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Use of fluoxetine to treat stereotypical pacing behavior in a brown bear (Ursus arctos)
Journal of Veterinary Behavior (2007) 2, 73-76
CASE REPORT
Use of fluoxetine to treat stereotypical pacing behavior in a brown bear (Ursus arctos) Ebru Yalcin, DVM, PhD, Nilufer Aytug, Prof Dr Department of Internal Medicine, Faculty of Veterinary Medicine, Uludag University, Bursa, Turkey. KEYWORDS: bear; stereotypical pacing; fluoxetine
Abstract A 12-year-old, male, brown bear (Ursus arctos) named Abdi exhibited stereotypical pacing behavior. He was kept as a pet for 10 years by local villagers, then he was rescued and taken to the Karacabey Bear Sanctuary in July 2001. His physical condition was extremely poor. Because he had never lived with other bears, he was terrified and refused to integrate with them. After 6 months he was healthy physically but observations by the keepers indicated that he was pacing all day. He was treated with fluoxetine (0.62 mg/kg orally every 24 hours) for 6 months, and had been observed totally for 18 months. After stereotypy ceased completely, he was transferred to the large naturalistic enclosure and did not show any stereotypical behavior during the subsequent observation period (1 year). He was treated successfully using a combination of fluoxetine, the provisioning of extra space, and the addition of novel stimulation in a naturalistic enclosure. The space and stimulation could be sufficient to mimic the therapeutic effect of the pharmacological therapy in the long term. © 2007 Elsevier Inc. All rights reserved.
Introduction A stereotypy is an intentional repetitive behavior—a nonfunctional, non injurious, highly predictable sequencing of actions, often carried out in a specific and rhythmic manner (Beaver, 1992). ‘Stereotypies’ or ‘stereotypic behaviors’ have long been interchangeably defined as repetitive, unvarying and apparently functionless behavior patterns (Mason, 1991). Captive bears seem to be particularly susceptible to stereotypies. In a survey of stereotypies in 33 carnivore species, ursids displayed both the highest frequency and maximum prevalence compared to other families (e.g., canids and felids) (Clubb and Mason, 2001). As seems typical of bears, and indeed all carnivores (Clubb and Mason, 2001), locomotory stereotypies, such as pacing,
Address reprint requests and correspondence: Ebru Yalcin, PhD, Department of Clinical Science, Faculty of Veterinary Medicine, Uludag University, Mudanya Cd. No. 2, Bursa, Turkey. Tel.: ⫹90 224 234 76 55-233 52 84; Fax: 90 224 234 63 95. E-mail: [email protected]
1558-7878/$ -see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.jveb.2007.04.001
predominated (Meyer-Holzapfel, 1957; Langenhorst, 1998; Ames, 2000). Stereotypic pacing is the rhythmic walk to one side of an enclosure, the flip of the head while turning, and the walk to the other side before repeating the turn (Beaver, 1992). Ursids or felids engage in stereotypies (e.g., head weaving, head throw back, and pacing) during 60% to 80% of the day (Wechsler, 1991). Brown bears in the wild spend approximately 50% of their time on active behaviors (Roth, 1983) of which approximately 50% is spent on foraging activities (Atwell et al., 1980; Phillips, 1987). Many studies have attempted to alleviate bear stereotypies, usually by enrichment (Carlstead et al., 1991; Forthman et al., 1992; Fischbacher and Schmid, 1999; Swaisgood et al., 2001), but also with the use of homeopathic (JordanOwers, 2003), anti-depressant, (Poulsen et al., 1996, 1998), and anti-psychotic (Uchida and Dodman, 1998) drugs. The use of psychotropic medications has become increasingly more common in veterinary medicine and combined with behavior and environmental modification, the use of various types of anxiolytics and anti-depressants has made the treatment of various disorders increasingly more successful. Use
74 of haloperidol in a bear was partially effective but did not result in a sufficient change in the bear’s behavior, although melatonin has been shown to reduce isolation-induced distress vocalization and seemed to be useful in the treatment of separation anxiety in this bear (Beaver, 1998). Although fluoxetine is not approved for use in animals, veterinarians have been recommending its use in an off-label manner to treat a variety of behavioral problems in companion animals. Dogs with problem behaviors such as compulsive disorder, separation anxiety, aggression, and various phobic conditions have been helped through the conscientious use of fluoxetine (Beaver, 1992; Simpson and Simpson, 1996; Poulsen et al., 1996). Poulsen et al. (1996) treated stereotypical pacing behavior in a captive polar bear with fluoxetine.
