Marine Biology

, Volume 144, Issue 5, pp 845–853 | Cite as

An annual cycle of steroid hormone concentrations and gonad development in the winter skate, Leucoraja ocellata, from the western Gulf of Maine

  • J. A. Sulikowski
  • P. C. W. Tsang
  • W. Huntting Howell
Research Article

Abstract

The winter skate, Leucoraja ocellata (Mitchill, 1815) is a large oviparous skate that is endemic to inshore waters of the western North Atlantic. The reproductive cycle of this species was characterized in monthly samples taken off the coast of New Hampshire, USA (42°15′N; 70°25′W), at depths of 9–107 m from November 2000 to October 2001. Plasma concentrations of the sex steroids testosterone (T), 17β-estradiol (E2), and progesterone (P4) were determined by radioimmunoassay in mature male and female skates. Changes in ovary weight, shell gland weight, and follicle size for 66 female skates were compared to patterns of all three steroid hormones. Beginning in January, ovary weight, shell gland weight, average diameter of the largest follicle, and plasma E2 increased steadily, culminating in a transient peak in July. This peak was followed by a steady decline in plasma E2 concentrations, which returned to the lowest values in December. Although T concentrations fluctuated throughout the year, a low concentration in July coincided with a peak in E2. Skates sampled in September, October, and November had the highest P4 concentrations, coinciding with the period of egg-case production. For males (n=64), annual cycles of T and E2 were compared to stages of spermatogenic development. Testosterone concentrations displayed two peaks, one in December/January and the other in July, which were associated with maximum spermatocyst concentration, while E2 peaks in February, June, and October coincided with maximum spermatocyte concentration. Along with our observations that some reproductive individuals were present throughout the year, these findings suggest that the winter skate has a partially defined reproductive cycle.

