Endocrine and behavioral changes in male African elephants: Linking hormone changes to sexual state and reproductive tactics

Hormones and Behavior

Volumn 54, Issue 4, 2008, Pages 539-548

  Rasmussen, Henrik B ^a,c,d   Ganswindt, Andre ^b,e   Douglas Hamilton, Iain ^c   Vollrath, Fritz ^c,d  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b GERMAN PRIMATE CENTER   (Germany)

^c SAVE THE ELEPHANTS   (Kenya)

^d UNIVERSITY OF OXFORD   (United Kingdom)

^e UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

Androgens; Elephants; Glucocorticoids; Musth; Reproductive tactics; Stress

Indexed keywords

ANDROGEN; GLUCOCORTICOID;

AFRICA; AMPHIBIA; ANIMAL EXPERIMENT; ARTICLE; ELEPHANT; ENDOCRINE SYSTEM; ENVIRONMENTAL FACTOR; HEREDITY; HORMONAL REGULATION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS GONAD SYSTEM; MALE; MAMMAL; MORPHOLOGY; NONHUMAN; PHENOTYPE; PREDATION; PRIORITY JOURNAL; REPRODUCTION; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION;

ANIMALS; BEHAVIOR, ANIMAL; ELEPHANTS; ENDOCRINE SYSTEM; ENVIRONMENT; FECES; FEMALE; GONADAL HORMONES; MALE; SEASONS; SEXUAL BEHAVIOR, ANIMAL; SEXUAL MATURATION; TIME FACTORS;

EID: 50049119648     PISSN: 0018506X     EISSN: 10956867     Source Type: Journal    
DOI: 10.1016/j.yhbeh.2008.05.008     Document Type: Article

References (71)