Material studied A 12-year-old, male, brown bear (Ursus arctos), “Abdi,” had stereotypical pacing behavior. The bear was born in the wild in February 1992 and his mother was shot by hunters in the Kure Mountains. He was taken by local villagers to be kept as a pet. He was left unattended on the end of a short chain in the heat of the sun and in the cold, rain, and snow for 2 years. After 2 years on the end of the short chain, he lived for 8 more years isolated, in a tiny, concrete floor cage (2 m ⫻ 4 m). Villagers fed and watered the bear from a dark hole but never cleaned the cage. Abdi was rescued in July 2001 and taken to the Karacabey Bear Sanctuary. His physical condition was extremely poor. In the Karacabey Sanctuary, he was kept alone in a concrete indoor– outdoor exhibit separated with a fence from the large outdoor enclosure before he was released into the large enclosure with other bears. He preferred to be in the indoor enclosure for the most part. After 1 month he was mixed with 2 female (neutered) bears in an attempt to socialize him to his conspecifics, but Abdi was forced to remain alone because even the sight of other bears in nearby enclosures frightened him so much that he refused to come out of his den. Fearing for his physical and emotional health, Abdi was moved to a small indoor– outdoor enclosure where he could see but could not have direct physical contact with the other bears. After 6 months he gained weight and reached a normal bear’s condition but he still was afraid of other bears and did not socialize with them. Keepers noticed that whenever he was outside, he was pacing.
Housing His enclosure was 200 m2 outdoors and 16 m2 indoors. There was a concrete pool in the outdoor enclosure. It was separated by a fence and hot wire from the large bear enclosure (40,000 m2) where 28 brown bears were living.
Journal of Veterinary Behavior, Vol 2, No 3, May/June 2007 The enclosure had direct sunlight and shaded areas and it was cleaned daily by use of a hose.
Health status When rescued in 2001, Abdi’s physical condition was extremely poor. After immobilization with 5 mg/kg zolazepam–tiletamine (Zoletile), he was examined clinically and blood samples were taken. There was no abnormality except his dull coat and alopecia in various areas. Results of the CBC and serum biochemical tests were within normal limits and fecal examination was positive for nematodes. Abdi received ivermectin (200 g/kg of body weight, orally every 30 days) for treatment of ectoparasites considered responsible for chronic, intermittent, recurring alopecia and associated pruritus. His diet included fruits, vegetables, nuts, and meat that were offered 3 times daily. Although he did not eat all of his food in the first few days after rescue, he started to eat normally during the second week. By the end of 6 months of treatment the bear was considered healthy by means of visual examination; obvious clinical abnormalities were not identified.
Observations All observations were carried out by the same person, positioned at the upper deck. The observer noted the amount of continuous time spent engaged in a particular behavior (duration of bout) and the number of times a bout of behavior was observed (number of bouts) in each 2-hour session. Percentage of time spent in stereotyped behavior was evaluated and social interaction was assessed. He was observed for 1 day in 1 week, in 2 sessions, each observation time was 1 hour (10:00-11:00/14:00-15:00), and total observation time was 144 hours in 18 months. Although it was not ideal, observation day included videotaping for 1 hour because the bear sanctuary is far from the city center. Additionally, bear keepers made observations every day and noted any unusual changes. Equipment was placed on the upper deck, which allowed approximately 100% of the enclosure to be videotaped. A daily log was kept, and pertinent information was recorded.
Stereotypies Abdi spent most of his time pacing continuously in front of the door to the outdoor quarters. He used 20% of his outdoor enclosure. He never used the pool. He paced all the time other than when he was feeding or sleeping. When we consider the observation times, a typical day consisted of 35 pacing bouts, each of which lasted a mean of 40 minutes. Bouts ranged from less than 30 minutes to 2 hours. Pacing bouts were composed of a mean 90 cycles. Each pacing
Yalcin and Aytug
Use of fluoxetine to treat stereotypical pacing behavior in a brown bear
cycle, up and back along the length of a wall once, took 20 seconds to complete. Grouping subjects of the same species is generally considered as a way to decrease boredom, even if the species is essentially solitary in nature. We took some calm bears to Abdi’s enclosure gradually. When other bears were taken to the same enclosure for socialization he was pacing as if they were not around. He never tried to catch food during feeding times, so we decided to leave him alone until the amount of stereotyped behavior decreased, which took 6 months.
