Addressing nonhuman primate behavioral problems through the application of operant conditioning: Is the human treatment approach a useful model?

Applied Animal Behaviour Science

Volumn 102, Issue 3-4, 2007, Pages 205-222

  Bloomsmith, Mollie A ^a,b   Marr, M Jackson ^b   Maple, Terry L ^b  

^a EMORY UNIVERSITY   (United States)

^b GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Abnormal behavior; Behavioral pathology; Experimental analysis of behavior; Operant conditioning; Self injurious behavior; Training

Indexed keywords

ANIMAL WELFARE; BEHAVIORAL ECOLOGY; CAPTIVE POPULATION; COMPARATIVE STUDY; CONDITIONING; PRIMATE; STEREOTYPIC BEHAVIOR;

ANIMALIA; PRIMATES;

EID: 33845670823     PISSN: 01681591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.applanim.2006.05.028     Document Type: Article

References (113)

1. Aarons L. Shaping monkey-human contact. Percept. Motor Skills 36 (1973) 235-243
2. Ahern A.H., Clark K.M., and Gardenier N.C. Persistence of stereotypic behavior: examining the effects of external reinforcers. J. Appl. Behav. Anal. 36 (2003) 439-448
3. Anderson J.R., and Chamove A.S. Self-aggression and social aggression in laboratory-reared macaques. J. Abnorm. Psychol. 89 (1980) 539-550
4. Anderson J.R., and Chamove A.S. Self-aggressive behaviour in monkeys. Curr. Psychol. Rev. 1 (1981) 139-158
5. Ayllon T., and Michael J. The psychiatric nurse as a behavioral engineer. J. Exp. Anal. Behav. 2 (1959) 323-334
6. Baker K.C. Straw and forage material ameliorate abnormal behaviors in adult chimpanzees. Zoo Biol. 16 (1997) 225-236
7. Baker K., Bloomsmith M., Griffis C., and Gierhart M. Self-injurious behavior and response to human interaction as enrichment in rhesus macaques. Am. J. Primatol. 60 (2003) 94-95 (abstract)
8. Bassett L., and Buchanan-Smith H.M. Effects of predictability on the welfare of captive animals. Appl. Anim. Behav. Sci. 102 (2007) 223-245
9. Bayne K., Haines M., Dexter S., Woodman D., and Evans C. Nonhuman primate wounding prevalence: a retrospective analysis. Lab Anim. 24 (1995) 40-44
10. Bellanca R.U., and Crockett C.M. Factors predicting increased incidence of abnormal behavior in male pigtailed macaques. Am. J. Primatol. 58 (2002) 57-69
11. Berkson G. Development of abnormal stereotyped behaviors. Dev. Psychobiol. 18 (1968) 118-132
12. Bloomsmith M.A., Alford P.L., and Maple T.L. Successful feeding enrichment for captive chimpanzees. Am. J. Primatol. 16 (1988) 155-164
13. Bloomsmith M., Baker K., Griffis C., Maloney M., Neu K., and Schoof V. Comparing training to human interaction as enrichment for captive rhesus monkeys. Am. J. Primatol. 66 Suppl. 1 (2005) 178-179 (abstract)
14. Bloomsmith M., Baker K., and Novak M. Understanding and managing self-injurious behavior in nonhuman primates. Am. J. Primatol. 2 (2004) 119 (abstract)
15. Bloomsmith, M.A., Baker, K.C., Ross, S.R., Lambeth, S.P., 2006. Early rearing conditions and captive chimpanzee behavior: some surprising findings. In: Sackett, G., Ruppenthal, G. (Eds.), Nursery Rearing of Nonhuman Primates in the 21st Century. Kluwer Academic Publishers, New York, NY, pp. 289-312.
16. Bloomsmith M.A., and Lambeth S.P. Effects of predictable versus unpredictable feeding schedules on chimpanzee behavior. Appl. Anim. Behav. Sci. 44 (1995) 65
17. Bloomsmith M.A., Lambeth S.P., Stone A.M., and Laule G.E. Comparing two types of human interaction as enrichment for chimpanzees. Am. J. Primatol. 42 (1997) 96 (abstract)
