The Value of Enrichment to Reintroduction Success

Zoo Biology

Volumn 32, Issue 3, 2013, Pages 332-341

  Reading, Richard P ^a   Miller, Brian ^b   Shepherdson, David ^c  

^a DENVER ZOO   (United States)

^b Wind River Ranch   (United States)

^c OREGON ZOO   (United States)

Author keywords

Animal behavior; Survivorship; Translocation; Welfare

Indexed keywords

ANIMAL; ANIMAL BEHAVIOR; ANIMAL HUSBANDRY; ANIMAL WELFARE; APPETITE; ARTICLE; ENVIRONMENTAL PROTECTION; LOCOMOTION; METHODOLOGY; PHYSIOLOGY; SEXUAL BEHAVIOR; SOCIAL BEHAVIOR; SPECIES DIFFERENCE; ZOO ANIMAL;

ANIMAL HUSBANDRY; ANIMAL WELFARE; ANIMALS; ANIMALS, ZOO; APPETITIVE BEHAVIOR; BEHAVIOR, ANIMAL; CONSERVATION OF NATURAL RESOURCES; LOCOMOTION; SEXUAL BEHAVIOR, ANIMAL; SOCIAL BEHAVIOR; SPECIES SPECIFICITY;

ANIMALIA; PRIMATES;

EID: 84879082533     PISSN: 07333188     EISSN: 10982361     Source Type: Journal    
DOI: 10.1002/zoo.21054     Document Type: Article

References (110)

