Dominance and Immunity in Chimpanzees (Pan troglodytes)

The study reported here examined the effect of dominance status on serum immunoglobulin (IgG and IgM) levels in chimpanzees living in five captive colonies. Blood samples were collected from each individual twice, and agonistic and grooming interactions were observed. After initial group observations, members of four of the five groups were caged singly. Thereafter blood samples were again taken. Both IgG and IgM levels of the animals living in groups were significantly negatively correlated with their dominance status in all five groups. The higher-ranked chimpanzees were likely to show lower levels of IgG and IgM. No such consistent correlation was found between individual Ig levels and frequency of aggressive behaviour or grooming. On transfer to isolated conditions, Ig levels of the chimpanzees did not correlate with their previous dominance status in the groups. Being of high rank is a biological cost for colony-living chimpanzees with regard to immunity levels.     

Blood pressure reference intervals for healthy adult chimpanzees (Pan troglodytes)

Background Cardiovascular disease is the primary cause of morbidity and mortality among captive chimpanzees. But there are no clinical definitions of normotension or hypertension in chimpanzees. Methods We analyzed 1 year of blood pressure (BP) data from a population of 261 healthy captive adult chimpanzees using a consistent set of criteria to ascertain health. Results Systolic BP varied by body weight. Diastolic BP varied by age. Median normotension was 126/63 mmHg, with an upper limit of 147/84 mmHg. We defined categories of pre‐hypertension (148/85—153/88 mmHg) and hypertension (≥154/89 mmHg). The prevalence of elevated BP was 15%. The relative risk of mortality was 2.60, compared to normotensive animals. Conclusions We used contemporary methods from human laboratory medicine to define reliable reference intervals for chimpanzee BP. Results allow accurate diagnosis of hypertension and pre‐hypertension, and demonstrate an effect of elevated BP on mortality.     

Development of guidelines for assessing obesity in captive chimpanzees (Pan troglodytes)

Many captive chimpanzees (Pan troglodytes) are subjectively considered to be overweight or obese. However, discussions of obesity in chimpanzees are rare in the literature, despite the acknowledged problem. No study to date has systematically examined obesity in captive chimpanzees. This project develops guidelines for defining obesity in captive chimpanzees through the examination of morphometric and physiologic characteristics in 37 adult female and 22 adult male chimpanzees. During each animal's biannual physical exam, morphometric data was collected including seven skinfolds (mm), body mass index (BMI), waist‐to‐hip ratio (WHR), and total body weight (kg). The morphometric characteristics were correlated with triglycerides and serum glucose concentration, to test the utility of morphometrics in predicting relative obesity in captive chimpanzees. Abdominal skinfold (triglyceride: F=3.83, P=0.05; glucose: F=3.83, P=0.05) and BMI (triglyceride: F=10.42, p=0.003; glucose: F=6.20, P=0.02) were predictive of increased triglycerides and serum glucose in females; however no morphometric characteristics were predictive of relative obesity in males. Results suggest that no males in this population are overweight or obese. For females, there were additional significant differences in morphometric (skinfolds, BMI, WHR, total body weight) and physiologic measurements (systolic and diastolic blood pressure, red blood cells) between individuals classified overweight and those classified non‐overweight. Skinfold measurements, particularly abdominal, seem to be an accurate measure of obesity and thus potential cardiovascular risk in female chimpanzees, but not males. By establishing a baseline for estimated body fat composition in female captive chimpanzees, institutions can track individuals empirically determined to be obese, as well as obesity‐related health problems. Zoo Biol 0:1–12, 2007. © 2007 Wiley‐Liss, Inc.     

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.     

