Marine Biology

, 156:301 | Cite as

Maturity, fecundity, and reproductive cycle of the spotted ratfish, Hydrolagus colliei

  • Lewis A. K. Barnett
  • Ryan L. Earley
  • David A. Ebert
  • Gregor M. Cailliet
Original Paper

Abstract

Size at maturity, fecundity, and reproductive periodicity were estimated for the spotted ratfish, Hydrolagus colliei (Lay and Bennett, 1839), off the coast of California, Oregon, and Washington. Maximum body size and size at median maturity were greater for females than males. Skeletal muscle concentrations of the steroid hormones testosterone (T) and estradiol (E2) predicted similar, but slightly smaller sizes at maturity than the morphological criterion. Stage of maturity for males was estimated identically using internal organs or external secondary sexual characters, thus allowing non-lethal maturity assessments. Size at median maturity was greater north of Point Conception for females, and north of Cape Mendocino for males. Peak parturition occurred from May to October, with increased concentrations of E2 in skeletal muscle of females correlating with ovarian recrudescence during November to February. No significant seasonal trends in female T were apparent, but mean female 11-ketotestosterone (11KT) was 300% greater in April than any other month during the parturition season. There was a marginal evidence for increased number and size of ova with maternal size. Extrapolation of the hypothesized 6 to 8-month egg-laying season to observed mean parturition rates of captive specimens yielded an estimated annual fecundity of 19.5–28.9 egg cases. Differences in fecundity among higher taxonomic classifications of chondrichthyans were detected with chimaeriform fishes more fecund than lamniform, myliobatiform, squaliform, and rhinobatiform fishes, and less fecund than rajiform fishes.

Supplementary material

227_2008_1084_MOESM1_ESM.doc (2.1 mb)
Appendices 1 to 11 (DOC 2275 kb)

References

  1. Abrams-Motz V, Callard IP (1989) Seasonal variations in oviduct myometrial activity, extensibility and tensile strength in Chrysemys picta. Gen Comp Endocrinol 72:453–460. doi:10.1016/0016-6480(88)90168-2 Google Scholar
  2. Alverson DL, Pruter AT, Ronholt LL (1964) A study of demersal fishes and fisheries of the northeastern Pacific Ocean. H.R. MacMillan Lectures in Fisheries. Institute of Fisheries, University of British Columbia, VancouverGoogle Scholar
  3. Anon (1997) Report of the study group of elasmobranch fishes. ICES CM 1997/G:2Google Scholar
  4. 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 Google Scholar
  5. Barnett LAK, Dagit DD, Long DJ, Ebert DA (2006) Hydrolagus mccoskeri sp. nov., a new species of chimaeroid fish from the Galápagos Islands (Holocephali: Chimaeriformes: Chimaeridae). Zootaxa 1328:27–38Google Scholar
  6. Bell JD (2003) Fisheries and reproductive biology of the elephant fish, Callorhinchus milii, in south-east Australia. Bachelor of Environmental Science (honours). Deakin UniversityGoogle Scholar
  7. Berkeley SA, Chapman C, Sogard SM (2004a) Maternal age as a determinant of larval growth and survival in a marine fish, Sebastes melanops. Ecology 85:1258–1264. doi:10.1890/03-0706 Google Scholar
  8. Berkeley SA, Hixon MA, Larson RJ, Love MS (2004b) Fisheries sustainability via protection of age structure and spatial distribution of fish populations. Fisheries 29:23–32. doi:10.1577/1548-8446(2004)29[23:FSVPOA]2.0.CO;2 Google Scholar
  9. Bobko SJ, Berkeley SA (2004) Maturity, ovarian cycle, fecundity, and age-specific parturition of black rockfish (Sebastes melanops). Fish Bull (Wash DC) 102:418–429Google Scholar
