Task Design Influences Prosociality in Captive Chimpanzees (Pan troglodytes)

Chimpanzees confer benefits on group members, both in the wild and in captive populations. Experimental studies of how animals allocate resources can provide useful insights about the motivations underlying prosocial behavior, and understanding the relationship between task design and prosocial behavior provides an important foundation for future research exploring these animals'' social preferences. A number of studies have been designed to assess chimpanzees'' preferences for outcomes that benefit others (prosocial preferences), but these studies vary greatly in both the results obtained and the methods used, and in most cases employ procedures that reduce critical features of naturalistic social interactions, such as partner choice. The focus of the current study is on understanding the link between experimental methodology and prosocial behavior in captive chimpanzees, rather than on describing these animals'' social motivations themselves. We introduce a task design that avoids isolating subjects and allows them to freely decide whether to participate in the experiment. We explore key elements of the methods utilized in previous experiments in an effort to evaluate two possibilities that have been offered to explain why different experimental designs produce different results: (a) chimpanzees are less likely to deliver food to others when they obtain food for themselves, and (b) evidence of prosociality may be obscured by more “complex” experimental apparatuses (e.g., those including more components or alternative choices). Our results suggest that the complexity of laboratory tasks may generate observed variation in prosocial behavior in laboratory experiments, and highlights the need for more naturalistic research designs while also providing one example of such a paradigm.     

‘Adoption’ by Maternal Siblings in Wild Chimpanzees

The adoption of unrelated orphaned infants is something chimpanzees and humans have in common. Providing parental care has fitness implications for both the adopter and orphan, and cases of adoption have thus been cited as evidence for a shared origin of an altruistic behaviour. We provide new data on adoptions in the free-living Sonso chimpanzee community in Uganda, together with an analysis of published data from other long-term field sites. As a default pattern, we find that orphan chimpanzees do not become adopted by adult group members but wherever possible associate with each other, usually as maternal sibling pairs. This occurs even if both partners are still immature, with older individuals effectively becoming ‘child household heads’. Adoption of orphans by unrelated individuals does occur but usually only if no maternal siblings or other relatives are present and only after significant delays. In conclusion, following the loss of their mother, orphaned chimpanzees preferentially associate along pre-existing social bonds, which are typically strongest amongst maternal siblings.     

A survey of entodiniomorphid ciliates in chimpanzees and bonobos

Intestinal entodiniomorphid ciliates are commonly diagnosed in the feces of wild apes of the genera Pan and Gorilla. Although some authors previously considered entodiniomorphid ciliates as possible pathogens, a symbiotic function within the intestinal ecosystem and their participation in fiber fermentation has been proposed. Previous studies have suggested that these ciliates gradually disappear under captive conditions. We studied entodiniomorphid ciliates in 23 captive groups of chimpanzees, three groups of captive bonobos and six populations of wild chimpanzees. Fecal samples were examined using Sheather's flotation and Merthiolate‐Iodine‐Formaldehyde Concentration (MIFC) methods. We quantified the number of ciliates per gram of feces. The MIFC method was more sensitive for ciliate detection than the flotation method. Ciliates of genus Troglodytella were detected in 13 groups of captive chimpanzees, two groups of bonobos and in all wild chimpanzee populations studied. The absence of entodiniomorphids in some captive groups might be because of the extensive administration of chemotherapeutics in the past or a side‐effect of the causative or prophylactic administration of antiparasitic or antibiotic drugs. The infection intensities of ciliates in captive chimpanzees were higher than in wild ones. We suppose that the over‐supply of starch, typical in captive primate diets, might induce an increase in the number of ciliates. In vitro studies on metabolism and biochemical activities of entodiniomorphids are needed to clarify their role in ape digestion. Am J Phys Anthropol 2010. © 2009 Wiley‐Liss, Inc.     

