Lethal aggression in Pan is better explained by adaptive strategies than human impacts.

Observations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) provide valuable comparative data for understanding the significance of conspecific killing. Two kinds of hypothesis have been proposed. Lethal violence is sometimes concluded to be the result of adaptive strategies, such that killers ultimately gain fitness benefits by increasing their access to resources such as food or mates. Alternatively, it could be a non-adaptive result of human impacts, such as habitat change or food provisioning. To discriminate between these hypotheses we compiled information from 18 chimpanzee communities and 4 bonobo communities studied over five decades. Our data include 152 killings (n = 58 observed, 41 inferred, and 53 suspected killings) by chimpanzees in 15 communities and one suspected killing by bonobos. We found that males were the most frequent attackers (92% of participants) and victims (73%); most killings (66%) involved intercommunity attacks; and attackers greatly outnumbered their victims (median 8:1 ratio). Variation in killing rates was unrelated to measures of human impacts. Our results are compatible with previously proposed adaptive explanations for killing by chimpanzees, whereas the human impact hypothesis is not supported.

Social tipping points in animal societies.

Animal social groups are complex systems that are likely to exhibit tipping points-which are defined as drastic shifts in the dynamics of systems that arise from small changes in environmental conditions-yet this concept has not been carefully applied to these systems. Here, we summarize the concepts behind tipping points and describe instances in which they are likely to occur in animal societies. We also offer ways in which the study of social tipping points can open up new lines of inquiry in behavioural ecology and generate novel questions, methods, and approaches in animal behaviour and other fields, including community and ecosystem ecology. While some behaviours of living systems are hard to predict, we argue that probing tipping points across animal societies and across tiers of biological organization-populations, communities, ecosystems-may help to reveal principles that transcend traditional disciplinary boundaries.

The timing and causes of a unique chimpanzee community fission preceding Gombe's "Four-Year War".

OBJECTIVES: While permanent group fissions are documented in humans and other primate species, they are relatively rare in male philopatric primates. One of the few apparent cases occurred in 1973 in Gombe National Park, Tanzania, when a community of chimpanzees split into two separate groups, preceding the famous "Four-Year War." We tested the hypothesis that the original group was a single cohesive community that experienced permanent fission, and investigated several potential catalysts. MATERIALS AND METHODS: We calculated association, grooming, and ranging metrics from historical data and used community detection algorithms and matrix permutation tests to determine the timing, dynamics, and causes of changes in social network subgrouping structure. RESULTS: We found that the two communities indeed split from one cohesive community, albeit one with incipient subgrouping. The degree of subgrouping in grooming and association networks increased sharply in 1971 and 1972, a period characterized by a dominance struggle between three high-ranking males and unusually high male:female sex ratios. Finally, we found a relationship between post-split community membership and previous association, grooming and ranging patterns in most periods of analysis, one that became more pronounced as the fission approached. DISCUSSION: Our analysis suggests that the community began to split during a time of an unusually male-biased sex ratio and a protracted dominance struggle, and that adult males remained with those with whom they had preferentially associated prior to the split. We discuss the costs and benefits of group membership in chimpanzees and contrast these results with group fissions in humans and other taxa.

Socioecological correlates of clinical signs in two communities of wild chimpanzees (Pan troglodytes) at Gombe National Park, Tanzania.

