Great ape cognition and captive care: Can cognitive challenges enhance well-being?

Applied Animal Behaviour Science

Volumn 135, Issue 1-2, 2011, Pages 1-12

  Clark, Fay E ^a,b  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b INSTITUTE OF ZOOLOGY   (United Kingdom)

Author keywords

Cognitive challenge; Cognitive enrichment; Great ape; Well being; Zoo

Indexed keywords

BEHAVIORAL ECOLOGY; CAPTIVITY; COGNITION; FUTURE PROSPECT; HOMINID; LEARNING; RESEARCH WORK; ZOO;

ANIMALIA; HOMINIDAE;

EID: 82555187070     PISSN: 01681591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.applanim.2011.10.010     Document Type: Review

References (158)

1. Akers J.S., Schildkraut D.S. Regurgitation/reingestion and coprophagy in captive gorillas. Zoo. Biol. 1985, 4:99-109.
2. Albiach-Serrano A., Call J., Barth J. Great apes track hidden objects after changes in the objects' position and in subject's orientation. Am. J. Primatol. 2010, 72:349-359.
3. Arbib M.A., Liebal K., Pika S. Primate vocalization, gesture, and the evolution of human language. Curr. Anthropol. 2008, 49:1053-1076.
4. Aureli F., de Waal F.B.M. Inhibition of social behaviour in chimpanzees under high-density conditions. Am. J. Primatol. 1997, 41:213-228.
5. Baker K.C. Straw and forage ameliorate abnormal behaviors in adult chimpanzees. Zoo. Biol. 1997, 16:225-236.
6. Baker K.C. Benefits of positive human interaction for socially-housed chimpanzees. Anim. Welf. 2004, 13:239-245.
7. Baker K.C. Chimpanzees in single cages and small social groups: Effects of housing on behavior. Contemp. Top. Lab. Anim. Sci. 1996, 35:71-74.
8. Baker K., Easley S. Regurgitation and reingestion in captive chimpanzees. Appl. Anim. Behav. Sci. 1996, 149:403-415.
9. Baker K.C., Aureli F. Behavioural indicators of anxiety: an empirical test in chimpanzees. Behaviour 1997, 134:1031-1050.
10. Bassett L., Buchanan-Smith H.M. Effects of predictability on the welfare of captive primates. Appl. Anim. Behav. Sci. 2007, 102:223-245.
11. Beck B.B. Animal Tool Behavior: The Use and Manufacture of Tools by Animals 1980, Garland, New York.
12. Bekoff M., Allen C., Burghardt G.M. The Cognitive Animal, Empirical and Theoretical Perspectives 2002, MIT Press, Cambridge.
13. Birkett L.P., Newton-Fisher N.E. How abnormal is the behaviour of captive, zoo-living chimpanzees?. PLoS ONE 2011, 6:e20101.
14. Bloomsmith M.A., Brent L.Y., Schapiro S.J. Guidelines for developing and managing an environmental enrichment program for nonhuman primates. Lab. Anim. Sci. 1991, 41:372-377.
15. Bloomsmith M.A., Lambeth S.P. Effects of predictable versus unpredictable feeding schedules on chimpanzee behavior. Appl. Anim. Behav. Sci. 1995, 44:65-74.
16. Bloomsmith M.A., Lambeth S.P. Videotapes as enrichment for captive chimpanzees (Pan troglodytes). Zoo. Biol. 2000, 19:541-551.
17. Bloomstrand M., Riddle K., Alford P.L., Maple T.L. Objective evaluation of a behavioral enrichment device for captive chimpanzees (Pan troglodytes). Zoo. Biol. 1986, 5:293-300.
18. Boesch C., Boesch H. Optimization of nut cracking with natural hammers by wild chimpanzees. Behaviour 1983, 3-4:265-286.
19. Brent L., Lee D.R., Eichberg J.W. The effects of single caging on chimpanzee behavior. Lab. Anim. Sci. 1989, 39:345-346.
20. Brent L., Lee D.R., Eichberg J.W. Evaluation of chimpanzee enrichment enclosure. J. Med. Primatol. 1991, 20:29-34.
21. Broom D.M. Cognitive ability and awareness in domestic animals and decisions about obligations to animals. Appl. Anim. Behav. Sci. 2010, 126:1-11.