18. Bourgeois S.R., and Brent L. Modifying the behaviour of singly caged baboons: evaluating the effectiveness of four enrichment techniques. Anim. Welfare 14 (2005) 71-81
19. Bourgeois S.R., Vazquez M., and Brasky K.M. Combination therapy reduces self-injurious behavior in a chimpanzee (Pan troglodytes): a case report. Am. J. Primatol. 66 (2005) 145 (abstract)
20. Breland K., and Breland M. The misbehavior of organisms. Am. Psychol. 16 (1961) 681-684
21. Broom D. Animal welfare: concepts and measurement. J. Anim. Sci. 15 (1991) 186
22. Capitanio J.P. Behavioral pathology. In: Mitchell G., and Erwin J. (Eds). Comparative Primate Biology, vol. 2, Part A: Behavior, Conservation, and Ecology (1986), Alan R. Liss, New York 411-454
23. Carlstead K. Determining the causes of stereotypic behaviors in zoo carnivores: toward appropriate enrichment strategies. In: Sheperdson D.J., Mellen J.D., and Hutchins M. (Eds). Second Nature: Environmental Enrichment for Captive Animals (1998), Smithsonian Institution Press, Washington, DC 172-183
24. Catania A.C., and Sagvolden T. Preference for free choice over forced choice in pigeons. J. Exp. Anal. Behav. 34 (1980) 77-86
25. Clarke A.S., Juno C.J., and Maple T.L. Behavioral effects of a change in the physical environment; a pilot study of captive chimpanzees. Zoo Biol. 1 (1982) 371-380
26. Cox C. Increase in the frequency of social interactions and the likelihood of reproduction among drills. Proceedings of the American Association of Zoological Parks and Aquariums Annual Conference. Portland, OR (1987)
27. Crockett C.M. Psychological well-being of captive nonhuman primates: lessons from laboratory studies. In: Sheperdson D.J., Mellen J.D., and Hutchins M. (Eds). Second Nature: Environmental Enrichment for Captive Animals (1998), Smithsonian Institution Press, Washington, DC 129-152
28. Crockett C.M., Shimoii M., and Bowden D.M. Behavior, appetite, and urinary cortisol responses by adult female pigtailed macaques to cage size, cage level, room change, and ketamine sedation. Am. J. Primatol. 52 (2000) 63-80
29. Cross H.A., and Harlow H.F. Prolonged and progressive effects of partial isolation on the behavior of macaque monkeys. J. Exp. Res. Person. 1 (1965) 39-49
30. Davenport Jr. R.K., and Menzel Jr. E.W. Stereotyped behavior of the infant chimpanzee. Arch. Gen. Psychiatr. 8 (1963) 99-104
31. DeLeon I.G., and Iwata B.A. Evaluation of a multiple-stimulus presentation format for assessing reinforcer preferences. J. Appl. Behav. Anal. 29 (1996) 519-532
32. Desmond T., Laule G., and McNary J. Training to enhance socialization and reproduction in drills. AAZPA (AM Assoc Zool Parks Aquariums) Annual Conference Proceedings (1987) 435-441
33. Dienske H., and Griffin R. Abnormal behaviour patterns developing in chimpanzee infants during nursery care: a note. J. Child Psychol. Psychiatr. Allied Disciplines 19 (1978) 387-391
34. Draper W.A., and Bernstein I.S. Stereotyped behavior and cage size. Percept. Motor Skills 16 (1963) 231-234
35. Eaton G.G., Worlein J.M., Kelley S.T., Vijayaraghavan S., Hess D.L., Axthelm M.K., and Bethea C.L. Self-injurious behavior is decreased by cyproterone acetate in adult male rhesus (Macaca mulatta). Horm. Behav. 35 (1999) 195-203
36. Erwin J., and Deni R. Strangers in a strange land: abnormal behaviors or abnormal environments?. In: Erwin J., Maple T.L., and Mitchell G. (Eds). Captivity and Behavior: Primates in Breeding Colonies, Laboratories, and Zoos (1979), Van Nostrand Reinhold Co., New York 1-28
