Bonding, biophilia, biosynergy, and the future of primates in the wild

Human and nonhuman primates bond with one another in countless ways, and the results are varied and vital to the individuals and species involved. The manifesto that is the basis for the collection of essays in which this commentary is included proposes that the "human/nonhuman bonds that arise in primatological research and practice deserve and demand study and research." An essential corollary of this proposal is that the primatologists themselves must be studied. The aim of this essay is to explore the influence of human/nonhuman primate bonding on conservation practice and on the future of primates in the wild. This commentary applies the author's professional experience as a conservation psychologist and his research on the impact of profound interspecies bonds on human worldviews, attitudes, and behavior. It examines two general categories of bonds: those driven by Biophilia (human fascination with life) and those influenced by Biosynergy (mutual enrichment of life). It is the author's premise that biosynergy promotes complex collaborative interspecies bonds that broaden the conservationist's desire to enhance synergy among all organisms in an ecosystem. Conversely, biophilia induces relatively simple unidirectional bonds between humans and other animals that deepen the conservationist's desire to understand and protect certain species. This contrast raises some crucial questions. Do biophilia-driven bonds between conservationists and their favorite primates blind them to the synergistic needs of all species and impair their ability to work for sustained preservation of threatened habitat? Does biosynergy-based human/nature bonding enhance focus on conservation as an ecological science and thus ignore species-specific factors crucial to assure survival of endangered primates? How can both types of bonds be optimally applied to the conservation of wildlife and wilderness?     

Nutritional Characteristics of Wild and Cultivated Foods for Chimpanzees (<Emphasis Type="Italic">Pan troglodytes</Emphasis>) in Agricultural Landscapes

Primate habitats are being transformed by human activities such as agriculture. Many wild primates include cultivated foods (crops) in their diets, calling for an improved understanding of the costs and benefits of crop feeding. We measured the macronutrient and antifeedant content of 44 wild and 21 crop foods eaten by chimpanzees (Pan troglodytes schweinfurthii) in a mosaic habitat at Bulindi, Uganda, to evaluate the common assertion that crops offer high nutritional returns compared to wild forage for primates. In addition, we analyzed 13 crops not eaten at Bulindi but that are consumed by chimpanzees elsewhere to assess whether nutritional aspects explain why chimpanzees in Bulindi ignored them. Our analysis of their wild plant diet (fruit, leaves, and pith) corresponds with previous chemical analyses of primate plant foods. Compared to wild food equivalents, crops eaten by the chimpanzees contained higher levels of digestible carbohydrates (mainly sugars) coupled with lower amounts of insoluble fiber and antifeedants. Cultivated fruits were relatively nutritious throughout the ripening process. Our data support the assumption that eating cultivated foods confers energetic advantages for primates, although crops in our sample were low in protein and lipids compared to some wild foods. We found little evidence that crops ignored by the chimpanzees were less nutritious than those that they did eat. Nonnutritional factors, e.g., similarity to wild foods, probably also influence crop selection. Whether cultivated habitats can support threatened but flexible primates such as chimpanzees in the long term hinges on local people’s willingness to share their landscape and resources with them.     

Vocal responsiveness in male wild chimpanzees: implications for the evolution of language

Several captive chimpanzees and bonobos have learned to use symbols and to comprehend syntax. Thus, compared with other nonhumans, these animals appear to have unusual cognitive powers that can be recruited for communicative behavior. This raises the possibility that wild chimpanzee vocal communication is more complex than heretofore demonstrated. To examine this possibility, I investigated whether wild chimpanzee vocal exchanges exhibit uniquely human conversational attributes. The results indicate that wild chimpanzees vocalize at low rates, tend not to respond to calls that they hear, and, when they do respond, tend to give calls that are similar to the ones they have heard. Thus, chimpanzee vocal interactions resemble those of other primate species, and show no special similarity to human conversations. The results support the view that we need to explore cognitive and social continuities and discontinuities with nonhuman primates to understand the origin and evolution of language, but also emphasize the need for fine-grained analyses of wild chimpanzee vocal interactions.     