22. Brüne M., Brüne-Cohrs U., McGrew W.C., Preuschoft S. Psychopathology in great apes: concepts, treatment options and possible homologies to human psychiatric disorders. Neurosci. Biobehav. Rev. 2006, 30:1246-1259.
23. Brydges N.M., Braithwaite V.A. Measuring animal welfare: what can cognition contribute?. Annu. Rev. Biomed. Sci. 2008, 10:T91-T103.
24. Byrne R.W., Whiten A. Machiavellian Intelligence: Social Expertise and the Evolution of Intellect in Monkeys, Apes, and Humans 1988, Oxford University Press, New York.
25. Call J. Trapping the minds of apes: causal knowledge and inferential reasoning about object-object interactions. The Mind of the Chimpanzee: Ecological and Experimental Perspectives 2010, 75-86. The University of Chicago Press, Chicago. E.V. Lonsdorf, S.R. Ross, T. Matsuzawa (Eds.).
26. Call J., Tomasello M. Do chimpanzees have a theory of mind? 30 years later. Trends. Cogn. Sci. 2008, 12:187-192.
27. Carlstead K., Shepherdson D. Alleviating stress in zoo animals with environmental enrichment. The Biology of Animal Stress 2000, 337-354. CABI Publishing, New York. G.P. Moberg, J.A. Mench (Eds.).
28. Celli M.L., Tomonaga M., Udono T., Teramoto M., Nagano K. Tool use task as environmental enrichment for captive chimpanzees. Appl. Anim. Behav. Sci. 2003, 81:171-182.
29. Chalmeau R. Do chimpanzees cooperate in a learning task?. Primates 1994, 35:385-392.
30. Chalmeau R., Lardeux K., Brandibas P., Gallo A. Cooperative problem solving by orangutans (Pongo pygmaeus). Int. J. Primatol. 1996, 18:23-32.
31. Chittka L., Jensen K. Animal cognition: concepts from apes to bees. Curr. Biol. 2011, 21:R116-R119.
32. Citrynell P. Cognitive enrichment: problem solving abilities of captive white-bellied spider monkeys. Primate Eye 1998, 6:16-17.
33. Clark F.E. Space to choose: network analysis of social preferences in a captive chimpanzee community, and implications for management. Am. J. Primatol. 2011, 73:748-757.
34. Clark F.E., Fitzpatrick M., Hartley A., King A.J., Lee T., Routh A., Walker S., George K. The relationship between behavior, adrenal activity and environment in zoo-housed Western lowland gorillas (Gorilla gorilla gorilla). Zoo. Biol. 2011, 10.1002/zoo.20396.
35. Clark, F.E., Hitchcock, D., Sainsbury, A.W., Wathes, C.M. In preparation. Can cognitive challenges be enriching? Behavioural responses of zoo-housed chimpanzees (Pan troglodytes) to a novel cognitive challenge device, in preparation.
36. Clay Z., Zuberbühler K. Bonobos extract meaning from call sequences. PLoS ONE 2011, 6:e18786.
37. Coe J., Dykstra G. New and sustainable directions in zoo exhibit design. Wild Mammals in Captivity: Principles and Techniques for Zoo Management 2010, 202-215. University of Chicago Press, Chicago. 2nd ed. G. Kleiman, K.V. Thompson, C. Kirk (Eds.).
38. Cohen J. Boxed about the ears, ape language research field is still standing. Science 2010, 328:38-39.
39. Conlee K.M. Chimpanzees in research and testing worldwide: overview, oversight and applicable laws. Proceedings of the Sixth World Congress on Alternatives and Animal Use in the Life Sciences 2008, 111-118.
40. Csatádi K., Leus K., Pereboom J.J.M. A brief note on the effects of novel enrichment on an unwanted behaviour of captive bonobos. Appl. Anim. Behav. Sci. 2008, 112:201-204.
41. Csikszentmihalyi M. The flow experience and human psychology. Optimal Experience: Psychological Studies of Flow in Consciousness 1988, 15-35. Cambridge University Press, New York. M. Csikszentmihalyi, I.S. Csikszentmihalyi (Eds.).
42. Dawkins M.S. How can we recognise and assess good welfare?. Coping with Challenge: Welfare in Animals Including Humans 2001, 67-76. Dahlem University Press, Berlin. D.M. Broom (Ed.).
43. de Azevedo C.S., Cipreste C.F., Young R.J. Environmental enrichment: a GAP analysis. Appl. Anim. Behav. Sci. 2007, 102:329-343.