Fluoxetine administration Based on the experience of Poulsen et al. (1996), 0.62 mg/kg fluoxetine was given every morning as 20-mg capsules (Depreks, Eczacibasi, Turkey) hidden in his favorite food (bread with raisins and nuts). Observations by the keepers indicated that the bear consumed the bread that contained the drug. Five observation periods were included: pretreatment phase (30 days before starting treatment), first treatment phase (0-30 days), second treatment phase (30120 days), third treatment phase (120-180 days), and posttreatment phase (180-550 days).
Results During the pretreatment phase, Abdi paced 80% of the observation time. He paced for 35 pacing bouts, bouts ranging from 20-25 minutes. Pacing bouts were composed of a mean 90 cycles. Each pacing cycle, up and back along the length of a wall once, took 20 seconds to complete. Similarly, during the first phase 0-30 days, the number of paces and the time he spent occupied with pacing were the same, between Days 30-120, a decrease in the number of pacing bouts was observed 25 pacing bouts, and bouts ranged from 10-15 minutes. Pacing bouts were composed of a mean 70 cycles and he occupied 60% of the total observation time pacing. Each pacing cycle, up and back along the length of a wall once, took 10 seconds to complete. On the third phase (Days 120-180), pacing became progressively shorter, 5 pacing bouts, with bouts lasting approximately 5 minutes with him occupied with pacing 10% of the total observation time. Pacing bouts were composed of a mean 10 cycles. Each pacing cycle, up and back along the length of a wall once, took 10 seconds to complete. He was not pacing during the observation time on Week 23, so we evaluated the situation as “stereotypy is ceased.” We continued to administer medication for 2 more weeks, then the fluoxetine was ceased and he was released to the large enclosure. During an observation period lasting 1 year, he did not show any stereotyped behavior and after a few days in the large enclosure, he had good relationships with the other bears.
75
Discussion Stereotypies often arise when a captive animal has prolonged exposure to an ecologically relevant problem that it is incapable of solving within its enclosure (Shepherdson, 1989). Well-developed stereotypies are often termed ‘established’ (Ödberg, 1978; Mason, 1991), a term that represents one extreme of a range of developmental stages. Although there seems to be no generally accepted means of distinguishing ‘established’ from ‘developing’ stereotypies, the former are generally classified on the basis that they occupy more time (Cronin and Wiepkema, 1984; Mason, 1993). Stereotypies typically become more frequent (i.e., occupy an increasing proportion of time) as they develop (Cronin and Wiepkema, 1984; Mason, 1993; Cooper et al., 1996). During their development stereotypies are thought to become more ‘internally controlled’ and therefore increasingly difficult to interrupt with external stimuli because the animal pays less attention to its environment (Fentress, 1976; Fentress, 1977). In support of this, animals with well-established stereotypies have sometimes been reported to be ‘not mentally alert’ or ‘trance-like’ while stereotyping (Cronin and Wiepkema, 1984; Ormrod, 1992; Moon-Fanelli and Dodman, 1998). Among 29 Asiatic black bears and sun bears, an individual’s age (ranging between 1.5-11 years) was correlated significantly with its stereotypy frequency, with older bears spending more time stereotyping (Vickery and Mason, 2003). When we consider Abdi’s history that can be effective on the development of his stereotypy, his insensitivity to his environment, his age, and the time he occupied with pacing (80% of the observation time), his stereotypy was evaluated as “established.” Established stereotypies are more difficult to interrupt with external stimuli (Cronin and Wiepkema, 1984; Sambraus, 1985). We decided to treat him medically. The use of psychotropic medications has become increasingly more common in veterinary medicine and combined with behavior and environmental modification, the use of various types of anxiolytics and anti-depressants has made the treatment of various disorders increasingly more successful (Simpson and Simpson, 1996). The selective 5-HT reuptake inhibitor (SSRI) fluoxetine exerts a rate-dependent effect on stereotypies by increasing stereotypies in low-stereotyping voles and decreasing stereotypies in high-stereotypers (Ödberg and Mers, 1998). In the bear described here, the cessation of the stereotypical behavior was maintained after the medical therapy (fluoxetine hydrochloride administration 0.62 mg/kg orally every 24 hours) was discontinued. He was released to a naturalistic large bear enclosure and he was observed for 1 year. He did not pace when in the concrete enclosure or in the large enclosure, he was active, and had contact with other bears. The results of the present study suggest that pharmacotherapy reduced stereotypical behavior in this case and the bear remained active and social in the naturalistic environment of the large bear enclosure. These results are similar to the results seen by Poulsen et al. (1996) in their study of
76 polar bears treated with fluoxetine for stereotypic behavior. This indicates that pharmacologic manipulation of the serotonergic system can eliminate stereotypical behaviors safely (Poulsen et al., 1996). Additionally, providing extra space and novel stimulation after ceasing medical therapy, could be sufficient to mimic the therapeutic effect of the pharmacological therapy in the long term.
