Fish Physiology and Biochemistry

, Volume 39, Issue 5, pp 1089–1099 | Cite as

Using estradiol and progesterone concentrations to assess individual variability in the reproductive cyclicity of captive female little skates, Leucoraja erinacea, from the western Gulf of Maine

  • Laura Jay Williams
  • Matthew D. Campbell
  • Paul C. W. Tsang
  • James A. Sulikowski


In the current study, plasma steroid hormones were used to assess the individual variability of Leucoraja erinacea over the course of 12 months, in hopes of further defining its reproductive cycle. No statistical differences in hormone concentrations were observed between the isolated and non-isolated female skates. Monthly E2 concentrations ranged from 1,430 pg ml−1 in August to 3,940 pg ml−1 in March, indicating the presence of mature ovarian follicles and supporting the conclusions from previous studies that L. erinacea is capable of reproducing year-round. Concentrations of E2 were significantly elevated or depressed during some months (February, March, June, July, August, and September) of the year, suggesting that reproductive activity may vary over the annual cycle. Even though monthly P4 concentrations were highly variable, ranging from 82 pg ml−1 in November to 816 pg ml−1 in September, no significant reproductive peaks were observed. In addition, a persistently large variation in E2 and P4 concentrations, indicative of reproductive asynchrony within (mean CV 62 % and CV 69 %, respectively) and between (mean range CV 78 and 125 %, respectively) individual skates, was observed throughout the study. Collectively, the continually high E2 concentrations and variability in both hormones observed in the current study are indicative of an oviparous species that reproduces actively throughout the year. However, the weekly sampling frequency revealed that plasma E2 concentrations, not P4, were more useful to assess reproductive status in asynchronous continuously breeding oviparous elasmobranchs.


Life history Radioimmunoassay Rajidae Steroid hormones 



We would like to thank captain J. Jurek of the F.V. “Mystique Lady” and Puggy Jr. of the F.V. “Lady Victoria” for collection of the little skates and the University of New England’s Graduate School and Marine Science Center for funding and use of the wet laboratory facilities. We would also like to extend our gratitude to K. Coutré, R. Knotek, C. Peterson, and A. Traverse-Taylor for assisting with the collection and processing of samples and Dr. David Koester for his thoughtful review of this manuscript. This manuscript represents MSC contribution number 48.


