The spotted hyena (Crocuta crocuta) as a model system for study of the evolution of intelligence

Journal of Mammalogy

Volumn 88, Issue 3, 2007, Pages 545-554

  Holekamp, Kay E ^a   Sakai, Sharleen T ^a   Lundrigan, Barbara L ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Crocuta; Hyaena; Hyena; Intelligence; Social cognition

Indexed keywords

COGNITION; EVOLUTION; FITNESS; MAMMAL; PRIMATE; SOCIAL BEHAVIOR;

CARNIVORA; CROCUTA; CROCUTA CROCUTA; HYAENA; HYAENIDAE; MAMMALIA; PRIMATES;

EID: 34347240416     PISSN: 00222372     EISSN: None     Source Type: Journal    
DOI: 10.1644/06-MAMM-S-361R1.1     Document Type: Review

References (116)

1. ADOLPHS, R. 2001. The neurobiology of social cognition. Current Opinion in Neurobiology 11:231-239.
2. AIELLO, L. C., AND P. WHEELER. 1995. The expensive tissue hypothesis: the brain and the digestive system in human and primate evolution. Current Anthropology 36:199-221.
3. AMODIO, D. M., AND C. D. FRITH. 2006. Meeting of the minds: the medial frontal cortex and social cognition. Nature Reviews Neuroscience 7:268-277.
4. ANDELMAN, S. J. 1985. Ecology and reproductive strategies of vervet monkeys (Cercopithecus aethiops) in Amboseli National Park, Kenya. Ph.D. dissertation, University of Washington, Seattle.
5. ASCHOFF, J., B. GUNTHER, AND K. KRAMER. 1971. Energiehaushalt und Temperaturregulation. Urban and Schwarzenberg, Munich, Germany.
6. AURELI, F. 1992. Post-conflict behavior among wild long-tailed macaques. Behavioral Ecology and Sociobiology 31:329-337.
7. AURELI, F., AND F. B. M. DE WAAL. 2000. Natural conflict resolution. University of California Press, Berkeley.
8. AURELI, F., AND C. P. VAN SCHAIK. 1991a. Post-conflict behavior in long-tailed macaques (Macaca fascicularis): I. The social events. Ethology 89:89-100.
9. AURELI, F., AND C. P. VAN SCHAIK. 1991b. Post-conflict behavior in long-tailed macaques (Macaca fascicularis): II. Coping with uncertainty. Ethology 89:101-114.
10. BACHMANN, C., AND H. KUMMER. 1980. Male assessment of female choice in hamadryas baboons. Behavioral Ecology and Sociobiology 6:315-321.
11. BARTON, R. A., AND R. I. M. DUNBAR. 1997. Evolution of the social brain. Pp. 240-263 in Machiavellian intelligence II: extensions and evaluations (A. Whiten and R. W. Byrne, eds.). Cambridge University Press, Cambridge, United Kingdom.
12. BARTON, R. A., AND P. H. HARVEY. 2000. Mosaic evolution of brain structure in mammals Nature 405:1055-1058.
13. BERGMAN, T. J., J. C. BEEHNER, D. L. CHENEY, AND R. M. SEYFARTH. 2003. Hierarchical classification by rank and kinship in baboons. Science 302:1234-1236.
14. BOYDSTON, E. E., K. M. KAPHEIM, R. C. VAN HORN, L. SMALE, AND K. E. HOLEKAMP. 2005. Sexually dimorphic patterns of space use throughout ontogeny in the spotted hyaena (Crocuta crocuta). Journal of Zoology (London) 267:271-281.
15. BOYDSTON, E. E., T. L. MORELLI, AND K. E. HOLEKAMP. 2001. Sex differences in territorial behavior exhibited by the spotted hyena (Crocuta crocuta). Ethology 107:369-385.
16. BROTHERS, L. 1990. The social brain: a project for integrating primate behaviour and neurophysiology in a new domain. Concepts in Neuroscience 1:27-51.
