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Behavioral restriction effects on activity motivation of a captive lion (Panthera leo persica)
Journal of Veterinary Behavior 17 (2017) 14e18
Contents lists available at ScienceDirect
Journal of Veterinary Behavior journal homepage: www.journalvetbehavior.com
Small Mammal/Wildlife Research
Behavioral restriction effects on activity motivation of a captive lion (Panthera leo persica) Daisuke Kohari a, *, Ayaka Sunada a, Yukiko Matsui b, Ayumi Ootaki c, Hidemasa Hori d a
College of Agriculture Ibaraki University, Ibaraki, Japan Tama Zoological Park, Tokyo, Japan c Zoolasia Yokohama Zoological Gardens, Asahi-ku, Kanagawa, Japan d Inokashira Park Zoo, Tokyo, Japan b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 26 May 2016 Received in revised form 6 September 2016 Accepted 4 November 2016 Available online 14 November 2016
It has been suggested that the locomotive needs of zoo animals are not always satisfied in captive conditions. However, these reasons for movement and locomotion differ among species. This study investigated the locomotive motivation of captive lions, which are regarded as having relatively low motivation to move compared to other zoo animals. Four Indian lions including 1 noncastrated male and 3 females were observed as subject animals. Two captive conditions were set as experimental days: 1 was a confined condition in a bed chamber all day long (confined day); another was a released condition, with access to the exhibition area during daytime (released day). The observation periods were also defined as “daytime” (9:00-16:00) and “nighttime” (16:30-9:00 of the next morning). We counted the lions’ behavior repertories and recorded their maintenance, social, reproductive, and abnormal pacing behavior of 24 hours each day 5 times from the beginning of August to the end of November. Results show no difference in the numbers of behavior repertories between the released and confined days (c2 ¼ 0.084, NS), suggesting that the conditions in this zoo might be sufficient for captive lions to express various behavior repertories. However, the maintenance behavior percentages were significantly different when confined and released days were compared (daytime, c2 ¼ 19.17, P < 0.01; nighttime, c2 ¼ 13.06, P < 0.05). All the lions rested nearly all day long except around evening housing time or in the morning on the released days. However, on confined days, they were usually restless. Furthermore, abnormal pacing during walking (c2 ¼ 3.94, P < 0.05) was significantly different on each day. These results suggest that the lion’s locomotor needs were not satisfied when the lions were confined in the bed chamber all day, even though they did not always move actively. It might be important for the lions to have some opportunity to ramble. Ó 2016 Elsevier Inc. All rights reserved.
Keywords: behavior motivation lion pacing stress welfare
Introduction Exhibiting the active life of animals is one mission of zoos. Zoos are constantly being required to evaluate the behavioral needs and welfare of animals. Generally, many zoo animals are kept in more restricted environments than in their natural habitat (Clubb and Mason, 2003; Hosey et al., 2009; Rees 2011a). Especially, for animals with complex or energetic behavioral needs, some of these
* Address for reprint requests and correspondence: College of Agriculture Ibaraki University, Ami 4668-1 Inashiki-gun, Ibaraki, 300-0331 Japan. Tel/Fax: þ81 29 888 8705. E-mail address: [email protected] (D. Kohari). http://dx.doi.org/10.1016/j.jveb.2016.11.002 1558-7878/Ó 2016 Elsevier Inc. All rights reserved.
might not be satisfied sufficiently in such a zoo environment. Reportedly, zoo animals become stressed and show abnormal behaviorsdthose not occurring or occurring in an altered frequency from that shown in the wild and with no readily apparent goal or function. Such behaviors include stereotypies but also other behaviors such as overgrooming and regurgitation and reingestion (Rushen and Mason, 2006), which occur when the individual is unable to reach a particular goal by performing appetitive behavior, unable to reach a desired place, or unable to escape from a disturbance (Carlstead, 1996). For example, stereotypic pacing levels in Indian leopard were increased in environmental conditions that lacked both space and complexity (Mallapur and Chellam, 2002). Asiatic black bears performed a high proportion of stereotypy, which might be derived from territorial patrolling or attempts to
D. Kohari et al. / Journal of Veterinary Behavior 17 (2017) 14e18
15
prompt interaction with the neighboring animals with their neighboring conditions (Vickery and Mason, 2004). These behaviors, which have been thought to have developed as a means of coping with aversive environments, should be taken as a warning sign of potential suffering (Swaisgood and Shepherdson 2005). Therefore, it is important to consider the effects of restrictive conditions that might prevail in a zoo environment, various behavioral motivations of animals, and their relations with abnormal behaviors for stress control during zoo animal management. Lions (Panthera leo) are widely reported as a species with individuals that typically move inactively (Rees, 2011b) and which spend long periods sleeping, about 10-15 h/day under some captive conditions (Haas, 1958). Furthermore, Schaller (1972) reported that lions have been observed to rest almost 20-21 h/day in the wild. Consequently, their behavioral motivation for movement might be low. Effects of environment on their behavior might be slight, even when under a restricted condition, but some correlation exists between the frequencies of abnormal behavior and the home range size in the wild for each species (Clubb and Mason, 2003). Although lions may not be constantly active, a restricted condition might therefore be stressful, even when temporary, because their average home range size is 80-100 km2 in the wild. This study investigated the number of behavior repertoires, the time spent on maintenance behaviors, and the abnormal behavior of the lions to learn whether their behavioral motivations are affected by the restrictions of behavior opportunities under captive conditions. Materials and methods Animals and management Four Indian lions (Panthera leo persica) kept in Ueno Zoological Park were observed. Three of them (Mohan_, Shakti\, and Anita\) were 10 years old. One of them (Chandi\) was 16 years old. Chandi was born in Zoolasia Yokohama Zoological Gardens in 1996 and moved to Ueno Zoological Park in 2002. The same year, she gave birth to Mohan, Shakti, and Anita. Reproduction was controlled by estrus behavior observation of females. Mohan was not castrated during the experiment. Their exhibition area is enclosed by imitation rock walls, wire fences, and tempered glass (Figure 1). There are electrically wired fences on the top of the lions’ enclosure and trees in the exhibition area to prevent escape and to protect planted trees. The enclosure size is about 540 m2. The earthen floor slopes gently from the center to the south corner of the area. A pond is situated in the northeastern area, with imitation arched wood placed at the center of the enclosure. Imitation rocks or wood, as well as real rocks, are also placed there. Four sleep chambers are located at the rear of the exhibition area. One chamber (2.5 2.9 m2) is used by Mohan. Two rooms (2.5 4.9 m2/room) are used by the three females. A water pool is situated at the corner of the rest chamber and at a den under the steps in a rest chamber. In addition, a scratching log (1.5 m long) is in the female’s rest chamber. They are fed horse, rabbit, and chicken meat once a day after evening housing. In addition, they are fasted irregularly once a week. Behavior observation Two experimental days were set up for this observation. One is a “released day,” on which the lions were released to the exhibition area from 9:00 to 16:30 and were housed in the rest chamber at other times. Another is a “confined day,” during which they were in the rest chamber all day long. Observations were conducted 5 times on 2 successive days, a confined day and the subsequent released
Figure 1. Diagram of the study area. Dotted areas show the exhibition area. Striped areas are the lion’s rest chambers. “P” denotes a pond. “R” denotes the two imitation rocks in the enclosure. Black bars show imitation woods. Double lines around the enclosure show the viewpoint of this exhibition.
