Physiological and welfare consequences of transport, relocation, and acclimatization of chimpanzees (Pan troglodytes)

Applied Animal Behaviour Science

Volumn 138, Issue 1-2, 2012, Pages 183-193

  Schapiro, Steven J ^a,b   Lambeth, Susan P ^a   Jacobsen, Kirsten Rosenmaj ^b   Williams, Lawrence E ^a   Nehete, Bharti N ^a   Nehete, Pramod N ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Acclimatization; Chimpanzees; Pan troglodytes; Relocation; Transport; Welfare

Indexed keywords

ACCLIMATION; ANIMAL WELFARE; BEHAVIORAL ECOLOGY; BLOOD; CAPTIVE POPULATION; DEVELOPMENTAL BIOLOGY; HOMINID; IMMUNE SYSTEM; RELOCATION;

ARIZONA; TEXAS; UNITED STATES;

ANIMALIA; PAN; PAN TROGLODYTES; PRIMATES;

EID: 84859445766     PISSN: 01681591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.applanim.2011.11.004     Document Type: Article

References (64)

1. Barasa M., MM G., Kagasi A., Hastings O. Characterisation of placental malaria in olive baboons (Papio anubis) infected with Plasmodium knowlesi H strain. Int. J. Integr. Biol. 2010, 9:54-58.
2. Bergeron R., Scott S., Emond J., Mercier F., Cook N., Schaefer A. Physiology and behavior of dogs during air transport. Can. J. Vet. Res. 2002, 66:211-216.
3. Bloomsmith M.A., Else J.G. Behavioral management of chimpanzees in biomedical research facilities: the state of the science. ILAR J. 2005, 46:192-201.
4. Bloomsmith M.A., Schapiro S.J., Strobert E.A. Preparing chimpanzees for laboratory research. ILAR J. 2006, 47:316-325.
5. Boinski S., Swing S.P., Gross T.S., Davis J.K. Environmental enrichment of brown capuchins (Cebus apella): behavioral and plasma and fecal cortisol measures of effectiveness. Am. J. Primatol. 1999, 48:49-68.
6. Capitanio J., Lerche N. Social separation, housing relocation, and survival in simian AIDS: a retrospective analysis. Psychosom. Med. 1998, 60:235-244.
7. Capitanio J.P., Kyes R.C., Fairbanks L.A. Considerations in the selection and conditioning of Old World Monkeys for laboratory research: animals from domestic sources. ILAR J. 2006, 47:294-306.
8. Carlsson H., Lyberg K., Royo F., Hau J. Quantification of stress sensitive markers in single fecal samples do not accurately predict excretion of these in the pig. Res. Vet. Sci. 2007, 82:423-428.
9. Clay A., Bloomsmith M., Marr M., Maple T. Habituation and desensitization as methods for reducing fearful behavior in singly housed rhesus macaques. Am. J. Primatol. 2009, 71:30-39.
10. Crockett C.M., Bowers C.L., Sackett G.P., Bowden D.M. Urinary cortisol responses of longtailed macaques to five cage sizes, tethering, sedation, and room change. Am. J. Primatol. 1993, 30:55-74.
11. Dalin A., Magnusson U., Haggendal J., Nyberg L. The effect of transport stress on plasma levels of catecholamines, cortisol, corticosteroid-binding globulin, blood-cell count, and lymphocyte-proliferation in pigs. Acta Vet. Scand. 1993, 34:59-68.
12. Davenport M., Lutz C., Tiefenbacher S., Novak M., Meyer J. A rhesus monkey model of self-injury: effects of relocation stress on behavior and neuroendocrine function. Biol. Psychiatry 2008, 63:990-996.
13. Deckardt K., Weber I., Kasper S., Hellwig J., Tennekes H., van Ravenzwaay B. The effects of inhalation anesthetics on common clinical pathology parameters in laboratory rats. Food Chem. Toxicol. 2007, 45:1709-1718.
