Fecal corticosterone concentrations and reproductive success in captive female southern white rhinoceros

General and Comparative Endocrinology

Volumn 171, Issue 3, 2011, Pages 283-292

  Metrione, Lara C ^a,b   Harder, John D ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b WHITE OAK CONSERVATION CENTER   (United States)

Author keywords

Corticosterone; Dominance; Enzyme immunoassay; Reproduction; White rhinoceros

Indexed keywords

CORTICOSTERONE;

AGGRESSION; ANIMAL BEHAVIOR; ANIMAL HOUSING; ARTICLE; BLOOD ANALYSIS; CONTROLLED STUDY; DOMINANCE BEHAVIOR; ENVIRONMENTAL FACTOR; ENZYME IMMUNOASSAY; FECES LEVEL; FEMALE; GROUP STRUCTURE; HORMONE DETERMINATION; HORMONE METABOLISM; HUMAN; NULLIPARA; PRIORITY JOURNAL; REPRODUCTIVE SUCCESS; SEXUAL BEHAVIOR; WHITE RHINOCEROS; WILD ANIMAL;

EID: 79953733653     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2011.02.010     Document Type: Article

References (70)

1. Altmann J. Observational study of behavior: sampling methods. Behaviour 1974, 49:227-265.
2. Anderson S.M., Saviolakis G.A., Bauman R.A., Chu K.Y., Ghosh S., Kant G.J. Effects of chronic stress on food acquisition, plasma hormones, and the estrous cycle of female rats. Physiol. Behav. 1996, 60:325-329.
3. Association of Zoos and Aquariums Rhinoceros Taxon Advisory Group, Rhino Research Council, Rhino Research Masterplan 2009, 2009.
4. T.L. Blanchard, D.D. Varner, J. Schumacher, C.C. Love, S.P. Brinsko, S.L. Rigby, Pregnancy loss, in: E.M. Fathman (Ed.), Manual of Equine Reproduction, Mosby, St. Louis, 2003, pp. 77-91.
5. Boonstra R., Hik D., Singleton G.R., Tinnikov A. The impact of predator-induced stress on the snowshoe hare cycle. Ecol. Monogr. 1998, 79:371-394.
6. Brown J.L., Bellem A.C., Fouraker M., Wildt D.E., Roth T.L. Comparative analysis of gonadal and adrenal activity in the black and white rhinoceros in North America by noninvasive endocrine monitoring. Zoo Biol. 2001, 20:463-486.
7. Carlstead K. Effects of captivity on the behavior of wild mammals. Wild Mammals in Captivity: Principles and Techniques 1996, 317-333. University of Chicago Press, Chicago. D.G. Kleiman, M.E. Allen, K.V. Thompson, S. Lumpkin, H. Harris (Eds.).
8. Carlstead K., Brown J.L. Relationships between patterns of fecal corticoid excretion and behavior, reproduction, and environmental factors in captive black (Diceros bicornis) and white (Ceratotherium simum) rhinoceros. Zoo Biol. 2005, 24:215-232.
9. Carlstead K., Fraser J., Bennett C., Kleiman D.G. Black rhinoceros (Diceros bicornis) in US zoos: II. Behavior, breeding success, and mortality in relation to housing facilities. Zoo Biol. 1999, 18:35-52.
10. Carlstead K., Mellen J., Kleiman D.G. Black rhinoceros (Diceros bicornis) in US zoos: I. Individual behavior profiles and their relationship to breeding success. Zoo Biol. 1999, 18:17-34.
11. Centeno M.L., Sanchez R.L., Cameron J.L., Bethea C.L. Hypothalamic gonadotrophin-releasing hormone expression in female monkeys with different sensitivity to stress. J. Neuroendocrinol. 2007, 19:594-604.
12. Centeno M.L., Sanchez R.L., Reddy A.P., Cameron J.L., Bethea C.L. Corticotropin-releasing hormone and pro-opiomelanocortin gene expression in female monkeys with differences in sensitivity to stress. Neuroendocrinology 2007, 86:277-288.
13. J. Christman, Southern White Rhinoceros Studbook Ceratotherium simum simum, North American Regional Studbook, 2007.
14. J. Christman, Southern White Rhinoceros Studbook Ceratotherium simum simum, North American Regional Studbook, 2009.