Disease and other health hazards pose serious threats to the persistence of wild ape populations. The total chimpanzee population at Gombe National Park, Tanzania, has declined from an estimated 120 to 150 individuals in the 1960's to around 100 individuals by the end of 2013, with death associated with observable signs of disease as the leading cause of mortality. In 2004, we began a non-invasive health-monitoring program in the two habituated communities in the park (Kasekela and Mitumba) with the aim of understanding the prevalence of health issues in the population, and identifying the presence and impacts of various pathogens. Here we present prospectively collected data on clinical signs (observable changes in health) in the chimpanzees of the Kasekela (n = 81) and Mitumba (n = 32) communities over an 8-year period (2005-2012). First, we take a population approach and analyze prevalence of clinical signs in five different categories: gastrointestinal system (diarrhea), body condition (estimated weight loss), respiratory system (coughing, sneezing etc.), wounds/lameness, and dermatologic issues by year, month, and community membership. Mean monthly prevalence of each clinical sign per community varied, but typically affected <10% of observed individuals. Secondly, we analyze the presence of clinical signs in these categories as they relate to individual demographic and social factors (age, sex, and dominance rank) and simian immunodeficiency virus (SIVcpz) infection status. Adults have higher odds of being observed with diarrhea, loss of body condition, and wounds or lameness when compared to immatures, while males have a higher probability of being observed with wounds or lameness than females. In contrast, signs of respiratory illness appear not to be related to chimpanzee-specific factors and skin abnormalities are very rare. For a subset of known-rank individuals, dominance rank predicts the probability of wounding/lameness in adult males, but does not predict any adverse clinical signs in adult females. Instead, adult females with SIVcpz infection are more likely to be observed with diarrhea, a finding that warrants further investigation. Comparable data are needed from other sites to determine whether the prevalence of clinical signs we observe are relatively high or low, as well as to more fully understand the factors influencing health of wild apes at both the population and individual level. Am. J. Primatol. 80:e22562, 2018. © 2016 Wiley Periodicals, Inc.

Predation by female chimpanzees: Toward an understanding of sex differences in meat acquisition in the last common ancestor of Pan and Homo.

Among modern foraging societies, men hunt more than women, who mostly target relatively low-quality, reliable resources (i.e., plants). This difference has long been assumed to reflect human female reproductive constraints, particularly caring for and provisioning mates and offspring. Long-term studies of chimpanzees (Pan troglodytes) enable tests of hypotheses about the possible origins of human sex differences in hunting, prior to pair-bonding and regular provisioning. We studied two eastern chimpanzee communities (Kasekela, Mitumba) in Gombe, Tanzania and one (Kanyawara) in Kibale, Uganda. Relative to males, females had low hunting rates in all three communities, even where they encountered red colobus monkeys (the primary prey of chimpanzees) as often as males did. There was no evidence that clinging offspring hampered female hunting. Instead, consistent with the hypothesis that females should be more risk-averse than males, females at all three sites specialized in low-cost prey (terrestrial/sedentary prey at Gombe; black and white colobus monkeys at Kanyawara). Female dominance rank was positively correlated with red colobus hunting probability only at Kasekela, suggesting that those in good physical condition were less sensitive to the costs of possible failure. Finally, the potential for carcass appropriation by males deterred females at Kasekela (but not Kanyawara or Mitumba) from hunting in parties containing many adult males. Although chimpanzees are not direct analogs of the last common ancestor (LCA) of Pan and Homo, these results suggest that before the emergence of social obligations regarding sharing and provisioning, constraints on hunting by LCA females did not necessarily stem from maternal care. Instead, they suggest that a risk-averse foraging strategy and the potential for losing prey to males limited female predation on vertebrates. Sex differences in hunting behavior would likely have preceded the evolution of the sexual division of labor among modern humans.

Incomplete control and concessions explain mating skew in male chimpanzees.

Sexual selection theory predicts that because male reproductive success in mammals is limited by access to females, males will attempt to defend access to mates and exclude rivals from mating. In mammals, dominance rank is correlated with male reproductive success; however, the highest-ranking (alpha) male rarely monopolizes reproduction completely. To explain why, incomplete control models propose that alpha males simply cannot control other males' access to mates. If true, then dominance rank should be a key factor influencing subordinate (non-alpha) male mating success. Alternatively, the concession model states that alpha males can prevent other males from gaining access to mates but posits that they concede matings to subordinates in exchange for social favours. This predicts that a male's grooming interactions with the alpha should mediate his access to females. We test these predictions using 36 years of data, encompassing the tenures of eight alpha male chimpanzees at Gombe National Park, Tanzania. Incomplete control models were most strongly supported. At a given copulation event, the probability that the alpha was the male that mated was negatively associated with the number of males and sexually receptive females in the party. Additionally, as the number of males increased, high dominance rank was associated with an increased likelihood that a particular non-alpha male mated. The concession model, however, was also supported. The amount of time a male spent grooming with the alpha was positively associated with his likelihood of mating when the alpha was present in the party. As grooming is a major affiliative component of male social relationships, our results suggest that social bonds with dominant individuals are leveraged for mating access, particularly in species in which males form coalitions.