14. Depoyster J. Transportation of primates and the Animal Welfare Act. International Perspectives: The Future of Nonhuman Primate Resources. Proceeding of the Workshop 2003, 183-186. Institute for Laboratory Animal Research, N.R.C. (Ed.).
15. Dolbier C.L., Cocke R.R., Leiferman J.A., Steinhardt M.A., Schapiro S.J., Nehete P.N., Perlman J.E., Sastry J. Differences in functional immune responses of high vs. low hardy healthy individuals. J. Behav. Med. 2001, 24:219-229.
16. Fazio E., Alberghina D., Medica P., Cavalier S., Ferlazzo A. Total and free iodothyronine levels before and after short and long road transport in Limousine calves. Biotechnol. Agron. Soc. Environ. 2001, 5:76-77.
17. Fazio E., Ferlazzo A. Evaluation of stress during transport. Vet. Res. Commun. 2003, 27:519-524.
18. Fazio E., Medica P., Cravana C., Giacoppo E., Ferlazzo A. Physiological variables of horses after road transport. Animal 2009, 3:1313-1318.
19. Fernstrom A.L., Sutian W., Royo F., Westlund K., Nilsson T., Carlsson H.E., Paramastri Y., Pamungkas J., Sajuthi D., Schapiro S.J., Hau J. Stress in cynomolgus monkeys (Macaca fascicularis) subjected to long-distance transport and simulated transport housing conditions. Stress 2008, 11:467-476.
20. Fritz J., Howell S. Captive chimpanzee social group formation. The Care and Management of Captive Chimpanzees 2001, 173-204. American Society of Primatologists, San Antonio, TX. L. Brent (Ed.).
21. Gil A., Slivan G., Gil-Cabrera F., Garcia C., Prieto I., Illera J. Effects of halothane and isoflourane anesthesia on selected serum biochemical parameters in NZW rabbits. J. Am. Assoc. Lab. Anim. Sci. 2007, 46:125-126.
22. Herndon J.G., Tigges J. Hematologic and blood biochemical variables of captive chimpanzees: cross-sectional and longitudinal analyses. Comp. Med. 2001, 51:60-69.
23. Hill L.R., Nehete P.N., Schapiro S.J., Nehete B.P., Jagannadha Sastry K. SHIV transmission and susceptibility to re-exposure through social contact following vaccination with an HIV synthetic peptide-cocktail: a case study. J. Med. Primatol. 2004, 33:10-15.
24. Honess P.E., Johnson P.J., Wolfensohn S.E. A study of behavioural responses of non-human primates to air transport and re-housing. Lab. Anim. 2004, 38:119-132.
25. Ihrig M., Tassinary L.G., Bernacky B., Keeling M.E. Hematologic and serum biochemical reference intervals for the chimpanzee (Pan troglodytes) categorized by age and sex. Comp. Med. 2001, 51:30-37.
26. Kagira J.M., Ngotho M., Thuita J.K., Maina N.W., Hau J. Hematological changes in vervet monkeys (Chlorocebus aethiops) during eight months' adaptation to captivity. Am. J. Primatol. 2007, 69:1053-1063.
27. Kim C.Y., Han J.S., Suzuki T., Han S.S. Indirect indicator of transport stress in hematological values in newly acquired cynomolgus monkeys. J. Med. Primatol. 2005, 34:188-192.
28. Koban T.L., Schapiro S.J., Kusznir T., Lambeth S.P., Ogbin J., Garofalo E. Effects of international transit and relocation on cortisol values in cynomolgus macaques (Macaca fascicularis). Am. J. Primatol. 2010, 72(Suppl. 1):51.
29. Lambeth S.P., Hau J., Perlman J.E., Martino M., Schapiro S.J. Positive reinforcement training affects hematologic and serum chemistry values in captive chimpanzees (Pan troglodytes). Am. J. Primatol. 2006, 68:245-256.