Chronic diseases in captive geriatric female Chimpanzees (Pan troglodytes)

The current aging population of captive chimpanzees is expected to develop age-related diseases and present new challenges to providing their veterinary care. Spontaneous heart disease and sudden cardiac death are the main causes of death in chimpanzees (especially of male animals), but little is known about the relative frequency of other chronic diseases. Furthermore, female chimpanzees appear to outlive the males and scant literature addresses clinical conditions that affect female chimpanzees. Here we characterize the types and prevalence of chronic disease seen in geriatric (older than 35 y) female chimpanzees in the colony at Alamogordo Primate Facility. Of the 16 female chimpanzees that fit the age category, 87.5% had some form of chronic age-related disease. Cardiovascular-related disease was the most common (81.25%) followed by metabolic syndrome (43.75%) and renal disease (31.25%). These data show the incidence of disease in geriatric female chimpanzees and predict likely medical management challenges associated with maintaining an aging chimpanzee population.     

Hand Preferences for a Haptic Task in Chimpanzees (Pan troglodytes)

We tested the hand preferences of 20 chimpanzees (Pan troglodytes) for a haptic task requiring individuals to search for grapes in an opaque bucket filled with water. We compared these data to the hand preferences displayed by the same chimpanzees during reaching and bimanual feeding tasks. The chimpanzees displayed no significant hand preference for the reaching or bimanual feeding tasks, but exhibited a right-hand preference while performing the haptic task. In contrast, New and Old World monkeys display left-hand preferences for similar tasks. We discuss the relevance of these findings for the evolution of handedness in primates.     

Mandibular Shape, Ontogeny and Dental Development in Bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes)

The postnatal ontogenetic patterns and processes that underlie species differences in African ape adult mandibular morphology are not well understood and there is ongoing debate about whether African ape faces and mandibles develop via divergent or parallel trajectories of shape change. Using three-dimensional (3D) morphometric data, we first tested when in postnatal development differences in mandibular shape are initially evident between sister species Pan troglodytes and P. paniscus. Next, we tested whether each species has a distinct and non-parallel trajectory of mandibular development. Mandibles sampled across a broad developmental range of wildshot bonobos (n = 44) and chimpanzees (n = 59) were radiographed and aged from their dental development. We then collected 3D landmark surface data from all the mandibles. A geometric morphometric analysis of size-corrected 3D data found that bonobos and chimpanzees had parallel and linear ontogenetic trajectories of mandibular shape change. In contrast, mandibular shape was statistically different between P. paniscus and P. troglodytes as early as infancy, suggesting that species shape differences are already established near or before birth. A linear and stable trajectory of shape change suggests that mandibular ontogeny in these apes is unimpacted by non-linear variation in tooth developmental timing.     

Locomotor Adaptation and Leading Limb Asymmetries in Neonatal Chimpanzees (Pan troglodytes)

We assessed laterality for leading limb in crawling and leading limb in stepping in 13 chimpanzees (Pan troglodytes) during the first 3 months of life. Overall, there is a significant populational right-side bias for crawling but not for stepping. There is a significant negative correlation between laterality in stepping and crawling. The females are more right-sided in lateral bias than the males across both measures. These data suggest that asymmetries in postural organization are present early in life and are specific to the inherent locomotor behavior of a given species.     

Digestive Retention Times in Forest Guenons (Cercopithecus spp.) with Reference to Chimpanzees (Pan troglodytes)

Because the length of time food is maintained in the gut influences fermentation rates and its overall digestibility, information on digestive passage rates is critical to explain the overall feeding and foraging strategy of a species. I present results from digestive passage experiments conducted on captive Cercopithecus ascanius, C. mitis, C. neglectus, Miopithecus talapoin, and Pan troglodytes. I recorded several measures of digestive passage time, including transit time (time of first marker appearance; TT), mean retention time of markers (MRT), and time of last appearance of a marker (TLA). I conducted 4 trials on each of the 10 subjects. A trial consists of the administration of 20, non-toxic colored plastic markers. Overall, the 5 species varied in digestive times (p < 0.01), but there is no difference between Cercopithecus neglectus and Pan troglodytes (p = 0.131) or between C. mitis and C. ascanius (p = 0.661). When the effect of body size is removed (by computing the ratio y/x, where x = body mass, and y = MRT), Pan troglodytes exhibits a low ratio, suggesting relatively slow retention times in the 4 cercopithecines. My findings and other published digestive passage rates suggest that lengthy digestive retention times may be characteristic of cercopithecines. These data may help to interpret how the smaller-bodied guenons are able to consume a higher percentage of fiber than that of chimpanzees, a specialized frugivore. Small body size, in combination with long digestive passage times may be an adaptation on the part of Cercopithecus species to consume a high fiber diet, while maintaining a greater capacity to detoxify secondary metabolites.     

