Non-invasive monitoring of fecal androgens in spotted hyenas (Crocuta crocuta)

General and Comparative Endocrinology

Volumn 135, Issue 1, 2004, Pages 51-61

  Dloniak, Stephanie M ^a   French, Jeffrey A ^b   Place, Ned J ^c   Weldele, Mary L ^c   Glickman, Stephen E ^c   Holekamp, Kay E ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b UNIVERSITY OF NEBRASKA AT OMAHA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Crocuta crocuta; Fecal androgen metabolites; LHRH challenge; Non invasive; Spotted hyena

Indexed keywords

ANDROGEN; GONADORELIN; TESTOSTERONE;

ANIMAL EXPERIMENT; ARTICLE; CARNIVORA; COMPARATIVE STUDY; CONTROLLED STUDY; DEFECATION; DIET; ENZYME IMMUNOASSAY; FECES ANALYSIS; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYENA; IMMUNOREACTIVITY; LACTATION; MALE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; REPRODUCTION; SOCIAL STATUS; TESTOSTERONE BLOOD LEVEL; VALIDATION PROCESS;

EID: 0344825031     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2003.08.011     Document Type: Article

References (74)

1. Alberts S.C., Sapolsky R.M., Altmann J. Behavioral, endocrine, and immunological correlates of immigration by an aggressive male into a natural primate group. Horm. Behav. 26:1992;167-178.
2. Altmann J. Observational study of behavior: Sampling methods. Behaviour. 49:1974;227-256.
3. Barrett G.M., Shimizu K., Bardi M., Asaba S., Mori A. Endocrine correlates of rank, reproduction, and female-directed aggression in male Japanese macaques (Macaca fuscata). Horm. Behav. 42:2002;85-96.
4. Berger, D.M.P., Frank, L.G., Glickman, S.E., 1992. Unraveling ancient mysteries: biology, behavior, and captive management of the spotted hyena, Crocuta crocuta. In: The Proceedings of a joint meeting of the American Association of Zoo Veterinarians and the American Association of Wildlife Veterinarians, Oakland, California, pp. 139-148.
5. Bernstein I.S., Rose R.M., Gordon C.P. Behavioral and environmental events influencing primate testosterone levels. J. Hum. Evol. 3:1974;517-525.
6. Brockmann D.K., Whitten P.L., Richard A.F., Schneider A. Reproduction in free-ranging male Propithecus verreauxi: the hormonal correlates of mating and aggression. Am. J. Phys. Anthropol. 105:1998;137-151.
7. Boydston E.E., Morelli T.L., Holekamp K.E. Sex differences in territorial behavior exhibited by the spotted hyena (Hyaenidae, Crocuta crocuta). Ethology. 107:2001;369-385.
8. Brown J.L., Wasser S.K., Wildt D.E., Graham L.H. Comparative aspects of steroid hormone metabolism and ovarian activity in felids, measured noninvasively in feces. Biol. Reprod. 51:1994;776-786.
9. Brown J.L., Terio K.A., Graham L.H. Fecal androgen metabolite analysis for noninvasive monitoring of testicular steroidogenic activity in felids. Zoo Biol. 15:1996;425-434.
10. Brown J.L., Wildt D.E., Wielebnowski N., Goodrowe K.L., Graham L.H., Wells S., Howard J.G. Reproductive activity in captive female cheetahs (Acinonyx jubatus) assessed by fecal steroids. J. Reprod. Fertil. 106:1998;337-346.
11. Cavigelli S.A., Pereira M.E. Mating season aggression and fecal testosterone levels in male ring-tailed lemurs (Lemur catta). Horm. Behav. 37:2000;246-255.
12. Creel S., Creel N.M., Mills M.G.L., Monfort S.L. Rank and reproduction in cooperatively breeding African wild dogs: Behavioral and endocrine correlates. Behav. Ecol. 8:1997;298-306.
13. Curtis D., Zaramody A., Di G., Pickard A. Non-invasive monitoring of reproductive status in wild mongoose lemurs (Eulemur mongoz). Reprod. Fert. Dev. 12:2000;21-29.
