Skip to main content
SpringerLink
Log in

Plasma sex steroid profiles and the seasonal reproductive cycle in male and female winter flounder, Pleuronectes americanus

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The pattern of seasonal gonadal development and variations in plasma sex steroids were investigated in adult male and female winter flounder, Pleuronectes americanus (Walbaum), from Conception Bay Newfoundland beginning August 1987 to December 1988. The winter flounder reproductive cycle can be divided into five consecutive phases of relative reproductive activity including: (1) rapid gonadal recrudescence in the fall (August–December); (2) continued slow gondadal growth in females, or maintenance of the well developed gonads in males, during the winter (December–February); (3) a prespawning phase of gonadal maintenance in the spring (March–April); (4) spawning early in the summer (May–June) after the female gonads reach peak weight; and (5) the summer postspawned period (June–August) when the gonads remain regressed. Female gonadal recrudescence in August is characterized by small increases in plasma estrogen levels and recruitment of small oocytes (≥150 μm) into yolk accumulation. For the winter months, estradiol-17 β levels in the plasma remain stable, approximately 15 ng ml-1, until rising again together with testosterone to peak hormone levels just prior to spawning in conjunction with the highest seasonal values for the gonadosomatic index (GSI) and oocyte diameter. After spawning, the ovaries are regressed and sex steroids in the plasma fall to very low levels. Rapid seasonal recrudescence of the gonads in males is evident from rising GSI values, which reach a maximum in October, and from substantial early seasonal increases in plasma testosterone and 11-ketotestosterone. Afterwards, although GSI values subsequently decline presumably reflecting the process of spermiogenesis and/or onset of spermiation in some males, the testes remain relatively well developed with the presence of sperm throughout the spawning season. As the proportion of spermiating males increases, the plasma levels of the androgenic steroid hormones rise to peak circulating levels from April to June. At the end of the summer reproductive season, the testes of post-spawned males become regressed and plasma testosterone and 11-ketotestosterone levels fall, reaching the lowest seasonal values.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Barr WA (1963) The endocrine control of the sexual cycle in the plaice, Pleuronectes platessa (L). I. Cyclical changes in the normal ovary. Gen comp Endocr 3:197–204

    Google Scholar 

  • Billard R (1987) Testis growth and spermatogenesis in teleost fish: the problem of the large interspecies variability in testis size. In: Idler DR, Crim LW, Walsh J (eds) Proc 3rd int Symp Reproductive Physiology of Fish. Memorial University of Newfoundland, St. John's, Newfoundland, Canada, pp 183–186

    Google Scholar 

  • Bishop RL (1988) Observer's handbook. The Royal Astronomical Society of Canada, Toronto, Ontario

    Google Scholar 

  • Burke MG, Leatherland JF, Sumpter JP (1984) Seasonal changes in serum testosterone, 11-ketotestosterone, and 17 β-estradiol levels in the brown bullhead, Ictalurus nebulosus Lesueur. Can J Zool 62:1195–1199

    Google Scholar 

  • Burton MP, Idler DR (1984) The reproductive cycle in winter flounder, Pseudopleuronectes americanus (Walbaum). Can J Zool 62:2563–2567

    Google Scholar 

  • Burton MP, Idler DR (1987) An experimental investigation of the non-reproductive, post-mature state in winter flounder. J Fish Biol 30:643–650

    Google Scholar 

  • Bye VJ (1987) Environmental management of marine fish reproduction in Europe. In: Idler DR, Crim LW, Walsh J (eds) Proc 3rd int Symp Reproductive Physiology of Fish. Memorial University of Newfoundland, St. John's, Newfoundland, Canada, pp 289–298

    Google Scholar 

  • Bye VJ (1990) Temperate marine teleosts. In: Munro AD, Scott AP, Lam TJ (eds) Reproductive seasonality in teleosts: environmental influences. CRC Press, Inc, Boca Raton, Florida, USA, pp 125–143

    Google Scholar 

  • Campbell CM, Walsh JM, Idler DR (1976) Steroids in the plasma of winter flounder (Pseudopleuronectes americanus) Walbaum. A seasonal study and investigation of steroid involvement in oocyte maturation. Gen comp Endocr 29:14–20

