Behavioral correlates and welfare implications of informal interactions between caretakers and zoo-housed chimpanzees and gorillas

Applied Animal Behaviour Science 147 (2013) 306–315

Contents lists available at ScienceDirect

Applied Animal Behaviour Science journal homepage: www.elsevier.com/locate/applanim

Behavioral correlates and welfare implications of informal interactions between caretakers and zoo-housed chimpanzees and gorillas Gita I. Chelluri a,b,∗ , Stephen R. Ross a , Katherine E. Wagner a a b

Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, 2001 North Clark Street, Chicago, IL 60614, United States Division of Social Sciences, University of Chicago, 5801 South Ellis Avenue, Chicago, IL 60637, United States

a r t i c l e

i n f o

Article history: Received 6 December 2011 Received in revised form 1 June 2012 Accepted 12 June 2012 Keywords: Human–animal relationships Chimpanzee Gorilla Zoo Welfare

a b s t r a c t In captive animal facilities, human staff members are a relevant part of the animals’ social environment in addition to providing care and managing the social group. Structured, predictable interactions and relaxed, spontaneous contacts may all affect the animals’ behavior and well-being, both immediately and in the long term. This study examined the association between unstructured, affiliative caretaker–animal interactions and the behavior of zoo-housed chimpanzees (Pan troglodytes) and Western lowland gorillas (Gorilla gorilla gorilla). The interactions in question included play, spontaneous feeding, and other positive vocal and visual interactions performed through a protective mesh barrier. Behavioral data collected over 48 months were used to identify correlates of caretaker interactions among key behaviors relevant to welfare assessment, including agonism, sexual behavior, abnormal behavior, prosocial behavior, and self-directed behavior, as well as the presence of wounds. In observational sessions containing one or more caretaker interactions, chimpanzees and gorillas both showed higher agonism (P = 0.044 and P = 0.042, respectively) and lower self-directed behavior (P = 0.035 for chimpanzees and P = 0.001 for gorillas) than in control samples. Agonism rose in chimpanzees from an average of 0.01–0.12% of overall behaviors, and in gorillas from 0% to 0.1%, while self-directed behavior decreased in chimpanzees from an average of 9.54–7.81% and in gorillas from 11.02% to 7.38%. Chimpanzees also showed lower intraspecific prosocial behavior in samples with caretaker interactions (P = 0.044), decreasing from an average of 11.5% to 5.52% of overall behaviors. Finally, gorillas exhibited less abnormal behavior in caretaker interaction samples than in control samples (P = 0.029), decreasing from a mean of 2.42–1.77% of overall behaviors. In chimpanzees, higher agonism and lower prosocial behavior are indicative of greater arousal, although we would expect self-directed behavior to rise rather than decrease in that situation. The results in gorillas are mixed with respect to welfare outcomes: higher agonism is indicative of arousal, but lower abnormal and self-directed behaviors suggest a decrease in stress and anxiety. These findings underscore the importance of understanding the influence of all forms of interaction with heterospecifics and demonstrate a need for welfare assessments that include even positively intended interactions. © 2012 Elsevier B.V. All rights reserved.

1. Introduction

∗ Corresponding author at: Lester E. Fisher Center for the Study and Conservation of Apes, Lincoln Park Zoo, Chicago, IL, 60614, United States. Tel.: +1 609 865 8531; fax: +1 312 744 4738. E-mail address: [email protected] (G.I. Chelluri). 0168-1591/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.applanim.2012.06.008

Environments for captive animals are often designed to incorporate key aspects of the resident species’ socioecology in order to promote species-typical behavior and animal well-being (Coe et al., 2009; Dawkins, 1998; Jones and Pillay, 2004; Ross et al., 2009a; Wechsler, 2007; Wells,

G.I. Chelluri et al. / Applied Animal Behaviour Science 147 (2013) 306–315

2009). Regular interaction with human caretakers presents a unique challenge in this respect, since it has no direct corollary in the wild but is an important element of the captive environment, given the frequency with which interactions occur and the close individual relationships that can form (Carlstead, 2009; Melfi and Thomas, 2005; Mitchell et al., 1991). The human–animal interface in zoos, farms and research facilities has been intensively evaluated and includes a wide breadth of interactions with caretakers, researchers and visitors that have been shown to exert some influence on animal behavior and well-being (see Hosey, 2008; Hemsworth, 2003 and Bayne, 2002 for reviews in zoo, farm and laboratory settings, respectively). Managers and scientists rely on both behavioral and physiological measures to evaluate the welfare of captive animals (Dawkins, 2003; Wielebnowski, 2003). Welfare is generally understood to encompass an animal’s ability to cope with its environment (Hill and Broom, 2009), as well as the experience of positive or negative emotional states (Mason and Veasy, 2010). Behavior can be indicative of psychological states and is useful in that it can be measured non-invasively and at any time. Stress and anxiety are generally undesirable states for captive animals (Dawkins, 1998; Wielebnowski, 2003), and can be measured behaviorally through displacement activities such as self-directed behavior (Maestripieri et al., 1992), as well as abnormal behaviors and stereotypies (Mason, 2004). Similarly undesirable are behaviors detrimental to animal health, such as agonism and consequent wounding (Ross et al., 2009b). On the other end of the spectrum are behaviors indicative of well-being which managers seek to encourage, such as prosocial behaviors in social animals (Crockford et al., 2008) and mental engagement in the environment (Claxton, 2011). Great apes, especially chimpanzees, are among the most intensively studied taxonomic groups in zoo and laboratory settings (Melfi, 2005), with several studies examining the influence of interaction with humans on their behavior (Hosey, 2005; Roder and Timmermans, 2002). Caretakers interact with resident animals in contexts that range from predictable and structured, such as operant conditioning training (Perlman et al., 2010), exhibit shifting (Ross et al., 2010), research procedures (Rennie and BuchananSmith, 2006), and veterinary treatment (e.g. Laule et al., 1996), to friendly, spontaneous interactions such as play and casual feeding (Baker, 2004; Jensvold, 2008; Manciocco et al., 2009). Each of these contexts is of interest in welfare assessment. Even passive caretaker presence has been shown to influence behavior in certain contexts. In a study of a chimpanzee research colony, Lambeth et al. (1997) observed significantly more wounding on weekdays than on weekends, a trend that they attribute to greater staff presence and activity. Similarly, Maki et al. (1987) showed that the presence of unfamiliar humans was correlated with agonism in laboratory-housed chimpanzees. The authors of these studies note that routine interactions to which subjects have extensive exposure are associated with physiological and behavioral indicators of arousal and anxiety, and that effects may be escalate during periods of social instability in the subjects’ groups.

