Ape behavior in two alternating environments comparing exhibit and short-term holding areas.код для вставкиСкачать
American Journal of Primatology 72:951–959 (2010) RESEARCH ARTICLE Ape Behavior in Two Alternating Environments: Comparing Exhibit and Short-Term Holding Areas S.R. ROSS1,2, K.E. WAGNER1, S.J. SCHAPIRO3, AND J. HAU2 1 Lester E. Fisher for the Study and Conservation of Apes, Lincoln Park Zoo, Chicago, Illinois 2 Department of Experimental Medicine, University of Copenhagen, Copenhagen, Denmark 3 Michale E. Keeling Center for Comparative Medicine and Research, Department of Veterinary Sciences, University of Texas M.D. Anderson Cancer Center, Bastrop, Texas In many facilities, primates are voluntarily transferred between different enclosures on a daily basis to facilitate animal husbandry and exhibit maintenance. This procedure is particularly relevant in the management of great apes living in zoos, where the requirements of functional management must be balanced with the desire to maintain enriching and naturalistic exhibit enclosures that benefit ape residents and attract the visiting public. In these settings, examinations of ape behavior and welfare typically focus exclusively on activity in the primary exhibit area. However, physical, social and sensory experiences unique to each area may shape different patterns of behavior. In the current study, zooliving chimpanzees and gorillas were moved each day from exhibit areas to off-exhibit holding areas for a short duration as a part of regular management procedures. Behavioral data indicated species-specific reactions to the holding area, including increased aggression and self-directed behavior by chimpanzees and increased activity and prosocial behavior among gorilla subjects. Both species showed more feedingforaging behavior while in the exhibit enclosure. Results suggest that holding areas may not meet all behavior needs of captive great apes and demonstrate the importance of including all components of the captive enclosure in comprehensive analyses of great ape behavior and welfare. Am. J. Primatol. 72:951–959, 2010. r 2010 Wiley-Liss, Inc. Key words: captivity; chimpanzee; gorilla; enclosure alternation; management; behavior; welfare INTRODUCTION In many facilities, captive animals may spend some proportion of their time in a secondary enclosure, distinct from the primary environment. Some agricultural animals are restricted to indoor pens during winter months [O’Connell & Leonard, 1997; O’Driscoll et al., 2009] and laboratory-housed animals may be shifted between enclosures to facilitate regular cage disinfecting schedules [Duke et al., 2001; Mitchell & Gomber, 1976]. In zoos, animals including great apes are commonly moved from their exhibit space to an off-view holding area on a daily basis. This standard practice of moving animals to separately enclosed night-quarters during the evening hours has been used for decades. In an informal survey of the management practices for chimpanzees housed at zoos accredited by the Association of Zoos and Aquariums (AZA), 85% of the responding institutions (N 5 31) reported that chimpanzees spend more than 12 hr per 24-hour day in this off-exhibit space [Ross, unpublished data]. Despite this large proportion of time spent in the holding area, very few behavioral evaluations of zoohoused apes include data from off-exhibit spaces. As such, evaluations of activity that cease when the r 2010 Wiley-Liss, Inc. animals leave on-exhibit housing may fail to identify changes in behavior that impact the overall welfare of captive animals. In most zoological settings, holding areas for apes often differ substantially from exhibit spaces in both design and function. Although modern ape exhibits are often lush, naturalistic enclosures featuring a high degree of environmental complexity, holding areas are designed with primary attention to functionality. Traditionally, these uniform and lowmaintenance spaces are often constructed of concrete and steel mesh, with limited or no outdoor access, are typically smaller in volume and more constraining than the exhibit enclosure, and are more akin to conventional indoor laboratory housing [Hediger, 1969; Maple & Finlay, 1986; Maple & Perkins, 1996]. Contract grant sponsor: Leo S. Guthman Foundation. Correspondence to: S.R. Ross, Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, 2001 North Clark Street, Chicago, IL 60614. E-mail: firstname.lastname@example.org Received 2 February 2010; revised 12 May 2010; revision accepted 5 June 2010 DOI 10.1002/ajp.20857 Published online 7 July 2010 in Wiley Online Library (wiley onlinelibrary.com). 