Environmental enrichment of brown capuchins (Cebus apella): Behavioral and plasma and fecal cortisol measures of effectiveness

American Journal of Primatology

Volumn 48, Issue 1, 1999, Pages 49-68

  Boinski, Sue ^a,b   Swing, Sonya P ^c   Gross, Timothy S ^d   Davis, Jerry K ^b  

^a University of Florida   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d U S GEOLOGICAL SURVEY   (United States)

Author keywords

Capuchin; Cebus apella; Cortisol; Environmental enrichment; Psychological well being; Stress

Indexed keywords

HYDROCORTISONE;

ANIMAL; ANIMAL WELFARE; ARTICLE; BLOOD; CEBIDAE; CHEMISTRY; DIET; ENVIRONMENT; FECES; FEMALE; MALE; MENTAL STRESS; MOTOR ACTIVITY; PHYSIOLOGY; PSYCHOLOGICAL ASPECT; RANDOMIZATION; RECREATION; ZOO ANIMAL;

ANIMAL WELFARE; ANIMALS; ANIMALS, ZOO; CEBUS; DIET; ENVIRONMENT; FECES; FEMALE; HYDROCORTISONE; MALE; MOTOR ACTIVITY; PLAY AND PLAYTHINGS; RANDOM ALLOCATION; STRESS, PSYCHOLOGICAL;

ANIMALIA; CEBIDAE; CEBUS APELLA; MEDICAGO SATIVA; PRIMATES;

EID: 0032908364     PISSN: 02752565     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1098-2345(1999)48:1<49::AID-AJP4>3.0.CO;2-6     Document Type: Article

References (85)