307

The relatively few studies that have examined relaxed, affiliative interactions suggest that they improve the welfare of captive animals. Bloomsmith et al. (1999) introduced unstructured interactions to the management routine of both zoo- and laboratory-housed chimpanzees, and measured the immediate effects by comparing behavior shortly before and after the interactions took place. Relative to baseline, the subjects exhibited lower rates of inactivity and solitary behavior when interactors were present, as well as lower rates of stereotypies, self-directed behaviors, and agonism after the interactors had left, all of which suggest a decrease in arousal and anxiety (Maestripieri et al., 1992; Morgan and Tromborg, 2007); however, the authors also observed a decrease in prosocial behavior among subjects for reasons that are not clear. In a similar study, Baker (2004) assessed the more general outcomes of relaxed engagement between caretakers and laboratory-housed chimpanzees, by measuring behavior at least 30 min after the conclusion of 10-min sessions that were added to the management routine. The chimpanzees showed an increase from baseline in social grooming and observer-directed affiliative behavior, as well as a decrease in intragroup agonistic displays, orally directed abnormal behaviors, and reactivity to extragroup agonistic displays. Jensvold (2008) further contributed that the exclusive use of chimpanzee-like gestures by caretakers resulted in more prosocial behavior among subjects. Taken together, these studies show that human caretakers can function as social enrichment (Claxton, 2011), likely contributing to a positive appraisal of humans by chimpanzees. Since chimpanzees are especially well-studied, it is interesting to compare how closely related species respond in the same situation. Fewer studies have addressed this question in gorillas, which may be expected to behave differently from chimpanzees due to their less gregarious nature (Lonsdorf et al., 2009; Watts, 2003). However, the available evidence shows similar results. Carrasco et al. (2009) found that zoo gorillas that were engaged in training and play sessions with caretakers showed lower rates of autogrooming and abnormal behaviors, and higher rates of intragroup prosocial behavior. Similarly, Pizzutto et al. (2007) found that affiliative interactions with a caregiver reduced aggression in a singly housed gorilla. These studies supply preliminary evidence that gorillas respond to human social stimuli in a positive manner much like chimpanzees, although a direct comparison of different species living in a single facility will more reliably reveal interspecific similarities and differences. In this study, we investigated the association between unstructured, affiliative interactions with caretakers and the behavior of chimpanzees (Pan troglodytes) and Western lowland gorillas (Gorilla gorilla gorilla) living in the same zoo environment. We sought to test two competing hypotheses based on the results of previous studies, using behavioral measures relevant to welfare assessment. The “arousal” hypothesis, based on the findings of Lambeth et al. (1997), suggests that interaction with caretakers increases stress and competition among apes for human attention (Baker, 2004), leading to higher frequencies of agonism, stress-related behaviors, and possibly wounding, as well as decreases in prosocial behavior. The

308

G.I. Chelluri et al. / Applied Animal Behaviour Science 147 (2013) 306–315

alternative “enrichment” hypothesis, based on the findings of Bloomsmith et al. (1999), Baker (2004), Jensvold (2008), Carrasco et al. (2009), and Pizzutto et al. (2007) posits that this type of interaction fosters a positive human–animal relationship and mitigates other stressors, leading to species-typical affiliative behaviors and a lower incidence of arousal- and stress-related behaviors.

