Angela S. Kelling a b c, Meredith J. Bashaw a b d, Mollie A. Bloomsmith a e & Terry L. Maple a b f a Center for Conservation and Behavior, School of

This article was downloaded by: [Dr Kenneth Shapiro] On: 09 June 2015, At: 10:50 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK Journal of Applied Animal Welfare Science Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/haaw20 Socialization of a Single Hand- Reared Tiger Cub Angela S. Kelling a b c, Meredith J. Bashaw a b d, Mollie A. Bloomsmith a e & Terry L. Maple a b f a Center for Conservation and Behavior, School of Psychology, Georgia Institute of Technology b Zoo Atlanta, Atlanta, Georgia c School of Psychology, University of South Florida at Lakeland d Department of Psychology, Franklin and Marshall College e Yerkes National Primate Research Center, Emory University f Florida Atlantic University Published online: 02 Jan 2013. To cite this article: Angela S. Kelling, Meredith J. Bashaw, Mollie A. Bloomsmith & Terry L. Maple (2013) Socialization of a Single Hand-Reared Tiger Cub, Journal of Applied Animal Welfare Science, 16:1, 47-63, DOI: 10.1080/10888705.2013.741000 To link to this article: http://dx.doi.org/10.1080/10888705.2013.741000 PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the Content ) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and

are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages, and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content. This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions

JOURNAL OF APPLIED ANIMAL WELFARE SCIENCE, 16:47 63, 2013 Copyright Taylor & Francis Group, LLC ISSN: 1088-8705 print/1532-7604 online DOI: 10.1080/10888705.2013.741000 Socialization of a Single Hand-Reared Tiger Cub Angela S. Kelling, 1;2;3 Meredith J. Bashaw, 1;2;4 Mollie A. Bloomsmith, 1;5 and Terry L. Maple 1;2 1 Center for Conservation and Behavior, School of Psychology, Georgia Institute of Technology 2 Zoo Atlanta, Atlanta, Georgia 3 School of Psychology, University of South Florida at Lakeland 4 Department of Psychology, Franklin and Marshall College 5 Yerkes National Primate Research Center, Emory University Given the drawbacks of hand-rearing nonhuman animals in captivity, the practice is generally avoided, but it is sometimes necessary. A few scientific publications are available to guide managers toward best practices in hand-rearing, but the majority of articles focus on hand-rearing captive primates. Less is known about hand-rearing carnivores, but early socialization appears to be critical for adult social behavior. This article documents the successful hand-rearing and reintroduction of a single female Sumatran tiger cub at Zoo Atlanta. Reintroduction included a systematic procedure that used scent trials and introduction sessions through a barrier to gauge interest and determine whether or not aggression was a problem. Based on signs of interest, reduced stress-related behaviors, and a lack of aggression, animal managers decided to proceed with reintroduction. During the introductions, the animals were not aggressive and did occasionally interact, although typical mother infant interactions were rare. The cub has since bred naturally and successfully delivered and reared two litters of cubs. These data suggest limited exposure to an adult tiger may be adequate socialization for normal reproduction even if it is provided relatively late in the cub s development. Keywords: reintroduction, tiger behavior, hand-rearing Terry L. Maple is now at Florida Atlantic University. Correspondence should be sent to Angela S. Kelling, School of Psychology, University of South Florida at Lakeland, 3343 Winter Lake Road, Lakeland, FL 33803. Email: akelling5@gmail.com 47

48 KELLING, BASHAW, BLOOMSMITH, MAPLE In North American zoos, hand-rearing of newborn nonhuman animals in captivity was at one time preferred over allowing offspring to be raised by their parents. In 1988, Beck and Power found that nearly half of the captive-born gorillas in North American institutions had been hand-reared. Unfortunately, infant primates deprived of early social contact may exhibit high levels of abnormal behavior, such as self-sucking and stereotypic rocking (Meder, 1989; Novak & Sackett, 2006), abnormal reproductive behavior (Beck & Power, 1988; Duffy & Hendricks, 1973; Harlow, 1971; King & Mellen, 1994; Mellen, 1992), and deficits in maternal behavior (Ryan, Thompson, Roth, & Gold, 2002). Modern nursery rearing conditions ameliorate some of these problems, but some behavioral differences are still observed between animals reared in modern complex nursery environments and their mother-reared counterparts (Bloomsmith, Baker, Ross, & Lambeth, 2006), and it is unknown whether this is the case for all species. In modern zoos, hand-rearing techniques are no more than emergency measures to be put into practice when all else has failed (Read & Meier, 1996, p. 41). The best documented hand-rearing protocols have been provided for great apes. Research suggests that it is essential to integrate hand-reared infants into a diverse group of conspecifics as early as possible (Jendry, 1996; Maple & Hoff, 1982). Meder (1990) writes that the social group needs to be diverse enough to include species-typical social behaviors, such as copulation, communication, and maternal behaviors. She claims that this early access to conspecifics is central in the effort to reduce the effects of hand-rearing in gorillas. Although some data have been collected on the process and consequences of reintroducing young gorillas and chimpanzees into existing troops (e.g., Bashaw, Gullott, & Gill, 2010; Meder, 1990), little published information is available on this process in carnivores. There is some information available on hand-rearing captive carnivores. One study found that mother-reared domestic cats (Felis catus) were more likely to reproduce and less likely to be aggressive toward male partners (Mellen, 1992). Mellen generalizes her results to conclude that small exotic felids should not be nursery-reared unless it is unavoidable. Similarly, peer-reared giant pandas are not as socially competent as their mother-reared counterparts (Snyder et al., 2003). Meier (1986) states that hand raising exotic carnivores presents special challenges in terms of the development of normal behavior (p. 851), and Richardson (1988, 1991) suggests that proper socialization can take as long as 3 years and should include controlled exposure to a conspecific, especially a potential mate. Meier identifies critical periods for socialization seen in domestic dogs (Canis lupus familiaris) and hand-reared exotic carnivores. If they are not exposed to socialization within this critical period, behavioral problems may result, such as fear or aggression around conspecifics, lack of conspecific play, difficulty with reproduction, and fixation on humans. Meier suggests that if handrearing is obligatory, it is vital to provide young carnivores with enrichment and