day, from the beginning of August to the end of November. The observation periods were also defined as “daytime” (9:00-16:00) and “nighttime” (16:30-9:00 of the next morning). We recorded the behaviors of the respective lions in the exhibition area for 15 min/h by naked eye observation during the daytime. The nighttime or confined day behavior in the rest chamber was recorded using a wide angle camera (SM-C56N; Wireless Tsukamoto Co. Ltd., Japan) or an infrared-night vision camera (SM-CSW24A; Wireless Tsukamoto Co. Ltd.) with a digital video recorder (DVR-4200P; MotherTool Co. Ltd., Japan). The behavior repertories in each 24 hours of observation days were counted using ad libitum sampling method (Martin and Bateson, 1993). Maintenance behaviors (resting, eating, eliminating, self-grooming, walking, others), social behaviors, reproductive behaviors, abnormal pacing behaviors, and other behaviors were observed for each lion using 1-minute instantaneous sampling method. Data collection was conducted by the same observer throughout the experiment. Statistical analysis Observed behaviors were classified by reference to feline behavior (Sato et al., 2011). The numbers of the daytime and nighttime behavior repertories in subject lions were summed and compared between the released and the confined days using a 2 2 contingency table (chi-square test for independence). Furthermore, each behavior category such as maintenance, social, reproductive, abnormal, and other behavior were compared between the released and the confined days by a 2 3 contingency table. (The repertories of reproductive, abnormal, and other behaviors were summed because their numbers were 5, which does not satisfy the condition of chi-square tests.) The percentage of maintenance
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D. Kohari et al. / Journal of Veterinary Behavior 17 (2017) 14e18
Table Descriptions of the 53 specific behavior repertories of Indian lions (Panthera leo persica) observed for this study Behavior categories Maintenance behavior Feed Rest Eliminate Self-protect Self-groom Investigate Solitary play Locomote Social behavior Spacing Social investigate Agonistic Affiliative Social play Reproductive behavior Sexual Abnormal behavior Stereotypy Others
Descriptions
Specific behavior repertories
Behaviors of ingesting food and water Behaviors of staying motionless and relaxed various styles Behaviors of excreting feces or urine Behaviors of maintaining body temperature or homeostatic states Behaviors of cleaning body or relieving body itches or driving off bugs Behaviors of exploring environment information using sensory organs Behaviors of playing themselves Behaviors of moving from one to another place
Feeding, drinking Stand resting, sternum lying, lateral lying, dog sitting, lying with dorsal position (sleeping) Excretion, urination Panting, seeking shade, sunbathing, freezing Shivering, licking, biting, scratching, yawning, Tree clawing, rubbing, stretching Listening, watching Object play Walking, running, climbing
Behaviors of territoriality and keeping personal space Behaviors Behaviors Behaviors Behaviors
of of of of
exploring other lions aggressive interaction with other lions friendly interaction with other lions playing with other lions
Keeping individual distance, keeping social distance, vocalization, marking (rhythmic emission of urine), leading, following Listening, watching, sniffing Threatening, pawing, chasing, escaping, avoiding Touching, rubbing, licking Play chasing, rolling, mock fighting
Behaviors of sexual interaction with other lions
Vulva sniffing, flehmen
Behaviors of abnormal repetitive actions Other behaviors that do not fit above categories
Pacing Licking floor, scratching floor, pawing fence
behavior was compared using a 2 6 contingency table. The percentages of abnormal pacing done during walking were compared between the released and the confined days using a 2 2 contingency table, respectively, during the daytime and nighttime. Results In all, we observed 240 hours of these lions’ behavior and identified 53 behavior repertories (Table). On the released days, 51 repertories (daytime, 46; nighttime, 42) in all were observed, with 42 repertories (daytime, 42; nighttime, 41) observed on the confined days. However, the numbers of behavior repertories on the released and the confined days during the daytime and nighttime were not significantly different (c2 ¼ 0.084, df ¼ 1, NS, Figure 2). In addition, we compared these differences in each behavior category. Results show no difference between the released and confined days (c2 ¼ 0.429, df ¼ 2, NS, Figure 3).
Figure 2. The number of behavior repertories of the lions between the confined days and the released days. White bars represent the number of the daytime repertories. Black bars represent the number of the nighttime repertories observed.