Social Network Analysis Shows Direct Evidence for Social Transmission of Tool Use in Wild Chimpanzees

Social network analysis methods have made it possible to test whether novel behaviors in animals spread through individual or social learning. To date, however, social network analysis of wild populations has been limited to static models that cannot precisely reflect the dynamics of learning, for instance, the impact of multiple observations across time. Here, we present a novel dynamic version of network analysis that is capable of capturing temporal aspects of acquisition—that is, how successive observations by an individual influence its acquisition of the novel behavior. We apply this model to studying the spread of two novel tool-use variants, “moss-sponging” and “leaf-sponge re-use,” in the Sonso chimpanzee community of Budongo Forest, Uganda. Chimpanzees are widely considered the most “cultural” of all animal species, with 39 behaviors suspected as socially acquired, most of them in the domain of tool-use. The cultural hypothesis is supported by experimental data from captive chimpanzees and a range of observational data. However, for wild groups, there is still no direct experimental evidence for social learning, nor has there been any direct observation of social diffusion of behavioral innovations. Here, we tested both a static and a dynamic network model and found strong evidence that diffusion patterns of moss-sponging, but not leaf-sponge re-use, were significantly better explained by social than individual learning. The most conservative estimate of social transmission accounted for 85% of observed events, with an estimated 15-fold increase in learning rate for each time a novice observed an informed individual moss-sponging. We conclude that group-specific behavioral variants in wild chimpanzees can be socially learned, adding to the evidence that this prerequisite for culture originated in a common ancestor of great apes and humans, long before the advent of modern humans.     

Female Coalitions Against Male Aggression in Wild Chimpanzees of the Budongo Forest

In the wild, female chimpanzees (Pan troglodytes) are subject to male aggression that at times can be prolonged or particularly violent. There are no reports of cooperative retaliation to such aggression, a strategy observed in the congeneric Pan paniscus, from the wild despite >4 decades of detailed behavioral study across a number of populations and its occurrence among captive female chimpanzees. If the reports from captivity represent an inherent capacity, then the absence of similar reports from wild populations suggests that females may be able to form coalitions only under appropriate ecological and demographic conditions. During a study of male and female aggressive interactions among chimpanzees of the Budongo Forest, Uganda, wild adult female chimpanzees sometimes formed coalitions with one another to retaliate against male aggression. This may be possible because these females tend to be more gregarious than in other populations of East African chimpanzees, as other studies of the same population have suggested; the extent and variation of female chimpanzee social strategies may, therefore, need reconsideration. Further, my observations strengthen the argument that at least some of the differences between chimpanzees and bonobos may be more of degree than of kind.     

Relations between captive and noncaptive weights in anthropoid primates

This study explores the relations between captive and noncaptive (literature-reported wild) adult weights in 53 anthropoid primate species. Based on recent studies of variation in growth among wild populations, it is expected that captive and wild weights are highly correlated. In addition, the lack of a relation between species size and captive and wild weights is anticipated. Differences between wild and captive weights are investigated. Correlations between captive and wild weights are high. Within groups of closely related species, correlations can be expected to average r = .95 for both males and females. At low taxonomic levels (within genera), correlations are not generally as high. However, captive and noncaptive intrageneric correlations are comparable to intrageneric correlations based solely on wild weights reported by different literature sources. Size appears to be unrelated to differences in captive and wild weights. Species that appear to be at elevated risk of obesity are identified. This analysis finds that deviations between captive and wild weights are positively related to growth duration (measured for captive primates). This finding implies that, in long-growing species, wild weights may underestimate asymptotic size. Hypotheses explaining this phenomenon are developed. In general, extensive overlap in weight between samples of captive and wild primates is documented. © 1994 Wiley-Liss, Inc.     

Sexual behaviour of group-living adolescent chimpanzees

This paper reports a study of the heterosexual behavior of three male and four female captive adolescent chimpanzees living a semi-natural life style in a large field enclosure. Observations made with binoculars from an over-head deck were balanced over the daylight hours and the seven weekdays. We recorded 213 copulations in 741.25 hours of observation between February 14 and July 21, 1972. Analysis of the observations suggests that group-living chimpanzees in a large field enclosure behave more like free-living chimpanzees than like other captive chimpanzees paired in small cages. In this group, copulations were non-randomly distributed throughout the day, a finding in agreement with results on wild-living chimpanzees but not previously reported for captive chimpanzees. In this group, moreover, copulations were highly concentrated within each female's period of maximum tumescence, as are those of free-living chimpanzees; and individual differences in sexual attractiveness among females were apparently based on a maturational threshold of swelling size, a phenomenon that has also been reported for wild chimpanzees.     