  10. Boehlert GW, Barss WH, Lamberson PB (1982) Fecundity of the widow rockfish, Sebastes entomelas, off the coast of Oregon. Fish Bull (Wash DC) 80:881–884Google Scholar
  11. Bonfil R (1994) Overview of world elasmobranch fisheries. FAO Technical Paper 341Google Scholar
  12. Borg B (1987) Stimulation of reproductive behaviour by aromatizable and non-aromatizable androgens in the male three-spined stickleback, Gasterosteus aculeatus L. In: Kullander SOK, Fernholm B (eds) Proceedings of the 5th Congress European Ichthyol Stockholm. Swedish Museum of Natural History, Stockholm, pp 269–271Google Scholar
  13. Borg B (1994) Androgens in teleost fishes. Comp Biochem Physiol. C Toxicol Pharmacol 109:219–245Google Scholar
  14. Borg B, Antonopoulou E, Andersson E, Carlberg T, Mayer I (1993) Effectiveness of several androgens in stimulating kidney hypertrophy, a secondary sexual character, in castrated male three-spined stickleback, Gasterosteus aculeatus. Can J Zool/Rev Can Zool 71:2327–2329Google Scholar
  15. Cailliet GM (1990) Elasmobranch age determination and verification: an updated review. In: Pratt Jr HL, Gruber SH, Taniuchi T (eds) Elasmobranchs as living resources: advances in the biology, ecology, systematics, and the status of the fisheries. NOAA Technical Report 90, pp 157–165Google Scholar
  16. Cailliet GM, Goldman KJ (2004) Age determination and validation in chondrichthyan fishes. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, FL, pp 399–448Google Scholar
  17. Cailliet GM, Andrews AH, Burton EJ, Watters DL, Kline DE, Ferry-Graham LA (2001) Age determination and validation studies of marine fishes: do deep-dwellers live longer? Exp Gerontol 36:739–764. doi:10.1016/S0531-5565(00)00239-4 PubMedGoogle Scholar
  18. Callard IP, Etheridge K, Giannoukos G, Lamb T, Perez L (1991) The role of steroids in reproduction in female elasmobranchs and reptiles. J Steroid Biochem Mol Biol 40:571–575. doi:10.1016/0960-0760(91)90278-D PubMedGoogle Scholar
  19. Callard IP, Fileti LA, Koob TJ (1993) Ovarian steroid synthesis and the hormonal control of the elasmobranch reproductive tract. Environ Biol Fishes 38:175–185. doi:10.1007/BF00842914 Google Scholar
  20. Carlson JK, Parsons GR (1997) Age and growth of the bonnethead shark, Sphyrna tiburo, from northwest Florida, with comments on clinal variation. Environ Biol Fishes 50:331–341. doi:10.1023/A:1007342203214 Google Scholar
  21. Chen Y, Jackson DA, Harvey HH (1992) A comparison of von Bertalanffy and polynomial functions in modelling fish growth data. Can J Fish Aquat Sci 49:1228–1235Google Scholar
  22. Clarke MW, Kelly CJ, Connolly PL, Molloy JP (2003) A life history approach to the assessment and management of deepwater fisheries in the northeast Atlantic. Atl J Northwest Atl Fish Sci 31:401–411Google Scholar
  23. Compagno LJV (1990) Alternative life-history styles of cartilaginous fishes in time and space. Environ Biol Fishes 28:33–75. doi:10.1007/BF00751027 Google Scholar
  24. Compagno LJV (1999) Checklist of living elasmobranchs. In: Hamlett WC (ed) Sharks, skates, and rays: the biology of elasmobranch fishes. The Johns Hopkins University Press, BaltimoreGoogle Scholar
  25. Compagno LJV (2005) Checklist of living Chondrichthyes. In: Hamlett WC (ed) Reproductive biology and phylogeny of Chondrichthyes: sharks batoids and chimaeras. Science Publishers, Inc., Enfield, pp 503–548Google Scholar