TIGER SOCIALIZATION 49 interactions with conspecifics. In cases where the carnivore is a single birth, substitutions with a domestic cat, dog, or other young carnivore are advised (Meier, 1986). Unpublished data from the Tiger Species Survival Plan (Tiger SSP) found that hand-rearing female tigers did not significantly reduce their chances of becoming pregnant when paired with a male (Tiger SSP, 2012). Some hand-reared tiger cubs have matured and produced and reared litters, but systematic data is lacking so it is difficult to determine if this is the norm. An examination of the tiger studbooks from 2010 indicates that the majority of tigers are dam-reared and the majority of hand-reared female tigers have not produced offspring (Traylor- Holzer, 2010a, 2010b, 2010c). Of the 11 hand-reared female Amur tigers, 1 gave birth to a cub who also had to be hand-reared, 1 had 2 separate cubs who died the same day, and 1 dam successfully reared her first litter of 5 cubs (Traylor-Holzer, 2010a). None of the 3 hand-reared female Malayan tigers have had a cub (Traylor-Holzer, 2010b). Only 2 female Sumatran tigers have been hand-reared: the tiger discussed in this article, who has successfully reared two litters, and another female who has not produced a cub (Traylor-Holzer, 2010c). The Tiger SSP states that it is preferable, if possible, to have cubs remain with their mothers because it benefits the tigers, staff, and visitors (Bush, Phillips, & Montali, 1994). Parental rearing has nutritional, developmental, and behavioral benefits for offspring (Edwards & Hawes, 1997; Meier, 1986). Unfortunately, situations still arise in which infants must be hand-reared, and little published information is available to aid managers in socializing hand-reared animals. The need for hand-rearing may be influenced by many factors, including situations in which staff members are not aware of pregnancy, which can lead to mothers giving birth in unsuitable areas, excessive noise, or high levels of intervention in the first weeks postpartum (Hakala & Traylor-Holzer, 1994; Richardson 1988, 1991). Richardson (1988, 1991) suggests providing a cubbing box and leaving the mother alone from a week before the earliest estimated birth date until at least 6 weeks after birth may help avoid hand-rearing. If hand-rearing is required to keep the offspring alive, maintaining normal social behavior in hand-reared captive carnivores can be difficult. Choices made during hand-rearing, especially during the period of socialization, can influence the animal for the remainder of his or her life (Meier, 1986). Valuable reports on rearing captive felids (e.g., Hakala & Traylor-Holzer, 1994; Richardson, 1988, 1991) have been written based on people s personal experiences and expertise, but they lack data and specific protocols. The purpose of this article is to inform animal managers by describing Zoo Atlanta s decision to hand-rear a single Sumatran tiger cub (Panthera tigris sumatrae) and provide both behavioral data on the zoo s socialization efforts and specific descriptions of the socialization protocols used, including the cub s eventual reintroduction to her mother.

