Preference for structural environmental features in captive lowland gorillas (Gorilla gorilla gorilla)

Increased interest in the behavioral effects of captive environments and advances in zoo design have resulted in a proliferation of “naturalistic” animal habitats. Although scientists have demonstrated that such exhibits have some positive effects on behavior, very little is known about the complex relationships between these specialized environments and behavior. This study sought to determine preferences for structural environmental features, such as slope and trees, exhibited by captive lowland gorillas (Gorilla gorilla gorilla). An average of 496 location scans were collected on each of 23 gorillas, housed in 6 groups. The results indicate that enclosure usage was significantly associated with the features of slope, nearness to holding facility, and presence of environmental components additional to substrate (e.g., tree or rock). In particular, areas with flat ground that were near the holding building and that included at least one component additional to substrate were preferred by all animals. © 1993 Wiley-Liss, Inc.     

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.     

Effects of Selected Behavioral Enrichment Devices on Behavior of Western Lowland Gorillas (Gorilla gorilla gorilla)

Environmental complexity plays an integral role in the activity and psychological well-being of primates. The experiment described in this article evaluates the effects of nonintrusive, inexpensive, and easily managed behavioral enrichment devices on the behavior of a group of captive Western lowland gorillas. Devices used included cardboard boxes containing food items, paper bags containing food items, burlap rags, and willow and maple browse. The enrichment devices increased foraging, social play, and solitary play behaviors. Sedentary behaviors decreased. Rags, bags, browse, and boxes did not statistically decrease the incidence of regurgitation/reingestation or coprophagy. Depending on the type of enrichment item used, the effects on agonism and manipulation of enrichment item were variable. To make informed management decisions about the psychological well-being of captive animals, it is important to objectively quantify and examine the influences on their behavior.     

Effects of selected behavioral enrichment devices on behavior of Western Lowland Gorillas (Gorilla gorilla gorilla)

Environmental complexity plays an integral role in the activity and psychological well-being of primates. The experiment described in this article evaluates the effects of nonintrusive, inexpensive, and easily managed behavioral enrichment devices on the behavior of a group of captive Western lowland gorillas. Devices used included cardboard boxes containing food items, paper bags containing food items, burlap rags, and willow and maple browse. The enrichment devices increased foraging, social play, and solitary play behaviors. Sedentary behaviors decreased. Rags, bags, browse, and boxes did not statistically decrease the incidence of regurgitation/reingestation or coprophagy. Depending on the type of enrichment item used, the effects on agonism and manipulation of enrichment item were variable. To make informed management decisions about the psychological well-being of captive animals, it is important to objectively quantify and examine the influences on their behavior.     

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.     

A preliminary behavioral comparison of two captive all-male gorilla groups

Gorillas live in polygamous harem groups, generally composed of one male, several adult females, and their offspring. With an equal numbers of male and female gorillas born in captivity, however, housing gorillas in social breeding units inevitably means that some males will not have access to female social partners. Thus, the future of the captive gorilla population depends on the collective ability of zoos to house equal numbers of males and females. This study examined the behavioral profiles of two all-male groups of captive lowland gorillas (Gorilla gorilla gorilla) to provide information on this type of housing situation. One group consisted of three subadult individuals, while the other consisted of two subadults and a silverback. Data were collected during two 6-month intervals, for a total of 284 hr. The behavioral profiles of the animals were stable over the course of the study but proximity patterns changed. Differences in feeding, solitary play, and object-directed behavior were found between groups, while no significant differences were observed in affiliative or agonistic social behavior. At both institutions, group cohesion appeared to be high, particularly between subadults; these individuals spent approximately 10% of their time engaging in social behavior and 25-50% of their time in close proximity (within 5 m). However, the Zoo Atlanta males spent significantly more time within 1 m and 5 m of each other than the Santa Barbara males, which may reflect a higher level of cohesiveness among members of the Zoo Atlanta group. The behavioral profiles of the animals in this study were similar to those found in bachelor groups of wild mountain gorillas. One notable exception was the absence of homosexual behavior between the silverback and subadults in Santa Barbara and the low frequency of this behavior between subadults in both groups. Although more longitudinal data are needed, these data suggest that all-male groups can be a feasible housing strategy for males at certain periods of their life span. Zoo Biol 20:27-40, 2001. Copyright 2001 Wiley-Liss, Inc.     

