Skip to main content
SpringerLink
Log in

Ontogenetic testicular development and spermatogenesis in rays: the Cownose Ray, Rhinoptera bonasus, as a model

  • Published:
Environmental Biology of Fishes Aims and scope Submit manuscript

Abstract

An understanding of testicular anatomy, development, and seasonality has implications for studies of morphology, behavior, physiology, and bioenergetics of males. Ontogenetic testicular development and spermatogenesis is essentially unknown for chondrichthyans. We examined embryo, juvenile, and adult male Cownose Rays (Rhinoptera bonasus) during development and throughout the annual reproductive cycle. Spermatogonia and Sertoli cells originated from germ cells and somatic cells, respectively, in the embryonic testicular germinal epithelium. In embryos and small juveniles, discrete regions of spermatocyst production appeared within a series of papillae that projected from the dorsal surface of each testis. Because these papillary germinal zones appeared to proliferate through ontogeny, we hypothesize that (1) the germinal zones of juvenile and adult testes are derived from embryonic testicular papillae that form from the germinal epithelium and (2) the papillae become the dorso-central portion of the distinct testicular lobes that form at maturation due to increased spermatocyst production. Our observations indicate that testicular development and the process of spermatogenesis began during embryonic development and increased in scale through ontogeny until maturation, when distinct testicular lobes formed and began enlarging or shrinking based on the annual reproductive cycle. Gonadosomatic indices peaked corresponding to seasonal increased sperm production between January and April, just prior to the April–June mating period. In all life stages, spermatocysts had efferent ducts associated with them from their formation through all stages of development. Year-round presence in the Charlotte Harbor estuarine system, Florida made R. bonasus a good model for beginning to understand ontogenetic gonad development and spermatogenesis in chondrichthyans, especially viviparous rays.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11

Similar content being viewed by others

References

  • Babel JS (1967) Reproduction, life history, and ecology of the round stingray, Urolophus halleri Cooper. Calif Dep Fish Game Fish Bull 137:3–104

    Google Scholar 

  • Bigelow HB, Schroeder WC (1953) Fishes of the Western North Atlantic. Sawfishes, guitarfishes, skates, rays, and chimaeroids. Memoirs of the sears foundation for marine research 1, part 2. Yale University, New Haven

    Google Scholar 

  • Bukulmez O, Arici A (2000) Leukocytes in ovarian function. Hum Reprod Update 6:1–15

    Article  CAS  PubMed  Google Scholar 

  • Callard GV (1988) Reproductive physiology, part B: the male. In: Shuttleworth TJ (ed) Physiology of elasmobranch fishes. Springer, Berlin, pp 292–317

    Google Scholar 

  • Callard GV (1991) Spermatogenesis. In: Pang PKT, Schreibman MP (eds) Vertebrate endocrinology: fundamentals and biomedical implications, vol 4, Part A. Academic, New York, pp 303–341

    Google Scholar 

  • Casey JP, Poulakis GR, Stevens PW (2007) Habitat use by juvenile Gag, Mycteroperca microlepis (Pisces: Serranidae), in subtropical Charlotte Harbor, Florida (USA). Gulf Caribb Res 19:1–9

    Google Scholar 

  • Cope JM (2006) Exploring intraspecific life history patterns in sharks. Fish Bull 104:311–320

    Google Scholar 

  • De Roos AM, Boukal DS, Persson L (2006) Evolutionary regime shifts in age and size at maturation of exploited fish stocks. Proc R Soc B 273:1873–1880

    Article  PubMed Central  PubMed  Google Scholar 

  • Dodd JM (1983) Reproduction in cartilaginous fishes (Chondrichthyes). In: Hoar WS, Randall DJ, Donaldson EM (eds) Fish physiology, vol IX, Part A. Academic, New York, pp 31–95

    Google Scholar 

  • Engel KB, Callard GV (2005) The testis and spermatogenesis. In: Hamlett WC (ed) Reproductive biology and phylogeny of Chondrichthyes: sharks, batoids and chimaeras. Science Publishers, Inc., Enfield, pp 171–200