1. Alberts AC. 2007. Behavioral considerations of headstarting as a conservation strategy for endangered Caribbean rock iguanas. Appl Animal Behav Sci 102: 380-391.
2. Alcock J. 1984. Animal behavior: an evolutionary approach. Sunderland, MA: Sinauer Associates.
3. Apfelbach R. 1978. A sensitive phase for the development of olfactory preference in ferrets (Mustela putorius F. furo L.). Zeitschrift für Säugetierkunde 43: 289-295.
4. Apfelbach R. 1986. Impriting on prey odours in ferrets (Mustela putorius F. furo L.) and its neural correlates. Behav Processes 12: 363-381.
5. Backhouse GN, Clark TW, Reading RP. 1994. Reintroductions for recovery of the eastern barred bandicoot Perameles gunnii in Victoria, Australia. In: Serena M, editor. Reintroduction biology of Australian and New Zealand fauna. Chipping Norton, Victoria, Australia: Surrey Beatty and Sons. p 209-218.
6. Bangs EE, Fritts SH. 1996. Reintroducing the gray wolf to central Idaho and Yellowstone National Park. Wildl Soc Bull 24: 402-413.
7. Banks PB, Norrdahl K, Kropimäki E. 2002. Mobility decisions and the predation risks of reintroduction. Biol Conserv 103: 133-138.
8. Beck BB, Kleiman DG, Dietz JM, et al. 1991. Losses and reintroduced golden-lion tamarins (Leontopithicus rosalia). Dodo, J Jersey Wildl Preserv Trust 27: 50-61.
9. Beck BB, Rapaport LG, Wilson AC. 1994. Reintroduction of captive-born animals. In: Mace GM, Onley PJS, Feistner ATC, editors. Creative conservation. London, UK: Chapman and Hall. p 265-286.
10. Beldon RC, McCown JW. 1996. Florida panther reintroduction feasibility study. Final report, study # 7507. Tallahassee, FL, USA: Florida Game and Fresh Water Fish Commission.
11. Berg WE. 1982. Reintroduction of fisher, pine marten, and river otter. In: Sanderson GC, editor. Midwest Furbearer Management. Wichita, KS, USA: Kansas Chapter of the Wildlife Society. p 159-173.
12. Berger J, Cunningham C. 1994. Bison: mating and conservation in small populations. New York: Columbia University Press.
13. Biggins DE, Hanebury LH, Miller B, Powell RA, Wemmer C. 1991. Release of Siberian ferrets (Mustela eversmanni) to facilitate reintroduction of black-footed ferrets. Internal Report. Ft. Collins, CO, USA: U.S. Fish and Wildlife Service.
14. Biggins DE, Vargas A, Godbey J, Anderson SH. 1999. Influence of pre-release experience on reintroduced black-footed ferrets (Mustela nigripes). Biol Conserv 89: 121-129.
15. Box HO. 1991. Training for life after release: simian primates as examples. In: Gipps JHW, editor. Beyond captive breeding: re-introducing endangered mammals to the wild. Oxford, UK: Clarendon Press. p 111-123.
16. Boyd L, Bandi N. 2002. Reintroduction of takhi, Equus ferus przewalskii, to Hustai National Park, Mongolia: time budget and synchrony of activity pre- and post-release. Appl Animal Behav Sci 78: 97-102.
17. Bremmer-Harrison S, Prodohl PA, Elwood RW. 2004. Behavioral trait assessment as a release criterion: boldness predicts early death in a reintroduction programme of captive-bred swift fox (Vulpes velox). Anim Conserv 7: 313-320.
18. Brightsmith D, Hilburn J, del Campo A, et al. 2005. The use of hand-raised psittacines for reintroduction: a case study of scarlet macaws (Ara macao) in Peru and Costa Rica. Biol Conserv 121: 465-472.
19. Cade TJ, Redig PT, Tordoff HB. 1989. Peregrine falcon restoration: expectation versus reality. Loon 61: 160-162.
20. Campbell B, Altman B, Bangs E, et al. 2006. Restoring wildlife populations. In: Apostle D, Sinclair M, editors. Restoring the Pacific Northwest: the art and science of ecological restoration in Cascadia. Washington, DC: Society for Ecological Restoration International. p 351-373.
21. Carlstead K, Shepherdson DJ. 1994. Effects of environmental enrichment on reproduction. Zoo Biol 13: 447-458.
22. Carlstead K, Brown JL, Montfort SL, Killens R, Wildt DE. 1992. Urinary monitoring of adrenal responses to psychological stressors in domestic and nondomestic felids. Zoo Biol 11: 165-176.
23. Cheyne SM, Chivers DJ, Sugardjito J. 2007. Covariation in the great calls of rehabilitant and wild gibbons (Hylobates albibarbis). Raffles Bull Zool 55: 201-207.
24. Cheyne SM, Chivers DJ, Sugardjito J. 2008. Biology and behavior of reintroduced gibbons. Biodiv Conserv 17: 1741-1751.
25. Colorado Division of Wildlife. 2000. Colorado lynx recovery project 2000 progress report to the U.S. Fish and Wildlife Service. Unpublished report. Denver, CO: Colorado Division of Wildlife.
26. Crews D. 1975. Psychobiology of reptilian reproduction. Science 189: 1059-1065.
27. de Azevedo CS, Young RJ. 2006a. Behavioral responses of captive-born greater rheas Rhea americana Linnaeus (Rheiformes, Rheidea) submitted to antipredator training. Rev Brasil Zool 23: 186-193.