  1. Awruch CA, Frusher SD, Pankhurst NW, Stevens JD (2008) Non-lethal assessment of reproductive characteristics for management and conservation of sharks. Mar Ecol Prog Ser 355:277–285. doi: 10.3354/meps07227 CrossRefGoogle Scholar
  2. Bigelow HB, Schroeder WC (1953) Fishes of the Gulf of Maine. Fisheries Bulletin, U.S. Fisheries Wildlife Service, Revision 1.0, 74:577Google Scholar
  3. Castro JI (1996) Biology of the blacktip shark, Carcharhinus limbatus, off the Southeastern United States. Bull Mar Sci 59:508–522Google Scholar
  4. Cicia AM, Driggers WB III, Ingram GW Jr, Kneebone J, Tsang PCW, Koester DM, Sulikowski JA (2009) Size and age estimates at sexual maturity for the little skate Leucoraja erinacea from the western Gulf of Maine, U.S.A. J Fish Biol 75:1648–1666. doi: 10.1111/j.1095-8649.2009.02392.x PubMedCrossRefGoogle Scholar
  5. Colonello JH, Lucifora LO, Massa AM (2007) Reproduction of the angular angel shark (Squatina guggenheim) geographic differences, reproductive cycle, and sexual dimorphism. ICES J Mar Sci 64:131–140. doi: 10.1093/icesjms/fsl004 Google Scholar
  6. Compagno LJV (2001) Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Vol. 2. Bullhead, mackerel and carpet sharks (Heterodontiformes, Lamniformes and Orectolobiformes). FAO Species Catalogue for Fishery Purposes No. 1, Rome, p 269Google Scholar
  7. Dulvy NK, Reynolds JD (2002) Predicting extinction vulnerability in skates. Conserv Biol 16:440–450. doi: 10.1046/j.1523-1739.2002.00416.x CrossRefGoogle Scholar
  8. Dulvy NK, Metcalfe JD, Glanville J, Pawson MG, Reynolds JD (2000) Fishery stability, local extinctions, and shifts in community structure in skates. Conserv Biol 14:283–293. doi: 10.1046/j.1523-1739.2000.98540.x CrossRefGoogle Scholar
  9. Dulvy NK, Sadovy Y, Reynolds JD (2003) Extinction vulnerability in marine populations. Fish Fish 4:25–64. doi: 10.1046/j.1467-2979.2003.00105.x CrossRefGoogle Scholar
  10. Francis MP, Maolagáin CO, Stevens D (2001) Age, growth, and sexual maturity of two New Zealand endemic skates, Dipturus nasutus and D. innominatus. NZ J Mar Fresh Res 35:831–842. doi: 10.1080/00288330.2001.9517045 CrossRefGoogle Scholar
  11. Grainger RJR, Garcia SM (1996) Chronicles of marine fishery landings (1950–1994): Trend analysis and fisheries potential. FAO Fish Tech T359, p 51Google Scholar
  12. Hamlett WC (2005) Reproductive biology and phylogeny of Chondrichthyes: Sharks, Batoids and Chimeras. Science Publishers, Inc., Enfield, pp 171–299Google Scholar
  13. Hammerschlag N, Sulikowski J (2011) Killing for conservation: the need for alternatives to lethal sampling of apex predatory sharks. Endanger Species Res 14:135–140. doi: 10.3354/esr00354 CrossRefGoogle Scholar
  14. Heupel MR, Simpfendorfer CA (2010) Science or slaughter: need for lethal sampling of sharks. Conserv Biol 24:1212–1218. doi: 10.1111/j.1523-1739.2010.01491.x PubMedCrossRefGoogle 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 284:586–594PubMedCrossRefGoogle Scholar
  16. Johnson GF (1979) The biology of the little skate, Raja erinacea Mitchill 1825, in Block Island Sound, Rhode Island. Master’s thesis. University of Rhode Island, KingstonGoogle Scholar
  17. Kneebone J, Ferguson DE, Sulikowski JA, Tsang PCW (2007) Endocrinological investigation into the reproductive cycles of two sympatric skate species, Malacoraja senta and Amblyraja radiata, in the western Gulf of Maine. Environ Biol Fishes 80:257–265. doi: 10.1007/978-1-4020-9703-4_10 CrossRefGoogle Scholar
  18. Koob TJ, Callard IP (1999) Reproductive endocrinology of female elasmobranchs: lessons from the little skate (Raja erinacea) and spiny dogfish (Squalus acanthias). J Exp Zool 284:557–574. doi: 10.1002/(SICI)1097-010X(19991001)284:5<557:AID-JEZ12>3.0.CO;2-P PubMedCrossRefGoogle Scholar
  19. Koob TJ, Tsang P, Callard IP (1986) Plasma estradiol, testosterone and progesterone levels during the ovulatory cycle of the skate (Raja erinacea). Biol Reprod 35:267–275. doi: 10.1095/biolreprod35.2.267 PubMedCrossRefGoogle Scholar
  20. Leonard JBK, Summers AP, Koob TJ (1999) Metabolic rate of embryonic little skate, Raja erinacea (Chondrichthyes: Batiodea): the cost of active pumping. J Exp Zool 283:13–18CrossRefGoogle Scholar
  21. 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 97:366–376. doi: 10.1006/gcen PubMedCrossRefGoogle Scholar
  22. McEachran JD, Musick JA (1975) Distribution and relative abundance of seven species of skates (Pisces: Rajidae) which occur between Nova Scotia and Cape Hatteras. Fish Bull 73:110–136Google Scholar