17. BUCHAN, J. C., S. C. ALBERTS, J. B. SILK, AND J. ALTMANN. 2003. True paternal care in a multi-male primate society. Nature 425:179-181.
18. BYRNE, R. W. 1994. The evolution of intelligence. Pp. 223-265 in Behaviour and evolution (P. J. B. Slater and T. R. Halliday, eds.). Cambridge University Press, Cambridge, United Kingdom.
19. BYRNE, R. W., AND A. WHITEN (EDS.) 1988. Machiavellian intelligence. Clarendon Press, Oxford, United Kingdom.
20. CARO, T. 1994. Cheetahs of the Serengeti Plains. University of Chicago Press, Chicago, Illinois.
21. CHAPAIS, B. 1992. The role of alliances in the social inheritance of rank among female primates. Pp. 29-60 in Coalitions and alliances in humans and other animals (A. H. Harcourt and F. B. M. de Waal, eds.). Oxford Science, Oxford, United Kingdom.
22. CHAPAIS, B., AND S. SCHULMAN. 1980. An evolutionary model of female dominance relations in primates. Journal of Theoretical Biology 82:47-89.
23. CHENEY, D. L. 1977. The acquisition of rank and the development of reciprocal alliances among free-ranging immature baboons. Behavioral Ecology and Sociobiology 2:303-318.
24. CHENEY, D. L., AND R. M. SEYFARTH. 1980. Vocal recognition in free-ranging vervet monkeys. Animal Behaviour 28:362-367.
25. CHENEY, D. L., AND R. M. SEYFARTH. 1983. Non-random dispersal in free-ranging vervet monkeys: social and genetic consequences. American Naturalist 122:392-412.
26. CHENEY, D. L., AND R. M. SEYFARTH. 1986. The recognition of social alliances by vervet monkeys. Animal Behaviour 34:1722-1731.
27. CHENEY, D. L., AND R. M. SEYFARTH. 1989. Redirected aggression and reconciliation among vervet monkeys, Cercopithecus aethiops. Behaviour 110:258-275.
28. CHENEY, D. L., AND R. M. SEYFARTH. 1990. How monkeys see the world. University of Chicago Press, Chicago, Illinois.
29. CHENEY, D. L., AND R. M. SEYFARTH. 2003. The structure of social knowledge in monkeys. Pp. 207-229 in Animal social complexity (F. B. M. De Waal and P. L. Tyack, eds.). Harvard University Press, Cambridge, Massachusetts.
30. CHENEY, D. L., R. M. SEYFARTH, AND B. SMUTS. 1986. Social relationships and social cognition in nonhuman primates. Science 234:1361-1366.
31. CORDS, M. 1988. Resolution of aggressive conflicts by immature long-tailed macaques Macaca fascicularis. Animal Behaviour 36:1124-1135.
32. DASSER, V. 1988. A social concept in Java monkeys. Animal Behaviour 36:225-230.
33. DATTA, S. B. 1986. The role of alliances in the acquisition of rank. Pp. 219-225 in Primate ontogeny, cognition and social behavior (J. G. Else and P. C. Lee, eds.). Cambridge University Press, Cambridge, United Kingdom.
34. DEANER, R. O., A. V. KHERA, AND M. L. PLATT. 2005. Monkeys pay per view: adaptive value of social images by rhesus macaques. Current Biology 15:543-548.
35. DE WAAL, F. B. M. 1993. Reconciliation among primates: a review of empirical evidence and unresolved issues. Pp. 11 1-144 in Primate social conflict (W. A. Mason and S. P. Mendoza, eds.). State University of New York Press, New York.
36. DE WAAL, F. B. M., AND P. TYACK (EDS.) 2003. Animal social complexity. University of Chicago Press, Chicago, Illinois.
37. DREA, C. M., AND L. G. FRANK. 2003. The social complexity of spotted hyenas. Pp. 121-148 in Animal social complexity (F. B. M. de Waal and P. L. Tyack, eds.). Harvard University Press, Cambridge, Massachusetts.
