Endocrine and energetic mediation of play behavior in free-living Belding's ground squirrels

Hormones and Behavior

Volumn 36, Issue 2, 1999, Pages 153-165

  Nunes, Scott ^a,b   Muecke, Eva Maria ^a   Anthony, Jessica A ^a   Batterbee, Aaron S ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEBRASKA AT OMAHA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

TESTOSTERONE;

AGGRESSION; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BODY GROWTH; BODY MASS; CONTROLLED STUDY; COPULATION; ENERGY EXPENDITURE; FEMALE; FOOD INTAKE; HORMONE RESPONSE; MALE; NONHUMAN; PHYSICAL DEVELOPMENT; PLAY; PRIORITY JOURNAL; SEX DIFFERENCE; SEXUAL BEHAVIOR; SQUIRREL;

EID: 0032853624     PISSN: 0018506X     EISSN: None     Source Type: Journal    
DOI: 10.1006/hbeh.1999.1538     Document Type: Article

References (86)

1. Abbott, D. H. (1984). Differentiation of sexual behavior in female marmoset monkeys: Effects of neonatal testosterone or a male co-twin. Prog. Brain Res. 61, 349-358.
2. Altmann, J. (1974). Observational study of behavior: Sampling methods. Behaviour 48, 227-267.
3. Armitage, K. B., and Downhower, J. F. (1974). Demography of yellow-bellied marmot populations. Ecology 55, 1233-1244.
4. Arnold, A. P. (1980). Sexual differences in the brain. Am. Scientist 68, 165-173.
5. Arnold, A. P., and Breedlove, S. M. (1985). Organizational and activational effects of sex steroids on vertebrate brain and behavior: A re-analysis. Horm. Behav. 19, 469-498.
6. Bachman, G. C. (1993). The effect of body condition on the trade-off between vigilance and foraging in Belding's ground squirrels. Anim. Behav. 46, 233-244.
7. Baldwin, J. D., and Baldwin, J. I. (1976). Effects of food ecology on social play: A laboratory simulation. Z. Tierpshychol. 40, 1-14.
8. Barber, N. (1991). Play and energy regulation in mammals. O. Rev. Biol. 66, 129-147.
9. Barnes, B. M. (1984). Influence of energy stores on activation of reproductive function in male golden-mantled ground squirrels. J. Comp. Physiol. B154, 421-425.
10. Barrett, L., Dunbar, R. I. M., and Dunbar, P. (1992). Environmental influences on play behaviour in immature gelada baboons. Anim. Behav. 44, 111-115.
11. Beatty, W. W. (1992). Gonadal hormones and sex differences in nonreproductive behaviors. In A. A. Gerall, H. Moltz, and I. L. Ward (Eds.), Handbook of Behavioral Neurobiology, Volume 11, Sexual Differentiation, pp. 85-128. Plenum, New York.
12. Beatty, W. W., Dodge, A. M., Traylor, K. L., and Meaney, M. J. (1981). Temporal boundary of the sensitive period for hormonal organization of social play in juvenile rats. Physiol. Behav. 26, 241-243.
13. Bekoff, M. (1976). Animal play: Problems and perspectives. In P. P. G. Bateson and P. H. Klopfer (Eds.), Perspectives in Ethology, Vol. 2. Plenum, New York.
14. Bekoff, M., and Byers, J. A. (1981). A critical reanalysis of the ontogeny and phylogeny of mammalian social and locomotor play: An ethological hornet's nest. In K. Immelmann, G. W. Barlow, L. Petrinovich, and M. Main (Eds.), Behavioral Development: The Bielefield Interdisciplinary Conference, pp. 296-337. Cambridge Univ. Press, Cambridge.
15. Bekoff, M., and Byers, J. A. (1985). The development of behavior from evolutionary and ecological perspectives in mammals and birds. Evol. Biol. 19, 215-286.
16. Bronson, F. H. (1989). Mammalian Reproductive Biology. Univ. of Chicago Press, Chicago.
17. Byers, J. A., and Walker, C. (1995). Refining the motor training hypothesis for the evolution of play. Am. Nat. 146, 25-40.