Reproductive state and rank influence patterns of meat consumption in wild female chimpanzees (Pan troglodytes schweinfurthii).

An increase in faunivory is a consistent component of human evolutionary models. Animal matter is energy- and nutrient-dense and can provide macronutrients, minerals, and vitamins that are limited or absent in plant foods. For female humans and other omnivorous primates, faunivory may be of particular importance during the costly periods of pregnancy and early lactation. Yet, because animal prey is often monopolizable, access to fauna among group-living primates may be mediated by social factors such as rank. Wild chimpanzees (Pan troglodytes) across Africa habitually consume insects and/or vertebrates. However, no published studies have examined patterns of female chimpanzee faunivory during pregnancy and early lactation relative to non-reproductive periods, or by females of different rank. In this study, we assessed the influence of reproductive state and dominance rank on the consumption of fauna (meat and insects) by female chimpanzees of Gombe National Park, Tanzania. Using observational data collected over 38 years, we tested (a) whether faunivory varied by reproductive state, and (b) if high-ranking females spent more time consuming fauna than lower-ranking females. In single-factor models, pregnant females consumed more meat than lactating and baseline (meaning not pregnant and not in early lactation) females, and high-ranking females consumed more meat than lower-ranking females. A two-factor analysis of a subset of well-sampled females identified an interaction between rank and reproductive state: lower-ranking females consumed more meat during pregnancy than lower-ranking lactating and baseline females did. High-ranking females did not significantly differ in meat consumption between reproductive states. We found no relationships between rank or reproductive state with insectivory. We conclude that, unlike insectivory, meat consumption by female chimpanzees is mediated by both reproductive state and social rank. We outline possible mechanisms for these patterns, relate our findings to meat-eating patterns in women from well-studied hunter-gatherer societies, and discuss potential avenues for future research.

Transparency, usability, and reproducibility: Guiding principles for improving comparative databases using primates as examples.

Recent decades have seen rapid development of new analytical methods to investigate patterns of interspecific variation. Yet these cutting-edge statistical analyses often rely on data of questionable origin, varying accuracy, and weak comparability, which seem to have reduced the reproducibility of studies. It is time to improve the transparency of comparative data while also making these improved data more widely available. We, the authors, met to discuss how transparency, usability, and reproducibility of comparative data can best be achieved. We propose four guiding principles: 1) data identification with explicit operational definitions and complete descriptions of methods; 2) inclusion of metadata that capture key characteristics of the data, such as sample size, geographic coordinates, and nutrient availability (for example, captive versus wild animals); 3) documentation of the original reference for each datum; and 4) facilitation of effective interactions with the data via user friendly and transparent interfaces. We urge reviewers, editors, publishers, database developers and users, funding agencies, researchers publishing their primary data, and those performing comparative analyses to embrace these standards to increase the transparency, usability, and reproducibility of comparative studies.

Cheating monkeys undermine group strength in enemy territory.

In many social animals, group-mates cooperate to defend their range against intrusion by neighboring groups. Because group size tends to be highly variable, such conflicts are often asymmetric. Although numerical superiority is assumed to provide a competitive advantage, small groups can generally defend their ranges, even when greatly outnumbered. The prevailing explanation for this puzzling phenomenon is that individuals in relatively large groups experience a greater temptation to flee from conflicts, in effect leveling the balance of power. Using playback experiments simulating territorial intrusions by wild capuchin monkey (Cebus capucinus) groups, we show that such a collective action problem does indeed undermine the competitive ability of large groups. Focal capuchins were more likely to run away from territorial intrusions when their group had a numeric advantage; each one-individual increase in relative group size raised the odds of flight by 25%. However, interaction location had a more important impact on individuals' reactions, creating a strong home-field advantage. After controlling for relative group size, the odds that a focal animal fled were 91% lower in experiments that occurred in the center compared with on the edge of its group's range, whereas the odds that it rushed toward the speaker were more than sixfold higher. These location-dependent patterns of defection and cooperation create a competitive advantage for residents over intruders across a wide range of relative group sizes, which may stabilize range boundaries and provide a general explanation for how groups of widely divergent sizes can coexist, even in the face of intense intergroup competition.