952 / Ross et al. A survey of zoo ape exhibits (circa 2001) indicated that across 11 AZA-accredited zoos in northern climates, the average size of the exhibit was over 40 times bigger than the holding space available to those same ape groups (E 5 4,812.75 m2; H 5 11.43 m2) [Lukas & Ross, unpublished data]. Additionally, in holding areas, apes may experience unique forms of food availability, social access and human interaction, including specialized training and management activity surrounding medical procedures [Beisner & Isbell, 2008; Caws & Aureli, 2003]. These attributes may shape ape behavior in ways distinct from those that characterize the exhibit area. The influence of systematic alternation between enclosures on ape behavior has been addressed primarily in the context of testing various social density hypotheses as apes move between enclosures of very different sizes and compositions. In a study of long-term, seasonal transfers between large outdoor areas and smaller indoor winter housing, Nieuwenhuijsen and de Waal  found relatively little evidence of a negative ‘‘crowding’’ effect and relatively small increases in aggression, activity, and locomotion while in the smaller indoor area. However, they suggested that these social strategies may change in the context of shorter-term alternations. When Aureli and de Waal  investigated such short-term (o5 days) alternation between a small indoor space and a larger indoor–outdoor enclosure, they found that chimpanzees’ social behavior (grooming and agonism) decreased in frequency in the smaller area. Videan and Fritz  found a similar effect when observing female chimpanzees, whereas males tended to show increased affiliative behavior in the smaller indoor space. Similar studies have been conducted on other great ape species with even more variable results. Cordoni and Palagi  studied the alternation of gorillas between large outdoor enclosures and much smaller indoor enclosures and found increased self-directed behavior, touching, and reconciliation, but no change in agonism in the smaller area. Hoff et al.  similarly found an increase in self-directed behaviors and low-intensity social interactions among gorilla subjects in the holding area, additionally accompanied by increased aggression. Forthman et al. , the only other known study to examine daily alternation between zoo exhibits and holding areas, found that Sumatran orangutans showed few behavioral differences, despite substantial differences in the size and complexity of the spaces. Together these studies offer mixed results as to the effect of regularly moving zoo-housed apes between different types of enclosures and leave open questions regarding the potential welfare and management implications of these alternations. Facility-related differences in enclosure type and management indicate the need for a comparative approach within a single setting to reliably document Am. J. Primatol. the behavioral influences of different enclosure components on multiple ape species [Stoinski et al., 2001]. Most notably, authors of the previous studies admit to the potential confounding factor of outdoor access, as animals were only allowed to access the outdoors in the larger (low density) spaces. In the current study, daily alternations between two very different, but indoor, spaces will be investigated. We compared behavioral differences expressed by zoohoused chimpanzees and gorillas in an indoor, naturalistic exhibit and a smaller, indoor off-exhibit holding area, where the animals were held during daily exhibit maintenance. We predicted that, in association with the smaller size, lack of environmental complexity, and different human interaction patterns, subjects in the holding area would show depressed activity and increased rates of anxietyrelated behavior, including self-directed and stereotypical activity. Characterizing the expression of behavioral differences between holding and exhibit spaces will further elucidate ape behavioral reactions to different captive environments, contribute to our understanding of daily management strategies for gregarious great ape species, and ultimately affect efforts to improve psychological well-being. METHODS Subject and Housing Subjects were seven chimpanzees and seven gorillas, housed at the Regenstein Center for African Apes (RCAA) at Lincoln Park Zoo (Chicago, IL) (Table I). The Lincoln Park Zoo is an accredited member of the Association of Zoos and Aquariums and all management and data collection procedures herein reported complied with all state and federal animal care and welfare regulations and the standards set forth in the American Society of Primatologists Principles for the Ethical Treatment of Nonhuman Primates. Subject characteristics are included in Table I. The chimpanzee group included three males and four females ranging in age from 8 to 25 years. The gorilla group included one adult male, four adult females and two juveniles ranging in age from 4 to 28 years. All subjects had comparable diets, exposure to TABLE I. Subject Demographics Chimpanzees Name Hank Optimus Kipper Cashew Kathy Nana Chuckie Gorillas Sex Age Name Sex Age Male Male Male Female Female Female Female 17 9 8 23 17 14 8 Jojo Azizi Makari Bahati Tabibu Rollie Susie Male Male Female Female Female Female Female 28 4 21 17 16 11 3 Ape Behavior and Enclosure Alternation / 953 humans, training and enrichment experience, and opportunity for outdoor access. Subjects in both groups also had