Conclusion In conclusion it was observed that behavioral pharmacotherapy can be very effective in eliminating persistent stereotypical behaviors in bears and a naturalistic exhibit design has a very important role together with pharmacotherapy to maintain non stereotypical locomotor behavior.
Acknowledgments We are grateful to ProAnimale Germany for financial support for the fluoxetine hydrochloride.
References Ames, A., 2000. The management and behaviour of captive polar bears. Ph.D. dissertation, Open University, UK. Atwell, G.C., Boone, D.L., Gustafson, J., Berns, V.D., 1980. Brown bear summer use of alpine habitat on the Kodiak National Wildlife Refuge. International Conference on Bear Research and Management 4, 297305. Beaver, B., 1992. Canine Behavior: A Guide for Veterinarians (1st ed.). W.B. Saunders Co., Philadelphia, PA. pp. 80-83. Beaver, B., 1998. Vet med today: Animal behavior case of the month. J. Am. Vet. Med. Assoc. 212, 354-355. Carlstead, K., Seidensticker, J., Baldwin, R., 1991. Environmental enrichment for zoo bears. Zoo. Biol. 10, 3-16. Clubb, R., Mason, G., 2001. Captivity effects on wide-ranging carnivores. Nature 425, 473-474. Cooper, J.J., Ödberg, F.O., Nicol, C.J., 1996. Limitations on the effectiveness of environmental improvement in reducing stereotypic behavior in bank voles (Clethrionomys glareolus). Appl. Anim. Behav. Sci. 48, 237-248. Cronin, G.M., Wiepkema, P.R., 1984. An analysis of stereotyped behavior in tethered sows. Ann. Rech. Vet. 15, 263-270. Fentress, J.C., 1976. Dynamic boundaries of a patterned behaviour: Interaction and self-organisation. In: Bateson, P.P.G., Hinde. R.A. (Eds.). Perspectives in Ethology 1. Cambridge University Press, Cambridge, UK. pp. 135-169. Fentress, J.C., 1977. The tonic hypothesis and the patterning of behavior. Ann. N. Y. Acad. Sci. 290, 370-395. Fischbacher, M., Schmid, H., 1999. Feeding enrichment and stereotypic behavior in spectacled bears. Zoo. Biol. 18, 363-371.
