Circulating inhibin and testosterone during sexual maturation and reproductive seasonality of captive male killer whales (Orcinus orca) https://doi.org/10.12982/VIS.2021.019
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Published:
Apr 12, 2021
Keywords:
Inhibin Male killer whale Sertoli cells Sexual maturation Testosterone
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Abstract
The present study aimed to investigate the reproductive biology of male killer whales. Changes in the concentrations of two circulating testicular hormones, inhibin and testosterone, were monitored during sexual maturation of two male Type 1 Eastern Northern Atlantic killer whales over a period of 20 years. The two killer whales grew rapidly at the pubertal stage and reached a plateau at the age of 23 and 20 years, respectively, after which growth slowed down. In the younger male, circulating inhibin was higher in the juvenile than in the pubertal and mature stages; whereas circulating testosterone exhibited the opposite trend. The pubertal period was estimated to last approximately 5 years, from 12 to 17 years of age. In the elder male, circulating testosterone was high from the onset of this study (12 years of age), when the animal also sired successfully for the first time. This finding shows that the male killer whale is possible to sire even if it is not socially matured, if there is opportunity for copulation. During the mature stage, both animals exhibited significantly higher circulating testosterone concentrations in spring compared to autumn and winter; whereas no seasonal change was observed for circulating inhibin. These results clearly demonstrate that the male killer whale is a seasonal breeder, even though it is fertile throughout the year. This is the first study to elucidate the inhibin concentration and secretory source in the male killer whale
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How to Cite
Katsumata, H. ., Katsumata, E. ., Jaroenporn, S. ., Ueda, Y. ., Konno, S. ., Watanabe, G. ., & Taya, K. . (2021). Circulating inhibin and testosterone during sexual maturation and reproductive seasonality of captive male killer whales (Orcinus orca) : https://doi.org/10.12982/VIS.2021.019. Veterinary Integrative Sciences, 19(2), 209–222. Retrieved from https://he02.tci-thaijo.org/index.php/vis/article/view/250464
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References
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Kaneko, H., Kishi, H., Watanabe, G., Taya, K., Sasamoto, S. & Hasegawa, Y. 1995. Changes in plasma concentrations of immunoreactive inhibin, estradiol and FSH associated with
follicular waves during the estrous cycle of the cow. J. Reprod. Dev. 41, 311-320.
Kaneko, H., Noguchi, J., Kikuchi, K., Akagi, S., Shimada, A., Taya, K., Watanabe, G., 2001. Production and endocrine role of inhibin during the early development. Biol. Reprod.
65: 209-215.
Kaneko, H., Matsuzaki, M., Noguchi, J., Kikuchi, K., Ohnuma, K., Ozawa, M., 2006. Changes in circulating and testicular levels of inhibin A and B during postnatal development in
bulls. J. Reprod. Dev. 52: 741-749.
Kanematsu, N., Jin, W. Z., Watanabe, G., Taya, K., 2006. Age-related changes of reproductive hormones in young Meishan boars. J. Reprod. Dev. 52: 651-656.
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Katsumata, E., Jaroenporn, S., Katsumata, H., Konno, S., Maeda, Y., Watanabe, G., Taya, K., 2006. Body temperature and circulating progesterone levels before and after
parturition in Killer whales (Orcinus orca). J. Reprod. Dev. 52: 65-71.
Katsumata, E., Ueda, Y., Arai, K., Katsumata, H., Kishimoto, M., Watanabe, G., Taya, K., 2012. Circulating testosterone and inhibin levels at different ages in the male beluga
(Delphinapterus leucas). J. Vet. Med. Sci. 74: 293-300.
Katsumata, E, Jaroenporn, S., Ueda, Y., Arai, K., Katsumata, H., Watanabe, G., Taya, K., 2017. Circulating gonadotropins and testicular hormones during sexual maturation
and annual changes in male bottlenose dolphins (Tursiops truncatus). J. Vet. Med. Sci. 79: 1899-1905.
Matsuzaki, S., Cruzana, M. B. C., Budipitojo, T., Hondo, E., Watanabe, G., Taya, K., Sasaki, M., Kitamura, N., Yamada, J., 2001a. Immunohistochemical localization of inhibin
subunits in the testis of the bull. Anat. Histol. Embryol. 30: 375-378.
Matsuzaki, S., Uenoyama, Y., Okuda, K., Watanabe, G., Kitamura, N., Taya, K., Yamada, J., 2000. Age-related changes in the serum levels of inhibin, FSH, LH and testosterone
in Holstein bulls. J. Reprod. Dev. 46, 245-248.