similar levels of experience with and exposure to a number of noninvasive behavioral and cognitive research protocols. The two housing areas of interest were the publically viewed, naturalistic exhibit space (hereafter the ‘‘exhibit’’) and the off-view, hardscape, basement-level holding space (hereafter the ‘‘holding area’’). All apes slept in their exhibit overnight and every morning (at approximately 8 am), they voluntarily moved from the exhibit to the downstairs holding areas at the request of animal care staff. During the period of study, shifting compliance of the apes averaged 99% for gorilla subjects and 92% for chimpanzees. Although chimpanzee and gorilla subjects differ in terms of shifting experience in previous facilities, all subjects have been managed with comparable protocols since entering the current facility in 2004. The holding areas were composed of a set of six individual enclosures around a central keeper area, making a distinct ‘‘suite’’ for each social group (10.8 m2) (Figs. 1 and 2). Upon reaching the holding area, each ape participated in a short period of husbandry training and received its daily morning ration of fruit and primate chow (the bulk of each ape’s daily diet, including produce and primate chow, was provided later in the day, scattered in the exhibit area). During this time, individual apes were physically separated from each other (visual and olfactory access were maintained) for short periods depending on factors such as age, training experience, and other management and research protocols. Following exhibit maintenance, all apes were returned to the public exhibit at approximately 10 am. These naturalistic enclosures consisted of natural and artificial climbing elements, elevated nesting platforms and a deep mulch substrate (Fig. 3). Enclosures measured 109 m2 for gorillas and 124 m2 for chimpanzees. From 10 am until 5 pm, zoo visitors were present at varying densities and were separated from the ape exhibits by a glass barrier. Immediately upon entry to the exhibit from the holding area, apes had access to scattered foraging resources (including produce, grains, and chow). Though an adjacent outdoor yard was available to the apes during warm weather, this study is limited to times when the apes were restricted to their indoor spaces only. In both indoor enclosures, temperature was electronically regulated to maintain a consistent 201C. Fig. 2. Chimpanzee subjects in a single enclosure in a holding area suite, during a period of free access (following training and research protocols). Photograph was taken from the central caretaker area. Hallway observation area Human management area Fig. 1. Schematic representation of a typical holding area suite for an individual chimpanzee or gorilla social group at the Regenstein Center for African Apes. Shaded areas indicate animal enclosures; noncolored areas are sections of human activity (caretakers and data collectors). [Color figures can be viewed in the online issue, which is available at www.inter science.wiley.com.] Fig. 3. A representative indoor on-exhibit enclosure for the focal gorilla group at the Regenstein Center for African Apes. The exhibit enclosure provided the primary housing for subjects, was the site of most feeding activity, and included natural and artificial climbing structures, a mulch substrate and multiple areas of exploratory enrichment. Periods of free access to a large outdoor yard (excluded from the data set) was provided through exhibit-wide rear glass windows. Am. J. Primatol. 954 / Ross et al. Data Collection Behavioral data were collected on the apes in the exhibit during public hours (10 am–5 pm) 5 days a week, across all social, environmental, and management conditions. Holding area data were typically collected between 8 and 10 am each weekday. In both settings, observations were recorded using 10-minute focal animal follows with a 30-second intersample interval on a handheld computer [Pocket Observer 2.0, Noldus Observer, Noldus Information Technology, 2003] employing a 40-item ethogram. Immediately before the initiation of each data collection session, observers recorded the size of the public crowd on a four-point scale, ranging from the absence of visitors (only familiar staff were present) (‘‘0’’) to the presence of more than 50 visitors in the immediate exhibit area (‘‘3’’). Eight observers (staff not directly involved in ape training or care) collected holding and exhibit area data on the apes. Each observer met an interobserver reliability criterion, which required a mean 85% agreement with the first two authors during live data collection sessions conducted on at least four individuals in each social group. Observations of the apes in their exhibit area were taken from the public visitor floor and mezzanine-level observation areas. Three of the trained and tested observers also collected data in the holding area. Data collection in that context began only after all of the social groups had entered their individual holding suites, all training and/or other