predicted by priority-of-access. Thus, an expanded dataset covering a broader demographic range confirms that bonobos have high male reproductive skew. Detailed comparison of data from Pan highlights that reproductive skew models should consider male–male dynamics including the effect of between-group competition on incentives for reproductive concessions, but also female grouping patterns and factors related to male–female dynamics including the expression of female choice.
Isaac Schamberg, Zanna Clay, Simon Townsend, and Martin Surbeck. 2023. “Between-group variation in production of pant-grunt vocalizations by wild bonobos (Pan paniscus) .” Behavioral Ecology and Sociobiology, 77, 14. Publisher's VersionAbstract

The potential for aggression is inherent in social interaction, and strategies to reduce the costs of aggression are ubiquitous among group-living animals. One strategy employed by lower-ranking individuals in a variety of species is the production of subordination signals, which are formal signals that communicate the signaler’s inferior status relative to the recipient of the signal. Here, we report the results of our investigations into (1) the presence and usage of the pant-grunt vocalization in two populations of wild bonobos; (2) the relationship between the production of pant-grunts and agonistic predictability across the genus Pan. We find stark differences in production of pant-grunts in the two populations: bonobos at the LuiKotale field site regularly used pant-grunts as a signal of subordination (primarily, though not exclusively, among male-male dyads); in contrast, at the Kokolopori field site, adult bonobos were never observed producing pant-grunts. Across Pan, we find weak support for an association between agonistic predictability and production of pant-grunt vocalizations.

There have been conflicting reports on whether bonobos, like chimpanzees, produce the submissive pant-grunt vocalization. We confirm the presence of the pant-grunt in the bonobo vocal repertoire, and document variation in its production across communities. We also suggest that variation in pant-grunt production across the genus Pan may be explained by the predictability of dominance interactions.

Liran Samuni and Martin Surbeck. 2023. “Cooperation across social borders in bonobos.” Science, 382, 6672, Pp. 805-809. Publisher's VersionAbstract
Cooperation beyond familial and group boundaries is core to the functioning of human societies, yet its evolution remains unclear. To address this, we examined grooming, coalition, and food-sharing patterns in bonobos (Pan paniscus), one of our closest living relatives whose rare out-group tolerance facilitates interaction opportunities between groups. We show that, as in humans, positive assortment supports bonobo cooperation across borders. Bonobo cooperative attitudes toward in-group members informed their cooperative relationships with out-groups, in particular, forming connections with out-group individuals who also exhibited high cooperation tendencies. Our findings show that cooperation between unrelated individuals across groups without immediate payoff is not exclusive to humans and suggest that such cooperation can emerge in the absence of social norms or strong cultural dispositions.
2022
Liran Samuni, Kevin E Langergraber, and Martin Surbeck. 2022. “Characterization of Pan social systems reveals in-group/out-group distinction and out-group tolerance in bonobos.” Proceedings of the National Academy of Sciences, 119, 26, Pp. e2201122119. Publisher's VersionAbstract
Human between-group interactions are highly variable, ranging from violent to tolerant and affiliative. Tolerance between groups is linked to our unique capacity for large-scale cooperation and cumulative culture, but its evolutionary origins are understudied. In chimpanzees, one of our closest living relatives, predominantly hostile between-group interactions impede cooperation and information flow across groups. In contrast, in our other closest living relative, the bonobo, tolerant between-group associations are observed. However, as these associations can be frequent and prolonged and involve social interactions that mirror those within groups, it is unclear whether these bonobos really do belong to separate groups. Alternatively, the bonobo grouping patterns may be homologous to observations from the large Ngogo chimpanzee community, where individuals form within-group neighborhoods despite sharing the same membership in the larger group. To characterize bonobo grouping patterns, we compare the social structure of the Kokolopori bonobos with the chimpanzee group of Ngogo. Using cluster analysis, we find temporally stable clusters only in bonobos. Despite the large spatial overlap and frequent interactions between the bonobo clusters, we identified significant association preference within but not between clusters and a unique space use of each cluster. Although bonobo associations are flexible (i.e., fission–fusion dynamics), cluster membership predicted the bonobo fission compositions and the spatial cohesion of individuals during encounters. These findings suggest the presence of a social system that combines clear in-group/out-group distinction and out-group tolerance in bonobos, offering a unique referential model for the evolution of tolerant between-group interactions in humans.