  26. Conover DO, Munch SB (2002) Sustaining fisheries yields over evolutionary time scales. Science 297:94–96. doi:10.1126/science.1074085 PubMedGoogle Scholar
  27. Cooper DW, Pearson KE, Gunderson DR (2005) Fecundity of shortspine thornyhead (Sebastolobus alascanus) and longspine thornyhead (S. altivelis) (Scorpaenidae) from the northeastern Pacific Ocean, determined by stereological and gravimetric techniques. Fish Bull (Wash DC) 103:15–22Google Scholar
  28. Cortés E (2000) Life history patterns and correlations in sharks. Rev Fish Sci 8:299–344Google Scholar
  29. Craik JCA (1978) An annual cycle of vitellogenesis in the elasmobranch Scyliorhinus canicula L. J Mar Biol Assoc UK 58:719–726Google Scholar
  30. Craik JCA (1979) Simultaneous measurement of rates of vitellogenin synthesis and plasma levels of estradiol in an elasmobranch. Gen Comp Endocrinol 38:264–266. doi:10.1016/0016-6480(79)90215-6 PubMedGoogle Scholar
  31. Cross JN (1981) Structure of a rocky intertidal fish assemblage. Ph.D. Thesis, University of WashingtonGoogle Scholar
  32. Dean B (1903) An outline of the development of a chimaeroid. Biol Bull 4:270–286. doi:10.2307/1535744 Google Scholar
  33. Dean B (1906) Chimaeroid fishes and their development. Carnegie Institute Publication, Washington, DCGoogle Scholar
  34. Di Giacomo EE, Perier MR (1994) Reproductive biology of the cockfish, Callorhynchus callorhinchus (Holocephali: Callorhynchidae), in Patagonian waters (Argentina). Fish Bull (Wash DC) 92:531–539Google Scholar
  35. Didier DA (1995) Phylogenetic systematics of extant Chimaeroid fishes (Holocephali, Chimaeroidei). Am Mus Novit 3119:1–86Google Scholar
  36. Didier DA, Rosenberger LJ (2002) The spotted ratfish, Hydrolagus colliei: notes on its biology with a redescription of the species (Holocephali: Chimaeridae). Calif Fish Game 88:112–125Google Scholar
  37. Didier DA, LeClair EE, Vanbuskirk DR (1998) Embryonic staging and external features of development of the chimaeroid fish, Callorhinchus milii (Holocephali, Callorhinchidae). J Morphol 236:25–47. doi:10.1002/(SICI)1097-4687(199804)236:1<25::AID-JMOR2>3.0.CO;2-NGoogle Scholar
  38. Dodd JM, Goddard CK (1961) Some effects of oestradiol benzoate on the reproductive ducts of the female dogfish Scyliorhinus caniculus. Proc Zool Soc Lond 137:325–331Google Scholar
  39. Dulvy NK, Reynolds JD (1997) Evolutionary transitions among egg-laying, live-bearing and maternal inputs in sharks and rays. Proc R Soc Lond. Ser B Biol Sci 264:1309–1315. doi:10.1098/rspb.1997.0181 Google Scholar
  40. 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 Google Scholar
  41. Ebert DA (1996) Biology of the sevengill shark, Notorynchus cepedianus (Peron, 1807) in the temperate coastal waters of Southern Africa. S Afr J Mar Sci 17:93–103Google Scholar
  42. Ebert DA, Davis CD (2007) Descriptions of skate egg cases (Chondrichthyes: Rajiformes: Rajoidei) from the eastern North Pacific. Zootaxa 1393:1–18Google Scholar
  43. Economakis AE, Lobel PS (1998) Aggregation behavior of the grey reef shark, Carcharhinus amblyrhynchos, at Johnston Atoll, Central Pacific Ocean. Environ Biol Fishes 51:129–139. doi:10.1023/A:1007416813214 Google Scholar
  44. Edeline E, Carlson SM, Stige LC, Winfield IJ, Fletcher JM, James JB, Haugen TO, Vollestad LA, Stenseth NC (2007) Trait changes in a harvested population are driven by a dynamic tug-of-war between natural and harvest selection. Proc Natl Acad Sci USA 104:15799–15804. doi:10.1073/pnas.0705908104 PubMedGoogle Scholar