experimental testing were complete, and all management staff had left the immediate area. Subjects in the holding area were observed unobtrusively from a hallway adjacent to the front of the enclosures, separate from the area in which training interactions occurred. During observation periods, subjects had free access to all group members and typically all sections of the holding suite. Data Analysis Data were collected over the course of 15 months, between September 2007 and January 2009. To minimize variability associated with environmental factors while in the exhibit enclosure, we utilized only those data collected while subjects were restricted to their indoor enclosure. The resulting data set comprised 208 hr of observations collected in the exhibit as well as the 73 hr collected in the holding area. Raw counts of each behavior on the ethogram were calculated for each area (exhibit and holding) and combined into 12 behavioral categories for analysis (Table II). The in-view behavioral frequencies for each subject were averaged across sessions and compared between areas first using a Multivariate Analysis of Variance (MANOVA) with a critical a level of 0.05. We subsequently compared Am. J. Primatol. TABLE II. Behavioral Categories Used Analysis (From a 40-item Ethogram) in Data Behavior Defining criteria Abnormal Subject engages in idiosyncratic or stereotypical behavior, including coprophagy and regurgitation Subject directs an agonistic gesture (contact or noncontact) toward a conspecific Subject directs a sustained (3 sec) gaze to enclosure or maintenance areas while adjacent to the enclosure barrier Subject actively consumes, searches for and/or collects items for ingestion Subject rests or is motionless Subject moves more than 1 body lengths in any direction Subject interacts with a feature of the environment, including natural and non-natural items Subject engages in an affiliative interaction with a conspecifc Subject rakes the fingers over the skin in long, brusque strokes Subject touches, manipulates or examines the body, skin, or hair Subject engages in copulation, masturbation, and/or manipulation of the genitals Subject engages in a boisterous and nonpurposeful bout of nonsocial activity Aggression Attention Feed/forage Inactivity Locomotion Object manipulation Prosocial Scratching Self-directed Sexual Solitary play Proximity Close Subject is within 1 m of or in direct contact with the nearest neighbor rates of each behavior between areas using paired t-tests with a Bonferroni-adjusted a level of 0.05. Although previous research suggested that the behavior of apes at this facility is not significantly affected by the presence of zoo visitors [Ross et al., 2008; Milstein & Ross, in preparation], there is sufficient concern about these potential effects to include them in our analyses. Before conducting any statistical tests that compared holding and exhibit spaces, we determined if there were significant effects of crowd size on behavior in the exhibit area using a two factor MANOVA (species crowd size). Because the holding area is a restricted-access location, all holding area-based data collection occurred in the context of a ‘‘0’’-level crowd size (staff only) and hence was not included in the crowdsize analysis. RESULTS Crowd Size Effects We conducted preliminary analyses to determine potential effects of human presence on behavior in Ape Behavior and Enclosure Alternation / 955 TABLE III. Rates of Focal Behaviors Produced by Subjects in the Exhibit and Holding Areas Mean frequency (%) (SE) Behavior t-Value (df 5 6) P-Value Exhibit Holding (a) Chimpanzee subjects Abnormal Aggression Attention Feed-forage Locomotion Object manipulation Prosocial Scratching Self-directed Sexual Solitary play 1.4 2.8 2.3 5.6 0.3 1.0 0.6 2.5 2.8 0.5 1.5 0.2 0.03 0.06 0.001 0.8 0.3 0.6 0.04 0.03 0.6 0.2 3.8 0.1 0.7 18.1 8.2 7.0 17.3 0.4 12.3 1.0 0.0 Proximity Close 4.1 0.006 46.8 (0.04) 57.6 (0.05) (b) Gorilla subjects Abnormal Aggression Attention Feed-forage Locomotion Object manipulation Prosocial Scratching Self-directed Sexual Solitary play 0.8 2.3 1.9 5.4 2.9 1.1 2.5 1.4 2.3 2.4 2.3 0.5 0.06 0.1 0.002 0.03 0.3 0.04 0.2 0.06 0.05 0.06 3.2 0.1 1.8 30.6 7.2 5.0 4.1 0.2 11.7 0.1 0.6 2.7 0.7 4.4 5.4 11.6 6.7 8.2 0.6 18.0 0.0 1.8 Proximity Close 2.5 0.049 21.2 (0.06) the exhibit enclosure. A two-way MANOVA (Wilks’ l), with the factors of species and crowd size in the exhibit area did not indicate a main effect of crowd size on behavior (F(22,52) 5 1.34, P 5 0.19) or a species crowd size interaction (F(22,52) 5 1.31, P 5 0.21). As such, we did not include crowd size in the subsequent analysis and consider resulting behavioral patterns to emerge from environmental, sensory and management differences between the holding and exhibit areas. Location Effects A two-way MANOVA indicated significant main effects of species (F(10,15) 5 9.20, Po0.001) and location (holding vs. exhibit) (F(10,15) 5 6.8, P 5 0.001), but no species location interaction effects (F(10,15) 5 1.23, P 5 0.35). As a result, we conducted