A review of the reproductive physiology of rhinoceros species in captivity

International Zoo Yearbook

Volumn 40, Issue 1, 2006, Pages 130-143

  Roth, T L ^a  

^a Cincinnati Zoo and Botanical Garden   (United States)

Author keywords

Embryo loss; Ovarian function; Pregnancy; Pregnancy loss; Reproductive cycle; Reproductive endocrinology; Reproductive pathology; Rhinoceros; Semen collection; Sperm; Ultrasonography

Indexed keywords

EID: 34247532116     PISSN: 00749664     EISSN: 17481090     Source Type: Journal    
DOI: 10.1111/j.1748-1090.2006.00130.x     Document Type: Article

References (51)

1. Adams, G. P., Kastelic, J. P., Bergfelt, D. R. & Ginther, O. J. (1987): Effect of uterine inflammation and ultrasonically-detected uterine pathology on fertility in the mare. Journal of Reproduction & Fertility 35: 445 – 454.
2. Adams, G. P., Plotka, E. D., ASA, C. S. & Ginther, O. J. (1991): Feasibility of characterizing reproductive events in large nondomestic species by trans-rectal ultrasonic imaging. Zoo Biology 10: 246 – 259.
3. AZA, Rhinoceros Advisory, Group (RAG) (2005): AZA Species Survival Plan for rhinoceros. Cumberland, OH: Association of Zoos and Aquariums (AZA) RAG.
4. Berkeley, E. V., Kirkpatrick, J. F., Schaffer, N. E., Bryant, W. M. & Threlfall, W. R. (1997): Serum and fecal steroid analysis of ovulation, pregnancy, and parturition in the black rhinoceros (Diceros bicornis). Zoo Biology 16: 121 – 132.
5. Brett, R. A., Hodges, J. K. & Wanjohi, E. (1989): Assessment of reproductive status of the black rhinoceros (Rhinoceros bicornis) in the wild. Symposia of The Zoological Society of London No. 61: 147 – 161.
6. Brown, J. L., Bellem, A. C, Fouraker, M., Wildt, D. E. & Roth, T. L. (2001): Comparative analysis of gonadal and adrenal activity in the black and white rhinoceros in North American by noninvasive endocrine monitoring. Zoo Biology 20: 463 – 485.
7. Carlstead, K. & Brown, J. L. (2005): Relationships between patterns of fecal corticoid excretion and behavior, reproduction, and environmental factors in captive black (Diceros bicornis) and white (Cer-atotherium simum) rhinoceros. Zoo Biology 24: 215 – 232.
8. Chevalier-Clement, F. (1989): Pregnancy loss in the mare. Animal Reproduction and Science 20: 231 – 244.
9. Crump, J. P. & Crump, J. W. (1994): Manual semen collection from a Grevy’s zebra stallion (Equus grevyi), onset of sperm production, semen characteristics, and cryopreservation of semen with a comparison to the sperm production from a Grant’s zebra stallion (Equus burchelli boehmi). Theriogenology 41: 1011 – 1021.
10. Czekala, N. M. & Callison, L. (1996): Pregnancy diagnosis in the black rhinoceros (Diceros bicornis) by salivary hormone analysis. Zoo Biology 15: 37 – 44.
11. Fouraker, M. & Wagener, T. (1996): AZA rhinoceros husbandry resource manual. Fort Worth, TX: Fort Worth Zoological Park.
12. Garnier, J. N., Holt, W. V. & Watson, P. F. (2002): Non-invasive assessment of oestrous cycles and evaluation of reproductive seasonality in the female wild black rhinoceros (Diceros bicornis minor). Reproduction 123: 877 – 889.
13. Ginther, O. J. (1995): Ultrasonic imaging and animal reproduction: Horses book 2. Cross Plains, WI: Equiservices Publishing.
14. Godfrey, R. W., Pope, C. E., Dresser, B. L. & Olsen, J. H. (1991): Gross anatomy of the reproductive tract of female black (Diceros bicornis michaeli) and white rhinoceros (Ceratotherium simum simum). Zoo Biology 10: 165 – 175.
15. Gomez, A., Jewell, E., Walker, S. L., & Brown, J. L. (2004): Use of salivary steroid analyses to assess ovarian cycles in an Indian rhinoceros at the National Zoological Park. Zoo Biology 23: 501 – 512.
16. Heistermann, M., Agil, M., Buthe, A. & Hodges, J. K. (1998): Metabolism and excretion of oestradiol-173 and progesterone in the Sumatran rhinoceros (Dicer orhinus sumatrensis). Animal Reproduction Science 53: 157 – 172.
17. Hermes, R., Bryant, B., Göritz, F., Portas, T., Thorne, A., O’Brien, J. & Hildebrandt, T. (2004): Testicular neoplasia in a white rhinoceros (Ceratotherium simum): fertility and assisted reproductive measures to minimize genetic loss. Proceedings American Association of Zoo Veterinarians 2004: 387.
