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Jul 27, 2005 - Use of space in a non-naturalistic environment by chimpanzees (Pan troglodytes) and lowland gorillas (Gorilla gorilla gorilla). Stephen R. Ross.
Applied Animal Behaviour Science 96 (2006) 143–152 www.elsevier.com/locate/applanim

Use of space in a non-naturalistic environment by chimpanzees (Pan troglodytes) and lowland gorillas (Gorilla gorilla gorilla) Stephen R. Ross a,*, Kristen E. Lukas b,1 a

b

Lincoln Park Zoo, 2001 North Clark St., Chicago, IL 60614, USA Cleveland Metroparks Zoo, 3900 Wildlife Way, Cleveland, OH 44109, USA Accepted 7 June 2005 Available online 27 July 2005

Abstract 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. # 2005 Elsevier B.V. All rights reserved. Keywords: Captive environment; Space use; Chimpanzees; Gorillas; Environmental preferences

1. Introduction Animal facilities face numerous challenges in providing for the physical and psychological needs of their animal residents. Inappropriate housing can result in poor * Corresponding author. Tel.: +1 312 742 7263. E-mail addresses: [email protected] (S.R. Ross), [email protected] (K.E. Lukas). 1 Tel.: +1 216 635 2523. 0168-1591/$ – see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2005.06.005

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breeding success, animal safety concerns, or compromised animal well-being often expressed through stereotyped behavior patterns (Mason, 1991; Carlstead, 1996). With these risks in mind, animal managers have sought effective methods to improve the ways in which a variety of captive animals are housed. Because of their size, strength and intelligence, great apes pose some of the greatest challenges to those invested in designing effective captive environments for animals. Designers and managers must consider issues of safety, functionality and durability (Coe et al., 2001) as well as meeting federal standards that require that captive environments appropriately provide for the psychological wellbeing of the apes (USDA, APHIS, 1991). Chimpanzees and gorillas are the two most common great apes found in captive facilities in North America (Fulk, 2004). In captivity, their behavior has been shown to be affected by a variety of factors including a wide range of environmental enrichment strategies. Although research on temporary environmental enhancements has flourished, there has been relatively little focus on how captive apes interact with more permanent elements in their environment. Anecdotal and descriptive information on the relevance of environmental features for captive apes suggests that they tend to locate themselves near vertical structures and show differential use of particular parts of habitats (Traylor-Holzer and Fritz, 1985; Steele et al., 1993; Goff et al., 1994; Bloomsmith et al., 1999; Ross and Lukas, 2000). Adult chimpanzees in captive environments seem to have strong preferences for particular areas of their space. Studies have shown increased use of enclosure perimeters and climbing structures (Riss and Goodall, 1976; Clarke et al., 1982; Riddle et al., 1982). Gorillas have been shown to prefer flat ground, especially near the holding buildings (Ogden et al., 1993; Stoinski et al., 2001; Stoinski et al., 2002); however, gorillas’ inordinate use of areas near holding buildings may be diffused with regular alternations between exhibits (Lukas et al., 2003a). In addition to the challenges of providing environments that function properly, zoo exhibits must also live up to expectations placed on them by the visiting public. Naturalistic exhibits have become the standard for new zoo exhibits, providing a range of benefits for the visitor experience and to the animals that inhabit them. They have been shown to decrease stereotypical behavior patterns in a variety of ape species while having a positive effect on rates of aggression and affiliation (Clarke et al., 1982; Akers and Schildkraut, 1985; Maple and Finlay, 1986). But despite their apparent benefits, there are many situations where naturalistic enclosures are unlikely to ever be used. Laboratories and sanctuaries that do not cater to a visiting public are unlikely to spend funding on features that increase the aesthetic quality of an enclosure when an equally effective functional solution might be available. Likewise, some small zoos may not have the funding to spend on naturalistic exhibits that may cost several million dollars more than similarly structured, but less aesthetically pleasing exhibits. As such, there is a need to understand not only how apes use naturalistic spaces, but also non-naturalistic spaces. Recent data on these environments are less abundant. The primary goal of this study was to provide such data to help facilities direct the future design of great ape habitats, specifically those that are unlikely to utilize naturalistic themes. A subsequent objective was to compare space use patterns of chimpanzees and gorillas in similar non-naturalistic zoo environments and to document their structural preferences. The ability to study chimpanzees and gorillas in virtually identical physical

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environments provides a rare opportunity to equitably compare and contrast the specific requirements of the two species.

