Characterization of the estrous cycle in female beluga (Delphinapterus leucas) using urinary endocrine monitoring and transabdominal ultrasound: Evidence of facultative induced ovulation

General and Comparative Endocrinology

Volumn 175, Issue 3, 2012, Pages 389-397

  Steinman, K J ^a,b   O'Brien, J K ^a   Monfort, S L ^b   Robeck, T R ^a  

^a SeaWorld and Busch Gardens Reproductive Research Center   (United States)

^b SMITHSONIAN CONSERVATION BIOLOGY INSTITUTE   (United States)

Author keywords

Estrous cycle; Follicular ultrasonography; Induced ovulation; Prolactin; White whale

Indexed keywords

ESTROGEN; GESTAGEN; LUTEINIZING HORMONE; OVULATORY LUTEINIZING HORMONE; UNCLASSIFIED DRUG;

ARTICLE; BELUGA WHALE; BREEDING SUCCESS; CONTROLLED STUDY; DELPHINAPTERUS LEUCAS; ECHOGRAPHY; ESTROGEN URINE LEVEL; ESTRUS CYCLE; FEMALE; FOLLICULAR PHASE; HORMONE DETERMINATION; IMMUNOASSAY; MALE; NONHUMAN; OVARY CYCLE; OVULATION INDUCTION; PRIORITY JOURNAL; PROGESTERONE URINE LEVEL; REPRODUCTIVE HEALTH; SEASONAL VARIATION; SEXUAL BEHAVIOR; URINALYSIS;

EID: 84856121159     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2011.11.008     Document Type: Article

References (61)