37. Falcomata T.S., Roane H.S., Hovanetz A.N., Kettering T.L., and Keeney K.M. An evaluation of response cost in the treatment of inappropriate vocalizations maintained by automatic reinforcement. J. Appl. Behav. Anal. 37 (2004) 83-87
38. Fischer S.M., Iwata B.A., and Worsdell A.S. Attention as an establishing operation and as reinforcement during functional analysis. J. Appl. Behav. Anal. 30 (1997) 335-338
39. Fisher W.W., and Mazur J.E. Basic and applied research on choice responding. J. Appl. Behav. Anal. 30 (1997) 387-410
40. Fraser D., and Broom D.B. Farm Animal Behaviour and Welfare (1990), CAB International, Wallingford, Oxon
41. Fritz J., and Fritz P. The hand-rearing unit: management decisions that may affect chimpanzee development. In: Graham C.E., and Bowen J.A. (Eds). Clinical Management of the Infant Great Apes (1985), Liss, New York 1-34
42. Hagopian L.P., Fisher W.W., Sullivan M.T., Acquisto J., and LeBlanc L.A. Effectiveness of functional communication training with and without extinction and punishment: a summary of 21 inpatient cases. J. Appl. Behav. Anal. 31 (1998) 211-235
43. Hanley G.P., Iwata B.A., and McCord B.E. Functional analysis of problem behavior: a review. J. Appl. Behav. Anal. 36 (2003) 147-185
44. Harlow H.F., and Mears C. The Human Model: Primate Perspectives (1979), John Wiley and Sons, New York pp. viii and 312
45. Iwata B.A., Pace G.M., Dorsey M.F., Zarcone J.R., Vollmer T.R., Smith R.G., Rogers T.A., Lerman D.C., Shore B.A., Mazeleski J.L., Goh H.L., Cowdery G.E., Kalsher M.J., McCosh K.C., and Willis K.D. The functions of self-injurious behavior: an experimental-epidemiological analysis. J. Appl. Behav. Anal. 27 (1994) 215-240
46. Iwata B.A., Smith R.G., and Michael J. Current research on the influence of establishing operations on behavior in applied settings. J. Appl. Behav. Anal. 33 (2000) 411-418
47. Jorgensen M.J., Kinsey J., and Novak M.A. Effects of cage size on self-injurious and abnormal behavior in macaques. Am. J. Primatol. 42 (1997) 120 (abstract)
48. Kahng S., Iwata B.A., and Lewin A.B. Behavioral treatment of self-injury, 1964 to 2000. Am. J. Ment. Retard. 107 (2000) 212-221
49. Kennedy C.H., Meyer K.A., Knowles T., and Shulka S. Analyzing the multiple functions of stereotypical behavior for students with autism: implications for assessment and treatment. J. Appl. Behav. Anal. 33 (2000) 559-571
50. Kinsey J.H., Jorgensen M., and Novak M. The effects of grooming boards on abnormal behavior in rhesus monkeys (Macaca mulatta). Am. J. Primatol. 42 (1997) 122-123 (abstract)
51. Kinsey, J.H., Jorgensen, M.J., Platt, D.M., Hazen, T.J., 1996. Food puzzle feeders: effects on self-biting and stereotypy in individually housed monkeys. IPS/ASP Congress Abstracts 1996, p. 683 (abstract).
52. Koban T., Miyamoto M., Donmoyer G., and Hammar A. Effects of positive reinforcement training on cortisol, hematology and cardiovascular parameters in cynomolgus macaques, Macaca fasicularis. Presented at the International Conference on Environmental Enrichment. New York, NY (2005)
53. Kraemer G.W., and Clarke A.S. The behavioral neurobiology of self-injurious behavior in rhesus monkeys. Prog. Neuro-Psychopharmacol. Biol. 14 (1990) 141-168
54. Kraemer G.W., Schmidt D.E., and Ebert M.H. The behavioral neurobiology of self-injurious behavior in rhesus monkeys-current concepts and relations to impulsive behavior in humans. Ann. NY Acad. Sci. 836 (1997) 12-38