Percentages of daytime behavior were significantly different between the released and confined days (c2 ¼ 19.17, df ¼ 6, P < 0.01, Figure 4). The resting behavior was 69.8% on confined days but 86.0% on released days. Walking was 22.3% on confined days but only 3.0% on released days. Similarly, percentages of nighttime behavior were significantly different between days (c2 ¼ 13.06, df ¼ 6, P < 0.05). Resting behavior was 75.5% on confined days but 93.1% on released days. Walking was 14.8% on confined days but only 3.3% on released days. Average transitions of these behaviors during 24hour observation were presented in Figure 5. All the lions rested nearly all day long except around evening housing time (16:0017:00) or in the morning (8:00-9:00) on the released days. However, on the confined days, they were usually restless. They spent about 60.7% of their time walking at 9:00. There was a steady decrease in percentage of time spent walking until evening housing. However, time spent walking increased again at 16:00 and continued until around 20:00. Furthermore, walking increased from 3:00 on the confined days. It reached 42.3% at 8:00, but it increased from 6:00 on the released days and became 21.1% at 8:00.
Figure 3. Differences of numbers of respective behavior repertories of the lions between the confined days and the released days. White bars represent the number of the daytime repertories. Striped bars represent the number of the nighttime repertories observed.
D. Kohari et al. / Journal of Veterinary Behavior 17 (2017) 14e18
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Figure 5. Twenty-four-hour transition of resting and walking behaviors of lions between confined days and the released days. The upper line graph shows the behavior on confined days. The lower one shows the behavior on released days. Dotted lines with filled circles show percentages of walking. Normal lines with open circles show percentages of resting each hour.
Figure 4. Difference of the percentages of the maintenance behavior of the lions between the confined days and the released days. The upper bar graph shows daytime percentages. The lower bar graph shows nighttime percentages.
The respective percentages of abnormal pacing during walking on the released days and the confined days during daytime and nighttime were found to be significantly different (c2 ¼ 3.94, df ¼ 1, P < 0.05, Figure 6) and were lower by about one-fourth on confined compared to released days during the daytime (confined days, 81.3%; released days, 63.6%). In addition, these percentages were lower by about half on confined compared to released days during the nighttime (confined days, 84.5%; released days, 39.9%). Discussion We had expected that the number of the behavior repertories of the lions would be few because lions generally spend almost the entire day resting or sleeping under captive conditions, as they apparently also do in the wild (Schaller, 1972). Nevertheless, we recorded 53 behavior repertories during the observation periods, covering almost all normal feline behavior repertories under captive conditions (84 repertories; Sato et al., 2011). Some behaviors related to reproduction or aggression, which in felines are reported to be 17 and 13 repertoires, respectively (Sato et al., 2011), were infrequently observed because members of the observed group were all of a single consanguine family. However, some agonistic behaviors were only observed from male to female lions. Social play and spacing behavior among them was observed only during released days. These results were affected mainly by the difference in environmental conditions. On the other hand, no difference was observed in the number of behavior repertories shown on released and confined days. Barren and restrictive
environments such as that of the confined day condition, compared to the released condition, often lead to decreased behavior diversity and development of higher levels of stereotypy (Dantzer, 1986; Gunn and Morton, 1995); therefore, we had expected that the confined condition would affect the numbers of the behavior repertories of the lions. However, the numbers of behavior repertories were not significantly different in these 2 experimental conditions. Therefore, these conditions in this zoo might be sufficient for captive lions to express various behavior repertories. The difference of the experimental conditions did not affect the lions’ behavioral diversity. The condition of the behavior, such as the time spent resting and walking, differed significantly. The time spent walking on confined days was greater than that on released days. The time spent resting shows opposite results. When these percentages of resting are converted to a 24-hour scale, the resting time on released days became 22.3 hours and that on confined days became 18.1 hours. Although the results are slightly longer, as reported by Schaller (1972), the effect of about 4 hours decreased resting time might
Figure 6. Percentages of pacing behavior during walking time between confined days and released days. White bars show percentages of pacing on the released days. Black bars show the percentages of pacing on confined days.
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D. Kohari et al. / Journal of Veterinary Behavior 17 (2017) 14e18
be extremely great for lions, which spend most of the day sleeping. In addition, the behavioral transition of walking and resting was influenced by the daytime locomotive situation. These results suggested that the restriction of the opportunity to get around the exhibition area or for social contact had disturbed the daytime and nighttime behaviors. That is to say, the limitations against moving around the exhibition area in this study might present some stress. No matter how they exercised in the rest chamber, the lions were unable to resolve their modest locomotive motivation, even though the expression of their behavior repertories was almost assured. Abnormal pacing, which accounted for almost the entire walking time, was higher than on released days. Reportedly, that stereotyped behavior in carnivores derives from various factors such as motivation involved in feeding (Carlstead, 1998; Rees, 2009), range restriction or restriction of normal activity (van Keulen-Kromhout, 1978; Clubb and Vickery, 2008), and motivations to approach conspecifics (Vickery and Mason, 2004; Clubb and Vickery, 2008). Locomotive stereotypies are also reduced when some animals are moved from a small enclosure to a large enclosure (Carlstead 1991; Langenhorst 1998). Compared to the exhibition area, the space in the rest chamber is too small for exercise. The enclosure was less stimulating. Although we thought that locomotive motivations of lions might be low, getting around the exhibition area and contacting one