15. Creel S., Creel N.M., Mills N.G.L., Monfort S.L. Rank and reproduction in cooperatively breeding African wild dogs: behavioral and endocrine correlates. Behav. Ecol. 1997, 8:298-306.
16. Creel S., Creel N.M., Monfort S.L. Social stress, dominance. Nature 1996, 379:212.
17. Dantzer R., Mormède P. Stress in farm animals: a need for reevaluation. J. Anim. Sci. 1983, 57:6-18.
18. DeVries A.C., Glasper E.R., Detillion C.E. Social modulation of stress responses. Physiol. Behav. 2003, 79:399-407.
19. Dobson H., Ghuman S., Prabhakar S., Smith R. A conceptual model of the influence of stress on female reproduction. Reproduction 2003, 125:151-163.
20. Erickson K., Gabry K.E., Schulkin J., Gold P., Lindell S., Higley J.D., Champoux M., Suomi S.J. Social withdrawal behaviors in nonhuman primates and changes in neuroendocrine and monoamine concentrations during a separation paradigm. Dev. Psychobiol. 2005, 46:331-339.
21. Flint A.P.F., Albon S.D., Loudon A.S.I., Jabbour H.N. Behavioral dominance and corpus luteum function in red deer Cervus elaphus. Horm. Behav. 1997, 31:296-304.
22. Ganslosser U., Brunner C. Influence of food distribution on behavior in captive bongos, Taurotragus euryceros: an experimental investigation. Zoo Biol. 1997, 16:237-245.
23. Graham L.H., Reid K., Webster T., Richards M., Joseph S. Endocrine patterns associated with reproduction in the Nile hippopotamus (Hippopotamus amphibious) as assessed by fecal progestagen analysis. Gen. Comp. Endocrinol. 2002, 128:74-81.
24. Graham L., Schwarzenberger F., Möstl E., Galama W., Savage A. A versatile enzyme immunoassay for the determination of progestogens in feces and serum. Zoo Biol. 2001, 20:227-236.
25. Gutiérrez-Adán A., Crespo-Perez M., Fernandez-Gonzalez R., Ramirez M.A., Moreira P., Pintado B., Lonergan P., Rizos D. Developmental consequences of sexual dimorphism during pre-implantation embryonic development. Reprod. Domest. Anim. 2006, 41:54-62.
26. Hediger H. The problem of food. Wild Animals in Captivity 1964, 120-153. Dover Publications, New York. H. Hediger (Ed.).
27. Hermes R., Hildebrandt T.B., Walzer C., Göritz F., Patton M.L., Silinski S., Anderson M.J., Reid C.E., Wibbelt G., Tomasova K., Schwarzenberger F. The effect of long non-reproductive periods on the genital health in captive female white rhinoceros (Ceratotherium simum simum, C.s. cottoni). Theriogenology 2006, 65:1492-1515.
28. Hermes R., Schwarzenberger F., Walzer C.H., Göritz F., Tomasova K., Patton M., Hildebrandt T. Proceedings of the Fourth International Symposium on Physiology and Behavior of Wild and Zoo Animals 2002, 138. Leibniz Institute for Zoo and Wildlife Research, Berlin. M. Dehnhard, H. Hofer (Eds.).
29. Jarvis J.U.M. Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 1981, 212:571-573.
30. Kimura K., Spate L.D., Green M.P., Roberts R.M. Effects of d-glucose concentration, d-fructose, and inhibitors of enzymes of the pentose phosphate pathway on the development and sex ratio of bovine blastocysts. Mol. Reprod. Dev. 2005, 72:201-207.
31. Krackow S. The developmental asynchrony hypothesis for sex ratio manipulation. J. Theor. Biol. 1995, 176:273-280.
32. Krackow S. Further evaluation of the developmental asynchrony hypothesis of sex ratio variation. Appl. Anim. Behav. Sci. 1997, 51:243-250.
33. Larson M.A., Kimura K., Kubisch H.M., Roberts R.M. Sexual dimorphism among bovine embryos in their ability to make the transition to expanded blastocyst and in the expression of the signaling molecule IFN-τ. Proc. Natl. Acad. Sci. 2001, 98:9677-9682.