Journal of Veterinary Behavior, Vol 2, No 3, May/June 2007 Forthman, D.L., Elder, S.D., Bakeman, R., Kurkowski, T.W., Noble, C.C., Winslow S.W., 1992. Effects of feeding enrichment on behavior of three species of captive bears. Zoo. Biol. 11, 187-195. Jordan-Owers, L., 2003. Homeopathy for stereotypic behaviour in bears [abstract]. In: Proceedings of the British Veterinary Zoological Society (BVZS), Dublin, Ireland. Langenhorst, T., 1998. Effects of a behavioral enrichment program on the stereotypic behavior of brown bears (Ursus arctos) [in German]. Zool. Garten N. F. 68, 341-354. Mason, G.J., 1991. Stereotypies: A critical review. Anim. Behav. 41, 1015-1037. Mason, G.J., 1993. Forms of stereotypic behaviour. In: Lawrence, A.B., Rushen, J. (Eds.), Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare. CAB International, Wallingford, UK. pp. 7-40. Meyer-Holzapfel, M., 1957. Das Verhalten der Baren (Ursidae) [in German]. Handb. Zool. Berl. 8, 1-28. Moon-Fanelli, A.A., Dodman, N.H., 1998. Description and development of compulsive tail chasing in terriers and response to clomipramine treatment. J. Am. Vet. Med. Assoc. 212, 1252-1257. Ormrod, S.A., 1992. A review of captive polar bears in Great Britain and Ireland. Unpublished report commissioned by the Born Free Foundation, Horsham, West Sussex, UK. Ödberg, F.O., 1978. Abnormal behaviours (stereotypies). In: Grasi, J. (Ed), Proceedings of the First World Congress on Ethology Applied to Zootechnics. Industrias Graficas, Madrid, Spain. pp. 475-480. Ödberg, F.O., Mers, L., 1998. Rate-dependent effect of fluoxetine on captivity-induced stereotypies in bank voles. In: Proceedings of the 32nd Congress of ISEA. pp. 179. Phillips, M.K., 1987. Behavior and habitat use of grizzly bears in northeastern Alaska. In: Zager, P. (Ed), Bears–their biology and management. Seventh International Conference on Bear Research and Management. Williamsburg, VA, pp. 199-202. Poulsen, E.M.B., Honeyman, V., Valentine, P.A., Teskey, G.C., 1996. Use of fluoxetine for the treatment of stereotypical pacing behavior in a captive polar bear. J. Am. Vet. Med. Assoc. 209, 1470-1474. Poulsen, E.M.B., Hutchinson, J., Honeyman, V., Cooper, R., Teskey, G.C., 1998. Using enrichment as a diagnostic tool in one captive polar bear. In: Proceedings of the 3rd International Conference on Environmental Enrichment, Orlando. pp. 251-257. Roth, H.U., 1983. Diel activity of a remnant population of European brown bears. In: Meslow, E.C. (Ed), Bears–their biology and management. International Conference on Bear Research and Management 5, pp. 223-229. Sambraus, H.H., 1985. Stereotypies. In: Fraser, A.F. (Ed.), Ethology of Farm Animals. Elsevier, Amsterdam. pp. 431-441. Simpson, B.S., Simpson, D.M., 1996. Behavioral pharmacotherapy. In: Voith, V.L., Borchelt, P.L. (Eds), Readings Companion Animal Behavior. Veterinary Learning Systems. pp. 100-115. Shepherdson, D., 1989. Stereotypic behavior: what is it and how can it be eliminated or prevented? Ratel. 16, 100-105. Swaisgood, R.R., White A.M., Zhou, X., Zhang, H., Zhang, G., Wei, R., Hare, V.J., Teper, E.M., Lindburg, D.G., 2001. A quantitative assessment of the efficacy of an environmental enrichment programme for giant pandas. Anim. Behav. 61, 447-457. Uchida, Y., Dodman, N.H., 1998. Animal behavior case of the month. J. Am. Vet. Med. Assoc. 212, 354-355. Vickery, S., Mason, G., 2003. Behavioural persistence in captive bears: Implications for reintroduction. Ursus 14, 35-43. Wechsler, B., 1991. Stereotypies in polar bears. Zoo. Biol. 10, 177-188.
CASE REPORT
Use of fluoxetine to treat stereotypical pacing behavior in a brown bear (Ursus arctos) Ebru Yalcin, DVM, PhD, Nilufer Aytug, Prof Dr Department of Internal Medicine, Faculty of Veterinary Medicine, Uludag University, Bursa, Turkey. KEYWORDS: bear; stereotypical pacing; fluoxetine
Abstract A 12-year-old, male, brown bear (Ursus arctos) named Abdi exhibited stereotypical pacing behavior. He was kept as a pet for 10 years by local villagers, then he was rescued and taken to the Karacabey Bear Sanctuary in July 2001. His physical condition was extremely poor. Because he had never lived with other bears, he was terrified and refused to integrate with them. After 6 months he was healthy physically but observations by the keepers indicated that he was pacing all day. He was treated with fluoxetine (0.62 mg/kg orally every 24 hours) for 6 months, and had been observed totally for 18 months. After stereotypy ceased completely, he was transferred to the large naturalistic enclosure and did not show any stereotypical behavior during the subsequent observation period (1 year). He was treated successfully using a combination of fluoxetine, the provisioning of extra space, and the addition of novel stimulation in a naturalistic enclosure. The space and stimulation could be sufficient to mimic the therapeutic effect of the pharmacological therapy in the long term. © 2007 Elsevier Inc. All rights reserved.