another during the released days appears to have important meaning for them, even though these times were few and short. On the other hand, how much space and what kind of stimuli an animal needs remain unclear. Ödberg (1987) reported that bank voles in a small enriched cage exhibited less stereotypic behavior than those kept in large and barren cage. Similarly, Wilson (1982) pointed out that objects within environments may be more important for captive apes than the size or construction of the enclosure. Consequently, it is necessary to clarify the reason that the pacing behavior was increased in lions and the difference in quality between the respective enclosures. In conclusion, our results suggest that the restrictions of behavior opportunity under the captive conditions strongly affect the resting and walking behavior and their activities during the daytime and nighttime. Staying in small and less stimulative rest chambers all day led to decreased resting time, increased walking time, and increased percentages of pacing during walking. These results might reflect that their motivation for activity was not satisfied in that condition. It might be important for lions, which do not always move around, to have the opportunities to ramble around the enclosure, whether they choose to exercise that opportunity. Zoo managers must consider the quality of animal behavior and the environment at the time of the behavior. In addition, the length of restrictive period must be considered. Longterm residence in barren and inadequate environments is well known to lead to accumulation of animals’ frustration and the development of specialized abnormal behavior and reduced behavioral diversity (Dantzer, 1986, Clubb and Vickery, 2008). In this study, our restrictive conditions such as the confined days were only 24 hours. However, in some cases such as medical treatment or perinatal care, animals might need to be restricted for a long time. Consequently, more research might be necessary to clarify the effects not only of the difference of the temporal behavioral opportunity but also of the restrictive period for lions. Acknowledgments The authors thank the Ueno Zoological Garden for providing animals for cooperation with this study and the staff at the Ueno Zoological Garden at that time for their enthusiastic assistance with the research. Daisuke Kohari was responsible for the research idea,
experimental design, and writing the article. Data collection, care of animals, and research schedule management were performed by Ayaka Sunada, Yukiko Matsui, Ayumi Ootaki, and Hidemasa Hori with data analysis by Daisuke Kohari. Ethical considerations We read the policy of the journal on ethical consent and standard animal care, and our work was carried out in accordance with these policies. Furthermore, we limited animal use in accordance with “Three Rs” indicated in Directive 2010/63/EU. Conflict of interest The authors declare no conflict of interest. References Carlstead, K., 1991. Husbandry of the Fennec fox: Fennecus zerda: environmental conditions influencing stereotypic behaviour. Int. Zoo Yearb. 30, 202e207. Carlstead, K., 1996. Effect of captivity on the behaviour of wild mammals. In: Kleiman, D.G., Allen, M.E., Thompson, K.V., Lumpkins, S. (Eds.), Wild Mammals in Captivity: Principles and Techniques. University of Chicago press, Chicago, pp. 317e333. Carlstead, K., 1998. Determining the causes of stereotypic behaviors in zoo carnivores: towards developing appropriate enrichment strategies. In: Shepherdson, D.J., Mellen, J., Hutchins, M. (Eds.), Second Nature Environmental Enrichment for Captive Animals. Smithsonian Institution Press, Washington, D.C., pp. 172e183. Clubb, R., Mason, G., 2003. Animal welfare: captivity effects on wide-ranging carnivores. Nature 425, 473e474. Clubb, R., Vickery, S., 2008. Locomotory stereotypies in carnivores: does pacing stem from hunting, ranging or frustrated escape? In: Mason, G., Rushen, J. (Eds.), Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare, Second edition. CAB International, Wallingford, pp. 58e85. Dantzer, R., 1986. Behavioral, physiological and functional aspects of stereotyped behavior: review and a re-interpretation. J. Anim. Sci. 62, 1776e1786. Gunn, D., Morton, D.B., 1995. Inventory of the behaviour of New Zealand white rabbits in laboratory cages. Appl. Anim. Behav. Sci. 45, 277e292. Haas, G., 1958. 24-Stunden-Periodik von Grosskatzen im Zoologischen garten. Saugetierk. Mitt. 6, 113e117. Hosey, G., Melfi, V., Pankhurst, S., 2009. Behavioural Response to the Zoo Environment: Zoo animals behaviour, management, and welfare, Second edition. Oxford University Press, Oxford, p. 93. Langenhorst, T., 1998. Behavior of a brown bear group (Ursus arctos) with behavioral enrichment at the Hellbrunn/Salzburg. Der Zoologische Garten 68, 167e186. Mallapur, A., Chellam, R., 2002. Environmental influences on stereotypy and the activity budget of Indian leopards (Panthera pardus) in four zoos in southern India. Zoo Biol. 21, 585e595. Martin, P., Bateson, P., 1993. Measuring Behavior an Introductory Guide. Cambridge University Press, Cambridge, pp. 84e100. Ödberg, F.O., 1987. The influence of cage size and environmental enrichment othe development of stereotypies in bank voles (Clethrionomys glareolus). Behav. Process. 14, 155e176. Rees, P.A., 2009. Activity budgets and the relationship between feeding and stereotypic behaviors in Asian elephants (Elephas maximus) in a zoo. Zoo Biol. 28, 79e97. Rees, P.A., 2011. Zoo and exhibit design. In: An Introduction to Zoo Biology and Management. Wiley Blackwell, Oxford, pp. 137e145. Rees, P.A., 2011. Zoo and exhibit design. In: An Introduction to Zoo Biology and Management. Wiley Blackwell, Oxford, pp. 189e199. Rushen, J., Mason, G., 2006. A decade-or-more’s progress in understanding stereotypic behaviour. In: Mason, G., Rushen, J. (Eds.), Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare, second edition. CAB International, Wallingford, pp. 1e18. Sato, S., Kondo, S., Tanaka, T., Kusunose, R., Mori, Y., Idani, G., 2011. Ethograms of Animals in Captivity. Asakurashoten, Tokyo, pp. 22e162. (Japanese). Schaller, G.B., 1972. The Serengeti Lion: A Study of Predator-prey Relations. University of Chicago press, Chicago, pp. 119e125. Swaisgood, R.R., Shepherdson, D.J., 2005. Scientific approaches to enrichment and stereotypies in zoo animals: what’s been done and where should we go next? Zoo Biol. 24, 499e518. van Keulen-Kromhout, G., 1978. Zoo enclosure for zoo bears Ursidae: their influence on captive behaviour and reproduction. Int. Zoo Yearb. 18, 177e186. Vickery, S., Mason, G., 2004. Stereotypic behavior in Asiatic black and Malayan sun bears. Zoo Biol. 23, 409e430. Wilson, S.F., 1982. Environmental influences on the activity of captive apes. Zoo Biol. 1, 201e209.