1. Barnes R.F.W. Mate searching behaviour of the elephant bulls in a semi-arid environment. Anim. Behav. 30 (1982) 1217-1223
2. Brain P.F. Effects of the pituitary-gonadal axis on behaviour. In: Brown K., and Cooper S.J. (Eds). Chemical Influences on Behaviour (1979), Academic Press, London 255-329
3. Brown L.B., Somerville M., Riddle H.S., Keele M., Duer C.K., and Freeman E.W. Comparative endocrinology of testicular, adrenal and thyroid function in captive Asian and African elephant bulls. Gen. Comp. Endocr. 151 (2007) 153-162
4. Carlin J.B., Wolfe R., Brown C.H., and Gelman A. A case study on the choice, interpretation and checking of multilevel models for longitudinal binary outcomes. Biostatistics 2 (2001) 397-416
5. Cooper K.A., Harder J.D., Clawson D.H., Fredrick D.L., Lodge G.A., Peachey H.C., Spellmire T.J., and Winstel D.P. Serum testosterone and musth in captive male African and Asian elephants. Zool. Biol. 9 (1990) 297-306
6. Creel S. Social dominance and stress hormones. TREE 16 (2001) 491-497
7. Douglas-Hamilton, I. 1972. On the ecology and behaviour of the African elephant.: PhD. Thesis. University of Oxford.
8. Eisenberg J.F., McKay G.M., and Jainudeen M.R. Reproductive behaviour of the Asiatic elephant (Elphas maximus maximus L.). Behaviour 38 (1971) 192-225
9. Foley C.A.H., Papageorge S., and Wasser S.K. Noninvasive stress and reproductive measures of social and ecological presurres in free-ranging African elephants. Conserv. Biol. 15 (2001) 1134-1142
10. Ganswindt, A. 2004. Endocrine, physical and behavioural correlates of musth in African Elephants (Loxodonta africana). PhD. Thesis, Munster University, Westfalen.
11. Ganswindt A., Heistermann M., Borragan S., and Hodges J.K. Assessment of testicular endocrine function in captive African elephants by measurements of urinary and fecal androgens. Zool. Biol. 21 (2002) 27-36
12. Ganswindt A., Heistermann M., Palm R., Borragan S., and Hodges J.K. Non-invasive assesment of adrenal function in the male African elephant (Loxodonato africana) and its relation to musth. Gen. Comp. Endocr. 134 (2003) 156-166
13. Ganswindt A., Heistermann M., and Hodges J.K. Physical, physiological and behavioural correlates of musth in captive African elephants (Loxodonta africana). Physiol. Biochem. Zool. 78 (2005) 505-514
14. Ganswindt A., Rasmussen H.B., Heistermann M., and Keith J. The sexually active states of free-ranging male African elephants(Loxodonta africana): defining musth and non-musth using endocrinology, physical signals, and behavior. Horm. Behav. 47 (2005) 83-91
15. Gross M.R. Alternative reproductive strategies and tactics:diversity within sexes. TREE 11 (1996) 92-98
16. Hall-Martin A.J. Plasma testosterone levels in relation to musth in the male African elephant. Koedoe 27 (1984) 147-149
17. Hall-Martin A.J. Role of musth in the reproductive strategy of the African elephants (Loxodonta africana). S. Afr. J. Sci. 83 (1987) 616-620
18. Hollister-Smith J.A., Poole J.H., Archie E.A., Vance E.A., Georgiadis N.J., Moss C.J., and Alberts S.C. Age, musth and paternity success in wild male African elephants, Loxodonta africana. Anim. Behav. 74 (2007) 287-296
19. Howard J., Bush M., de Vos V., and Wildt D.E. Electroejaculation, semen characteristics and serum testosterone concentrations of free-ranging African elephants (Loxodonta africana). J. Reprod. Fertil. 72 (1984) 187-195
20. Hunt K.E., and Wasser S.K. Effect of long-term preservation methods on fecal glucocorticoid concentrations of grizzly bear and African elephant. Physiol. Biochem. Zoo 76 (2003) 918-928
21. Isvaran K. Variation in male mating behaviour within ungulate populations: patterns and processes. Curr. Sci. India 89 (2005) 1192-1199
22. Jainudeen M.R., Katongole C.B., and Short R.V. Plasma testosterone levels in relation to musth and sexual activity in the male Asiatic elephant, Elphas maximus. J. Reprod. Fertil. 29 (1972) 99-103
23. Kenagy G.J., Place N.J., and Veloso C. Relation of glucocorticosteroids and testosterone to the annual cycle of free-living Degus in semiarid central Chile. Gen. Comp. Endocr 115 (1999) 236-243