    Google Scholar 

  • Canario AVM (1991) Sex steroids in marine flatfish. In: Scott AP, Sumpter JP, Kime DE, Rolfe MS (1991) Proc 4th int Symp Reproductive Physiology of Fish. University of East Anglia, Norwich, UK, FishSymp 91, Sheffield, pp 71–73

    Google Scholar 

  • Canario AVM, Scott AP (1990a) Effects of steroids and human chorionic gonadotropin on in vitro oocyte final maturation in two marine flatfish: the dab, Limanda limanda, and the plaice, Pleuronectes platessa. Gen comp Endocr 77:161–176

    Google Scholar 

  • Canario AVM, Scott AP (1990b) Plasma levels of ovarian steroids, including 17 α,20α-dihydroxy-4-pregnen-3-one and 3β, 17 α,20α-trihydroxy-5β-pregnane, in female dabs (Limanda limanda) —marine flatfis — induced to mature and ovulate with human chorionic gonadotrophin. Gen comp Endocr 77:177–191

    Google Scholar 

  • Chan KK (1977) Effects of synthetic luteinizing hormone releasing hormone (LH-RH) on ovarian development in Japanese medaka, Oryzias latipes. Can J Zool 55:155–160

    Google Scholar 

  • Cochran RC (1987) Serum androgens during the annual reproductive cycle of the male mummichog, Fundulus heteroclitus. Gen comp Endocr 65:141–148

    Google Scholar 

  • Crim LW, Evans DM (1983) Influence of testosterone and/or luteinizing hormone releasing hormone analogue on precocious sexual development in juvenile rainbow trout. Biol Reprod 29: 137–142

    Google Scholar 

  • Crim LW, Evans DM, Vickery BH (1983) Manipulation of the seasonal reproductive cycle of the landlocked salmon (Salmo salar) by LHRH analogues administered at various stages of gonadal development. Can J Fish aquat Sciences 40:61–67

    Google Scholar 

  • Crim LW, Glebe BD (1984) Advancement and synchrony of ovulation in Atlantic salmon with pelleted LHRH analog. Aquaculture, Amsterdam 43:47–56

    Google Scholar 

  • Devauchelle N, Alexandre JC, Le Corre N, Letty Y (1988) Spawning of turbot (Scophthalmus maximus) in captivity. Aquaculture, Amsterdam 69:159–184

    Google Scholar 

  • De Vlaming V (1983) Oocyte development patterns and hormonal involvements among teleosts. In: Rankin JC, Pitcher T, Duggan R (eds) Control processes in fish physiology. Croom-Helm, London, pp 176–199

    Google Scholar 

  • De Vlaming V, Fitzgerald R, Delahunty G, Cech JJ, Selman K, Barkley M (1984) Dynamics of oocyte development and related changes in serum estradiol-17 β, yolk precursor and lipid levels in the teleostean fish, Leptocottus armatus. Comp Biochem Physiol 77A:599–610

    Google Scholar 

  • Dickhoff WW, Swanson P (1990) Functions of salmon pituitary glycoprotein hormones: the maturational surge hypothesis. Progress in comparative endocrinology. Wiley-Liss, New York, pp 349–356

    Google Scholar 

  • Dunn KS (1970) Further evidence for a three-year oocyte maturation time in the winter flounder (Pseudopleuronectes americanus). J Fish Res Bd Can 27:957–960

    Google Scholar 

  • Dunn RS, Tyler AV (1969) Aspects of the anatomy of the winter flounder ovary with hypotheses on oocyte maturation time. J Fish Res Bd Can 26:1943–1947

    Google Scholar 

  • Fitzpatrick SM, Redding JM, Ratti FD, Ratti FD, Shreck CB (1987) Plasma testosterone concentration predicts the ovulatory response of coho salmon (Oncorhynchus kisutch) to gonadotropin-releasing hormone analog. Can J Fish aquat Sciences 44:1351–1357