Eve Davidian, Martin Surbeck, Dieter Lukas, Peter M Kappeler, and Elise Huchard. 2022. “The eco-evolutionary landscape of power relationships between males and females.” Trends in Ecology & Evolution, 37, 8, Pp. 706-718. Publisher's VersionAbstract
In animal societies, control over resources and reproduction is often biased towards one sex. Yet, the ecological and evolutionary underpinnings of male–female power asymmetries remain poorly understood. We outline a comprehensive framework to quantify and predict the dynamics of male–female power relationships within and across mammalian species. We show that male–female power relationships are more nuanced and flexible than previously acknowledged. We then propose that enhanced reproductive control over when and with whom to mate predicts social empowerment across ecological and evolutionary contexts. The framework explains distinct pathways to sex-biased power: coercion and male-biased dimorphism constitute a co-evolutionary highway to male power, whereas female power emerges through multiple physiological, morphological, behavioural, and socioecological pathways.
Leveda Cheng, Liran Samuni, Stefano Lucchesi, Tobias Deschner, and Martin Surbeck. 2022. “Love thy neighbour: behavioural and endocrine correlates of male strategies during intergroup encounters in bonobos.” Animal Behaviour, 187, Pp. 319-330. Publisher's VersionAbstract
Across group-living taxa, males act aggressively towards outgroup males because they represent a threat to reproduction with ingroup females. This intergroup aggression can entail agonistic coalition formation between group members, is typically associated with higher testosterone levels and prevents extended associations between members of different groups. However, in a few species, including humans, groups can interact peacefully, allowing the exchange of resources and information. To better understand how social relationships are manifested between groups and the involvement of males in these relationships, we investigated behavioural and endocrine correlates of male strategies during intergroup encounters in bonobos, Pan paniscus. We found that, despite overt intergroup aggression, males rarely engaged in coalitionary attacks against outgroup individuals and their testosterone levels did not rise during intergroup encounters. Also, males sacrificed the time available to affiliate with ingroup individuals and actively affiliated with outgroup individuals, especially outgroup males. The paucity of cooperative group defence and high levels of intergroup affiliation suggest that male bonobos play a role in maintaining tolerant intergroup relationships. We discuss how our findings relate to the establishment of male–male social relationships beyond the group level in other species.
Leveda Cheng, Amber Shaw, and Martin Surbeck. 2022. “Mothers stick together: how the death of an infant affects female social relationships in a group of wild bonobos (Pan paniscus).” Primates, 63, Pp. 343–353. Publisher's VersionAbstract
Sociality is widespread among group-living primates and is beneficial in many ways. Sociality amongst female bonobos (Pan paniscus) has been proposed to have evolved as a female counterstrategy to male infanticide and sexual coercion. In male-philopatric bonobo societies, females mostly form relationships with unrelated females. Among these social relationships, it has been proposed that females with infants (also referred to as mothers) tend to have strong relationships with each other (mother-bonding hypothesis). In this paper, we use the case of an infant death in a group of wild bonobos in the Kokolopori Bonobo Reserve, Democratic Republic of Congo, to test this hypothesis. By using dyadic sociality indices for grooming, proximity, and aggression, we investigated whether the infant death influenced dyadic relationships the mother had with other group members. Before the infant death, grooming index (GI) and proximity index (PI) scores were the highest between the focal mother and another mother. After the death, the relationship of this mother dyad weakened, as indicated by lower GI and PI scores, whereas the relationship of another mother dyad became stronger. Aggression index scores among the mothers were comparable before and after the death, suggesting that changes in mother affiliative relationships were not a by-product of changes in overall interaction frequencies. Also, PI scores increased between the focal mother and three non-mothers after the death. Collectively, the shift in social dynamics between the focal mother and other group members after the infant death partially supported the mother-bonding hypothesis.