50 KELLING, BASHAW, BLOOMSMITH, MAPLE METHODS AND RESULTS Decision to Hand-Rear Introductions and copulations between the adult male and female Sumatran tigers began on January 7, 2000. The two tigers were introduced approximately six days each month between January and November. The tigers mated consistently when given the opportunity, and all interactions for the first 3 months were monitored by a behavioral scientist. As described by Richardson (1988), the staff were unaware that the female tiger was pregnant. No signs of pregnancy were detected the female s eating habits, weight, and appearance did not noticeably change. Additionally, continued interest was observed between the tigers, which is unusual but not unheard of for pregnant female tigers (e.g., Kleiman, 1974; Seager & Demorest, 1986). On November 27, 2000, the female gave birth to a single cub in her exhibit. When care staff attempted to shift the dam into the holding area for the night, she hesitated to leave the exhibit. After she shifted inside, they inspected the area of the exhibit where she had been lying and discovered a single female cub. The cub was wet and cold, but she appeared to have been cleaned by her mother. Read and Meier (1996) organize the factors that may contribute to a decision to hand-rear into five categories: environmental, social, health, conditioning, and preventative medicine. In the current case, the factors that contributed to the initial decision to not immediately reintroduce the cub were environmental, social, and health factors. First, it was unseasonably cold in Atlanta that November (low temperature the night of the birth was 39 ı F [3.9 ı C]), and the cub was hypothermic. The cub s survival and the necessary medical treatment for her hypothermia were the most influential components for the decision to remove her from the building. Neonate carnivores have difficulty thermoregulating for approximately two weeks (McManamon & Hedberg, 1993), and hypothermia is a common medical concern (Hedberg, 2002). In the wild, tigers stay with their offspring almost continuously for at least the first few days after birth (Thapar, 1986), and it is recommended that captive cubs be sheltered in an enclosure kept at 85 ı F (29.4 ı C; Hoff, 1961). Neither the holding area nor the exhibit was adequately climate controlled, thus veterinary staff feared that the cub might become hypothermic regardless of the dam s behavior. In addition, Carnivores are notorious for cannibalizing their young, especially if stressed (Read & Meier, 1996, p. 43). As a result, the cub was taken to the veterinary clinic for the night instead of being immediately reintroduced to her mother. During the evening and the next morning (Day 1), staff at Zoo Atlanta began contacting members of the Tiger SSP Management Committee and other tiger experts to obtain their input about possibilities for socialization or reintroduction. No data were available on which to base the decision and the opinions of

TIGER SOCIALIZATION 51 the experts consulted, based on their own sometimes conflicting experiences, were contradictory. Some people recommended introduction within the first 2 weeks, especially because she was a single cub. Others recommended that the cub be hand-reared so as not to risk cannibalism by the mother. Everyone agreed that reintroductions should not be attempted unless the mother was showing interest in, or at least ambivalence to, the cub in an introduction situation with a barrier between the animals, so the cub was placed on the other side of a mesh barrier (91 cm wide by 121 cm high) from the dam for varying lengths of time (determined by her body temperature) on Days 1 and 2 to look for signs of interest. Although the dam did sniff and vocalize at the cub, she spent most of each barrier introduction pacing and seemed very agitated. Although these behaviors may have indicated a desire to be reunited with her cub, they also raised concerns about the potential for stress-induced cannibalization. At the end of Day 2, staff decided to postpone introductions indefinitely to let the dam calm down and so that they could complete needed housing alterations. Hand-Rearing Environment and Procedures While the holding area was being modified, the cub was placed in a nursery in the veterinary clinic. The nursery room was maintained under quarantine conditions and was staffed by five zoo employees and long-term volunteers (hereafter, nursery staff). Given that reintroduction was a goal from the beginning of the hand-rearing, caretakers were instructed to hesitate entering the nursery when the cub cried to see if the episode would pass in an attempt to decrease her reliance on humans for comfort. They also were instructed to use tiger vocalizations, mainly prusten (also called chuffing; a breathy, vibrating vocalization that occurs in friendly encounters with other tigers), for greetings and interactions. The cub was provided with many enrichment items, including a sound machine, pacifiers, teething rings, fleece cloths, and various toys. Additionally, she was exposed to her dam s urine regularly. Initially, at least one nursery staff member remained in or just outside the nursery 24 hr/day. The cub was kept in an incubator until about one week of age, and then she was allowed free access to the nursery room. The 24-hr monitoring continued until Day 13, at which point nursery staff members left after the midnight feeding and returned at 6 a.m. Before the cub became mobile, a 5-ft (1.5-m) wall was constructed about 3 ft (0.9 m) inside the door of the nursery room as a primary barrier. Weather permitting, the cub also began to have access to a temporary outdoor enclosure when she was 10 weeks old and spent time with nursery staff in the otherwise empty adult tiger holding area when she was 11 weeks old. At 14 weeks of age, the cub was introduced to one of the tiger exhibits, with the level of water in the pool lowered for safety

52 KELLING, BASHAW, BLOOMSMITH, MAPLE and nursery staff present to monitor her. She was on public display beginning at 19 weeks old. The cub was burped and manually stimulated to encourage elimination until Week 6, and she was weighed approximately twice a day in order to track her weight gain and adjust feeding amounts (see Figure 1). She was bottlefed a mixture of Lactaid and Esbilac supplemented with clam juice or 250-mg taurine tablets six times a day (6 a.m., 10 a.m., 1 p.m., 4 p.m., 8 p.m., 12 a.m.) from birth until she was 10 weeks old, gradually increasing the volume at each feeding. Beginning in Week 2, chicken baby food was blended into the Esbilac mixture. The number of feedings was decreased to 5/day in Week 10 (6 a.m., 10 a.m., 1 p.m., 6 p.m., 10 p.m.) and 4/day in Week 11 (6 a.m., 10 a.m., 4 p.m., 10 p.m.). ZuPreem was presented before the bottle beginning in Week 11, and bottle-feeding was discontinued in Week 12. Although the cub continued to be fed the Esbilac mixture, it was poured over the ZuPreem to encourage her to eat solid food. Consistent with Richardson (1991) and Meier (1986), a companion animal was sought for the cub. Dogs have been used as social companions for several captive felid species, including a tiger cub, during rearing (e.g., D. M. Richardson, 1991; personal communication; Thomas & Philips, 1978), but an immediate FIGURE 1 Cub s average daily weight in kilograms from Day 2 through Day 58. Days 41 and 49 are missing.