28. de Azevedo CS, Young RJ. 2006b. Shyness and boldness in greater rheas Rhea americana Linnaeus (Rheiformes, Rheidea): the effects of antipredator training on the personality of the birds. Rev Brasil Zool 23: 202-210.
29. Derrickson SR, Snyder NFR. 1992. Potential and limits of captive breeding in parrot conservation. In: Beissinger SR, Snyder NFR, editors. New World parrots in crisis: solutions from conservation biology. Washington, DC: Smithsonian Institution Press. p 133-163.
30. Devineu O, Shenk TM, Doherty PF, Jr., White GC, Kahn RH. 2011. Assessing release protocols for Canada lynx reintroduction in Colorado. J Wildl Manage 75: 623-630.
31. Frankham R. 1995. Conservation genetics. Ann Rev Gen 29: 305-337.
32. Fraser DJ. 2008. How well can captive breeding programs conserve biodiversity? A review of salmonids. Evol Appl 1: 535-586.
33. Fraser D. 2010. Toward a synthesis of conservation and animal welfare science. Anim Welf 19 (2 Sp Iss SI): 121-124.
34. Gerrodette T, Gilmartin WG. 1990. Demographic consequences of changed pupping and hauling sites of the Hawaiian monk seal. Conserv Biol 4: 423-430.
35. Gossow H. 1970. Vergleichende verhaltensstudien an Marderartigen. I. Uber LautauBerungen und zum Beuteurhalten. Zeits Tierpsychol 27: 405-480.
36. Griffin AS, Blumstein DT, Evans CS. 2000. Training captive-bred or translocated animals to avoid predators. Conserv Biol 14: 1317-1326.
37. Griffin AS, Evans CS, Blumstein DT. 2001. Learning specificity in acquired predator recognition. Anim Behav 62: 577-589.
38. Griffith B, Scott JM, Carpenter JW, Reed C. 1989. Translocation as a species conservation tool: status and strategy. Science 345: 447-480.
39. Hutchins M, Kreger MD. 2006. Rhinoceros behavior: implications for captive management and conservation. Int Zoo YB 40: 150-173.
40. IUCN. 1987. Translocation of living organisms: introductions, reintroductions, and restocking. IUCN Position Statement. Gland, Switzerland: IUCN.
41. Jacuart HC, Flinders JT, Coffeen MP, Hassenyager R. 1986. Prescriptive transplanting and monitoring of Utah prairie dogs (Cynomys parvidens) populations. Internal report. Salt Lake City, UT, USA: Utah Division of Wildlife Resources.
42. Kelly GM. 1977. Fisher (Martes pennanti) biology in the White Mountain National Forest and surrounding areas [Ph.D. dissertation]. Amherst, MA: University of Massachusetts.
43. Kleiman DG. 1989. Reintroductions of captive mammals for conservation: guidelines for reintroducing endangered species into the wild. BioScience 39: 152-161.
44. Kleiman DG, Beck BB, Baker AJ, et al. 1990. The conservation program for the golden lion tamarin, Leontopithecus rosalia. Endang Sp Update 8: 82-85.
45. Kleiman DG, Stanley-Price MR, Beck BB. 1994. Criteria for reintroductions. In: Mace GM, Onley PJS, Feistner ATC, editors. Creative conservation. London, UK: Chapman and Hall. p 287-303.
46. Kleiman DG, Reading RP, Miller BJ, et al. 2000. The importance of improving evaluation in conservation. Conserv Biol 14: 1-11.
47. Kraaijeveld-Smit FJJ, Griffiths RA, Moore RD, Beebee TJC. 2006. Captive breeding and the fitness or reintroduced species: a test of the responses to predators in a threatened amphibian. J Appl Ecol 43: 360-365.
48. Linnell JDC, Aanes R, Swenson JE, Odden J, Smith ME. 1997. Translocation of carnivores as a method for managing problem animals: a review. Biodiv Conserv 6: 1245-1257.
49. Lott D. 2002. American bison: a natural history. Berkeley, CA: University of California Press.
50. Macdonald DW, Sidorovich VE, Maran T, Kruuk H. 2002. European mink, Mustela lutreola: analyses for conservation. Oxford, UK: The Darwin Initiative and Wildlife Conservation Research Unit.
51. Maloney RF, McLean IG. 1995. Historical and experimental learned predator recognition in free-living New Zealand robins. Anim Behav 50: 1193-1201.
52. Martin MS. 2009. Applications of mate choice to captive breeding of an endangered species (Brachylagus idahoensis) [Master's thesis]. Portland, OR: Portland State University.
53. Martin M, Shepherdson D. 2012. The role of familiarity and preference on reproductive success in ex-situ conservation breeding programs. Conserv Biol 26: 649-656.
54. Mathews F, Orros M, McLaren G, Gelling M, Foster R. 2005. Keeping fit on the ark: assessing the suitability of captive-bred animals for release. Biol Conserv 121: 569-577.
55. Matipano C. 2004. Post-release ranging behavior of hand-raised black rhinoceros, Diceros bicornis, L. in Matusandona National Park, Zimbabwe with recommendation for management of introduction to the wild. Koedoe 47: 89-101.
56. May RM. 1991. The role of ecological theory in planning the reintroduction of endangered species. Symp Zool Soc Lond 62: 145-163.