44. de Waal F.B.M. Chimpanzee Politics 1982, Cape Publishing, London.
45. de Waal F., Lanting F. Bonobo: The Forgotten Ape 1997, University of California Press, Berkley.
46. de Waal F.B.M., Ferrari P.F. Towards a bottom-up perspective on animal and human cognition. Trends Cogn. Sci. 2010, 14:201-207.
47. Dunbar R.I.M. The social brain hypothesis. Evol. Anthropol. 1998, 6:178-190.
48. Duncan I.J.H., Wood-Gush D.G.M. Thwarting of feeding behaviour in the domestic fowl. Anim. Behav. 1972, 20:444-451.
49. Elder C.M., Menzel C.R. Dissociation of cortisol and behavioral indicators of stress in an orangutan (Pongo pygmaeus) during a computerized task. Primates 2001, 42:345-358.
50. Ernst K., Puppe B., Schon P.C., Manteuffel G. A complex automatic feeding system for pigs aimed to induce successful behavioural coping by cognitive adaptation. Appl. Anim. Behav. Sci. 2005, 91:205-281.
51. Fernie, A., 2008. The creation and implementation of a great ape welfare index. Ph.D. Thesis. School of Animal Studies, University of Queensland, St. Lucia.
52. Fritz J. Resocialization of asocial chimpanzees. The Road to Self-Sustaining Populations 1986, 351-359. Springer-Verlag, New York. K. Benirschke (Ed.).
53. Fritz J., Howell S. Psychological wellness for captive chimpanzees: an evaluative program. Hum. Innov. Alts. 1993, 7:426-433.
54. Gibeault S., MacDonald S.E. Spatial memory and foraging competition in captive western lowland gorillas (Gorilla gorilla gorilla). Primates 2000, 4:147-160.
55. Gilloux I., Gurnell J., Shepherdson D. An enrichment device for great apes. Anim. Welfare 1992, 1:279-289.
56. Goodall J. Tool-using and aimed throwing in a community of free-living chimpanzees. Nature 1964, 201:1264-1266.
57. Hagan K., Broom D.M. Emotional reactions to learning in cattle. Appl. Anim. Behav. Sci. 2004, 85:203-213.
58. Hare B., Melis A.P., Woods V., Hastings S., Wrangham R.W. Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr. Biol. 2007, 17:619-623.
59. Hirata S. A note on the responses of chimpanzees (Pan troglodytes) to live self-images on television monitors. Behav. Process. 2007, 75:85-90.
60. Hopkins W.D., Morris R.D. Handedness in great apes: a review of findings. Int. J. Primatol. 1993, 14:1-25.
61. Hopkins W.D., Phillips K.A., Bania A., Calcutt S.E., Gardner M., Russell J., Schaeffer J., Lonsdorf E.V., Ross S.R., Schapiro S.J. Hand preferences for coordinated bimanual actions in 777 great apes: implications for the evolution of handedness in Hominins. J. Hum. Evol. 2011, 60:605-611.
62. Howell S., Schwandt M., Fritz J., Roeder E., Nelson C. A stereo music system as environmental enrichment for captive chimpanzees. Lab. Anim. 2003, 32:31-36.
63. Inglis I.R., Forkman B., Lazarus J. Free food or earned food? A review and fuzzy model of contrafreeloading. Anim. Behav. 1997, 53:1171-1191.
64. Inoue S., Matsuzawa T. Working memory of numerals in chimpanzees. Curr. Biol. 2007, 17:R1004-R1005.
65. International Species Information System (ISIS), 2011. Accessed at http://www.isis.org/.
66. Iversen I.H., Matsuzawa T. Acquisition of navigation by chimpanzees (Pan troglodytes) in an automated fingermaze task. Anim. Cogn. 2001, 4:179-192.
67. Jones T.A., Chu C.J., Grande L.A., Gregory A.D. Motor skills training enhances lesion-induced structural plasticity in the motor cortex of adult rats. J. Neurosci. 1999, 19:10153-10163.
68. Kirkwood J.K., Hubrecht R. Consciousness, cognition and animal welfare. Anim. Welfare 2001, 10:S5-S17.
69. Köhler W. The Mentality of Apes 1925, Routledge, London.
70. Krief S., Jamart A., Hladik C.M. On the possible adaptive value of coprophagy in free-ranging chimpanzees. Primates 2004, 45:141-145.