Supplementary material

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References

  1. Borg B (1994) Androgens in teleost fishes. Comp Biochem Physiol 109C:219–245Google Scholar
  2. Callard G, Pudney JA, Mak P, Canick JA (1985) Stage-dependent changes in steroidogenic enzymes and estrogen receptors during spermatogenesis in the testis of the dogfish Squalus acanthias. Endocrinology 117:1328–1335PubMedGoogle Scholar
  3. Callard IP, Fileti LA, Perez LE, Sorbera LA, Gianmoukos G, Klosterman LL, Tsang P, McCracken JA (1992) Role of the corpus luteum and progesterone in the evolution of vertebrate viviparity. Am Zool 32:264–275Google Scholar
  4. Collette B, Klein-MacPhee G (eds) (2002) Bigelow and Schroeder’s fishes of the Gulf of Maine, 3rd edn. Smithsonian Institution Press, Washington, D.C., USAGoogle Scholar
  5. Conrath CL, Musick JA (2002) Reproductive biology of the smooth dogfish, Mustelus canis, in the northwest Atlantic Ocean. Environ Biol Fishes 64:367–377CrossRefGoogle Scholar
  6. Craik JCA (1978) An annual cycle of vitellogenesis in the elasmobranch Scyliorhinus canicula. J Mar Biol Assoc UK 58:719–726Google Scholar
  7. Cuevas ME, Callard GV (1989) In vitro secretion by Sertoli/germ cell units (spermatocysts) derived from dogfish (Squalus acanthias) testis. Bull Mt Desert Isl Biol Lab 28:30–31Google Scholar
  8. Du Bois W, Mak P, Callard GV (1989) Sertoli cell function during spermatogenesis: the shark testis model. Fish Physiol Biochem 7:221–227Google Scholar
  9. Fasano S, D’Antonio M, Pierantoni R, Chieffi G (1992) Plasma and follicular tissue steroid levels in the elasmobranch fish Torpedo marmorata. Gen Comp Endocrinol 85:327–333PubMedGoogle Scholar
  10. Gay VL, Kerlan JT (1978) Serum LH and FSH following passive immunization against circulating testosterone in the intact male rat and in orchidectomized rats bearing subcutaneous silastic implants of testosterone. Arch Androl 1:257–266PubMedGoogle Scholar
  11. Gibori G, Antczak E, Rothchild I (1997) The role of estrogen in regulation of luteal progesterone secretion in the rat after day 12 of pregnancy. Endocrinology 100:1483–1495Google Scholar
  12. Goldberg MJ, Moses MA, Tsang PCW (1996) Identification of matrix metalloproteinases and metalloproteinase inhibitors in bovine corpora lutea and their variation during the estrous cycle. J Anim Sci 74:849–857PubMedGoogle Scholar
  13. Hamlett WC, Koob TJ (1999) Female reproductive system. In: Hamlett WC (ed) Sharks, skates and rays; the biology of elasmobranch fish. Johns Hopkins University Press, Baltimore, Md., USAGoogle Scholar
  14. Henderson AC, Casey A (2001) Reproduction and growth in the lesser-spotted dogfish Scyliorhinus canicula (Elasmobranchii: Scyliorhinidae), from the west coast of Ireland. Cah Biol Mar 42:397–405Google Scholar
  15. Heupel MR, Whittier JM, Bennett MB (1999) Plasma steroid hormone profiles and reproductive biology of the epaulette shark, Hemiscyllium ocellatum. J Exp Zool 284:586–594CrossRefPubMedGoogle Scholar
  16. Johnson GF (1979) The biology of the little skate, Raja erinacea, in Block Island Sound, Rhode Island. MA thesis, University of Rhode Island, Kingston, R.I., USAGoogle Scholar
  17. Koob TJ, Tsang P, Callard IP (1986) Plasma estradiol, testosterone and progesterone levels during the ovulatory cycle of the little skate, Raja erinacea. Biol Reprod 35:267–275PubMedGoogle Scholar
  18. Korenman SG, Stevens RH, Carpenter LA, Robb M, Niswender GD, Sherman BM (1974) Estradiol radioimmunoassay without chromatography: procedure validation and normal values. J Clin Endocrinol Metab 38:718–720PubMedGoogle Scholar
  19. Manire CA, Rasmussen LEL, Hess DL, Hueter HE (1995) Serum steroid hormones and the reproductive cycle of the female bonnet head shark, Sphyrna tiburo. Gen Comp Endocrinol 97:366–376CrossRefPubMedGoogle Scholar
  20. 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 284:595–603CrossRefPubMedGoogle Scholar
  21. Martin LK (1982) Growth and reproduction of the bat ray, Myliobatis californica, gill, in California. MA thesis, San Jose State University and Moss Landing Marine Laboratory, Monterey Bay, Calif., USAGoogle Scholar
  22. Maruska KP, Cowie EG, Tricas TC (1996) Periodic gonadal activity and protracted mating in elasmobranch fishes. J Exp Zool 276:219–232CrossRefGoogle Scholar
  23. Northeast Fisheries Science Center (1999) 30th Northeast Regional Stock Assessment Workshop. NFSC, Woods Hole, Mass., USAGoogle Scholar
  24. Parsons GR, Grier HJ (1992) Seasonal changes in the shark testicular structure and spermatogenesis. J Exp Zool 261:173–184Google Scholar
  25. Rasmussen LEL, Gruber SH (1993) Serum concentrations of reproductively related circulating steroid hormones in the free ranging lemon shark, Negaprion brevirostris. Environ Biol Fishes 38:167–174Google Scholar
  26. Rasmussen LEL, Murru FL (1992) Long term studies of serum concentrations of reproductively related steroid hormones in individual captive carcharhinids. Aust J Mar Freshw Res 43:273–281Google Scholar
  27. 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 284:575–585CrossRefPubMedGoogle Scholar
  28. Richards SW, Merriman D, Calhoun LH (1963) Studies in the marine resources of southern New England. IX. The biology of the little skate Raja erinacea, Mitchill. Bull Bingham Oceanogr Collect Yale Univ 18:311–407Google Scholar
  29. Robins CR, Ray GC (1986) A field guide to Atlantic coast fishes of North America. Houghton Mifflin, Boston, Mass., USAGoogle Scholar
  30. Simon JE, Frank KT (1998) Assessment of the winter skate fishery in division 4VsW. DFO Atl Fish Res Doc 98/145Google Scholar
  31. Snelson FF Jr, Williams-Hopper SE, Schmid TH (1988) Reproduction and ecology of the Atlantic stingray, Dasyatis sabina, in Florida coastal lagoons. Copeia 3:729–739Google Scholar
  32. 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 108:67–79CrossRefPubMedGoogle Scholar
  33. Sulikowski JA, Morin MD, Suk SH, Howell WH (2003) Age and growth of the winter skate, Leucoraja ocellata, in the Gulf of Maine. Fish Bull (Wash DC) 101:405–413Google Scholar
  34. Sumpter JP, Dodd JM (1979) The annual reproductive cycle of the female lesser spotted dogfish, Scyliorhinus canicula, and its endocrine control. J Fish Biol 15:687–695Google Scholar
  35. Teshima K (1981) Studies on the reproduction of the Japanese smooth dogfishes, Mustelus manazo and Mustelus griseus. J Shimonoseki Coll Fish 29:113–199Google Scholar
  36. 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 118:209–225CrossRefPubMedGoogle Scholar
  37. Tsang P, Callard IP (1982) Steroid production by isolated skate ovarian follicular cells. Bull Mt Desert Isl Biol Lab 22:96–97Google Scholar
  38. Tsang P, Callard IP (1987) Morphological and endocrine correlates of the reproductive cycle of the aplacental viviparous dogfish, Squalus acanthias. Gen Comp Endocrinol 66:182–189PubMedGoogle Scholar
  39. Tsang PCW, Callard IP (1992) Regulation of ovarian steroidogenesis in vitro in the viviparous shark, Squalus acanthias. J Exp Zool 261:97–104PubMedGoogle Scholar
  40. Wourms JP (1977) Reproduction and development in chondrichthyan fishes. Am Zool 17:379–410Google Scholar
  41. Wourms JP, Demski LS (1993) The reproduction and development of sharks, skates, rays and ratfishes: introduction, history, overview and future prospects. Environ Biol Fishes 38:7–21Google Scholar
  42. Yoccoz NG (1991) Use, overuse, and misuse of significance tests in evolutionary biology and ecology. Bull Ecol Soc Am 71:106–111Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • J. A. Sulikowski
    • 1
  • P. C. W. Tsang
    • 2
  • W. Huntting Howell
    • 1
  1. 1.Zoology DepartmentUniversity of New HampshireDurhamUSA
  2. 2.Department of Animal and Nutritional SciencesUniversity of New HampshireDurhamUSA

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