  45. FitzPatrick MS, van der Kraak G, Schreck CB (1986) Profiles of plasma sex steroids and gonadotropins in coho salmon, Oncorhynchus kisutch, during final maturation. Gen Comp Endocrinol 62:437–451. doi:10.1016/0016-6480(86)90054-7 PubMedGoogle Scholar
  46. Gordon JDM (1999) Management considerations of deepwater shark fisheries. In: Shotton R (ed) Case studies of the management of elasmobranch fisheries. FAO Fisheries Technical Paper No. 378, part 2. FAO, Rome, pp 774–818Google Scholar
  47. Gorman TBS (1963) Biological and economic aspects of the elephant fish Callorhynchus milii Bory in Pegasus Bay and the Canterbury Bight. Department of Fisheries Technical Report 8, New ZealandGoogle Scholar
  48. Grinols RB (1965) Check-list of the offshore marine fishes occurring in the northeastern Pacific Ocean, principally off the coasts of British Columbia, Washington, and Oregon. MS thesis. University of Washington, WashingtonGoogle Scholar
  49. Grogan ED, Lund R (2004) The origin and relationships of early Chondrichthyes. In: Carrier JC, Musick JA, Heithaus MR (eds) Biology of sharks and their relatives. CRC Press, Boca Raton, pp 3–32Google Scholar
  50. Heibo E, Magnhagen C, Vollestad LA (2005) Latitudinal variation in life-history traits in Eurasian perch. Ecology 86:3377–3386. doi:10.1890/04-1620 Google Scholar
  51. Heppell SA, Sullivan CV (2000) Identification of gender and reproductive maturity in the absence of gonads: muscle tissue levels of sex steroids and vitellogenin in gag (Mycteroperca microlepis). Can J Fish Aquat Sci 57:148–159. doi:10.1139/cjfas-57-1-148 Google Scholar
  52. Hishida T, Kawamoto N (1970) Androgenic and male-inducing effects of 11-ketotestosterone on a teleost, the medaka (Oryzias latipes). J Exp Zool 173:279–284. doi:10.1002/jez.1401730306 Google Scholar
  53. Ho S, Wulczyn G, Callard IP (1980) Induction of vitellogenin synthesis in the spiny dogfish, Squalus acanthias. Bull Mt Desert Isl Biol Lab 19:37–38Google Scholar
  54. Hoenig JM, Gruber SH (1990) Life history patterns in the elasmobranchs: implications for fisheries management. In: Pratt Jr HL, Gruber SH, Taniuchi T (eds) Elasmobranchs as living resources: advances in the biology, ecology, systematics, and the status of the fisheries. NOAA Technical Report 90, pp 1–16Google Scholar
  55. Hoff GR (2007) Reproductive biology of the Alaska skate Bathyraja parmifera, with regard to nursery sites, embryo development and predation. Ph.D. Thesis, University of WashingtonGoogle Scholar
  56. Holden MJ (1973) Are long-term sustainable fisheries for elasmobranchs possible? Rapp. P.-V. Reun. CIESM 164:360–367Google Scholar
  57. Holden MJ (1974) Problems in the rational exploitation of elasmobranch populations and some suggested solutions. In: Harden-Jones FR (ed) Sea fisheries research. Logos Press, London, pp 117–138Google Scholar
  58. Holden MJ (1975) The fecundity of Raja clavata in British waters. J Cons Int Explor Mer 36:110–118Google Scholar
  59. Holden MJ, Rout DW, Humphreys CN (1971) The rate of egg laying by three species of ray. J Cons Int Explor Mer 33:335–339Google Scholar
  60. Hollander M, Wolfe DA (1999) Nonparametric statistical methods. Wiley, New YorkGoogle Scholar
  61. Hothorn T, Hornik K, van de Wiel MA, Zeileis A (2006) A lego system for conditional inference. Am Stat 60(3):257–263. doi:10.1198/000313006X118430 Google Scholar
  62. Idler DR, Bitners II, Schmidt PJ (1961) 11-Ketotestosterone: an androgen for sockeye salmon. Can J Biochem Physiol 39:1737–1742Google Scholar