2. Methods 2.1. Study population The study population consists of two groups of chimpanzees and two groups of gorillas housed in the Regenstein Center for African Apes at the Lincoln Park Zoo (Chicago, IL, USA). The size of the population varied slightly over the 4-year study period due to births, deaths and inter-institutional transfers. Here we present data on a total of 21 apes (12 chimpanzees and nine gorillas) ranging in age from 5.5 to 51 years (Table 1). We excluded three gorilla juveniles that were younger than 5.5 years during the collection period from analysis. All animals were captive-born in a zoo setting with the exception of three older wild-born chimpanzees. Both gorilla groups were naturally structured harems, ranging in size from four to seven individuals and both containing juvenile offspring. One chimpanzee group was structured similarly, with one adult male and four (later three) adult females. The second chimpanzee group contained multiple males and multiple females, including adolescents, with a total of six individuals. Each group is housed in a separate semi-naturalistic indoor–outdoor enclosure with free access to outdoor yards in appropriate weather (>5 ◦ C). Indoor spaces ranged from 72 m2 to 124 m2 in size, all similarly furnished with a deep mulch substrate and a range of climbing structures reaching up to 10 m in height. Adjacent outdoor yards ranged in size from 116 m2 to 1127 m2 . Three enclosures are visible to the public during regular hours (10:00 h to 17:00 h), with the fourth in an area not accessible to visitors. Groups were shifted between exhibits approximately twice annually for management and enrichment purposes. Only the chimpanzee groups occupied the offexhibit enclosure; one group (Chimpanzee 2) occupied the area predominantly, switching with the other chimpanzee group (Chimpanzee 1) for a discontinuous 5 months of the study period. Using trained cues, the apes are solicited to move to a lower-level holding area for 2 h every morning (8:00 h to 10:00 h) where they are engaged in a 5–10 min operant conditioning training session to facilitate veterinary and research procedures. No behavioral data collected during these routine management procedures were used in this study. During this time and typically again in the afternoon, fresh produce and biscuits are widely distributed in the exhibits to allow the apes to forage throughout the day. There is an additional training session for one of the groups each day at 13:30 h for public education. Caretakers and researchers interact with the apes through mesh panels in both the exhibits and holding areas. The resident apes

interacted with a total of 12 caretakers during the study period. 2.2. Data collection Data for this analysis were pulled from a continuous, long-term behavioral monitoring study in place since the facility opened in 2004 (Ross et al., 2010). We used data collected between January 2005 and December 2009 (48 months) for chimpanzees, and data collected between January 2005 and November 2009 (47 months) for gorillas, due to the transfer of one gorilla subject between groups at this facility in December 2009. Data were collected in 10-min focal sessions using a 30-s intersample interval (Altmann, 1974), by trained observers who had met a criteria of 85% inter-observer reliability with the authors. Data were collected live using handheld computers (Pocket Observer 2.0, Noldus Observer, Noldus Information Technology, Wageningen, The Netherlands). Observers used a randomized schedule that was uniquely generated each day to determine which subjects to follow. Observations were balanced throughout the day (10:00 h – 17:00 h), though samples collected between 13:00 h and 14:00 h were omitted from the analysis to remove the potentially confounding effect of the scheduled on-exhibit operant conditioning training and research session. The behavioral monitoring study employed an ethogram with six primary behavioral categories: agonism, sexual behavior, abnormal behavior, prosocial behavior, solitary behavior, and feeding/foraging. To allow for comparison with the extant literature on the topic, we included behaviors relevant to stress, arousal, prosocial behavior and attention to caretakers in our analysis (Baker, 2004) (Table 2). All occurrences of observable interactions with caretakers were recorded during the sampling period, and we excluded interactions with other present humans (e.g. displays directed at observer). Events recorded as caretaker interactions were all positive in nature, and included the provision of small quantities of food, drink and enrichment objects, tactile contact and examination through the mesh barrier (e.g. soliciting a subject to briefly present a body part), noncontact play (e.g. chase play), and similar unstructured affiliative interactions, such as making friendly gestures toward the apes. As the data were collected for multiple purposes, caretakers and observers were blind to all hypotheses concerning the association between these interactions and the apes’ behavior. Sessions that included a caretaker interaction were labeled as “CI” and were compared to control sessions that included no such interactions. The control sessions were selected using the following matched-control methodology: for each CI session, we identified the temporally closest interaction-free sample for the same subject during the same hour of the day, on a day either preceding or following the CI sample (n = 628 sample pairs). Time elapsed between matched samples ranged from 1 to 30 days. The relatively short duration between paired samples was designed to control for seasonality and ontogeny of the subjects. We selected control samples that matched CI samples in time of day, social group composition, and exhibit occupied. Consistency between paired samples with respect to

G.I. Chelluri et al. / Applied Animal Behaviour Science 147 (2013) 306–315

309

Table 1 Study population of chimpanzees and gorillas at Lincoln Park Zoo from January 2005 to December 2009. ID

Group/species membership

Sex

Date of birth (month/day/year)

Rearing history

Number of sample pairs

Hank Optimus Kathy Chuckie Cashew Kipper Nana Keo Donna June Vicky Kibali Kwan Kowali Bulera Madini JoJo Makari Bahati Tabibu Rollie

Chimpanzee 1 Chimpanzee 1 Chimpanzee 1 Chimpanzee 1 Chimpanzee 1 Chimpanzee 1 Chimpanzee 1 Chimpanzee 2 Chimpanzee 2 Chimpanzee 2 Chimpanzee 2 Chimpanzee 2 Gorilla 1 Gorilla 1 Gorilla 1 Gorilla 1 Gorilla 2 Gorilla 2 Gorilla 2 Gorilla 2 Gorilla 2

M M F F F M F M F F F F M F F F M F F F F

11/30/1990 2/9/1999 9/2/1990 9/24/1999 8/18/1984 1/23/2000 1/20/1994 6/30/1958 6/30/1965 10/26/1965 6/30/1964 8/24/1980 3/9/1989 1/9/1978 1/22/1989 6/20/1996 4/30/1980 7/12/1987 9/20/1990 4/30/1992 10/3/1996