18. Byrne, G., and Suomi, S. J. (1995). Development of activity patterns, social interactions, and exploratory behavior in infant tufted capuchins (Cebus apella). Am. J. Priamtol. 35, 255-270.
19. Caro, T. M. (1995). Short-term costs and correlates of play in cheetahs. Anim. Behav. 49, 333-345.
20. Darwin, C. (1871). The Descent of Man and Selection in Relation to Sex. Murray, London.
21. Fagen, R. (1981). Animal Play Behavior. Oxford Univ. Press, New York.
22. Ficken, M. S. (1977). Avian play. The Auk 94, 573-582.
23. Goy, R. W. (1978). Development of play and mounting behavior in female rhesus virilized prenatally with esters of testosterone or dihydrotestosterone. In D. J. Chivers and J. Herbert (Eds.), Recent Advances in Primatology, Vol. 1, pp. 449-462. Academic Press, London.
24. Goy, R. W., and Phoenix, C. H. (1972). The effects of testosterone proprionate administered before birth on the development of behavior in genetic female rhesus monkeys. In C. Sawyer and R. Gorski (Eds.), Steroid Hormones and Brain Function, pp. 193-201. Univ. of California Press, Berkeley.
25. Greenwood, P. J. (1980). Mating systems, philopatry and dispersal in birds and mammals. Anim. Behav. 28, 1140-1162.
26. Haas, C. C., and Jenni, D. A. (1993). Social play among juvenile bighorn sheep: Structure, development, and relationship to adult behavior. Ethology 93, 105-116.
27. Hole, G. (1988). Temporal features of social play in the laboratory rat. Ethology 78, 1-20.
28. Holekamp, K. E. (1983). Proximal Mechanisms of Natal Dispersal in Belding's Ground Squirrels (Spermophilus beldingi beldingi). Ph.D. dissertation. University of California, Berkeley, CA.
29. Holekamp, K. E. (1984a). Natal dispersal in Belding's ground squirrels (Spermophilus beldingi). Behav. Ecol. Sociobiol. 16, 21-30.
30. Holekamp, K. E. (1984b). Dispersal in ground-dwelling sciurids. In J. O. Murie and G. R. Michener (Eds.), The Biology of Ground-Dwelling Sciurids, pp. 297-320. Univ. of Nebraska Press, Lincoln.
31. Holekamp, K. E., and Smale, L. (1998). Behavioral development in the spotted hyena. Bioscience 48, 997-1005.
32. Holekamp, K. E., Smale, L., Simpson, H. B., and Holekamp, N. A. (1984). Hormonal influences on natal dispersal in free-living Belding's ground squirrels (Spermophilus beldingi). Horm. Behav. 18, 465-483.
33. Holmes, W. G. (1994). The development of littermate preferences in juvenile Belding's ground squirrels. Anim. Behav. 48, 1071-1084.
34. Holmes, W. G. (1995). The ontogeny of littermate preferences in juvenile golden-mantled ground squirrels: Effects of rearing and relatedness. Anim. Behav. 50, 309-322.
35. Hrdy, S. B. (1979). Infanticide among animals: A review, classification, and examination of the implications for the reproductive strategies of females. Ethol. Sociobiol. 1, 12-30.
36. Jamieson, S. H., and Armitage, K. B. (1987). Sex differences in the play behavior of yearling yellow-bellied marmots. Ethology 74, 237-253.
37. Jenkins, S. H., and Eshelman, B. D. (1984). Spermophilus beldingi. Mamm. Species 221, 1-8.
38. Kenagy, G. H. (1980). Interrelation of endogenous annual rhythms of reproduction and hibernation in the golden-mantled ground squirrel. J. Comp. Physiol. 135, 333-339.
39. Kilgore, D. L. (1972). Energy Dynamics of the Yellow-Bellied Marmot (Marmota flaviventris): A Hibernator. Ph.D. dissertation, University of Kansas, Lawrence, KS.
40. Martin, P. (1984). The time and energy costs of play behaviour in the cat. Z. Tierpsychol. 64, 298-312.
41. Martin, P., and Bateson, P. (1985). The ontogeny of locomotor play behaviour in the domestic cat. Anim. Behav. 33, 502-510.