18. Hermes, R., Hildebrandt, T. B. & Goritz, F. (2004): Reproductive problems directly attributable to long-term captivity-asymmetric reproductive aging. Animal Reproductive Science 82-83: 49 – 60.
19. Hermes, R., Hildebrandt, T. B., Blottner, S., Walzer, C., Silinski, S., Patton, M. L., Wibbelt, G., Schwarzenberger, F. & Göritz, F. (2005): Reproductive soundness of captive southern and northern white rhinoceroses (Ceratotherium simum, C. s. cottoni): Evaluation of male genital tract morphology and semen quality before and after cryo-preservation. Theriogenology 63: 219 – 238.
20. Hindle, J. E. & Hodges, J. K. (1990): Metabolism of oestradiol-17/i and progesterone in the white rhinoceros (Ceratotherium simum simum). Journal of Reproduction & Fertility 90: 571 – 580.
21. Hindle, J. E., Möstl, E. & Hodges, J. K. (1992): Measurement of urinary oestrogens and 20a-dihy-droprogesterone during ovarian cycles of black (Diceros bicornis) and white (Ceratotherium simum) rhinoceroses. Journal of Reproduction & Fertility 94: 237 – 249.
22. Hlavacek, G., Zschokke, S. & Guldenschuh, G. (2002): International studbook for the greater one-horned or Indian rhinoceros, Rhinoceros unicornis: 6 – 26. Basel: Zoo Basel.
23. Hodges, J. K. & Green, D. I. (1989): The development of an enzyme-immunoassay for urinary preg-nanediol-3-glucuronide and its application to reproductive assessment in exotic mammals. Journal of Zoology 219: 89 – 99.
24. Kasman L. H., Ramsay, E. C. & Lasley, B. L. (1986): Urinary steroid evaluations to monitor ovarian function in exotic ungulates. III. Estrone sul-fate and pregnanediol-3-glucuronide excretion in the Indian rhinoceros (Rhinoceros unicornis). Zoo Biology 5: 355 – 361.
25. Kassam, A. H. & Lasley, B. L. (1981): Estrogen excretory patterns in the Indian rhinoceros (Rhinoceros unicornis), determined by simplified urinary analysis. American Journal of Veterinarian Research 42: 251 – 255.
26. Kock, R. & Garnier, J. (1993): Veterinary management of three species of rhinoceroses in zoological collections. Proceedings of an International Conference Rhinoceros Biology and Conservation 1993: 325 – 338.
27. 2 pregnanes from fecal extracts of a pregnant black rhinoceros (Diceros bicornis minor). Steroids 66: 875 – 881.
28. McDonnell, S. M. & Love, C. C. (1990): Manual stimulation collection of semen from stallions; training time, sexual behavior and semen. Theriogenology 33: 1201 – 1210.
29. Montali, R. J. & Citino, S. B. (1993): Pathological findings in captive rhinoceroses. Proceedings of an International Conference Rhinoceros Biology and Conservation 1993: 346 – 349.
30. O’Brien, J. K. & Roth, T. L. (2000): Post-coital sperm recovery and cryopreservation in the Sumatran rhinoceros (Dicerorhinus sumatrensis) and application to gamete rescue in the African black rhinoceros (Diceros bicornis). Journal of Reproduction & Fertility 118: 263 – 271.
31. Pashen, R. L. & Allen, W. R. (1979): The role of the fetal gonads and placenta in steroid production, maintenance of pregnancy and parturition in the mare. Journal of Reproduction & Fertility 27 (suppl.): 499 – 509.
32. Patton, M. L., Swaisgood, R. R., Czekala, N. M., White, A. M., Fetter, G. A., Montagne, J. P., Rieches, R. G. & Lance, V. A. (1999): 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 Biology 18: 111 – 127.
33. Platz, C., Seager, S. W. J. & Bush, M. (1979): Collection and analysis of semen from a black rhinoceros. Journal of American Veterinary Medical Association 175: 1002 – 1004.
34. Radcliffe, R. M., Hendrickson, D. A., Richardson, G. L., Zuba, J. R. & Radcliffe, R. W. (2000): Standing laparoscopic-guided uterine biopsy in a southern white rhinoceros (Ceratotherium simum simum). Journal of Zoo and Wildlife Medicine 31: 201 – 207.
35. Radcliffe, R. W., Czekala, N. M. & Osofsky, S. A. (1997): Combined serial ultrasonography and fecal progestin analysis for reproductive evaluation of the female white rhinoceros (Ceratotherium simum simum): Preliminary results. Zoo Biology 16: 445 – 456.
