Characterization of Enteroviruses from Non-Human Primates in Cameroon Revealed Virus Types Widespread in Humans along with Candidate New Types and Species

Enteroviruses (EVs) infecting African Non-Human Primates (NHP) are still poorly documented. This study was designed to characterize the genetic diversity of EVs among captive and wild NHP in Cameroon and to compare this diversity with that found in humans. Stool specimens were collected in April 2008 in NHP housed in sanctuaries in Yaounde and neighborhoods. Moreover, stool specimens collected from wild NHP from June 2006 to October 2008 in the southern rain forest of Cameroon were considered. RNAs purified directly from stool samples were screened for EVs using a sensitive RT-nested PCR targeting the VP1 capsid coding gene whose nucleotide sequence was used for molecular typing. Captive chimpanzees (Pan troglodytes) and gorillas (Gorilla gorilla) were primarily infected by EV types already reported in humans in Cameroon and elsewhere: Coxsackievirus A13 and A24, Echovirus 15 and 29, and EV-B82. Moreover EV-A119, a novel virus type recently described in humans in central and west Africa, was also found in a captive Chimpanzee. EV-A76, which is a widespread virus in humans, was identified in wild chimpanzees, thus suggesting its adaptation and parallel circulation in human and NHP populations in Cameroon. Interestingly, some EVs harbored by wild NHP were genetically distinct from all existing types and were thus assigned as new types. One chimpanzee-derived virus was tentatively assigned as EV-J121 in the EV-J species. In addition, two EVs from wild monkeys provisionally registered as EV-122 and EV-123 were found to belong to a candidate new species. Overall, this study indicates that the genetic diversity of EVs among NHP is more important than previously known and could be the source of future new emerging human viral diseases.     

The Occurrence and Ape-to-Ape Transmission of the Entodiniomorphid Ciliate Troglodytella abrassarti in Captive Gorillas

ABSTRACT. Entodiniomorphid ciliates are often present in the colons of wild apes. In captive apes the infection tends to gradually disappear, with the exception of Troglodytella abrassarti . We used fecal examinations to screen the gorillas ( Gorilla gorilla gorilla ) in European (Czech Republic, UK) and Australian Zoos to explore the ape-to-ape transmission pattern of T. abrassarti . Gorillas from two out of three European Zoos were positive for T. abrassarti , while gorillas from the Australian Zoo were negative. We documented a horizontal transmission of T. abrassarti to a non-infected adult gorilla introduced into a Troglodytella -positive group in the Prague Zoo and traced the origin of the ciliate infection to the Paignton Zoo (UK) using serial fecal examinations. During this study, two infant gorillas born in the Prague Zoo (CZ) first became positive for T. abrassarti at the age of 9 mo. Ciliate morphology and the sequencing of the small subunit rRNA gene and the internal transcribed spacer rDNA spacer region revealed that T. abrassarti affects both captive gorillas and chimpanzees. We conclude that zoo transport plays a major role in the distribution of T. abrassarti among captive gorillas.     

Behavioral Ecology of Sympatric Chimpanzees and Gorillas in Bwindi Impenetrable National Park,Uganda: Diet

Via a field study of chimpanzees (Pan troglodytes schweinfurthii) and gorillas (Gorilla gorilla beringei) in Bwindi Impenetrable National Park, Uganda, we found that their diets are seasonally similar, but diverge during lean seasons. Bwindi chimpanzees fed heavily on fruits of Ficus sp., which were largely ignored by the gorillas. Bwindi gorilla diet was overall more folivorous than chimpanzee diet, but was markedly more frugivorous than that of gorillas in the nearby Virunga Volcanoes. During 4 mo of the year Bwindi gorilla diet included more food species than that of the chimpanzees. Three factors in particular—seasonal consumption of fibrous foods by gorillas, interspecific differences in preferred fruit species, and meat consumption by chimpanzees—contributed to dietary divergence between the two species. When feeding on fruits, gorillas ate Myrianthus holstii more frequently than chimpanzees did, while chimpanzees included more figs in their annual diet. Chimpanzee diet included meat of duikers and monkeys; gorilla frequently consumed decaying wood.     

Socialization processes in a female lowland gorilla

A low-interactive, captive, female lowland gorilla, Molly, was studied following the introduction into her enclosure of three gorillas, two males and a female, raised from birth in captive gorilla groups. Observations were made 6 mo after the new gorillas were introduced. Throughout the period of observation, Molly interacted in an affiliative manner with one of the males, playing or sitting quietly with him in a tree (where Molly spent most of her time) and occasionally on the ground. Agonistic displays between Molly and the new female decreased after they were released in the enclosure without the males for a series of days. Molly, however, continued to react to the other male, the most dominant, in an agonistic manner, and usually retreated from his reach, climbed the tree, and/or grimaced and piloerected whenever he approached. Although Molly's continued avoidance of the dominant male impeded her complete socialization, we propose that the interventions employed in this study—introduction of new younger gorillas into and an enclosure, and a series of dyadic separations between the noninteractive gorilla and each of the new group members—are possible strategies that can be used to facilitate socialization of captive, noninteractive gorillas.     