the subsequent paired t-tests independently for each species. Chimpanzees Behavior and proximity rates shown by the chimpanzees in both exhibit and holding areas are (0.01) (0.001) (0.002) (0.02) (0.01) (0.007) (0.02) (0.001) (0.02) (0.003) (0.00) (0.02) (0.001) (0.005) (0.05) (0.01) (0.02) (0.02) (0.001) (0.03) (0.001) (0.004) 2.8 0.5 2.5 10.5 8.6 8.2 18.8 1.6 17.4 1.1 0.4 (0.01) (0.002) (0.007) (0.01) (0.01) (0.02) (0.03) (0.004) (0.02) (0.003) (0.002) (0.02) (0.003) (0.02) (0.007) (0.02) (0.02) (0.04) (0.003) (0.03) (0.001) (0.009) 27.9 (0.07) shown in Table IIIa. Compared with their behavior on exhibit, chimpanzees demonstrated higher rates of aggression (t(6) 5 2.8, P 5 0.03) in the holding area, though at relatively low rates in both locations. Scratching behavior (t(6) 5 2.5, P 5 0.04) and selfdirected behavior (t(6) 5 2.8, P 5 0.03) also occurred significantly more often in the holding area. Chimpanzees showed higher rates of feeding and foraging while on exhibit (t(6) 5 5.6, P 5 0.001). In the holding area, chimpanzees were more frequently within close proximity to group mates (t(6) 5 4.1, P 5 0.006). There was no location effect on the other behavioral categories. Gorillas Rates of behaviors in each area are shown in Table IIIb. Gorillas performed higher rates of locomotion (t(6) 5 2.9, P 5 0.03) and prosocial behavior (t(6) 5 2.5, P 5 0.04) in the holding area, and increased feeding and foraging behavior (t(6) 5 5.4, P 5 0.002) in the exhibit area. Gorilla subjects also showed increases in aggression (t(6) 5 2.3, P 5 0.06), self-directed behavior (t(6) 5 2.3, P 5 0.06) Am. J. Primatol. 956 / Ross et al. and solitary play (t(6) 5 2.3, P 5 0.06) in the holding area and increased sexual behavior in the exhibit enclosure (t(6) 5 2.4, P 5 0.05) at levels that approached significance. As with chimpanzees, gorillas maintained higher rates of close proximity in the holding area (t(6) 5 2.5, Po0.05). There were no location effects on the other behavioral categories. DISCUSSION This is one of the few examinations of the effects of the regular zoological practice of systematically alternating African great apes between smaller, functional holding spaces and larger, complex indoor exhibits on a daily basis. Unlike former studies of regular alternations between differential spaces, this investigation does not include data from an outdoor space, therefore limiting that potentially confounding variable. The results of this study suggest that these very different environments produce distinct behavioral patterns for both chimpanzees and gorillas. Consideration of these differences and the motivational factors that cause them is important to promoting optimized environments for captive primates in a variety of settings. The holding and exhibit areas exposed apes to unique combinations of many sensory categories. Along with the overt contrast in size and complexity, the two areas also differed with respect to cross-species presence and human interaction, senvironmental factors such as ambient light, and management variables, including the daily time of exposure (subjects were housed in the holding area only for a short period in the morning, and transferred to the exhibit area during a later, nonoverlapping period of data collection). The extent of these differences limits the ability to relate changes in behavior to a particular feature of environment. Although we expect that size and complexity were especially significant factors, the current interpretation emerges from a consideration of the holistic experience of each area rather than an attempt at a feature-based comparison. Within this broad comparison, both species showed evidence of a behavioral sensitivity to the change in enclosure type, whereas observed species differences suggest an influence of species traits on the particular nature of this response [Lukas et al., 2003]. Chimpanzee patterns were generally more robust than that of gorillas, occurred in a wider range of behavioral categories and were consistent with a negatively arousing response to the smaller and less complex holding area. Gorillas offered a less clearly interpretable reaction to the holding area. Subjects demonstrated increased prosocial behavior and locomotor activity in holding—both frequently identified as indicators of beneficial changes in welfare. These patterns were accompanied by behavioral changes suggestive of a negative reaction: there was a five-fold, Am. J. Primatol. though nonsignificant, increase in rates of aggression in holding, and a 54% increase in self-directed behavior that reached statistical significance when the adult male gorilla was removed from the data set. These different reactions may reflect species-typical forms of reactivity and sociality in interaction with attributes unique to the holding enclosure. Other work has suggested that chimpanzees demonstrate a weak control over response inhibition [Boysen & Berntson, 1995, 1996, 2001] and are potentially impulsive in their responses, compared with gorillas [Wagner & Ross, 2010]. This