TIGER SOCIALIZATION 53 source for a domestic dog who could be certified free of health problems was not available. Instead, a domestic cat was obtained from the collection of medically clean felines housed at the University of Georgia veterinary hospital. No females were available in the collection, so an adult male cat was used. The cat was introduced to the cub on December 4, 2000 (Day 7). The cat was allowed access to the cub only when nursery staff members were present, and very little interaction was observed between cat and cub. The rare interactions did not noticeably increase over time. During this period, the cub developed a herniated umbilicus that required surgery. Surgery was conducted on Day 22, and the domestic cat was returned to the University of Georgia Hospital at that time. The cub was given 2 weeks to recover from surgery, and 24-hr monitoring resumed for the first 5 days after surgery. Preparation for Reintroduction When staff at Zoo Atlanta asked for opinions on whether or not to reintroduce the cub at this point, zoo professionals again gave varying advice. Some pointed out that social access is crucial for future interactions with conspecifics and her mother was the only option. Some claimed that too much time had passed and it would be too risky. A few stated that they had a policy of once they pulled a cub for hand-rearing, they never reintroduced. Therefore, a systematic reintroduction and documentation that allowed a slow and reversible progression to actual introductions was undertaken. The first step in this process involved controlled scent trials. There were eight trials in total, and each trial included 15 min with fleece with the cub s scent (removed from her bedding before the trial) behind a mesh barrier (91 cm wide by 121 cm high) and 15 control min with no fleece, in a randomly selected order. The scent trials allowed the staff to assess the dam s response to scent from the cub and habituated her to being moved off exhibit during the day for later introduction sessions. Cameras were set up in the holding area so that all sessions could be remotely observed. During the 4 hr of scent trials, the frequency and (when appropriate) duration of behaviors indicating the dam s stress level (pacing, behavior directed at the barrier in front of the keepers, and roaring) and interest in the scented fleece (olfactory investigation, behavior directed at the barrier in front of where the fleece was placed) were examined. The mean duration/frequency was calculated when the fleece with the cub s scent was present and when it was absent for each behavior (see Figure 2). The absolute values of the differences (D) between these means were evaluated with randomization tests (Colegrave, Engel, & Plowman, 2006). The dam paced for significantly less time (D D 53%, p D.0005) and significantly less frequently (D D 38, p D.0005) when the cub s scent was present, and the frequency of roaring was significantly lower when the cub s

54 KELLING, BASHAW, BLOOMSMITH, MAPLE FIGURE 2 Behavior of the dam during exposure to either a piece of fleece scented by her cub or exposure to the same environment with no fleece. The top panel shows the frequency of each behavior, whereas the bottom panel shows its duration measured as the percentage of the 15-min session spent performing that behavior. Error bars show standard deviations and stars indicate significant differences between conditions at D.05. scent was present (D D 38, p D.0005). There was no difference in frequency or duration of behaviors directed toward the barrier separating the dam from the keepers. Although the duration of olfactory investigation and behaviors directed at the barrier in front of the fleece did not differ between conditions, significantly fewer of each of these behaviors were observed when the fleece was present (olfactory investigations: D D 34, p D.01; barrier-directed in front the fleece: D D 34, p D.001). There were no significant effects of order of presentation of fleece versus no-fleece trials on the dam s behavior. The dramatic decrease in the dam s pacing and roaring associated with the presence of the fleece was interpreted as a sign that being exposed to her cub s scent reduced the stress associated with being moved inside and held there for 30 min. This difference was not a result of how much time had passed since she was moved inside as there was no significant difference between the first