Contents lists available at ScienceDirect
Journal of Veterinary Behavior journal homepage: www.journalvetbehavior.com
Small Mammal/Wildlife Research
Behavioral restriction effects on activity motivation of a captive lion (Panthera leo persica) Daisuke Kohari a, *, Ayaka Sunada a, Yukiko Matsui b, Ayumi Ootaki c, Hidemasa Hori d a
College of Agriculture Ibaraki University, Ibaraki, Japan Tama Zoological Park, Tokyo, Japan c Zoolasia Yokohama Zoological Gardens, Asahi-ku, Kanagawa, Japan d Inokashira Park Zoo, Tokyo, Japan b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 26 May 2016 Received in revised form 6 September 2016 Accepted 4 November 2016 Available online 14 November 2016
It has been suggested that the locomotive needs of zoo animals are not always satisfied in captive conditions. However, these reasons for movement and locomotion differ among species. This study investigated the locomotive motivation of captive lions, which are regarded as having relatively low motivation to move compared to other zoo animals. Four Indian lions including 1 noncastrated male and 3 females were observed as subject animals. Two captive conditions were set as experimental days: 1 was a confined condition in a bed chamber all day long (confined day); another was a released condition, with access to the exhibition area during daytime (released day). The observation periods were also defined as “daytime” (9:00-16:00) and “nighttime” (16:30-9:00 of the next morning). We counted the lions’ behavior repertories and recorded their maintenance, social, reproductive, and abnormal pacing behavior of 24 hours each day 5 times from the beginning of August to the end of November. Results show no difference in the numbers of behavior repertories between the released and confined days (c2 ¼ 0.084, NS), suggesting that the conditions in this zoo might be sufficient for captive lions to express various behavior repertories. However, the maintenance behavior percentages were significantly different when confined and released days were compared (daytime, c2 ¼ 19.17, P < 0.01; nighttime, c2 ¼ 13.06, P < 0.05). All the lions rested nearly all day long except around evening housing time or in the morning on the released days. However, on confined days, they were usually restless. Furthermore, abnormal pacing during walking (c2 ¼ 3.94, P < 0.05) was significantly different on each day. These results suggest that the lion’s locomotor needs were not satisfied when the lions were confined in the bed chamber all day, even though they did not always move actively. It might be important for the lions to have some opportunity to ramble. Ó 2016 Elsevier Inc. All rights reserved.
Keywords: behavior motivation lion pacing stress welfare
Introduction Exhibiting the active life of animals is one mission of zoos. Zoos are constantly being required to evaluate the behavioral needs and welfare of animals. Generally, many zoo animals are kept in more restricted environments than in their natural habitat (Clubb and Mason, 2003; Hosey et al., 2009; Rees 2011a). Especially, for animals with complex or energetic behavioral needs, some of these
* Address for reprint requests and correspondence: College of Agriculture Ibaraki University, Ami 4668-1 Inashiki-gun, Ibaraki, 300-0331 Japan. Tel/Fax: þ81 29 888 8705. E-mail address: [email protected] (D. Kohari). http://dx.doi.org/10.1016/j.jveb.2016.11.002 1558-7878/Ó 2016 Elsevier Inc. All rights reserved.
might not be satisfied sufficiently in such a zoo environment. Reportedly, zoo animals become stressed and show abnormal behaviorsdthose not occurring or occurring in an altered frequency from that shown in the wild and with no readily apparent goal or function. Such behaviors include stereotypies but also other behaviors such as overgrooming and regurgitation and reingestion (Rushen and Mason, 2006), which occur when the individual is unable to reach a particular goal by performing appetitive behavior, unable to reach a desired place, or unable to escape from a disturbance (Carlstead, 1996). For example, stereotypic pacing levels in Indian leopard were increased in environmental conditions that lacked both space and complexity (Mallapur and Chellam, 2002). Asiatic black bears performed a high proportion of stereotypy, which might be derived from territorial patrolling or attempts to
D. Kohari et al. / Journal of Veterinary Behavior 17 (2017) 14e18
15
prompt interaction with the neighboring animals with their neighboring conditions (Vickery and Mason, 2004). These behaviors, which have been thought to have developed as a means of coping with aversive environments, should be taken as a warning sign of potential suffering (Swaisgood and Shepherdson 2005). Therefore, it is important to consider the effects of restrictive conditions that might prevail in a zoo environment, various behavioral motivations of animals, and their relations with abnormal behaviors for stress control during zoo animal management. Lions (Panthera leo) are widely reported as a species with individuals that typically move inactively (Rees, 2011b) and which spend long periods sleeping, about 10-15 h/day under some captive conditions (Haas, 1958). Furthermore, Schaller (1972) reported that lions have been observed to rest almost 20-21 h/day in the wild. Consequently, their behavioral motivation for movement might be low. Effects of environment on their behavior might be slight, even when under a restricted condition, but some correlation exists between the frequencies of abnormal behavior and the home range size in the wild for each species (Clubb and Mason, 2003). Although lions may not be constantly active, a restricted condition might therefore be stressful, even when temporary, because their average home range size is 80-100 km2 in the wild. This study investigated the number of behavior repertoires, the time spent on maintenance behaviors, and the abnormal behavior of the lions to learn whether their behavioral motivations are affected by the restrictions of behavior opportunities under captive conditions. Materials and methods Animals and management Four Indian lions (Panthera leo persica) kept in Ueno Zoological Park were observed. Three of them (Mohan_, Shakti\, and Anita\) were 10 years old. One of them (Chandi\) was 16 years old. Chandi was born in Zoolasia Yokohama Zoological Gardens in 1996 and moved to Ueno Zoological Park in 2002. The same year, she gave birth to Mohan, Shakti, and Anita. Reproduction was controlled by estrus behavior observation of females. Mohan was not castrated during the experiment. Their exhibition area is enclosed by imitation rock walls, wire fences, and tempered glass (Figure 1). There are electrically wired fences on the top of the lions’ enclosure and trees in the exhibition area to prevent escape and to protect planted trees. The enclosure size is about 540 m2. The earthen floor slopes gently from the center to the south corner of the area. A pond is situated in the northeastern area, with imitation arched wood placed at the center of the enclosure. Imitation rocks or wood, as well as real rocks, are also placed there. Four sleep chambers are located at the rear of the exhibition area. One chamber (2.5 2.9 m2) is used by Mohan. Two rooms (2.5 4.9 m2/room) are used by the three females. A water pool is situated at the corner of the rest chamber and at a den under the steps in a rest chamber. In addition, a scratching log (1.5 m long) is in the female’s rest chamber. They are fed horse, rabbit, and chicken meat once a day after evening housing. In addition, they are fasted irregularly once a week. Behavior observation Two experimental days were set up for this observation. One is a “released day,” on which the lions were released to the exhibition area from 9:00 to 16:30 and were housed in the rest chamber at other times. Another is a “confined day,” during which they were in the rest chamber all day long. Observations were conducted 5 times on 2 successive days, a confined day and the subsequent released
Figure 1. Diagram of the study area. Dotted areas show the exhibition area. Striped areas are the lion’s rest chambers. “P” denotes a pond. “R” denotes the two imitation rocks in the enclosure. Black bars show imitation woods. Double lines around the enclosure show the viewpoint of this exhibition.