Mother-reared Mother-reared Mother-reared Mother-reared Mother-reared Mother-reared Mother-reared Wild-born Wild-born Mother-reared Wild-born Mother-reared Mother-reared Mother-reared Mother-reared Mother-reared Mother-reared Mother-reared Mother-reared Surrogate-reared Surrogate-reared

14 16 15 24 19 16 23 72 25 40 57 53 39 23 24 20 36 40 19 30 23

Table 2 Behavioral categories used in data analysis (from a 62-item ethogram) arranged in order of descending hierarchical priority. Category

Criteria

Examples

Agonism

Subject performs or is object of an aggressive act, or exhibits submissive behavior (excludes interactions with humans). Subject engages in sexually directed behavior, either alone or with conspecific(s).

Hitting, biting, or charging at a conspecific, displaying, displacement.

Sexual

Abnormal

Subject engages in maladaptive idiosyncratic activity.

Prosocial

Subject engages in affiliative interaction with conspecific(s). Subject touches, examines, or scratches body.

Self-directed Attention to caretaker area

Mounting, masturbation, examination or manipulation of own or conspecific’s genitals. Coprophagy, urophagy, regurgitation and reingestion, plucking hair, stereotypical movement or body manipulation. Social grooming, play, infant handling, begging. Scratching, licking, patting self, and removing foreign objects from body.

Subject visually attends to adjacent staff area for ≥3 s while within 1 m of barrier

public crowd size (including no visitors), outdoor temperature, weather, and access to the outdoors and holding areas was validated with chi-square tests. Consequently, the only difference between CI and control samples for a given subject was the presence of one or more direct interactions with a caretaker. The number of paired samples for each subject in the study is listed in Table 1 and ranged from 14 to 72 sample pairs. For a peripheral analysis, we catalogued wounds observed by caretakers during the study period from daily caretaker records containing information on events relevant to the apes’ care. Caretakers noted the appearance of wounds and whether they observed or heard aggression in the apes. Since agonistic episodes among apes in this facility are frequently short-lived, caretakers did not often directly observe the apes sustaining agonistic wounds; however, incidental wounding is unlikely to account for many of the wounds that were recorded based on our observations at this facility, and we excluded any wounds that the caretakers observed and described as incidental

(e.g. sustained in an accidental fall). Using the caretakers’ descriptions, we recorded the date of occurrence and severity rating for each wound based on the methods of Ross et al. (2009b), and only included wounds that ranged in severity from ‘2’ to ‘5’ (Table 3). We excluded wounds for which there was insufficient information to assign a severity rating.

Table 3 Criteria for wounding severity levels (from Ross et al., 2010). Severity rating

Criteria

1

Superficial scratch or scrape; may have partial break of skin Shallow cut, skin broken Moderate wound, less than 1 in deep, blood visible Deep wound, more than 1 in deep, blood exiting wound Severe wound, gaping, tissue or bone visible, may be missing body part

2 3 4 5

310

G.I. Chelluri et al. / Applied Animal Behaviour Science 147 (2013) 306–315

2.3. Statistical analyses We calculated the mean frequency per sample of relevant behaviors in CI and control samples, respectively, for each subject and used these in a two-way MANOVA (˛ = 0.05). We used interaction condition and species membership as fixed factors in the model, and the mean frequencies of each behavioral category listed in Table 2 for each subject as the outcome measures. We followed this analysis with paired t-tests to compare mean frequencies of each behavior of interest between CI and control samples separately for each species (˛ = 0.05). We verified that the residuals were normally distributed and homoscedastic by visually inspecting histograms and plots of residuals versus expected values, and no transformation of the data was necessary for parametric analysis. In order to investigate a correlation between wounds and interactions, we cross-tabulated binary variables for both caretaker interaction and wounding events on each day of the study period and used these data in a Chi-square analysis (˛ = 0.05). All statistics were performed in PASW Statistics 17.0.3 (SPSS Inc., Chicago, IL, USA).

(T8 = −4.284, P = 0.003; Fig. 1). Gorillas also showed significantly higher agonism in CI samples than control samples (T8 = −2.422, P = 0.042; Fig. 2). Both self-directed behavior (T8 = 5.313, P = 0.001; Fig. 3) and abnormal behavior (T8 = 2.656, P = 0.029; Fig. 5) were lower in CI samples than control samples. Gorillas showed no significant differences between CI and control samples in social behavior (T8 = 1.894, P = 0.095) or sexual behavior (T8 = −0.276, P = 0.790). 3.3. Wounding There was no significant association between caretaker interactions and wounding in either chimpanzees (2 = 1.091, df = 1, P = 0.296) or gorillas (2 = 0.050, df = 1, P = 0.823). Chimpanzees sustained a total of 10 wounds on days with one or more CI samples (compared to 7.4 expected wounds), and 33 wounds on days without a CI sample (compared to 35.6 expected). The distribution of observed wounds in gorillas almost exactly matched the expected random distribution (44 wounds observed on non-CI days and six wounds observed on CI days).