Identifying conservation units within captive chimpanzee populations

One of the primary objectives in the captive management of any endangered primate is to preserve as much as possible the genetic diversity that has evolved and still exists in wild gene pools. The rationale for this is based on the theoretical understanding of the relationship between genetic diversity and fitness in response to selection. There remains little consensus, however, as to the type of genetic data that should be used to monitor captive populations. In order to develop a deeper understanding of the degree and nature of genetic diversity among "wild" chimpanzee gene pools, as well as to determine if one type of genetic data is more useful than others, DNA sequence data were generated at three unlinked, nonrepetitive nuclear loci, one polymorphic microsatellite, and the mitochondrial D-loop for 59 unrelated common and pygmy chimpanzees. The results suggest that: 1) data from nuclear loci can be used to differentiate common chimpanzee subspecies; 2) pygmy chimpanzees may have less genetic diversity than common chimpanzees; 3) shared microsatellite alleles do not always indicate identity by descent; and 4) nonrepetitive loci provide unique insights into evolutionary relationships and provide useful information for captive management programs.     

Gene flow in wild chimpanzee populations: what genetic data tell us about chimpanzee movement over space and time

The isolation of phylogenetically distinct primate immunodeficiency viruses from at least seven wild-born, captive chimpanzees indicates that viruses closely related to HIV-1 may be endemic in some wild chimpanzee populations. The search for the chimpanzee population or populations harbouring these viruses is therefore on. This paper attempts to answer the question of whether or not such populations of chimpanzees are likely to exist at all, and, if so, where they are likely to be found. We summarize what is known about gene flow in wild populations of chimpanzees, both between major phylogeographical subdivisions of the species, and within these subdivisions. Our analysis indicates that hitherto undocumented reproductively isolated chimpanzee populations may in fact exist. This conclusion is based on the observation that, despite limited geographical sampling and limited numbers of genetic loci, conventional notions of the nature and extent of chimpanzee gene flow have recently been substantially revised. Molecular genetic studies using mitochondrial DNA sequences and hypervariable nuclear microsatellite markers have indicated the existence of heretofore undocumented barriers to chimpanzee gene flow. These studies have identified at least one population of chimpanzees genetically distinct enough to be classified into a new subspecies (Pan troglodytes vellerosus). At the same time, they have called into question the long-accepted genetic distinction between eastern chimpanzees (Pan troglodytes schweinfurthii) and western equatorial chimpanzees (Pan troglodytes troglodytes). The same studies have further indicated that gene flow between local populations is more extensive than was previously thought, and follows patterns sometimes inconsistent with those documented through direct behavioural observation. Given the apparently incomplete nature of the current understanding of chimpanzee gene flow in equatorial Africa, it seems reasonable to speculate that a chimpanzee population or populations may exist which both harbour the putative HIV-1 ancestor, and which have remained reproductively isolated from other chimpanzee populations over the time-scale relevant to the evolution of the SIVcpz-HIV-1 complex of viruses. Continued extensive sampling of wild chimpanzee populations, both for their genes and their viruses, should be performed quickly considering the high probability of extinction that many wild chimpanzee populations face today. The history of human-chimpanzee contacts is discussed.     

Integration of a hand-reared chimpanzee (Pan troglodytes) infant into a social group of conspecifics

Rejections of infants among non-human primates occasionally occur in the wild as well as in captive settings. Controlled adoptions of orphans and introductions of individuals into new groups are therefore sometimes necessary in captivity. Consequently, behavioral research on integration procedures and on the acceptance of infants by adoptive mothers is much needed. In this study, the introduction and subsequent adoption were examined in an 18-month-old hand-reared chimpanzee (Pan troglodytes). The infant was introduced into an age/sex-diversified social group of conspecifics at Furuvik Zoo, Gävle, Sweden, and continuous focal data was collected during the final stage of integration, including infant care exhibited by the group members and the infant’s secure base behavior. The infant was successfully integrated into the group and engaged in positive social interactions with all group members. An adult primiparous female chimpanzee formed a bond resembling a mother–infant relationship with the infant, which continues to be maintained at publication. However, the female initially showed very limited interest in the infant. It was, in fact, two other younger female group members that exhibited most infant care. The infant’s secure base behavior patterns indicate that she adapted well to the new circumstances in the chimpanzee group as the integration progressed. This provides evidence that a final adopter does not necessarily initially show maternal interest and that there can be flexibility in maternal behavior in adult chimpanzee females. Moreover, the methods applied employing gradual familiarization with all the group members and the use of an integration enclosure, may have contributed to a successful result. These findings extend our knowledge of introduction procedures in captivity as well as provide information on foster mother–infant attachment in chimpanzees.     