30. Landi M., Kreider J., Lang C., Bullock L. Effects of shipping on the immune function in mice. Am. J. Vet. Res. 1982, 43:1654-1657.
31. Laule G., Whittaker M. Enhancing nonhuman primate care and welfare through the use of positive reinforcement training. J. Appl. Anim. Welfare Sci. 2007, 10:31-38.
32. Lutz C.K., Novak M.A. Environmental enrichment for nonhuman primates: theory and application. ILAR J. 2005, 46:178-191.
33. Malaga C., Weller R., Montoya E., Moro J., Buschbom R. Mortality and body-weight changes in Aotus nancymai shipped from Iquitos, Peru to Richland, Washington. J. Med. Primatol. 1991, 20:6-11.
34. McGlone J., Salak J., Lumpkin E., Nicholson R., Gibson M., Norman R. Shipping stress and social-status effects on pig performance, plasma-cortisol, natural-killer-cell activity and leukocyte numbers. J. Anim. Sci. 1993, 71:888-896.
35. Millspaugh J., Washburn B. Within-sample variation of fecal glucocorticoid measurements. Gen. Comp. Endocrinol. 2003, 132:21-26.
36. Nehete P.N., Murthy K.K., Satterfield W.C., Arlinghaus R.B., Sastry K.J. Studies on V3-specific cross-reactive T-cell responses in chimpanzees chronically infected with HIV-1(IIIB). AIDS 1995, 9:567-572.
37. Obernier J.A., Baldwin R.L. Establishing an appropriate period of acclimatization following transportation of laboratory animals. ILAR J. 2006, 47:364-369.
38. Paramastri Y., Royo F., Eberova J., Carlsson H., Sajuthi D., Fernstrom A., Pamungkas J., Hau J. Urinary and fecal immunoglobulin A, cortisol and 11,17 dioxoandrostanes, and serum cortisol in metabolic cage housed female cynomolgus monkeys (Macaca fascicularis). J. Med. Primatol. 2007, 36:355-364.
39. Perlman J.E., Horner V., Bloomsmith M.A., Lambeth S.P., Schapiro S.J. Positive reinforcement training, welfare, and chimpanzee social learning. The Mind of the Chimpanzee 2010, 320-331. Chicago Press, Chicago. E. Lonsdorf, S. Ross, T. Matsuzawa (Eds.).
40. Pihl L., Hau J. Faecal corticosterone and immunoglobulin A in young adult rats. Lab. Anim. 2003, 37:166-171.
41. Prescott M.J., Jennings M. Ethical and welfare implications of the acquisition and transport of non-human primates for use in research and testing. Altern. Lab. Anim. 2004, 32:323-327.
42. Ross S., Wagner K., Schapiro S., Hau J., Lukas K. Transfer and acclimatization effects on the behavior of two species of African great ape (Pan troglodytes and Gorilla gorilla gorilla) moved to a novel and naturalistic zoo environment. Int. J. Primatol. 2011, 32:99-117.
43. Schaffner C., Smith T. Familiarity may buffer the adverse effects of relocation on marmosets (Callithrix kuhlii): preliminary evidence. Zoo Biol. 2005, 24:93-100.
44. Schapiro S., Lambeth S., Perlman J., Thiele E., Nehete P., Sastry K. Immunological responses and captive procedures in rhesus monkeys and chimpanzees. Int. J. Primatol. 2006, 27(Suppl. 1):25.
45. Schapiro S., Lambeth S., Thiele E., Rousset O. The effects of behavioral management programs on dependent measures in biomedical research. Am. J. Primatol. 2007, 69:115.
46. Schapiro S.J. Effects of social manipulations and environmental enrichment on behavior and cell-mediated immune responses in rhesus macaques. Pharmacol. Biochem. Behav. 2002, 73:271-278.
47. Schapiro S.J., Bloomsmith M.A., Kessel A.L., Shively C.A. Effects of enrichment and housing on cortisol response in juvenile rhesus monkeys. Appl. Anim. Behav. Sci. 1993, 37:251-263.