57. McDougal PT, Réale D, Sol D, Reader SM. 2006. Wildlife conservation and animal temperament: causes and consequences of evolutionary change for captive, reintroduced, and wild populations. Anim Conserv 9: 39-48.
58. McLean IG, Schmitt NT, Jarman PJ, Duncan C, Wynne CDL. 2000. Learning for life: training marsupials to recognize introduced predators. Behavior 137: 1361-1376.
59. McPhee ME. 2003. Generations in captivity increases behavioral variance: considerations for captive breeding and reintroduction programs. Biol Conserv 115: 71-77.
60. McPhee ME. 2004. Morphological change in wild and captive oldfield mice Peromyscus polionatus subgriseus. J Mammal 85: 1130-1137.
61. McPhee ME, Silverman ED. 2004. Increased behavioral variation and the calculation of release numbers for reintroduction programs. Conserv Biol 18: 705-715.
62. Meehan CL, Mench JA. 2007. The challenge of challenge: can problem solving opportunities enhance animal welfare? Appl Animal Behav Sci 102: 246-261.
63. Miller B, Biggins D, Wemmer C, et al. 1990a. Development of survival skills in captive raised Siberian polecats (Mustela eversmanni) I. Locating Prey. J Ethol 8: 89-94.
64. Miller B, Biggins D, Wemmer C, et al. 1990b. Development of survival skills in captive raised Siberian polecats (Mustela eversmanni) II. Predator avoidance. J Ethol 8: 95-104.
65. Miller B, Biggins D, Hanebury L, Vargas A. 1994. Reintroduction of the black-footed ferret. In: Mace GM, Onley PJS, Feistner ATC, editors. Creative conservation. London, UK: Chapman and Hall. p 455-463.
66. Miller BJ, Reading RP, Forrest S. 1996. Prairie night: black-footed ferrets and the recovery of endangered species. Washington, DC: Smithsonian Press.
67. Miller B, Biggins D, Vargas A, et al. 1998. The captive environment and reintroduction: the black-footed ferret as a case study with comments on other taxa. In: Shepherdson DJ, Mellen JD, Hutchins M, editors. Second nature: environmental enrichment for captive animals. Washington, DC, USA: Smithsonian Institution Press. p 97-112.
68. Miller B, Ralls K, Reading RP, Scott JM, Estes J. 1999. Biological and technical considerations of carnivore translocation: a review. Anim Conserv 2: 59-68.
69. Moodie EM, Chamove AS. 1990. Brief threatening events are beneficial for captive tamarins. Zoo Biol 9: 275-286.
70. Ncube S, Ndagurwa HGT. 2010. Influence of social upbringing on the activity pattern of captive lion Panthera leo cubs: benefits of behavior enrichment. Curr Zool 56: 389-394.
71. Pfaffenberger CJ, Scott JP, Fuller JL, Ginsburg BE, Bielfelt SW. 1976. Guide dogs for the blind: their selection, development, and training. New York: Elsevier.
72. Powell DM, Gartner MC. 2011. Applications of personality to the management and conservation of nonhuman animals. In: Inoue-Murayama M, Kawamura S, Weiss A, editors. From genes to animal behavior: social structures, personalities, comminication by color. Primatology monographs. New York: Springer. p 185-199.
73. Rabin LA. 2003. Maintaining behavioural diversity in captivity for conservation: natural behaviour management. Anim Welf 12: 85-94.
74. Reading RP, Clark TW. 1996. An interdisciplinary examination of carnivore reintroductions. In: Gittleman JL, editor. Carnivore behavior, ecology, and evolution, Vol. II. Ithaca, NY: Cornell University Press. p 296-336.
75. Reading RP, Clark TW, Kellert SR. 1991. Toward an endangered species reintroduction paradigm. Endang Sp Update 8: 1-4.
76. Reading RP, Clark TW, Griffith B. 1997. The influence of valuational and organizational considerations to translocation success. Biol Conserv 79: 217-225.
77. Reading RP, Miller BJ, Stanley-Price M. 1999. Reintroducing animals into the wild: lessons for giant pandas. In: Mainka S, editor. International workshop on the feasibility of giant panda re-introduction, Woolong Nature Reserve, Sichuan, China, September 25-29, 1997. Beijing, China: China Forestry Publishing House. p 18-29; p 146-155 (in Chinese and English).
78. Reading RP, Kleiman DG, Miller BJ. 2004. Conservation and behavior: species reintroductions. In: Bekoff M, editor. Encyclopedia of animal behavior, Vol. 1. Westport, CT: Greenwood Press. p 426-435.
79. Reading RP, Miller BJ, Masching A, Edward R, Phillips M, editors. 2010. Awakening spirits: wolves in the Southern Rockies. Golden, CO: Fulcrum Publishing.
80. Reading RP, Haeffner R, Veer V, Mitchell N. 2011. Reintroduction of Turks and Caicos rock iguana (Cyclura carinata) to Long Cay. In: Soorae PS, editor. Global re-introduction perspectives: 2011. More case studies from around the globe. Abu Dhabi, UAE: IUCN/SSC Re-introduction Specialist Group. p 120-124.
81. Roe JH, Frank MR, Gibson SE, Attum O, Kingsbury BA. 2010. No place like home: an experimental comparison of reintroduction strategies using snakes. J Appl Ecol 47: 1253-1261.