Percussive technology in human evolution: an introduction to a comparative approach in fossil and living primates

Percussive technology is part of the behavioural suite of several fossil and living primates. Stone Age ancestors used lithic artefacts in pounding activities, which could have been most important in the earliest stages of stone working. This has relevant evolutionary implications, as other primates such as chimpanzees and some monkeys use stone hammer-and-anvil combinations to crack hard-shelled foodstuffs. Parallels between primate percussive technologies and early archaeological sites need to be further explored in order to assess the emergence of technological behaviour in our evolutionary line, and firmly establish bridges between Primatology and Archaeology. What are the anatomical, cognitive and ecological constraints of percussive technology? How common are percussive activities in the Stone Age and among living primates? What is their functional significance? How similar are archaeological percussive tools and those made by non-human primates? This issue of Phil. Trans. addresses some of these questions by presenting case studies with a wide chronological, geographical and disciplinary coverage. The studies presented here cover studies of Brazilian capuchins, captive chimpanzees and chimpanzees in the wild, research on the use of percussive technology among modern humans and recent hunter–gatherers in Australia, the Near East and Europe, and archaeological examples of this behaviour from a million years ago to the Holocene. In summary, the breadth and depth of research compiled here should make this issue of Philosophical Transactions of the Royal Society B, a landmark step forward towards a better understanding of percussive technology, a unique behaviour shared by some modern and fossil primates.     

How can social network analysis improve the study of primate behavior?

When living in a group, individuals have to make trade-offs, and compromise, in order to balance the advantages and disadvantages of group life. Strategies that enable individuals to achieve this typically affect inter-individual interactions resulting in nonrandom associations. Studying the patterns of this assortativity using social network analyses can allow us to explore how individual behavior influences what happens at the group, or population level. Understanding the consequences of these interactions at multiple scales may allow us to better understand the fitness implications for individuals. Social network analyses offer the tools to achieve this. This special issue aims to highlight the benefits of social network analysis for the study of primate behaviour, assessing it's suitability for analyzing individual social characteristics as well as group/population patterns. In this introduction to the special issue, we first introduce social network theory, then demonstrate with examples how social networks can influence individual and collective behaviors, and finally conclude with some outstanding questions for future primatological research.     

Intelligence, Coalitional Killing, and the Antecedents of War

Advances in primatological research have recently led to a hypothesis that lethal coalitionary raiding in chimpanzees is the product of an evolutionarily adaptive "dominance drive" that disposes adult males to seek out low-cost opportunities for conspecific killing. This conclusion has been extended into a claim that human warfare and other forms of coalitional killing are outcomes of a hardwired, "demonic male" complex. Reversing this evidential approach, I argue from data on conspecific killing in humans that humans and chimpanzees have an aversion to killing conspecifics. Their lethal violence, I propose, is more parsimoniously explained as the result of a developed intelligence capable of envisioning the future and, when necessary, of disabling this aversion to achieve desired goals.     

Essay on Contemporary Issues in Ethology: Variation among Mammalian Alarm Call Systems and the Problem of Meaning in Animal Signals

Understanding the information conveyed by animal signals requires studies of both production and perception. It is important to determine the relationship between signal morphology and the circumstances of production, the way signaller behavior varies with motivational state and the role of context in mediating responses to signals. Alarm calls are well-suited to research of this type because they are widespread in birds and mammals and typically evoke unambiguous responses. We review studies of alarm calling in primates and ground-dwelling sciurid rodents, concentrating especially on whether these signal systems may be viewed as ‘functionally referential’, that is, as conveying sufficient information about an event for receivers to select appropriate responses. Comparisons of the physical, behavioral and habitat characteristics of these species suggest that incompatibility of the escape responses required to avoid different classes of predators may have been an important factor in the evolution of functionally referential alarm calls.     

