Advertisement

Fish Physiology and Biochemistry

, Volume 26, Issue 4, pp 389–401 | Cite as

Serum steroid concentrations and development of reproductive organs during puberty in male bonnethead sharks, Sphyrna tiburo

  • J. Gelsleichter
  • L.E.L. Rasmussen
  • C.A. Manire
  • J. Tyminski
  • B. Chang
  • L. Lombardi-Carlson
Article

Abstract

Puberty is a critical, hormone-mediated event during which an animal acquires the ability to breed and propagate. Despite the importance of this stage in animal reproduction, little is known regarding the physiological factors that regulate and/or accompany puberty in several vertebrate groups including elasmobranchs. To address the need for such information, the present study investigated morphological and hormonal changes that occur during puberty in male bonnethead sharks (Sphyrna tiburo). Serial changes in development of claspers, paired copulatory organs in male elasmobranchs, and serum steroid concentrations during puberty were evaluated in captive-held male S. tiburo. Captive-animal studies were supplemented by observations on gonadal development, gonaduct morphology, and serum steroid concentrations in feral, peripubertal male S. tiburo. Changes in size and histological architecture of testes and gonaducts of peripubertal sharks mirrored the seasonal progression of events that occur in these structures in mature males. Claspers grew in length continuously during puberty, but sharks did not reach functional maturity until a short period before mating activity commences in the mature population. Clasper growth appeared to be strictly regulated in S. tiburo, perhaps to ensure growth of these organs to sizes deemed critical for reproductive success. Serum concentrations of testosterone, dihydrotestosterone, progesterone, and 17β-estradiol increased in both captive and feral sharks during pubertal development, and may be associated with development of the gonads and gonaducts. Differences in hormone profiles of captive and feral sharks were observed at certain periods during puberty, but their origin remains unclear.