Introduction A stereotypy is an intentional repetitive behavior—a nonfunctional, non injurious, highly predictable sequencing of actions, often carried out in a specific and rhythmic manner (Beaver, 1992). ‘Stereotypies’ or ‘stereotypic behaviors’ have long been interchangeably defined as repetitive, unvarying and apparently functionless behavior patterns (Mason, 1991). Captive bears seem to be particularly susceptible to stereotypies. In a survey of stereotypies in 33 carnivore species, ursids displayed both the highest frequency and maximum prevalence compared to other families (e.g., canids and felids) (Clubb and Mason, 2001). As seems typical of bears, and indeed all carnivores (Clubb and Mason, 2001), locomotory stereotypies, such as pacing,
Address reprint requests and correspondence: Ebru Yalcin, PhD, Department of Clinical Science, Faculty of Veterinary Medicine, Uludag University, Mudanya Cd. No. 2, Bursa, Turkey. Tel.: ⫹90 224 234 76 55-233 52 84; Fax: 90 224 234 63 95. E-mail: [email protected]
1558-7878/$ -see front matter © 2007 Elsevier Inc. All rights reserved. doi:10.1016/j.jveb.2007.04.001
predominated (Meyer-Holzapfel, 1957; Langenhorst, 1998; Ames, 2000). Stereotypic pacing is the rhythmic walk to one side of an enclosure, the flip of the head while turning, and the walk to the other side before repeating the turn (Beaver, 1992). Ursids or felids engage in stereotypies (e.g., head weaving, head throw back, and pacing) during 60% to 80% of the day (Wechsler, 1991). Brown bears in the wild spend approximately 50% of their time on active behaviors (Roth, 1983) of which approximately 50% is spent on foraging activities (Atwell et al., 1980; Phillips, 1987). Many studies have attempted to alleviate bear stereotypies, usually by enrichment (Carlstead et al., 1991; Forthman et al., 1992; Fischbacher and Schmid, 1999; Swaisgood et al., 2001), but also with the use of homeopathic (JordanOwers, 2003), anti-depressant, (Poulsen et al., 1996, 1998), and anti-psychotic (Uchida and Dodman, 1998) drugs. The use of psychotropic medications has become increasingly more common in veterinary medicine and combined with behavior and environmental modification, the use of various types of anxiolytics and anti-depressants has made the treatment of various disorders increasingly more successful. Use
74 of haloperidol in a bear was partially effective but did not result in a sufficient change in the bear’s behavior, although melatonin has been shown to reduce isolation-induced distress vocalization and seemed to be useful in the treatment of separation anxiety in this bear (Beaver, 1998). Although fluoxetine is not approved for use in animals, veterinarians have been recommending its use in an off-label manner to treat a variety of behavioral problems in companion animals. Dogs with problem behaviors such as compulsive disorder, separation anxiety, aggression, and various phobic conditions have been helped through the conscientious use of fluoxetine (Beaver, 1992; Simpson and Simpson, 1996; Poulsen et al., 1996). Poulsen et al. (1996) treated stereotypical pacing behavior in a captive polar bear with fluoxetine.
Material studied A 12-year-old, male, brown bear (Ursus arctos), “Abdi,” had stereotypical pacing behavior. The bear was born in the wild in February 1992 and his mother was shot by hunters in the Kure Mountains. He was taken by local villagers to be kept as a pet. He was left unattended on the end of a short chain in the heat of the sun and in the cold, rain, and snow for 2 years. After 2 years on the end of the short chain, he lived for 8 more years isolated, in a tiny, concrete floor cage (2 m ⫻ 4 m). Villagers fed and watered the bear from a dark hole but never cleaned the cage. Abdi was rescued in July 2001 and taken to the Karacabey Bear Sanctuary. His physical condition was extremely poor. In the Karacabey Sanctuary, he was kept alone in a concrete indoor– outdoor exhibit separated with a fence from the large outdoor enclosure before he was released into the large enclosure with other bears. He preferred to be in the indoor enclosure for the most part. After 1 month he was mixed with 2 female (neutered) bears in an attempt to socialize him to his conspecifics, but Abdi was forced to remain alone because even the sight of other bears in nearby enclosures frightened him so much that he refused to come out of his den. Fearing for his physical and emotional health, Abdi was moved to a small indoor– outdoor enclosure where he could see but could not have direct physical contact with the other bears. After 6 months he gained weight and reached a normal bear’s condition but he still was afraid of other bears and did not socialize with them. Keepers noticed that whenever he was outside, he was pacing.