1. Anderson JR, Chamove AS. 1984. Allowing captive primates to forage. In: Standards in laboratery animal management, vol 2. Potters Bar, UK: Universities Federation for Animal Welfare. p 253-256.
2. Anderson JR, Roeder J. 1989. Responses of capuchin monkeys (Cebus apella) to different conditions of mirror image stimulation. Primates 30:581-587.
3. Bayne KAL. 1991. Alternatives to continuous social housing. Lab Anim Sci 41:355-369.
4. Bayne K, Dexter S. 1992. Removing an environmental enrichment device can result in a rebound of abnormal behavior in rhesus monkeys (Macaca mulatta). Am J Primatol 27:15.
5. Bayne KA, Martin DP. 1998. AAALAC International: using performance standards to evaluate an animal care and use program. Lab Anim 27:32-35.
6. Bayne KAL, Mainzer H, Dexter S, Campbell G, Yamada F, Suomi, S. 1991. The reduction of abnormal behaviors in individually housed rhesus monkeys (Macaca mulatta) with a foraging/grooming board. Am J Primatol 23:23-35.
7. Bayne KAL, Dexter S, Mainzer H, Campbell G, McCully C, Campbell G, Yamada F. 1992. The use of artificial turf as a foraging substrate for individually housed rhesus monkeys (Macaca mulatta). Animal Welfare 1:39-53.
8. Bergeron RJ, Lin R, McManis JS. 1992. Structural alterations in desferrioxamine compatible with iron clearance in animals. J Med Chem 35:4739-4744.
9. Boinski S. 1988. Use of a club by a white-faced capuchin (Cebus capucinus) to attack a venomous snake (Bothrops asper). Am J Primatol 14:177-179.
10. Boinski S. 1998. Stress responses in primates: proximate mechanisms in the evolution of social organization. In: Foster SA, Endler JA, editors. Geographic variation in behavior: perspectives in evolutionary mechanisms. New York: Oxford University Press. p 95-120.
11. Boinski S, Noon C, Stans S, Samudio R, Sammarco P, Hayes A. 1994. The behavioral profile and environmental enrichment of a squirrel monkey colony: comparisons to wild populations. Laboratory Primate Newsletter 33:1-4.
12. Box HO. 1991. Responsiveness to environmental change: interrelationships among parameters. In: Box HO, editor. Primate responses to environmental change. London: Chapman & Hall. p 57-74.
13. Broom DM, Johnson KG. 1993. Stress and animal welfare. London: Chapman & Hall.
14. Byrne G, Suomi SJ. 1996. Individual differences in object manipulation in a colony of tufted capuchins. J Hum Evol 31:259-267.
15. Byrne G, Suomi SJ. 1998. Relationship of early infant state measures to behavior over the first year of life in the tufted capuchin monkey (Cebus apella). Am J Primatol 44:43-56.
16. Carlstead K. 1996. Effects of captivity on the behavior of wild mammals. In: Kleiman DG, Allen ME, Thompson KV, Lumpkin S, editors. Wild mammals in captivity. Chicago: University of Chicago Press. p 317-333.
17. Chapman CA. 1986. Boa constrictor predation and group response in white-faced Cebus monkeys. Biotropica 18:171-172.
18. Chapman CA. 1987. Flexibility in diets of three species of Costa Rican primates. Folia Primatol (Basel) 49:90-105.
19. Clarke AS, Boinski S. 1995. Temperament in nonhuman primates. Am J Primatol 37:103-125.
20. Clarke AS, Czekala NM, Lindburg DG. 1995. Behavioral and adrenocortical responses of male cynomolgus and lion-tailed macaques to social stimulation and group formation. Primates 36:41-56.
21. Clarke AS, Mason WA, Mendoza SP. 1994. Heart rate patterns under stress in three species of macaques. Am J Primatol 33: 133-148.
22. Coe CL. 1991. Is social housing of primates always the optimal choice? In: Novak MA, Petto AJ, editors. Through the looking glass: issues of psychological wellbeing in captive nonhuman primates. Washington, DC: American Psychological Association. p 78-92.
23. Cohen J. 1960. A coefficient of agreement for nominal scales. Educational and Psychological Measurement 20:37-46.
24. Collinge NE. 1989. Mirror reactions in a zoo colony of Cebus monkeys. Zoo Biology 8:89-98.
25. Combrette C, Anderson JR. 1991. Responses to two environmental enrichment techniques in two primate species in a laboratory setting (Cebus apella, Lemur macaca). Cahiers d'Ethologie 11:1-16.
26. Crockett CM, Bowers CL, Sackett GP, Bowden DM. 1993. Urinary cortisol responses of longtailed macaques to five cage sizes, tethering, sedation, and room change. Am J Primatol 30:55-74.
27. Crockett CM, Bowers CL, Bowden DM, Sackett GP. 1994. Sex differences in compatibility of pair-housed adult longtailed macaques. Am J Primatol 32:73-94.
28. Crockett CM, Bowers CL, Shimoji B, Leu M, Bowden DM, Sackett GP. 1995. Behavioral responses of longtailed macaques to different cage sizes and common laboratory experiences. J Comp Psychol 109:368-383.
29. de Palermo KE, Carbonetto CH, Malchiodi EL, Margni RA, Falalasca CA. 1988. Humoral and cellular parameters of the immune system of Cebus apella monkeys: cross reactivity between monkey and human immunoglobulins. Vet Immunol Immunopathol 19:341-349.