14. Drea C.M., Weldele M.L., Forger N.G., Coscia E.M., Frank L.G., Licht P., Glickman S.E. Androgens and masculinization of genitalia in the spotted hyaena (Crocuta crocuta). 2. Effects of prenatal anti-androgens. J. Reprod. Fert. 113:1998;117-127.
15. Drea C.M., Place N.J., Weldele M.L., Coscia E.M., Licht P., Glickman S.E. Exposure to naturally circulating androgens during foetal life incurs direct reproductive costs in female spotted hyenas, but is prerequisite for male mating. Proc. Royal Soc. London B. 269:2002;1981-1987.
16. East M.L., Hofer H. Male spotted hyenas (Crocuta crocuta) queue for status in social groups dominated by females. Behav. Ecol. 12:2001;558-568.
17. Engh A.L., Funk S.M., Van Horn R.C., Scribner K.T., Bruford M.W., Libants S., Szykman M., Smale L., Holekamp K.E. Reproductive skew among males in a female-dominated mammalian society. Behav. Ecol. 13:2002;193-200.
18. Farabollini F. Behavioral and endocrine aspects of dominance and submission in male rabbits. Aggress. Behav. 13:1987;247-258.
19. Frank L.G. Social organisation of the spotted hyaena (Crocuta crocuta). II. Dominance and reproduction. Anim. Behav. 35:1986;1510-1527.
20. Frank L.G., Davidson J.M., Smith E.R. Androgen levels in the spotted hyaena Crocuta crocuta: The influence of social factors. J. Zool. London A. 206:1985;525-531.
21. Frank L.G., Glickman S.G., Pouch I. Sexual dimorphism in the spotted hyaena (Crocuta crocuta). J. Zool. 221:1990;308-313.
22. Glickman S.E., Frank L.G., Davidson J.M., Smith E.R., Siiteri P.K. Androstenedione may organize or activate sex-reversed traits in female spotted hyenas. Proc. Natl. Acad. Sci. USA. 84:1987;3444-3447.
23. Glickman S.E., Frank L.G., Pavgi S., Licht P. Hormonal correlates of "masculinization" in female spotted hyaenas (Crocuta crocuta). 1. Infancy to sexual maturity. J. Reprod. Fert. 95:1992;451-462.
24. Glickman S.E., Coscia E.M., Frank L.G., Licht P., Weldele M.L., Drea C.M. Androgens and masculinization of genitalia in spotted hyaena (Crocuta crocuta). 3. Effects of juvenile gonadectomy. J. Reprod. Fert. 113:1998;129-135.
25. Goymann W. Hormone Physiology and Life History of Spotted Hyaenas (Doctoral Dissertation). 2000;Shaker Verlag, Aachen.
26. Goymann W., Möstl E., Van't Hof T., East M.L., Hofer H. Noninvasive fecal monitoring of glucocorticoids in spotted hyenas, Crocuta crocuta. Gen. Comp. Endocrinol. 114:1999;340-348.
27. Goymann W., East M.L., Hofer H. Androgens and the role of female "hyperaggressiveness" in spotted hyenas (Crocuta crocuta). Horm. Behav. 39:2001;83-92.
28. Goymann W., East M.L., Wachter B., Honer O.P., Möstl E., Van't Hof T.J., Hofer H. Social, state-dependent and environmental modulation of faecal corticosteroid levels in free-ranging female spotted hyaenas. Proc. Royal Soc. Lond. B. 268:2001;2453-2459.
29. Goymann W., East M.L., Wachter B., Höner O.P., Möstl E., Hofer H. Social status does not predict corticosteroid levels in postdispersal male spotted hyenas. Horm. Behav. 43:2003;474-479.
30. Hamilton III W.J., Tilson R.L., Frank L.G. Sexual monomorphism in spotted hyaenas, Crocuta crocuta. Ethology. 71:1986;63-73.
31. Hamilton R.A., Stanton P.G., O'Donnell L., Steele V.R., Taggart D.A., Temple-Smith P.D. Determination of seasonality in southern hairy-nosed wombats (Lasiorhinus latifrons) by analysis of fecal androgens. Biol. Reprod. 63:2000;526-531.
32. Henschel J.R., Skinner J.D. Social relationships and dispersal patterns in a clan of spotted hyaenas Crocuta crocuta in the Kruger National Park. S. Afric. J. Zool. 22:1987;18-24.
33. Holekamp K.E., Smale L. Provisioning and food sharing by lactating spotted hyaenas (Crocuta crocuta). Ethology. 86:1990;191-202.
