Serum levels of reproductive steroid hormones in captive sand tiger sharks, Carcharias taurus (Rafinesque), and comments on their relation to sexual conflicts

  • A. D. HenningsenEmail author
  • F. L. Murru
  • L. E. L. Rasmussen
  • B. R. Whitaker
  • G. C. Violetta


Levels of reproductively-related steroids were determined in captive male sand tiger sharks, Carcharias taurus, maintained at two institutions: SeaWorld Adventure Park Orlando and the National Aquarium in Baltimore. Sexual conflicts were absent at the former, but were documented at the latter. Serum titers of 17β-estradiol, progesterone, testosterone, and 5α-dihydrotestosterone were determined via radioimmunoassay in adult male sharks from 1988 to 2000. Sampling overlap between the two institutions occurred for 3 months of the year, but steroid concentrations were compared only for April due to the occurrence of sexual conflicts in the sharks at the National Aquarium in Baltimore in that month. For April, testosterone and dihydrotestosterone were significantly higher in the SeaWorld males, and progesterone was significantly higher in the National Aquarium in Baltimore males, while estradiol was not significantly different. Steroid levels were also determined from serial samples taken monthly over 17 months from three male sharks and one female shark at the National Aquarium in Baltimore in 2001–2002 and were compared with corresponding observed sexual conflicts. The steroid levels obtained showed distinct annual hormonal cycles in the male sharks and corroborated a biennial cycle for the single serially-sampled female shark. Furthermore, the steroid levels for individual males correlated with sexual conflicts as well as their position within the male dominance hierarchy. As this species is depleted in some regions globally, insight into the steroid profile of mature sand tiger sharks is important for a greater understanding of the relationship between their reproductive physiology and behavior, and may aid in captive management and reproduction.


Dihydrotestosterone Elasmobranch Hormone Progesterone Reproduction Sexual conflict Testosterone 



This work was supported by a NAIB Biological Programs Research Grant to ADH. We thank the Fishes and Animal Health departments at the NAIB for invaluable assistance in obtaining samples from the sharks. In addition, we thank SeaWorld Adventure Parks for the use of data from their sharks for comparison. Valuable suggestions provided by two anonymous reviewers and V. Lounsbury are sincerely appreciated. Finally, the paper is dedicated to the memory of Bets Rasmussen, a wonderful scientist whose dedication and insight led to significant advances in our understanding of the reproductive biology of both elasmobranchs and elephants.


