Ovarian cycle and effect of social changes on adrenal and ovarian function in Pygathrix nemaeus

International Journal of Primatology

Volumn 25, Issue 3, 2004, Pages 689-708

  Heistermann, Michael ^a   Ademmer, Christelle ^a   Kaumanns, Werner ^b  

^a GERMAN PRIMATE CENTER   (Germany)

^b Zoological Garden of Cologne   (Germany)

Author keywords

Douc langur; Fecal hormones; Ovarian cycle; Pygathrix nemaeus; Stress

Indexed keywords

CAPTIVE BREEDING; ENDANGERED SPECIES; PRIMATE; SOCIAL CHANGE; STRESS;

PRIMATES; PYGATHRIX; PYGATHRIX NEMAEUS; VERTEBRATA;

EID: 3442881438     PISSN: 01640291     EISSN: None     Source Type: Journal    
DOI: 10.1023/B:IJOP.0000023581.17889.0f     Document Type: Article

References (56)

1. Abbott, D. H. (1991). The social control of fertility. In Box, H. O. (ed.), Primate Responses to Environmental Change, Chapman and Hall, London, pp. 75-89.
2. Abbott, K. M., Harvey, N. C., Czekala, N. M., Fetter, A., and McGeehan, L. (1999). Hormonal correlates of reproductive behavior in captive douc langurs (Pygathrix nemaeus nemaeus). Am. J. Primatol. 49: 28.
3. Brockman, D. K., and Lippold, L. K. (1975). Gestation and birth of a douc langur, Pygathrix n. nemaeus, at San Diego Zoo. Int. Zoo Yb. 15: 126-129.
4. Cameron, J. L. (1997). Stress and behaviorally induced reproductive dysfunction in primates. Semin. Reprod. Endocrinol. 15: 37-45.
5. Carosi, M., Heistermann, M., and Visalberghi, E. (1999). Display of proceptive behaviors in relation to urinary and fecal progestin levels over the ovarian cycle in female tufted capuchin monkeys. Horm. Behav. 36: 252-265.
6. Clarke, A. S., Czekala, N. M., and Lindburg, D. G. (1995). Behavioral and adrenocortical responses of male cynomolgus and lion-tailed macaques to social stimulation and group formation. Primates 36: 41-56.
7. Curtis, D. J., Zaramody, A., Green, D. I., and Pickard, A. R. (2000). Non-invasive monitoring of reproductive status in wild mongoose lemurs (Eulemur mongoz). Reprod. Fertil. Dev. 12: 21-29.
8. Czekala, N. M., Hodges, J. K., and Lasley, B. L. (1981). Pregnancy monitoring in diverse primate species by estrogen and bioactive luteinizing hormone determinations in small volumes of urine. J. Med. Primatol. 10: 1-15.
9. Czekala, N. M., Reichard, T., and Lasley, B. L. (1991). Assessment of luteal competency by urinary hormone evaluation in the captive female gorilla. Am. J. Primatol. 24: 283-288.
10. Czekala, N. M., Roser, J. F., Mortensen, R. B., Reichard, T., and Lasley, B. L. (1988). Urinary hormone analysis as a diagnostic tool to evaluate the ovarian function of the gorilla (Gorilla gorilla). J. Reprod. Fertil. 82: 255-261.
11. Dailey, R. A., and Neill, J. D. (1981). Seasonal variation of reproductive hormones of rhesus monkeys: Anovulatory and short luteal phase menstrual cycles. Biol. Reprod. 25: 560-567.
12. Ferin, M. (1999). Stress and the reproductive cycle. J. Clin. Endocrinol. Metab. 84: 1768-1774.
13. Fieβ, M., Heistermann, M., and Hodges, J. K. (1999). Patterns of urinary and fecal steroid excretion during the ovarian cycle and pregnancy in the African elephant (Loxodonta africana). Gen. Comp. Endocrinol. 115: 76-89.
14. Fooden, J. (1996). Zoogeography of Vietnamese primates. Int. J. Primatol. 17: 845-899.
15. Ganswindt, A., Palme, R., Heistermann, M., Borragan, S., and Hodges, J. K. (2003). Non-invasive assessment of adrenocortical function in the male African elephant (Loxodonta africana) and its relation to musth. Gen. Comp. Endocrinol. 134:156-166.
16. Gerber, P., Moisson, P., and Heistermann, M. (2004). Urinary progestogen and estrogen excretion during pregnancy in Eulemur macaco flavifrons, E. rubriventer, and Hapalemur griseus occidentalis. Int. J. Primatol. 25: 449-463.
17. Gonzales, C. A., Hennessy, M. B., and Levine, S. (1981). Subspecies differences in hormonal and behavioral responses to group formation in squirrel monkeys. Am. J. Primatol. 1: 439-452.
18. Goo, G. P., and Sassenrath, E. N. (1980). Persistent adrenocortical activation in female rhesus monkeys after new breeding group formation. J. Med. Primatol. 9: 325-334.