factor may be important in interpreting the wider-ranging and more robust response to the holding area exhibited by chimpanzee subjects. Conversely, location effects on gorilla social behaviors may reflect the species-typical social avoidance and dispersal strategies in interaction with holding area-constraints on social proximity [Lonsdorf et al., 2009; Ross et al., in preparation; Stoinski et al., 2002]. In the Regenstein Center for African Apes, holding spaces were, on average, 9.3% of the size of exhibit spaces. Consistently, both species showed evidence of increased ‘‘crowding,’’ as demonstrated by the increase in close proximity to nearest neighbor in the holding area. Results of strict density-effect studies on ape behavior remain variable, with several hypotheses in question. The tension-reduction model predicts that great apes should increase affiliative behaviors, but decrease aggressive behavior as a means of actively reducing the risk of fighting [Videan & Fritz, 2007]. Alternatively, the conflict-avoidance hypothesis, in which subjects react to increased densities by decreasing all social interactions (i.e. both affiliative and aggressive behavior), has also garnered empirical support in studies of great apes [Aureli & de Waal, 1997]. In the current study, chimpanzees showed a significant increase in aggressive behavior in the holding area; though, across species, rates of aggressive encounters in both settings were very low and only rarely resulted in the need for veterinary intervention (during the 15-month data collection periods, there were no wounding events that required immobilization). The increase in agonism shown by chimpanzees is consistent with the density-aggression model [Calhoun, 1962], in which increased social density resulted in increased aggression, as demonstrated in rodents [Gregor et al., 1972; Van Loo et al., 2001] and some old world monkeys [Alexander & Roth, 1971; Boyce et al., 1998; Elton & Anderson, 1977]. The increase in prosocial behavior exhibited by gorillas may have similarly emerged from the change in social density experienced in the holding area, potentially in combination with an increase in perceived risk and/or rates of aggression. The significant space reduction of the holding area may have made ineffective gorillas’ typical dispersal strategy, causing them to rely instead on a partly Ape Behavior and Enclosure Alternation / 957 effective affiliative coping strategy that may have counteracted aggressive outcomes. It is also possible that this change, along with the observed activity increase, was an expression of eustress, elicited by the positively arousing aspects of the holding area (e.g. provisioning of high-value foods and reinforced human interactions). Future work that compares behavior around ‘‘holdingtypical’’ interactions that occur in exhibit areas (i.e. exhibit-based training sessions) may shed light on these opposing interpretations. Within the context of the current literature on enclosure alternation, the chimpanzee increase in agonism contradicts other reports showing no change in aggressive behavior [Nieuwenhuijsen & de Waal, 1982] and either an increase [Videan & Fritz, 2007] or decrease [Aureli & DeWaal, 1997] in prosocial behavior. Effects on gorilla social interactions were consistent with the Cordoni and Palagi  analysis, which indicated a similar rise in prosocial behavior with a nonsignificant increase in aggression. Hoff et al. [1994, 1997] also observed increased prosocial behavior in a holding area, along with an associated increase in aggression, among infant and adult gorillas and among adult gorillas alone. This cross-study observation of increased affiliation is suggestive of a species-wide trend. However, the numerous differences in such analyses, including the confounding provisioning of outdoor access in previous work, largely limit the ability to generalize results or connect patterns to characteristics of group composition, duration-of-stay, and management interactions unique to the holding area. Further inter-facility examinations with comparable protocols in zoological settings may offer the needed sample size to better illuminate the particular factors that influence the relationship between agonism, prosocial behavior, and social density among captive great apes. The unique configuration of the holding area likely also played a role in shaping the overall rate of all social interactions observed in that setting. Characteristic visually and physically constrained paths may have increased the probability of individuals meeting a group mate, increasing the rate of all social interactions in general. These incidental meetings, along with an expected, associated increase in mixed-sex and mixed-dominance status encounters, may have exacerbated competition, influenced perception of vulnerability and heightened arousal levels to additionally motivate the specific type of social response produced, in interaction with both species and facility characteristics [Baker & Aureli, 1996; Erwin & Deni, 1979; Maple, 