  63. Johnson AG, Horton HF (1972) Length-weight relationship, food habits, parasites, and sex and age determination of the ratfish, Hydrolagus colliei (Lay and Bennett). Fish Bull (Wash DC) 70:421–429Google Scholar
  64. Kime DE, Manning NJ (1982) Seasonal patterns of free and conjugated androgens in the brown trout, Salmo trutta. Gen Comp Endocrinol 48:222–231. doi:10.1016/0016-6480(82)90020-X PubMedGoogle Scholar
  65. Kindler PM, Bahr JM, Philipp DP (1991) The effect of exogenous 11-ketotestosterone, testosterone, and cyproterone acetate on prespawning and parental care behaviors of male bluegill. Horm Behav 25:410–423. doi:10.1016/0018-506X(91)90011-6 PubMedGoogle Scholar
  66. Klimley AP (1987) The determinants of sexual segregation in the scalloped hammerhead shark, Sphyrna lewini. Environ Biol Fishes 18:27–40. doi:10.1007/BF00002325 Google Scholar
  67. Kokuho T, Nakaya K, Kitagawa D (2003) Distribution and reproductive biology of the nine-spot ratfish Hydrolagus barbouri (Holocephali; Chimaeridae). Mem Grad Sch Fish Sci Hokkaido Univ 50:63–87Google Scholar
  68. 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-PPubMedGoogle Scholar
  69. Koob TJ, Laffan JJ, Callard IP (1984) Effects of relaxin and insulin on reproductive tract size and early fetal loss in Squalus acanthias. Biol Reprod 31:231–238. doi:10.1095/biolreprod31.2.231 PubMedGoogle Scholar
  70. 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 PubMedGoogle Scholar
  71. Lombardi-Carlson LA, Cortés E, Parsons GR, Manire CA (2003) Latitudinal variation in life-history traits of bonnethead sharks, Sphyrna tiburo (Carcharhiniformes: Sphyrnidae) from the eastern Gulf of Mexico. Mar Freshw Res 54:875–883. doi:10.1071/MF03023 Google Scholar
  72. Lund R, Grogan ED (1997) Relationships of the Chimaeriformes and the basal radiation of the Chondrichthyes. Rev Fish Biol Fish 7:65–123. doi:10.1023/A:1018471324332 Google Scholar
  73. Maisey JG (1984) Chondrichthyan phylogeny: a look at the evidence. J Vert Paleontol 4:359–371Google Scholar
  74. Maisey JG (1986) Heads and tails: a chordate phylogeny. Cladistics 2:201–256. doi:10.1111/j.1096-0031.1986.tb00462.x Google Scholar
  75. 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 284:595–603. doi:10.1002/(SICI)1097-010X(19991001)284:5<595::AID-JEZ15>3.0.CO;2-6PubMedGoogle Scholar
  76. Maruska KP, Cowie EG, Tricas TC (1996) Periodic gonadal activity and protracted mating in elasmobranch fishes. J Exp Zool 276:219–232. doi:10.1002/(SICI)1097-010X(19961015)276:3<219::AID-JEZ6>3.0.CO;2-QGoogle Scholar
  77. Matsubara M, Lokman PM, Senaha A, Kazeto Y, Ijiri S, Kambegawa A, Hirai T, Young G, Todo T, Adachi S, Yamauchi K (2003) Synthesis and possible function of 11–ketotestosterone during oogenesis in eel (Anguilla spp.). Fish Physiol Biochem 28:353–354. doi:10.1023/B:FISH.0000030585.22093.7a Google Scholar
  78. Matta EM (2006) Aspects of the life history of the Alaska skate, Bathyraja parmifera, in the eastern Bering Sea. MS. Thesis, University of WashingtonGoogle Scholar
  79. Mayer I, Schmitz M, Borg B, Schulz R (1992) Seasonal endocrine changes in male and female Arctic charr (Salvelinus alpinus). I. Plasma levels of three androgens, 17α-hydroxy-20β-dihydroxy-progesterone, and 17β-estradiol. Can J Zool 70:37–42. doi:10.1139/z92-006 Google Scholar
  80. Miller DJ, Lea RN (1972) Guide to the coastal marine fishes of California. California Department of Fish and Game, University of California Sea Grant Marine Advisory Program and Division of Agricultural Sciences, SacramentoGoogle Scholar