day, from the beginning of August to the end of November. The observation periods were also defined as “daytime” (9:00-16:00) and “nighttime” (16:30-9:00 of the next morning). We recorded the behaviors of the respective lions in the exhibition area for 15 min/h by naked eye observation during the daytime. The nighttime or confined day behavior in the rest chamber was recorded using a wide angle camera (SM-C56N; Wireless Tsukamoto Co. Ltd., Japan) or an infrared-night vision camera (SM-CSW24A; Wireless Tsukamoto Co. Ltd.) with a digital video recorder (DVR-4200P; MotherTool Co. Ltd., Japan). The behavior repertories in each 24 hours of observation days were counted using ad libitum sampling method (Martin and Bateson, 1993). Maintenance behaviors (resting, eating, eliminating, self-grooming, walking, others), social behaviors, reproductive behaviors, abnormal pacing behaviors, and other behaviors were observed for each lion using 1-minute instantaneous sampling method. Data collection was conducted by the same observer throughout the experiment. Statistical analysis Observed behaviors were classified by reference to feline behavior (Sato et al., 2011). The numbers of the daytime and nighttime behavior repertories in subject lions were summed and compared between the released and the confined days using a 2 2 contingency table (chi-square test for independence). Furthermore, each behavior category such as maintenance, social, reproductive, abnormal, and other behavior were compared between the released and the confined days by a 2 3 contingency table. (The repertories of reproductive, abnormal, and other behaviors were summed because their numbers were 5, which does not satisfy the condition of chi-square tests.) The percentage of maintenance
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Table Descriptions of the 53 specific behavior repertories of Indian lions (Panthera leo persica) observed for this study Behavior categories Maintenance behavior Feed Rest Eliminate Self-protect Self-groom Investigate Solitary play Locomote Social behavior Spacing Social investigate Agonistic Affiliative Social play Reproductive behavior Sexual Abnormal behavior Stereotypy Others
Descriptions
Specific behavior repertories
Behaviors of ingesting food and water Behaviors of staying motionless and relaxed various styles Behaviors of excreting feces or urine Behaviors of maintaining body temperature or homeostatic states Behaviors of cleaning body or relieving body itches or driving off bugs Behaviors of exploring environment information using sensory organs Behaviors of playing themselves Behaviors of moving from one to another place
Feeding, drinking Stand resting, sternum lying, lateral lying, dog sitting, lying with dorsal position (sleeping) Excretion, urination Panting, seeking shade, sunbathing, freezing Shivering, licking, biting, scratching, yawning, Tree clawing, rubbing, stretching Listening, watching Object play Walking, running, climbing
Behaviors of territoriality and keeping personal space Behaviors Behaviors Behaviors Behaviors
of of of of
exploring other lions aggressive interaction with other lions friendly interaction with other lions playing with other lions
Keeping individual distance, keeping social distance, vocalization, marking (rhythmic emission of urine), leading, following Listening, watching, sniffing Threatening, pawing, chasing, escaping, avoiding Touching, rubbing, licking Play chasing, rolling, mock fighting
Behaviors of sexual interaction with other lions
Vulva sniffing, flehmen
Behaviors of abnormal repetitive actions Other behaviors that do not fit above categories
Pacing Licking floor, scratching floor, pawing fence
behavior was compared using a 2 6 contingency table. The percentages of abnormal pacing done during walking were compared between the released and the confined days using a 2 2 contingency table, respectively, during the daytime and nighttime. Results In all, we observed 240 hours of these lions’ behavior and identified 53 behavior repertories (Table). On the released days, 51 repertories (daytime, 46; nighttime, 42) in all were observed, with 42 repertories (daytime, 42; nighttime, 41) observed on the confined days. However, the numbers of behavior repertories on the released and the confined days during the daytime and nighttime were not significantly different (c2 ¼ 0.084, df ¼ 1, NS, Figure 2). In addition, we compared these differences in each behavior category. Results show no difference between the released and confined days (c2 ¼ 0.429, df ¼ 2, NS, Figure 3).
Figure 2. The number of behavior repertories of the lions between the confined days and the released days. White bars represent the number of the daytime repertories. Black bars represent the number of the nighttime repertories observed.