Malignant Neoplasia of the Sex Skin in 2 Chimpanzees (Pan troglodytes)

This report describes 2 cases of spontaneous malignant neoplasia within the sex skin of aged female chimpanzees. In both cases, the initial presentation resembled nonhealing traumatic wounds to the sex skin, with different degrees of infection, ulceration, and tissue necrosis. Histopathology of the lesions confirmed the diagnosis of squamous cell carcinoma in one case and of adenocarcinoma with metastasis in the other. Advanced age and previous trauma likely contributed to the development of the neoplasias in both cases; long-term sun exposure may also have contributed to the development of the squamous cell carcinoma. To our knowledge, these 2 cases represent the first reports of sex skin neoplasia in chimpanzees.Abbreviation: SCC, squamous cell carcinomaThe term ‘sexual skin’ was first used in 1891 to describe the cyclically swelling skin on the buttocks and thighs of rhesus macaques.⁶ Since then, prominent sexual swellings have been described in multiple NHP species, including many cercopithecines, some colobines, and chimpanzees.^9-11,30 In chimpanzees, the sex skin is a thin, distensible, hairless, and hypopigmented region of skin that surrounds the vagina and extends dorsally around the anus.^27,34 Sex skin swelling during the menstrual cycle function to increase female attractiveness and stimulate male sexual arousal.^10,30,34 The onset of cyclical sex skin tumescence also is used to detect puberty in chimpanzees, which generally occurs in females between the ages of 8 and 11 y.²¹In NHP species that exhibit pronounced swellings, such as chimpanzees, there is often extensive variation in swelling size both among females and between the cycles of individual females.¹¹ Swelling increases progressively during the follicular phase of the estrous cycle, as the sex skin becomes smooth, shiny, and turgid and the color changes from dull pink to bright red.^6,34 Histologic examination of sex skin during the follicular phase reveals a thin stratum corneum and dilated dermal blood vessels.⁶ The skin remains at maximal turgescence for 5 to 6 d before the swelling begins to decrease during the luteal phase.³⁴ The bright color rapidly fades, the skin becomes flaccid and wrinkly and attains a scaly appearance due to a thickened stratum corneum.^6,34 There is then a resting phase before menstruation begins again, and during this stage, some females slough areas of epithelium.³² Traditionally, maximal sexual swelling (1 to 6 d prior to detumescence) has been an accepted marker to signal ovulation in chimpanzees.^2,21,30,34 However, this association is not certain, given that ovulation has been documented to occur at other times during the estrous cycle and in view of reports of sexual swelling during infertile times, such as adolescence and pregnancy.^2,9,26,35Although spontaneous neoplasia was once considered to be uncommon in NHP and especially in chimpanzees, cases are increasingly reported as captive primate colonies age.^3,828,31 A report of all neoplasia documented at 2 major chimpanzee facilities from inception through April 2008 and including both spontaneous and experimental tumors revealed that neoplasia was not uncommon in chimpanzees and that, although most tumors were benign, malignancies did occur.³ The incidence was much higher in female than male chimpanzees due to the high incidence of neoplasia in the female urogenital system, particularly uterine leiomyoma.³ However, in that report of 117 tumors, no sex skin or perineal neoplasms were documented.³ Sporadic spontaneous tumors of the perineal skin and subcutis in female baboons have been reported and include cases of squamous cell carcinoma, lipoma, spindle cell sarcoma, myxoma, myxofibroma, myxosarcoma, and benign angiomyxoid proliferation.^7,8Here we describe 2 cases of spontaneous malignant neoplasia within the sex skin of aged female chimpanzees. To our knowledge, this report represents the first documentation of sex skin neoplasia in chimpanzees.     