    Google Scholar 

  • Fänge R, Mattisson A (1981) The lymphomyeloid (hemopoietic) system of the Atlantic Nurse Shark, Ginglymostoma cirratum. Biol Bull 160:240–249

    Article  Google Scholar 

  • Frisk MG (2010) Life history strategies of batoids. In: Carrier JC, Musick JA, Heithaus MR (eds) Sharks and their relatives II: biodiversity, adaptive physiology, and conservation. CRC, Boca Raton, pp 283–316

    Chapter  Google Scholar 

  • Grier HJ (1992) Chordate testis: the extracellular matrix hypothesis. J Exp Zool 261:151–160

    Article  Google Scholar 

  • Grier HJ (1993) Comparative organization of Sertoli cells including the Sertoli cell barrier. In: Russell LD, Griswold MD (eds) The Sertoli cell. Cache River Press, Clearwater, pp 704–739

    Google Scholar 

  • Grier HJ (2002) The germinal epithelium: its dual role in establishing male reproductive classes and understanding the basis for indeterminate egg production in female fishes. In: Creswell RL (ed) Proceedings of the 53rd annual Gulf and Caribbean Fisheries Institute, November 2000. Mississippi/Alabama Sea Grant Consortium, Fort Pierce, pp 537–552

    Google Scholar 

  • Grusha DS (2005) Investigation of the life history of the Cownose Ray, Rhinoptera bonasus (Mitchill 1815). Master’s thesis. The College of William and Mary, Williamsburg, VA

  • Hamlett WC (1999) Male reproductive system. In: Hamlett WC (ed) Sharks, skates, and rays: the biology of elasmobranch fishes. The Johns Hopkins University Press, Baltimore, pp 444–470

    Google Scholar 

  • Hoar WS (1969) Reproduction. In: Hoar WS, Randall DJ (eds) Fish physiology: reproduction and growth, bioluminescence, pigments, and poisons. Academic, New York, pp 1–72

    Google Scholar 

  • Holstein AF (1969) Zur frage der lokalen steuerung der spermatogenese beim dornhai (Squalus acanthias L.). Z Zellforsch 93:265–281

    Article  CAS  PubMed  Google Scholar 

  • Jennings S, Greenstreet SPR, Reynolds JD (1999) Structural change in an exploited fish community: a consequence of differential fishing effects on species with contrasting life histories. J Anim Ecol 68:617–627

    Article  Google Scholar 

  • Lincoln GA (1989) Seasonal aspects of testicular function. In: Burger H, de Kretser D (eds) The testis, 2nd edn. Raven, New York, pp 329–385

    Google Scholar 

  • Marina P, Annamaria L, Barbara D, Loredana R, Piero A, Francesco A (2002) Fine structure of Leydig and Sertoli cells in the testis of immature and mature Spotted Ray Torpedo marmorata. Mol Reprod Dev 63:192–201

    Article  PubMed  Google Scholar 

  • Maruska KP, Cowie EG, Tricas TC (1996) Periodic gonadal activity and protracted mating in elasmobranch fishes. J Exp Zool 276:219–232

    Article  Google Scholar 

  • Matthews LH (1950) Reproduction in the Basking Shark, Cetorhinus maximus (Gunner). Phil Trans R Soc Lond B 234:247–316, plus 11 plates

    Article  CAS  Google Scholar 

  • Nagahama Y (1986) Testis. In: Pang PKT, Schreibman MP (eds) Vertebrate endocrinology: fundamentals and biomedical implications, vol 1, Morphological considerations. Academic, Orlando, pp 399–437

    Google Scholar 

  • Naylor GJP, Caira JN, Jensen K, Rosana KAM, White WT, Last PR (2012) A DNA sequence-based approach to the identification of shark and ray species and its implications for global elasmobranch diversity and parasitology. Bull Amer Mus Nat Hist Number 367