Erin Wessling, Liran Samuni, Roger Mundry, Miguel Adan Pascual, Stefano Lucchesi, Bienfait Kambale, and Martin Surbeck. 2022. “The potential for aggression is inherent in social interaction, and strategies to reduce the costs of aggression are ubiquitous among group-living animals. One strategy employed by lower-ranking individuals in a variety of species is the production of sub.” Ecology and Evolution, 12. Publisher's VersionAbstract
Characteristics of food availability and distribution are key components of a species' ecology. Objective ecological surveying used in animal behavior research does not consider aspects of selection by the consumer and therefore may produce imprecise measures of availability. We propose a method to integrate ecological sampling of an animal's environment into existing behavioral data collection systems by using the consumer as the surveyor. Here, we evaluate the consumer-centric method (CCM) of assessing resource availability for its ability to measure food resource abundance, distribution, and dispersion. This method catalogs feeding locations observed during behavioral observation and uses aggregated data to characterize these ecological metrics. We evaluated the CCM relative to traditional vegetation plot surveying using accumulated feeding locations across 3 years visited by a tropical frugivore, the bonobo (Pan paniscus), and compared it with data derived from over 200 vegetation plots across their 50 km2+ home ranges. We demonstrate that food species abundance estimates derived from the CCM are comparable to those derived from traditional vegetation plot sampling in less than 2 years of data collection, and agreement improved when accounting for aspects of consumer selectivity in objective vegetation plot sampling (e.g., tree size minima). Density correlated between CCM and plot-derived estimates and was relatively insensitive to home range inclusion and other species characteristics, however, it was sensitive to sampling frequency. Agreement between the methods in relative distribution of resources performed better across species than expected by chance, although measures of dispersion correlated poorly. Once tested in other systems, the CCM may provide a robust measure of food availability for use in relative food availability indices and can be incorporated into existing observational data collection. The CCM has an advantage over traditional sampling methods as it incorporates sampling biases relevant to the consumer, thereby serving as a promising method for animal behavioral research.
Peter M Kappeler, Elise Huchard, Alice Baniel, Charlotte Canteloup, Marie JE Charpentier, Leveda Cheng, Eve Davidian, Julie Duboscq, Claudia Fichtel, Charlotte K Hemelrijk, Oliver P Höner, Lee Koren, Jérôme Micheletta, Lea Prox, Tommaso Saccà, Lauren Seex, Nikolaos Smit, Martin Surbeck, Erica Van de Waal, and Cédric Girard-Buttoz. 2022. “Sex and dominance: How to assess and interpret intersexual dominance relationships in mammalian societies .” Front. Ecol. Evol. Publisher's VersionAbstract
The causes and consequences of being in a particular dominance position have been illuminated in various animal species, and new methods to assess dominance relationships and to describe the structure of dominance hierarchies have been developed in recent years. Most research has focused on same-sex relationships, however, so that intersexual dominance relationships and hierarchies including both sexes have remained much less studied. In particular, different methods continue to be employed to rank males and females along a dominance hierarchy, and sex biases in dominance are still widely regarded as simple byproducts of sexual size dimorphism. However, males and females regularly compete over similar resources when living in the same group, and sexual conflict takes a variety of forms across societies. These processes affect the fitness of both sexes, and are mitigated by intersexual hierarchies. In this study, we draw on data from free-ranging populations of nine species of mammals that vary in the degree to which members of one sex dominate members of the other sex to explore the consequences of using different criteria and procedures for describing intraand intersexual dominance relationships in these societies. Our analyses confirmed a continuum in patterns of intersexual dominance, from strictly male-dominated species to strictly female-dominated species. All indices of the degree of female dominance were well correlated with each other. The rank order among same-sex individuals was highly correlated between the intra- and intersexual hierarchies, and such correlation was not affected by the degree of female dominance. The relative prevalence of aggression and submission was sensitive to variation in the degree of female dominance across species, with more submissive signals and fewer aggressive acts being used in societies where female dominance prevails. Thus, this study provides important insights and key methodological tools to study intersexual dominance relationships in mammals.
Liran Samuni, David Lemieux, Alicia Lamb, Daiane Galdino, and Martin Surbeck. 2022. “Tool use behavior in three wild bonobo communities at Kokolopori.” American Journal of Primatology, 84, 1, Pp. e23342. Publisher's VersionAbstract
Comparative studies on tool technologies in extant primates, especially in our closest living relatives, offer a window into the evolutionary foundations of tool use in hominins. Whereas chimpanzee tool technology is well studied across populations, the scarcity of described tool technology in wild populations of our other closest living relative, the bonobo, is a mystery. Here we provide a first report of the tool use repertoire of the Kokolopori bonobos and describe in detail the use of leaf-umbrellas during rainfall, with the aim to improve our knowledge of bonobo tool use capacity in the wild. The tool use repertoire of the Kokolopori bonobos was most similar to that of the nearby population of Wamba and comprised eight behaviors, none in a foraging context. Further, over a 6-month period we documented 44 instances of leaf-umbrella use by 22 individuals from three communities, suggesting that this behavior is habitual. Most leaf-umbrella tool users were adult females, and we observed a nonadult using a leaf-umbrella on only a single occasion. While the study and theory of tool technologies is often based on the use of tools in foraging tasks, tool use in bonobos typically occurs in nonforaging contexts across populations. Therefore, incorporating both foraging and nonforaging contexts into our theoretical framework is essential if we wish to advance our understanding of the evolutionary trajectories of tool technology in humans.