    Google Scholar 

  • Fletcher GL, King MJ (1978) Seasonal dynamics of Cu, Zn, Ca, and Mg in gonads and liver of winter flounder (Pseudopleuronectes americanus): evidence for summer storage of Zn for winter gonad development in females. Can J Zool 56:284–290

    Google Scholar 

  • Fostier A, Billard R, Breton B, Legendre M, Marlot S (1982) Plasma 11-oxotestosterone and gonadotropin during the beginning of spermiation in rainbow trout (Salmo gairdneri R.). Gen comp Endocr 46:428–434

    Google Scholar 

  • Fostier A, Jalabert B, Billard R, Breton B, Zohar Y (1983) The gonadal steroids. In: Hoar WS, Randall DJ, Donaldson EM (eds) Fish physiology, Vol IXB. Academic Press, New York, pp 117–170

    Google Scholar 

  • Greeley MS, Calder DR, Wallace RA (1987) Oocyte growth and development in the striped mullet, Mugil cephalus, during seasonal ovarian recrudescence: relationship to fecundity and size at maturity. Fish Bull US 85:187–200

    Google Scholar 

  • Harmin SA, Crim LW (1992) Gonadotropic hormone-releasing hormone analog (GnRH-A) induced ovulation and spawning of winter flounder (Pseudopleuronectes americanus, Walbaum). Aquaculture, Amsterdam 104:375–390

    Google Scholar 

  • Harmin SA, Crim LW (1993) Influence of gonadotropic hormone-releasing hormone analog (GnRH-A) on plasma sex steroid profiles and milt production in male winter flounder, Pseudopleuronectes americanus (Walbaum). Fish Physiol Biochem 10: 399–407

    Google Scholar 

  • Howell WH (1982) Seasonal changes in the ovaries of adult yellowtail flounder, Limanda ferruginea. Fish Bull US 81:341–355

    Google Scholar 

  • Htun-Han M (1978) The reproductive biology of the dab, Limanda limanda in the North Sea: seasonal changes in the ovary. J Fish Biol 13:351–359

    Google Scholar 

  • Johnson LL, Casillas E, Myers MS, Rhodes LD, Olson OP (1991) Patterns of oocyte development and related changes in plasma 17 β-estradiol, Vitellogenin, and plasma chemistry in English sole Parophyrs vetulus Girard. J exp mar Biol Ecol 152:161–185

    Google Scholar 

  • Kagawa H, Young G, Nagahama Y (1984) In vitro estradiol-17 β and testosterone production by ovarian follicles of the goldfish, Carassius auratus. Gen comp Endocr 54:139–143

    Google Scholar 

  • Kime DE, Manning MJ (1982) Seasonal patterns of free and conjugated androgens in the brown trout Salmo trutta. Gen comp Endocr 48:222–231

    Google Scholar 

  • Klein-MacPhee G (1978) Synopsis of biological data for the winter flounder, Pseudopleuronectes americanus (Walbaum). NOAA Technical Report NMFS Circular 414, National Marine Fisheries Service, US Department of Commerce, Seattle, Washington

    Google Scholar 

  • Lam TJ (1982) Application of endocrinology to fish culture. Can J Fish aquat Sciences 39:111–137

    Google Scholar 

  • Methven DA, Crim LW (1991) Seasonal changes in spermatocrit, plasma sex steroids and motility of sperm from Atlantic halibut (Hippoglossus hippoglossus). In: Scott AP, Sumpter JP, Kime DE, Rolfe MS (eds) Proc 4th int Symp Reproductive Physiology of Fish. University of East Anglia, Norwich, UK, FishSymp 91, Sheffield, p 170

    Google Scholar 

  • Methven DA, Crim LW, Norberg B, Brown JA, Goff GP, Huse I (1992) Seasonal reproduction and plasma levels of sex steroids and vitellogenin in Atlantic halibut (Hippoglossus hippoglossus). Can J Fish aquat Sciences 49:754–759

    Google Scholar 

  • Ng TB, Idler DR (1980) Gonadotropic regulation of androgen production in flounder and salmonids. Gen comp Endocr 42:25–38

