Transfer and Acclimatization Effects on the Behavior of Two Species of African Great Ape (<Emphasis Type="BoldItalic">Pan troglodytes</Emphasis> and <Emphasis Type="BoldItalic">Gorilla gorilla gorilla</Emphasis>) Moved to a Novel and Naturalistic Zoo Environment

Studying the effects of moving animals to new enclosures is of value to both captive managers and to scientists interested in the complex interplay between environment and behavior. Great apes represent some of the greatest challenges in this regard. Given the cognitive sophistication of these species and the substantial investments in new primate facilities, these investigations are particularly important. Using post-occupancy evaluation (POE) methodology, we compared behavior exhibited by chimpanzees (Pan troglodytes) and gorillas (Gorilla gorilla gorilla) in indoor hardscape-type exhibits to behavior of the same individuals in new naturalistic enclosures with outdoor access. In the new facility, chimpanzees showed decreases in the frequency of abnormal behaviors and visual monitoring of humans (attention behaviors) whereas gorillas exhibited reduced agonism as well as decreased attention behaviors. Both gorillas and chimpanzees demonstrated higher rates of inactivity after transfer to the new facility. All subjects in addition demonstrated transitory changes in behavior after the move to the new facility (higher rates of scratching in yr 1 than in subsequent years), indicating a period of acclimatization. Seasonal effects on feeding behavior and activity levels (both species were more active in the winter) were evident as well. The results indicate that behavioral adjustment to a new facility is an extended process for both species and that seasonal effects should be considered in longitudinal analyses of acclimatization. Behavioral patterns supported the benefits of naturalistic, functional exhibit spaces and the utility of post-occupancy evaluations in assessing captive animal welfare.     

Food Neophobia and Social Learning Opportunities in Great Apes

Finding food resources and maintaining a balanced diet are major concerns for all animals. A compromise between neophobia and neophilia is hypothesised to enable animals to enlarge their diet while limiting the risk of poisoning. However, little is known about how primates respond to novel food items and whether their use is socially transmitted. By comparing how four different species of great apes respond to novel food items, we investigated how differences in physiology (digestive tract size and microbial content), habitats (predictability of food availability), and social systems (group size and composition) affect their response toward novelty. We presented two familiar foods, one novel fruit, four novel aromatic plants from herbal medicine, and kaolin to captive chimpanzees (Pan troglodytes), western gorillas (Gorilla gorilla), Bornean orangutans (Pongo pygmaeus) and Sumatran orangutans (Pongo abelii). We recorded smelling, approach-taste delays, ingestion, interindividual observations, and food transfers with continuous sampling. We found that behaviors differed between the apes: chimpanzees were the most cautious species and observed their conspecifics handling the items more frequently than the other apes. Close observations and food transfers were extremely rare in gorillas in comparison to orangutans and chimpanzees. We suggest that a low neophobia level reflects an adaptive response to digestive physiological features in gorillas and to unpredictable food availability in orangutans. Social interactions appeared to be predominant in chimpanzees and in both orangutan species to overcome food neophobia. They reflect higher social tolerance and more opportunities for social learning and cultural transmission in a feeding context.     

Interactions between zoo‐housed great apes and local wildlife

Although there are published reports of wild chimpanzees, bonobos, and orangutans hunting and consuming vertebrate prey, data pertaining to captive apes remain sparse. In this survey‐based study, we evaluate the prevalence and nature of interactions between captive great apes and various indigenous wildlife species that range into their enclosures in North America. Our hypotheses were threefold: (a) facilities housing chimpanzees will report the most frequent and most aggressive interactions with local wildlife; (b) facilities housing orangutans and bonobos will report intermediate frequencies of these interactions with low levels of aggression and killing; and (c) facilities housing gorillas will report the lowest frequency of interactions and no reports of killing local wildlife. Chimpanzees and bonobos demonstrated the most aggressive behavior toward wildlife, which matched our predictions for chimpanzees, but not bonobos. This fits well with expectations for chimpanzees based on their natural history of hunting and consuming prey in wild settings, and also supports new field data on bonobos. Captive gorillas and orangutans were reported to be much less likely to chase, catch and kill wildlife than chimpanzees and bonobos. Gorillas were the least likely to engage in aggressive interactions with local wildlife, matching our predictions based on natural history. However unlike wild gorillas, captive gorillas were reported to kill (and in one case, eat) local wildlife. These results suggest that some behavioral patterns seen in captive groups of apes may be useful for modeling corresponding activities in the wild that may not be as easily observed and quantified. Furthermore, the data highlight the potential for disease transmission in some captive settings, and we outline the associated implications for ape health and safety. Am. J. Primatol. 71:458–465, 2009. © 2009 Wiley‐Liss, Inc.     