bonnethead shark puberty spermatogenesis steroid hormones 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Amano, M., Kitamura, S., Ikuta, K., Suzuki, Y. and Aida, K. 1997. Activation of salmon GnRH mRNA expression prior to differentiation of precocious male in Masu salmon. Gen. Comp. Endocrinol. 105: 365–371.PubMedCrossRefGoogle Scholar
  2. Amer, M.A., Miura, T., Miura, C. and Yamauchi, K. 2001. Involvement of sex steroid hormones in the early stages of spermatogenesis in Japanese huchen (Hucho perryi). Biol. Reprod. 65: 1057–1066.PubMedCrossRefGoogle Scholar
  3. Arukwe, A. 2001. Cellular and molecular responses to endocrinemodulators and the impact on fish reproduction. Mar. Pollut. Bull. 42: 643–655.PubMedCrossRefGoogle Scholar
  4. Betka, M. and Callard, G.V. 1998. Negative feedback control of the spermatogenic progression by testicular oestrogen synthesis: insights from the shark testis model. APMIS 106: 252–258.PubMedCrossRefGoogle Scholar
  5. Birkhead, T. 2000. Promiscuity: An Evolutionary History of Sperm Competition and Sexual Conflict. Faber & Faber, London.Google Scholar
  6. Bourguignon, J.P. 1991. Growth and timing of puberty: reciprocal effects. Hormone Res. 36: 131–135.PubMedGoogle Scholar
  7. Bourguignon, J.P. and Plant, T.M. (eds) 2000. The Onset of Puberty in Perspective. Elsevier, Amsterdam.Google Scholar
  8. Callard, G.V. 1988. Reproductive physiology (Part B: The male). In: Physiology of Elasmobranch Fishes. pp. 292–317. Edited by T.J. Shuttleworth. Springer-Verlag, Berlin.Google Scholar
  9. Callard, G.V., Pudney, J.A., Mak, P. and Canick, J.A. 1985. Stage-dependent changes in steroidogenic enzymes and estrogen receptors during spermatogenesis in the testis of the dogfish, Squalus acanthias. Endocrinology 117: 1328–1335PubMedCrossRefGoogle Scholar
  10. Callard, I.P. and Klosterman, L. 1988. Reproductive physiology (Part A: The female). In: Physiology of Elasmobranch Fishes, pp. 277–292. Edited by T.J. Shuttleworth. Springer-Verlag, Berlin.Google Scholar
  11. Cavaco, J.E.B., Lambert, J.G.D., Schulz, R.W. and Goos, H.J.T. 1997. Pubertal development of male African catfish, Clarias gariepinus. In vitro steroidogenesis by testis and interregnal tissue and plasma levels of sexual steroids. Fish Physiol. Biochem. 16: 129–138.Google Scholar
  12. Cuevas, M.E. and Callard, G. 1992. Androgen and progesterone receptors in shark (Squalus) testis: Characteristics and stagerelated distribution. Endocrinology 130: 2173–2182.PubMedCrossRefGoogle Scholar
  13. Cuevas, M.E., Collins, K. and Callard, G.V. 1993. Stage-related changes in steroid-converting enzyme activities in Squalus testis: synthesis of biologically active metabolites via 3 betahydroxysteroid dehydrogenase/isomerase and 5 alpha-reductase. Steroids 58: 87–94.PubMedCrossRefGoogle Scholar
  14. Eberhard, W.G. 1985. Sexual Selection and Animal Genitalia. Harvard University Press, Cambridge.Google Scholar
  15. Frisch, R.E., Hefsted, M.D. and Yoshinaga, K. 1977. Carcass composition at first estrus of rats on high fat and low fat diets: Body water, protein and fat. Proc. Nat. Acad. Sci. USA 74: 379–383.PubMedCrossRefGoogle Scholar
  16. Garnier, D.H., Sourdaine, P. and Jegou, B. 1999. Seasonal variations in sex steroids and male sexual characteristics in Scyliorhinus canicula. Gen. Comp. Endocrinol. 116: 281–290.PubMedCrossRefGoogle Scholar
  17. Gelsleichter, J., Steinetz, B.G., Manire, C.A. and Ange, C. 2003. Serum relaxin concentrations and reproduction in male bonnethead sharks, Sphyrna tiburo. Gen. Comp. Endocrinol. 132: 27–34.PubMedCrossRefGoogle Scholar
  18. Gore, A.C. 2000. Modulation of the GnRH gene and the onset of puberty. In: The Onset of Puberty in Perspective. pp. 25–35. Edited by J.P. Bourguignon and T.M. Plant. Elsevier, Amsterdam.Google Scholar
  19. Heupel, M.R., Whittier, J.M. and Bennett, M.B. 1999. Plasma steroid hormone profiles and reproductive biology of the epaulette shark, Hemiscyllium ocellatum. J. Exp. Zool. 284: 586–594.PubMedCrossRefGoogle Scholar
  20. Holland, M.C., Hassin, S. and Zohar, Y. 2000. Gonadal development and plasma steroid levels during pubertal development in captive-reared striped bass, Morone saxatilis. J. Exp. Zool. 286: 49–63.PubMedCrossRefGoogle Scholar
  21. Huang, Y.-S., Rousseau, K., Le Belle, N., Vidal, B., Burzawa-Gérard, E., Marchelidon, I. and Dufour, S. 1998. Insulin-like growth factor-I stimulates gonadotropin production from eel pituitary cells: a possible metabolic signal for induction of puberty. J. Endocrinol. 159: 43–52.PubMedCrossRefGoogle Scholar
  22. Huynh, H. and Feldt, L.S. 1976. Estimation of the Box correction for degrees of freedom from sample data in the randomized block and split plot designs. J. Educ. Stat. 1: 69–82.CrossRefGoogle Scholar
  23. Jenkins, N., Joss, J.P. and Dodd, J.M. 1980. Biochemical and autoradiographic studies on the oestradiol-concentrating cells in the diencephalon and pituitary gland of the female dog-fish (Scyliorhinus canicula L.). Gen. Comp. Endocrinol. 40: 211–219.PubMedCrossRefGoogle Scholar