2. Methods Subjects were 20 apes (14 western lowland gorillas and six common chimpanzees) ranging from 3 to 42 years of age and housed at the Lester E. Fisher Great Ape House (GAH) at Lincoln Park Zoo in Chicago, IL. Gorillas lived in one of two social groups, each consisting of a single adult male, several adult females and their immature offspring. Chimpanzees lived in two subgroups of three (one adult male, two adult females) until the groups were merged to form a single multimale group of six. The GAH was made up of six similarly shaped rooms in a circular configuration (Fig. 1). Four of these rooms were used primarily for two gorilla groups (1 + 2, 4 + 5) and two for the chimpanzees (3 and 6). Individual rooms ranged in size from 35 to 55 m2 with ceilings ranging from 7.7 to 10.5 m high. The enclosures were bedded heavily with straw and food was routinely scattered in the straw to allow the gorillas and chimpanzees to actively forage throughout the day. All data were collected by the first author over a two-year period from August 2000 to September 2002. One 10 min observation per individual was taken every week at times balanced between 10:00 and 17:00 h. During the session, information on the subject’s location was recorded at 60 s intervals. The vertical locations were categorized as floorlevel, first-tier (above floor level but below 3 m high), second-tier (above 3 m from the floor and below 3 m from the ceiling), and a third-tier (within 3 m of the ceiling). Because the heights of the rooms varied, the second-tier ranged between 1.7 and 4.5 m. When an ape’s body overlapped two tiers, the determination was based on the location of the majority of their torso. In addition to vertical location the individual’s proximity (within 1 m) to structural elements of the environment was recorded. These elements included structural (walls, doorways, glass windows, mesh) features as well as permanent (steel climbing

Fig. 1. Schematic of GAH configuration.

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structures) and temporary (ropes, cargo nets) elements. Because the permanent and temporary elements were highly variable between exhibits, the analyses described in this paper will focus strictly on preferences for the structural features of the exhibit. In cases where apes were within 1 m of multiple elements, the element to which they were closest was scored. Between 67 and 101 sessions were collected for each ape for a total of 1876 sessions (312.7 h) over the course of the study. The variability in data quantity between subjects is a result of time that some subjects spent off exhibit, either because of illness or transfer to another facility. To quantify the space available to the apes, measurements in three dimensions were made for each of the six rooms. A fraction of the three-dimensional space could not be occupied by the apes due to the lack of supporting structures and therefore was not added to the total. The amount of available space included floor space and all areas that contained supporting features (such as climbing structures, ropes and mesh). This information was used to estimate the expected frequency of the dependent variables given a random distribution throughout the exhibit. For instance, 10.5% of the available space in Exhibit 1 was ‘‘adjacent to the public viewing glass’’. If the apes moved randomly through the exhibit without any environmental preferences, we would expect them to spend 10.5% of their time ‘‘adjacent to the public viewing glass’’. 2.1. Analysis Analyses were performed using Systat1 version 10. Data on vertical space use were summarized by individual and then by species. Subsequent non-parametric tests were used as each group contained a relatively small number of subjects. Chi-square tests were used to compare the ‘‘expected’’ values based on volumetric measurements to the observed values from the behavioral data for each species. Post-hoc Wilcoxon signed rank tests determined statistical differences between these values at each specific tier or location.

3. Results 3.1. Vertical space use Chimpanzees distributed their time relatively evenly between tiers of the exhibit. Time spent on the ground ranged from 16 to 52% and time spent within two meters of the ceiling ranged from 14 to 66%. Males proved to be the most extreme with the younger male (MC) spending the most time off the ground, and the older male (KE) spending the most time on the substrate. Gorillas were in two groups, but showed similar patterns of space use. Both males were considerably different than females by spending large amounts of time on the ground, 88 and 69% respectively. Among females, there was relatively little variability within groups in the way that they used vertical space. These behavioral data were compared to expected values based on volumetric measurements of the exhibits. Chi-square analyses showed that gorillas distributed their time in the four vertical tiers differently than would be expected by random movements (X2 = 16.4, p < 0.01, d.f. = 3). Post-hoc Wilcoxon tests were used to investigate

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Fig. 2. Expected and observed percent of time in each of four vertical tiers by gorillas (*P < 0.05).

differences between observed and expected values at each tier (Figs. 2 and 3). Gorillas spent more time on the floor than would be expected if they showed no environmental preferences (Z = 1.992, p = 0.044, n = 14). The middle tier was significantly under-utilized (Z = 3.180, P = 0.001, n = 14), but there were no significant differences in available space within the top 3 m of the exhibit, and the time that the gorillas spent there. For chimpanzees, the level showing the highest rates of use was the top tier, near the ceiling and skylights, where chimpanzees spent almost 42% of their time, even though it made up less than 20% of the exhibit. The time spent in the top tier was significantly greater than expected by the volumetric measurements (Z = 1.992, p = 0.044, n = 6). The middle tier was significantly under-utilized (Z = 2.201, p = 0.028, n = 6), and chimpanzees used the bottom two tiers at rates that did not differ from expected values.