Percentages of daytime behavior were significantly different between the released and confined days (c2 ¼ 19.17, df ¼ 6, P < 0.01, Figure 4). The resting behavior was 69.8% on confined days but 86.0% on released days. Walking was 22.3% on confined days but only 3.0% on released days. Similarly, percentages of nighttime behavior were significantly different between days (c2 ¼ 13.06, df ¼ 6, P < 0.05). Resting behavior was 75.5% on confined days but 93.1% on released days. Walking was 14.8% on confined days but only 3.3% on released days. Average transitions of these behaviors during 24hour observation were presented in Figure 5. All the lions rested nearly all day long except around evening housing time (16:0017:00) or in the morning (8:00-9:00) on the released days. However, on the confined days, they were usually restless. They spent about 60.7% of their time walking at 9:00. There was a steady decrease in percentage of time spent walking until evening housing. However, time spent walking increased again at 16:00 and continued until around 20:00. Furthermore, walking increased from 3:00 on the confined days. It reached 42.3% at 8:00, but it increased from 6:00 on the released days and became 21.1% at 8:00.
Figure 3. Differences of numbers of respective behavior repertories of the lions between the confined days and the released days. White bars represent the number of the daytime repertories. Striped bars represent the number of the nighttime repertories observed.
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Figure 5. Twenty-four-hour transition of resting and walking behaviors of lions between confined days and the released days. The upper line graph shows the behavior on confined days. The lower one shows the behavior on released days. Dotted lines with filled circles show percentages of walking. Normal lines with open circles show percentages of resting each hour.
Figure 4. Difference of the percentages of the maintenance behavior of the lions between the confined days and the released days. The upper bar graph shows daytime percentages. The lower bar graph shows nighttime percentages.
The respective percentages of abnormal pacing during walking on the released days and the confined days during daytime and nighttime were found to be significantly different (c2 ¼ 3.94, df ¼ 1, P < 0.05, Figure 6) and were lower by about one-fourth on confined compared to released days during the daytime (confined days, 81.3%; released days, 63.6%). In addition, these percentages were lower by about half on confined compared to released days during the nighttime (confined days, 84.5%; released days, 39.9%). Discussion We had expected that the number of the behavior repertories of the lions would be few because lions generally spend almost the entire day resting or sleeping under captive conditions, as they apparently also do in the wild (Schaller, 1972). Nevertheless, we recorded 53 behavior repertories during the observation periods, covering almost all normal feline behavior repertories under captive conditions (84 repertories; Sato et al., 2011). Some behaviors related to reproduction or aggression, which in felines are reported to be 17 and 13 repertoires, respectively (Sato et al., 2011), were infrequently observed because members of the observed group were all of a single consanguine family. However, some agonistic behaviors were only observed from male to female lions. Social play and spacing behavior among them was observed only during released days. These results were affected mainly by the difference in environmental conditions. On the other hand, no difference was observed in the number of behavior repertories shown on released and confined days. Barren and restrictive
environments such as that of the confined day condition, compared to the released condition, often lead to decreased behavior diversity and development of higher levels of stereotypy (Dantzer, 1986; Gunn and Morton, 1995); therefore, we had expected that the confined condition would affect the numbers of the behavior repertories of the lions. However, the numbers of behavior repertories were not significantly different in these 2 experimental conditions. Therefore, these conditions in this zoo might be sufficient for captive lions to express various behavior repertories. The difference of the experimental conditions did not affect the lions’ behavioral diversity. The condition of the behavior, such as the time spent resting and walking, differed significantly. The time spent walking on confined days was greater than that on released days. The time spent resting shows opposite results. When these percentages of resting are converted to a 24-hour scale, the resting time on released days became 22.3 hours and that on confined days became 18.1 hours. Although the results are slightly longer, as reported by Schaller (1972), the effect of about 4 hours decreased resting time might
Figure 6. Percentages of pacing behavior during walking time between confined days and released days. White bars show percentages of pacing on the released days. Black bars show the percentages of pacing on confined days.
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be extremely great for lions, which spend most of the day sleeping. In addition, the behavioral transition of walking and resting was influenced by the daytime locomotive situation. These results suggested that the restriction of the opportunity to get around the exhibition area or for social contact had disturbed the daytime and nighttime behaviors. That is to say, the limitations against moving around the exhibition area in this study might present some stress. No matter how they exercised in the rest chamber, the lions were unable to resolve their modest locomotive motivation, even though the expression of their behavior repertories was almost assured. Abnormal pacing, which accounted for almost the entire walking time, was higher than on released days. Reportedly, that stereotyped behavior in carnivores derives from various factors such as motivation involved in feeding (Carlstead, 1998; Rees, 2009), range restriction or restriction of normal activity (van Keulen-Kromhout, 1978; Clubb and Vickery, 2008), and motivations to approach conspecifics (Vickery and Mason, 2004; Clubb and Vickery, 2008). Locomotive stereotypies are also reduced when some animals are moved from a small enclosure to a large enclosure (Carlstead 1991; Langenhorst 1998). Compared to the exhibition area, the space in the rest chamber is too small for exercise. The enclosure was less stimulating. Although we thought that locomotive motivations of lions might be low, getting around the exhibition area and contacting one another during the released days appears to have important meaning