Hand preferences for coordinated bimanual actions in 777 great apes: implications for the evolution of handedness in hominins

Whether or not nonhuman primates exhibit population-level handedness remains a topic of considerable scientific debate. Here, we examined handedness for coordinated bimanual actions in a sample of 777 great apes including chimpanzees, bonobos, gorillas, and orangutans. We found population-level right-handedness in chimpanzees, bonobos and gorillas, but left-handedness in orangutans. Directional biases in handedness were consistent across independent samples of apes within each genus. We suggest that, contrary to previous claims, population-level handedness is evident in great apes but differs among species as a result of ecological adaptations associated with posture and locomotion. We further suggest that historical views of nonhuman primate handedness have been too anthropocentric, and we advocate for a larger evolutionary framework for the consideration of handedness and other aspects of hemispheric specialization among primates.     

Clinical and pathologic manifestation of oesophagostomosis in African great apes: does self‐medication in wild apes influence disease progression?

Nodular worms (Oesophagostomum spp.) are common intestinal parasites found in cattle, pig, and primates including humans. In human, they are responsible for serious clinical disease called oesophagostomosis resulting from the formation of granulomas, caseous lesions or abscesses in intestinal walls. In wild great apes, the fecal prevalence of this parasite is high, but little information is available concerning the clinical signs and lesions associated. In the present study, we describe six cases of multinodular oesophagostomosis in free-ranging and ex-captive chimpanzees and captive gorillas caused by Oesophagostomum stephanostomum. While severe clinical signs associated with this infection were observed in great apes raised in sanctuaries, nodules found in wild chimpanzees do not seem to affect their health status. One hypothesis to explain this difference would be that in wild chimpanzees, access to natural environment and behavior such as rough leaves swallowing combined with ingestion of plants having pharmacological properties would prevent severe infection and decrease potential symptoms.     

Use of space in a non-naturalistic environment by chimpanzees (Pan troglodytes) and lowland gorillas (Gorilla gorilla gorilla)

Chimpanzees and gorillas are the two most common species of great ape in captive facilities in North America. This study examined patterns of space use by 14 gorillas and six chimpanzees housed in similar non-naturalistic environments at Lincoln Park Zoo in Chicago, IL. The location of each individual was recorded in relation to elements of the environment over a two-year period. These data were compared to volumetric measurements of the enclosures to determine “preferences” for particular environmental elements. Chimpanzees preferred the highest tier of the enclosure and the gorillas preferred the floor level. Both species showed preferences for doorways, corners and the mesh barriers adjacent to keeper areas. These data supplement data from wild populations of apes and provide information useful for those seeking to design new ape enclosures or renovate existing facilities.     

Discrepancies in the occurrence of Balantidium coli between wild and captive African great apes

Balantidium coli is a ciliate reported in many mammalian species, including African great apes. In the former, asymptomatic infections as well as clinical balantidiasis have been reported in captivity. We carried out a cross-sectional study of B. coli in African great apes (chimpanzees, bonobos, and both species of gorillas) and examined 1,161 fecal samples from 28 captive facilities in Europe, plus 2 sanctuaries and 11 wild sites in Africa. Samples were analyzed with the use of Sheather's flotation and merthiolate-iodine-formaldehyde (MIFC) sedimentation. MIFC sedimentation was the more sensitive technique for diagnostics of B. coli in apes. Although not detected in any wild-ape populations, B. coli was diagnosed in 52.6% of captive individuals. Surprisingly, in the apes' feces, trophozoites of B. coli were commonly detected, in contrast with other animals, e.g., Old World monkeys, pigs, etc. Most likely reservoirs for B. coli in captive apes include synantropic rats. High starch diets in captive apes are likely to exacerbate the occurrence of balantidiasis in captive apes.     

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.     

Readiness to attend to visual foreground cues

Nonhuman primate genera are differentially inclined to attend to stimuli of the immediate foreground. When great apes were trained to a criterion on each of a series of two-choice visual discrimination problems and then given critical test trials with irrelevant visual cues ($\text{1}\text{2}$ in wire mesh) positioned immediately in front of each problem's objects, accuracy of performance was significantly more disrupted in orang-utans (Pongo) than in chimpanzees (Pan) and gorillas (Gorilla). Two groups of chimpanzees known to differ profoundly in complex-learning skills did not differ in their readiness to attend to irrelevant foreground cues; hence, it is concluded that the observed differences among the three genera of great apes must be species related and associated with how arboreal/terrestial they are in their natural habitats.     

Evidence of leopard predation on bonobos (Pan paniscus)

Current models of social organization assume that predation is one of the major forces that promotes group living in diurnal primates. As large body size renders some protection against predators, gregariousness of great apes and other large primate species is usually related to other parameters. The low frequency of observed cases of nonhuman predation on great apes seems to support this assumption. However, recent efforts to study potential predator species have increasingly accumulated direct and indirect evidence of predation by leopards (Panthera pardus) on chimpanzees and gorillas. The following report provides the first evidence of predation by a leopard on bonobos (Pan paniscus).     