Evolution of nuclear gene families in primates,Copy-number variation in the argininosuccinate synthetase (ASS) pseudogene family and the anonymous DNA sequence,D1S1

Changes in the copy number of nuclear genes provide the raw material for the creation of new gene functions. To better understand the mechanisms for such events, and their physiologic and evolutionary consequences, it is valuable to study a well characterized and closely related group of species such as primates. Fortuitously, most of the powerful molecular techniques and DNA probes developed for research in humans are equally applicable to non-human primates. We review what is known of copy number variation in primates and describe two informative DNA probes: pAS-1, a cDNA probe to the human urea cycle enzyme argininosuccinate synthetase (ASS), and an anonymous DNA probe, D1S1.In additon to the ASS structural locus on human chromosome 9, pAS-1 detects at least 14 dispersed, processed pseudogenes in humans. The number of pseudogene copies appears to be approximately the same in humans, chimpanzees, gorillas, orangutans and baboons; less in marmosets; and least in some rodents. Chimpanzees and gorillas appear to have all of the human pseudogenes though an Xp copy may be missing from gorillas. The Y pseudogene is apparently absent from orangutans and baboons, and, finally, a comparison of humans and chimpanzees revealed that the number of nucleotide substitutions in the Y chromosome pseudogenes is approximately 1 per 100.D1S1 maps to human chromosome 3 but also detects a high homology copy on chromosome 1. Chimpanzees, gorillas and orangutans all appear to have only the chromosome 3 homolog suggesting that this is the ancestral sequence and that the duplication occurred after separation of humans and the great apes.Both the ASS pseudogene family and the D1S1 system provide valuable information on the evolution of nuclear gene families in primates.     

Surviving at the extreme: Chimpanzee ranging is not restricted in a deforested human‐dominated landscape in Uganda

Endangered wildlife increasingly inhabits human‐dominated landscapes outside protected areas. Large‐bodied mammals require large spaces, and their ranging may be especially impacted by landscape modifications including farming, road development and urbanisation. We studied the Wagaisa community of chimpanzees (Pan troglodytes) in Uganda, which inhabit a landscape characterised by high human population density, widespread deforestation, and rapid agricultural and infrastructural development. We aimed to assess whether this dynamic, fragmented environment constrains the chimpanzees’ ranging, and to identify critical habitat patches to aid their conservation. During March–May 2018, we assessed range use from locations of direct observations and indirect signs, corroborated by longer‐term behavioural monitoring of the chimpanzees (June 2018–December 2019). No evidence of limited ranging was found. The Wagaisa chimpanzees used an area measuring ≥ 43 km² (100% MCP) and ranged extensively in the anthropogenic matrix. Most frequently used parts of the range (‘core habitat areas’) centred around small (5–20 acres), widely dispersed remnant forest patches and exotic eucalyptus plantations. Forty per cent of chimpanzee nests were constructed in eucalyptus trees, suggesting a behavioural adjustment to landscape changes. Actions to facilitate conservation of these ‘village chimpanzees’ and others surviving in transformed human‐dominated habitat need not conflict with the sustainable development of the region.     

Cerebral venous hemodynamics and the basicranium of Cebus

The study of basicranial foramina has played an important role in primatological investigations. They are often the only clues for deciphering cerebral vascular evolution in fossil forms. This study illustrates the significance of considering foraminal shape when analyzing or describing basicranial anatomy in living and fossil primates. It is suggested that certain hemodynamic properties of cerebral venous drainage in Cebus represent patterns that were most likely present in ancestral catarrhines.     

On the Meaning of Alarm Calls: A Review of Functional Reference in Avian Alarm Calling