71. Kuhlmeier V.A., Boysen S.T., Mukobi K.L. Scale-model comprehension by chimpanzees (Pan troglodytes). J. Comp. Psychol. 1999, 113:396-402.
72. Lambert K.G., Berry A.E., Griffin G., Amory-Meyer E.A., Madonia-Lomas L.F., Love G., Kinsley C.H. Pup exposure differentially enhances foraging ability in primiparous and nulliparous rats. Physiol. Behav. 2005, 85:799-806.
73. Lambeth S.P., Bloomsmith M.A. A grass foraging device for captive chimpanzees (Pan troglodytes). Anim. Welfare 1994, 3:13-24.
74. Langbein J., Siebert K., Nürnberg G. On the use of an automated learning device by group-housed dwarf goats: do goats seek cognitive challenges?. Appl. Anim. Behav. Sci. 2009, 120:150-158.
75. Leavens D.A., Aureli F., Hopkins W.D., Hyatt C.W. Effects of cognitive challenge on self-directed behaviors by chimpanzees (Pan troglodytes). Am. J. Primatol. 2001, 55:1-14.
76. Leighty K.A., Fragazsy D.M. Primates in cyberspace: using interactive computer tasks to study perception and action in nonhuman animals. Anim. Cogn. 2003, 6:137-139.
77. Lonsdorf E.V., Ross S.R., Linick S.A., Milstein M.S., Melber T.N. An experimental, comparative investigation of tool use in chimpanzees and gorillas. Anim. Behav. 2009, 77:1119-1126.
78. Lukas K.E. A review of the nutritional and motivational factors contributing to the performance of regurgitation and reingestion in captive lowland gorillas (Gorilla gorilla gorilla). Appl. Anim. Behav. Sci. 1999, 63:237-249.
79. Macdonald S.E., Agnes M.M. Orangutan (Pongo pygmaeus abelii) spatial memory and behavior in a foraging task. J. Comp. Psychol. 1999, 113:213-217.
80. Maestripieri D., Schino G., Aureli F., Troisi A. A modest proposal: displacement activities as indicators of emotions in primates. Anim. Behav. 1992, 44:967-979.
81. Maki S., Alford P.L., Bloomsmith M.A., Franklin J. Food puzzle device simulating termite fishing for captive chimpanzees (Pan troglodytes). Am. J. Primatol. Suppl. 1989, 1:71-78.
82. Manrique H.M., Gross A.N., Call J. Great apes select tools based on their rigidity. J. Exp. Psychol. Anim. B 2010, 36:409-422.
83. Manteuffel G., Langbein J., Puppe B. From operant learning to cognitive enrichment in farm animal housing: bases and applicability. Anim. Welfare 2009, 18:87-95.
84. Maple T.L., Hoff M.P. Gorilla Behavior 1982, Van Nostrand Reinhold Co., New York.
85. Markowitz H. Behavioral Enrichment in the Zoo 1982, Van Nostrand Reinhold, New York.
86. Markowitz H., Line S. Primate Research Models and Environmental Enrichment 1989, Noyes Publications, New Jersey.
87. Martin-Ordas G., Haun D., Colmenares F., Call J. Keeping track of time: evidence for episodic-like memory in great apes. Anim. Cogn. 2010, 13:331-340.
88. Mason G.J. Stereotypes and suffering. Behav. Process. 1991, 25:103-115.
89. Mason G.J., Rushen J. Stereotypic Animal Behaviour: Fundamentals and Applications to Welfare 2006, CABI Press, Wallingford. second ed.
90. Mason G.J., Clubb R., Latham N., Vickery S. Why and how should we use environmental enrichment to tackle stereotypic behaviour?. Appl. Anim. Behav. Sci. 2007, 102:163-188.
91. Matsuzawa T. The chimpanzee mind: bridging fieldwork and laboratory work. The Mind of the Chimpanzee: Ecological and Experimental Perspectives 2010, 1-22. The University of Chicago Press, Chicago. E.V. Lonsdorf, S.R. Ross, T. Matsuzawa (Eds.).
92. McGrew W.C. Why is ape tool use so confusing?. Comparative Socioecology: The Behavioural Ecology of Humans and Other Mammals 1989, 457-472. Blackwell Scientific Publications, Oxford. V. Standen, R.A. Foley (Eds.).