Erin Wessling and Martin Surbeck. 2022. “Failure to account for behavioral variability significantly compromises accuracy in indirect population monitoring.” Animal Conservation. Publisher's VersionAbstract
Indirect wildlife population surveying largely depends upon counts of artifacts of behavior (e.g., nests or dung). Likelihood to encounter these artifacts is derived from both artifact production and decay, and variability in production behavior is considered to contribute minimally to inaccuracy in wildlife estimation. Here, we demonstrate how ignoring behavioral variability leads to significant population misestimation, using an example of an endangered ape, the bonobo (Pan paniscus). Until now, a single estimate of nest construction rate has been used to extrapolate bonobo densities, assumed to be broadly representative of bonobo sign production behavior. We estimated nest construction rates across seasons and social groups at the Kokolopori Bonobo Reserve, Democratic Republic of the Congo, and find nest construction rates in bonobos to be highly variable across populations as well as seasonal within populations. Failure to account for this variability led to degradation in the accuracy of bonobo population density estimates, accounting for a likely overestimation of bonobo numbers by 34%, and at worst as high as 80%. With this example, we demonstrate that failure to account for inter- and intrapopulation behavioral variation compromises the ability to estimate both relative and absolute wildlife abundances. We argue that variation in sign production is but one of the several potential ways that behavioral variability can affect conservation monitoring, should be measured across contexts whenever possible, and must be considered in population estimation confidence intervals. With increasing attention to behavioral variability as a potential tool for conservation, conservationists must also account for the impact that behavioral variability can have upon wildlife population estimation. Our results underline the importance of observational research to wildlife monitoring schemes as a critical component of conservation management. We discuss the avenues through which behavioral variability is likely to impact wildlife monitoring accuracy and precision and propose potential approaches for accounting for behavioral variability in wildlife monitoring.
2021
Martin Surbeck, Cédric Girard-Buttoz, Liran Samuni, Christophe Boesch, Barbara Fruth, Catherine Crockford, Roman M Wittig, and Gottfried Hohmann. 2021. “Attractiveness of female sexual signaling predicts differences in female grouping patterns between bonobos and chimpanzees.” Communications biology, 4, 1, Pp. 1-11. Publisher's VersionAbstract
Here we show that sexual signaling affects patterns of female spatial association differently in chimpanzees and bonobos, indicating its relevance in shaping the respective social systems. Generally, spatial association between females often mirrors patterns and strength of social relationships and cooperation within groups. While testing for proposed differences in female-female associations underlying female coalition formation in the species of the genus Pan, we find only limited evidence for a higher female-female gregariousness in bonobos. While bonobo females exhibited a slightly higher average number of females in their parties, there is neither a species difference in the time females spent alone, nor in the number of female party members in the absence of sexually attractive females. We find that the more frequent presence of maximally tumescent females in bonobos is associated with a significantly stronger increase in the number of female party members, independent of variation in a behavioural proxy for food abundance. This indicates the need to look beyond ecology when explaining species differences in female sociality as it refutes the idea that the higher gregariousness among bonobo females is driven by ecological factors alone and highlights that the temporal distribution of female sexual receptivity is an important factor to consider when studying mammalian sociality.