    Google Scholar 

  • Ng TB, Idler DR, Burton MP (1980) Effects of teleost gonadotropins and their antibodies on gonadal histology in winter flounder. Gen comp Endocr 42:355–364

    Google Scholar 

  • Norberg B, Bjornsson BTH, Brown CL, Wichardt U-P, Deftos LJ, Haux C (1989) Changes in plasma vitellogenin, sex steroids, calcitonin and thyroid hormones related to sexual maturation in female brown trout (Salmo trutta). Gen comp Endocr 75:316–326

    Google Scholar 

  • Norberg B, Valkner V, Huse J, Karlsen I, Grung GL (1991) Ovulatory rhythms and egg viability in the Atlantic halibut (Hippoglossus hippoglossus). Aquaculture, Amsterdam 97:365–371

    Google Scholar 

  • Sangalang GB, Freeman AC (1974) Effects of sublethal cadmium on maturation and testosterone production in vivo in brook trout. Biol Reprod 1:429–435

    Google Scholar 

  • Scott AP, Bye VJ, Baynes SM (1980a) Seasonal variations in sex steroids of female rainbow trout. J Fish Biol 17:587–592

    Google Scholar 

  • Scott AP, Bye VJ, Baynes SM, Springate JRC (1980b) Seasonal variations in plasma concentrations of 11-ketotestosterone and testosterone in male rainbow trout Salmo gairdneri Richardson. J Fish Biol 17:495–505

    Google Scholar 

  • Scott AP, Canario AVM (1990) Plasma levels of ovarian steroids, including 17 α,21-dihydroxy-4-pregnene-3,20-dione and 3α, 17α, 21-trihydroxy-5β-pregnan-20-one, in female plaice (Pleuronectes platessa) induced to mature with human chorionic gonadotrophin. Gen comp Endocr 78:286–298

    Google Scholar 

  • Scott AP, Canario AVM (1992) 17α,20β-dihydroxy-4-pregnen-3-one 20-sulphate: a major new metabolite of the teleost oocyte maturation-inducing steroid. Gen comp Endocr 85:91–100

    Google Scholar 

  • Shehadeh ZH, Kuo CM, Milisen KK (1973) Validation of an in vivo method for monitoring ovarian development in the grey mullet (Muyil cephalus L.). J Fish Biol 5:489–496

    Google Scholar 

  • Wallace R, Selman K (1981) Cellular and dynamic aspects of oocyte growth in teleosts. Am Zool 21:325–343

    Google Scholar 

  • Weil C, Crim LW (1983) Administration of LHRH analogues in various ways. Effects of the advancement of spermiation in prespawning landlocked salmon, Salmo salar. Aquaculture, Amsterdam 35:103–116

    Google Scholar 

  • Wingfield JC, Grimm AS (1977) Seasonal changes in plasma cortisol, testosterone, and estradiol-17β in the plaice, Pleuronectes platessa L. Gen comp Endocr 31:1–11

    Google Scholar 

Download references

Author information

Author notes

  1. S. A. Harmin

    Present address: Department of Aquaculture, Faculty of Fisheries & Marine Sciences, Universiti Pertanian Malaysia, 43400 UPM, Serdang, Selangor, Malaysia

Authors and Affiliations

  1. Ocean Sciences Centre, Department of Biology, Memorial University of Newfoundland, A1C 5S7, St. John's, Newfoundland, Canada

    S. A. Harmin & L. W. Crim

  2. Department of Biology, University of Winnipeg, R3B 2E9, Winnipeg, Manitoba, Canada

    M. D. Wiegand

Authors
  1. S. A. Harmin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. W. Crim
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. D. Wiegand
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by J. P. Grassle, New Brunswick

Rights and permissions

Reprints and permissions

About this article

Cite this article

Harmin, S.A., Crim, L.W. & Wiegand, M.D. Plasma sex steroid profiles and the seasonal reproductive cycle in male and female winter flounder, Pleuronectes americanus . Marine Biology 121, 601–610 (1995). https://doi.org/10.1007/BF00349295

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00349295

Keywords

Search

Navigation