1979; Maple & Finlay, 1986; Wilson, 1982]. As might be predicted by this paradigm, anxietyrelated behaviors including scratching and selfdirected behaviors increased for chimpanzees in the holding area. The change in gorilla self-directed behavior only approached significance, contradicting the Cordoni and Palagi  report. It is possible that the absence of this expected increase in the current analysis stems from the positive experience of the holding area, in combination with the (predictably) short duration of daily exposure. However, as Cordoni and Palagi noted, comparatively few reports have examined the connection between SDB and arousal in gorillas. Preliminary analyses conducted by the authors also suggest that cognitive stress in gorillas, such as that experienced in the context of a computerized testing paradigm, is associated with very short-duration self-touches [Wagner & Ross, unpublished data], rather than the brusque scratches exhibited by chimpanzee [Baker & Aureli, 1997; Leavens et al., 2001, 2004; Wagner & Ross, 2008]. Hence, the lack of change in levels of gorilla SDB does not conclusively contradict the pattern of increased arousal indicated by other reports. In other species, increased locomotion (‘‘nervous energy’’) has been used as an index of anxiety [Casper, 2006; Gygax et al., 2008]. The observed increase in this category by gorillas in the holding area may reflect subjects’ redirection of arousal along alternative behavioral channels, with rates potentially further increased as a method of active social dispersal in the more constrained holding area. However, this potential association is inconsistent with other reports for gorillas, which found, for example, increased inactivity in an indoor holding area [Hoff et al., 1997]; such differences may again indicate the interaction with facility-specific characteristics. The ability to generalize these results to other facilities is dependent on structural and space differences in both holding and exhibit areas, as well as the degree to which the observed behavior changes are related to duration of stay in each area. The apes in this study were typically provided access to their most complex and enriching environment (the exhibit) for the greatest proportion of their day. As a result, the time spent in holding was substantially less than 85% of AZA-accredited facilities that house resident apes in comparable holding areas for more than 12 hr per day [Ross, unpublished data]. There is evidence that animals with longer-duration daily experience in a holding area, a ‘‘night quarters,’’ demonstrate a preference for these areas [Stoinski et al., 2001] and that long-term alternations between spaces differ from shorter-term alternations [Videan & Fritz, 2007]. In these cases, apes may demonstrate fewer behavioral changes between enclosures due to subject use of the area moreso as an extension of the home ‘‘territory’’ [Forthman et al., 1993; Ogden et al., 1990; Stoinski et al., 2001]. Nonetheless, responses to the holding area indicate that, even over short periods, apes are sensitive to the unique characteristics that define enclosure areas in a captive facility. In general, the Am. J. Primatol. 958 / Ross et al. holding area was the setting of a greater frequency of arousal-related and agonistic interactions for chimpanzees. Holding area-effects on behavior were more variable for gorillas, but suggested some association with increased social density and potentially also reflected increased arousal. It is notable that for both species, gross changes in behavior were generally limited and not exclusively negative: abnormal behaviors showed no change across settings and gorillas showed increases in typically ‘‘positive’’ behaviors, including prosocial behavior. If these patterns persist across studies, then entire facilities (including both exhibit and holding enclosures) may be further improved by integrating favored elements of each setting into the other [Stoinski et al., 2002]. Interfaces for holding-typical caretaker interactions in the exhibit enclosure may minimize necessary time spent in a holding area and facilitate the transition between areas. An increase in the number of enrichment and feeding opportunities and the opportunity for outside access in the holding area may further converge exhibit and holding behavior patterns, while preserving the functionality of the area for management purposes. As a result of these findings, we advocate consideration of species-typical functional, physical, and social preferences in designing enclosure components, particularly including those intended for management activities [Boese, 1990]. Ape sensitivities to location also demonstrate the need for comprehensive evaluations of behavior in each enclosure area occupied by captive apes, regardless of frequency of use. The current welfare evaluation paradigm must be extended with this recognition that captive ape needs must be addressed in every component of the captive environment. 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