Postconflict behavior in captive western lowland gorillas (Gorilla gorilla gorilla)

Postconflict (PC) behaviors, including reconciliation and consolation, have been observed in many primate and several nonprimate species. Using the PC-matched control (MC) method, PC behavior was examined in two groups (n=13) of captive western lowland gorillas, a species for which no conflict resolution data have been published. Analyses of 223 conflicts showed significantly more affiliation between former opponents after a conflict when compared to control periods, indicating reconciliation. Results also showed significantly more affiliation between the victim and a third-party after a conflict, indicating consolation. Both solicited and unsolicited consolation were observed. The majority of the affiliative interactions observed for both reconciliation and consolation were social proximity, which suggests that unlike most nonhuman primates, proximity, rather than physical contact, may be the main mechanism for resolving conflicts in western lowland gorillas. PC behavior was not uniform throughout the groups, but rather varied according to dyad type.     

Day-journey length and daily diet of solitary male gorillas in lowland and highland habitats

We compared day-journey length and daily diets of solitary male gorillas in lowland versus highland habitats. Solitary males in tropical forests of Zaire tend to travel longer distances, to visit more types of vegetation, and to consume more kinds of food than a solitary male mountain gorilla in the Virunga Volcanoes did. The number of feeding sites per day is larger and the mean distance between feeding sites is far longer for the former than the latter. These observations may reflect differences in food breadth and availability between highland and lowland habitats. The herbaceous plants that are eaten by mountain gorillas are densely and evenly distributed in the higher montane forest of the Virungas, where gorillas need not cover long distances to search for food. In contrast, herbaceous plants are scarce in primary and ancient secondary forests of lowland habitats, where gorillas travel long distances and eat various fruits and insects. The patchy and unpredictable distribution of foods may extend the distances over which gorillas search for food in the lowland habitat. However, solitary males showed a prominent reduction in day-journey length and changed their choices of food during the nonfruiting season (the long rainy and dry seasons) in the lowland habitats. This strategy may have developed during the Pleistocene and may have enabled them to enlarge their ranges to the higher montane forests, where fruits are sparse throughout the year.     

Gorilla ecology and behavior

Many factors influence the evolution of primate grouping patterns, including phylogeny, demographic and life-history variables, and ecological factors such as access to food, predation pressure, and avoidance of infanticide. The interaction between these factors determines social organization.¹ Because western lowland and mountain gorillas differ so dramatically in their habitats and foraging strategies, they provide a valuable opportunity to assess how changes in ecology influence this balance. Mountain gorillas live in high-altitude montane forests, are herbivorous, and live in stable and cohesive groups. Western lowland gorillas live in lowland rainforest and are much more frugivorous than mountain gorillas. It is not yet clear to what extent incorporating significant quantities of fruit in the diet influences western lowland gorilla sociality because they have been studied much less than have mountain gorillas. However, what is known about their behavior hints that there may also be considerable differences in their social organization, including changes in group size and cohesion and in the frequency and type of intergroup encounters. Gorillas thus provide a unique opportunity to reevaluate proposed models of ecological influences on social organization in African apes.© 1998 Wiley-Liss, Inc.     

Ecological divergence and talar morphology in gorillas

Gorillas occupy a variety of habitats from the west coast to eastern central Africa. These habitats differ considerably in altitude, which has a pronounced effect on forest ecology. Although all gorillas are obligate terrestrial knuckle‐walking quadrupeds, those that live in lowland habitats eat fruits and climb more often than do those living in highland habitats. Here we test the hypothesis that gorilla talus morphology falls along a morphocline that tracks locomotor function related to a more inverted or everted foot set. This proposed morphocline predicts that gorillas living in lowland habitats may have a talocrural joint configured to facilitate a more medially oriented foot during climbing, suggesting that they may be more adaptively committed to arboreality than gorillas living in highland habitats. To quantify the relative set of the foot in gorillas, we chose two three‐dimensional measurements of the talocrural joint: mediolateral curvature of the trochlea and relative surface area of the lateral malleolus. Our results show that, in comparison to their eastern counterparts, western gorillas have talar features that reflect a more medially directed sole of the foot. This morphology likely facilitates foot placement in a wider range of positions and minimization of shearing stresses across the joint when the foot is loaded on more curved or vertically oriented substrates as occurs during climbing and other arboreal behaviors. In contrast, eastern gorilla talar morphology is consistent with habitual placement of the foot with the sole directed more inferiorly, suggesting more effective loading during plantigrade push‐off on terrestrial substrates. Am J Phys Anthropol 153:526–541, 2014. © 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.     

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.     