  • Neer JA, Thompson BA (2005) Life history of the Cownose Ray, Rhinoptera bonasus, in the northern Gulf of Mexico, with comments on geographic variability in life history traits. Environ Biol Fish 73:321–331

    Article  Google Scholar 

  • Parenti LR, Grier HJ (2004) Evolution and phylogeny of gonad morphology in bony fishes. Integr Comp Biol 44:333–348

    Article  PubMed  Google Scholar 

  • Parsons GR, Grier HJ (1992) Seasonal changes in shark testicular structure and spermatogenesis. J Exp Zool 261:173–184

    Article  Google Scholar 

  • Pérez-Jiménez JC (2011) Biología reproductiva de la raya Rhinoptera bonasus (Elasmobranchii) en el sureste del Golfo de México [Reproductive biology of the ray Rhinoptera bonasus (Elasmobranchii) in the southeastern Gulf of Mexico]. Hidrobiológica 21:159–167

    Google Scholar 

  • Poulakis GR (2013) Reproductive biology of the Cownose Ray in the Charlotte Harbor estuarine system, Florida. Mar Coast Fish: Dyn Manag Ecosyst Sci 5:159–173. doi:10.1080/19425120.2013.795509

    Article  Google Scholar 

  • Poulakis GR, Stevens PW, Timmers AA, Wiley TR, Simpfendorfer CA (2011) Abiotic affinities and spatiotemporal distribution of the endangered Smalltooth Sawfish, Pristis pectinata, in a South-Western Florida nursery. Mar Freshw Res 62:1165–1177. doi:10.1071/MF11008

    Article  Google Scholar 

  • Pratt HL Jr (1979) Reproduction in the Blue Shark, Prionace glauca. Fish Bull 77:445–470

    Google Scholar 

  • Pratt HL Jr (1988) Elasmobranch gonad structure: a description and survey. Copeia 1988:719–729

    Article  Google Scholar 

  • Pratt HL Jr, Tanaka S (1994) Sperm storage in male elasmobranchs: a description and survey. J Morphol 219:297–308

    Article  PubMed  Google Scholar 

  • Quintero-Hunter I, Grier H, Muscato M (1991) Enhancement of histological detail using metanil yellow as counterstain in periodic acid Schiff’s haemtoxylin staining of glycol methacrylate tissue sections. Biotech Histochem 66:169–172

    Article  CAS  PubMed  Google Scholar 

  • Rago PJ, Sosebee KA, Brodziak JKT, Murawski SA, Anderson ED (1998) Implications of recent increases in catches on the dynamics of northwest Atlantic Spiny Dogfish (Squalus acanthias). Fish Res 39:165–181

    Article  Google Scholar 

  • Roosen-Runge EC (1977) The process of spermatogenesis in animals. Cambridge University Press, London

    Google Scholar 

  • Schwartz FJ (2003) Sharks, skates, and rays of the Carolinas. The University of North Carolina Press, Chapel Hill

    Google Scholar 

  • Setchell BP, Pilsworth LM (1989) The functions of the testes of vertebrate and invertebrate animals. In: Burger H, de Kretser D (eds) The testis, 2nd edn. Raven, New York, pp 1–66

    Google Scholar 

  • Simpson TH, Wardle CS (1967) A seasonal cycle in the testis of the Spurdog, Squalus acanthias, and the sites of 3 β-hydroxysteroid dehydrogenase activity. J Mar Biol Assoc UK 47:699–708

    Article  CAS  Google Scholar 

  • Smith JW, Merriner JV (1986) Observations on the reproductive biology of the Cownose Ray, Rhinoptera bonasus, in Chesapeake Bay. Fish Bull 84:871–877

    Google Scholar 

  • Stanley HP (1963) Urogenital morphology in the chimaeroid fish Hydrolagus colliei (Lay & Bennett). J Morphol 112:99–127