TIGER SOCIALIZATION 55 and second 15-min observation sessions. It was also not a function of greater total time spent investigating the fleece as total time showing interest in the location of the scented fleece did not differ as a function of whether the fleece was present. However, the time spent investigating was distributed differently in the two conditions. When the fleece was present, the dam investigated less often but stayed longer each time; when the fleece was absent, the dam investigated more often but spent little time on each visit. Reduced stress and a display of interest were considered positive signs for proceeding with introductions. After scent trials seemed promising and the cub became less dependent on bottle feeding, the second stage in preparing for reintroduction and testing reactions was begun. In these sessions, hereafter protected contact (PC) sessions, the cub was placed in the holding room next to the dam s so that the two tigers were separated by the same mesh barrier used for the scent trials. Initial PC sessions took place with the cub in a wooden box within the holding room to keep her within visual, olfactory, and auditory range of her dam on the other side of the barrier. Initial PC sessions were brief (15 30 min) because the cub was restless. Over the 30 sessions, PC sessions were extended to full-day events, and the cub was allowed access to the entire room next to the dam rather than being restricted to the box. Each PC session was observed by research staff from initiation until completion or until 1 hr had passed, whichever occurred first. PC sessions were monitored for aggression between the two animals, which would indicate a potential problem for reintroduction. In addition, each tiger was monitored for signs of stress. For the dam, pacing, which has been repeatedly linked to stress in captive big cats (e.g., Clubb & Mason, 2003), was recorded. For the cub selfsucking, which has been associated with stress in hand-reared primates (e.g., Nash, Fritz, Alford, & Brent, 1999), was recorded. Additionally, interest in the other animals (olfactory investigation, time spent proximate to or in contact with the barrier between animals, and prusten and whining vocalizations) was recorded. No aggression was observed. Stress-related behaviors did not appear to increase during reintroduction sessions. The dam s pacing occupied a mean of 30% of her observed time, a duration intermediate to those observed with and without the fleece present in scent trials, whereas the cub engaged in self-sucking less than 1% of the observed PC session duration. The tigers also showed interest in each other. Mean levels of olfactory investigation of the barrier or other tiger for the dam were similar to fleece trials (15%) and for the cub were about 4%. Both tigers spent between 30% and 40% of their time within one body length of the barrier separating them. Both animals were observed making prusten and whining vocalizations at the other (the dam s mean frequency was 120 vocalizations of this type per hour, whereas the cub averaged 23 per hour). On the basis of this information, animal managers decided to proceed with the reintroduction.

56 KELLING, BASHAW, BLOOMSMITH, MAPLE Reintroduction Both animal care staff and a data collector observed all introductions. Data collection began at the opening of the door between tigers and continued for 1 hr or until animals were separated, whichever occurred first. Given the desire to be systematic and move slowly to protect the cub, the first physical introduction did not occur until April 16, 2001, when the cub was 140 days old, and lasted 12 min. Early introductions took place in the holding area, which allowed for greater control and the ability to separate animals if problems have arose. Introductions continued daily, and after introductions were more than 2 hr in length, the animals were allowed to be together on exhibit. Unfortunately, the dam developed health problems, and the introductions had to be put on hold between Day 200 and 224. Introduction before this pause is presented as Phase 1 ; introduction after the pause is Phase 2. All Phase 2 introductions occurred outside in the exhibit area. Randomization tests of the F statistic were used to compare differences in aggression, behavioral indicators of stress (pacing and self-sucking), and behavioral indicators of interest (olfactory investigation, time spent proximate to the barrier between animals in PC sessions or the other animal during Phase 1 and 2) and prusten/whining vocalizations among PC sessions, Phase 1 introductions, and Phase 2 introductions for each individual. In addition to the behavioral indicators listed earlier, social interactions were recorded during introductions as a measure of interest. When significant differences were identified, randomization tests of the absolute value of the difference between the means for each pair of conditions were computed to locate the significant effect or effects. No aggression was observed, and at no time were the cub and her mother separated because of an interaction between them. Over time in Phase 1, the cub began to play with the dam (most often chasing the dam s tail) and would often watch or follow her. Figures 3 and 4 show changes in the frequency and duration of the monitored behaviors for the dam and cub, respectively. Behavioral indicators of stress differed across socialization conditions for both animals. For the dam, there was no significant difference in the frequency of pacing across conditions, but pacing occupied a significantly greater duration (F D 3.44, p D.047) in Phase 2 than in PC sessions (D D 18.8, p D.0165) with Phase 1 pacing at an intermediate level. The cub had a higher frequency of self-sucking (F D 5.57, p D.006) in Phase 2 than in PC sessions (D D 1.2, p D.0035) with Phase 1 self-sucking at an intermediate level. The cub also self-sucked for a greater percentage of the session (F D 8.65, p <.0005) in Phase 2 than in either PC sessions (D D 4.2, p <.0005) or Phase 1 (D D 4.1, p <.0005). Behaviors indicating social interest were also affected by condition (see Table 1). Introductions decreased the frequency and duration of olfactory in-

TIGER SOCIALIZATION 57 FIGURE 3 Behavior of dam during the introduction process. The top panel shows the frequency of each behavior, whereas the bottom panel shows its duration measured as the percentage of the session spent performing that behavior. Error bars show standard deviations. A star on a line between two conditions indicates a significant difference between the two conditions at the ends of the line, whereas a star over a single column indicates that that condition was significantly different from both other conditions at D.05. PC D protected contact.

58 KELLING, BASHAW, BLOOMSMITH, MAPLE FIGURE 4 Behavior of the tiger cub during the introduction process. The top panel shows the frequency of each behavior, whereas the bottom panel shows its duration measured as the percentage of the session spent performing that behavior. Error bars show standard deviations. A star on a line between two conditions indicates a significant difference between the two conditions at the ends of the line, whereas a star over a single column indicates that that condition was significantly different from both of the other conditions at D.05. PC D protected contact.