  23. Natanson LJ, Sulikowski JA, Kneebone JR, Tsang PC (2007) Age and growth estimates for the smooth skate, Malacoraja senta, in the Gulf of Maine. Environ Biol Fishes 80:293–308. doi: 10.1007/s10641-007-9220-y CrossRefGoogle Scholar
  24. Oddone MC, Amorim AF, Mancini PL, Norbis W, Velasco G (2007) The reproductive biology and cycle of Rioraja agassizi (Müller and Henle, 1841) (Chondrichthyes: Rajidae) in southeastern Brazil, SW Atlantic Ocean. Scientia Marina 71:593–604. doi: 10.3989/scimar.2007.71n3593 CrossRefGoogle Scholar
  25. Palm BD, Koester DM, Driggers WB, Sulikowski JA (2011) Seasonal variation in fecundity, egg case viability, gestation, and neonate size for little skates, Leucoraja erinacea, in the Gulf of Maine. Environ Biol Fishes 92:585–589. doi: 10.1007/s10641-011-9854-7 CrossRefGoogle Scholar
  26. Perez LE, Callard IP (1992) Identification of vitellogenin in the little skate (Rajah erinacea). Comp Biochem Physiol B 103:699–705. doi: org/10.1016/0305-0491(92)90393-6 PubMedGoogle Scholar
  27. Rasmussen LEL, Gruber SH (1993) Serum concentrations of reproductively-related circulating steroid hormones in the free-ranging lemon shark, Negaprion brevirostris. Environ Biol Fishes 38:167–174. doi: 10.1007/BF00842913 CrossRefGoogle Scholar
  28. 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 43:273–281. doi: 10.1071/MF9920273 CrossRefGoogle Scholar
  29. 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 284:575–585. doi: 10.1002/(SICI)1097-010X(19991001)284:5<575:AID-JEZ13>3.0.CO;2-I PubMedCrossRefGoogle Scholar
  30. Richards S, Merriman D, Calhoun LH (1963) Studies on the marine resources of southern New England. IX. The biology of the little skate, Raja erinacea, Mitchell. Bull Bingham Oceanogr Collect 18:5–67Google Scholar
  31. Ruocco NL, Lucifora LO, Díaz de Astarloa JM, Wöhler O (2006) Reproductive biology and abundance of the white-dotted skate, Bathyraja albomaculata, in the Southwest Atlantic. ICES J Mar Sci 63:105–116. doi: 10.1016/j.icesjms.2005.08.007 CrossRefGoogle 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 108:67–79. doi: 10.1006/gcen.1997.6949 PubMedCrossRefGoogle Scholar
  33. Sulikowski JA, Tsang PCW, Howell WH (2004) An annual cycle of steroid hormone concentrations and gonad development in the winter skate, Leucoraja ocellata, from the western Gulf of Maine. Mar Biol 144:845–853. doi: 10.1007/s00227-003-1264-8 CrossRefGoogle Scholar
  34. Sulikowski JA, Tsang PCW, Howell WH (2005) Age and size at sexual maturity for the winter skate, Leucoraja ocellata, in the western Gulf of Maine based on morphological, histological and steroid hormone analyses. Environ Biol Fishes 72:429–441. doi: 10.1007/s10641-004-2866-9 CrossRefGoogle Scholar
  35. Sulikowski JA, Kneebone J, Elzey S, Jurek J, Howell WH, Tsang PCW (2006) Using the composite variables 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 69:1449–1465. doi: 10.1111/j.1095-8649.2006.01207.x CrossRefGoogle Scholar
  36. 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 Fishes 80:285–292. doi: 10.1007/s10641-007-9257-y CrossRefGoogle Scholar
  37. 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 118:209–225. doi: 10.1006/gcen.2000.7466 PubMedCrossRefGoogle Scholar
  38. Tsang P, Callard IP (1982) Steroid production by isolated skate ovarian follicular cells. Bull Mt Desert Isl Biol Lab 22:96–97Google Scholar
  39. Tsang PCW, Callard IP (1987a) Morphological and endocrine correlates of the reproductive cycle of the aplacental viviparous dogfish, Squalus acanthias. Gen Comp Endocrinol 66:182–189. doi: 10.1016/0016-6480(87)90266-8 PubMedCrossRefGoogle Scholar
  40. Tsang P, Callard IP (1987b) Luteal progesterone production and regulation in the viviparous dogfish, Squalus acanthias. J Exp Zool 241:377–382. doi: 10.1002/jez.1402410313 CrossRefGoogle Scholar
  41. Walker TI (2005) Reproduction in fisheries science. In Reproductive Biology and Phylogeny of Chondrichthyes: Sharks, Batoids and Chimaeras (Hamlett, W. C., volume ed.) in the series: Reproduction Biology and Phylogeny (Jamieson, B. G. M., series ed.) Plymouth: Science Publishers, Inc, pp 81–127Google Scholar
  42. Whitney NM, Crow GL (2007) Reproductive biology of the tiger shark (Galeocerdo cuvier) in Hawaii. Mar Biol 151:63–70. doi: 10.1007/s00227-006-0476-0 CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Laura Jay Williams
    • 1
  • Matthew D. Campbell
    • 2
  • Paul C. W. Tsang
    • 3
  • James A. Sulikowski
    • 1
  1. 1.Marine Science CenterUniversity of New EnglandBiddefordUSA
  2. 2.National Marine Fisheries ServiceMississippi LaboratoriesPascagoulaUSA
  3. 3.Department of Cellular, Molecular and Biomedical SciencesUniversity of New HampshireDurhamUSA

Personalised recommendations