55. Kurtz P.F., Chin M.D., Huete J.M., Tarbox R.S.F., O'Connor J.T., Paclawskyj T.R., and Rush K.S. Functional analysis and treatment of self-injurious behavior in young children: a summary of 30 cases. J. Appl. Behav. Anal. 36 (2003) 205-219
56. Lambeth S.P., Hau J., Perlman J.E., Martino M.A., Bernacky B.J., and Schapiro S.J. Positive reinforcement training affects hematologic and serum chemistry values in captive chimpanzees (Pan troglodytes). Am. J. Primatol. 62 (2004) 37-38 (abstract)
57. Lambeth S.P., Perlman J.E., Thiele E., and Schapiro S. Changes in hematology and blood chemistry parameters in captive chimpanzees (Pan troglodytes) as a function of blood sampling technique: trained vs. anesthetized samples. Am. J. Primatol. 66 (2005) 182 (abstract)
58. Laule G. The use of behavioral management techniques to reduce or eliminate abnormal behavior. Anim. Welfare Inform. Center Newslett. 4 (1993) 8-11
59. In: Lawrence A.B., and Rushen J. (Eds). Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare (1993), CAB International, Oxon, UK pp. x and 212
60. Lindberg J.S., Iwata B.A., and Kahng S. On the relation between object manipulation and stereotypic self-injurious behavior. J. Appl. Behav. Anal. 32 (1999) 51-62
61. Lindberg J.S., Iwata B.A., Rosco E.M., Worsdell A.S., and Hanley G.P. Treatment efficacy on noncontingent reinforcement during brief and extended application. J. Appl. Behav. Anal. 36 (2003) 1-19
62. Lukas K.E. A review of nutritional and motivational factors contributing to the performance of regurgitation and reingestation in captive lowland gorillas (Gorilla gorilla gorilla). Appl. Anim. Behav. Sci. 63 (1999) 249-273
63. Lutz C., Well A., and Novak M. Stereotypic and self-injurious behavior in rhesus macaques: a survey and retrospective analysis of environment and early experience. Am. J. Primatol. 60 (2003) 1-15
64. Macy Jr. J.D., Beattie T.A., Morgenstern S.E., and Arnstern A.F.T. The use of guanfacine to control self-injurious behavior in nonhuman primates. Contemp. Top. Lab. Anim. Sci. 38 (1999) 34 (abstract)
65. Maple T.L. Environmental psychology and great ape reproduction. Int. J. Study Anim. Prob. 4 (1983) 295-299
66. Maple T.L., and Finlay T.W. Evaluating captive primate environments. In: Benirschke K. (Ed). Primates: The Road to Self-sustaining Populations (1986), Springer-Verlag, New York 480-488
67. Maple T.L., and Finlay T.W. Postoccupancy evaluation in the zoo. Appl. Anim. Behav. Sci. 18 (1987) 5-18
68. Mason G.J. Stereotypies: a critical review. Anim. Behav. 41 (1991) 1015-1037
69. Mason G.J. Forms of stereotypic behavior. In: Lawrence A.B., and Rushen J. (Eds). Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare (1993), Cab International, Wallingford 7-40
70. Mason G.J., and Latham N.R. Can't stop, won't stop: is stereotypy a reliable animal welfare indicator?. Anim. Welfare 13 (2004) S57-S69
71. Mason G., Clubb R., Latham N., and Vickery S. Why and how should we use environmental enrichment to tackle stereotypic behaviour?. Appl. Anim. Behav. Sci. 102 (2007) 163-188
72. Meder A. Effects of hand-rearing on the behavioral development of infant and juvenile gorillas (Gorilla g. gorilla). Dev. Psychobiol. 22 (1989) 357-376
73. Miller N., and Neuringer A. Reinforcing variability in adolescents with autism. J. Appl. Behav. Anal. 33 (2000) 151-165
74. Morgan L., Howell S.M., and Fritz J. Regurgitation and reingestion in a captive chimpanzee (Pan troglodytes). Lab Anim. 22 (1993) 42-45