36. Radcliffe, R. W., Eyres, A. I., Patton, M. L., Czekala, N. M. & Emslie, R. H. (2001): Ultrason-ographic characterization of ovarian events and fetal gestational parameters in two southern black rhinoceros (Diceros bicornis minor) and correlation to fecal progesterone. Theriogenology 55: 1033 – 1049.
37. Ramsay, E. C, Kasman, L. H. & Lasley, B. L. (1987): Urinary steroid evaluations to monitor ovarian function in exotic ungulates. V. Estrogen and pregnanediol-3-gluronide excretion in the black rhinoceros (Diceros bicornis). Zoo Biology 6: 275 – 282.
38. Roth, T. L., O’Brien, J. K., Mcrae, M. A., Bellem, A. C., Romo, S. J., Kroll, J. L. & Brown, J. L. (2001): Ultrasound and endocrine evaluation of the ovarian cycle and early pregnancy in the Sumatran rhinoceros, Dicerorhinus sumatrensis. Reproduction 121: 139 – 149.
39. Roth, T. L., Bateman, H. L., Kroll, J. L., Stei-Netz, B. G. & Reinhart, P. R. (2004): Endocrine and ultrasonographic characterization of a successful pregnancy in a Sumatran rhinoceros (Dicerorhinus sumatrensis) supplemented with a synthetic progestin. Zoo Biology 23: 219 – 238.
40. Roth, T. L., Stoops, M. A., Atkinson, M. W., Blumer, E. S., Campbell, M. K., Cameron, K. N., Citino, S. B. & Maas, A. K. (2005): Semen collection in the rhinoceros by electroejaculation with a uniquely designed probe. Journal of Zoo and Wildlife Medicine 36: 617 – 627.
41. Schaffer, N. E., Beehler, B., Jeyendran, R. S. & Balke, B. (1990): Methods of semen collection in an ambulatory greater one-horned rhinoceros (Rhinoceros unicornis). Zoo Biology 9: 211 – 221.
42. Schaffer N. E., Zainal-Zahari, Z., Suri, M. S. M., Jainudeen, M. R. & Jeyendran, R. S. (1994): Ultra-sonography of the reproductive anatomy in the Sumatran rhinoceros (Dicerorhinus sumatrensis). Journal of Zoo and Wildlife Medicine 25: 337 – 348.
43. Schaffer, N., Bryant, W., Agnew, D., Meehan, T. & Beehler, B. (1998): Ultrasonographic monitoring of artificially stimulated ejaculation in three rhinoceros species (Ceratotherium simum, Dicer os bicornis, Rhinoceros unicornus). Journal of Zoo and Wildlife Medicine 29: 386 – 393.
44. Schwarzenberger, F., Franke, R. & Goltenboth, R. (1993): Concentrations of faecal immunoreactive progestagen metabolites during the oestrous cycle and pregnancy in the black rhinoceros (Diceros bicornis michaeli). Journal of Reproduction & Fertility 98: 285 – 291.
45. Schwarzenberger, F., Tomasova, K., Holeckova, D., Matern, B. & Möstl, E. (1996): Measurement of fecal steroids in the black rhinoceros (Diceros bicornis) using group-specific enzyme immunoassays for 20-oxo-pregnanes. Zoo Biology 15: 159 – 171.
46. Schwarzenberger, F., Walzer, C, Tomasova, K., Vahala, J., Meister, J., Goodrowe, K. L., Zima, J., Straub, F. & Lynch, M. (1998): Fecal progesterone metabolite analysis for non-invasive monitoring of reproductive function in the white rhinoceros (Ceratotherium simum). Animal Reproduction Science 53: 1723 – 190.
47. Schwarzenberger, F., Rletschel, W., Vahala, J., Holeckova, D., Thomas, P., Maltzan, J., Baum-Gartner, K. & Schaftenaar, W. (2000): Fecal progesterone, estrogen, and androgen metabolites for noninvasive monitoring or reproductive function in the female Indian rhinoceros, Rhinoceros unicornis. General and Comparative Endocrinology 119: 300 – 307.
48. Sherman, G. B., Lund, L. A., Bunick, D. & Winn, R. J. (1997): Characterization and phylogenetic significance of rhinoceros luteinizing hormone beta (LHbeta) subunit messenger RNA structure, complementary DNA sequence and gene copy number. Gene 195: 131 – 139.
49. Steinetz, B. G., Brown, J. L., Roth, T. L. & Czekala, N. (2005): Relaxin concentrations in serum and urine of endangered species: Correlations with physiologic events and use as a marker of pregnancy. Annals of New York Academy of Science 1041: 367 – 378.
50. Stoops, M. A., Pairan, R. D. & Roth, T. L. (2004): Follicular, endocrine and behavioral dynamics of the Indian rhinoceros (Rhinoceros unicornis) oestrous cycle. Reproduction 128: 843 – 856.
51. Swaisgood, R. R., Dickman, D. M. & White, A. M. (2006): A captive population in crisis: Testing hypotheses for reproductive failure in captive-born southern white rhinoceros females. Biological Conservation 129: 468 – 476.