30. Dettmer EL, Phillips KA, Rager DR, Bernstein IS, Fragaszy DM. 1996. Behavioral and cortisol responses to repeated capture and venipuncture in Cebus apella. Am J Primatol 38:357-362.
31. Erwin J, Sackett G. 1990. Effects of management methods, social organization, and physical space on primate behavior and health. Am J Primatol 20:23-30.
32. Flow BL, Jacques JT. 1997. Effect of room arrangement and blood sample collection sequence on serum thyroid hormone and cortisol concentrations in cynomolgus macaques (Macaca fascicularis). Contemporary Topics in Laboratory Animal Science 36:65-68.
33. Fragaszy DM, Adams-Curtis LE. 1991. Environmental challenges in groups of capuchins. In: Box HO, editor. Primate responses to environmental change. London: Chapman & Hall. p 239-264.
34. Fragaszy DM, Boinski S. 1995. Patterns of individual choice and efficiency of foraging and diet in the wedge-capped capuchin monkey, Cebus olivaceus. J Comp Psychol 109:339-348.
35. Fragaszy DM, Visalberghi E. 1989. Social influences on the acquisition of tool-using behaviors in capuchin monkeys. J Comp Psychol 103:159-170.
36. Fragaszy DM, Boinski S, Whipple J. 1992. Behavioral sampling in the field: a comparison of focal and group methods. Am J Primatol 26:259-275.
37. Garcez LM, Silveira FT, ElHarith A, Lainson R, Shaw JJ. 1997. Humoral responses of Cebus apella (Primates: Cebidae) to infections of Leshmania (Leishmania) amazonensis, L. (Viana) lainsoni and L. (V.) brasiliensis using the direct agglutination test. Acta Trop (Basel) 68:65-76.
38. Graham LH, Brown JL. 1996. Cortisol metabolism in the domestic cat and implications for non-invasive monitoring of adrenocortical function in endangered felids. Zoo Biology 15:71-82.
39. Gust DA, Gordon TP, Wilson ME, Brodie AR, AhmedAnsari A, McClure HM. 1996. Group formation of female pigtail macaques (Macaca nemestrina). Am J Primatol 39:263-273.
40. Hall CL, Fedigan LM. 1997. Spatial benefits afforded by high rank in white-faced capuchins. Animal Behaviour 53:1069-1082.
41. Harlow HF, Suomi SJ. 1971. Social recovery by isolation-reared monkeys. Proc Natl Acad Sci U S A 68:1534-1538.
42. Hayes SL. 1990. Increasing foraging opportunities for a group of captive capuchin monkeys (Cebus capucinus). Lab Anim Sci 40:515-519.
43. Hien E, Deputte BL. 1997. Influence of a capuchin monkey companion on the social life of a person with quadriplegia: an experimental study. Anthrozoos 10:101-107.
44. Janson CH. 1988. Food competition in brown capuchin monkeys (Cebus apella): quantitative effects of group size and tree productivity. Behaviour 105:53-76.
45. Janson CH, Boinski S. 1992. Morphological and behavioral adaptations for foraging in generalist primates: the case of the cebines. Am J Phys Anthropol 88:483-498.
46. Jurke MH, Czekala NM, Lindburg DG, Millard SE. 1997. Fecal corticoid metabolite measurement in the cheetah (Acinonyx jubatus). Zoo Biology 16:133-147.
47. Leichnetz GR, GonzaloRuiz A. 1996. Prearcuate cortex in the Cebus monkey has cortical and subcortical connections like the macaque frontal eye field and projects to fastigial-recipient oculomotor-related brain-stem nuclei. Brain Res Bull 41:1-29.
48. Line SW. 1987. Environmental enrichment for laboratory primates. J Am Vet Med Assoc 190:854-859.
49. Line SW, Morgan KN. 1991. The effects of two novel objects on the behavior of singly caged adult rhesus macaques. Lab Anim Sci 42:365-369.
50. Line SW, Morgan KN, Markowitz H, Strong S. 1990. Increased cage size does not alter heart rate or behavior in female rhesus monkeys. Am J Primatol 20:107-113.
51. Ludes E, Anderson JR. 1996. Comparison of the behaviour of captive white-faced capuchin monkeys (Cebus capucinus) in the presence of four kinds of deep litter. Applied Animal Behaviour Science 49:293-303.
52. Lutz CK, Novak MA. 1995. Use of foraging racks and shavings as enrichment tools for groups of rhesus monkeys (Macaca mulatta). Zoo Biology 14:463-474.
53. Maestripieri D, Schino G, Aureli F, Troisi A. 1992. A modest proposal: displacement activities as an indicator of emotions in primates. Animal Behaviour 44:967-979.
54. Markowitz H. 1982. Behavioral enrichment in the zoo. New York: Van Nostrand and Reinhold.
55. Mason JG. 1991. Stereotypies: a critical review. Animal Behaviour 41:1015-1037.
56. McGrew WC, Brennan JA, Russel J. 1986. An artificial "gum tree" for marmosets (Callithrix j. jachus). Zoo Biology 5:45-50.
57. Mendoza SP, Moberg GP. 1985. Species differences in adrenocortical activity of New World primates: response to dexamethasone suppression. Am J Primatol 8:215-224.
58. Mittermeier RA, Konstant WR, Mast RB. 1994. Use of Neotropical and Malagaszy primate species in biomedical research. Am J Primatol 34:73-80.