75. New A.S., Trestman R.L., Mitropoulou V., Benishay D.S., Coccaro E., Silverman J., and Siever L.J. Serotonergic function and self-injurious behavior in personality disorder patients. Psychiatr. Res. 3 (1997) 17-26
76. Novak M.A. Self-injurious behavior in rhesus monkeys: new insights into its etiology, physiology, and treatment. Am. J. Primatol. 59 (2003) 3-19
77. Novak M.A., Kinsey J.H., Jorgensen M.J., and Hazen T.J. Effects of puzzle feeders on pathological behavior in individually housed rhesus monkeys. Am. J. Primatol. 46 (1998) 213-227
78. Novak M.A., and Suomi S.J. Psychological well-being of primates in captivity. Am. Psychol. 40 (1988) 765-773
79. Ogden J.J., Bruner G., and Maple T.L. A survey of the use of electric fencing with captive great apes. Int. Zoo Yearbook 31 (1992) 229-236
80. Ogden J.J., Finlay T.W., and Maple T.L. Gorilla adaptations to naturalistic environments. Zoo Biol. 9 (1990) 107-121
81. Ogden J.J., Lindburg D.G., and Maple T.L. Preferences for structural environmental features in captive lowland gorillas. Zoo Biol. 12 (1993) 381-396
82. Paulk H.H., Dienske H., and Ribbens L.G. Abnormal behavior in relation to cage size in rhesus monkeys. J. Abnorm. Psychol. 86 (1977) 87-92
83. Pazol K.A., and Bloomsmith M.A. The development of stereotyped body rocking in chimpanzee (Pan troglodytes) reared in a variety of nursery settings. Anim. Welfare 2 (1993) 113-129
84. Piazza C.C., Fisher W.W., Hanley G.P., LeBlanc L.A., Worsdell A.S., Lindauer S.E., and Keeney K.M. Treatment of pica through multiple analyses of its reinforcing functions. J. Appl. Behav. Anal. 31 (1998) 165-189
85. Pierce W.D., and Cheney C.D. Behavior Analysis and Learning (2004), Lawrence Erlbaum and Associates, Mahwah, NJ
86. Preilowsiki B., Reger M., and Engele H. Combining scientific experimentation with conventional housing: a pilot study with rhesus monkeys. Am. J. Primatol. 14 (1988) 223-234
87. Priest G. Training a diabetic drill (Mandrillus leucophaeus) to accept insulin injections and venipuncture. Lab. Primate Newslett. 30 (1991) 1-4
88. Prosen H., and Bell B. A psychiatrist consulting at the zoo (The therapy of brain bonobo). The Apes: Challenges for the 21st Century Conference Proceedings. Brookfield, IL, May 10-13 (2000) 161-164
89. Pryor K. Don't Shoot The Dog! The New Art of Teaching and Training (1999), Bantan Books
90. Raper J.R., Bloomsmith M.A., Stone A., and Mayo L. Use of positive reinforcement training to decrease stereotypic behaviors in a pair of orang-utangs (Pongo pygmaeus). Am. J. Primatol. 57 (2002) 70-71 (abstract)
91. Rapp J.T., Miltenberger R.G., Galensky T.L., Ellingston S.A., and Long E.S. A functional analysis of hair-pulling. J. Appl. Behav. Anal. 32 (1999) 329-337
92. Reinhardt V., Cowley D., Eisele S., and Scheffler J. Avoiding undue cortisol responses to venipuncture in adult rhesus macaques. Anim. Technol. 42 (1991) 83-86
93. Reinhardt V., and Rossel M. Self-biting in caged macaques: cause, effect, and treatment. J. Appl. Anim. Welfare Sci. 4 (2001) 285-294
94. Ringdahl J.E., Vollmer T.R., Marcus B.A., and Roane H.S. An analogue evaluation of environmental enrichment: the role of stimulus preference. J. Appl. Behav. Anal. 30 (1997) 203-216
95. Sackett G.P. Persistence of abnormal behaviour in monkeys following isolation rearing. The Role of Learning in Psychotherapy; A Ciba Foundation Symposium Proceedings (1968) 3-37