82. Schadweiler JD, Tester JR. 1972. Survival and behavior of hand-reared mallards released into the wild. J Wildl Manage 36: 1118-1127.
83. Shepherdson DJ. 1988. The application of behavioural enrichment in zoos. Primate Rep 22: 35-42.
84. Shepherdson DJ. 1994. The role of environmental enrichment in the captive breeding and reintroduction of endangered species. In: Mace GM, Onley PJS, Feistner ATC, editors. Creative conservation. London, UK: Chapman and Hall. p 167-177.
85. Shepherdson DJ. 1998. Introduction: tracing the path of environmental enrichment in zoos. In: Shepherdson DJ, Mellen JD, Hutchins M, editors. Second nature: environmental enrichment for captive animals. Washington, DC: Smithsonian Institution Press. p 1-12.
86. Shepherdson D, Lewis K, Carlstead K, Bauman J, Perrin N. In press. Individual and environmental factors associated with stereotypic behavior and fecal glucocorticoid metabolite levels in zoo housed polar bears. J Appl Anim Behav.
87. Shier DM. 2004. Social and ecological influences on the survival skills of black-tailed prairie dogs: a role for behavior in conservation [Ph.D. Dissertation]. Davis, CA: University of California at Davis.
88. Shier DM, Owings DH. 2006. Effects of predator training on behavior and post-release survival of captive prairie dogs (Cynomys ludovicianus). Biol Conserv 132: 126-135.
89. Silver R. 1978. The parental behavior of ring doves. Am Sci 66: 209-215.
90. Snyder R. 1977. Putting the wild back into the zoo. Int Zoo News 24: 11-18.
91. Snyder N, Snyder H. 2000. The California condor: a saga of natural history and conservation. San Diego, CA: Academic Press.
92. Snyder NRF, Derrickson SR, Beissinger SR, et al. 1996. Limitations of captive breeding in endangered species recovery. Conserv Biol 10: 338-348.
93. Soorae PS, editor. 2008. Global re-introduction perspectives: re-introduction case-studies from around the globe. Abu Dhabi, UAE: IUCN/SSC Re-introduction Specialist Group.
94. Soorae PS, editor. 2010. Global re-introduction perspectives: 2010. Additional case-studies from around the globe. Abu Dhabi, UAE: IUCN/SSC Re-introduction Specialist Group.
95. Soorae PS, editor. 2011. Global re-introduction perspectives: 2011. More case studies from around the globe. Abu Dhabi, UAE: IUCN/SSC Re-introduction Specialist Group.
96. Stanley-Price MR. 1989. Animal reintroductions: the Arabian Oryx in Oman. New York, NY: Cambridge University Press.
97. Stoinski TS, Beck BB. 2004. Changes in locomotor and foraging skills in captive-born, reintroduced golden lion tamarins (Leontropithecus rosalia rosalia). Am J Primat 62: 1-13.
98. Stoinski TS, Beck BB, Bloomsmith MA, Maple TL. 2003. A behavioral comparison of captive-born, reintroduced golden lion tamarins and their wild-born offspring. Behavior 140: 137-160.
99. Swaisgood RR. 2010. The conservation-welfare nexus in reintroduction programmes: a role for sensory ecology. Anim Welf 19 (2 Sp Iss SI): 125-137.
100. Thorpe SKS, Holder R, Crompton RH. 2009. Orangutans employ unique strategies to control branch flexibility. Proc Nat Acad Sci 106: 12646-12651.
101. Tidwell KS, Shepherdson DJ, Hayes M. In press. Inter-populational variability in evasive behavior in the Oregon spotted frog (Rana pretiosa). J Herp.
102. Utt AC, Harvey NC, Hayes WK, Carter RL. 2008. The effects of rearing method on social behaviors of mentored, captive-reared juvenile California condors. Zoo Biol 27: 1-18.
103. Vargas A. 1994. Ontogeny of the black-footed ferret (Mustela nigripes) and effects of captive-upbringing on predatory behavior and post-release survival [Ph.D. Dissertation]. Laramie, WY: University of Wyoming.
104. Walters JR, Derrickson SR, Fry DM, et al. 2010. Status of the California condor (Gymnogyps californianus) and effort to achieve its recovery. Auk 127: 969-1001.
105. Watters JV, Meehan CL. 2007. Different strokes: can managing behavioral types increase post-release success? Appl Anim Behav Sci 102: 364-379.
106. Watters JV, Powell DM. 2012. Measuring animal personality for use in population management in zoos: suggested methods and rationale. Zoo Biol 31: 1-12.
107. Welbergen PF, Van Dijken R, Scharloo W. 1987. Collation of the courtship behavior of the sympatric species Droshophila melanogaster and Drosophila simulans. Behavior 101: 253-274.
108. Wiley JW, Snyder NFW, Gnam RS. 1992. Reintroduction as a strategy for parrots. In: Beissinger SR, Snyder NFR, editors. New world Parrots in Crisis. Washington, DC: Smithsonian Institution Press. p 165-200.
109. Wolf CM, Griffith B, Reed C, Temple SA. 1996. Avian and mammalian translocations: an update and reanalyzes of 1987 survey data. Conserv Biol 10: 1142-1154.
110. Young RJ. 1997. The importance of food presentation for animal welfare and conservation. Proc Nutr Soc 56: 1095-1104.