Research on reproductive biology of gorillas

Laboratory research has implicated several variables which contribute to the regulation of reproductive behaviour of captive gorillas. Females were found to be increasingly attractive to males during the follicular phase of the menstrual cycle when estrogen and testosterone concentrations in the female were increasing. Females solicited mating from the males primarily at midcycle, about the time when the concentration of testosterone was maximal. No mating occurred during the mid- to late luteal phase after progesterone concentrations were elevated. Both males and females initiated mating during the midcycle, periovulatory period, but male initiative accounted for most mating that was temporally dissociated from that period. Individual differences between males and among females contributed to the variability in results. Confinement of a male and female in relatively small quarters appears to interact with certain aspects of species-typical behaviour to distort patterns of mating in laboratory tests. Data on behaviour of gorillas in the wild contributed to interpretation of the laboratory results and suggest an enlightened approach to the captive maintenance and breeding of gorillas. An important consideration in promoting captive breeding of gorillas seems to be the provision of options to the female for regulating the frequency and distribution of mating in the cycle.     

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.     

Species and sex identification of western lowland gorillas (Gorilla gorilla gorilla), eastern lowland gorillas (Gorilla beringei graueri) and humans

Methods for the identification of the sex and species of individuals from samples non-invasively taken from humans and gorillas were established. Amplification of a segment of amelogenin (AMG), which is an X–Y homologous gene, using two pairs of primers from human AMG, revealed both X- and Y-specific bands. The possibility of sex identification was examined by typing the AMG gene using hair and fecal samples from captive western lowland gorillas (Gorilla gorilla gorilla) in Japan and hair samples from wild eastern lowland gorillas (Gorilla beringei graueri) in the Kahuzi-Biega National Park, Democratic Republic of Congo, which were sexed by direct observation. Species-specific bands of AMG in gorillas and humans were identified by restriction fragment length polymorphisms analysis. These tests could be used for sexing unidentified individuals of wild western and eastern lowland gorillas, and screening contamination of human DNA from non-invasively acquired samples.     

Effects of a recurring late-night event on the behavior and welfare of a population of zoo-housed gorillas

The impact of visitors on the well-being of captive animals presents both positive and potentially negative consequences. While some amount of novelty through visitor stimulation offers the opportunity for a more complex captive environment, anecdotal evidence from primate staff observations at the Smithsonian's National Zoo and Conservation Biology Institute suggested that gorillas exhibited increased restlessness during the annual month-long late night ZooLights (ZL) event than before it. The current study compared activity budgets, aggression (interactions involving contact between conspecifics and displays toward visitors), and abnormal behaviors in two groups of socially housed gorillas for 1-month periods before, during, and after the 2015 ZL event. We also compared the fecal glucocorticoid metabolite profiles of all six gorillas across these same observation periods. Physiologically, most individuals appeared to cope appropriately with the increased visitor presence during the event. We saw little difference in contact aggression; however, abnormal behavior was observed in some gorillas during and after the event, which highlights the importance of individual analysis and data interpretation. As predicted, we found that the majority of gorillas rested less during ZL than during other observation periods, particularly adult females in the mixed sex troop. Preliminary results of this study aided the decision of zoo management to close initially the Great Ape House and subsequently most animal buildings during future ZL events to avoid the potential disruption of normal activity patterns. While the findings of this study were mixed as to the impact of the event on these gorillas, the results suggest that zoos should carefully consider the possible ramifications of keeping great ape buildings open for lengthy multi-night events.     

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.     

Exchange of objects between humans and captive western lowland gorillas

An experiment was carried out to assess the ability of captive western lowland gorillas (Gorilla g. gorilla) to exchange objects with a human partner. Before the exchange itself, individuals had to learn to give an item to the experimenter. Four individuals out of nine performed active giving. After that familiarization with giving behaviour, two kinds of exchanges, of increasing complexity, were tested with gorillas. Simple exchange (give C to obtain D) was the first procedure and six gorillas out of nine succeeded. Double exchange (give B to receive C, then give back C to obtain D) was performed only by three individuals and triple exchange (give A to receive B, give back B to receive C, then give back C to obtain D) was performed only by two individuals. Different types of errors were scored, as well as social constraints on learning. Results showed that (1) naive gorillas are able to get a reward (D) in an experimental exchange situation; and (2) the complex rules of multiple successive exchanges were not easily understood by gorillas.     