3. Results

4. Discussion

3.1. Controls

Reflective of the extant literature, results from this zoo setting suggest that spontaneous interactions with caretakers were significantly associated with changes in the behavior of chimpanzees and gorillas. Of the two hypotheses that we tested regarding ape behavior in the context of unstructured interactions with caretakers, the “arousal” hypothesis predicted higher rates of stress-related behavior and lower rates of behaviors associated with positive welfare, such as prosocial behavior, while the alternative “enrichment” hypothesis predicted the opposite. We found support for the arousal hypothesis in chimpanzees, due to higher observed agonism and lower prosocial behavior in CI samples. Gorillas also showed higher agonism in CI samples, although they also showed behavioral signs of lower arousal. The difference in agonism aligns with the results reported by Lambeth et al. (1997), who observed increased wounding among chimpanzees during periods of high staff presence, but two factors are noteworthy in this respect: we found no significant changes in rates of physical wounding in either species, and the frequency of agonism in CI samples comprised an extremely low proportion of overall behavior for both species (see Fig. 2). This implies that the agonism observed in concordance with caretaker interactions was not a serious compromise to the apes’ health and welfare. Aggression is a part of the natural behavioral repertoire of primates (Honess and Marin, 2006), and at low rates it is unlikely to cause excessive stress and anxiety. Supplementing behavioral observations with physiological markers of arousal, such as glucocorticoid levels (Muller and Wrangham, 2004; Wielebnowski, 2003), collected around unstructured interactions in future studies will further elucidate how these interactions affect the well-being of ape subjects. It is surprising that agonism was more frequent in the period surrounding caretaker presence, given the positive nature of the interactions studied here. Similar studies

Our use of the matched-samples technique was successful in controlling for potential environmental confounds: public crowd size (2 = 0.754, df = 3, P = 0.861), outdoor temperature (2 = 12.584, df = 10, P = 0.248), weather (2 = 7.423, df = 5, P = 0.191) and access to the outdoors or holding area (2 = 0.065, df = 3, P = 0.996) did not differ significantly between control and CI samples. 3.2. Behavioral outcomes 3.2.1. Two-way MANOVA Our MANOVA model showed significant effects of staff (F6,33 = 10.104, P < 0.001) and species (F6,33 = 8.841, P < 0.001), but no staff x species interaction (F6,33 = 1.547, P = 0.194). Consequently, we performed paired t-tests for each behavioral outcome separately for each species. 3.2.2. Chimpanzees Chimpanzees showed significantly more attention to caretaker areas in CI samples than control samples (T10 = −7.882, P < 0.001; Fig. 1). Caretaker interactions were significantly associated with higher mean agonism (T10 = −2.297, P = 0.044; Fig. 2). Self-directed behavior was lower in CI samples than in control samples (T10 = 2.433, P = 0.035; Fig. 3), as was prosocial behavior (T10 = 4.051, P = 0.002; Fig. 4). There were no significant differences in abnormal behavior (T10 = −0.888, P = 0.395) or sexual behavior (T10 = −1.961, P = 0.078) between control and CI samples for chimpanzees. 3.2.3. Gorillas Like chimpanzees, gorillas showed more attention to caretaker areas in CI samples than control samples

Mean % Attention to Caretaker Area (+/- S.E.)

G.I. Chelluri et al. / Applied Animal Behaviour Science 147 (2013) 306–315

311

7% *

*

6%

5%

4%

3%

2%

1%

0% Chimpanzee

Gorilla

Fig. 1. Comparison of mean attention to caretaker areas between control (black) and caretaker interaction (white) samples as a function of species membership (paired t-test, *P < 0.05).

on chimpanzees and gorillas found that relaxed, affiliative interactions reduced the frequency of behaviors related to stress and arousal, including agonism, on both immediate and more extended time scales (Baker, 2004; Bloomsmith et al., 1999; Carrasco et al., 2009; Jensvold, 2008; Pizzutto et al., 2007). One possible explanation for our result is competition over preferred food and enrichment items that were provisioned in some (but not all) of the recorded interactions, although we were unable to separately analyze these. However, the aforementioned studies also analyzed provisioning and non-provisioning interactions together, but found different behavioral outcomes than we did. Future research that considers resource provision separately from other unstructured interactions may clarify the arousal-related artifacts associated with caretaker interactions.

It is further possible that the recorded interactions with caretakers were a result, rather than cause, of differences in subject behavior. Our study identified correlations between these interactions and subject behavior, but we did not have the data to investigate causation. Periods of intragroup aggression may have drawn caretaker attention to the group, similar to the “reverse visitor effect” reported by Margulis et al. (2003) for felids. While caretakers at this facility do not interfere in typical aggressive encounters, they solicit apes to check for wounds if they observe an agonistic episode; this practice may have contributed to the observed association between agonism and interactions, although it is unlikely that this was the case for every instance of aggression in our dataset, especially since caretakers do not observe every bout of agonism or immediately solicit apes to check for wounds when they

0.18% *

*

Mean % Agonism (+/- S.E.)

0.16% 0.14% 0.12% 0.10% 0.08% 0.06% 0.04% 0.02% 0.00%

Chimpanzee

Gorilla

Fig. 2. Comparison of mean agonism between control (black) and caretaker interaction (white) samples as a function of species membership (paired t-test, *P < 0.05).

312

G.I. Chelluri et al. / Applied Animal Behaviour Science 147 (2013) 306–315

12%

Mean % Self-directed Behavior (+/- S.E.)