Polymerase chain reaction detection of Clostridium perfringens in feces from captive and wild chimpanzees, Pan troglodytes

Background For veterinary management of non‐human primates in captivity, and conservation of wild‐living primates, management of their health risks is necessary. Incidences of pathogenic bacteria in the fecal specimens are considered as one of the useful indicators for non‐invasive health monitoring. Methods We carried out the detection of Clostridium perfringens in feces from captive and wild chimpanzees by the rapid polymerase chain reaction method. Results The bacterium was detected in most fecal specimens (80%) in captive chimpanzees. Contrarily, the detection rate in the wild chimpanzees was low, with 23% (n = 12) of 53 fecal samples from the Bossou group, Guinea, and 1.2% (1/81) in the Mahale group, Tanzania. Conclusions These results show that the intestinal microflora differs between Pan populations under various living conditions, being influenced by their diet and environment.     

Reproductive aging in captive and wild common chimpanzees: factors influencing the rate of follicular depletion

We examine and discuss evidence of contrasting differences in fertility patterns between captive and wild female chimpanzees, Pan troglodytes, as they age; in the wild females reproduce in their 40s, but captive studies suggest that menopause occurs around that time. Thus, despite the increased longevity generally observed in captive populations reproductive life span is shortened. We outline a hypothesis to explain the apparent differential pace of reproductive decline observed between wild and captive populations. The breeding schedules of captive primates may contribute to accelerated reproductive senescence because continuous cycling in captive animals results in early depletion of the ovarian stock and premature senescence. Available evidence supports the hypothesis that women with patterns of high oocyte loss experience earlier menopause. Chimpanzees in captivity live longer, and thus, similar to humans, they may experience follicular depletion that precedes death by many years. In captivity, chimpanzees typically have an early age at menarche and first birth, shorter interbirth intervals associated with short lactational periods as young mature faster, and nursery rearing, which allows mothers to begin cycling earlier. Variables typical of wild chimpanzee populations, including late age at menarche and first birth, long interbirth intervals associated with prolonged lactational periods, and a long period of female infertility after immigration, spare ovulations and may be responsible for the later age at reproductive termination. Finally, we describe and discuss the timing of specific reproductive landmarks that occur as female chimpanzees age, distinguishing between functional menopause (age at last birth) and operational menopause (end of cycling). Am. J. Primatol. 71:271–282, 2009. © 2008 Wiley‐Liss, Inc.     

Why do goose parents adopt unrelated goslings? A review of hypotheses and empirical evidence,and new research questions

Adoption of unrelated offspring by successful breeders is one form of brood mixing and alloparental care that is widespread among geese and other waterfowl. Biparental care and long-lasting family bonds in geese are likely to affect the costs and benefits of adoption. Most hypotheses that have been proposed to explain this behaviour assume that the separation of the gosling from its original family is accidental, and that adoption forms the 'best of a bad job' solution. For the gosling, adoption is therefore thought to be the only, and thus adaptive, option. For parents, some hypotheses assume that there are costs of adoption (intergeneration conflict), while others assume that there are benefits (mutually beneficial). The few studies of adoption in wild goose populations indicate cost-neutrality or that there are small benefits to parents of adopting young. This agrees with studies of brood size, which suggest that large families provide benefits for goslings and parents alike. By contrast, most observed adoption attempts involve parental aggression against the lone gosling. However, incidental observations are likely to be biased towards adoptions that involve conspicuous behaviour, such as aggression, and might overlook inconspicuous adoptions. Studies of individually marked goslings are needed to identify the background of the adoption goslings in order to identify whether in geese, as in some larids and altricial species, adoption might be an active strategy of offspring to improve their fitness prospects. In addition, more experimental studies are needed to test predictions about the costs and benefits of large families in geese.     