TIGER SOCIALIZATION 59 TABLE 1 Results of Randomization Analyses for Behavioral Indicators of Social Interest During the Introduction Process Interest Indicator Animal Measure Overall ANOVA Protected Contact Vs. Phase 1 Protected Contact Vs. Phase 2 Phase 1 Vs. Phase 2 Olfactory investigation Social interaction Proximate <1 body length Prusten or whine Dam Frequency F D 25.0* D D 22.9* D D 19.6* D D 3.4 Duration F D 7.27* D D 15.3* D D 13.0* D D 2.2 Cub Frequency F D 7.5* D D 8.0* D D 7.4* D D 0.6 Duration F D 6.1* D D 3.0* D D 3.5* D D 0.5 Dam Frequency F D 24.6* D D 10.8* D D 1.9 D D 8.9* Duration F D 17.1* D D 0.4* D D 0.1 D D 0.3* Cub Frequency F D 33.8* D D 26.8* D D 7.1 D D 19.7* Duration F D 8.5* D D 2.3* D D 0.3 D D 2.1* Dam Frequency F D 9.3* D D 34.5* D D 38.2* D D 3.7 Duration F D 7.1* D D 10.4 D D 23.0* D D 12.6 Cub Frequency F D 7.0* D D 0.7 D D 11.5* D D 10.7* Duration F D 0.5 Dam Frequency F D 28.7* D D 103.2* D D 105.1* D D 1.8 Cub Frequency F D 4.3* D D 12.2 D D 21.0* D D 8.8 Note. Asterisk indicates significant differences between conditions at D.05. vestigation for both animals. Frequency and duration of social interaction were significantly higher for both animals in Phase 1 than they were in either PC sessions or Phase 2 introductions. The frequency and duration of the dam s proximity decreased after the PC sessions, whereas the cub s duration of proximity was unchanged across conditions and her frequency of entering proximity did not significantly decrease until Phase 2. Finally, both the dam and cub showed significantly higher frequencies of prusten and whining in PC sessions than the introductions. Comparisons of proximity (contact, proximate, or distant) among the conditions are complicated by the different definitions for this behavior. In PC sessions, proximity was measured to the mesh barrier between animals as an indication of effort to be near the other individual. In Phase 1 and 2 introductions, however, proximity was measured to the other individual. Unlike the barrier, the other tiger was able to move away when approached in Phases 1 and 2. This difference probably caused the decreased proximity for the dam in Phases 1 and 2 compared with the PC sessions. For the cub, however, the duration of proximity did not significantly differ across conditions and the frequency of entering proximity did not decrease until Phase 2. Perhaps this lack of change in proximity for the cub during Phase 1, together with the high levels

60 KELLING, BASHAW, BLOOMSMITH, MAPLE of social interaction observed, indicates the cub sought out and interacted with her dam despite the greater effort required. This finding could be construed as an indication that the cub was strongly motivated to stay close to a conspecific when possible. DISCUSSION Based on the conversations with tiger managers and members of the Tiger SSP management committee, this cub was the oldest tiger cub to be successfully reintroduced to her mother. Early in the hand-rearing process the cub was exposed to a domestic cat, as has been suggested (Meier, 1986; Richardson, 1991). There were few interactions between them and it did not appear costeffective to use a domestic companion in this case. Efforts to return the cub to her dam as soon as possible appeared more effective. Scent trials and PC sessions facilitated the introduction process by confirming that aggression was absent, PC sessions and introductions did not increase stress for either individual, and both tigers were interested in each other. Although little direct interest was observed in either scent trials or PC sessions, the presence of the scent of the cub or the cub herself noticeably reduced stress-related behaviors for the dam. Observing a reduction in stress-related behaviors in the presence of another animal appears to be a sufficient criterion for proceeding with an introduction. Our data suggest that high levels of interest in or interaction with the other tiger, although a good sign, are not necessary to predict success if success is defined as the ability of the tigers to cohabitate without aggression. Although a reduction in stress-related behaviors (social comfort) in the presence of a familiar conspecific is well documented for ungulates (e.g., in domestic cattle, Bos Taurus; Takeda, Sato, & Sugawara, 2003), this effect has not been reported in carnivores whose adults are typically solitary, like tigers. Likewise, social comfort in the presence of a single-modality cue from a conspecific has not been studied in tigers, but it occurs in sheep. da Costa, Leigh, Man, & Kendrick (2004) have demonstrated that isolated adult domestic sheep (Ovis aries) show less behavioral and physiological stress when exposed to pictures of the faces of familiar sheep but not goats (Capra hircus) or triangles. It is of some interest that the cub s scent produces social comfort as the dam had less than 7 hr of exposure to her. This result suggests that social comfort in tigers may not be limited to familiar animals, especially if the scent is from a cub, or the 7-hr time frame may be adequate for the development of scent recognition in a mother tiger. Significant differences were observed between Phase 1 and Phase 2 of introductions with more social interactions and proximity occurring in Phase 1 and more stress-related behaviors occurring in Phase 2. As a result, Phase 2