Why do chimpanzees hunt? Considering the benefits and costs of acquiring and consuming vertebrate versus invertebrate prey.

Understanding the benefits and costs of acquiring and consuming different forms of animal matter by primates is critical for identifying the selective pressures responsible for increased meat consumption in the hominin lineage. Chimpanzees (Pan troglodytes) are unusual among primates in the amount of vertebrate prey they consume. Still, surprisingly little is known about the nutritional benefits of eating meat for this species. In order to understand why chimpanzees eat vertebrates, it is critical to consider the relative benefits and costs of other types of faunivory - including invertebrates. Although we lack specific nutritional data on the flesh and organs of chimpanzee prey, the macronutrient profiles of insects and wild vertebrate meat are generally comparable on a gram-to-gram basis. There are currently very few data on the micronutrient (vitamin and mineral) content of meat consumed by chimpanzees. With few exceptions, the advantages of hunting vertebrate prey include year-round availability, rapid acquisition of larger packages and reduced handling/processing time (once prey are encountered or detected). The disadvantages of hunting vertebrate prey include high potential acquisition costs per unit time (energy expenditure and risk of injury) and greater contest competition with conspecifics. Acquiring an equivalent mass of invertebrates (to match even a small scrap of meat) is possible, but typically takes more time. Furthermore, in contrast to vertebrate prey, some insect resources are effectively available only at certain times of the year. Here we identify the critical data needed to test our hypothesis that meat scraps may have a higher (or at least comparable) net benefit:cost ratio than insect prey. This would support the 'meat scrap' hypothesis as an explanation for why chimpanzees hunt in groups even when doing so does not maximize an individual's energetic gain.

Personality traits, rank attainment, and siring success throughout the lives of male chimpanzees of Gombe National Park.

Personality traits in many taxa correlate with fitness. Several models have been developed to try to explain how variation in these traits is maintained. One model proposes that variation persists because it is linked to trade-offs between current and future adaptive benefits. Tests of this model's predictions, however, are scant in long-lived species. To test this model, we studied male chimpanzees living in Gombe National Park, Tanzania. We operationalized six personality traits using ratings on 19 items. We used 37 years of behavioral and genetic data to assemble (1) daily rank scores generated from submissive vocalizations and (2) records of male siring success. We tested whether the association between two personality traits, Dominance and Conscientiousness, and either rank or reproductive success, varied over the life course. Higher Dominance and lower Conscientiousness were associated with higher rank, but the size and direction of these relationships did not vary over the life course. In addition, independent of rank at the time of siring, higher Dominance and lower Conscientiousness were related to higher siring success. Again, the size and direction of these relationships did not vary over the life course. The trade-off model, therefore, may not hold in long-lived and/or slowly reproducing species. These findings also demonstrate that ratings are a valid way to measure animal personality; they are related to rank and reproductive success. These traits could therefore be used to test alternative models, including one that posits that personality variation is maintained by environmental heterogeneity, in studies of multiple chimpanzee communities.

Reproductive inequality among males in the genus Pan.

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. This article is part of the theme issue 'Evolutionary ecology of inequality'.

Correlates of individual participation in boundary patrols by male chimpanzees.