Stefano Lucchesi, Leveda Cheng, Erin G Wessling, Bienfait Kambale, Albert L Lokasola, Sylvia Ortmann, and Sylvia Ortmann. 2021. “Importance of subterranean fungi in the diet of bonobos in Kokolopori.” American Journal of Primatology, 83, 9, Pp. e23308. Publisher's VersionAbstract
Nonstaple food is a food resource which sole consumption does not allow the maintenance of regular physiological functions, thus constituting a minor portion of an individual's diet. Many primates consume nonstaple food such as meat, insects, and fungi. Hypotheses on the dietary importance of nonstaple food include its role as fallback food and as source of specific nutrients. We tested these two hypotheses by investigating mycophagy (i.e., the consumption of fungi) in a population of wild bonobos in the Kokolopori Bonobo Reserve, DRC. Specifically, we examined the relationship between fungus consumption and various factors relevant to bonobo feeding ecology (i.e., fruit abundance and the consumption of other food types). Additionally, we measured the deviation from linear travel when bonobos searched for fungi to evaluate the nature of fungus consumption (e.g., opportunistic or targeted). Lastly, we examined the nutritional content of the major fungus species consumed (Hysterangium bonobo) to test whether this food item was potentially consumed as source of specific nutrients. We found that bonobos spent a higher proportion of their time feeding on fungi when fruit abundance was higher, indicating that fungi were not consumed as a fallback food. Moreover, bonobos deviated from linear travel when visiting fungus patches more than observed when visiting fruit patches, suggesting that they actively sought out fungi. Lastly, initial analyses suggest that H. bonobo samples contained high concentration of sodium. Collectively, these results suggest that subterranean fungi appear to be attractive food source to Kokolopori bonobos, and that mycophagy may serve to supplement nutrients, like sodium, in bonobo diet.
Jan F Gogarten, Malte Rühlemann, Elizabeth Archie, Jenny Tung, Chantal Akoua-Koffi, Corinna Bang, Tobias Deschner, Jean-Jacques Muyembe-Tamfun, Martha M Robbins, Grit Schubert, Martin Surbeck, Roman M Wittig, Klaus Zuberbühler, John F Baines, Andre Franke, Fabian Leendertz, and Sébastien Calvignac-Spencer. 2021. “Primate phageomes are structured by superhost phylogeny and environment.” Proceedings of the National Academy of Sciences, 118, 15, Pp. e2013535118. Publisher's VersionAbstract
Humans harbor diverse communities of microorganisms, the majority of which are bacteria in the gastrointestinal tract. These gut bacterial communities in turn host diverse bacteriophage (hereafter phage) communities that have a major impact on their structure, function, and, ultimately, human health. However, the evolutionary and ecological origins of these human-associated phage communities are poorly understood. To address this question, we examined fecal phageomes of 23 wild nonhuman primate taxa, including multiple representatives of all the major primate radiations. We find relatives of the majority of human-associated phages in wild primates. Primate taxa have distinct phageome compositions that exhibit a clear phylosymbiotic signal, and phage–superhost codivergence is often detected for individual phages. Within species, neighboring social groups harbor compositionally and evolutionarily distinct phageomes, which are structured by superhost social behavior. Captive nonhuman primate phageome composition is intermediate between that of their wild counterparts and humans. Phage phylogenies reveal replacement of wild great ape–associated phages with human-associated ones in captivity and, surprisingly, show no signal for the persistence of wild-associated phages in captivity. Together, our results suggest that potentially labile primate-phage associations have persisted across millions of years of evolution. Across primates, these phylosymbiotic and sometimes codiverging phage communities are shaped by transmission between groupmates through grooming and are dramatically modified when primates are moved into captivity.
 
Leveda Cheng, Stefano Lucchesi, Roger Mundry, Liran Samuni, Tobias Deschner, and Martin Surbeck. 2021. “Variation in aggression rates and urinary cortisol levels indicates intergroup competition in wild bonobos.” Hormones and behavior, 128, Pp. 104914. Publisher's VersionAbstract

Intergroup competition is a widespread phenomenon across taxa and groups typically compete over access to limited resources, such as food and mates. Such competition may be quantified by changes in individuals' behavioral and physiological status in response to intergroup encounters (IGEs). Bonobos, one of our closest living relatives, are often regarded as xenophilic and exhibit high tolerance towards out-group individuals. This tolerance between groups may still be accompanied by intergroup competition over resources. We hereby compared variation in aggression rates and urinary cortisol levels of bonobos during and outside contexts of IGEs in the Kokolopori Bonobo Reserve and investigated whether food and mate availability influenced males' and females' aggression and cortisol levels, when controlling for dominance rank and the number of individuals present. We found that although females had higher aggression rates and urinary cortisol levels during than outside contexts of IGEs, these increases were not related to food availability or changes in between-group dynamics when maximally tumescent females were present, rather than absent. Furthermore, males showed higher aggression rates and urinary cortisol levels during than outside contexts of IGEs. However, males' responses during IGEs were not related to the presence of maximally tumescent females and food availability. Taken together, while competition intensified during seemingly tolerant IGEs in bonobos, such competition was unrelated to short-term changes in food and mate availability. Despite physical and physiological costs of aggression, bonobos associate with out-group individuals frequently and for extended periods. This suggests potential benefits of bonobo intergroup associations.