A Longitudinal Assessment of Vocabulary Retention in Symbol-Competent Chimpanzees (Pan troglodytes)

A number of studies from the 1960s to 1990s assessed the symbolic competence of great apes and other animals. These studies provided varying forms of evidence that some species were capable of symbolically representing their worlds, both through productive symbol use and comprehension of symbolic stimuli. One such project at the Language Research Center involved training chimpanzees (Pan troglodytes) to use lexigram symbols (geometric visual stimuli that represented objects, actions, locations, and individuals). Those studies now are more than 40 years old, and only a few of the apes involved in those studies are still alive. Three of these chimpanzees (and a fourth, control chimpanzee) were assessed across a 10-year period from 1999 to 2008 for their continued knowledge of lexigram symbols and, in the case of one chimpanzee, the continued ability to comprehend human speech. This article describes that longitudinal assessment and outlines the degree to which symbol competence was retained by these chimpanzees across that decade-long period. All chimpanzees showed retention of lexigram vocabularies, although there were differences in the number of words that were retained across the individuals. One chimpanzee also showed continual retention of human speech perception. These retained vocabularies largely consisted of food item names, but also names of inedible objects, locations, individuals, and some actions. Many of these retained words were for things that are not common in the daily lives of the chimpanzees and for things that are rarely requested by the chimpanzees. Thus, the early experiences of these chimpanzees in symbol-rich environments have produced long-lasting memories for symbol meaning, and those competencies have benefited research in a variety of topics in comparative cognition.     

Environmental Influences on Sleep Behavior in Captive Male Chimpanzees (Pan troglodytes)

Little is known as to the influence of captivity and stressful events on sleep patterns in primates. We investigated the sleep patterns of 19 male chimpanzees living under similar conditions at the Chimpanzee Sanctuary Uto (CSU) in Kumamoto, Japan, using a behavioral sleep index. We conducted nighttime observations of all subjects during a stable period and then observed three subjects after relocation to an unfamiliar facility at CSU. We estimated length of sleep and nonsleep periods over 13-h video recordings using instantaneous sampling at 1-min intervals to record sleep, which we defined operationally as an inactive posture with the body lying down with the head on the floor or on nesting materials. The 19 subjects slept for a mean ± SEM of 11.3?±?0.26?h during the stable period, and sleep patterns varied significantly among the subjects. The three relocated subjects all showed temporarily decreased sleep duration in the post-move period but subsequently recovered to the levels observed during the stable period when habituated to the new living quarters. These results suggest that a stressful event may induce temporary sleep shortage lasting for >1?wk in captive chimpanzees. Sleep patterns may serve as a useful behavioral index of the stress response, as it is less confounded by other behaviors and the actions of human caretakers than other indices.     

Stability and Change of Social Relationship Quality in Captive Chimpanzees (Pan troglodytes)

In social animals an individual’s fitness depends partly on the quality of relationships with others. Qualitative variation in relationships has been conceptualized according to a three-dimensional structure, consisting of relationship value, compatibility, and security. However, the determinants of the components and their temporal stability are not well understood. We studied relationship quality in a newly formed group of 20 captive chimpanzees made up of several previously existing social groups. We assessed dyadic relationship quality 2?yr and again 7?yr after grouping. We confirmed the existence and stability of three relationship components and labeled them value, compatibility, and approach symmetry. Previously familiar dyads had a higher value than unfamiliar dyads, especially when they were maternally or paternally related. Compatibility was higher in dyads with only females than in dyads containing a male, but familiarity did not influence compatibility. Approach symmetry was initially higher, but later lower, in familiar than unfamiliar dyads, indicating that approach symmetry of familiar dyads decreased over time. Dyadic value and compatibility were highly stable over time, which is similar to the long relationship duration found in wild chimpanzees. In sum, relationships formed earlier in life became more valuable than those formed in later adulthood, whereas nonaggressive, compatible relationships could be formed throughout life. This suggests that for immigrating individuals, high-value relationships may be relatively difficult to establish, partly explaining why wild female chimpanzees have relatively few high-quality relationships with other females. Our study supports the multicomponent structure and durability of relationships in social species.     