Group territory defence poses a collective action problem: individuals can free-ride, benefiting without paying the costs. Individual heterogeneity has been proposed to solve such problems, as individuals high in reproductive success, rank, fighting ability or motivation may benefit from defending territories even if others free-ride. To test this hypothesis, we analysed 30 years of data from chimpanzees (Pan troglodytes) in the Kasekela community, Gombe National Park, Tanzania (1978-2007). We examined the extent to which individual participation in patrols varied according to correlates of reproductive success (mating rate, rank, age), fighting ability (hunting), motivation (scores from personality ratings), costs of defecting (the number of adult males in the community) and gregariousness (sighting frequency). By contrast to expectations from collective action theory, males participated in patrols at consistently high rates (mean ± s.d. = 74.5 ± 11.1% of patrols, n = 23 males). The best predictors of patrol participation were sighting frequency, age and hunting participation. Current and former alpha males did not participate at a higher rate than males that never achieved alpha status. These findings suggest that the temptation to free-ride is low, and that a mutualistic mechanism such as group augmentation may better explain individual participation in group territorial behaviour. This article is part of the theme issue 'Intergroup conflict across taxa'.

Vocal signals facilitate cooperative hunting in wild chimpanzees.

Cooperation and communication likely coevolved in humans. However, the evolutionary roots of this interdependence remain unclear. We address this issue by investigating the role of vocal signals in facilitating a group cooperative behavior in an ape species: hunting in wild chimpanzees. First, we show that bark vocalizations produced before hunt initiation are reliable signals of behavioral motivation, with barkers being most likely to participate in the hunt. Next, we find that barks are associated with greater hunter recruitment and more effective hunting, with shorter latencies to hunting initiation and prey capture. Our results indicate that the coevolutionary relationship between vocal communication and group-level cooperation is not unique to humans in the ape lineage and is likely to have been present in our last common ancestor with chimpanzees.

Adult male chimpanzees inherit maternal ranging patterns.

Space use often correlates with reproductive success [1, 2]. Individual site fidelity is ubiquitous across a variety of taxa, including birds, mammals, insects, and reptiles [3-9]. Individuals can benefit from using the same area because doing so affords access to known resources, including food and/or breeding sites. The majority of studies on site fidelity have focused upon strictly territorial species in which individuals range in well-defined, exclusive areas (e.g., [4, 9]). By comparison, the transient groups that define fission-fusion species allow for considerable flexibility in individual space use. Although there is evidence that individual space use can influence reproductive success [2], relatively little is known about individual ranging patterns in fission-fusion species. Here, we investigate three potential correlates of male site fidelity (age, habitat quality, and maternal space use) in wild chimpanzees (Pan troglodytes). We found that when alone, each male preferentially concentrated his space use near the area where his mother ranged when he was dependent. We suggest that solitary ranging allows males to avoid direct competition with conspecifics and that foraging in familiar areas maximizes foraging efficiency. These results highlight the importance of male foraging strategies in a species in which male ranging is typically explained in terms of mating access to females.

Interaction location outweighs the competitive advantage of numerical superiority in Cebus capucinus intergroup contests.

Numerical superiority confers a competitive advantage during contests among animal groups, shaping patterns of resource access, and, by extension, fitness. However, relative group size does not always determine the winner of intergroup contests. Smaller, presumably weaker social groups often defeat their larger neighbors, but how and when they are able to do so remains poorly understood. Models of competition between individuals suggest that location may influence contest outcome. However, because of the logistical difficulties of studying intergroup interactions, previous studies have been unable to determine how contest location and group size interact to shape relationships among groups. We address this question by using an automated radio telemetry system to study intergroup interactions among six capuchin monkey (Cebus capucinus) social groups of varying sizes. We find that the odds of winning increase with relative group size; one additional group member increases the odds of winning an interaction by 10%. However, this effect is not uniform across space; with each 100 m that a group moves away from the center of its home range, its odds of winning an interaction decrease by 31%. We demonstrate that contest outcome depends on an interaction between group size and location, such that small groups can defeat much larger groups near the center of their home range. The tendency of resident groups to win contests may help explain how small groups persist in areas with intense intergroup competition.

Social bonds provide multiple pathways to reproductive success in wild male chimpanzees.

In most male mammals, fitness is strongly shaped by competitive access to mates, a non-shareable resource. How, then, did selection favor the evolution of cooperative social bonds? We used behavioral and genetic data on wild chimpanzees (Pan troglodytes schweinfurthii) in Gombe National Park, Tanzania, to study the mechanisms by which male-male social bonds increase reproductive success. Social bonds increased fitness in several ways: first, subordinate males that formed strong bonds with the alpha male had higher siring success. Independently, males with larger networks of strong bonds had higher siring success. In the short term, bonds predicted coalition formation and centrality in the coalition network, suggesting that males benefit from being potential allies to numerous male rivals. In the long term, male ties influenced fitness via improved dominance rank for males that attain alpha status. Together, these results suggest that male bonds evolved in chimpanzees by affording both short- and long-term pathways to reproductive success.