34. Li C., Jiang Z., Tang S., Zeng Y. Influence of enclosure size and animal density on fecal cortisol concentration and aggression in Père David's deer stags. Gen. Comp. Endocrinol. 2007, 151:202-209.
35. Linklater W.L. Translocation reverses birth sex ratio bias depending on its timing during gestation: evidence for the action of two sex-allocation mechanisms. Reprod. Fertil. Dev. 2007, 19:831-839.
36. Menargues A., Urios V., Mauri M. Welfare assessment of captive Asian elephants (Elephas maximus) and Indian rhinoceros (Rhinoceros unicornis) using salivary cortisol measurement. Anim. Welfare 2008, 17:305-312.
37. L.C. Metrione, The influences of social behavior on reproduction in captive white rhinoceros (Ceratotherium simum simum), Thesis, Southern Illinois University, Carbondale, 2005.
38. L.C. Metrione, Relationships of social behavior and the captive environment to reproduction in female southern white rhinoceros (Ceratotherium simum simum), Dissertation, The Ohio State University, Columbus, 2010.
39. L.C. Metrione, J.D. Harder, Relationships of social behavior and the captive environment to reproduction in female southern white rhinoceros (Ceratotherium simum simum), in preparation.
40. Metrione L.C., Norton T.M., Beetem D., Penfold L.M. Seasonal reproductive characteristics of female and male Jackson's hartebeest (Alcelaphus buselaphus jacksoni). Theriogenology 2008, 70:871-879.
41. Metrione L.C., Penfold L.M., Waring G.H. Social and spatial relationships in captive southern white rhinoceros (Ceratotherium simum simum). Zoo Biol. 2007, 26:487-502.
42. Moberg G.P. How behavioral stress disrupts the endocrine control of reproduction in domestic animals. J. Dairy Sci. 1991, 74:304-311.
43. Moberg G.P. Biological response to stress: implications for animal welfare. The Biology of Animal Stress Basic Principles and Implications for Animal Welfare 2000, 1-22. CABI Publishing, New York. G.P. Moberg, J.A. Mench (Eds.).
44. Munro C., Stabenfeldt G. Development of a microtitre plate enzyme immunoassay for the determination of progesterone. J. Endocrinol. 1984, 101:41-49.
45. Nelson R.J. Biological rhythms. An Introduction to Behavioral Endocrinology 2005, 587-667. Sinauer Associates, Sunderland. R.J. Nelson (Ed.).
46. Nelson R.J. Stress. An Introduction to Behavioral Endocrinology 2005, 669-720. Sinauer Associates, Sunderland. R.J. Nelson (Ed.).
47. North L.A., Harder J.D. Characterization of the estrous cycle and assessment of reproductive status in Matschie's tree kangaroo (Dendrolagus matschiei) with fecal progestin profiles. Gen. Comp. Endocrinol. 2008, 156:173-180.
48. R.N. Owen-Smith, The behavioural ecology of the white rhinoceros, Dissertation, University of Wisconsin, Madison, 1973.
49. Owen-Smith R.N. The social ethology of the white rhinoceros Ceratotherium simum. Z. Tierpsychol. 1975, 38:337-384.
50. Patton M.L., Swaisgood R.R., Czekala N.M., White A.M., Fetter G.A., Montagne J.P., Rieches R.G., Lance V.A. Reproductive cycle length and pregnancy in the southern white rhinoceros (Ceratotherium simum simum) as determined by fecal pregnane analysis and observations of mating behavior. Zoo Biol. 1999, 18:111-127.
51. Pienaar D. Social organization and behaviour of the white rhinoceros. Proceedings of a Symposium on Rhinos as Game Ranch Animals 1994, 87-92. South African Veterinary Association, Onderstepoort. B.L. Penzhorn, N.J. Kriek (Eds.).
52. Proctor C.M., Freeman E.W., Brown J.L. Influence of dominance status on adrenal activity and ovarian cyclicity status in captive African elephants. Zoo Biol. 2010, 29:168-178.