48. Schapiro S.J., Lambeth S.P. Control, choice, and assessments of the value of behavioral management to nonhuman primates in captivity. J. Appl. Anim. Welfare Sci. 2007, 10:39-47.
49. Schapiro S.J., Lambeth S.P. Chimpanzees. The UFAW Handbook on the Care and Management of Laboratory Animals 2010, 618-634. Wiley-Blackwell, Oxford, UK. R. Hubrecht, J. Kirkwood (Eds.).
50. Schapiro S.J., Nehete P.N., Perlman J.E., Sastry K.J. A comparison of cell-mediated immune responses in rhesus macaques housed singly, in pairs, or in groups. Appl. Anim. Behav. Sci. 2000, 68:67-84.
51. Schapiro S.J., Perlman J.E., Boudreau B.A. Manipulating the affiliative interactions of group-housed rhesus macaques using positive reinforcement training techniques. Am. J. Primatol. 2001, 55:137-149.
52. Schapiro S.J., Perlman J.E., Thiele E., Lambeth S. Training nonhuman primates to perform behaviors useful in biomedical research. Lab. Anim. 2005, 34:37-42.
53. Swallow J., Anderson D., Buckwell A., Harris T., Hawkins P., Kirkwood J., Lomas M., Meacham S., Peters A., Prescott M., Owen S., Quest R., Sutcliffe R., Thompson K. Guidance on the transport of laboratory animals. Lab. Anim. 2005, 39:1-39.
54. Tardif S., Bales K., Williams L., Moeller E.L., Abbott D., Schultz-Darken N., Mendoza S., Mason W., Bourgeois S., Ruiz J. Preparing New World monkeys for laboratory research. ILAR J. 2006, 47:307-315.
55. van Ruiven R., Meijer G., Wiersma A., Baumans V., van Zutphen L., Ritskes-Hoitinga R. The influence of transportation stress on selected nutritional parameters to establish the necessary minimum period for adaptation in rat feeding studies. Lab. Anim. 1998, 32:446-456.
56. Veeder C., Bloomsmith M., McMillan J., Perlman J., Martin A. Positive reinforcement training to enhance the voluntary movement of group-housed sooty mangabeys (Cercocebus atys atys). J. Am. Assoc. Lab. Anim. Sci. 2009, 48:192-195.
57. Videan E., Fritz J., Murphy J. Effects of aging on hematology and serum clinical chemistry in chimpanzees (Pan troglodytes). Am. J. Primatol. 2008, 70:327-338.
58. Videan E., Fritz J., Schwandt M., Smith H., Howell S. Controllability in environmental enrichment for captive chimpanzees (Pan troglodytes). J. Appl. Anim. Welfare Sci. 2005, 8:117-130.
59. Wall H., Worthman C., Else J. Effects of ketamine anesthesia, stress and repeated bleeding on the hematology of vervet monkeys. Lab. Anim. 1985, 19:138-144.
60. Watson S., McCoy J., Stavisky R., Greer T., Hanbury D. Cortisol response to relocation stress in Garnett's bushbaby (Otolemur garnettii). Contemp. Top. Lab. Anim. Sci. 2005, 44:22-24.
61. Whiten A., Spiteri A., Horner V., Bonnie K.E., Lambeth S.P., Schapiro S., de Waal F.B.M. Transmission of multiple traditions within and between chimpanzee groups. Curr. Biol. 2007, 17:1038-1043.
62. Whitten P., Stavisky R., Aureli F., Russell E. Response of fecal cortisol to stress in captive chimpanzees. Am. J. Primatol. 1998, 44:57-69.
63. Williams L., Nehete P., Schapiro S., Lambeth S. Effects of relocation on immunological measures in two captive nonhuman primate species: squirrel monkeys and owl monkeys. Am. J. Primatol. 2010, 72(Suppl. 1):28.
64. Wolfensohn S.E. Brief review of scientific studies of the welfare implications of transporting primates. Lab. Anim. 1997, 31:303-305.