Conflict and reconciliation behavior trends of the bottlenose dolphin (Tursiops truncatus)

Wild bottlenose dolphin (Tursiops truncatus) populations display societal structures characterized by numerous and frequent changes in group composition, complex social relationships, and high levels of cooperation, attributes also observed in human and nonhuman primate cultures. Maintaining social relationships under such elemental conditions can frequently create conflict—and the opportunity for reconciliation—among group members. The conflict and reconciliation behavior patterns of the chimpanzee (Pan troglodytes) have been studied extensively; trends are well‐documented in the wild and in captivity. Apparent cultural similarities have prompted several analogous studies on wild and captive bottlenose dolphins. This research attempted to corroborate previous efforts by analyzing the social behavior of seven captive bottlenose dolphins to determine the effects of sex and age on the frequency of conflict and reconciliation, and to investigate the incidence of consolatory behavior within the group. A total of 3,428 interactions involving focal animals, 414 of which were conflict episodes, were documented during 261 hr of videotaped observations. Although the sample size precluded meaningful statistical evaluation of the influence of sex on conflict and reconciliation, participant age was a significant determinant of conflict frequency. Conversely, age did not impact frequency of reconciliation, which only occurred after 18% of all conflict interactions. Little to no definitive evidence of consolation was apparent within the study group. While results partially support the findings of previous dolphin reconciliation research, extensive behavioral studies of wild populations should be conducted before generating broad comparisons between human terms and nonhuman behavioral interactions. Zoo Biol 29:567–585, 2010. © 2009 Wiley‐Liss, Inc.     

乌干达野生动物研究中心外来黑猩猩融入笼养群体的过程

1967至1997的30年间,生活在非洲热带地区自然栖息地的野生黑猩猩数量由60万降至不足20万,至今这个数字仍在减少,因此引起了全球的关注并急需要开展迁地保护。笼养黑猩猩与野外种群一样营群居生活,为了有效进行野生黑猩猩的迁地保护,将野外捕获的野生黑猩猩个体成功引入已在动物园的黑猩猩群体中十分必要。2004年10月至2005年3月,乌干达野生动物研究中心首先开展了这一实验。同时为更好地了解外来黑猩猩融入笼养群体的过程,2006年9月至2007年1月间收集其活动数据。选取5只黑猩猩个体并记录它们的食性、行为、体重变化及身体健康状况。除直接观察和记录外,与兽医和研究中心管理人员进行合作,以获取较多笼养个体的信息。我们发现,野生个体比笼养个体多病,因此影响了它们的取食、社会行为及活动水平。尽管笼养黑猩猩有人照料,但仍具备野生个体的行为,所以,理解外来黑猩猩融入笼养群体的过程对于黑猩猩的迁地保护和就地保护是非常重要的。     

Asian Elephant (Elephas maximus), Pig-Tailed Macaque (Macaca nemestrina) and Tiger (Panthera tigris) Populations at Tourism Venues in Thailand and Aspects of Their Welfare

This study focused on determining the size and welfare aspects of Asian elephant, pig-tailed macaque and tiger populations at facilities open to tourists in Thailand. Data were gathered from 118 venues through direct observations and interviews with staff. A score sheet-based welfare assessment was used to calculate scores between 1 and 10, indicating each venue’s welfare situation. Factors such as freedom of movement for the animals, access to veterinary care, environmental noise quality, hygiene standards and work intensity were included in the score sheet. 1688 elephants, 371 macaques and 621 tigers were found at the venues. 89 venues exclusively kept elephants, 9 designated ‘Monkey schools’ offered macaque shows, 4 venues kept primarily tigers, mostly for petting and photo opportunities, and the remaining venues kept a mix of these animals. A strong imbalance in female to male gender ratios was recorded with about 4:1 for adult elephants and 1:4 for adult macaques. Severely inadequate welfare conditions were common, with 75% of macaques and 99% of tigers being kept at venues with scores less than 5. 86% of elephants were kept in inadequate conditions at venues with scores between 3 and 5, but a significant number of venues with scores above 5 were found. 4.6% of elephants were provided commendable conditions, reaching assessment scores of 8 and above. 71% of venues did not offer any sort of education about animals to visitors. This study is the first to assess welfare aspects of captive wild animals at tourism venues across Thailand. It concludes that significant concerns exist about the welfare of wild animals in the tourism sector of Thailand. Urgent attention needs to be given to address these concerns and prevent further suffering. But also to ensure the demand for wild animals doesn’t have a negative impact on wild populations.     