*

*

10%

8%

6%

4%

2%

0% Chimpanzee

Gorilla

Fig. 3. Comparison of mean self-directed behaviors between control (black) and caretaker interaction (white) samples as a function of species membership (paired t-test, *P < 0.05).

do observe aggression. In order to determine the causal direction of interaction effects, future replications will need to sample behavior both before and after human–animal interactions of interest, after the fashion of Bloomsmith et al. (1999). Lower prosocial behavior among chimpanzees in CI samples represents another departure from the results of previous studies (Baker, 2004; Jensvold, 2008), and may be further evidence for higher arousal when they interact with caretakers. Alternatively, the difference may be related to distraction in the form of attention to the caretaker areas. Caretakers often initiated interactions when a chimpanzee subject was alone and attending to caretaker areas, creating an inherent difference in behavioral context between CI and control samples. This would help to explain

Mean % Prosocial Behavior (+/- S.E.)

18%

the difference in results seen between this study and Baker (2004), since in the latter the subjects’ behavior was sampled after the interactions with caretakers had taken place. Indeed, Baker (2004) posits that competition for human attention accounts for the decrease in prosocial behavior among chimpanzees in the presence of a human interactor seen in Bloomsmith et al. (1999). Such distraction may also help to explain the lower incidence of self-directed behaviors concomitant with caretaker interactions in both species, which was puzzling since it would be expected to rise when it coincides with higher agonism (Baker and Aureli, 1997), and since interactions that are often intermittent and unpredictable may be stressful for the animals. Our results for gorillas are ambiguous with respect to whether they experienced higher or lower stress in CI

*

16% 14% 12% 10% 8% 6% 4% 2% 0% Chimpanzee

Gorilla

Fig. 4. Comparison of mean prosocial behavior between control (black) and caretaker interaction (white) samples as a function of species membership (paired t-test, *P < 0.05).

G.I. Chelluri et al. / Applied Animal Behaviour Science 147 (2013) 306–315

313

4%

Mean % Abnormal Behavior (+/- S.E.)

*

3%

2%

1%

0% Chimpanzee

Gorilla

Fig. 5. Comparison of mean abnormal behavior between control (black) and caretaker interaction (white) samples as a function of species membership (paired t-test, *P < 0.05).

samples. As discussed, higher agonism in our CI condition is indicative of arousal, but lower self-directed behavior and abnormal behavior both suggest less stress and anxiety (Shyne, 2006). It is worth mentioning, however, that since a robust relationship between anxiety and self-directed behavior has not been established in gorillas the way it has in other species of primate (Baker and Aureli, 1997; Castles and Whiten, 1998; Maestripieri et al., 1992), it may not be possible to draw inferences from this observation for this species. Lower incidence of prosocial behavior among chimpanzees, compared with no difference in gorillas, was the only other interspecific contrast that we observed. However, given the low levels of social proximity and interaction typically exhibited by gorillas relative to chimpanzees (Lonsdorf et al., 2009; Stoinski et al., 2003; Watts, 2003), this is unsurprising. Observations from the wild reflect a possible connection between speciestypical gregariousness and interest in humans: in reports of the habituation of sympatric chimpanzees and gorillas in Cameroon, chimpanzees primarily showed curiosity toward unfamiliar humans while gorillas usually avoided them (Werdenich et al., 2003). Notably, despite a potential connection between species-typical social traits and reactivity to human interaction, chimpanzees and gorillas showed similar indications of arousal, including agonism, in our CI condition. The class of unstructured interactions investigated here may consistently represent important social stimuli to captive animals and contribute significantly to the dynamic relationship with caretakers (Hosey, 2008). As Baker (2004) notes, even when the immediate presence of caretakers is arousing, using unstructured interactions to build a social relationship between humans and animals can produce strong positive benefits for the animals in the long run. Spontaneous, friendly contacts are unusual in that they may often be initiated by the animal rather than the human (Jensvold, 2008), and may more closely resemble

conspecific prosocial behavior than the structured management routine. In some settings where animals have little or no conspecific contact, the quality of the humananimal relationship has been shown to be a significant driver of positive welfare outcomes (Chang and Hart, 2002; Hemsworth, 2003). Additionally, a positive relationship with caretakers may enhance a primate’s appraisal of potential social support in conflict and hence suppress social-related stress levels in general, in the same manner as positive, stable relationships with conspecifics (Crockford et al., 2008). This is not without potential drawbacks: as a consequence of this appraisal, apes may come to inappropriately perceive human caretakers as potential allies, to the detriment of intragroup stability (Association of Zoos and Aquariums Ape Taxonomic Advisory Group, 2010), although there is as yet no empirical evidence to test this hypothesis. Nevertheless, the bonds that form between zookeepers and the animals in their care are a driving force of beneficial outcomes on both sides (Carlstead, 2009; Hosey and Melfi, 2012), and it is important to continue investigating techniques that help to cultivate strong, positive caretaker–animal relationships. 5. Conclusions These results help expand our understanding of the complex dynamics between captive apes and their human caregivers. Continued attention to these relationships will aid in optimizing management practices in a range of captive settings, including zoos, research facilities and sanctuaries. Given that these data suggest that even positive unstructured interactions may have unintended effects, managers should further consider practices that minimize the degree to which caretakers insert themselves into the social milieu of captive apes. A reduction in human interactions during social introduction of unfamiliar chimpanzees has been advocated in the past (AZA