Housing His enclosure was 200 m2 outdoors and 16 m2 indoors. There was a concrete pool in the outdoor enclosure. It was separated by a fence and hot wire from the large bear enclosure (40,000 m2) where 28 brown bears were living.
Journal of Veterinary Behavior, Vol 2, No 3, May/June 2007 The enclosure had direct sunlight and shaded areas and it was cleaned daily by use of a hose.
Health status When rescued in 2001, Abdi’s physical condition was extremely poor. After immobilization with 5 mg/kg zolazepam–tiletamine (Zoletile), he was examined clinically and blood samples were taken. There was no abnormality except his dull coat and alopecia in various areas. Results of the CBC and serum biochemical tests were within normal limits and fecal examination was positive for nematodes. Abdi received ivermectin (200 g/kg of body weight, orally every 30 days) for treatment of ectoparasites considered responsible for chronic, intermittent, recurring alopecia and associated pruritus. His diet included fruits, vegetables, nuts, and meat that were offered 3 times daily. Although he did not eat all of his food in the first few days after rescue, he started to eat normally during the second week. By the end of 6 months of treatment the bear was considered healthy by means of visual examination; obvious clinical abnormalities were not identified.
Observations All observations were carried out by the same person, positioned at the upper deck. The observer noted the amount of continuous time spent engaged in a particular behavior (duration of bout) and the number of times a bout of behavior was observed (number of bouts) in each 2-hour session. Percentage of time spent in stereotyped behavior was evaluated and social interaction was assessed. He was observed for 1 day in 1 week, in 2 sessions, each observation time was 1 hour (10:00-11:00/14:00-15:00), and total observation time was 144 hours in 18 months. Although it was not ideal, observation day included videotaping for 1 hour because the bear sanctuary is far from the city center. Additionally, bear keepers made observations every day and noted any unusual changes. Equipment was placed on the upper deck, which allowed approximately 100% of the enclosure to be videotaped. A daily log was kept, and pertinent information was recorded.
Stereotypies Abdi spent most of his time pacing continuously in front of the door to the outdoor quarters. He used 20% of his outdoor enclosure. He never used the pool. He paced all the time other than when he was feeding or sleeping. When we consider the observation times, a typical day consisted of 35 pacing bouts, each of which lasted a mean of 40 minutes. Bouts ranged from less than 30 minutes to 2 hours. Pacing bouts were composed of a mean 90 cycles. Each pacing
Yalcin and Aytug
Use of fluoxetine to treat stereotypical pacing behavior in a brown bear
cycle, up and back along the length of a wall once, took 20 seconds to complete. Grouping subjects of the same species is generally considered as a way to decrease boredom, even if the species is essentially solitary in nature. We took some calm bears to Abdi’s enclosure gradually. When other bears were taken to the same enclosure for socialization he was pacing as if they were not around. He never tried to catch food during feeding times, so we decided to leave him alone until the amount of stereotyped behavior decreased, which took 6 months.
Fluoxetine administration Based on the experience of Poulsen et al. (1996), 0.62 mg/kg fluoxetine was given every morning as 20-mg capsules (Depreks, Eczacibasi, Turkey) hidden in his favorite food (bread with raisins and nuts). Observations by the keepers indicated that the bear consumed the bread that contained the drug. Five observation periods were included: pretreatment phase (30 days before starting treatment), first treatment phase (0-30 days), second treatment phase (30120 days), third treatment phase (120-180 days), and posttreatment phase (180-550 days).