93. McGrew W.C., Marchant L.F. On which side of the apes? Ethological study of laterality of hand use. Great Ape Societies 1996, 255-272. University of Cambridge Press, Cambridge. W.C. McGrew, L.F. Marchant, T. Nishida (Eds.).
94. Meehan C.L., Mench J.A. The challenge of challenge: can problem solving opportunities enhance animal welfare?. Appl. Anim. Behav. Sci. 2007, 102:246-261.
95. Mellen J., Sevenich MacPhee M. Philosophy of environmental enrichment: past, present, and future. Zoo. Biol. 2001, 20:211-226.
96. Mench J.A., Mason G.J. Behaviour. Anim. Welf. 1997, 127-141. CABI Publishing, Wallingford. M.C. Appleby, B.O. Hughes (Eds.).
97. Mendl M., Burman O.H.P., Parker R.M.A., Paul E.S. Cognitive bias as an indicator of animal emotion and welfare: emerging evidence and underlying mechanisms. Appl. Anim. Behav. Sci. 2009, 118:161-181.
98. Menzel E.W., Premack D., Woodruff G. Map reading by chimpanzees. Folia Primatol. 1978, 29:241-249.
99. Meyer S., Puppe B., Langbein J. Cognitive enrichment in zoo and farm animals - implications for animal behaviour and welfare. Berliner und Münchener Tierärztliche Wochenschrift 2011, 123:446-456.
100. Milgram N.W. Cognitive experience and its effect on age-dependent cognitive decline in beagle dogs. Neurochem. Res. 2003, 28:1677-1682.
101. Milgram N.W., Siwak-Tapp C.T., Araujo J., Head E. Ageing. Res. Rev. 2006, 5:354-369.
102. Morgan K.N., Tromborg C.T. Sources of stress in captivity. Appl. Anim. Behav. Sci. 2007, 102:262-302.
103. Morimura, N., 2003. Cognitive Enrichment in Chimpanzees: An Approach of Welfare Entailing an Animal's Entire Resources. In: Matsuzawa T, Tomonaga M, Tanaka M. (Eds.), 2006 Cognitive development in chimpanzees, Tokyo, Japan, Springer, p. 368-391.
104. Mulcahy N.J., Call J. Apes save tools for future use. Science 2006, 312:1038-1040.
105. Mundy N.I., Ancrenaz M., Wickings J., Lunn P.G. Protein deficiency in a colony of Western lowland gorillas (Gorilla g. gorilla). J. Zoo. Wildl. Med. 1998, 29:261-268.
106. Myers D.G., Diener E. Who is happy?. Psychol. Sci. 1995, 6:10-19.
107. Nakamichi M. Tool-use and tool-making by captive, group-living orangutans (Pongo pygmaeus abelii) at an artificial termite mound. Behav. Process. 2004, 65:87-93.
108. Nash V.J. Tool use by captive chimpanzees at an artificial termite mound. Zoo. Biol. 1982, 1:211-221.
109. Nash L.T., Fritz J., Alford P.L., Brent L. Variables influencing the origins of diverse abnormal behaviors in a large sample of captive chimpanzees (Pan troglodytes). Am. J. Primatol. 1999, 48:15-29.
110. Novak M.A., Suomi S. Psychological well-being of primates in captivity. Am. Psychol. 1988, 43:765-773.
111. Ostrower S., Brent L. Olfactory enrichment for captive chimpanzees: responses to different odors. Lab. Primate Newslett. 2000, 36:8-12.
112. Paquette D., Prescott J. Use of novel objects to enhance environments of captive chimpanzees. Zoo. Biol. 1988, 7:15-23.
113. Parker H.L., Miles H.L., Mitchell R.W. The Mentality of Gorillas and Orangutans 1999, Cambridge University Press, Cambridge.
114. Paul E.S., Harding E.J., Mendl M. Measuring emotional processes in animals: the utility of a cognitive approach. Neurosci. Biobehav. Rev. 2005, 29:469-491.
115. Perlman J.E., Horner V., Bloomsmith M.A., Lambeth S.P., Schapiro S.J. Positive reinforcement training, social learning, and chimpanzee welfare. The Mind of the Chimpanzee: Ecological and Experimental Perspectives 2010, 320-332. The University of Chicago Press, Chicago. E.V. Lonsdorf, S.R. Ross, T. Matsuzawa (Eds.).