for them, even though these times were few and short. On the other hand, how much space and what kind of stimuli an animal needs remain unclear. Ödberg (1987) reported that bank voles in a small enriched cage exhibited less stereotypic behavior than those kept in large and barren cage. Similarly, Wilson (1982) pointed out that objects within environments may be more important for captive apes than the size or construction of the enclosure. Consequently, it is necessary to clarify the reason that the pacing behavior was increased in lions and the difference in quality between the respective enclosures. In conclusion, our results suggest that the restrictions of behavior opportunity under the captive conditions strongly affect the resting and walking behavior and their activities during the daytime and nighttime. Staying in small and less stimulative rest chambers all day led to decreased resting time, increased walking time, and increased percentages of pacing during walking. These results might reflect that their motivation for activity was not satisfied in that condition. It might be important for lions, which do not always move around, to have the opportunities to ramble around the enclosure, whether they choose to exercise that opportunity. Zoo managers must consider the quality of animal behavior and the environment at the time of the behavior. In addition, the length of restrictive period must be considered. Longterm residence in barren and inadequate environments is well known to lead to accumulation of animals’ frustration and the development of specialized abnormal behavior and reduced behavioral diversity (Dantzer, 1986, Clubb and Vickery, 2008). In this study, our restrictive conditions such as the confined days were only 24 hours. However, in some cases such as medical treatment or perinatal care, animals might need to be restricted for a long time. Consequently, more research might be necessary to clarify the effects not only of the difference of the temporal behavioral opportunity but also of the restrictive period for lions. Acknowledgments The authors thank the Ueno Zoological Garden for providing animals for cooperation with this study and the staff at the Ueno Zoological Garden at that time for their enthusiastic assistance with the research. Daisuke Kohari was responsible for the research idea,
experimental design, and writing the article. Data collection, care of animals, and research schedule management were performed by Ayaka Sunada, Yukiko Matsui, Ayumi Ootaki, and Hidemasa Hori with data analysis by Daisuke Kohari. Ethical considerations We read the policy of the journal on ethical consent and standard animal care, and our work was carried out in accordance with these policies. Furthermore, we limited animal use in accordance with “Three Rs” indicated in Directive 2010/63/EU. Conflict of interest The authors declare no conflict of interest. References Carlstead, K., 1991. Husbandry of the Fennec fox: Fennecus zerda: environmental conditions influencing stereotypic behaviour. Int. Zoo Yearb. 30, 202e207. Carlstead, K., 1996. Effect of captivity on the behaviour of wild mammals. In: Kleiman, D.G., Allen, M.E., Thompson, K.V., Lumpkins, S. (Eds.), Wild Mammals in Captivity: Principles and Techniques. University of Chicago press, Chicago, pp. 317e333. Carlstead, K., 1998. Determining the causes of stereotypic behaviors in zoo carnivores: towards developing appropriate enrichment strategies. In: Shepherdson, D.J., Mellen, J., Hutchins, M. (Eds.), Second Nature Environmental Enrichment for Captive Animals. Smithsonian Institution Press, Washington, D.C., pp. 172e183. Clubb, R., Mason, G., 2003. Animal welfare: captivity effects on wide-ranging carnivores. Nature 425, 473e474. Clubb, R., Vickery, S., 2008. Locomotory stereotypies in carnivores: does pacing stem from hunting, ranging or frustrated escape? In: Mason, G., Rushen, J. (Eds.), Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare, Second edition. CAB International, Wallingford, pp. 58e85. Dantzer, R., 1986. Behavioral, physiological and functional aspects of stereotyped behavior: review and a re-interpretation. J. Anim. Sci. 62, 1776e1786. Gunn, D., Morton, D.B., 1995. Inventory of the behaviour of New Zealand white rabbits in laboratory cages. Appl. Anim. Behav. Sci. 45, 277e292. Haas, G., 1958. 24-Stunden-Periodik von Grosskatzen im Zoologischen garten. Saugetierk. Mitt. 6, 113e117. Hosey, G., Melfi, V., Pankhurst, S., 2009. Behavioural Response to the Zoo Environment: Zoo animals behaviour, management, and welfare, Second edition. Oxford University Press, Oxford, p. 93. Langenhorst, T., 1998. Behavior of a brown bear group (Ursus arctos) with behavioral enrichment at the Hellbrunn/Salzburg. Der Zoologische Garten 68, 167e186. Mallapur, A., Chellam, R., 2002. Environmental influences on stereotypy and the activity budget of Indian leopards (Panthera pardus) in four zoos in southern India. Zoo Biol. 21, 585e595. Martin, P., Bateson, P., 1993. Measuring Behavior an Introductory Guide. Cambridge University Press, Cambridge, pp. 84e100. Ödberg, F.O., 1987. The influence of cage size and environmental enrichment othe development of stereotypies in bank voles (Clethrionomys glareolus). Behav. Process. 14, 155e176. Rees, P.A., 2009. Activity budgets and the relationship between feeding and stereotypic behaviors in Asian elephants (Elephas maximus) in a zoo. Zoo Biol. 28, 79e97. Rees, P.A., 2011. Zoo and exhibit design. In: An Introduction to Zoo Biology and Management. Wiley Blackwell, Oxford, pp. 137e145. Rees, P.A., 2011. Zoo and exhibit design. In: An Introduction to Zoo Biology and Management. Wiley Blackwell, Oxford, pp. 189e199. Rushen, J., Mason, G., 2006. A decade-or-more’s progress in understanding stereotypic behaviour. In: Mason, G., Rushen, J. (Eds.), Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare, second edition. CAB International, Wallingford, pp. 1e18. Sato, S., Kondo, S., Tanaka, T., Kusunose, R., Mori, Y., Idani, G., 2011. Ethograms of Animals in Captivity. Asakurashoten, Tokyo, pp. 22e162. (Japanese). Schaller, G.B., 1972. The Serengeti Lion: A Study of Predator-prey Relations. University of Chicago press, Chicago, pp. 119e125. Swaisgood, R.R., Shepherdson, D.J., 2005. Scientific approaches to enrichment and stereotypies in zoo animals: what’s been done and where should we go next? Zoo Biol. 24, 499e518. van Keulen-Kromhout, G., 1978. Zoo enclosure for zoo bears Ursidae: their influence on captive behaviour and reproduction. Int. Zoo Yearb. 18, 177e186. Vickery, S., Mason, G., 2004. Stereotypic behavior in Asiatic black and Malayan sun bears. Zoo Biol. 23, 409e430. Wilson, S.F., 1982. Environmental influences on the activity of captive apes. Zoo Biol. 1, 201e209.