TIGER SOCIALIZATION 61 introductions could be classified as less positive than Phase 1. These differences could have been a result of any number of factors, including the cub s increasing age, the health problems suffered by the dam, or the interruption of the introductions. It is impossible to determine which of these factors reduced the amount of interactions in Phase 2, but to be safe we recommend that introductions be conducted as early in the cub s development as is feasible. Overall, the introduction can be considered moderately successful in that the animals were not aggressive toward one another and did occasionally interact, though typical mother infant interactions, like social play and sustained contact, were rare. Although the generalizability of these data is limited by their focus on a single individual, this study provides some comparison data for evaluating the behavior of future hand-reared tigers during the introduction process. Additionally, this case study adds context to the mixed information obtained from the tiger studbooks concerning the reproductive and maternal success of hand-reared female tigers. Although primate data suggest that modern nursery rearing tends not to be as detrimental as it once was, conspecific socialization is still preferred (Bloomsmith et al., 2006). The process used in this study allowed the cub to be exposed to a conspecific and therefore have a richer social experience that may have mitigated the typical social problems of hand-rearing. The cub was transferred to the Sacramento Zoo, where on November 24, 2006, at almost six years old, she successfully naturally mated, delivered, and reared her first litter of three cubs. She also produced another litter on March 18, 2010, which resulted in one surviving cub. Therefore, it appears that some exposure to an adult tiger may provide adequate socialization for normal reproduction in Sumatran tigers, even if the exposure is limited and provided relatively late in the cub s development. CONCLUSION In conclusion, this study demonstrates that a systematic, stepwise reintroduction procedure did not lead to aggression between a Sumatran tiger cub and her dam or indications of increased stress in either individual. Although the full introduction did not take place until the cub was almost five months old, the exposure to a conspecific was most likely beneficial, as when the cub matured, she successfully reproduced and reared offspring. ACKNOWLEDGMENTS The cooperation and support of animal care staff, nursery staff and volunteers, veterinary staff, and curators at Zoo Atlanta made this project possible. In partic-

62 KELLING, BASHAW, BLOOMSMITH, MAPLE ular, Dr. Maria Crane, Dr. Rita McManamon, Dr. Dwight Lawson, and Debora Anderson were open to sharing decisions that were made during the rearing and reintroduction of the cub and discussing the reasoning behind these decisions. Richard Hezlep and Scott Paul set up and maintained the camera system for remote observations. Ron Tilson, Kathy Traylor-Holzer, Gerry Brady, Jeff Wyatt, Steve Taylor, Michelle Stanzer, Lee Nesler, and Alan Sironen provided helpful information and recommendations about hand-rearing and reintroducing the cub. Drs. Maria Crane, Jill Mellen, and Rebecca Snyder commented on earlier drafts of this manuscript. REFERENCES Bashaw, M. J., Gullott, R. L., & Gill, E. C. (2010). What defines successful integration into a social group for hand-reared chimpanzee infants? Primates, 51, 139 147. Beck, B. B., & Power, M. L. (1988). Correlates of sexual and maternal competence in captive gorillas. Zoo Biology, 7, 339 350. Bloomsmith, M. A., Baker, K. C., Ross, S. R., & Lambeth, S. P. (2006). Early rearing conditions and captive chimpanzee behavior: Some surprising findings. In G. P. Sackett, G. C. Ruppentahal, & K. Elias (Eds.), Nursery rearing of nonhuman primates in the 21st century (pp. 289 312). New York, NY: Springer Science C Business Media. Bush, M., Phillips, L., & Montali, R. (1994). Hand-rearing of cubs. In R. Tilson, G. Brady, K. Traylor-Holzer, & D. Armstrong (Eds.), Management and conservation of captive tigers (pp. 76 80). Apple Valley, MN: Minnesota Zoo. Clubb, R., & Mason, G. (2003). Captivity effects on wide-ranging carnivores. Nature, 425, 473 474. Colegrave, N., Engel, J., & Plowman, A. B. (2006). Randomisation tests. In A. B. Plowman (Ed.), Zoo research guidelines: Statistics for typical zoo datasets (pp. 7 16). London, UK: BIAZA. da Costa, A. P., Leigh, A. E., Man, M., & Kendrick, K. M. (2004). Face pictures reduce behavioural, autonomic, endocrine, and neural indices of stress and fear in sheep. Proceedings of the Royal Society of London B: Biological Sciences, 271, 2077 2084. Duffy, J. A., & Hendricks, S. E. (1973). Influences of social isolation during development on sexual behavior of the rat. Animal Learning and Behavior, 1, 223 227. Edwards, M. S., & Hawes, J. (1997). An overview of small felid hand-rearing techniques and a case study for Mexican margay Leopardus wiedii glaucula at the Zoological Society of San Diego. International Zoo Yearbook, 35, 90 94. Hakala, S., & Traylor-Holzer, K. (1994). Early maternal and cub behavior. In R. Tilson, G. Brady, K. Traylor-Holzer, & D. Armstrong (Eds.), Management and conservation of captive tigers (pp. 73 75). Apple Valley, MN: Minnesota Zoo. Harlow, H. (1971). Learning to love. Chicago, IL: Aldine. Hedberg, G. (2002). Exotic felids. In L. J. Gage (Ed.), Hand-rearing wild and domestic mammals (pp. 207 220). Ames, IA: Blackwell. Hoff, W. (1961). Hand raising baby cats at Lincoln Park Zoo. International Zoo Yearbook, 2, 86 89. Jendry, C. (1996). Utilization of surrogates to integrate hand-reared infant gorillas into an age/sex diversified group of conspecifics. Applied Animal Behaviour Science, 48, 173 186. King, N. E., & Mellen, J. D. (1994). The effects of early experience on adult copulatory behavior in zoo-born chimpanzees Pan troglodytes. Zoo Biology, 13, 51 59. Kleiman, D. G. (1974). The estrus cycle in the tiger. In R. L. Eaton (Ed.), The world s cats: Volume II (pp. 60 75). Seattle, WA: Feline Research Group.