Digesta Passage,Digestibility and Behavior in Captive Gorillas Under Two Dietary Regimens

Gorilla adaptation has been debated in recent years given the wide variation among diets of gorillas in different habitats. Gorillas are the largest of living primates, have large colons and should be capable of processing tough foods. Preliminary captive studies have suggested that they may well have long average gut retention times relative to smaller hominoids, which should facilitate digestive efficiency in their wild counterparts. Indeed, wild gorillas consume large amounts of fibrous foods as staples or fall-back foods across their range, in response to habitat-related or seasonal changes in fruit availability. Fluctuations in diet might be matched by changes in digesta passage and digestibility, with possible selective retention of harder to digest items. We further studied digestive processes via chemical cobalt and chromium markers to track liquid and solids, as they passed through the guts of gorillas at the San Francisco Zoo (SFZ). In addition, we examined the effects of variation in captive diets on intake, digesta passage, digestion and behavior. The SFZ gorillas exhibited high digestibility coefficients, and gut passage was long relative to those of smaller-bodied hominoids. The results permit us to understand more fully the relationships of digestive processes to adaptation and dietary flexibility in the wild and to inform the development of dietary recommendations to improve the well-being of captive gorillas.     

Paternity determination in captive lowland gorillas and orangutans and wild mountain gorillas by microsatellite analysis

Paternity exclusion studies provide useful information for testing certain theories of behavioral ecology and for the management and conservation of both wild and captive populations of endangered species. This study used eight human nuclear microsatellite loci, in the absence of species-specific PCR primers, to genetically identify the sires of 12 captive lowland gorillas (Gorilla gorilla gorilla) and 2 captive orangutans (Pongo pygmaeus pygmaeus andPongo p. abelii). Parentage assignments were confirmed by excluding all except a single potential sire for each offspring with the least two loci. Sire-offspring relationships were verified in 12 of the 14 cases, and reassigned in the case of two gorilla offspring. The orangutan paternity typing was supplemented by DNA fingerprinting. Additionally, five of the eight microsatellite loci, in conjunction with behavioral data, were used for a non-exhaustive set of paternity exclusions for five wild mountain gorillas (Gorilla g. beringei). The eight loci described in this study should be useful additions to the tools available for the study of genetics in the great apes.     

The cryptic genetic structure of the North American captive gorilla population

Western lowland gorillas (Gorilla gorilla gorilla) were imported from across their geographical range to North American zoos from the late 1800s through 1974. The majority of these gorillas were imported with little or no information regarding their original provenance and no information on their genetic relatedness. Here, we analyze 32 microsatellite loci in 144 individuals using a Bayesian clustering method to delineate clusters of individuals among a sample of founders of the captive North American zoo gorilla collection. We infer that the majority of North American zoo founders sampled are distributed into two distinct clusters, and that some individuals are of admixed ancestry. This new information regarding the existence of ancestral genetic population structure in the North American zoo population lays the groundwork for enhanced efforts to conserve the evolutionary units of the western lowland gorilla gene pool. Our data also show that the genetic diversity estimates in the founder population were comparable to those in wild gorilla populations (Mondika and Cross River), and that pairwise relatedness among the founders is no different from that expected for a random mating population. However, the relatively high level of relatedness (R = 0.54) we discovered in a pair of known breeding pairs reveals the need for incorporating genetic relatedness estimates in the captive management of western lowland gorillas.     

Plasma alpha-tocopherol, retinol, cholesterol, and mineral concentrations in captive gorillas

Vitamins A, E, cholesterol, and mineral (calcium, copper, iron, magnesium, phosphorus, selenium, sodium, and zinc) concentrations were examined in the plasma of 74 captive lowland gorillas aged newborn to 41 years. Effects of age or sex on measured parameters were not significant. Plasma Mg and Ca concentrations were lower than reported captive gorilla means, whereas Na and P were higher. Since comparative gorilla values for certain blood components (vitamins E and A, copper, and selenium) are lacking, normal human values may provide the best available indicators for evaluating the plasma levels of these components in gorillas.     