Matsuzaki, S., Uenoyama, Y., Okuda, K., Watanabe, G., Kitamura, N., Taya, K., Cruzana, M. B. C., Yamada, J., 2001b. Prepubertal changes in immunoreactive inhibin
concentration in blood serum and testicular tissue in Holstein bull calves. J. Vet. Med. Sci. 63: 1303-1307.
Medan, M.S, Arai, K., Watanabe, G and Taya, K., 2007. Inhibin: Regulation of reproductive function and practical use in females. Anim. Sci. J. 78: 16-27.
O’Brien, J., K., Robeck, T., R., 2010. The value of Ex Situ Cetacean populations in understanding reproductive physiology and developing assisted reproductive
technology for Ex Situ and In Situ species management and conservation efforts. Int’l. J. comp. psychol. 23: 227-24.
O’Brien, J., K., Steinman, K., J., Fetter, G., A., Robeck, T., R., 2017. Androgen and glucocorticoid production in the male killer whale (Orcinus orca): Influence of age,
maturity, and environmental factors. Andrology. 5: 180-190.
Olesiuk, P., F., Bigg, M., A., Ellis, G., M., 1990. Life history and population dynamics of resident killer whales (Orcinus orca) in the coastal waters of British Columbia and
Washington State. In Report of the International Whaling Commission (Special Issue 12). International whaling commission, Cambridge. pp.209-242.
Olesiuk, P., F., Ellis G., M., , Ford, J., K., B., 2005. Life History and Population Dynamics of Northern Resident Killer Whales (Orcinus orca) in British Columbia. Research
Document 2005/045. ISSN 1499-3848 (Printed) Her Majesty the Queen in Right of Canada.
Pittman, R., L., 2007. Killer whales, Ecotypes & Forms. http://swfsc.noaa.gov./pre- killer whale/
Robeck, T., R., Schneyer, A., L., McBain, J., F., Dalton, L., M., Walsh, M., T., Czekala, N., Kraemer, D., C., 1993. 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). Zool. Biol. 12:173–188.
Robeck, T., R., Steinman, K., J., Gearhart, S., Reidarson, T. R., McBain, J. F., Monfort, S.L., 2004. Reproductive physiology and development of artificial insemination
technology in killer whales (Orcinus orca). Biol. Reprod. 71: 650–660.
Robeck, T., R., Monfort, S., L., 2006. Characterization of male killer whale (Orcinus orca) sexual maturation and reproductive seasonality. Theriogenology 66, 242-250.
Robeck, T., R., Steinman, K., J., O’Brien J., K., 2016. Characterization and longitudinal monitoring of serum progestogens and estrogens during normal pregnancy in the
killer whale (Orcinus orca). Gen. Comp. Endocrinol. 236: 83–97.
Robeck, T., R., Steinman, K., J., O’Brien, J., K., 2017. Characterization and longitudinal monitoring of serum androgens and glucocorticoids during normal pregnancy in the
killer whale (Orcinus orca). Gen, Comp, Endocrinol, 247:116-129.
Schroder, J., P., 1990. Breeding bottlenose dolphins in captivity. In The Bottlenose Dolphin (Leatherwood, S. and Reeves, R. R. eds). Academic Press, San Diego. pp. 435-446.
Taya, K., Watanabe, G., Sasamoto, S., 1985. Radioimmunoassay for progesterone, testosterone and estradiol-17β using 125I-iodohistamine radioligands. J. Reprod. Dev. 31:186-
197.
Yang, P., X., Medan, M., S., Arai, K,. Y., Watanabe, G., Taya, K., 2005a. Plasma concentrations of immunoreactive (ir)-inhibin, gonadotropins and steroid hormones during the
ovulatory cycle of the duck. J. Reprod. Dev. 51: 353-358.
Yang, P., X., Medan, M., S., Watanabe, G., Taya. K., 2005b. Developmental changes of plasma inhibin, gonadotropins, steroid hormones, and thyroid hormones in male and
female Shao ducks. Gen. Comp. 143:161-167.
Yang, P., X., Medan, M., S., Arai, K., Y., Jin, W., Z., Watanabe, G., Taya, K., 2005c. Ontogeny of testicular inhibin and activin in ducks: an immunocytochemical analysis. Anim.
Sci. J. 76: 427-434.
Best, P., B., 1970. The sperm whale (Physeter catodon) off the west coast of South Africa 5, Age growth and mortality. Investl Rep. Div. Seafish. S. Afr. 79: 1-27.
Bogin, B., 1999. Evolutionary perspective on human growth. Annu. Rev. Anthropol. 28:109-153.