How to Repair Relationships – Reconciliation in Wild Chimpanzees (Pan troglodytes)

Reconciliation appears to repair the relationships of former opponents after being disturbed by aggressive interactions. Despite a consensus about the benefit of reconciliation, how former opponents achieve this benefit remains unclear. Variation within reconciliation is evident in many species, but understanding what causes the variation has been mostly neglected until now. We collected 178 events of reconciliation of both sexes in a community of wild chimpanzees (Pan troglodytes) in the Taï National Park, Côte d'Ivoire. Our data provide evidence for the relationship‐repair function of reconciliation, as aggression disturbed tolerance levels among former opponents and reconciliation restored tolerance to normal levels again. Partners with highly beneficial relationships reconciled more often compared with partners of low mutual benefit. Latency and duration of reconciliation varied in combination, such that short reconciliations were initiated soon after the conflict, while long reconciliations were initiated later. Latency increased with the risk of further aggression, while duration decreased when costs were incurred from interruption of beneficial activities. In contrast, the complexity of reconciliation varied according to the intensity of the preceding conflict, such that reconciliation was more complex after more intense conflicts. Our results suggest that relationships between opponents are increasingly disturbed with increasing conflict intensity and reconciliation repairs all relationships independent of their relationship value. We propose that the function of reconciliation is to reduce the disturbance created by aggression, but the more frequent the reconciliation, the more beneficial it is for former opponents.     

The Foraging Costs of Mating Effort in Male Chimpanzees (Pan troglodytes schweinfurthii)

Costs of mating effort can affect the reproductive strategies and lifetime fitness of male primates, but interspecific and interindividual variation in the magnitude and distribution of costs is poorly understood. Male costs have primarily been recognized in seasonally breeding species that experience concentrated periods of mating competition. Here, we examine foraging costs associated with male mating effort in chimpanzees (Pan troglodytes schweinfurthii), a polygynandrous species, in which mating opportunities occur intermittently throughout the year. To quantify male feeding, aggression, and mating, we conducted focal follows on 12 males in a wild community (Kanyawara, Kibale National Park, Uganda) for 11 mo. Males fed less on days when high-value mating opportunities (estrous parous females) were available than on days without any mating opportunities. Reductions in feeding time were related to increased rates of aggression and copulation, indicating that the proximate cause of changes in male foraging was mating effort. Surprisingly, however, there was no relationship between dominance rank and the extent to which feeding time was reduced. High costs of mating effort may reduce the degree of reproductive skew and limit the use of possessive tactics in chimpanzees. We suggest that male bonding in chimpanzees may be favored not only for its benefits but because intragroup competition is so costly. Our results complement the available data on mammals, and primates in particular, by showing that mating effort can have measurable foraging costs even in species, in which breeding is aseasonal and only moderately skewed.     

Gastrointestinal Parasites of Savanna Chimpanzees (Pan troglodytes schweinfurthii) in Ugalla,Tanzania