42. Martin, P., and Caro, T. M. (1985). On the functions of play and its role in behavioral development. Adv. Study Behav. 15, 59-103.
43. Meaney, M. J. (1988). The sexual differentiation of social play. Trends in Neuroscience 11, 54-58.
44. Meaney, M. J., and McEwen, B. S. (1986). Testosterone implants into the amygdala during the neonatal period masculinize the social play of juvenile female rats. Brain Res. 398, 324-328.
45. Meaney, M. J., and Stewart, J. (1981). Neonatal androgens influence the social play of prepubescent rats. Horm. Behav. 15, 197-213.
46. Meaney, M. J., Stewart, J., and Beatty, W. W. (1985). Sex differences in social play: The socialization of sex roles. Adv. Study Behav. 15, 1-57.
47. McEwen, B. S. (1981). Neural gonadal steroid actions. Science 211, 1301-1311.
48. Meder, A. (1990). Sex differences in the behaviour of immature captive lowland gorillas. Primates 31, 51-63.
49. Meyer, S., and Weber, J.-M. (1996). Ontogeny of dominance in free-living red foxes. Ethology 102, 1008-1019.
50. Morton, M. L., and Gallup, J. S. (1975). Reproductive cycle of the Belding ground squirrel (Spermophilus beldingi beldingi). Great Basin Nat. 35, 427-433.
51. Morton, M. L., Maxwell, C. S., and Wade, C. E. (1974). Body size, body composition, and behavior of juvenile Belding ground squirrels. Great Basin Nat. 34, 121-134.
52. Nunes, S. (1997). Physiological and Ecological Mediation of Natal Dispersal Behavior in Belding's Ground Squirrels. Ph.D. dissertation. Michigan State University, East Lansing, Michigan.
53. Nunes, S., and Holekamp, K. E. (1996). Mass and fat influence the timing of natal dispersal in Belding's ground squirrels. J. Mammal. 77, 807-817.
54. Nunes, S., Zugger, P. A., Engh, A. L., Reinhart, K. O., and Holekmap, K. E. (1997). Why do female Belding's ground squirrels disperse away from food resources? Behav. Ecol. Sociobiol. 40, 199-207.
55. Nunes, S., Ha, C.-D. T., Garrett, P. J., Muecke, E.-M., Smale, L., and Holekmap, K. E. (1998). Body fat and time of year interact to mediate dispersal behaviour in ground squirrels. Anim. Behav. 55, 605-614.
56. Nunes, S., Duniec, T. R., Schweppe, S. A., and Holekamp, K. E. (1999). Energetic and endocrine mediation of natal dispersal behavior in Belding's ground squirrels. Horm. Behav. 35, 113-124.
57. Orgeur, P. (1995). Sexual play behavior in lambs androgenized in utero. Physiol. Behav. 57, 185-187.
58. Ortega, J. C., and Bekoff, M. (1987). Avian play: Comparative evolutionary and developmental trends. The Auk 104, 338-341.
59. Pederson, J. M., Glickman, S. E., Frank, L. G., and Beach, F. A. (1990). Sex differences in the play behavior of immature spotted hyenas, Crocuta crocuta. Horm. Behav. 24, 403-420.
60. Pellis, S. M. (1988). Agnostic versus amicable targets of attack and defense: Consequences for the origin, function, and descriptive classification of play-fighting. Aggr. Behav. 14, 85-104.
61. Pellis, S. M., Field, E. F., Smith, L. K., and Pellis, V. C. (1997). Multiple differences in the play fighting of male and female rats: Implications for the causes and functions of play. Neurosci. Biobehav. Rev. 21, 105-120.
62. Phoenix, C. H., Goy, R. W., Gerall, A. A., and Young, W. C. (1959). Organizing action of prenatally administered testosterone proprionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65, 369-382.
63. Pierce, J. D., Pellis, V. C., Dewsbury, D. A., and Pellis, S. M. (1991). Targets and tactics of agonistic precopulatory behavior in montane and prairie voles: Their relationship to juvenile play fighting. Aggr. Behav. 17, 337-349.