19. Gower, D. B., and Honour, J. W. (1984). Part 1: Steroid catabolism and urinary excretion. Part 2: Biliary excretion and enterohepatic circulation. In Makin, H. J. L. (ed.), Steroid Biochemistry. Blackwell Scientific Publications, Oxford, pp. 349-407.
20. Gust, D. A., Gordon, T. P., Wilson, M. F., Ahmed-Ansari, A., Brodie, A. R., and McClure, H. M. (1991). Formation of a new social group of unfamiliar female rhesus monkeys affects the immune and pituitary adrenocortical systems. Brain Behav. Immun. 5: 296-307.
21. Hagino, N. (1972). the effect of synthetic corticosteroids on ovarian function in the baboon. J. Clin. Endocrinol. Metab. 35: 716-721.
22. Hama, N., Han Jun, Q., Bo, D., Yasuda, S., Murata, K., Wan Hua, X., and Gondo, M. (1997). Reproduction in a pair of golden monkeys, Pygathrix (Rhinopithecus) roxellana, at Kobe Oji Zoo. Int. Zoo Yb. 35: 266-271.
23. Hayashi, K. T., and Moberg, G. P. (1990). Influence of the hypothalamic-pituitary-adrenal axis on the menstrual cycle and pituitary responsiveness to estradiol in the female rhesus monkey (Macaca mulatta). Biol. Reprod. 42: 260-265.
24. He, Y., Pei, Y., and Ji, W. (2001). Changes of urinary steroid conjugates and gonadotropin excretion in the menstrual cycle and pregnancy in the Yunnan snub-nosed monkey (Rhinopithecus bieti). Am. J. Primatol. 55: 223-232.
25. Heistermann, M., Finke, M., and Hodges, J. K. (1995a). Assessment of female reproductive status in captive-housed Hanuman langurs (Presbytis entellus) by measurement of urinary and fecal steroid excretion patterns. Am. J. Primatol. 37: 275-284.
26. Heistermann, M., Möhle, U., Vervaecke, H., van Elsacker, L., and Hodges, J. K. (1996). Application of urinary and fecal steroid measurements for monitoring ovarian function and pregnancy in the bonobo (Pan paniscus) and evaluation of perineal swelling patterns to endocrine events. Biol. Reprod. 55: 844-853.
27. Heistermann, M., Möstl, E., and Hodges, J. K. (1995b). Non-invasive endocrine monitoring of female reproductive status: Methods and applications to captive breeding and conservation of exotic species. In Gansloßer, U., Hodges, J. K., and Kaumanns, W. (eds.), Research and Captive Propagation, Filander Verlag, Fürth, pp. 36-48.
28. Heistermann, M., Uhrigshardt, J., Husung, A., Kaumanns, W., and Hodges, J. K. (2001). Measurement of faecal steroid metabolites in the lion-tailed macaque (Macaca silenus): A non-invasive tool for assessing female ovarian function. Primate Rep. 59: 27-42.
29. Hodges, J. K., Heistermann, M., Beard, A., and van Aarde, R. J. (1997). Concentrations of progesterone and the 5α-reduced progestins, 5α-pregnane-3,20-dione and 3α-hydroxy-5α- pregnan-20-one, in luteal tissue and circulating blood and their relationship to luteal function in the African elephant, Loxodonta africana. Biol. Reprod. 556: 640-646.
30. Janssen, D. L. (1994). Morbidity and mortality of douc langurs (Pygathrix nemaeus) at the San Diego Zoo. Proc. Am. Assoc. Zoo Veterin. Pittsburgh. 221-226.
31. Ji, W., Rujin, Z., Enyuan, S., Hongwu, Z., Shangchuan, Y., and Baoping, T. (1998). Maintenance and breeding of Yunnan snub-nosed monkeys (Rhinopithecus bieti) in captivity. In Jablonski, N. G. (ed.), Recent Advances in Human Biology, Vol. 4: The Natural History of the Doucs and Snub-Nosed Monkeys, World Scientific, Singapore, pp. 323-336.
32. Keverne, E. B., Meller, R. E., and Eberhardt, J. A. (1982). Dominance and subordination: concepts or physiological states? In Chiarelli, O. (ed), Advanced Views in Primate Biology, Springer-Verlag, New York, pp. 81-94.
33. Kirkpatrick, R. C. (1998). Ecology and behavior in snub-nosed and douc langurs. In Jablonski, N. G. (ed.), Recent Advances in Human Biology, Vol. 4: The Natural History of the Doucs and Snub-Nosed Monkeys, World Scientific, Singapore, pp. 155-190.
34. Klumpe, K. (2001). Nahrungsaufnahme des Kleideraffen (Pygathrix n. nemaeus, LINNAEUS 1771) in menschlicher Obhut, Diploma Thesis, University of Potsdam.