314

G.I. Chelluri et al. / Applied Animal Behaviour Science 147 (2013) 306–315

Ape TAG, 2010; Brent, 2001) and our results may serve to further extend this practice into routine daily management. Nonetheless, we assert that finding ways to improve human–animal relationships in captive settings will only result in positive outcomes for captive animal welfare, and we encourage continued study of the consequences of interactions that may vary in action, context and timing. Such work is especially needed in a wider sample of species and facilities, which may carry unique and unpredictable implications for caretaker appraisals by animals (Carlstead, 2009). Since the caretaker–animal relationship is relevant to captive animals’ health and emotional well-being, understanding all aspects of it is critical to optimizing the care of animals in all captive settings. Acknowledgement We are grateful to E. Lonsdorf, C. Hoffman, the editor, and two anonymous reviewers for helpful comments on the manuscript, and to the Fisher Center volunteer intern staff for collecting the data used in this study. We also thank the Leo S. Guthman Foundation for continuing financial support of the Lester E. Fisher Center for the Study and Conservation of Apes. References Altmann, J., 1974. Observational study of behavior: sampling methods. Behaviour 49, 227–267. Association of Zoos and Aquariums (AZA) Ape Taxonomic Advisory Group (TAG), 2010. Chimpanzee (Pan troglodytes) Care Manual. Association of Zoos and Aquariums, Silver Spring, MD. Baker, K., 2004. Benefits of positive human interaction for socially housed chimpanzees. Anim. Welf. 13, 238–245. Baker, K., Aureli, F., 1997. Behavioural indicators of anxiety: an empirical test in chimpanzees. Behaviour 134, 1031–1050. Bayne, K., 2002. Development of the human–research animal bond and its impact on animal well-being. Inst. Lab. Anim. Res. J. 43, 4–9. Bloomsmith, M.A., Baker, K.C., Ross, S.R., Lambeth, S.P., 1999. Comparing animal training to non-training human interaction as environmental enrichment for chimpanzees. Am. J. Primatol. 49, 35–36. Brent, L., 2001. A brief history of captive chimpanzees in the United States. In: Brent, L. (Ed.), The Care and Management of Captive Chimpanzees. American Society of Primatologists, San Antonio, TX, pp. 1–15. Carlstead, K., 2009. A comparative approach to the study of keeper–animal relationships in the zoo. Z. Biol. 28, 589–608. Carrasco, L., Collel, M., Calvo, M., Abello, M.T., Velasco, M., Posada, S., 2009. Benefits of training/playing therapy in a group of captive lowland gorillas (Gorilla gorilla gorilla). Anim. Welf. 18, 9–19. Castles, D.L., Whiten, A., 1998. Post-conflict behavior of wild olive baboons. II. Stress and self-directed behavior. Ethology 104, 148–160. Chang, F.T., Hart, L.A., 2002. Human–animal bonds in the laboratory: how animal behavior affects the perspective of caregivers. Inst. Lab. Anim. Res. J. 43, 10–18. Claxton, A.M., 2011. The potential of the human–animal relationship as an environmental enrichment for the welfare of zoo-housed animals. Appl. Anim. Behav. Sci. 133, 1–10. Coe, J.C., Scott, D., Lukas, K.E., 2009. Facility design for bachelor gorilla groups. Z. Biol. 28, 144–162. Crockford, C., Wittig, R.M., Whitten, P.L., Seyfarth, R.A., Cheney, D.L., 2008. Social stressors and coping mechanisms in wild female baboons (Papio hamadryas ursinus). Horm. Behav. 53, 254–265. Dawkins, M.S., 1998. Evolution and animal welfare. Q. Rev. Biol. 73, 305–328. Dawkins, M.S., 2003. Behaviour as a tool in the assessment of animal welfare. Zoology 106, 383–387. Hemsworth, P.H., 2003. Human–animal interactions in livestock production. Appl. Anim. Behav. Sci. 81, 185–198. Hill, S.P., Broom, D.M., 2009. Measuring zoo animal welfare: theory and practice. Z. Biol. 28, 531–544.