Understanding variability in patterns of parasite infections requires studies of multiple populations inhabiting a variety of habitats. Gastrointestinal parasites of chimpanzees (Pan troglodytes) have been studied extensively at several forested sites, but the parasite fauna of chimpanzees living in dry, open habitats is less well known. We studied the parasites of savanna chimpanzees (Pan troglodytes schweinfurthii) living in the Issa Valley, Ugalla (Tanzania). We examined 119 fresh fecal samples using standard coproscopical methods. We detected protozoans including Blastocystis sp., Entamoeba coli, E. histolytica/dispar, Iodamoeba buetschlii, Troglodytella abrassarti, and Troglocorys cava, but only two types of spirurid nematodes among the helminths. The parasites of the Ugalla chimpanzees differ from those of forest chimpanzees in the absence of Strongyloides sp. and strongylid nematodes and a high prevalence of spirurids. Strongylids and Strongyloides sp. have thin-shelled eggs and larvae, which develop in the external environment; thus they may not be able to survive for prolonged periods in the extreme environment of Ugalla. The Ugalla chimpanzees also live at a lower population density and exhibit a larger home range than forest chimpanzees, factors that may lead to lower exposure to infective nematode larvae. Spirurid eggs, however, have thick shells and a life cycle dependent on intermediary hosts, making their survival and transmission in such extreme conditions more feasible. These differences between parasite fauna of closed and open forest chimpanzees contribute to our understanding of the ecology of infectious disease, and have the potential to contribute to conservation policies and practices.     

The Apolipoprotein E (APOE) Gene Appears Functionally Monomorphic in Chimpanzees (Pan troglodytes)

Background

The human apolipoprotein E (APOE) gene is polymorphic, with three primary alleles (E2, E3, E4) that differ at two key non-synonymous sites. These alleles are functionally different in how they bind to lipoproteins, and this genetic variation is associated with phenotypic variation for several medical traits, including cholesterol levels, cardiovascular health, Alzheimer’s disease risk, and longevity. The relative frequencies of these alleles vary across human populations, and the evolution and maintenance of this diversity is much debated. Previous studies comparing human and chimpanzee APOE sequences found that the chimpanzee sequence is most similar to the human E4 allele, although the resulting chimpanzee protein might function like the protein coded for by the human E3 allele. However, these studies have used sequence data from a single chimpanzee and do not consider whether chimpanzees, like humans, show intra-specific and subspecific variation at this locus.

Methodology and Principal Findings

To examine potential intraspecific variation, we sequenced the APOE gene of 32 chimpanzees. This sample included 20 captive individuals representing the western subspecies (P. troglodytes verus) and 12 wild individuals representing the eastern subspecies (P. t. schweinfurthii). Variation in our resulting sequences was limited to one non-coding, intronic SNP, which showed fixed differences between the two subspecies. We also compared APOE sequences for all available ape genera and fossil hominins. The bonobo APOE protein is identical to that of the chimpanzee, and the Denisovan APOE exhibits all four human-specific, non-synonymous changes and appears functionally similar to the human E4 allele.

Conclusions

We found no coding variation within and between chimpanzee populations, suggesting that the maintenance of functionally diverse APOE polymorphisms is a unique feature of human evolution.     

Food Preferences Among Captive Western Gorillas (Gorilla gorilla gorilla) and Chimpanzees (Pan troglodytes)

I used a zoological park setting to address food preferences among gorillas (Gorilla gorilla gorill) and chimpanzees (Pan troglodytes). Gorillas and chimpanzees are different sizes, and consequently, have been traditionally viewed as ecologically distinct. Sympatric western gorillas and chimpanzees have proved difficult to study in the wild. Limited field data have provided conflicting information about whether gorillas are fundamentally different from chimpanzees in diet and behavior. Fruit eating shapes the behavior of most apes, but it is unclear whether the large-bodied gorillas are an exception to this rule, specifically whether they are less selective and more opportunistic fruit eaters than chimpanzees are. My research provides experimental observational data to complement field data and to better characterize the diets and food preferences of the African apes. During laboratory research at the San Francisco Zoological Gardens, I examined individual and specific differences in food preferences of captive gorillas and chimpanzees via experimental paired-choice food trials with foods that varied in nutritional content. During the study, I offered 2500 paired-food choices to 6 individual gorillas and 2000 additional pairs to them as a group. I also proffered 600 food pairs to 4 individual chimpanzees. Despite expectations of the implications of body size differences for diet, gorillas and chimpanzees exhibited similar food preferences. Both species preferred foods high in non-starch sugars and sugar-to-fiber ratios, and low in total dietary fiber. Neither species avoided foods containing tannins. These data support other suggestions of African apes sharing a frugivorous adaptation.