59. Molzen EM, French JA. 1989. The problem of foraging in captive callitrichid primates: behavioral time budgets and foraging skills. In: Segal FF, editor. Housing, care and psychological well-being in captive laboratory primates. Park Ridge, NJ: Noyes Publ. p 89-101.
60. National Research Council, Institute for Laboratory Animal Resources. 1996. Guide for the care and use of laboratory animals. Washington, DC: National Academy Press.
61. Newberry RC. 1995. Environmental enrichment: increasing the biological relevance of captive environments. Applied Animal Behaviour Science 44:229-243.
62. Novak MA, Suomi S. 1988. Psychological well-being of primates in captivity. Am Psychol 43:765-773.
63. O'Neill P. 1988. Developing effective social and environmental enrichment strategies for macaques in captive groups. Lab Anim 17:23-24.
64. Parker ST, Gibson KR. 1977. Object manipulation, tool use and sensorimotor intelligence as feeding adaptations in Cebus monkeys and great apes. J Hum Evol 6:623-641.
65. Parr LA, Matheson MD, Bernstein IS, de Waal FBM. 1997. Grooming down the hierarchy allogrooming in captive brown capuchin monkeys, Cebus apella. Animal Behaviour 54:361-367.
66. Perry S. 1997. Male-female social relationships in wild white-faced capuchins (Cebus capucinus). Behaviour 134:477-510.
67. Poole TB. 1991. Criteria for the provision of captive environments. In: Box HO, editor. Primate responses to environmental change. London: Chapman & Hill. p 357-373.
68. Paquette D, Prescott J. 1988. Use of novel objects to enhance environments of captive chimpanzees. Zoo Biology 7:15-23.
69. Reinhardt V, Houser D, Eisele S. 1989. Pairing previously singly caged rhesus monkeys does not interfere with common research protocols. Lab Anim Sci 39:73-74.
70. Reinhardt V, Houser D, Eisele S, Cowley D, Vertein R. 1995. Behavioral responses of unrelated rhesus monkey females paired for the purpose on environmental enrichment. Am J Primatol 14:135-140.
71. Schapiro SJ, Bloomsmith MA. 1995. Behavioral effects of enrichment on singly-housed, yearling rhesus monkeys: an analysis including three enrichment conditions and a control group. Am J Primatol 35:89-101.
72. Schapiro SJ, Bloomsmith MA, Kessel AL, Shively CA. 1993. Effects of enrichment and housing on cortisol response in juvenile rhesus monkeys. Applied Animal Behaviour Science 37:251-263.
73. Schapiro SJ, Porter LM, Suarez SA, Bloom-smith MA. 1995. The behavior of singly-caged, yearling rhesus monkeys is affected by the environment outside of the cage. Applied Animal Behaviour Science 45:151-163.
74. Schapiro SJ, Bloomsmith MA, Porter LM, Suarez SA. 1996a. Effects of social and inanimate enrichment on the behavior of yearling rhesus monkeys. Am J Primatol 40:247-260.
75. Schapiro SJ, Suarez SA, Porter LM, Bloom-smith MA. 1996b. The effects of different types of feeding enhancements on the behaviour of single-caged, yearling rhesus macaques. Animal Welfare 5:129-138.
76. Spring SE, Clifford JO, Tomko DL. 1997. Effect of environmental enrichment devices on behaviors of single- and group-housed squirrel monkeys (Saimiri sciureus). Contemporary Topics In Laboratory Animal Science 36:72-75.
77. Stoskopf MK, Gibbons EF Jr. 1994. Quantitative evaluation of the effects of environmental parameters on the physiology, behavior, and health of animals in naturalistic captive environments. In: Gibbons EF Jr, Wyers EJ, Waters E, Menzel EW Jr, editors. Naturalistic environments in captivity for animal behavior research. Albany: State University of New York Press. p 140-160.
78. Terpstra AH, Strucchi AF, Nicolos RJ. 1991. Estimation of HDL cholesteryl ester kinetic parameters in the Cebus monkey, an animal species with high plasma cholesteryl ester transfer activity. Atherosclerosis 88:243-248.
79. Visalberghi E, McGrew WC. 1997. Cebus meets Pan. International Journal of Primatology 18:677-681.
80. Visalberghi E, Vitale AF. 1991. Coated nuts as an enrichment device to elicit tool use in tufted capuchins (Cebus apella). Zoo Biology 9:65-71.
81. Westergaard GC, Fragaszy DM. 1985. Effects of manipulatable objects on the activity of captive capuchin monkeys (Cebus apella). Zoo Biology 4:317-327.
82. Westergaard GC, Kuhn HE, Suomi SJ. 1998. Laterality of hand function in tufted capuchin monkeys (Cebus apella): comparison between tool-use actions and spontaneous non-tool actions. Ethology 104: 119-125.
83. Whitten PL, Stavisky R, Aureli F, Russell E. 1998. Response of fecal cortisol to stress in captive chimpanzees (Pan troglodytes). Am J Primatol 44:57-69.
84. Wolff AV. 1989. Polyvinyl chloride piping as perch material for squirrel monkeys. Laboratory Primate Newsletter 28:7.
85. Yamada ES, Silveira LCL, Perry VH. 1996. Morphology, dendritic field size, somal size, density, and coverage of M and P retinal ganglion cells of dichromatic Cebus monkeys. Vis Neurosci 13:1011-1029.