96. Savastano G. The effects of operant conditioning on cortisol levels in captive snow leopards. Presented at the International Conference on Environmental Enrichment. New York, NY (2005)
97. Schapiro S.J., and Bloomsmith M.A. Behavioral effects of enrichment on singly-housed, yearling rhesus monkeys: an analysis including three enrichment conditions and a control group. Am. J. Primatol. 35 (1995) 89-101
98. Schapiro S.J., Bloomsmith M.A., Porter L.M., and Suarez S.A. Enrichment effects on rhesus monkeys successively housed singly, in pairs, and in groups. Appl. Anim. Behav. Sci. 48 (1996) 159-172
99. Schapiro S.J., Porter L.M., Suarez S.A., and Bloomsmith M.A. The behavior of singly-caged, yearling rhesus monkeys is affected by the environment outside of the cage. Appl. Anim. Behav. Sci. 45 (1995) 151-163
100. Skinner B.F. An operant analysis of problem-solving. In: Catania A.C., and Harnand S. (Eds). The Selection of Behavior: The Operant Behaviorism of B.F. Skinner (Comments and Consequences) (1988), Cambridge University Press, New York 218-277
101. Snowdon C.T., and Savage A. The psychological well-being of nonhuman primates: general considerations and examples from callitrichids. In: Segal E.F. (Ed). Housing, Care and Psychological Wellbeing of Captive and Laboratory Primates (1989), Noyes Publications, Park Ridge, NJ 75-88
102. Tarou L.R., and Bashaw M.J. Maximizing the effectiveness of environmental enrichment: Suggestions from the experimental analysis of behavior. Appl. Anim. Behav. Sci. 102 (2007) 189-204
103. Tiefenbacher S., Jorgensen M.J., Novak M.A., and Meyer J.S. Hypothalamic-pituitary-adrenal and hypothalamic-pituitary-gonadal activity in rhesus monkeys with self-injurious behavior. Am. J. Primatol. 49 (1999) 108-109 (abstract)
104. Tiefenbacher S., Fahey M.A., Pouliot A.L., Kaufman B.M., Rowlett J.K., and Novak M.A. Effects of diazepam treatment on the incidence of self-injurious behavior in individually housed male rhesus monkeys. Am. J. Primatol. 62 (2004) 112
105. Ullmann L.P., and Krasner L. A Psychological Approach to Abnormal Behavior. 2nd ed. (1975), Prentice-Hall, Englewood Cliffs, NJ
106. Videan E.N., Fritz J., Murphy J., Howell S., and Heward C.B. Does training chimpanzees to present for injection lead to reduced stress?. Lab. Primate Newslett. 44 3 (2005) 1-2
107. Vollmer T.R. The concept of automatic reinforcement: implications for behavioral research in developmental disabilities. Res. Dev. Disabil. 15 (1994) 187-207
108. Watson L.M. Effect of an enrichment device on stereotypic and self-aggressive behaviors in singly-caged macaques: a pilot study. Lab. Primate Newslett. 31 (1992) 8-9
109. Webster J. Animal Welfare: Limping Towards Eden (2005), Universities Federation for Animal Welfare (UFAW) Blackwell Publishing
110. Weed J.L., Wagner P.O., Byrum R., Parrish S., Knezevich M., and Powell D.A. Treatment of persistent self-injurious behavior in rhesus monkeys through socialization: preliminary report. Contemp. Top. Lab. Anim. Sci. 42 (2003) 21-23
111. Weld K.P. The role of serotonin in the modulation of aggressive and affiliative behavior in laboratory housed rhesus monkeys (Macaca mulatta). Dissert. Abstr. Int. B 59 (1999) 5262
112. Whittaker M., Laule G., Perlman J., Shapiro S., and Keeling M. A behavioral management approach to caring for great apes. The Apes: Challenges for 21st Century. Conference Proceedings (2001), Brookfield Zoo, Brookfield 131-134
113. Young R.J. Environmental Enrichment for Captive Animals (2003), Blackwell Science, Oxford