Nest Building in Captive Gorilla gorilla gorilla

Although various aspects of gorilla nest building have been described in wild populations, nest-building behavior of captive gorillas has not been subject to much scientific review. We observed nest building in 17 gorillas during three periods: summer baseline, winter baseline, and winter treatment, in which the amount of available nesting material was doubled. We conducted observations exclusively in the indoor holding area in the hour following evening departure of animal care staff. During baseline, gorillas engaged in nest-building on 3.1% of scans and were on a constructed nest on 27.9% of scans. Overall, gorillas spent significantly more time on elevated nests than on floor nests. There were no statistically significant sex, age class, or rearing history differences in nest building, time spent on a nest, or nest location preference. Nest building consisted of both gathering and manipulating materials. The gorillas spent significantly more time building nests in winter than in summer. Additionally, they were more often on elevated nests during winter than summer. Doubling the amount of nesting material did not increase nest building, but it increased the number of floor nests. Our results suggest that providing adequate materials to captive gorillas for nest building may facilitate performance of species-typical nest-building, minimize competition among individuals for nesting sites and materials, and permit individual thermoregulation.     

Variability in the developmental life history of the genus Gorilla

Life history is influenced by factors both intrinsic (e.g., body and relative brain size) and extrinsic (e.g., diet, environmental instability) to organisms. In this study, we examine the prediction that energetic risk influences the life history of gorillas. Recent comparisons suggest that the more frugivorous western lowland gorilla shows increased infant dependence, and thus a slower life history, than the primarily folivorous mountain gorilla to buffer against the risk of starvation during periods of food unpredictability. We further tested this hypothesis by incorporating additional life history data from wild western lowland gorillas and captive western lowland gorillas with the assumption that the latter live under ecological conditions of energetic risk that more closely resemble those of mountain gorillas and thus should show faster life histories than wild members of the species. Overall, we found captive western lowland and wild mountain gorillas to have faster developmental life histories than wild western lowland gorillas, weaning their infants approximately a year earlier and thus reducing interbirth intervals by a year. These results provide support that energetic risk plays an important role in determining gorilla life history. Unlike previous assertions, gorillas do not have substantially faster life histories, at least at the genus level, than other great apes. This calls for a re‐evaluation of theories concerning comparative ape life history and evolution and highlights the need for data from additional populations that vary in energetic risk. Am J Phys Anthropol 152:165–172, 2013. © 2013 Wiley Periodicals, Inc.     

Environmental influences on the activity of captive apes

Forty-one zoological gardens in seven European countries were visited to investigate activity level in captive environments for great apes. Forty-three groups of gorillas and 68 groups of orangutans were observed. The seven factors quantified for each of the environments were size of the enclosure, usable surface area, frequency of feeding, number of animals, and number of objects (stationary, temporary, and movable). Activity level of each group was measured by instantaneous scan sampling for one hour on two consecutive days. For both species, the factors most highly related to activity level were number of animals, and stationary, temporary, and movable objects. The usefulness of these variables for predicting group activity level was different for the two species, however. Factors important for gorillas were stationary and temporary objects, while stationary and movable objects were significant for orangutans. These findings suggest that objects within environments may be more important for captive apes than the size or construction of the enclosure. Also, the types of objects that need to be included in environments may be related to the natural behavior of the individual species.     

Attempting to reduce regurgitation and reingestion in a captive chimpanzee through increased feeding opportunities: a case study

Persistent regurgitation and reingestion is an abnormal behavior seen in many captive NHPs, particularly gorillas and chimpanzees. Successful reduction of regurgitation in captive gorillas has been achieved by providing browse, such as branches and leaves, and feeding continuously throughout the day. However, this modality has not been tested in chimpanzees. The authors tested these methods in a 15-year-old male chimpanzee (Pan troglodytes) with a seven-year history of regurgitation and reingestion by alternately providing additional opportunities to forage or giving daily browse. The results show that providing browse on a daily basis models the feeding behavior of wild chimpanzees and is a successful way to reduce regurgitation and reingestion in a chimpanzee unresponsive to previous dietary changes.     

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.     

Long‐term proximity relationships in a captive social group of western lowland gorillas (Gorilla gorilla gorilla)

To visualize long‐term social relationships among 12 gorillas in a captive breeding group at the San Diego Wild Animal Park, San Diego, CA, the multidimensional scaling (MDS) procedure was applied to proximity (within 5 m) values collected in five different periods over 2.5 years. The resulting two‐dimensional representations clearly show that in samples taken during this 2.5‐year period, the silverback male was surrounded by five adult females, while three infant or young juvenile females, gathered in a body, remained between the silverback male and adult females. Some adult females maintained proximity to the silverback male more frequently than other adult females throughout the five periods. Unlike mountain gorillas in the wild, females with dependent offspring did not tend to stay near the silverback male more frequently than other females, and related females did not tend to spend more time near each other than non‐related females. Three older juvenile or young adult males were plotted the furthest from the silverback male, with gradual changes with increasing age. The usefulness of the MDS procedure, which can be used to visualize easily and clearly the social relationships among individuals, is discussed from the viewpoint of the management of breeding groups of captive gorillas. Zoo Biol 20:197–209, 2001. © 2001 Wiley‐Liss, Inc.