Results During the pretreatment phase, Abdi paced 80% of the observation time. He paced for 35 pacing bouts, bouts ranging from 20-25 minutes. Pacing bouts were composed of a mean 90 cycles. Each pacing cycle, up and back along the length of a wall once, took 20 seconds to complete. Similarly, during the first phase 0-30 days, the number of paces and the time he spent occupied with pacing were the same, between Days 30-120, a decrease in the number of pacing bouts was observed 25 pacing bouts, and bouts ranged from 10-15 minutes. Pacing bouts were composed of a mean 70 cycles and he occupied 60% of the total observation time pacing. Each pacing cycle, up and back along the length of a wall once, took 10 seconds to complete. On the third phase (Days 120-180), pacing became progressively shorter, 5 pacing bouts, with bouts lasting approximately 5 minutes with him occupied with pacing 10% of the total observation time. Pacing bouts were composed of a mean 10 cycles. Each pacing cycle, up and back along the length of a wall once, took 10 seconds to complete. He was not pacing during the observation time on Week 23, so we evaluated the situation as “stereotypy is ceased.” We continued to administer medication for 2 more weeks, then the fluoxetine was ceased and he was released to the large enclosure. During an observation period lasting 1 year, he did not show any stereotyped behavior and after a few days in the large enclosure, he had good relationships with the other bears.
75
Discussion Stereotypies often arise when a captive animal has prolonged exposure to an ecologically relevant problem that it is incapable of solving within its enclosure (Shepherdson, 1989). Well-developed stereotypies are often termed ‘established’ (Ödberg, 1978; Mason, 1991), a term that represents one extreme of a range of developmental stages. Although there seems to be no generally accepted means of distinguishing ‘established’ from ‘developing’ stereotypies, the former are generally classified on the basis that they occupy more time (Cronin and Wiepkema, 1984; Mason, 1993). Stereotypies typically become more frequent (i.e., occupy an increasing proportion of time) as they develop (Cronin and Wiepkema, 1984; Mason, 1993; Cooper et al., 1996). During their development stereotypies are thought to become more ‘internally controlled’ and therefore increasingly difficult to interrupt with external stimuli because the animal pays less attention to its environment (Fentress, 1976; Fentress, 1977). In support of this, animals with well-established stereotypies have sometimes been reported to be ‘not mentally alert’ or ‘trance-like’ while stereotyping (Cronin and Wiepkema, 1984; Ormrod, 1992; Moon-Fanelli and Dodman, 1998). Among 29 Asiatic black bears and sun bears, an individual’s age (ranging between 1.5-11 years) was correlated significantly with its stereotypy frequency, with older bears spending more time stereotyping (Vickery and Mason, 2003). When we consider Abdi’s history that can be effective on the development of his stereotypy, his insensitivity to his environment, his age, and the time he occupied with pacing (80% of the observation time), his stereotypy was evaluated as “established.” Established stereotypies are more difficult to interrupt with external stimuli (Cronin and Wiepkema, 1984; Sambraus, 1985). We decided to treat him medically. The use of psychotropic medications has become increasingly more common in veterinary medicine and combined with behavior and environmental modification, the use of various types of anxiolytics and anti-depressants has made the treatment of various disorders increasingly more successful (Simpson and Simpson, 1996). The selective 5-HT reuptake inhibitor (SSRI) fluoxetine exerts a rate-dependent effect on stereotypies by increasing stereotypies in low-stereotyping voles and decreasing stereotypies in high-stereotypers (Ödberg and Mers, 1998). In the bear described here, the cessation of the stereotypical behavior was maintained after the medical therapy (fluoxetine hydrochloride administration 0.62 mg/kg orally every 24 hours) was discontinued. He was released to a naturalistic large bear enclosure and he was observed for 1 year. He did not pace when in the concrete enclosure or in the large enclosure, he was active, and had contact with other bears. The results of the present study suggest that pharmacotherapy reduced stereotypical behavior in this case and the bear remained active and social in the naturalistic environment of the large bear enclosure. These results are similar to the results seen by Poulsen et al. (1996) in their study of
76 polar bears treated with fluoxetine for stereotypic behavior. This indicates that pharmacologic manipulation of the serotonergic system can eliminate stereotypical behaviors safely (Poulsen et al., 1996). Additionally, providing extra space and novel stimulation after ceasing medical therapy, could be sufficient to mimic the therapeutic effect of the pharmacological therapy in the long term.
Conclusion In conclusion it was observed that behavioral pharmacotherapy can be very effective in eliminating persistent stereotypical behaviors in bears and a naturalistic exhibit design has a very important role together with pharmacotherapy to maintain non stereotypical locomotor behavior.
Acknowledgments We are grateful to ProAnimale Germany for financial support for the fluoxetine hydrochloride.
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