38. DREA, C. M., S. N. VIGNIERI, S. B. CUNNINGHAM, AND S. E. GLICKMAN. 2002a. Responses to olfactory stimuli in spotted hyenas (Crocuta crocuta): I. Investigation of environmental odors and the function of rolling. Journal of Comparative Psychology 116:331-341.
39. DREA, C. M., S. N. VIGNIERI, H. S. KIM, M. L. WELDELE, AND S. E. GLICKMAN. 2002b. Responses to olfactory stimuli in spotted hyenas (Crocuta crocuta): II. Discrimination of conspecific scent. Journal of Comparative Psychology 116:342-349.
40. DUNBAR, R. I. M. 1992. Neocortex size as a constraint on group size in primates. Journal of Human Evolution 20:469-493.
41. DUNBAR, R. I. M. 1995. Neocortex size and group size in primates: a test of the hypothesis. Journal of Human Evolution 28:287-296.
42. DUNBAR, R. I. M. 2003. The social brain: mind, language and society in evolutionary perspective. Annual Review of Anthropology 325:163-181.
43. DUNBAR, R. I. M., AND J. BEVER. 1998. Neocortex size predicts group size in carnivores and some insectivores. Ethology 104:695-708.
44. EAST, M. L., AND H. HOFER. 1991a. Loud-calling in a female-dominated mammalian society: I. Structure and composition of whooping bouts of spotted hyaenas, Crocuta crocuta. Animal Behaviour 42:637-649.
45. EAST, M. L., AND H. HOFER. 1991b. Loud-calling in a female-dominated mammalian society: II. Behavioural contexts and functions of whooping of spotted hyaenas, Crocuta crocuta. Animal Behaviour 42:651-669.
46. EAST, M. L., AND H. HOFER. 2001. Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females. Behavioral Ecology 12:558-568.
47. EAST, M. L., H. HOFER, AND W. WICKLER. 1993. The erect 'penis' as a flag of submission in a female-dominated society: greetings in Serengeti spotted hyenas. Behavioral Ecology and Sociobiology 33:355-370.
48. ENGH, A. L., K. ESCH, L. SMALE, AND K. E. HOLEKAMP. 2000. Mechanisms of maternal rank 'inheritance' in the spotted hyaena, Crocuta crocuta. Animal Behaviour 60:323-332.
49. ENGH, A. L, E. R. SIEBERT, D. A. GREENBERG, AND K. E. HOLEKAMP. 2005. Patterns of alliance formation and post-conflict aggression indicate spotted hyenas recognize third party relationships. Animal Behaviour 69:209-217.
50. FRANK, L. G. 1986. Social organization of the spotted hyaena (Crocuta crocuta): II. Dominance and reproduction. Animal Behaviour 35:1510-1527.
51. FRANK, L. G., K. E. HOLEKAMP, AND L. SMALE. 1995. Dominance, demography, and reproductive success of female spotted hyenas. Pp. 364-384 in Serengeti II: conservation, research, and management (A. R. E. Sinclair and P. Arcese, eds.). University of Chicago Press, Chicago, Illinois.
52. GITTLEMAN, J. L. 1989. Carnivore behavior, ecology and evolution. Cornell University Press, Ithaca, New York.
53. GITTLEMAN, J. L. 1996. Carnivore behavior, ecology and evolution II. Cornell University Press, Ithaca, New York.
54. GUGGISBERG, C. A. W. 1962. Simba. Bailey Brothers and Swinfen, London, United Kingdom.
55. HARCOURT, A. H., AND F. B. M. DE WAAL. 1992. Coalitions and alliances in humans and other animals. Pp. 445-471 in Coalitions and alliances in humans and other animals (A. H. Harcourt and F. B. M. de Waal, eds.). Oxford Science, Oxford, United Kingdom.
56. HARVEY, P. H., AND J. R. KREBS. 1990. Comparing brains. Science 249:140-146.
57. HAUSER, M. D., M. K. CHEN, F. CHEN, AND E. CHUANG. 2003. Give unto others: genetically unrelated cotton-top tamarin monkeys preferentially give food to those who altruistically give food back. Proceedings of the Royal Society of London, B. Biological Sciences 270:2363-2370.