A long‐standing question in animal communication is whether signals reveal intrinsic properties of the signaller or extrinsic properties of its environment. Alarm calls, one of the most conspicuous components of antipredator behaviour, intuitively would appear to reflect internal states of the signaller. Pioneering research in primates and fowl, however, demonstrated that signallers may produce unique alarm calls during encounters with different types of predators, suggesting that signallers through selective production of alarm calls provide to conspecific receivers information about predators in the environment. In this article, we review evidence for such ‘functional reference’ in the alarm calls of birds based on explicit tests of two criteria proposed in Macedonia & Evans’ (Ethology 93, 1993, 177) influential conceptual framework: (1) that unique alarm calls are given to specific predator categories, and (2) that alarm calls isolated from contextual information elicit antipredator responses from receivers similar to those produced during actual predator encounters. Despite the importance of research on birds in development of the conceptual framework and the ubiquity of alarm calls in birds, evidence for functionally referential alarm calls in this clade is limited to six species. In these species, alarm calls are associated with the type of predator encountered as well as variation in hunting behaviour; with defence of reproductive effort in addition to predators of adults; with age‐related changes in predation risk; and with strong fitness benefits. Our review likely underestimates the occurrence of functional reference in avian alarm calls, as incomplete application and testing of the conceptual framework has limited our understanding. Throughout, therefore, we suggest avian taxa for future studies, as well as additional questions and experimental approaches that would strengthen our understanding of the meaning of functional reference in avian alarm calls.     

Welfare based primate rehabilitation as a potential conservation strategy: does it measure up?

Many primate species are threatened with extinction and are the focus of extensive conservation efforts including re-introduction, captive breeding and habitat conservation. Welfare-based rehabilitation (hereafter also ‘rehabilitation’) is a management strategy commonly used for primates, particularly those species targeted by the pet and bush meat trades. Rehabilitation of rescued primates typically has the dual motivation of welfare and conservation, but has not been assessed as a conservation strategy. As the species involved in rehabilitation are often endangered (e.g. chimpanzees, gorillas, orang-utans), it is important for rehabilitation projects to follow a ‘best practice’ model in order to increase positive outcomes. In this study, we compared the approaches of 28 welfare-based primate rehabilitation projects to the ‘IUCN guidelines for nonhuman primate re-introductions’, in addition to components of the ‘Best practice guidelines for the re-introduction of great apes’ in order to assess where additional work might be needed for released animals to contribute to conservation outcomes. Few projects examined complied with the guidelines for re-introduction, failing to incorporate important factors such as quarantine, long term post-release monitoring and training for predator awareness. Further development of species-specific rehabilitation guidelines may improve the outcomes of future rehabilitation projects. To support this, we recommend that detailed methods and results be published for all rehabilitation efforts, regardless of the outcome.     

Troublesome neighbours: Changing attitudes towards chimpanzees (Pan troglodytes) in a human-dominated landscape in Uganda

Long-term human–wildlife sympatry depends on the willingness and capacity of local people to coexist with wild animals. With human population growth and deforestation for agriculture, farmers increasingly live in proximity to wildlife, including large mammals of conservation concern. Understanding local perspectives and concerns regarding wildlife is essential for informing appropriate management strategies that reduce conflicts and promote sustainable coexistence. Social science approaches therefore have a critical role in integrated conservation programmes. We undertook an attitude survey to understand residents’ perspectives about sharing a landscape with chimpanzees (Pan troglodytes) in an unprotected forest–agriculture mosaic in Uganda. Interviews (n = 134) in 12 villages demonstrate residents’ ambivalence towards living alongside these protected yet potentially troublesome mammals. Chimpanzee behaviour is reported to have undergone recent changes. Residents claim apes increasingly enter villages for food, threaten people, and pose a particular threat to children's safety. Chimpanzee numbers are believed to have increased locally. Most interviewees fear chimpanzees, considering them dangerous. Crop losses to chimpanzees were widely reported. Farmers tolerate raiding of domestic fruits, but not cash-crops. Results demonstrate that attitudes towards wildlife are not fixed. Reported changes to chimpanzee behaviour are challenging villagers’ traditionally benign attitude towards them. Even so, residents acknowledge benefits to chimpanzees because they reportedly displace other crop-raiding wildlife which, unlike chimpanzees, damage important staple food crops. Survey findings are contextualised with respect to recent, major land-use changes in Uganda (clearance of unprotected forest for timber and agriculture) that have precipitated a sharp rise in farmer–chimpanzee interactions. We discuss the study's broader implications for protected mammal management and conflict mitigation in human-dominated landscapes, and ask whether it is appropriate to expect impoverished rural farmers to accommodate large-bodied mammals that pose a potential threat to their safety and livelihoods.     