  81. Mollet HF, Cliff G, Pratt HL Jr, Stevens JD (2000) Reproductive biology of the female shortfin mako, Isurus oxyrinchus Rafinesque, 1810, with comments on the embryonic development of lamnoids. Fish Bull (Wash DC) 98:299–318Google Scholar
  82. Moura T, Figueiredo I, Machado PB, Gordo LS (2004) Growth pattern and reproductive strategy of the holocephalan Chimaera monstrosa along the Portuguese continental slope. J Mar Biol Assoc UK 84:801–804. doi:10.1017/S002531540400997Xh Google Scholar
  83. Moura T, Figueiredo I, Bordalo-Machado P, Almeida C, Gordo LS (2005) A new deep-water chimaerid species, Hydrolagus lusitanicus n. sp., from off mainland Portugal with a proposal of a new identification key for the genus Hydrolagus (Holocephali: Chimaeridae) in the north-east Atlantic. J Fish Biol 67:742–751. doi:10.1111/j.0022-1112.2005.00774.x Google Scholar
  84. Musick JA, Ellis JK (2005) Reproductive evolution of chondrichthyans. In: Hamlett WC (ed) Reproductive biology and phylogeny of chondrichthyans: sharks, batoids, and chimaeras. Science Publishers, Inc., Enfield, pp 45–71Google Scholar
  85. Neer JA, Cailliet GM (2001) Aspects of the life history of the Pacific electric ray, Torpedo californica (Ayres). Copeia 2001:842–847. doi:10.1643/0045-8511(2001)001[0842:AOTLHO]2.0.CO;2 Google Scholar
  86. Olsen EM, Heino M, Lilly GR, Morgan MJ, Brattey J, Ernande B, Dieckmann U (2004) Maturation trends indicative of rapid evolution preceded the collapse of northern cod. Nature 428:932–935. doi:10.1038/nature02430 PubMedGoogle Scholar
  87. Pankhurst NW (2008) Gonadal steroids: functions and patters of change. In: Rocha MJ, Arukwe A, Kapoor BG (eds) Fish reproduction. Science Publishers, Enfield, pp 67–111Google Scholar
  88. Pankhurst NW, McMillan PJ, Tracey DM (1987) Seasonal reproductive cycles in three commercially exploited fishes from the slope waters off New Zealand. J Fish Biol 30:193–211. doi:10.1111/j.1095-8649.1987.tb05745.x Google Scholar
  89. Parsons GR (1993) Geographic variation in reproduction between two populations of the bonnethead shark, Sphyrna tiburo. Environ Biol Fishes 38:25–35. doi:10.1007/BF00842901 Google Scholar
  90. Parsons GR, Grier HJ (1992) Seasonal changes in shark testicular structure and spermatogenesis. J Exp Zool 261:173–184. doi:10.1002/jez.1402610208 Google Scholar
  91. Pottinger TG, Pickering AD (1985) The effects of 11-ketotestosterone and testosterone on the skin structure of brown trout, Salmo trutta L. Gen Comp Endocrinol 59:335–342. doi:10.1016/0016-6480(85)90389-2 PubMedGoogle Scholar
  92. Quaranta KL, Didier DA, Long DJ, Ebert DA (2006) A new species of chimaeroid, Hydrolagus alphus sp. nov. (Chimaeriformes: Chimaeridae) from the Galapagos Islands. Zootaxa 1377:33–45Google Scholar
  93. R Development Core Team (2007) R: A language and environment for statistical computing. Version 2.4.1. R Foundation for Statistical Computing, Vienna, AustriaGoogle Scholar
  94. 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-IPubMedGoogle Scholar
  95. Roa R, Ernst B, Tapia F (1999) Estimation of size at sexual maturity: an evaluation of analytical and resampling procedures. Fish Bull (Wash DC) 97:570–580Google Scholar
  96. Roberts CM (2002) Deep impact: the rising toll of fishing in the deep sea. Trends Ecol Evol 17:242–245. doi:10.1016/S0169-5347(02)02492-8 Google Scholar
  97. Roff DA (2002) Life history evolution. Sinauer Associates, SunderlandGoogle Scholar
  98. Ruhl HA, Smith KL Jr (2004) Shifts in deep-sea community structure linked to climate and food supply. Science 305:513–515. doi:10.1126/science.1099759 PubMedGoogle Scholar