1. Aronson L.R., Cooper M.L. Penile spines of the domestic cat: their endocrine-behavior relations. Anat. Rec. 1967, 157:71-78.
2. Bakker J., Baum M.J. Neuroendocrine regulation of GnRH release in induced ovulators. Front. Neuroendocrin. 2000, 2:220-262.
3. K. Benirshcke, M.L. Johnson, R.L. Benirschke, Is ovulation in dolphins Stenella longirostrus and Stenella attenuata, always copulation induced? Fish. Bull. 78 (2) (1980) 507-528.
4. Bourke D.A., Adam C.L., Kyle C.E. Ultrasonography as an aid to controlled breeding in the llama (Llama glama). Vet. Rec. 1992, 130:424-428.
5. H.W. Braham, Review of reproduction in the white whale, Delphinapterus leucas, narwhale, Mondon monoceros, and irrawaddy dolphin, Orcaella brevirostris, with comments on stock assessment, in: W.F. Perrin, R.J. Brownell Jr, D.P. Demaster (Eds.), Reproduction in whales, dolphins and porpoises, Special Issue 6. International Whaling Commission, Cambridge, UK, 1984, pp. 81-90.
6. Brodie P.F. A reconsideration of aspects of growth, reproduction, and behavior of the white whale (Delphinapterus leucas) with reference to the Cumberland Sound, Baffin Island, population. J. Fish. Res. Bd. Can. 1971, 28:1309-1318.
7. Brook F.M. Sonographic imaging of the reproductive tract of the female bottlenose dolphin Tursiops truncatus aduncus. Reprod. 2001, 121:419-428.
8. F.M. Brook, R. Kinoshita, K. Benirschke. Histology of the ovaries of a bottlenose dolphin, Tursiops truncatus aduncus, of known reproductive history. Mar. Mamm. Sci. 18 (2) (2002) 540-544.
9. Brown J.L., Lehndhardt J. Secretory patterns of serum prolcatin in Asian (Elephas maximus) and African (Loxodonta africana) elephants during different reproductive states: comparison with concentrations with a non-cycling African elephant. Zoo Bio. 1997, 16:159-164.
10. Brown J.L., Graham L.H., Wielebnowski N.H., Swanson W.F., Wildt D.E., Howard J.G. Understanding the basic reproductive biology of wild felids by monitoring faecal steroids. J. Reprod. Fert. 2001, 57:71-82.
11. J.J. Burns, G.A. Seaman, Investigations of beluga whales in western and northern Alaska II. Biology and ecology. Fairbanks, Alaska. Report by the Alaska Department of Fish and Game. 1986 p. 129.
12. Chen B.X., Yuen Z.X., Pan G.W. Semen-induced ovulation in the Bactrian camel (Camelus bactrianus). J. Reprod. Fert. 1985, 73:335-339.
13. Doidge D.W. Age-length and length-weight comparisons in beluga, Delphinapterus leucas. Can. Bull. Fish. Aqua. Sci. 1990, 224:59-68.
14. O.J. Ginther, Follicles. In: Ultrasonic Imaging and Animal Reproduction: Horses Book 2. Wisconsin Equiservices Publishing, Cross Plains, WI, 1995, pp. 43-72.
15. Goodman A.L. Reflex (Induced) Ovulation. Encyclopedia of Reproduction 1988, 206-211. Academic Press, San Diego, CA. E. Knobil, J.D. Neill (Eds.).
16. Graham L.H., Bolling J., Miller G., Pratt-Hawkes N., Joseph S. Enzyme-immunoassay for the measurement of luteinizing hormone in the serum of African elephants (Loxodonta africana). Technical report. Zoo Biol. 2002, 21:403-408.
17. Greensides R.D., Mead R.A. Ovulation in the spotted skunk (Spilogale putorius latifrons). Biol. Reprod. 1973, 8:576-584.
18. Greulich W.W. Artificially induced ovulation in the cat (Felis domesticus). Anat. Rec. 1934, 58:217-224.
19. Harrison R.J., Boice R.C., Brownell R.L. Reproduction in wild and captive dolphins. Nature 1969, 222:1143-1147.
20. Harrison R.J., Ridgway S.H. Gonadal activity in some bottlenose dolphins (Tursiops truncatus). J. Zool. 1971, 165:355-366.
21. Heide-Jorgensen M.P. Small cetaceans in Greenland: hunting and biology. N. Atl. Stud. 1990, 2:55-58.
22. Heide-Jorgensen M.P., Teilmann J. Growth, reproduction, age structure and feeding habits of white whales (Delphinapterus leucas) in West Greenland waters. Biosci. 1994, 39:195-212.
23. Hermes R., Olson D., Goritz F., Brown J.L., Schmitt D.L., Hagan D., Peterson J.S., Guido F., Hildebrandt T.B. Ultrasonography of the estrous cycle in female African elephants (Loxodonta africana). Zoo Biol. 2000, 19:369-382.