53. Radcliffe R.W., Czekala N.M., Osofsky S.A. Combined serial ultrasonography and fecal progestin analysis for reproductive evaluation of the female white rhinoceros (Ceratotherium simum simum): preliminary results. Zoo Biol. 1997, 16:445-456.
54. Radcliffe R.W., Eyres A.I., Patton M.L., Czekala N.M., Emslie R.H. Ultrasonographic characterization of ovarian events and fetal gestational parameters in two southern black rhinoceros (Diceros bicornis minor) and correlation to fecal progesterone. Theriogenology 2001, 55:1033-1049.
55. Rivier C., Rivier J., Vale W. Stress-induced inhibition of reproductive functions: role of endogenous corticotrophin-releasing factor. Science 1986, 231:607-609.
56. Roth T.L. A review of the reproductive physiology of rhinoceros species in captivity. Int. Zoo Yearb. 2006, 40:130-143.
57. Roth T.L., O'Brien J.K., McRae M.A., Bellem A.C., Romo S.J., Kroll J.L., Brown J.L. Ultrasound and endocrine evaluation of the ovarian cycle and early pregnancy in the Sumatran rhinoceros, Dicerorhinus sumatrensis. Reproduction 2001, 121:139-149.
58. SAS Institute, SAS 9.1.3, Cary, North Carolina, 2002-2003.
59. Schwarzenberger F., Walzer C., Tomasova K., Vahala J., Meister J., Goodrowe K.L., Zima J., Strauß G., Lynch M. Faecal progesterone metabolite analysis for non-invasive monitoring of reproductive function in the white rhinoceros (Ceratotherium simum). Anim. Reprod. Sci. 1998, 53:173-190.
60. Selye H. A syndrome produced by diverse nocuous agents. Nature 1936, 138:32.
61. Shrader A.M., Owen-Smith N. The role of companionship in the dispersal of white rhinoceros (Ceratotherium simum). Behav. Ecol. Sociobiol. 2002, 52:255-261.
62. Swaisgood R.R., Dickman D.M., White A.M. A captive population in crisis: testing hypotheses for reproductive failure in captive-born southern white rhinoceros females. Biol. Conserv. 2006, 129:468-476.
63. Terio K.A., Marker L., Munson L. Evidence for chronic stress in captive but not free-ranging cheetahs (Acinonyx jubatus) based on adrenal morphology and function. J. Wildl. Dis. 2004, 40:259-266.
64. Thompson K.V. Aggressive behavior and dominance hierarchies in female sable antelope, Hippotragus niger: implications for captive management. Zoo Biol. 1993, 12:189-202.
65. Turner J.W., Tolson P., Hamad N. Remote assessment of stress in white rhinoceros (Ceratotherium simum) and black rhinoceros (Diceros bicornis) by measurement of adrenal steroids in feces. J. Zoo Wildl. Med. 2002, 33:214-221.
66. VanSchaik C.P. The ecology of social relationships amongst female primates. Comparative Socioecology 1989, 195-218. Blackwell Scientific, Oxford. V. Standen, R.A. Foley (Eds.).
67. Wasser S.K., Hunt K.E., Brown J.L., Cooper K., Crockett C.M., Bechert U., Millspaugh J.J., Larson S., Monfort S.L. A generalized fecal glucocorticoid assay for use in a diverse array of nondomestic mammalian and avian species. Gen. Comp. Endocrinol. 2000, 120:260-275.
68. Wielebnowski N.C., Fletchall N., Carlstead K., Busso J.M., Brown J.L. Noninvasive assessment of adrenal activity associated with husbandry and behavioral factors in the North American clouded leopard population. Zoo Biol. 2002, 21:77-98.
69. Williams N.I., Berga S.L., Cameron J.L. Synergism between psychosocial and metabolic stressors: impact on reproduction function in cynomolgus monkeys. Am. J. Physiol. Endocrinol. Metab. 2007, 293:270-276.
70. Wingfield J.C., Raminofsky M. The impact of stress on animal reproductive activities. Stress Physiology in Animals 1999, 130-163. CRC Press LLC, Boca Raton. P.H. Balm (Ed.).