The role of taste in food selection by African apes: implications for niche separation and overlap in tropical forests

Ripe fruit eating shapes the behavior of most of the apes. Gorillas (Gorilla gorilla) and chimpanzees (Pan troglodytes) are very different sizes and, consequently, have been traditionally viewed as ecologically distinct, but few studies have explored the behavioral and physiological foundations of their diets. Debate continues on the extent that large-bodied gorillas may be less selective and more opportunistic fruit eaters than chimpanzees. Taste responses have been predicted to relate to body size and digestive strategies. This study employs laboratory research on taste perception and discrimination among captive zoo-housed chimpanzees and relates it to previous work on gorillas to better characterize diets and niche separation among these apes. During the captive trials, differences were recorded in consumption patterns of water and varying concentrations of dilute aqueous fructose (sweet) and tannic acid solutions (astringent), compounds commonly found in wild foods. The chimpanzees exhibited similar preference thresholds for fructose (50 mM) to other primates studied. They exhibited slightly lower inhibition thresholds for tannic acid solutions than gorillas, but higher than smaller primates studied to date. These preliminary findings suggest that tannin tolerance may well be mediated by body size, though possible species differences in salivary proteins or other sensory differences remain to be explored. This research furthers our efforts to understand the roles of body size and physiological adaptations in shaping diet and niche separation of chimpanzees and gorillas.     

Hunting behavior of wild chimpanzees in the Taï National Park

Hunting is often considered one of the major behaviors that shaped early hominids' evolution, along with the shift toward a drier and more open habitat. We suggest that a precise comparison of the hunting behavior of a species closely related to man might help us understand which aspects of hunting could be affected by environmental conditions. The hunting behavior of wild chimpanzees is discussed, and new observations on a population living in the tropical rain forest of the Taï National Park, Ivory Coast, are presented. Some of the forest chimpanzees' hunting performances are similar to those of savanna-woodlands populations; others are different. Forest chimpanzees have a more specialized prey image, intentionally search for more adult prey, and hunt in larger groups and with a more elaborate cooperative level than savanna-woodlands chimpanzees. In addition, forest chimpanzees tend to share meat more actively and more frequently. These findings are related to some theories on aspects of hunting behavior in early hominids and discussed in order to understand some factors influencing the hunting behavior of wild chimpanzees. Finally, the hunting behavior of primates is compared with that of social carnivores.     

Neuroendocrine control in social relationships in non-human primates: Field based evidence

Primates maintain a variety of social relationships and these can have fitness consequences. Research has established that different types of social relationships are unpinned by different or interacting hormonal systems, for example, the neuropeptide oxytocin influences social bonding, the steroid hormone testosterone influences dominance relationships, and paternal care is characterized by high oxytocin and low testosterone. Although the oxytocinergic system influences social bonding, it can support different types of social bonds in different species, whether pair bonds, parent-offspring bonds or friendships. It seems that selection processes shape social and mating systems and their interactions with neuroendocrine pathways. Within species, there are individual differences in the development of the neuroendocrine system: the social environment individuals are exposed to during ontogeny alters their neuroendocrine and socio-cognitive development, and later, their social interactions as adults. Within individuals, neuroendocrine systems can also have short-term effects, impacting on social interactions, such as those during hunting, intergroup encounters or food sharing, or the likelihood of cooperating, winning or losing. To understand these highly dynamic processes, extending research beyond animals in laboratory settings to wild animals living within their natural social and ecological setting may bring insights that are otherwise unreachable. Field endocrinology with neuropeptides is still emerging. We review the current status of this research, informed by laboratory studies, and identify questions particularly suited to future field studies. We focus on primate social relationships, specifically social bonds (mother-offspring, father-offspring, cooperative breeders, pair bonds and adult platonic friendships), dominance, cooperation and in-group/out-group relationships, and examine evidence with respect to the ‘tend and defend’ hypothesis.     