  1. Branstetter S, Musick JA (1994) Age and growth estimates for the sand tiger in the Northwest Atlantic Ocean. Trans Am Fish Soc 123:242–254CrossRefGoogle Scholar
  2. Carrier JC, Pratt HL Jr, Castro JI (2004) Reproductive biology of elasmobranchs. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC, Boca RatonGoogle Scholar
  3. Castro JI (1983) The sharks of North American waters. Texas A&M University Press, College StationGoogle Scholar
  4. Dicken ML, Smale MJ, Booth AJ (2006) Spatial and seasonal distribution patterns of the ragged-tooth shark Carcharias taurus along the coast of South Africa. Afr J Mar Sci 28(3):603–616Google Scholar
  5. Garnier DH, Sourdaine P, Jégou B (1999) Seasonal variations in sex steroids and male sexual characteristics in Sclyliorhinus canicula. Gen Comp Endocrinol 116:281–290PubMedCrossRefGoogle Scholar
  6. Gelsleichter J (2004) Hormonal regulation of elasmobranch physiology. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC, Boca RatonGoogle Scholar
  7. Gelsleichter J, Rasmussen LEL, Manire CA, Tyminski J, Chang B, Lombardi-Carlson L (2002) Serum steroid concentrations and development of reproductive organs during puberty in male bonnethead sharks, Sphyrna tiburo. Fish Physiol Biochem 26:389–401CrossRefGoogle Scholar
  8. Gilmore RG (1993) Reproductive biology of lamnoid sharks. Environ Biol Fish 38:95–114CrossRefGoogle Scholar
  9. Gilmore RG, Dodrill JW, Linley PA (1983) Reproduction and embryonic development of the sand tiger shark, Odontaspis taurus (Rafinesque). Fish Bull 81(2):201–225Google Scholar
  10. Goldman KJ, Branstetter S, Musick JA (2006) A re-examination of the age and growth of sand tiger sharks, Carcharias taurus, in the western North Atlantic: the importance of ageing protocols and use of multiple back-calculation techniques. Environ Biol Fish 77(3–4):241–252CrossRefGoogle Scholar
  11. Gordon I (1993) Pre-copulatory behavior of captive sand tiger sharks, Carcharias taurus. Environ Biol Fish 38:159–164CrossRefGoogle Scholar
  12. Henningsen AD, Smale M, Garner R, Gordon I, Marin-Osorno R, Kinnunen N (2004) Captive breeding and sexual conflict. In: Smith M, Warmolts D, Thoney D, Hueter R (eds) Elasmobranch husbandry manual. Ohio Biological Survey, ColumbusGoogle Scholar
  13. Heupel MR, Whittier JM, Bennett MB (1999) Plasma steroid hormone profiles and reproductive biology of the epaulette shark, Hemiscyllium ocellatum. J Exp Zool 284:586–594PubMedCrossRefGoogle Scholar
  14. Lucifora LO, Menni RC, Escalante AH (2002) Reproductive ecology and abundance of the sand tiger shark, Carcharias taurus, from the southwestern Atlantic. ICES J Mar Sci 59:553–561CrossRefGoogle Scholar
  15. Manire CA, Rasmussen LEL (1997) Serum concentrations of steroid hormones in the mature male bonnethead shark, Sphyrna tiburo. Gen Comp Endocrinol 107:414–420PubMedCrossRefGoogle Scholar
  16. Manire CA, Rasmussen LEL, Hess DL, Hueter RE (1995) Serum steroid hormones and the reproductive cycle of the female bonnethead shark, Sphyrna tiburo. Gen Comp Endocrinol 97:366–376PubMedCrossRefGoogle Scholar
  17. Manire CA, Rasmussen LEL, Gross TS (1999) Serum steroid hormones including 11-ketotestosterone, 11-ketoandrostenedione and dihydroprogesterone in juvenile and adult bonnethead sharks, Sphyrna tiburo. J Exp Zool 284:595–603PubMedCrossRefGoogle Scholar
  18. Pollard DA, Lincoln Smith MP, Smith AK (1996) The biology and conservation status of the grey nurse shark (Carcharias taurus Rafinesque 1810) in New South Wales, Australia. Aquat Conserv Mar Freshw Ecosyst 6:1–20CrossRefGoogle Scholar
  19. Pratt HL Jr, Carrier JC (2001) A review of elasmobranch reproductive behavior with a case study of the nurse shark, Ginglymostoma cirratum. Environ Biol Fish 60:157–188CrossRefGoogle Scholar
  20. Pratt HL Jr, Carrier JC (2005) Elasmobranch courtship and mating behavior. In: Hamlett WC (ed) Reproductive biology and phylogeny of Chondrichthyes. Science. QueenslandGoogle Scholar
  21. Rasmussen LEL, Gruber SH (1990) Serum levels of circulating steroid hormones in free-ranging carcharhinoid sharks. In: Pratt HL Jr, Gruber SH, Taniuchi T (eds) Elasmobranchs as living resources: advances in the biology, ecology, systematics, and the status of the fisheries. NOAA technical Report NMFS 90. US Department of Commerce, pp 143–155Google Scholar
  22. Rasmussen LEL, Gruber SH (1993) Serum concentrations of reproductively-related circulating steroid hormones in the free-ranging lemon shark, Negaprion brevirostris. Environ Biol Fish 38:167–174CrossRefGoogle Scholar
  23. Rasmussen LEL, Murru FL (1992) Long-term studies of serum concentrations of reproductively related steroid hormones in individual captive carcharhinids. Austr J Mar Freshw Res 43:273–281CrossRefGoogle Scholar
  24. Rasmussen LEL, Hess DL, Luer CA (1999) Alterations in serum steroid concentrations in the clearnose skate, Raja eglanteria: correlations with season and reproductive status. J Exp Zool 284:575–585PubMedCrossRefGoogle Scholar
  25. Sabalones J (1995) Considerations on the husbandry of sharks for display purposes. Int Zool Yearbook 34:77–87CrossRefGoogle Scholar
  26. Sartor JS, Ball GF (2005) Social suppression of song is associated with a reduction in volume of a song-control nucleus in European starlings (Sturnus vulgaris). Behav Neurosci 119(1):233–244PubMedCrossRefGoogle Scholar
  27. Sisneros JA, Tricas TC (2000) Androgen-induced changes in the response dynamics of ampullary electrosensory primary afferent neurons. J Neurosci 20(22):8586–8595PubMedGoogle Scholar
  28. Snelson FF Jr, Rasmussen LEL, Johnson MR, Hess DL (1997) Serum concentrations of steroid hormones during reproduction in the Atlantic stingray, Dasyatis sabina. Gen Comp Endocrinol 108:67–79PubMedCrossRefGoogle Scholar
  29. Stoskopf MK (1993) Shark pharmacology and toxicology. In: Stoskopf MK (ed) Fish medicine. Saunders, PhiladelphiaGoogle Scholar
  30. Sulikowski JA, Kneebone J, Elzey S, Howell WH, Tsang PCW (2006) Using the composite parameters of reproductive morphology, histology and steroid hormones to determine age and size at sexual maturity for the thorny skate, Amblyraja radiata, in the western Gulf of Maine. J Fish Biol 69:1449–1465CrossRefGoogle Scholar
  31. Sulikowski JA, Driggers WB, Ingram GW, Kneebone J, Ferguson DE, Tsang PCW (2007) Profiling plasma steroid hormones: a non-lethal approach for the study of skate reproductive biology and its potential use in conservation management. Environ Biol Fish 80(2–3):285–292CrossRefGoogle Scholar
  32. Tricas TC, Maruska KP, Rasmussen LEL (2000) Annual cycles of steroid hormone production, gonad development, and reproductive behavior in the Atlantic stingray. Gen Comp Endocrinol 118:209–225PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • A. D. Henningsen
    • 1
    Email author
  • F. L. Murru
    • 2
  • L. E. L. Rasmussen
    • 3
  • B. R. Whitaker
    • 1
    • 4
  • G. C. Violetta
    • 5
  1. 1.Biological Programs, National Aquarium in BaltimoreBaltimoreUSA
  2. 2.Kerzner InternationalPlantationUSA
  3. 3.Oregon Graduate Institute of Science and TechnologyBeavertonUSA
  4. 4.Center of Marine Biotechnology, University of MarylandBaltimoreUSA
  5. 5.SeaWorld Adventure Park, OrlandoOrlandoUSA

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