  24. Jobling, S., Beresford, N., Nolan, M., Rodgers-Gray, T., Brighty, G.C., Sumpter, J.P. and Tyler, C.R. 2002. Altered sexual maturation and gamete production in wild roach (Rutilus rutilus) living in rivers that receive treated sewage effluents. Biol. Reprod. 66: 272–281.PubMedCrossRefGoogle Scholar
  25. Kennedy, C.C. and Mitra, J. 1963. Body weight and food intake as initiating factors for puberty in the rat. J. Physiol. 166: 408–418.PubMedGoogle Scholar
  26. Le Bail, P.Y. 1988. Growth-reproduction interaction in salmonids. In: Reproduction in Fish - Basic and Applied Aspects in Endocrinology and Genetics. pp. 91–108. Edited by Y. Zohar and B. Breton. INRA, Paris.Google Scholar
  27. Lombardi-Carlson, L.A., Cortes, E., Parsons, G.R. and Manire, C.A. Accepted. Latitudinal variation in life-history traits of bonnethead sharks, Sphyrna tiburo (Carcharhiniformes: Sphyrnidae) from the eastern Gulf of Mexico. Mar. Freshwater Res.Google Scholar
  28. Manire, C.A. and Rasmussen, L.E.L. 1997. Serum concentrations of steroid hormones in the mature male bonnethead shark, Sphyrna tiburo. Gen. Comp. Endocrinol. 107: 414–420.PubMedCrossRefGoogle Scholar
  29. Manire, C.A., Rasmussen, L.E.L. and Gross, T.S. 1999. Serum steroid hormones including 11–ketotestosterone, 11–ketoandrostenedione and dihydroprogesterone in juvenile and adult bonnethead sharks, Sphyrna tiburo. J. Exp. Zool. 284: 595–603.PubMedCrossRefGoogle Scholar
  30. Manire, C.A., Rasmussen, L.E.L., Hess, D.L. and Hueter, R.E. 1995. Serum steroid hormones and the reproductive cycle of the female bonnethead shark, Sphyrna tiburo. Gen. Comp. Endocrinol. 97: 366–376.PubMedCrossRefGoogle Scholar
  31. Parsons, G.R. 1993. Geographic variation in reproduction between two populations of the bonnethead shark, Sphyrna tiburo. Environ. Biol. Fish. 38: 25–35.CrossRefGoogle Scholar
  32. Parsons, G.R. and Grier, H. 1992. Seasonal changes in shark testicular structure and spermatogenesis. J. Exp. Zool. 261: 173–184.CrossRefGoogle Scholar
  33. Paster, M.B. 1991. Avian reproductive endocrinology. Vet. Clin. N. Am.-Small 21: 1343–1359.Google Scholar
  34. Rasmussen, L.E.L, Hess, D.L. and Luer, C.A. 1999. Alterations in serum steroid concentrations in the clearnose skate, Raja eglanteria: correlations with season and reproductive status. J. Exp Zool. 284: 575–585.PubMedCrossRefGoogle Scholar
  35. Rowe, D.K. and Thorpe, J.E. 1990. Suppression of maturation in male Atlantic salmon (Salmo salar L.) parr by reduction in feeding and growth during spring months. Aquaculture 86: 291–313.CrossRefGoogle Scholar
  36. Silver, R. 1993. Environmental factors influencing hormone secretion. In: Behavioral Endocrinology. pp. 401–422. Edited by J.B. Becker, S.M. Breedlove and D. Crews. MIT Press, Cambridge.Google Scholar
  37. Sisneros, J.A. and Tricas, T.C. 2000. Androgen-induced changes in the response dynamics of ampullary electrosensory primary afferent neurons. J. Neurosci. 20: 8586–8595.PubMedGoogle Scholar
  38. Snelson, F.F., Jr., Rasmussen, L.E.L., Johnson, M.R. and Hess, D.L. 1997. Serum concentrations of steroid hormones during reproduction in the Atlantic stingray, Dasyatis sabina. Gen. Comp. Endocrinol. 108: 67–79.PubMedCrossRefGoogle Scholar
  39. Sourdaine, P., Garnier, D.H. and Jegou, B. 1990. The adult dog-fish (Scyliorhinus canicula L.) testis: a model to study stagedependent changes in steroid levels during spermatogenesis. J. Endocrinol. 127: 451–460.PubMedCrossRefGoogle Scholar
  40. Sourdaine, P. and Garnier, D.H. 1993. Stage-dependent modulation of Sertoli cell steroid production in dogfish (Scyliorhinus canicula). J. Reprod. Fertil. 97: 133–142.PubMedCrossRefGoogle Scholar
  41. Thorpe, J.E., Talbot, C., Miles, M.S, and Keay, D.S. 1990. Control of maturation in cultured Atlantic salmon, Salmo salar, in pumped seawater tanks, by restricting food intake. Aquaculture 86: 315–326.CrossRefGoogle Scholar
  42. Tricas, T.C., Maruska, K.P. and Rasmussen, L.E. 2000. Annual cycles of steroid hormone production, gonad development, and reproductive behavior in the Atlantic stingray. Gen. Comp. Endocrinol. 118: 209–225.PubMedCrossRefGoogle Scholar
  43. Tricas, T.C., Michael, S.W. and Sisneros, J.A. 1995. Electrosensory optimization to conspecific phasic signals for mating. Neurosci. Lett. 202: 129–131.PubMedCrossRefGoogle Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  • J. Gelsleichter
    • 1
  • L.E.L. Rasmussen
    • 2
  • C.A. Manire
    • 1
  • J. Tyminski
    • 1
  • B. Chang
    • 3
  • L. Lombardi-Carlson
    • 4
  1. 1.Elasmobranch Physiology and Environmental Biology Program, Center for Shark Research, Mote Marine LaboratorySarasotaUSA
  2. 2.Department of Chemistry, Biochemistry, and Molecular BiologyOregon Graduate InstitutePortlandUSA
  3. 3.Stanford UniversityStanfordUSA
  4. 4.National Marine Fisheries Service, Southeastern Fisheries Science CenterPanama CityUSA

Personalised recommendations