Space use as an indicator of enclosure appropriateness: A novel measure of captive animal welfare

Empirical measures of animal behavior and space use within the captive environment can provide critical information about animals’ requirements, preferences and internal states. The trend toward naturalistic environments has shown promise in terms of behavioral benefits for animals such as great apes, and there have been several studies of the effects of complex environments on captive apes. However, few recent investigations have objectively compared environmental preferences between two distinct enclosures. In this study, we assessed how ape space use varied within and across two very different environments: an indoor, hardscape enclosure and an indoor/outdoor, naturalistic enclosure. Within-facility tests were conducted by comparing data from behavioral observations of the apes’ position in the enclosures to measurements of the space and the availability of individual environmental elements. Between-facility comparisons utilized electivity index calculations to assess both the degree of use for specific features and the degree to which these selections strengthened or weakened in the new facility. Both gorillas and chimpanzees showed significant structural preferences in the older, hardscape environment: positioning themselves by mesh barriers (chimpanzees: P = 0.005; gorillas: P < 0.001) and corners (P = 0.005; gorillas: P < 0.001) more than would be expected by random spatial utilization, and avoiding open spaces (chimpanzees: P = 0.005; gorillas: P < 0.001) not adjacent to any physical structure. A new, naturalistic enclosure was constructed using preference data from the previous facility. In the new facility, both species of ape substantially altered the way in which they chose to position themselves in the enclosure. Chimpanzees used most of the environmental elements at rates more similar to the proportions they were available. While gorilla's preference corners was maintained in the new facility, preferences for doorways and mesh barriers disappeared. Comparing electivity indices facilitated an empirical comparison of space use preferences. Chimpanzees showed significant differences in how they used structural elements (P = 0.021), mesh barriers (P = 0.009) and corners (P = 0.016) in the new facility. Gorillas’ environmental selections were similarly altered in the new facility, as selections of areas adjacent to doorways (P = 0.003), glass barriers (P = 0.005), structural elements (P < 0.001), and mesh barriers (P = 0.012) were all significantly affected by the transfer. This approach is useful for understanding how captive animals utilize their enclosures and we advocate that electivity indices can be added to a growing list of tools to assess the effect of captive environments on animal welfare.     

Successful treatment of idiopathic dilated cardiomyopathy in an adult chimpanzee (Pan troglodytes)

Various congenital and acquired forms of heart disease have been reported in captive lowland gorillas, and heart disease is a major cause of morbidity and mortality in geriatric humans. However, the prevalence of heart disease is unknown in nonhuman great apes species. Indeed, little is known about heart disease in chimpanzees, although the species has been used in research for decades. This report details the clinical presentation and diagnostics (thoracic radiography, electrocardiography, and echocardiography) utilized to diagnose idiopathic dilated cardiomyopathy in a 27-year-old male chimpanzee. Treatment decisions--indicated by follow-up diagnostics including repeat electrocardiography, echocardiography, and clinical laboratory data--over the 22-month period during which he continues to be treated are described. In addition, electrocardiographic and echocardiographic findings obtained from 20 clinically normal adult (11 female and 9 male) chimpanzees are presented for comparison.     

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.     

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.     

Relationship between sunlight exposure, housing condition, and serum vitamin D and related physiologic biomarker levels in captive chimpanzees (Pan troglodytes)

In primates, the primary source of vitamin D is synthesis in the skin through sun exposure. Decreased sun exposure may lead to vitamin D deficiency and consequently other health issues. In laboratory, sanctuary, and zoo settings, chimpanzees (Pan troglodytes) may be housed indoors for prolonged periods of time without regular exposure to unfiltered sunlight. However, little research has examined the relationship between housing conditions and vitamin D serum levels in captive chimpanzees. In this study, we retrospectively compared serum levels of total vitamin D, calcium, ionic calcium, phosphorous, albumin, and alkaline phosphatase in 18 female and 12 male chimpanzees as they cycled between indoor-only and indoor-outdoor enclosures. Total vitamin D was significantly lower and alkaline phosphatase significantly higher when subjects were in the indoor-only enclosures compared with when they had regular access to outdoor enclosures. A vitamin D effect occurred only in young and prime-adult animals. Changes were significant in female but not in male chimpanzees. Calcium, ionic calcium, phosphorus, and albumin did not differ between indoor-only and indoor-outdoor enclosures. However, female chimpanzees exhibited significantly lower calcium and phosphorous levels while in the indoor-only enclosures. These results suggest that adult captive chimpanzees experience vitamin D deficiency when housed without regular access to unfiltered sunlight and that these effects may be more acute for adult female animals.     