  99. de Ruiter AJH, Mein CG (1982) Testosterone-dependent changes in vivo and in vitro. Gen Comp Endocrinol 47:70–83PubMedGoogle Scholar
  100. Sathyanesan AG (1966) Egg-laying of the chimaeroid fish Hydrolagus collei. Copeia (1):132–134. doi:10.2307/1440776
  101. Schaeffer B (1981) The xenacanth shark neurocranium with comments on the elasmobranch phylogeny. Bull Am Mus Nat Hist 169:3–66Google Scholar
  102. Schreibman MP, Margolis-Nunno H, Halpern-Sebold LR, Goos HJT, Perlman PW (1986) The influence of androgen administration on the structure and function of the brain-pituitary-gonad axis of sexually immature platyfish, Xiphophorus maculatus. Cell Tissue Res 245:519–524. doi:10.1007/BF00218552 PubMedGoogle Scholar
  103. Semenkova TB, Canario AVM, Bayunova LV, Couto E, Kolmakov NN, Barannikova IA (2006) Sex steroids and oocyte maturation in the sterlet (Acipenser ruthenus L.). J Appl Ichthyol 22:340–345Google Scholar
  104. Simpfendorfer CA (1992) Biology of tiger sharks (Galeocerdo cuvier) caught by the Queensland Shark Meshing Program off Townsville, Australia. Aust J Mar Freshwater Res 43:33–43. doi:10.1071/MF9920033 Google Scholar
  105. Slater CH, Schreck CB, Swanson P (1994) Plasma profiles of the sex steroids and gonadotropins in maturing female spring chinook salmon (Oncorhynchus tshawytscha). Comp Biochem Physiol 109A:167–175. doi:10.1016/0300-9629(94)90323-9 Google Scholar
  106. Smith RM, Walker TI, Hamlett WC (2004) Microscopic organisation of the oviducal gland of the holocephalan elephant fish, Callorhynchus milii. Mar Freshw Res 55:155–164. doi:10.1071/MF01078 Google Scholar
  107. Sosebee KA (2005) Are density-dependent effects on elasmobranch maturity possible? J Northwest Atl Fish Sci 35:115–124. doi:10.2960/J.v35.m492 Google Scholar
  108. Springer S (1967) Social organization of shark populations. In: Gilbert PW, Mathewson RF, Rall DP (eds) Sharks, skates and rays. Johns Hopkins University Press, Baltimore, pp 149–174Google Scholar
  109. Stanley HP (1961) Studies on the genital systems and reproduction in the chimaeroid fish Hydrolagus colliei (Lay and Bennett). Ph.D. Thesis, Oregon State UniversityGoogle Scholar
  110. Stanley HP (1963) Urogenital morphology in the chimaeroid fish Hydrolagus colliei (Lay and Bennett). J Morphol 112:99–127. doi:10.1002/jmor.1051120202 PubMedGoogle Scholar
  111. Stearns SC (1992) The evolution of life histories. Oxford University Press, New YorkGoogle Scholar
  112. Steven GA (1933) Rays and skates of Devon and Cornwall III. The proportions of the sexes in nature and in commercial landings, and their significance to the fishery. J Mar Biol Assoc UK 18:611–625Google Scholar
  113. Stevens JD, Bonfil R, Dulvy NK, Walker PA (2000) The effects of fishing on sharks, rays, and chimeras (chondrichthyans), and the implications for marine ecosystems. ICES J Mar Sci 57:476–494. doi:10.1006/jmsc.2000.0724 Google Scholar
  114. Strasburg DW (1958) Distribution, abundance, and habits of pelagic sharks in the central Pacific Ocean. Fish Bull (Wash DC) 138:335–361Google Scholar
  115. Sulikowski JA, Tsang PCW, Huntting Howell W (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 (Berl) 144:845–853. doi:10.1007/s00227-003-1264-8 Google Scholar
  116. Sumpter JP, Dodd JM (1979) The annual reproductive cycle of the female lesser spotted dogfish, Scyliorhinus canicula L., and its endocrine control. J Fish Biol 15:687–695. doi:10.1111/j.1095-8649.1979.tb03678.x Google Scholar