116. Pomerantz O., Terkel J. Effects of positive reinforcement training techniques on the psychological welfare of zoo-housed chimpanzees (Pan troglodytes). Am. J. Primatol. 2009, 71:687-695.
117. Poss S.R., Rochat P. Referential understanding of videos in chimpanzees (Pan troglodytes), orangutans (Pongo pygmaeus), and children (Homo sapiens). J. Comp. Psychol. 2003, 117:420-428.
118. Puppe B., Ernst K., Schön P.C., Manteuffel G. Cognitive enrichment affects behavioural reactivity in domestic pigs. Appl. Anim. Behav. Sci. 2007, 105:75-86.
119. Reimers M., Schwarzenberger F., Preuschoft S. Rehabilitation of research chimpanzees: stress and coping after long-term isolation. Horm. Behav. 2007, 51:428-435.
120. Ross S.R. Sequential list-learning by an adolescent lowland gorilla (Gorilla gorilla gorilla) using an infrared touchframe apparatus. Int. Stud. 2009, 10:115-129.
121. Ross S.R. How cognitive studies help shape our obligations for the ethical care of chimpanzees. The Mind of the Chimpanzee: Ecological and Experimental Perspectives 2010, 309-319. The University of Chicago Press, Chicago. E.V. Lonsdorf, S.R. Ross, T. Matsuzawa (Eds.).
122. Rumbaugh D.M., Washburn D., Savage-Rumbaugh E.S. On the care of captive chimpanzees: methods of enrichment. Housing, Care and Psychological Wellbeing of Captive and Laboratory Primates 1989, 357-375. Noyes Publications, New Jersey. E. Segal (Ed.).
123. Russell N. Evidence for the social revolution: trends in great ape behavioral research between 1992 and 2006. Mind Matters: The Wesleyan Journal of Psychology 2008, 3:17-20.
124. Russon A.E., Bard K.A., Taylor Parker S. Reaching into Thought: The Minds of the Great Apes 1998, Cambridge University Press, Cambridge.
125. Russon A.E. Great ape cognitive systems. The Evolution of Great Ape Intelligence 2004, 76-100. Cambridge University Press, Cambridge. A.E. Russon, D.R. Begun (Eds.).
126. Ryan E.B., Proudfoot K.L., Fraser D. The effect of feeding enrichment methods on the behavior of captive Western lowland gorillas. Zoo. Biol 2011, 10.1002/zoo.20403.
127. Sakamaki T. Coprophagy in wild bonobos (Pan paniscus) at Wamba in the Democratic Republic of the Congo: a possibly adaptive strategy?. Primates 2010, 51:87-90.
128. Sambrook T., Buchanan-Smith H. Control and complexity in novel object enrichment. Anim. Welfare 1997, 6:207-216.
129. Shepherdson D.J. Tracing the path of environmental enrichment in zoos. Second Nature: Environmental Enrichment for Captive Animals 1998, 1-14. Smithsonian Institution, Washington. D.J. Shepherdson, J.D. Mellen, M. Hutchins (Eds.).
130. Shettleworth S.J. Cognition, Evolution and Behavior 2010, Oxford University Press, Oxford.
131. Shumaker R.W., Walkup K.R., Beck B.B. Animal Tool Behavior: The Use and Manufacture of Tools by Animals 2011, Johns Hopkins University Press, Baltimore.
132. Shyne A. Meta-analytic review of the effects of enrichment on stereotypic behavior in zoo mammals. Zoo. Biol. 2006, 25:317-337.
133. Slocombe K., Kaller T., Call J., Zuberbühler K. Chimpanzees extract social information from agonistic screams. PLoS ONE 2010, 5:e11473.
134. Struthers E.J., Campbell J. Scent-specific behavioral response to olfactory enrichment in captive chimpanzees (Pan troglodytes). Presented at the XVIth Congress of the International Primatological Society and the XIXth Conference of the American Society of Primatology 1996.
135. Suedmeyer W.K. Hypothyroidism in an Orangutan (Pongo pygmaeus pygmaeus): Clinical Management and Long-term Monitoring 1997, American Association of Zoo Veterinarians, Florida, pp. 71-72.
136. Swaisgood R.R., Shepherdson D.J. Scientific approaches to enrichment and stereotypies in zoo animals: what's been done and where should we go next?. Zoo. Biol. 2005, 24:499-518.