58. HENSCHEL, J. R., AND J. D. SKINNER. 1987. Social relationships and dispersal patterns in a clan of spotted hyaenas Crocuta crocuta in the Kruger National Park. South African Journal of Zoology 22: 18-24.
59. HENSCHEL, J. R., AND J. D. SKINNER. 1991. Territorial behavior by a clan of spotted hyenas (Crocuta crocuta). Ethology 88:223-235.
60. HOFER, H., AND M. L. EAST. 1993. The commuting system of Serengeti spotted hyaenas: how a predator copes with migratory prey. II. Intrusion pressure and commuter's space use. Animal Behaviour 46:559-574.
61. HOFER, H., AND M. L. EAST. 2000. Conflict management in female-dominated spotted hyenas. Pp. 232-234 in Natural conflict resolution (F. Aureli and F. B. M. de Waal, eds.). University of California Press, Berkeley.
62. HOFER, H., AND M. L. EAST. 2003. Behavioral processes and costs of co-existence in female spotted hyenas: a life-history perspective. Evolutionary Ecology 17:315-331.
63. HOFER, H., M. L. EAST, I. SAMMANG, AND M. DEHNHARD. 2001. Analysis of volatile compounds in scent-marks of spotted hyenas (Crocuta crocuta) and their possible function in olfactory communication. Chemical Signals in Vertebrates 9:141-148.
64. HOLEKAMP, K. E., E. E. BOYDSTON, AND L. SMALE. 2000. Group travel in social carnivores. Pp. 587-627 in On the move: how and why animals travel in groups (S. Boinksi and P. Garber, eds.). University of Chicago Press, Chicago, Illinois.
65. HOLEKAMP, K. E., et al. 1999. Vocal recognition in the spotted hyaena and its possible implications regarding the evolution of intelligence. Animal Behaviour 58:383-395.
66. HOLEKAMP, K. E., S. M. COOPER, C. I. KATONA, N. A. BERRY, L. G. FRANK, AND L. SMALE. 1997a. Patterns of association among female spotted hyenas (Crocuta crocuta). Journal of Mammalogy 78:55-64.
67. HOLEKAMP, K. E., S. T. SAKAI, AND B. L. LUNDRIGAN. 2007. Social intelligence in the spotted hyena (Crocuta crocuta). Philosophical Transactions of the Royal Society, B. Biological Sciences 362:523-538.
68. HOLEKAMP, K. E., AND L. SMALE. 1991. Rank acquisition during mammalian social development: the 'inheritance' of maternal rank. American Zoologist 31:306-317.
69. HOLEKAMP, K. E., AND L. SMALE. 1993. Ontogeny of dominance in free-living spotted hyaenas: juvenile rank relations with other immature individuals. Animal Behaviour 46:451-466.
70. HOLEKAMP, K. E., L. SMALE, R. BERG, AND S. M. COOPER. 1997b. Hunting rates and hunting success in the spotted hyaena. Journal of Zoology (London) 242:1-15.
71. HOLEKAMP, K. E., L. SMALE, AND M. SZYKMAN. 1996. Rank and reproduction in the female spotted hyaena. Journal of Reproduction and Fertility 108:229-237.
72. HORROCKS, J., AND W. HUNTE. 1983. Maternal rank and offspring rank in vervet monkeys: an appraisal of the mechanisms of rank acquisition. Animal Behaviour 31:772-782.
73. HUMPHREY, N. K. 1976. The social function of intellect. Pp. 303-317 in Growing points in ethology (P. P. G Bateson and R. A. Hinde, eds.). Cambridge University Press, Cambridge, United Kingdom.
74. JENKS, S. M., M. L. WELDELE, L. G. FRANK, AND S. E. GLICKMAN. 1995. Acquisition of matrilineal rank in captive spotted hyaenas - emergence of a natural social system in peer-reared animals and their offspring. Animal Behaviour 50:893-904.