    Article  CAS  PubMed  Google Scholar 

  • Stanley HP (1966) The structure and development of the seminiferous follicle in Scyliorhinus caniculus and Torpedo marmoratus (Elasmobranchii). Z Zellforsch 75:453–468

    Article  CAS  PubMed  Google Scholar 

  • Stanley HP (1990) Fine structural observations on the process of spermiation in the holocephalan fish Hydrolagus colliei. J Morphol 204:295–304

    Article  Google Scholar 

  • Stevens JD, Bonfil R, Dulvy NK, Walker PA (2000) The effects of fishing on sharks, rays, and chimaeras (chondrichthyans), and the implications for marine ecosystems. ICES J Mar Sci 57:476–494

    Article  Google Scholar 

  • 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 144:845–853

    Article  CAS  Google Scholar 

  • Teshima K (1981) Studies on the reproduction of the Japanese Smooth Dogfishes, Mustelus manazo and M. griseus. J Shimonoseki Univ Fish 29:113–199

    Google Scholar 

  • Vu Tan Tue P (1972) Variations cycliques des gonades et de quelques glandes endocrines chez Chimaera monstrosa Linné (Pisces, Holocephali). Ann Sci Nat Zool Biol 14:49–94

    Google Scholar 

  • Wartenberg H (1989) Differentiation and development of the testes. In: Burger H, de Kretser D (eds) The testis, 2nd edn. Raven, New York, pp 67–118

    Google Scholar 

  • Wourms JP (1977) Reproduction and development in chondrichthyan fishes. Am Zool 17:379–410

    Google Scholar 

Download references

Acknowledgments

We thank the volunteers who collected R. bonasus and recorded data during dissections, especially Amy Timmers, Sarah Erickson, Chrystal Murray, Julia Shaw, Jackie DeAngelo, and J. Patrick Casey. We also thank Fish and Wildlife Research Institute histology laboratory staff and volunteers for sample processing, especially Noretta Perry and Yvonne Waters. Thanks to Joe Quattro and Mark Roberts for sequencing and analyzing the mtDNA samples. Thanks to Theresa Cody, Jan Landsberg, and Yasu Kiryu of the Fish and Wildlife Research Institute for access to their Olympus BX50 compound light microscope with DP71 camera. Thanks to Kevan Main and Nicole Rhody of the Mote Aquaculture Research Park for access to their Olympus BX53 compound light microscope with DP72 camera. Bland Crowder, Phil Stevens, and two anonymous reviewers improved earlier versions of this manuscript. Jessica Carroll produced the final versions of Figs. 1, 2, 3, 4, 5, 6, 7, 8, and 9. Special thanks to the Save Our Seas Foundation for sponsorship and to Matt Ajemian and Julie Neer for organizing the stingray symposium at the 2013 American Elasmobranch Society meeting in Albuquerque, NM, where some of these data were presented for the first time. Animals were sacrificed humanely according to normal animal care and ethics practices. This work was supported in part by Florida recreational saltwater fishing license sales and U.S. Department of the Interior, U.S. Fish and Wildlife Service, Federal Aid for Sportfish Restoration Project Number F-43 to the Florida Fish and Wildlife Conservation Commission.

Author information

Authors and Affiliations

  1. Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, Charlotte Harbor Field Laboratory, 585 Prineville Street, Port Charlotte, FL, 33954-1006, USA

    Gregg R. Poulakis

  2. Florida Fish and Wildlife Conservation Commission, Fish and Wildlife Research Institute, 100 Eighth Avenue SE, St. Petersburg, FL, 33701-5095, USA

    Harry J. Grier

Authors
  1. Gregg R. Poulakis
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Harry J. Grier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Gregg R. Poulakis.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Poulakis, G.R., Grier, H.J. Ontogenetic testicular development and spermatogenesis in rays: the Cownose Ray, Rhinoptera bonasus, as a model. Environ Biol Fish 97, 1013–1029 (2014). https://doi.org/10.1007/s10641-014-0267-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10641-014-0267-2

Keywords

Search

Navigation