64. Rutberg, A. T., and Keiper, R. R. (1993). Proximate causes of natal dispersal in feral ponies: Some sex differences. Anim. Behav. 46, 969-975.
65. Scott, J. P., Stewart, J. M., and DeGhett, V. J. (1974). Critical periods in the organization of systems. Dev. Psychobiol. 7, 489-513.
66. Sherman, P. W. (1976). Natural Selection among Some Group-Living Organisms. Ph.D. dissertation. University of Michigan, Ann Arbor, MI.
67. Sherman, P. W., and Morton, M. L. (1984). Demography of Belding's ground squirrels. Ecology 65, 1617-1628.
68. Sivy, S. M., and Atrens, D. M. (1992). The energetic costs of rough-and-tumble play in the juvenile rat. Dev. Psychobiol. 25, 137-148.
69. Smith, L. K., Field, E. F., Forgie, M. L., and Pellis, S. M. (1996). Dominance and age-related changes in the play fighting of intact and post-weaning castrated male rats (Rattus norvegicus). Aggr. Behav. 22, 215-226.
70. Smith, P. K. (1982). Does play matter? Functional and evolutionary aspects of animal and human play. Behav. Brain Sci. 5, 138-184.
71. Sokal, R. R., and Rohlf, F. J. (1981). Biometry: The Principles and Practice of Statistics in Biological Research, 2nd ed. Freeman, San Francisco.
72. Svendsen, G. E. (1973). Behavioral and Environmental Factors in the Spatial Distribution and Population Dynamics of a Yellow-Bellied Marmot Population. Ph.D. dissertation, University of Kansas, Lawrence, KS.
73. Thompson, K. V. (1996). Play-partner preferences and the function of social play in infant sable antelope, Hippotragus niger. Anim. Behav. 52, 1143-1155.
74. Thor, D. H., and Holloway, W. R., Jr. (1986). Social play soliciting by male and female juvenile rats: Effects of neonatal androgenization and sex of cagemates. Behav. Neurosci. 2, 275-279.
75. Torran-Allerand, C. D. (1978). Gonadal hormones and brain development: Cellular aspects of sexual differentiation. Am. Zool. 18, 553-565.
76. Trombulak, S. C. (1991). Maternal influence on juvenile growth rates in Belding's ground squirrels (Spermophilus beldingi). Can. J. Zool. 69, 2140-2145.
77. Wade, G. N., and Schneider, J. E. (1992). Metabolic fuels and reproductive function in female mammals. Neurosci. Biobehav. Rev. 16, 235-272.
78. Wade, G. N., Schneider, J. E., and Li, H.-Y. (1996). Control of fertility by metabolic cues. Am. J. Physiol. 270, E1-E19.
79. Wallen, K., Maestripieri, D., and Mann, D. R. (1995). Effects of neonatal testicular suppression with a GnRH antagonist on social behavior in group-living rhesus monkeys. Horm. Behav. 29, 322-337.
80. Ward, I. L., and Stehm, K. (1991). Prenatal stress feminizes juvenile play patterns in male rats. Physiol. Behav. 50, 601-605.
81. Watson, D. M. (1993). The play associations of red-necked wallabies (Macropus furogriseus banksianus) and relation to other social contexts. Ethology 94, 1-20.
82. Watt, B. K., Merrill, A. L., Pecot, R. K., Adams, C. F., Orr, M. L., and Miller, D. F. (1975). Handbook of the Nutritional Contents of Foods. Dover, New York.
83. Wilson, M. E. (1992). Factors determining the onset of puberty. In A. A. Gerall, H. Moltz, and I. L. Ward (Eds.), Handbook of Behavioral Neurobiology, Vol. 11, Sexual Differentiation, pp. 275-312. Plenum, New York.
84. Wolff, J. O. (1993). Why are female small mammals territorial? Oikos 68, 364-370.
85. Zucker, E. L., and Clarke, M. R. (1992). Developmental and comparative aspects of social play of mantled howling monkeys in Costa Rica. Behaviour 123, 144-171.
86. Zucker, I., and Boshes, M. (1982). Circannual body weight rhythms of ground squirrels: Role of gonadal hormones. Am. J. Physiol. 243, R546-R551.