Chimpanzee social intelligence: selfishness,altruism, and the mother–infant bond

To better understand the human mind from an evolutionary perspective, a great deal of research has focused on the closest living relative of humans, the chimpanzee, using various approaches, including studies of social intelligence. Here, I review recent research related to several aspects of social intelligence, including deception, understanding of perception and intention, social learning, trading, cooperation, and regard for others. Many studies have demonstrated that chimpanzees are proficient in using their social intelligence for selfish motives to benefit from their interactions with others. In contrast, it is not yet clear whether chimpanzees engage in prosocial behaviors that benefit others; however, chimpanzee mother–infant interactions indicate the possibility of such behaviors. Therefore, I propose that chimpanzees possess rudimentary traits of human mental competence not only in terms of theory of mind in a broader sense but also in terms of prosociality involving regard for others. Mother–infant interactions appear to be particularly important to understanding the manifestation of social intelligence from an evolutionary perspective.     

Chimpanzee insectivory in the northern half of Uganda’s Rift Valley: do Bulindi chimpanzees conform to a regional pattern?

Insects are a nutritious food source for many primates. In chimpanzees, insectivory is most prevalent among communities that manufacture tools to harvest social insects, particularly ants and termites. In contrast to other long-term study sites, chimpanzees (Pan troglodytes schweinfurthii) in Budongo Forest and Kibale National Park, Uganda, rarely eat insects and have small foraging tool kits, supporting speculation that infrequent insectivory—technically aided or otherwise—characterises chimpanzees in this part of Uganda’s Rift Valley. To expand the dataset for this region, insect foraging was investigated at Bulindi (25 km from Budongo) over 19 months during two studies in 2007–2008 and 2012–2013. Systematic faecal analysis demonstrated that insectivory is a habitual foraging activity at this site. Overall levels of insect consumption varied considerably across months but were not predicted by monthly changes in rainfall or fruit intake. Unlike their Budongo and Kibale counterparts, Bulindi chimpanzees often consume ants (principally weaver ants, Oecophylla longinoda) and use sticks to dig out stingless bee (Meliponini) ground nests. In other respects, however, insectivory at Bulindi conforms to the pattern observed elsewhere in this region: they do not manufacture ‘fishing’ or ‘dipping’ tools to harvest termites and aggressive or hard-to-access ants (e.g., army ants, Dorylus spp.), despite availability of suitable prey. The Bulindi data lend support to the supposition that chimpanzees in this part of the Rift Valley rarely exploit termites and Dorylus ants, apparently lacking the ‘cultural knowledge’ that would enable them to do so most efficiently (i.e., tool use). The study’s findings contribute to current debates about the relative influence of genetics, environment and culture in shaping regional and local variability in Pan foraging ecology.     

Problem Solving in the Presence of Others: How Rank and Relationship Quality Impact Resource Acquisition in Chimpanzees (Pan troglodytes)

In the wild, chimpanzees (Pan troglodytes) are often faced with clumped food resources that they may know how to access but abstain from doing so due to social pressures. To better understand how social settings influence resource acquisition, we tested fifteen semi-wild chimpanzees from two social groups alone and in the presence of others. We investigated how resource acquisition was affected by relative social dominance, whether collaborative problem solving or (active or passive) sharing occurred amongst any of the dyads, and whether these outcomes were related to relationship quality as determined from six months of observational data. Results indicated that chimpanzees obtained fewer rewards when tested in the presence of others compared to when they were tested alone, and this loss tended to be greater when paired with a higher ranked individual. Individuals demonstrated behavioral inhibition; chimpanzees who showed proficient skill when alone often abstained from solving the task when in the presence of others. Finally, individuals with close social relationships spent more time together in the problem solving space, but collaboration and sharing were infrequent and sessions in which collaboration or sharing did occur contained more instances of aggression. Group living provides benefits and imposes costs, and these findings highlight that one cost of group living may be diminishing productive individual behaviors.