Temporal Variation in Insect-eating by Chimpanzees and Gorillas in Southeast Cameroon: Extension of Niche Differentiation

I studied insect-foraging strategies of great apes and aimed to define niche differentiation in their insect diet. I investigated seasonality in fruit-, foliage-, insect-, and meat-eating by great apes in southeast Cameroon via indirect methods and measured activity and nest densities of insect prey. I used a multinomial logistic regression to analyze the data. Gorilla and chimpanzee insect-, ant-, and termite-eating does not correlate with rainfall. Ant- and nonwinged termite-eating by chimpanzees increased in periods of succulent fruit scarcity and provided protein and energy, which might have compensated for the protein-low foliage eaten then. The apes ate winged termites when succulent fruit was abundant. Ant and winged termite consumption by gorillas correlates positively with that of chimpanzees. Ant-eating by gorillas increased when fruit was scarce, but was also associated with temporal ant activity and nest density. Both ape species also encountered more ant nests and trails in that period, as they predominantly foraged for herbs in vegetation types with high ant availability. In contrast, fruit-eating correlates positively with nonwinged termite-eating by gorillas, but again temporal prey availability is also associated. Termites might have provided 1) supplemental iron when tannin-rich fruits were eaten or 2) antidiarrheal properties when gorillas ate too much laxative fruit. Termite-eating by both ape species is not associated with spatial termite availability. In conclusion, there is niche differentiation in their insect diet. Based on the trade-off between foraging effort and nutritional gain, chimpanzees use a high-energy and gorillas a low-energy strategy when feeding on termites, but both use a low-energy strategy when feeding on ants. However, more information on the consumption of ant larvae is necessary to define niche differentiation in their ant diet.     

Genome of the apes.

The Human Genome Project has generated both the information and technological infrastructure needed to accelerate genetic comparisons between humans and the African great apes (chimpanzees and gorillas). Sequence and chromosomal organization differences between these highly related genomes will provide clues to the genetic basis for recently evolved, specifically human traits such as bipedal gait and advanced cognitive function. Recent studies comparing the primate genomes have the potential to affect many aspects of human biomedical research and could benefit primate conservation efforts.     

Rotator cuff muscle function and its relation to scapular morphology in apes

It is widely held that many differences among primate species in scapular morphology can be functionally related to differing demands on the shoulder associated with particular locomotor habits. This perspective is largely based on broad scale studies, while more narrow comparisons of scapular form often fail to follow predictions based on inferred differences in shoulder function. For example, the ratio of supraspinous fossa/infraspinous fossa size in apes is commonly viewed as an indicator of the importance of overhead use of the forelimb, yet paradoxically, the African apes, the most terrestrial of the great apes, have higher scapular fossa ratios than the more suspensory orangutan. The recent discovery of several nearly complete early hominin scapular specimens, and their apparent morphological affinities to scapulae of orangutans and gorillas rather than chimpanzees, has led to renewed interest in the comparative analysis of human and extant ape scapular form. To facilitate the functional interpretation of differences in ape scapulae, particularly in regard to relative scapular fossa size, we used electromyography (EMG) to document the activity patterns in all four rotator cuff muscles in orangutans and gibbons, comparing the results with previously published data for chimpanzees.     

Pathology and diseases of great apes at the National Zoological Park

Knowledge of the diseases of great apes in captivity is essential for captive management of self-sustaining populations. This survey of medical and pathology records of orangutans, gorillas, and one chimpanzee at the National Zoological Park was conducted to provide a data base for improving health care of captive apes. Strongyloidiasis, balantidiasis, and entamoebiasis were recurrent problems in adult and juvenile apes of all species. Cardiac fibrosis also was prevalent in middle-aged apes and was a major cause of mortality. Bacterial infections were prevalent in perinatal orangutans and resulted in the death of two. For gorillas, rheumatoid arthritis associated with mycoplasma infections, and infertility were major problems. Because the pathogenesis of many of these lesions is unknown, survival of great ape populations in captivity may depend on future research on these problems.     

Plantigrady and foot adaptation in African apes: implications for hominid origins.

In living primates, except the great apes and humans, the foot is placed in a heel-elevated or semi-plantigrade position when these animals move upon arboreal or terrestrial substrates. Heel placement and bone positions in the non-great ape primate foot are designed to increase mobility and flexibility in the arboreal environment. Orangutans have further enhanced foot mobility by adapting their feet for suspension and thus similarly utilize foot positions where the heel does not touch the substrate. Chimpanzees and gorillas represent an alternative pattern (plantigrady), in which the heel contacts the surface of the support at the end of swing phase, especially during terrestrial locomotion. Thus, chimpanzees and gorillas possess feet adapted for both arboreal and terrestrial substrates. African apes also share several osteological features related to plantigrady and terrestrial locomotion with early hominids. From this analysis, it is apparent that hominid locomotor evolution passed through a quadrupedal terrestrial phase.