24. Høier R., Heide-Jørgensen M.P. Steroid hormones and prolactin in white whales (Delphinapterus leucas) from West Greenland. Biosci. 1994, 39:227-238.
25. IUCN, The red list of threatened animals, in: IUCN Red List of Threatened Species. Version 2009.2, (2010). Available from http://www.iucn.redlist.org.
26. T.A. Jefferson, L. Karczmarski, K. Laidre, G. O'Corry-Crowe, R.R. Reeves, L. Rojas-Braco, E.R. Secchi, E. Slooten, B.D. Smith, J.Y. Wang, K. Zhou, Delphinapterus leucas Version 3.1 in: IUCN 2009 IUCN Redlist of Threatened Species. Version 2009.2, (2008). Available from http://www.iucnredlist.org/apps/redlist/details/6335/0.
27. Jochle W. Coitus-induced ovulation. Contracep. 1977, 7:523-564.
28. Johnston S.D., O'Callaghan P., Nilsson K., Tzipori G., Curlewis J.D. Semen-induced luteal phase and identification of a LH surge in the koala (Phascolarctos cinereus). Reprod. 2004, 128:629-634.
29. Karsch F.J., Cummins J.T., Thomas G.B., Clarke I.J. Steroid feedback inhibition of pulsatile secretion of gonadotropin-releasing hormone in the ewe. Biol. Reprod. 1987, 36:1207-1218.
30. Katsumata E., Furuta C., Katsumata H., Watanabe G., Taya K. Basal body temperature method for detecting ovarian cycle in the captive beluga (Delphinapterus leucas). J. Reprod. Dev. 2006, 52:59-63.
31. V.L. Kirby, S.H. Ridgway, Hormonal evidence of spontaneous ovulation in captive dolphins (Tursiops truncatus and Delphinus delphis). in: W.F. Perrin, R.J. Brownell Jr., D.P. Demaster (Eds.), Reproduction in whales, dolphins and porpoises, Special Issue 6. International Whaling Commission, Cambridge, UK, 1984, pp. 459-464.
32. S.E. Kleinenberg, A.V. Yablokov, B.M. Bel'kovich, M.N. Tarasevich, Urogenital system, in: Beluga (Delphinapterus leucas) an investigation of the species. Translated from Russian. Izdatel'stvo Nauka, Moskva 1964. (1969) Israel Program for Scientific Translation, Jerusalem.
33. Lees C.M., Wilcken J. Sustaining the Ark: the challenges faced by zoos in maintaining viable populations. Int. Zoo. Yb. 2009, 43:6-18.
34. MacDonald E.A., Northrop L.E., Czekala N.M. Pregnancy detection from fecal progestin concentrations in the red panda (Ailurus fulgens fulgens). Zoo Biol. 2005, 24:419-429.
35. H. Marsh, T. Kasuya. Changes in the ovaries of short-finned pilot whales, Globicephala macrorhynchus, off the pacific coast of Japan, in: W.F. Perrin, R.J. Brownell Jr., D.P. Demaster (Eds.), Reproduction in whales, dolphins and porpoises, Special Issue 6. International Whaling Commission, Cambridge, UK, 1984, pp. 311-336.
36. Moreira N., Monterio-Filho E.L.A., Moraes W., Swanson W.F., Graham L.H., Pasquali O.L., Gomes M.L.F., Morais R.N., Wildt D.E., Brown J.L. Reproductive steroid hormones, ovarian activity in felids of the Leopardus Genus. Zoo Bio. 2001, 20:103-116.
37. P. Nagy, J. Juhasz, U. Wernery, Incidence of spontaneous ovulation and development of the corpus luteum in non-mated dromedary camels (Camelus dromedarius). Theriogen. 64 (2) (2005) 292-304.
38. W.F. Perrin, S.B. Reilly. Reproductive parameters of dolphins and small whales of the family Delphinidae. in: W.F. Perrin, R.J. Brownell Jr., D.P. Demaster (Eds.), Reproduction in whales, dolphins and porpoises, Special Issue 6. International Whaling Commission, Cambridge, UK, 1984, pp. 97-134.
39. O'Brien J.K., Steinman K.J., Schmitt T., Robeck T.R. Semen collection, characterisation and artificial insemination in the beluga (Delphinapterus leucas) using liquid-stored spermatozoa. Reprod. Fertil. Dev. 2008, 20:770-783.
40. O'Brien J.K., Robeck T.R. Preservation of beluga (Delphinapterus leucas) spermatozoa using a trehalose-based cryodiluent and directional freezing technology. Reprod. Fert. Dev. 2010, 22:653-663.
41. O'Corry-Crowe G.M. Beluga Whale. Encyclopedia of Marine Mammals 2009, 108-112. Academic Press, San Diego, CA. W.F. Perrin, B. Wursig, J.G.M. Thewissen (Eds.).
42. Ohsumi S. Comparison of maturity and accumulation rate of corpora albicantia between the left and right ovaries in cetacean. Tokyo Whale Res. Inst. 1964, 18(1964):123-149.
43. Palmer S.S., Nelson R.A., Ramsay M.A., Stirling I., Bahr J.M. Annual changes in serum sex steroids in male and female black (Ursus americanus) and polar (Ursus maritimus) bears. Biol. Reprod. 1988, 38:1044-1050.