35. Lippold, L. K. (1977): The douc langur: A time for conservation. In Prince Rainier III, and Bourne, G. H. (eds.), Primate Conservation, Academic Press, New York, pp. 513-538.
36. Lippold, L. K. (1981). Monitoring female reproductive status in the douc langur, Pygathrix nemaeus, at San Diego Zoo. Int. Zoo Yb. 21: 184-187.
37. Lippold, L. K. (1989). Reproduction and survivorship in douc langurs, Pygathrix nemaeus, in zoos. Int. Zoo Yb. 28: 252-255.
38. Lippold, L. K., and Than, V. N. (1998). Primate conservation in Vietnam. In Jablonski, N. G. (ed.), Recent Advances in Human Biology, Vol. 4: The Natural History of the Doucs and Snub-Nosed Monkeys, World Scientific, Singapore, pp. 293-300.
39. Mori, U., and Dunbar, R. I. M. (1985). Changes in the reproductive constitution of female gelada baboons following the takeover of one-male units. Z. Tierpsychol. 67: 215-224.
40. Orstead, K. M., Hess, D. L., and Spies, H. G. (1984). Opiatergic inhibition of pulasatile luteinizing hormone release during the menstrual cycle of the rhesus macaque. Proc. Soc. Exp. Biol. Med. 184: 312-319.
41. Ostner, J., and Heistermann, M. (2003). Endocrine characterization of female reproductive status in wild redfronted lemurs (Eulemur fulvus rufus). Gen. Comp. Endocrinol. 131: 274-283.
42. Roos, C., and Nadler, T. (2001). Molecular evolution of the douc langurs. Zool. Garten N.F. 71: 1-6.
43. Ruempler, U. (1998). Husbandry and breeding of Douc langurs, Pygathrix nemaeus nemaeus, at Cologne Zoo. Int. Zoo Yb. 36: 73-81.
44. Sapolsky, R. (1982). The endocrine stress-responce and social status in the wild baboon. Horm. Behav. 16: 279-292.
45. Schwarzenberger, F., Möstl, E., Palme, R., and Bamberg, E. (1996). Fecal steroid analysis for monitoring of reproductive status in farm, wild and zoo animals. Anim. Reprod. Sci. 42: 515-526.
46. Streicher, U. (1999). Health problems in confiscated douc langurs (Pygathrix sp.). EPRC-Newslett. 4: 20-24.
47. Timmins, R. J., and Duckworth, J. W. (1999). Status and conservation of douc langurs (Pygathrix nemaeus) in Laos. Int. J. Primatol. 20: 469-489.
48. Whitten, P. L., Brockman, D. K., and Stavisky, R. C. (1998a). Recent advances in noninvasive techniques to monitor hormone-behavior interactions. Ybk. Phys. Anthropol. 41: 1-23.
49. Whitten, P. L., Stavisky, R., Aurelli, F. and Russel, E. (1998b). Response of fecal cortisol to stress in captive chimpanzees (Pan troglodytes). Am. J. Primatol. 44: 57-69.
50. Williams, N. I., Caston-Balderrama, A. L., Helmreich, D. L., Parfitt, D. B., Nosbisch, C., and Cameron, J. L. (2001). Longitudinal changes in reproductive hormones and menstrual cyclicity in cynomolgus monkeys during strenous exercise training: Abrupt transition to exercise-induced amenorrhea. Endocrinology 142: 2381-2389.
51. Xiao, E., and Ferin, M. (1997). Stress-related disturbances of the menstrual cycle. Ann. Med. 29: 215-219.
52. Xiao, E., Xia-Zhang, L., Barth, A., Zhu, J., and Ferin, M. (1998). Stress and the menstrual cycle: Relevenace of cycle quality in the short- and long-term response to a 5-day endotoxin challenge during the follicular phase in the rhesus monkey. J. Clin. Endocrinol. Metab. 83: 2454-2460.
53. Xiao, E., Xia-Zhang, L., and Ferin, M. (2002). Inadequate luteal function is the initial clinical cyclic defect in a 12-day stress model that includes a psychogenic component in the rhesus monkey. J. Clin. Endocrinol. Metab. 87: 2232-2237.
54. Yen, S. S. C. (1986). Chronic anovulation due to CNS-hypothalamic- pituitary dysfunction. In Yen, S. S. C., and Jaffe, R. B. (eds.), Reproductive Endocrinology, Physiology, Pathophysiology and Clinical Management, W.B. Saunders, Philadelphia, pp. 500-545.
55. Ziegler, T., Hodges, J. K., Winkler, P., and Heistermann, M. (2000). Hormonal correlates of reproductive seasonality in wild female hanuman langurs (Presbytis entellus). Am. J. Primatol. 51: 119-134.
56. Ziegler, T. E., Savage, A., Scheffler, G., and Snowdon, C. T. (1987). The endocrinology of puberty and reproductive functioning in female cotton-top tamarins (Saguinus oedipus) under varying social conditions. Biol. Reprod. 37: 618-627.