3.2. Environmental elements Fig. 4 shows the gorillas’ preferences for different types of vertical surfaces in their exhibit. The gorillas in this study showed significant preferences for the areas adjacent to the mesh barrier to the keeper area (Z = 3.180, p = 0.001, n = 14), and corners (Z = 2.201, p = 0.028, n = 14). Between 12 and 15% of the space was not adjacent to any form of vertical structure. The time spent in these open areas was significantly lower (Z = 3.180, p = 0.001, n = 14) than would be predicted by the volumetric measurements. Finally,

Fig. 3. Expected and observed percent of time in each of four vertical tiers by chimpanzees (*P < 0.05).

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Fig. 4. Expected and observed percent of total time spent adjacent to environmental elements by gorillas (*P < 0.05).

Fig. 5. Expected and observed percent of total time spent adjacent to environmental elements by chimpanzees (*P < 0.05).

doorways were highly preferred areas as the gorillas spent nine times more time there than expected (Z = 2.201, p = 0.028, n = 14). Fig. 5 illustrates the chimpanzees’ use of space adjacent to vertical elements. The chimpanzees in this study spent more time than expected adjacent to the mesh barrier to the keeper area (Z = 2.201, p = 0.028, n = 6) and in corners (Z = 3.180, p = 0.001, n = 6). The time spent adjacent to the public glass barrier and the solid concrete walls were statistically similar to values predicted by volumetric measurements. Doorways were used much more than predicted by the space they occupied (Z = 1.992, p = 0.044, n = 6) and they occupied open areas significantly less than expected (Z = 3.180, p = 0.001, n = 6).

4. Discussion Partitioning the exhibit into vertical tiers and areas adjacent to prominent features illustrates the environmental preferences of these gorillas and chimpanzees. In a nonnaturalistic setting, both species showed strong preferences for particular features of the environment that were consistent with previous studies in a variety of settings, both naturalistic and non-naturalistic. Prioritizing these features can be a useful design tool when planning for the renovation or redesign of existing ape enclosures at zoological parks and other animal facilities.

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4.1. Use of vertical space Gorillas tended to use the lower tiers of the exhibit much more so than those closer to the ceiling. This is not surprising as wild gorillas are likely the least arboreal of the great ape species, and much less arboreal than chimpanzees that live in similar habitats in Africa (Remis, 1998). They tend to use trees primarily for feeding and in the case of lowland gorillas, for night nests (Remis, 1993). There are substantial differences in arboreality between mountain gorillas and lowland gorillas but recent studies suggest this is a behavioral difference that reflects environmental adaptations rather than a species–specific pattern of obligate terrestriality based on body-size (Remis, 1998). The same author suggests that several factors, including tree size, party size, body size, and social context, influence the arboreal behavior of lowland gorillas. Many of these factors have reduced impact in captive environments. For instance, tree limbs are much less likely to break if they are made of steel or concrete and therefore should not limit larger bodied individuals from climbing off the ground as natural tree limbs might. There is relatively little literature on the use of vertical space by captive gorillas, but in one study of nest-building behavior in captive lowland gorillas, Lukas et al. (2003b) reported that gorillas spent significantly more time on elevated nests than on floor nests, especially during winter months. Lack of arboreality may be due not only from the species natural history but also to lack of opportunities. An unpublished survey of 25 gorilla exhibits at 12 accredited North American zoos showed that only 28% provided trees with which the apes could climb (Lukas and Ross, unpublished). Exhibits such as those studied here demonstrate that gorillas will use the highest tier of their exhibit at approximately equal proportions to its availability. Chimpanzees in this study showed significant preferences for available spaces high off the ground. These patterns are consistent with observations of wild chimpanzees that spend between 33 and 68% of their time in trees and the degree of arboreality varies with their habitat (Doran and Hunt, 1994). Other studies of vertical space use with captive chimpanzees have shown similar patterns of arboreal preferences (Nadler and Braggio, 1974; Traylor-Holzer and Fritz, 1985). Enclosures that provide these types of vertical opportunities are much more common for chimpanzees, with structures as high as 15 m (Primate Research Center, Kyoto University). As with gorillas, the middle tier of the enclosure was used significantly less than expected based on volumetric measurements. One explanation for this is that the majority of elements in this tier were transitory, that is they were used almost exclusively for locomotion rather than as a resting location. This tier was primarily made up of ropes without many platforms or nesting sites and emphasizes the need to plan captive environments carefully for efficient use of the space available. 4.2. Element preferences Both species’ avoidance of open spaces supports earlier studies conducted in naturalistic environments (Ogden et al., 1990; Ogden et al., 1993; Stoinski et al., 2002). While these studies used log-linear analysis to determine the variables that best accounted for the variation they observed in enclosure usage, the present study directly measured time adjacent to individual elements as way of addressing specific environmental preferences.

