Failure to account for behavioral variability significantly compromises accuracy in indirect population monitoring (advance online)

Abstract 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

Mothers stick together: how the death of an infant affects female social relationships in a group of wild bonobos (Pan paniscus)

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

The eco-evolutionary landscape of power relationships between males and females

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

Tool use behavior in three wild bonobo communities at Kokolopori

Abstract 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

Variable use of polyadic grooming and its effect on access to social partners in wild chimpanzees and bonobos

In mammals, allogrooming is prominent in forming and maintaining social and cooperative relationships. Yet an animal's social time is constrained, which may limit its access to a large number of partners. Dunbar (1993, Behavioral and Brain Sciences, 16 (4), 681–694) proposed that human polyadic conversations, which allow access to several social partners simultaneously, evolved as a form of social grooming to circumvent this time constraint. In nonhuman primates, polyadic grooming (PG), in contrast to dyadic grooming, may similarly be a time-efficient way to maintain weak social relationships with many partners which can be important for group level cooperation. It remains unknown whether PG is used to fulfil specific cooperative needs by accessing numerous weakly bonded partners and increasing the number of partners accessed per unit of time. We compared the use and effect of PG between chimpanzees, Pan troglodytes, which are highly territorial and collaborative (especially males), and bonobos, Pan paniscus, which are less territorial and collaborative and in which females are the main co-operators. We carried out focal grooming observations in one bonobo and two chimpanzee communities in the wild. As predicted, chimpanzees engaged in more PG than bonobos. Surprisingly, males engaged in PG more than females in both species. While chimpanzees accessed more partners per minute of grooming than bonobos via dyadic grooming, PG increased the number of partners accessed per minute only in bonobos. Finally, chimpanzees primarily used PG with individuals who were close in rank and frequent grooming partners, whereas bonobos used PG with individuals who were distant in rank, close party associates and frequent grooming partners. We suggest that bonobo males use PG to enhance conspecific social tolerance and mate choice. The overall higher rate of PG in chimpanzees suggests that between-group competition may promote polyadic affiliation, which possibly reinforces group cohesion and coordination. © 2020 The Author

Methodological considerations in the analysis of fecal glucocorticoid metabolites in tufted capuchins (Cebus apella)

Analysis of fecal glucocorticoid (GC) metabolites has recently become the standard method to monitor adrenocortical activity in primates noninvasively. However, given variation in the production, metabolism, and excretion of GCs across species and even between sexes, there are no standard methods that are universally applicable. In particular, it is important to validate assays intended to measure GC production, test extraction and storage procedures, and consider the time course of GC metabolite excretion relative to the production and circulation of the native hormones. This study examines these four methodological aspects of fecal GC metabolite analysis in tufted capuchins (Cebus apella). Specifically, we conducted an adrenocorticotrophic hormone (ACTH) challenge on one male and one female capuchin to test the validity of four GC enzyme immunoassays (EIAs) and document the time course characterizing GC me- tabolite excretion in this species. In addition, we compare a common field-friendly technique for extracting fecal GC metabolites to an established laboratory extraction methodology and test for effects of storing “field extracts” for up to 1 yr. Results suggest that a corticosterone EIA is most sensitive to changes in GC production, provides reliable measures when extracted according to the field method, and measures GC metabolites which remain highly stable after even 12 mo of storage. Further, the time course of GC metabolite excretion is shorter than that described yet for any primate taxa. These results provide guidelines for studies of GCs in tufted capuchins, and underscore the importance of validating methods for fecal hormone analysis for each species of interest