44. Robeck T.R., Schneyer A.L., McBain J.F., Dalton L.M., Walsh M.T., Czekala N., Kraemer D.C. Analysis of urinary immunoreactive steroid metabolites and gonadotropins for characterization of the estrous cycle, breeding period, and seasonal estrous activity of captive killer whales (Orcinus orca). Zoo Biol. 1993, 12:173-188.
45. Robeck T.R., Steinman K.J., Gearhart S., Reidarson T.R., McBain J.F., Monfort S.L. Reproductive physiology and development of artificial insemination technology in killer whales (Orcinus orca). Biol. Reprod. 2004, 71:650-660.
46. Robeck T., Monfort S., Calle P., Dunn L., Jensen E., Boehm J., Young S., Clark S. Growth and development in captive beluga (Delphinapterus leucas). Zoo Biol. 2005, 24:29-49.
47. Robeck T.R., Steinman K.J., Yoshioka M., Jensen E., O'Brien J.K., Katsumata E., Gili C., McBain J.F., Sweeney J., Monfort S.L. Estrous cycle characterization and artificial insemination using frozen-thawed spermatozoa in the bottlenose dolphin (Tursiops truncatus). Reprod. 2005, 129(2005):659-674.
48. Robeck T.R., Steinman K.J., Ramirez K., Greenwell M., Van Bonn W., Yoshioka M., Katsumata E., Dalton L., Osborn S., O'Brien J.K. Seasonality, estrous cycle characterization, estrus synchronization, semen cryopreservation and artificial insemination in the Pacific white-sided dolphin (Lagenorhynchus obliquidens). Reprod. 2009, 138:391-405.
49. T.R. Robeck, K.J. Steinman, G.A. Montano, E. Katsumata, S. Osborn, L. Dalton, J.L. Dunn, T.T Schmitt, T.R. Reidarson, J.K. O'Brien, Deep intra-uterine Artificial inseminations using cryopreserved spermatozoa in the beluga (Delphinapterus leucas). Theriogen. 74 (6) (2010) 989-1001.
50. 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. Reprod. 2001, 21:139-149.
51. M. Sato, T. Tsubota, T. Komatsu, G. Watanabe, K. Taya, T. Murase, I. Kita, T. Kudo, Changes in sex steroids, gonadotropins, prolactin, and inhibin in pregnant and nonpregnant Japanese black bears (Ursus thibetanus japonicus). Biol. Reprod. 65 (4) (2001) 1006-1012.
52. Schroeder J.P. Reproductive Aspects of Marine Mammals. Handbook of Marine Mammal Medicine: Health, Disease and Rehabilitation 1990, 353-369. CRC Press, Boca Raton, FL. L.A. Dierauf (Ed.).
53. Skidmore J.A., Billah M., Allen W.R. The ovarian follicular wave pattern and induction of ovulation in the mated and non-mated one humped camel (Camelus dromedarius). Reprod. Fert. Dev. 1996, 106:185-192.
54. Stoops M.A., Pairan R.D., Roth T.L. Follicular, endocrine, and behavioural dynamics of the Indian rhinoceros (Rhinoceros unicornus) oestrous cycle. Reprod. 2004, 128:843-856.
55. Sumar J.B. Effects of various ovulation induction stimuli in alpacas and llamas. J. Arid Environ. 1994, 54:169-178.
56. Taussky H.H. A microcolorimetric determination of creatine in urine by the Jaffe reaction. J. Biol. Chem. 1954, 208:853-861.
57. J. Thimonier, J.P. Ravault, R. Ortavant, Plasma prolactin variations and cyclic ovarian activity in ewes submitted to different light regimens. Ann. Biol. Anim. Bioch. Biophys. 18 (5) (1978) 1229-1235.
58. Walker L.A., Cornell L., Dahl K.D., Czekala N.M., Dargen C.M., Joseph B.E., Hsueh A.J.W., Lasley B.L. Urinary concentrations of ovarian steroid hormone metabolites and bioactive follicle-stimulating hormone in killer whales (Orcinus orca) during ovarian cycles and pregnancy. Biol. Reprod. 1988, 39:1013-1020.
59. Walton J.S., McNeilly J.R., McNeilly A.S., Cunningham F.J. Changes in concentrations of follicle-stimulating hormone, luteinizing hormone, prolactin and progesterone in the plasma of ewes during the transition from anoestrus to breeding activity. J. Endocrinol. 1977, 75:127-136.
60. D. Woodie, Beluga North American Studbook, American Zoological and Aquarium Association Marine Mammal Taxon Advisory Group, Silver Spring, MD, 2009.
61. Yoshioka M., Mohri E., Tobayama T., Aida K., Hanyu I. Annual changes in serum reproductive hormone levels in captive female bottlenose dolphins. Bull. Jpn. Soc. Sci. Fish. 1986, 11:1939-1946.