75. JERISON, H. J. 1973. Evolution of the brain and intelligence. Academic Press, New York.
76. JOLLY, A. 1966. Lemur social behavior and primate intelligence. Science 152:501-506.
77. JONES, M. L. 1982. Longevity of captive mammals. Der Zoologische Garten 52:113-128.
78. KAMIL, A. C. 1987. A synthetic approach to the study of animal intelligence. Nebraska Symposium on Motivation 7:257-308.
79. KAPPELER, P. M. 1993. Reconciliation and post-conflict behavior in ringtailed lemurs, Lemur catta and redfronted lemurs, Eulemur fulvus rufus. Animal Behaviour 45:901-915.
80. KOEPFLI, K. P., S. M. JENKS, E. EIZIRIK, T. ZAHIRPOUR, B. VALKENBURGH, AND R. K. WAYNE. 2006. Molecular systematics of the Hyaenidae: relationships of a relictual lineage resolved by a molecular supermatrix. Molecular Phylogeny and Evolution 38:603-620.
81. KRUUK, H. 1972. The spotted hyena: a study of predation and social behavior. University of Chicago Press, Chicago, Illinois.
82. KRUUK, H. 1976. Feeding and social behavior of the striped hyaena (Hyaena vulgaris). East African Wildlife Journal 14:91-111.
83. KUDO, H., AND R. I. M. DUNBAR. 2001. Neocortex size and social network size in primates. Animal Behaviour 62:711-722.
84. KURLAND, J. A. 1977. Kin selection in the Japanese monkey. Contributions to Primatology 12:1-145.
85. LACEY, E. A. 2000. Spatial and social systems of subterranean rodents. Pp. 257-296 in Life underground: the biology of subterranean rodents (E. A. Lacey, J. L. Patton, and G. N. Cameron, eds.). University of Chicago Press, Chicago, Illinois.
86. LEWIS, K. 2001. A comparative study of primate play behaviour: implications for the study of cognition. Folia Primatologica 71:417-421.
87. MACPHAIL, E. M. 1982. Brain and intelligence in vertebrates. Clarendon Press, Oxford, United Kingdom.
88. MILLS, M. G. L. 1990. Kalahari hyaenas: the behavioral ecology of two species. Unwin Hyman, London, United Kingdom.
89. MILTON, K. 1981. Distribution patterns of tropical plant food as an evolutionary stimulus to primate mental development. American Anthropologist 83:534-548.
90. NOË, R., AND P. HAMMERSTEIN. 1994. Biological markets: supply and demand determine the effect of partner choice in cooperation, mutualism, and mating. Behavioral Ecology and Sociobiology 35:1-11.
91. NORTHCUTT, R. G. 2002. Understanding vertebrate brain evolution. Integrative and Comparative Biology 42:743-756.
92. POVINELLI, D. J., AND J. G. H. CANT. 1995. Arboreal clambering and the evolution of self-conception. Quarterly Review of Biology 70:393-421.
93. RICHARDSON, P. R. K. 1988. Mate desertion in response to female promiscuity in the socially monogamous aardwolf, Proteles cristatus. South African Journal of Zoology 23:306-308.
94. SAPOLSKY, R. M. 1993. Endocrinology alfresco: psychoendocrine studies of wild baboons. Recent Progress in Hormone Research 48:437-468.
95. SCHALLER, G. 1972. The Serengeti lion. University of Chicago Press, Chicago, Illinois.
96. SCHINO, G. 2001. Grooming, competition, and social rank among female primates: a meta-analysis. Animal Behaviour 62:265-271.
97. SEYFARTH, R. M. 1980. The distribution of grooming and related behaviors among adult female vervet monkeys. Animal Behaviour 28:798-813.
98. SEYFARTH, R. M., AND D. L. CHENEY. 1984. Grooming, alliances, and reciprocal altruism in vervet monkeys. Nature 308:541-543.