Clark, S., T., Odell, D., K., 1999. Allometric relationships and sexual dimorphism in captive killer whales (Orcinus orca). J. Mammal. 80: (3), 777-785
Clark, S., T., Odell, D., K., Lacinak, C., T., 2000. Aspects of growth in captive killer whales (Orcinus orca). Mar. Mammal Sci. 16: (1), 110-123
Chaichanathong, S., Taya, K., Watanabe, G., Nagaoka, K., Wajjwalku, W., Sudsukh, A., Thongtip, N., 2018. Immunohistochemical localization of inhibin/activin subunits in
adult Asian elephant (Elephas maximus) testis. J. Vet. Med. Sci. 80: (3), 549-552.
Christensen, I., 1984. Growth and reproduction of killer whales, Orcinus orca, in Norwegian coastal waters. In: Rrp. Int. whal. Commn. (special issue 6) (Perrin W.F. ed).
International whaling commission, Cambridge, pp.253-259.
Clinton, W., L., 1994. Sexual selection and growth in male Northern Elephant seals. In: Elephant seals (Le Boenf, B. J. and Laws, R. M. eds) , University of California press,
Berkeley, CA, pp.154 -168.
Dhakal, P., Tsunoda, N., Nakai, R., Nagaoka, K., Nambo, Y., Sato, F., Taniyama, H., Watanabe, G., Taya, K., 2011. Post-natal dynamic changes in circulating follicle-stimulating
hormone, luteinizing hormone, immunoreactive inhibin, progesterone, testosterone and estradiol-17β in thoroughbred colts until 6 months of age. J. Equ. Sci. 22: 9-15.
Dhakal, P., Hirama, A., Nambo, Y., Harada, T., Sato, F, Nagaoka, K., Watanabe, G., Taya, K., 2012. Circulating pituitary and gonadal hormones in spring-born Thoroughbred
fillies and colts from birth to puberty. J Reprod. Dev. 58: 522-530.
Hamada, T., Watanabe, G., Kokuho, T., Taya, K., Sasamoto, S., Hasegawa, Y., Miyamoto, K., Igarashi, M., 1989. Radioimmunoassay of inhibin in various mammals. J. Endocrinol.
122: 697-704.
Kaneko, H., Kishi, H., Watanabe, G., Taya, K., Sasamoto, S. & Hasegawa, Y. 1995. Changes in plasma concentrations of immunoreactive inhibin, estradiol and FSH associated with
follicular waves during the estrous cycle of the cow. J. Reprod. Dev. 41, 311-320.
Kaneko, H., Noguchi, J., Kikuchi, K., Akagi, S., Shimada, A., Taya, K., Watanabe, G., 2001. Production and endocrine role of inhibin during the early development. Biol. Reprod.
65: 209-215.
Kaneko, H., Matsuzaki, M., Noguchi, J., Kikuchi, K., Ohnuma, K., Ozawa, M., 2006. Changes in circulating and testicular levels of inhibin A and B during postnatal development in
bulls. J. Reprod. Dev. 52: 741-749.
Kanematsu, N., Jin, W. Z., Watanabe, G., Taya, K., 2006. Age-related changes of reproductive hormones in young Meishan boars. J. Reprod. Dev. 52: 651-656.
Kasuya, T. and Marsh, H.,1984. Life history and reproductive biology of the short-finned pilot whale, Globicephala macrorhyncus, off coast of Japan. In Reproduction in
whales and dolphins and porpoises. Perrin, W. F., Brownell, R. L. and DeMaster, D. P. eds. International whaling commission (Special issue 6), Cambridge. pp. 251-310.
Kasuya, T., 2011. Bottlenose dolphin. In: Conservation Biology of Small Cetaceans around Japan, University of Tokyo Press, Tokyo, pp. 363-400.
Katsumata, E., Jaroenporn, S., Katsumata, H., Konno, S., Maeda, Y., Watanabe, G., Taya, K., 2006. Body temperature and circulating progesterone levels before and after
parturition in Killer whales (Orcinus orca). J. Reprod. Dev. 52: 65-71.
Katsumata, E., Ueda, Y., Arai, K., Katsumata, H., Kishimoto, M., Watanabe, G., Taya, K., 2012. Circulating testosterone and inhibin levels at different ages in the male beluga
(Delphinapterus leucas). J. Vet. Med. Sci. 74: 293-300.
Katsumata, E, Jaroenporn, S., Ueda, Y., Arai, K., Katsumata, H., Watanabe, G., Taya, K., 2017. Circulating gonadotropins and testicular hormones during sexual maturation
and annual changes in male bottlenose dolphins (Tursiops truncatus). J. Vet. Med. Sci. 79: 1899-1905.
Matsuzaki, S., Cruzana, M. B. C., Budipitojo, T., Hondo, E., Watanabe, G., Taya, K., Sasaki, M., Kitamura, N., Yamada, J., 2001a. Immunohistochemical localization of inhibin
subunits in the testis of the bull. Anat. Histol. Embryol. 30: 375-378.