Honess, P.E., Marin, C.M., 2006. Enrichment and aggression in primates. Neurosci. Biobehav. Rev. 30, 413–436. Hosey, G.R., 2005. How does the zoo environment affect the behavior of captive primates? Appl. Anim. Behav. Sci. 90, 107–129. Hosey, G., 2008. A preliminary model of human–animal relationships in the zoo. Appl. Anim. Behav. Sci. 109, 105–127. Hosey, G., Melfi, V., 2012. Human–animal bonds between zoo professionals and the animals in their care. Z. Biol. 31, 13–26. Jensvold, M.L.A., 2008. Chimpanzee (Pan troglodytes) responses to caregiver use of chimpanzee behaviors. Z. Biol. 27, 345–359. Jones, M., Pillay, N., 2004. Foraging in captive hamadryas baboons: implications for enrichment. Appl. Anim. Behav. Sci. 88, 101–110. Lambeth, S.P., Bloomsmith, M.A., Alford, P.L., 1997. Effects of human activity on chimpanzee wounding. Z. Biol. 16, 327–333. Laule, G.E., Thurston, R.H., Alford, P.L., Bloomsmith, M.A., 1996. Training to reliably obtain blood and urine samples from a young diabetic chimpanzee (Pan troglodytes). Z. Biol. 15, 87–91. Lonsdorf, E.V., Ross, S.R., Linick, S.A., Milstein, M.S., Melber, T.N., 2009. An experimental, comparative investigation of tool use in chimpanzees and gorillas. Anim. Behav. 77, 1119–1126. Maestripieri, D., Schino, G., Aureli, F., Troisi, A., 1992. A modest proposal: displacement activities as an indicator of emotions in primates. Anim. Behav. 44, 967–979. Maki, S., Alford, P.L., Bramblett, C., 1987. The effects of unfamiliar humans on aggression in captive chimpanzee groups. Am. J. Primatol. 12, 358. Manciocco, A., Chiarotti, F., Vitale, A., 2009. Effects of positive interaction with caretakers on the behaviour of socially housed common marmosets (Callithrix jacchus). Appl. Anim. Behav. Sci. 120, 100– 107. Margulis, S.W., Hoyos, C., Anderson, M., 2003. Effect of felid activity on zoo visitor interest. Z. Biol. 22, 587–599. Mason, G., 2004. Can’t stop, won’t stop: is stereotypy a reliable animal welfare indicator? Anim. Welf. 13, 57–69. Mason, G.J., Veasy, J.S., 2010. How should the psychological well-being of zoo elephants be objectively investigated? Z. Biol. 29, 237–255. Melfi, V., 2005. The appliance of science to zoo-housed primates. Appl. Anim. Behav. Sci. 90, 97–106. Melfi, V.A., Thomas, S., 2005. Can training zoo-housed primates compromise their conservation? A case study using Abyssinian colobus monkeys (Colobus guereza). Anthrozoos 18, 304–317. Mitchell, G., Obradovich, S.D., Herring, F.H., Dowd, B., Tromborg, C., 1991. Threats to observers, keepers, visitors, and others by zoo mangabeys (Cercocebus galeritus chrysogaster). Primates 32, 515–522. Morgan, K.N., Tromborg, C.T., 2007. Sources of stress in captivity. Appl. Anim. Behav. Sci. 102, 262–302. Muller, M.N., Wrangham, R.W., 2004. Dominance, cortisol and stress in wild chimpanzees (Pan troglodytes schweinfurthii). Behav. Ecol. Sociobiol. 55, 332–340. Perlman, J.E., Horner, V., Bloomsmith, M.A., Lambeth, S.P., Schapiro, S.J., 2010. Positive reinforcement training, social learning, and chimpanzee welfare. In: Lonsdorf, E.V., Ross, S.R., Matsuzawa, T. (Eds.), The Mind of the Chimpanzee: Ecological and Experimental Perspectives. University of Chicago Press, Chicago, IL, pp. 320– 331. Pizzutto, C.S., Nichi, M., Ramiro Correa, S.H., Ades, C., De BarrosVaz Guimaraes, M.A., 2007. Reduction of abnormal behavior in a gorilla (Gorilla gorilla gorilla) through social interaction with a human being. Lab. Primate Newsl. 46, 6–10. Rennie, A.E., Buchanan-Smith, H.M., 2006. Refinement of the use of nonhuman primates in scientific research. Part I. The influence of humans. Anim. Welf. 15, 203–213. Roder, E.L., Timmermans, P.J.A., 2002. Housing and care of monkeys and apes in laboratories: adaptations allowing essential species-specific behavior. Lab. Anim. 36, 221–242. Ross, S.R., Schapiro, S.J., Hau, J., Lukas, K.E., 2009a. Space use as an indicator of exhibit appropriateness: a novel measure of animal welfare. Appl. Anim. Behav. Sci. 121, 42–50. Ross, S.R., Bloomsmith, M.A., Bettinger, T.L., Wagner, K.E., 2009b. The influence of captive adolescent male chimpanzees on wounding: management and welfare implications. Z. Biol. 28, 623–634. Ross, S.R., Wagner, K.E., Schapiro, S.J., Hau, J., 2010. Ape behavior in two alternating environments: comparing exhibit and short-term holding areas. Am. J. Primatol. 71, 1–9. Shyne, A., 2006. Meta-analytic review of the effects of enrichment on stereotypic behavior in zoo mammals. Z. Biol. 25, 317–337. Stoinski, T.S., Hoff, M.P., Maple, T.L., 2003. Proximity patterns of female western lowland gorillas (Gorilla gorilla gorilla) during the six months after parturition. Am. J. Primatol. 61, 61–72.

G.I. Chelluri et al. / Applied Animal Behaviour Science 147 (2013) 306–315 Watts, D.P., 2003. Gorilla social relationships: a comparative review. In: Taylor, A.B., Goldsmith, M.L. (Eds.), Gorilla Biology: A Multidisciplinary Perspective. Cambridge University Press, Cambridge, England, pp. 302–327. Wechsler, B., 2007. Normal behaviour as a basis for animal welfare assessment. Anim. Welf. 16, 107–110. Wells, R.S., 2009. Learning from nature: Bottlenose dolphin care and husbandry. Z. Biol. 28, 635–651.

315

Werdenich, D., Dupain, J., Arnheim, E., Julve, C., Deblauwe, I., van Elsacker, L., 2003. Reactions of chimpanzees and gorillas to human observers in a non-protected area in South-Eastern Cameroon. Folia Primatol. (Basel) 74, 97–100. Wielebnowski, N., 2003. Stress and distress: evaluating their impact for the well-being of zoo animals. J. Am. Vet. Med. Assoc. 223, 973–977.