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Chimpanzees and gorillas were observed more frequently adjacent to mesh barriers rather than solid walls. The mesh walls were adjacent to keeper-occupied spaces and were the most likely site of human interaction such as feeding, training, playing and informal interactions. Given the behavioral benefit of both structured and non-structured interactions with human caretakers (Bloomsmith et al., 1999), the attraction to these areas is not surprising. Both ape species also preferred corners and doorways. Corners likely offer some sense of security while doorways have the benefit of providing access to adjacent areas. Given that doorways were almost always closed during this study, this preference seems to be rooted in the concept of access rather than access itself. Unlike many other studies of space use at zoos, the chimpanzees and gorillas at GAH did not move to a separate holding area to sleep overnight. However, the tendency to stay near doorways and adjacent areas remained strong. Overall, there seems to be noticeable differences in how gorillas and chimpanzees used vertical space but striking similarities in how they preferred structural elements. 4.3. Non-structural factors and alternative explanations Social factors likely influence space utilization, however, these factors were not examined in this analysis. Examination of the individual data for vertical space use suggests that male and female gorillas may be using space in very different ways: males staying on or near the ground and females accessing areas higher up in the exhibit. One explanation for this is that females have an intrinsic preferences for upper regions of the space but it is also possible that they might be spacing themselves from the silverback. In the case of the smaller gorilla group, the male (KW) was not fully socially competent and there was sporadic aggression. It is possible that the large disparity in arboreal behavior between males and females in this group may be due to social avoidance as much as structural preferences. This might also be predicted by studies of arboreality in wild western gorillas that have found silverbacks nesting on arboreal nests only 2% of time compared to females that nest arboreally 21% of time (Mehlman and Doran, 2002). Remis (1999) and Lukas et al. (2003b) similarly reported that males were less arboreal than females. The case of the apes’ environmental preference for the area around doorways may be closely associated with social rank. The highest levels of doorway use were by highranking individuals (silverback gorillas and alpha male chimpanzees) who may have used their proximity to doorways as a way of controlling individuals in their group. Multiple doorways between adjacent and accessible animal areas should be encouraged in exhibit design not only as they are preferred areas, but it reduces the ability for a single individual to restrict movement between areas. Likewise, it may be possible that the presence of visitors plays a role in exhibit use patterns although data from this building shows no effect of crowd size on ape behavior (Ross and Lukas, unpublished). While it is difficult to separate non-structural effects from true environmental preferences, we believe the way these apes use their space is comparable to other captive apes in social groups of this size. The results of this study have been used in the design of a new ape facility at Lincoln Park Zoo: The Regenstein Center for African Apes (Ross, 2004). Vertical space has been

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maximized for both gorilla and chimpanzee exhibits, providing areas at multiple levels for not only activity but also resting. A variety of vertical elements have been included to provide visual barriers and environmental complexity. Finally, the shape of the rooms themselves is extremely angular to provide as many corners as possible as these are highly preferred areas. Although these exhibits are designed to look like the African forest, similar non-naturalistic animal areas could be constructed with equivalent functionality. Special attempts were made to locate highly preferred environmental features adjacent to public viewing areas to increase the likelihood that apes will be visible to zoo visitors. Designing animal enclosures with functionality that complements behavioral needs of animals is a strategy often overlooked in favor of practical considerations such as ease of cleaning or visitor impressions. Likewise, elements that look particularly attractive to us as humans may or may not be preferred areas for another species. Given that the cost of construction or renovation of animal areas can be significant for laboratories, zoos or sanctuaries, it seems wise to be efficient in allocating resources to areas that for which the animals have known preferences. This and other studies of environmental preferences can help guide designers to pay more attention to these factors, thereby facilitating behaviorally healthy groups of great apes in captivity.

Acknowledgments This paper was greatly improved by the helpful comments of Megan Reinertsen Ross, Elizabeth Lonsdorf, Katie Beranek and two anonymous reviewers. Assistance with statistical analyses provided by Kathleen Holt. The help of Michael Brown-Palsgrove and Lisa Scanlon was invaluable in recording the dimensions of the exhibits. Special thanks to the staff of the Lester E. Fisher Great Ape House at Lincoln Park Zoo for their assistance in facilitating this study.

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