Stefano Lucchesi, Leveda Cheng, Tobias Deschner, Roger Mundry, Erin G Wessling, and Martin Surbeck. 2021. “Better together? How intergroup associations affect energy balance and feeding behavior in wild bonobos.” Behavioral Ecology and Sociobiology, 75, 1, Pp. 1-17. Publisher's VersionAbstract
When the benefits of interacting with out-group members exceed the associated costs, social groups may be expected to be tolerant towards each other. However, in many species exhibiting intergroup tolerance, the nature of benefits gained from intergroup encounters remains unclear. We investigated the potential costs and benefits associated with intergroup associations in bonobos, a species with varying degrees of intergroup tolerance, by testing whether these associations conferred energetic benefits to participants under different socioecological contexts and whether the consequences of these associations substantially differed from within-group competition. We used measures of socioecological factors (fruit abundance and group size), feeding and ranging behaviors, and a physiological marker of energy balance (urinary c-peptide of insulin) collected over a 19-month period from two neighboring wild communities in the Kokolopori Bonobo Reserve, Democratic Republic of the Congo. We found that intergroup associations were not related to individuals’ energy balance, but they were related to variations in individuals’ ranging and feeding behavior. Specifically, bonobos traveled longer distances, visited larger fruit patches, and increased the time spent feeding on fruits on days they associated with the neighboring group. These adaptations in feeding behavior may be strategies to offset the energetic costs of increased travel distances. In the absence of obvious energetic benefits and with clear strategies employed to offset energetic costs, it is likely that intergroup associations in bonobos provide benefits unrelated to energy acquisition, such as social benefits. Our study sheds light on the potential incentives promoting social networks to extend beyond and across groups in a tolerant species.
2020
Liran Samuni, Franziska Wegdell, and Martin Surbeck. 2020. “Behavioural diversity of bonobo prey preference as a potential cultural trait.” Edited by Detlef Weigel, Erica Van de Waal, and Erica Van de Waal. eLife, 9, Pp. e59191. Publisher's VersionAbstract
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.
Cédric Girard-Buttoz, Martin Surbeck, Liran Samuni, Patrick Tkaczynski, Christophe Boesch, Barbara Fruth, Roman M. Wittig, Gottfried Hohmann, and Catherine Crockford. 2020. “Information transfer efficiency differs in wild chimpanzees and bonobos, but not social cognition.” Proceedings of the Royal Society B: Biological Sciences, 287, 1929, Pp. 20200523. Publisher's VersionAbstract
Several theories have been generated to understand the socio-cognitive mechanisms underlying the unique cooperative abilities of humans. The ‘interdependence hypothesis' posits first, that the cognitive dimension of human cooperation evolved in contexts when several individuals needed to act together to achieve a common goal, like when hunting large prey. Second, the more interdependent individuals are, the more likely they are to provide services to conspecifics in other contexts. Alternatively, the ‘social tolerance hypothesis' proposes that higher social tolerance allows conspecifics to cooperate more efficiently and with a wider range of partners. We conducted the first field experimental evaluation of both hypotheses in our closest living relatives by contrasting chimpanzees to the less interdependent but more tolerant bonobos. We compared each species' performance during a cooperative task: informing conspecifics about a danger. We presented Gaboon viper models to 82 individuals from five wild communities. Chimpanzees arriving late at the snake were significantly more likely to have heard a call and less likely to startle, indicating that chimpanzees were better informed about the presence of the threat than bonobos. This stems from clear species differences in how individuals adjusted their calling decisions to the level of information already available. Chimpanzees were more likely to call and produced more alarm calls when they had not yet heard a call, whereas bonobos did so when they already heard a call. Our results confirm the link between interdependence and cooperation performance. These species differences were most likely driven by differences in motivation rather than in cognitive capacities because both species tended to consider audience knowledge in their decision to call. Our results inform theories on the evolution of human cooperation by linking inter-group competition pressure and in-group cooperative motivation and/or capability.

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