34. Holekamp K.E., Smale L. Dominance acquisition during mammalian social development: the 'inheritance' of maternal rank. Amer. Zool. 31:1991;306-317.
35. Holekamp K.E., Smale L. Dispersal status influences hormones and behavior in the male spotted hyena. Horm. Behav. 33:1998;205-216.
36. Holekamp K.E., Smale L., Simpson H.B., Holekamp N.A. Hormonal influences on natal dispersal in free-living Belding's ground squirrels (Spermophilus beldingi). Horm. Behav. 18:1984;465-483.
37. Holekamp K.E., Smale L., Szykman M. Rank and reproduction in female spotted hyenas. J. Reprod. Fert. 108:1996;229-237.
38. Jainudeen M.R., Katongole C.B., Short R.V. Plasma testosterone levels in relation to musth and sexual activity in the male asiatic elephant, Elephas maximus. J. Reprod. Fert. 29:1972;99-103.
39. Khan M.Z., Altmann J., Isani S.S., Yu J. A matter of time: Evaluating the storage of fecal samples for steroid analysis. Gen. Comp. Endocrinol. 128:2002;57-64.
40. Kruuk H. The Spotted Hyena. 1972;University of Chicago Press, Chicago.
41. Licht P., Frank L.G., Pavgi S., Yalcinkaya T.M., Siiteri P.K., Glickman S.E. Hormonal correlates of "masculinization" in female spotted hyaenas (Crocuta crocuta). 2. Maternal and fetal steroids. J. Reprod. Fert. 95:1992;463-474.
42. Licht P., Hayes T., Tsai P., Cunha G., Kim H., Golbus M., Hayward S., Martin M.C., Jaffe R.B., Glickman S.E. Androgens and masculinization of genitalia in the spotted hyaena (Crocuta crocuta). 1. Urogenital morphology and placental androgen production during fetal life. J. Reprod. Fert. 113:1998;105-116.
43. Lincoln G.A., Guiness F., Short R.V. The way in which testosterone controls the social and sexual behavior of the red deer stag (Cervus elaphus). Horm. Behav. 3:1972;375-396.
44. Lindeque M., Skinner J.D. Fetal androgens and sexual mimicry in spotted hyaenas (Crocuta crocuta). J. Reprod. Fert. 65:1982;405-410.
45. Lunstra D.D., Ford J.J., Echternkamp S.E. Puberty of beef bulls: hormone concentrations, growth, testicular development, sperm production and sexual aggressiveness in bulls of different breeds. J. Anim. Sci. 46:1978;1054-1062.
46. Martin P., Bateson P. Measuring Behaviour: An Introductory Guide. 1988;Cambridge University Press, Cambridge.
47. Matthews L.H. Reproduction in the spotted hyena, Crocuta crocuta (Erxleben). Philos. Trans. R. Soc. Lond. Ser. B. 230:1939;1-78.
48. Möhle U., Heistermann M., Palme R., Hodges J.K. Characterization of urinary and fecal metabolites of testosterone and their measurement for assessing gonadal endocrine function in male nonhuman primates. Gen. Comp. Endocrinol. 129:2002;135-145.
49. Monaghan E.P., Glickman S.E. Hormones and aggressive behavior. Becker J.B., Breedlove S.M., Crews D. Behavioral Endocrinology. 1992;261-285 MIT Press, Cambridge.
50. Monfort S.L., Wasser S.K., Mashburn K.L., Burke M., Brewer B.A., Creel S.R. Steroid metabolism and validation of noninvasive monitoring in the African wild dog (Lycaon pictus). Zoo Biol. 16:1997;533-548.
51. Moss A.M., Clutton-Brock T.H., Monfort S.L. Longitudinal gonadal steroid excretion in free-living male and female meerkats (Suricata suricatta). Gen. Comp. Endocrinol. 122:2001;158-171.
52. Neaves W.B., Griffin J.E., Wilson J.D. Sexual dimorphism of the phallus in spotted hyenas (Crocuta crocuta). J. Reprod. Fert. 59:1980;509-513.
53. Nunes S., Fite J.E., French J.A. Variation in steroid hormones associated with infant care behaviour and experience in male marmosets (Callithrix kuhli). Anim Behav. 60:2000;857-865.