Gorilla Behavior Index revisited: Age,housing and behavior

While personality and temperament assessments are becoming more common in animal science as a means for predicting behavior patterns, they are virtually unstudied in exotic animals outside of chimpanzees. We assessed behavioral profiles of 119 male gorillas using the Gorilla Behavior Index (GBI) and paired this assessment with behavior data on 25 male gorillas from our ongoing analysis of multi-male gorilla groups in North America. This comparison was made to determine if the GBI could be predictive of behavior patterns, with the hope that this could eventually be utilized to aid in the management of multi-male gorilla groups. With few exceptions, GBI factor scores were not related to age of subjects or their current housing condition. Individuals scoring high on the Extroverted factor were more likely to initiate and receive affiliative behaviors, but they were also more likely to initiate contact aggression. Those gorillas who scored high on the Dominant factor were more likely to initiate displacements and less likely to receive them. Gorillas rated as more Fearful were less likely to initiate displacements and those rated as less Understanding were more likely to initiate non-contact aggression. Two facts are evident from these data: (1) further work needs to be done to verify that the GBI is indeed assessing traits and not current behavioral states and (2) any relationships with behavior frequency are relatively weak. In addition to further exploration of the GBI we recommend other assessments to compliment the GBI to establish stronger links between subjective assessments and objective behavior patterns. If established, these short-term assessments may be combined with other historical information on these animals, such as age, rearing history, the number of animals in the group, and the design of the exhibit, to aid in forming and maintaining multi-male gorilla groups in captivity.     

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.     

Proximity patterns of female western lowland gorillas (Gorilla gorilla gorilla) during the six months after parturition

Studies of wild mountain gorillas have demonstrated strong preferences among new mothers for the silverback. Protection against infanticide has been theorized to be the primary cause for this attraction. We examined social partner preferences in captive western lowland mothers during the 6 mo after parturition and found that juveniles and females were the primary members of the new mothers' social network. Mothers spent significantly more time in close proximity with both of these subgroups than with the silverback. Proximity patterns changed over time: new mothers spent more time near females in the month after parturition than in the month prior to parturition, and spatial proximity increased again in months 2-6 postparturition. These findings differ from those reported for wild mountain gorillas, which may reflect the lack of infanticide risk in captivity. Given current hypotheses that infanticide may be a limited in western lowland gorillas, the social partner preferences observed here may be indicative of patterns in wild populations.     

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.     

Space use selectivity by chimpanzees and gorillas in an indoor-outdoor enclosure

Understanding the relationship between physical environments and nonhuman primate behavior is a key element for effective care and management in a range of settings. The physical features of the captive environment, including not only gross useable space but also environmental complexity, can have a significant influence on primate behavior and ultimately, animal welfare. But despite this connection, there remains relatively little conclusive data on how captive primates, especially great apes, use the spaces provided to them, especially in modern, indoor-outdoor enclosures that have become more prevalent in recent years. In this study, we used four years of detailed data on where 23 great apes (chimpanzees and gorillas) positioned themselves within a modern, indoor-outdoor zoo enclosure to determine not only how the apes utilized their space but also how access to outdoor areas affected their spatial selectivity. We found that both species used relatively little of their available space: chimpanzees and gorillas spent half their time in only 3.2 and 1.5% of their useable three-dimensional space, respectively. Chimpanzees utilized the outdoor space more than gorillas, but access to the outdoors did not affect space selectivity in the indoor area for either species. Although both species of ape were highly selective in their space use, consideration should be given to the importance of providing the choice to locate in a variety of spaces, including outdoor areas. These data represent an extremely detailed account of space selectivity by great apes in an indoor-outdoor environment and have substantial implications for future facility design and captive primate management.     

Testicular atrophy in captive gorillas (Gorilla g. gorilla)

Testes were obtained at post mortem from three Western lowland gorillas, two Bornean orang-utans and one Chimpanzee. All specimens were adults which had died in captivity. Histological examination revealed that two gorillas exhibited complete degeneration of the seminiferous tubules and that the testes contained large amounts of interstitial tissue. Some, less obvious, signs of degeneration were noted in the third specimen but poor preservation of the material hampered interpretation of these features. The testes of the Orang-utans and Chimpanzee were structurally normal. Testicular atrophy in captive gorillas may be more common than is generally realized and there is a need for research on fertility and reproductive endocrinology of male specimens. At the moment it is not possible to identify the causes of testicular dysfunction in captive gorillas.     

Sexual behavior and urinary ovarian hormone concentrations during the lowland Gorilla menstrual cycle

Sexual behaviors were recorded and urinary concentrations of total estrogens and pregnanediol-3-glucuronide (Pdg) measured during six normal menstrual cycles from two female lowland gorillas in a stable, captive group. Frequencies of female presentations, mounts, and copulations were positively associated with peak estrogen values but not with elevations of Pdg. These results support the observation that sexual behaviors in the gorilla occur most frequently in the periovulatory period and that copulations serve primarily a sexual function.     

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.