137. Swartz K.B., Himmanen S.A. Individual response strategies in list learning by orangutans. Int. J. Psychol. Psychol. Therapy 2006, 6:233-240.
138. Tarou L.R., Bloomsmith M.A., Hoff M.P., Erwin J.M., Maple T.L. The behavior of aged great apes. Aging in Nonhuman Primates 2002, 209-231. Karger, Basel. J.M. Erwin, P.R. Hof (Eds.).
139. Tarou L.R., Kuhar C.W., Adcock D., Bloomsmith M.A., Maple T.L. Computer-assisted enrichment for zoo-housed orangutans (Pongo pygmaeus). Anim. Welfare 2004, 13:445-453.
140. Tomasello M., Call C.J. Primate Cognition 1997, Oxford University Press, Oxford.
141. Tomasello M., Herrmann E. Ape and human cognition: what's the difference?. Curr. Dir. Psychol. Sci. 2010, 19:3-8.
142. Tsuchida J., Kawasaki K., Sankai T., Kubo N., Keiji T., Koyama T., Makino J., Yoshikawa Y. New type of puzzle-task finger maze learning in Macaca fascicularis. Int. J. Primatol. 2003, 24:261-270.
143. Van Schaik C.P., Deaner R.O., Merrill M.Y. The conditions for tool use in primates: implications for the evolution of material culture. J. Hum. Evol. 1999, 36:719-741.
144. Videan E.N., Fritz J., Howell S., Murphy J. Effects of two types and genres of music on social behaviour in captive chimpanzees (Pan troglodytes). J. Am. Assoc. Lab. Anim. Sci. 2007, 46:66-70.
145. Vlamings P.H.J.M., Uher J., Call J. How the Great apes (Pan troglodytes, Pongo pygmaeus, Pan paniscus, and Gorilla gorilla) perform on the reversed contingency task: the effects of food quantity and food visibility. J. Exp. Psychol. Anim. Behav. Process. 2006, 32:60-70.
146. Walsh S., Bramblett C.A., Alford P.L. A vocabulary of abnormal behaviors in restrictively reared chimpanzees. Am. J. Primatol. 1982, 3:315-319.
147. Washburn D.A., Astur R.S. Exploration of virtual mazes by rhesus monkeys (Macaca mulatta). Anim. Cogn. 2003, 6:161-168.
148. Washburn D.A., Rumbaugh D.M. Testing primates with joystick-based automated apparatus: Lessons from the Language Research Center's Computerized Test System. Behav. Res. Meth. Instr. Comput. 1992, 24:157-164.
149. Wasserman E.A., Zentall T.R. Comparative Cognition: Experimental Explorations of Animal Intelligence 2006, Oxford University Press, London.
150. Wells D.L., Hepper P.G., Coleman D., Challis M.G. A note on the effect of olfactory stimulation on the behaviour and welfare of zoo-housed gorillas. Appl. Anim. Behav. Sci. 2007, 106:155-160.
151. Wemelsfelder F. The concept of animal boredom and its relationship to stereotyped behaviour. Stereotypical Animal Behaviour: Fundamentals and Applications to Welfare 1993, 65-96. CABI Publishing, Wallingford. J.B. Lawrence, J. Rushen (Eds.).
152. Wemelsfelder F., Birke L.I.A. Environmental challenge. Animal Welfare 1997, 35-47. CAB International, Wallingford. M.C. Appleby, B.O. Hughes (Eds.).
153. Whiten A., Goodall J., McGrew W.C., Nishida T., Reynolds V., Sugiyama Y., Tutin C.E.G., Wrangham R.W., Boesch C. Cultures in chimpanzees. Nature 1999, 399:682-685.
154. Wolfe-Coote S. The Laboratory Primate 2005, Elsevier Academic Press, London.
155. Wood-Gush D.G.M., Vestergaard K. Exploratory behavior and the welfare of intensively kept animals. J. Agric. Ethics 1989, 2:161-169.
156. Yamanashi Y., Matsuzawa T. Emotional consequences when chimpanzees (Pan troglodytes) face challenges: individual differences in self-directed behaviours during cognitive tasks. Anim. Welfare 2010, 19:25-30.
157. Yerkes R.M. The Mental Life of Monkeys and Apes 1916, Scholars' Facsimiles & Reprints, New York.
158. Yerkes R.M. Almost Human 1925, Jonathan Cope, London.