Urine as a high-quality source of host genomic DNA from wild populations.

The ability to generate genomic data from wild animal populations has the potential to give unprecedented insight into the population history and dynamics of species in their natural habitats. However, for many species, it is impossible legally, ethically or logistically to obtain tissue samples of quality sufficient for genomic analyses. In this study we evaluate the success of multiple sources of genetic material (faeces, urine, dentin and dental calculus) and several capture methods (shotgun, whole-genome, exome) in generating genome-scale data in wild eastern chimpanzees (Pan troglodytes schweinfurthii) from Gombe National Park, Tanzania. We found that urine harbours significantly more host DNA than other sources, leading to broader and deeper coverage across the genome. Urine also exhibited a lower rate of allelic dropout. We found exome sequencing to be far more successful than both shotgun sequencing and whole-genome capture at generating usable data from low-quality samples such as faeces and dental calculus. These results highlight urine as a promising and untapped source of DNA that can be noninvasively collected from wild populations of many species.

Gregariousness is associated with parasite species richness in a community of wild chimpanzees.

Increased risk of pathogen transmission through proximity and contact is a well-documented cost of sociality. Affiliative social contact, however, is an integral part of primate group life and can benefit health. Despite its importance to the evolution and maintenance of sociality, the tradeoff between costs and benefits of social contact for group-living primate species remains poorly understood. To improve our understanding of this interplay, we used social network analysis to investigate whether contact via association in the same space and/or physical contact measured through grooming were associated with helminth parasite species richness in a community of wild chimpanzees (Pan troglodytes schweinfurthii). We identified parasite taxa in 381 fecal samples from 36 individuals from the Kasekela community of chimpanzees in Gombe National Park, Tanzania, from November 1, 2006 - October 31, 2012. Over the study period, eight environmentally transmitted helminth taxa were identified. We quantified three network metrics for association and grooming contact, including degree strength, betweenness, and closeness. Our findings suggest that more gregarious individuals - those who spent more time with more individuals in the same space - had higher parasite richness, while the connections in the grooming network were not related to parasite richness. The expected parasite richness in individuals increased by 1.13 taxa (CI: 1.04, 1.22; p = 0.02) per one standard deviation increase in degree strength of association contact. The results of this study add to the understanding of the role that different types of social contact plays in the parasite richness of group-living social primates.

No evidence of short-term exchange of meat for sex among chimpanzees.

The meat-for-sex hypothesis posits that male chimpanzees (Pan troglodytes) trade meat with estrous females in exchange for short-term mating access. This notion is widely cited in the anthropological literature and has been used to construct scenarios about human evolution. Here we review the theoretical and empirical basis for the meat-for-sex hypothesis. We argue that chimpanzee behavioral ecology does not favor the evolution of such exchanges because 1) female chimpanzees show low mate selectivity and require little or no material incentive to mate, violating existing models of commodity exchange; and 2) meat-for-sex exchanges are unlikely to provide reproductive benefits to either partner. We also present new analyses of 28 years of data from two East African chimpanzee study sites (Gombe National Park, Tanzania; Kanyawara, Kibale National Park, Uganda) and discuss the results of previously published studies. In at least three chimpanzee communities, 1) the presence of sexually receptive females did not increase hunting probability, 2) males did not share preferentially with sexually receptive females, and 3) sharing with females did not increase a male's short-term mating success. We acknowledge that systematic meat sharing by male chimpanzees in expectation of, or in return for, immediate copulations might be discovered in future studies. However, current data indicate that such exchanges are so rare, and so different in nature from exchanges among humans, that with respect to chimpanzees, sexual bartering in humans should be regarded as a derived trait with no known antecedents in the behavior of wild chimpanzees.