Genetic structure of chimpanzee populations

Little is known about the history and population structure of our closest living relatives, the chimpanzees, in part because of an extremely poor fossil record. To address this, we report the largest genetic study of the chimpanzees to date, examining 310 microsatellites in 84 common chimpanzees and bonobos. We infer three common chimpanzee populations, which correspond to the previously defined labels of “western,” “central,” and “eastern,” and find little evidence of gene flow between them. There is tentative evidence for structure within western chimpanzees, but we do not detect distinct additional populations. The data also provide historical insights, demonstrating that the western chimpanzee population diverged first, and that the eastern and central populations are more closely related in time.     

Baboons, chimpanzees, and tools

Wild chimpanzees make and use tools with far greater frequency and variety than wild baboons. Sampling differences; differences in the sensory, motor, or cognitive capacities for skilled tool use; or environmental differences are not responsible. Fortuitous discovery of novel forms of tool behavior probably occurs as rarely among chimpanzees as among baboons. However, research on wild and captive chimpanzees reveals that the discovery is transmitted quickly among chimpanzee groups by observation learning, and thus becomes well-established in the group's behavioral repertoire. In contrast, study of captive baboons reveals that they acquire little information about tool behavior by observation. With little observation learning the behavior is not likely to be acquired by other group members since repeated independent discovery is improbable. Thus chimpanzees' more proficient tool behavior is due mainly to their greater capacity for observation learning. This suggests that the advent of hominid tool traditions was accompanied by a capacity for facile observation learning and thus, perhaps, by language ability.     

Spontaneous altruism by chimpanzees and young children

People often act on behalf of others. They do so without immediate personal gain, at cost to themselves, and even toward unfamiliar individuals. Many researchers have claimed that such altruism emanates from a species-unique psychology not found in humans' closest living evolutionary relatives, such as the chimpanzee. In favor of this view, the few experimental studies on altruism in chimpanzees have produced mostly negative results. In contrast, we report experimental evidence that chimpanzees perform basic forms of helping in the absence of rewards spontaneously and repeatedly toward humans and conspecifics. In two comparative studies, semi–free ranging chimpanzees helped an unfamiliar human to the same degree as did human infants, irrespective of being rewarded (experiment 1) or whether the helping was costly (experiment 2). In a third study, chimpanzees helped an unrelated conspecific gain access to food in a novel situation that required subjects to use a newly acquired skill on behalf of another individual. These results indicate that chimpanzees share crucial aspects of altruism with humans, suggesting that the roots of human altruism may go deeper than previous experimental evidence suggested.     

The implementation and initial evaluation of a physical therapy program for captive chimpanzees (Pan troglodytes)

Due to advances in captive nonhuman primate (NHP) medical care, the number of geriatric chimpanzees (≥35-years old) is growing. With old age comes a variety of physical conditions, including arthritis, stroke, and mobility impairments. Programs aimed at enhancing the welfare of geriatric chimpanzees are now quite common, but there are few published empirical evaluations of the efficacy of such programs. The current study aimed to create, implement, and evaluate the effects of participation in a physical therapy (PT) program on physical health, mobility, welfare, and behavior. Nine chimpanzees with mobility impairments participated in personalized PT routines (using positive reinforcement training) twice per week for 5 months. Additionally, nine control chimpanzees (non-mobility-impaired, matched with PT chimpanzees on age and gender) participated in body exam behavior sessions (also using positive reinforcement training) twice per week. All chimpanzees were rated on 14 health, well-being, and behavior items, as well as level of mobility throughout the PT program. Chimpanzees that participated in the PT program showed significant increases in ratings of physical health, well-being, and activity levels across phases of the program. Furthermore, compared to control chimpanzees, PT chimpanzees showed significant increases in ratings of ease of movement. Because raters were not blind to physical therapy treatment, our results represent an initial evaluation of the program that may suggest that participation in the PT program has physical, behavioral, and welfare benefits. Assessments of novel geriatric-focused care strategies and programs are essential to further enhance the welfare of the captive chimpanzee population, which is currently comprised of many geriatric animals, whose proportion of the captive population will only increase.