99. SILK, J. B. 1999. Male bonnet macaques use information about third-party rank relationships to recruit allies. Animal Behaviour 58:45-51.
100. SMALE, L., L. G. FRANK, AND K. E. HOLEKAMP. 1993. Ontogeny of dominance in free-living spotted hyenas: juvenile rank relations with adults. Animal Behaviour 46:467-477.
101. SMALE, L., S. NUNES, AND K. E. HOLEKAMP. 1997. Sexually dimorphic dispersal in mammals: patterns, causes and consequences. Advances in the Study of Behavior 26:181-250.
102. SMITH, J. E., S. K. MEMENIS, AND K. E. HOLEKAMP. 2007. Rank-related partner choice in the fission-fusion society of the spotted hyena (Crocuta crocuta). Behavioral Ecology and Sociobiology. 61:753-765.
103. SPRINGER, M. S., W. J. MURPHY, E. EIZIRIK, AND S. O'BRIEN. 2003. Placental mammal diversification and the Cretaceous-Tertiary boundary. Proceedings of the National Academy of Sciences 100:1056-1061.
104. SPRINGER, M. S., W. J. MURPHY, E. EIZIRIK, AND S. O'BRIEN. 2005. Molecular evidence for major placental clades. Pp. 37-49 in The rise of placental mammals (K. D. Rose and J. D. Archibald, eds.). Johns Hopkins University Press, Baltimore, Maryland.
105. SZYKMAN, M., A. L. ENGH, R. C. VAN HORN, S. FUNK, K. T. SCRIBNER, AND K. E. HOLEKAMP. 2001. Association patterns between male and female spotted hyenas reflect male mate choice. Behavioral Ecology and Sociobiology 50:231-238.
106. THEIS, K. R., K. M. GREENE, S. R. BENSON- AMRAM, AND K. E. HOLEKAMP. In press a. Sources of variation in the long-distance vocalizations of spotted hyenas. Behaviour.
107. THEIS, K. R., A. L. HECKLA, J. R. VERGE, AND K. E. HOLEKAMP. In press b. The ontogeny of pasting behavior in free-living spotted hyenas (Crocuta crocuta). In Chemical signals in vertebrates 11 (J. Hurst and R. Beynon, eds.). Springer-Verlag, New York.
108. TILSON, R. T., AND W. J. HAMILTON. 1984. Social dominance and feeding patterns of spotted hyaenas. Animal Behaviour 32: 715-724.
109. TOMASELLO, M., AND J. CALL. 1997. Primate cognition. Oxford University Press, Oxford, United Kingdom.
110. VAN HORN, R. C., S. A. WAHAJ, AND K. E. HOLEKAMP. 2004. Role-reversed nepotistic interactions between sires and offspring in the spotted hyena. Ethology 110:1-14.
111. WAGNER A. P. In press. Hyaena hyaena (Linnaeus). In The mammals of Africa (J. Kingdon, D. Happold, and T. Butynski, eds.). Elsevier Science, London, United Kingdom.
112. WAHAJ, S., K. GUZE, AND K. E. HOLEKAMP. 2001. Reconciliation in the spotted hyena (Crocuta crocuta). Ethology 107:1057-1074.
113. WAHAJ, S. A., ET AL. 2004. Kin discrimination in the spotted hyena (Crocuta crocuta): nepotism among siblings. Behavioral Ecology and Sociobiology 56:237-247.
114. WALTERS, J. 1980. Interventions and the development of dominance relationships in female baboons. Folia Primatologica 34: 61-89.
115. ZABEL, C. J., S. E. GLICKMAN, L. G. FRANK, K. B. WOODMANSEE, AND G. KEPPEL. 1992. Coalition formation in a colony of prepubertal spotted hyaenas. Pp. 113-135 in Coalitions and alliances in humans and other animals (A. H. Harcourt and F. B. M. de Waal, eds.). Oxford Science, Oxford, United Kingdom.
116. ZAJONC, R. B. 1965. Social facilitation. Science 149:269-274.