24. Ketterson E.D., and Nolan V. Hormones and life histories: an interactive approach. Am Nat 140 (1992) 33-62 supplement
25. Knapp R. Endocrine mediation of vertebrate male alternative reproductive tactics: the next generation of studies. Integr. Comp. Biol. 43 (2004) 658-668
26. Knapp R., Hews D.K., Thompson C.W., Ray L.E., and Moore M. Environmental and endocrine correlates of tactic switching by nonterritorial male tree lizards (Urosaurus ornatus). Horm. Behav. 43 (2003) 83-92
27. Laws R.M., Parker I.S.C., and Johnstone R.C.B. Elephants and their Habitat: the Ecology of Elephants in North Bunyoro, Uganda (1975), Clarendon Press, Oxford
28. Leary C.J., Garcia A.M., and Knapp R. Elevated corticosterone levels elicit non-calling mating tactics in male toads independently of changes in circulating androgens. Horm. Behav. 49 (2006) 425-432
29. Leshner A.I., and Moyer J.A. Androgens and agonistic behavior in mice: relevance to aggression and irrelevance to avoidance-of-attack. Physiol. Behav. 15 (1975) 695-699
30. Monder C., Sakai R.R., Miroff Y., Blanchard D.C., and Blanchard R.J. Reciprocal changes in plasma corticosterone and testosterone in stressed male rats maintained in a visible burrow system: evidence for a mediating role of testicular 11beta-hydroxysteroid dehydrogenase. Endocrinology 134 (1994) 1193-1198
31. Moore M. Application of organization-activation theory to alternative reproductive strategies: a review. Horm. Behav. 25 (1991) 154-179
32. Moore M., Hews D.K., and Knapp R. Hormonal control and evolution of alternative male phenotypes: generalizations of models for sexual differentiation. Am. Zool. 38 (1998) 133-151
33. Mooring M.S., Patton M.L., Lance V.A., Hall B.M., Schaad E.W., Fetter G.A., Fortin S.S., and McPeak K.M. Glucocorticoids of bison bulls in relation to social status. Horm. Behav. 49 (2006) 369-375
34. Moss C.J. Oestrus behaviour and female choice in the African elephant. Behaviour 86 (1983) 167-196
35. Moss C.J. Chapter 7: getting to know a population. In: Kangwana K.F. (Ed). Studying elephants (1996), African Wildlife Foundation, Nairobi
36. Moss C.J., and Poole J.H. Relationships and social structure of the African elephants. In: Hinde R.A. (Ed). Primate Social Relationships: An. Integrated Approach (1983), Blachwell Scientific, Oxford 315-325
37. Möstl E., Maggs J.L., Schrötter G., Besenfelder U., and Palm R. Measurement of cortisol metabolites in faeces of ruminants. Vet. Res. Com. 30 (2002) 74-84
38. Ogawa S., Robbins A., Kumar N., Pfaff D.W., Sundaram K., and Bardin C.W. Effects of testosterone and 7a-methyl-19-nortestosterone (MENT) on sexual behaviors in two inbred strains of male mice. Horm. Behav. 30 (1996) 74-84
39. Oliveira R.F., Canario A.V.M., and Grober M.S. Male sexual polymorphism, alternative reproductive tactics, and androgens in combtooth blennies (Pisces:Blenniidae). Horm. Behav. 40 (2001) 266-275
40. Palm R., and Möstl E. Biotin-streptavidin enzyme immunoassay for the determination of oestrogens and androgens in boar faeces. In: Görög S. (Ed). Advances of Steroid Analysis (1993), Akade' miai Kiado', Budapest 111-117
41. Pelletier F., Bauman J., and Festa-Bianchet M. Fecal testosterone in bighorn sheep (Ovis canadensis): behaviour and endocrine correlates. Can. J. Zool. 81 (2003) 1678-1684
42. Poole J.H. Rutting behaviour in the African elephants: the phenomenon of musth. Behaviour 102 (1987) 283-316
43. Poole J.H. Announcing intent: the aggressive state of musth in African elephants. Anim. Behav. 37 (1989) 140-152
44. Poole J.H. Mate guarding, reproductive success and female choice in African elephants. Anim. Behav. 37 (1989) 842-849
45. Poole J.H. Sex differences in the behaviour of African elephants. In: Short R., and Balaban E. (Eds). The Differences Between the Sexes (1994), Cambridge University Press, Cambridge 331-346
46. Poole J.H., and Moss C.J. Musth in the African elephant, Loxodonta africana. Nature 292 (1981) 830-831
47. Poole J.H., Kasman L.H., Ramsay E.C., and Lasley B.L. Musth and urinary testosterone concentrations in the African elephant (Loxodonta africana). J. Reprod. Fertil. 70 (1984) 255-260