Matsuzaki, S., Uenoyama, Y., Okuda, K., Watanabe, G., Kitamura, N., Taya, K., Yamada, J., 2000. Age-related changes in the serum levels of inhibin, FSH, LH and testosterone
in Holstein bulls. J. Reprod. Dev. 46, 245-248.
Matsuzaki, S., Uenoyama, Y., Okuda, K., Watanabe, G., Kitamura, N., Taya, K., Cruzana, M. B. C., Yamada, J., 2001b. Prepubertal changes in immunoreactive inhibin
concentration in blood serum and testicular tissue in Holstein bull calves. J. Vet. Med. Sci. 63: 1303-1307.
Medan, M.S, Arai, K., Watanabe, G and Taya, K., 2007. Inhibin: Regulation of reproductive function and practical use in females. Anim. Sci. J. 78: 16-27.
O’Brien, J., K., Robeck, T., R., 2010. The value of Ex Situ Cetacean populations in understanding reproductive physiology and developing assisted reproductive
technology for Ex Situ and In Situ species management and conservation efforts. Int’l. J. comp. psychol. 23: 227-24.
O’Brien, J., K., Steinman, K., J., Fetter, G., A., Robeck, T., R., 2017. Androgen and glucocorticoid production in the male killer whale (Orcinus orca): Influence of age,
maturity, and environmental factors. Andrology. 5: 180-190.
Olesiuk, P., F., Bigg, M., A., Ellis, G., M., 1990. Life history and population dynamics of resident killer whales (Orcinus orca) in the coastal waters of British Columbia and
Washington State. In Report of the International Whaling Commission (Special Issue 12). International whaling commission, Cambridge. pp.209-242.
Olesiuk, P., F., Ellis G., M., , Ford, J., K., B., 2005. Life History and Population Dynamics of Northern Resident Killer Whales (Orcinus orca) in British Columbia. Research
Document 2005/045. ISSN 1499-3848 (Printed) Her Majesty the Queen in Right of Canada.
Pittman, R., L., 2007. Killer whales, Ecotypes & Forms. http://swfsc.noaa.gov./pre- killer whale/
Robeck, T., R., Schneyer, A., L., McBain, J., F., Dalton, L., M., Walsh, M., T., Czekala, N., Kraemer, D., C., 1993. 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). Zool. Biol. 12:173–188.
Robeck, T., R., Steinman, K., J., Gearhart, S., Reidarson, T. R., McBain, J. F., Monfort, S.L., 2004. Reproductive physiology and development of artificial insemination
technology in killer whales (Orcinus orca). Biol. Reprod. 71: 650–660.
Robeck, T., R., Monfort, S., L., 2006. Characterization of male killer whale (Orcinus orca) sexual maturation and reproductive seasonality. Theriogenology 66, 242-250.
Robeck, T., R., Steinman, K., J., O’Brien J., K., 2016. Characterization and longitudinal monitoring of serum progestogens and estrogens during normal pregnancy in the
killer whale (Orcinus orca). Gen. Comp. Endocrinol. 236: 83–97.
Robeck, T., R., Steinman, K., J., O’Brien, J., K., 2017. Characterization and longitudinal monitoring of serum androgens and glucocorticoids during normal pregnancy in the
killer whale (Orcinus orca). Gen, Comp, Endocrinol, 247:116-129.
Schroder, J., P., 1990. Breeding bottlenose dolphins in captivity. In The Bottlenose Dolphin (Leatherwood, S. and Reeves, R. R. eds). Academic Press, San Diego. pp. 435-446.
Taya, K., Watanabe, G., Sasamoto, S., 1985. Radioimmunoassay for progesterone, testosterone and estradiol-17β using 125I-iodohistamine radioligands. J. Reprod. Dev. 31:186-
197.
Yang, P., X., Medan, M., S., Arai, K,. Y., Watanabe, G., Taya, K., 2005a. Plasma concentrations of immunoreactive (ir)-inhibin, gonadotropins and steroid hormones during the
ovulatory cycle of the duck. J. Reprod. Dev. 51: 353-358.
Yang, P., X., Medan, M., S., Watanabe, G., Taya. K., 2005b. Developmental changes of plasma inhibin, gonadotropins, steroid hormones, and thyroid hormones in male and
female Shao ducks. Gen. Comp. 143:161-167.
Yang, P., X., Medan, M., S., Arai, K., Y., Jin, W., Z., Watanabe, G., Taya, K., 2005c. Ontogeny of testicular inhibin and activin in ducks: an immunocytochemical analysis. Anim.
Sci. J. 76: 427-434.