54. Place N.J., Holekamp K.E., Sisk C.L., Weldele M.L., Coscia E.M., Drea C.M., Glickmann S.E. Effects of prenatal androgens on LH secretion and sex steroid concentrations in adult spotted hyenas, Crocuta crocuta. Biol. Reprod. 67:2002;1405-1413.
55. Racey P.A., Skinner J.D. Endocrine aspects of sexual mimicry in spotted hyaenas Crocuta crocuta. J. Zool. Lond. 187:1979;315-326.
56. Rose R.M., Holaday J.W., Bernstein I.S. Plasma testosterone, dominance rank and aggressive behavior in male rhesus monkeys. Nature. 231:1971;366-368.
57. Rose R.M., Gordon T.P., Bernstein I.S. Plasma testosterone levels in the male rhesus: Influence of sexual and social stimuli. Science. 178:1972;643-645.
58. Smale L., Frank L.G., Holekamp K.E. Ontogeny of dominance in free-living spotted hyaenas: juvenile rank relations with adult females and immigrant males. Anim. Behav. 46:1993;467-477.
59. Smale L., Nunes S., Holekamp K.E. Sexually dimorphic dispersal in mammals: Patterns, causes, and consequences. Adv. Study Behav. 26:1997;180-250.
60. Steklis H.D., Brammer G.L., Raleigh M.J., McGuire M.T. Serum testosterone, male dominance, and aggression in captive groups of vervet monkeys (Cercopithecus aethiops sabaeus). Horm. Behav. 19:1985;154-163.
61. Strier K.B., Ziegler T.E., Wittwer D.J. Seasonal and social correlates of fecal testosterone and cortisol levels in wild male muriquis (Brachyteles arachnoides). Horm. Behav. 35:1999;125-134.
62. Sousa M.B., Ziegler T.E. Diurnal variation in the excretion patterns of fecal steroids in common marmoset (Callithrix jacchus) females. Am. J. Primatol. 46:1998;105-117.
63. Szykman, M. Engh, A.L., Van Horn, R.C., Scribner, K.T., Smale, L., Holekamp, K.E. Rare male aggression directed toward females in a female-dominated society: baiting behavior in the spotted hyena. Aggress. Behavior, in press.
64. Terio K.A., Brown J.L., Morelund R., Munson L. Comparison of different drying and storage methods on quantifiable concentrations of fecal steroids in the cheetah. Zoo Biol. 21:2002;215-222.
65. Tilson R.T., Hamilton W.J. Social dominance and feeding patterns of spotted hyaenas. Anim Behav. 32:1984;715-724.
66. Van Horn R.C., McElhinney T.L., Holekamp K.E. Age estimation and dispersal in the spotted hyena (Crocuta crocuta). J. Mamm. 84:2003;1019-1030.
67. van Jaarsveld A.S., Skinner J.D. Adrenocortical responsiveness to immobilization stress in spotted hyenas (Crocuta crocuta). Comp. Biochem. Physiol. A. 103:1992;73-79.
68. Velloso A.L., Wasser S.K., Monfort S.L., Dietz J.M. Longitudinal fecal steroid excretion in maned wolves (Chrysocyon brachyurus). Gen. Comp. Endocrinol. 112:1998;96-107.
69. Walker S.L., Waddell W.T., Goodrowe K.L. Reproductive endocrine patterns in captive female and male red wolves (Canis rufus) assessed by fecal and serum hormone analysis. Zoo Biol. 21:2002;321-335.
70. Wasser S.K., Thomas R., Nair P.P., Guidry C., Southers J., Lucas J., Wildt D.E., Monfort S.L. Effects of dietary fiber on faecal steroid measurements in baboons (Papio cynocephalus cynocephalus). J. Reprod. Fertil. 101:1993;213-220.
71. Wingfield J.C., Ball G.F., Dufty A.M., Hegner R.E., Ramenofsky M. Testosterone and aggression in birds. Am. Sci. 75:1987;602-608.
72. Yalcinkaya T.M., Siiteri P.K., Vigne J., Licht P., Pavgi S., Frank L.G., Glickman S.E. A mechanism for virilization of female spotted hyenas in utero. Science. 260:1993;1929-1931.
73. Zar J.H. Biostatistical Analysis. 1996;Prentice-Hall, Upper Saddle River, NJ.
74. Zumpe D., Michael R.P. Social factors modulate the effects of hormones on sexual and aggressive behavior of macaques. Am. J. Primatol. 38:1996;233-261.