TIGER SOCIALIZATION 63 Maple, T. L., & Hoff, M. P. (1982). Gorilla behavior. New York, NY: Van Nostrand Reinhold. McManamon, R., & Hedberg, G. (1993). Practical tips in nursery rearing of exotic cats. Journal of Small Exotic Animal Medicine, 2, 137 140. Meder, A. (1989). Effects of hand-rearing on the behavioral development of infant and juvenile gorillas Gorilla g. gorilla. Developmental Psychobiology, 22, 357 376. Meder, A. (1990). Integration of hand-reared gorillas into breeding groups. Zoo Biology, 9, 157 164. Meier, J. E. (1986). Neonatology and hand-rearing of carnivores. In M. E. Fowler (Ed.), Zoo and wild animal medicine (2nd ed., pp. 842 852). Philadelphia, PA: W.B. Saunders. Mellen, J. D. (1992). Effects of early rearing experience on subsequent adult sexual behavior using domestic cats Felis catus as a model for exotic small felids. Zoo Biology, 11, 17 32. Nash, L. T., Fritz, J., Alford, P. A., & Brent, L. (1999). Variables influencing the origins of diverse abnormal behaviors in a large sample of captive chimpanzees Pan troglodytes. American Journal of Primatology, 48, 15 29. Novak, M. A., & Sackett, G. P. (2006). The effects of rearing experience: The early years. In G. P. Sackett, G. C. Ruppentahal, & K. Elias (Eds.), Nursery rearing of nonhuman primates in the 21st century (pp. 3 19). New York, NY: Springer Science C Business Media. Read, B. W., & Meier, J. E. (1996). Neonatal care protocols. In D. G. Kleiman, M. E. Allen, K. V. Thompson, & S. Lumpkin (Eds.), Wild mammals in captivity: Principles and techniques (pp. 41 55). Chicago, IL: University of Chicago. Richardson, D. M. (1988). Hand-rearing exotic felids. In R. Colley (Ed.), The hand-rearing of wild animals (pp. 51 54). Bristol, UK: Association of British Wild Animal Keepers. Richardson, D. M. (1991). Guidelines for handrearing exotic felids. In J. Partridge (Ed.), Management guidelines for exotic cats (pp. 116 117). Bristol, UK: Association of British Wild Animal Keepers. Ryan, S., Thompson, S. D., Roth, A. M., & Gold, K. C. (2002). Effects of hand-rearing on the reproductive success of western lowland gorillas in North America. Zoo Biology, 21, 389 401. Seager, S. W. J., & Demorest, C. N. (1986). Reproduction in captive wild carnivores. In M. E. Fowler (Ed.), Zoo and wild animal medicine (2nd ed., pp. 852 882). Philadelphia, PA: W.B. Saunders. Snyder, R. J., Zhang, A. J., Zhang, Z. H., Li, G. H., Tian, Y. Z., Huang, X. M., : : : Maple, T. L. (2003). Behavioral and developmental consequences of early rearing experience for captive giant pandas (Ailuropoda melanoleuca). Journal of Comparative Psychology, 117, 235 245. Takeda, K., Sato, S., & Sugawara, K. (2003). Familiarity and group size affect emotional stress in Japanese Black heifers. Applied Animal Behavior Science, 82, 1 11. Thapar, V. (1986). Tiger: Portrait of a predator. New York, NY: Facts on File. Thomas, P., & Philips, R. (1978). Hand rearing fennec foxes Fennecus zerda using a domestic dog as a foster mother. International Zoo Yearbook, 18, 208 209. Tiger Species Survival Plan. (2012). Unpublished data. Traylor-Holzer, K. (2010a). North American regional Amur tiger studbook: Panthera tigris altaica. Apple Valley, MN: Minnesota Zoo. Traylor-Holzer, K. (2010b). North American regional Malayan tiger studbook: Panthera tigris jacksoni. Apple Valley, MN: Minnesota Zoo. Traylor-Holzer, K. (2010c). North American regional Sumatran tiger studbook: Panthera tigris sumatrae. Apple Valley, MN: Minnesota Zoo.