  117. Takemura A, Kim BH (2001) Effects of estradiol-17[beta] treatment on in vitro and in vivo synthesis of two distinct vitellogenins in tilapia. Comp Biochem Physiol A Mol Integr Physiol 129:641–651. doi:10.1016/S1095-6433(01)00328-2 PubMedGoogle Scholar
  118. Tolimieri N (2007) Patterns in species richness, species density, and evenness in groundfish assemblages on the continental slope of the U.S. Pacific coast. Environ Biol Fishes 78:241–256. doi:10.1007/s10641-006-9093-5 Google Scholar
  119. Tovar-Ávila J (2006) Reproduction, age validation, growth determination and effects of fishing on the Port Jackson shark (Heterodontus portjacksoni) in South-Eastern Australia. Ph.D. Thesis, University of MelbourneGoogle Scholar
  120. Tovar-Ávila J, Walker TI, Day RW (2007) Reproduction of Heterodontus portusjacksoni in Victoria, Australia: evidence of two populations and reproductive parameters for the eastern population. Mar Freshwat Res 58:956–965Google Scholar
  121. Vu-Tan-Tue (1972) Variations cycliques des gonades et de quelques glandes endocrines chez Chimaera montrosa Linne (Pisces: Holocephali). Sci Nat Zool 14:49–94Google Scholar
  122. Walker TI (1998) Can shark resources be harvested sustainably? A question revisited with a review of shark fisheries. Mar Freshwater Res 49:553–572. doi:10.1071/MF98017 Google Scholar
  123. Walker TI (2007) Spatial and temporal variation in the reproductive biology of gummy shark Mustelus antarcticus (Chondrichthyes : Triakidae) harvested off southern Australia. Mar Freshw Res 58:67–97. doi:10.1071/MF06074 Google Scholar
  124. Walmsley-Hart SA, Sauer WHH, Buxton CD (1999) The biology of the skates Raja wallacei and R. pullopunctata (Batoidea: Rajidae) on the Agulhas Bank, South Africa. S Afr J Mar Sci 21:165–179Google Scholar
  125. Whittier JM, Crews D (1987) Seasonal reproduction: patterns and control. In: Norris DO, Jones RE (eds) Hormones and reproduction in fishes, amphibians, and reptiles. Plenum Press, New York, pp 385–409Google Scholar
  126. Wilimovsky NJ (1954) List of the fishes of Alaska. Stanf Ichthyol Bull 4:279–294Google Scholar
  127. Woodhead PMJ (1969) Effects of estradiol and thyroxine upon the plasma calcium content of a shark Scyliorhinus canicula. Gen Comp Endocrinol 13:310–312. doi:10.1016/0016-6480(69)90254-8 PubMedGoogle Scholar
  128. Wourms JP (1977) Reproduction and development in chondrichthyan fishes. Am Zool 17:379–410Google Scholar
  129. Wourms JP, Lombardi J (1992) Reflections on the evolution of piscine viviparity. Am Zool 32:276–293Google Scholar
  130. Yamaguchi A, Taniuchi T, Shimizu M (2000) Geographic variations in reproductive parameters of the starspotted dogfish, Mustelus manazo, from five localities in Japan and in Taiwan. Environ Biol Fishes 57:221–233. doi:10.1023/A:1007558324902 Google Scholar
  131. Yano K (1995) Reproductive biology of the black dogfish, Centroscyllium fabricii, collected from waters off western Greenland. J Mar Biol Assoc UK 75:285–310CrossRefGoogle Scholar
  132. Zar JH (1996) Biostatistical Analysis, 3rd edn edn. Prentice-Hall, Upper Saddle RiverGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Lewis A. K. Barnett
    • 1
    • 2
  • Ryan L. Earley
    • 3
  • David A. Ebert
    • 1
  • Gregor M. Cailliet
    • 1
  1. 1.Pacific Shark Research Center, Moss Landing Marine LaboratoriesMoss LandingUSA
  2. 2.Southwest Fisheries Science Center, Fisheries Ecology DivisionNOAA FisheriesSanta CruzUSA
  3. 3.Department of Biological SciencesUniversity of AlabamaTuscaloosaUSA

Personalised recommendations