48. Rasmussen, H.B. 2005. Reproductive tactics in male African savannah elephants (Loxodonta africana). PhD. Thesis Dept of Zoology Oxford University.
49. Rasmussen L.E.L., and Perrin T.E. Physiological correlates of musth: lipid metabolites and chemical composition of exudates. Physiol. Behav. 67 (1999) 539-549
50. Rasmussen L.E.L., Hall-Martin A.J., and Hess D.L. Chemical profiles of male African elephants, Loxodonta africana: physiological and ecological implications. J. Mammal. 77 (1996) 422-439
51. Rasmussen H.B., Wittemyer G., and Douglas-Hamilton I. Estimating age of immobilized elephants from teeth impressions using dental silicon. Afr. J. Ecol. 43 (2005) 215-219
52. Rasmussen H.B., Wittemyer G., and Douglas-Hamilton I. Predicting time specific variation in demographic processes using remote sensing data. J. Appl. Ecol. 43 (2006) 366-376
53. Rasmussen H.B., Okello J., Wittemyer G., Siegismund H.R., Arctander P., Vollrath F., and Douglas-Hamilton I. Age and tactic related paternity success in male African elephants. Behav. Ecol. 19 (2008) 9-15
54. Rhen T., and Crews D. Variation in reproductive behaviour within a sex: neural systems and endocrine activation. J. Neuroendocrinol. 14 (2002) 517-531
55. Rose R.M., Bernstein I.S., Gordon T.P., and Catlin S.F. Androgens and aggression: a review and recent findings in primates. In: Holloway R.L. (Ed). Primate Aggression, Territoriality, and Xenophobia (1974), Academic Press, New York 275-304
56. Rosner V. The functions of corticosteriod binding globulin and sex hormone binding globulin: recent advances. Endocr. Rev. 11 (1990) 80-91
57. Scanlon T.M., Albertson J.D., Caylor K.K., and Williams C.A. Determining land surface fractional cover from NDVI and rainfall time series for a savanna ecosystem. Remote Sens. Environ. 82 (2002) 376-388
58. Slotow R., van Dyk G., Poole J., Page B., and Klocke A. Older bull elephants control younger males. Nature 408 (2000) 425-426
59. Uglem I., Mayer I., and Rosenquist G. Variation in plasma steroids and reproductive traits in dimorphic males of corkwing wrasse (Symphodus melops L.). Horm. Behav. 41 (2002) 396-404
60. Viau V. Functional cross-talk between the hypothalamic-pituitary-gonadal and -adrenal axes. J. Neuroendocrinol. 14 (2002) 506-513
61. Viau V., and Meaney M.J. Testosterone-dependent variations in plasma and intrapituitary corticosteroid binding globulin and stress hypothalamic-pituitary-adrenal activity in the male rat. J. Endocrinol. 181 (2004) 223-231
62. Virgin C.E., and Sapolsky R.M. Styles of social behaviour and thier endocrine correlates among low-ranking baboons. Am. J. Primatol. 42 (1997) 25-39
63. Wasser S.K., Risler L., and Steiner R.A. Excretory steroids in primate feces over the menstrual cycle and pregnancy. Biol. Reprod. 39 (1988) 862-872
64. Wikelski M., Steiger S.S., Gall B., and Nelson K.N. Sex, drug, and mating role: testosterone-induced phenotype-switching in Galapagos marine iguanas. Behav. Ecol. 16 (2004) 260-268
65. Wingfield J.C. Androgens and mating systems: testosterone-induced polygony in normally monogamous birds. Auk 101 (1984) 665-671
66. Wingfield J.C., Hegner R.E., Dufty A.M., and Ball G.F. The "challenge hypothesis": theoretical implications for patterns of testosterone secretion, mating systems, and breeding strategies. Am. Nat. 136 (1990) 829-846
67. Wingfield J.C., and Sapolsky R.M. Review article: reproduction and resistance to stress when and how. J. Neuroendocrinol. 15 (2003) 711-724
68. Wittemyer G. The elephant population of Samburu and Buffalo Springs National Reserves, Kenya. Afri J Ecol 39 (2001) 357-365
69. Wittemyer G., Daballen D., Rasmussen H.B., Kahindi O., and Douglas-Hamilton I. Demographic status of elephants in the Samburu and Buffalo Springs National Reserves, Kenya. Afr. J. Ecol. 43 (2005) 44-47
70. Wittemyer G., Ganswindt A., and Hodges K. The impact of ecological variability on the reproductive endocrinology of wild female African elephants. Horm. Behav. 51 (2007) 346-354
71. Wittemyer G., Rasmussen H.B., and Douglas-Hamilton I. Breeding phenology in relation to NDVI variability in free-ranging African elephant. Ecography 30 (2007) 42-50