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Advances in the aquatic sciences
RESEARCH ARTICLE

Reproductive strategy of Scyliorhinus canicula (L., 1758): a holistic approach based on macroscopic measurements and microscopic observations of the reproductive organs

Vasiliki Kousteni https://orcid.org/0000-0003-3455-5357 A B and Persefoni Megalofonou A
+ Author Affiliations
- Author Affiliations

A Department of Zoology–Marine Biology, Faculty of Biology, National and Kapodistrian University of Athens, Panepistimiopolis, Ilisia, 157 84 Athens, Greece.

B Corresponding author. Email: kousteni@hcmr.gr; bkousten@geol.uoa.gr

Marine and Freshwater Research 71(6) 596-616 https://doi.org/10.1071/MF18474
Submitted: 25 April 2018  Accepted: 7 June 2019   Published: 20 September 2019

Abstract

Understanding reproductive features of elasmobranchs that affect population recovery and natural mortality is essential for conservation management planning. Considering macroscopic and microscopic observations of the reproductive tract in 2253 individuals, sampled in Hellenic waters over a 7-year period, four reproductive stages were described. The presence of advanced spermatocyst stages in immature testes supported the early gamete development and long maturation process. The simultaneous presence of follicles of all developmental stages in mature ovaries indicated a protracted egg-laying season. An extended reproductive period was also supported by monthly records of egg-laying females, sexually active males, large egg cases and high values of the gonadosomatic (GSI) and hepatosomatic (HSI) indices. Size at maturity was similar for both sexes. Females and males exhibited no depth segregation compared with individuals of different maturity stages regardless of sex. Sex, size and maturity stage significantly affected GSI, HSI and the relative condition factor. All three somatic indices showed a similar monthly variation, supporting a fat assimilation rate that follows maturation rate, with both affecting physiological condition. The severe population decline that Scyliorhinus canicula has recently undergone should focus our attention on future research supporting robust population modelling to help management of the species.

Additional keywords: conservation, elasmobranchs, histology, maturity scales, reproductive biology.


References

Andreuccetti, P., Iodice, M., Prisco, M., and Gualtieri, R. (1999). Intercellular bridges between granulosa cells and the oocyte in the elasmobranch R. asterias. The Anatomical Record 255, 180–187.
Intercellular bridges between granulosa cells and the oocyte in the elasmobranch R. asterias.Crossref | GoogleScholarGoogle Scholar | 10359519PubMed |

Barausse, A., Correale, V., Curkovic, A., Finotto, L., Riginella, E., Visentin, E., and Mazzoldi, C. (2014). The role of fisheries and the environment in driving the decline of elasmobranchs in the Northern Adriatic Sea. ICES Journal of Marine Science 71, 1593–1603.
The role of fisheries and the environment in driving the decline of elasmobranchs in the Northern Adriatic Sea.Crossref | GoogleScholarGoogle Scholar |

Barone, M., De Ranieri, S., Fabiani, O., Pirone, A., and Serena, F. (2007). Gametogenesis and maturity scale of Raja asterias Delaroche, 1809 (Chondrichthyes, Rajidae) from the South Lingurian Sea. Hydrobiologia 580, 245–254.
Gametogenesis and maturity scale of Raja asterias Delaroche, 1809 (Chondrichthyes, Rajidae) from the South Lingurian Sea.Crossref | GoogleScholarGoogle Scholar |

Bellan-Santini, D., Lacaze, J. C., and Poizat, C. (1994). ‘Les biocenoses marines et littorales de la Mediterranée, synthèse, menaces et perspectives.’ (Muséum National d’Histoire Naturelle: Paris, France.)

Capapé, C. (1977). Contribution à la biologie des Scyliorhinidae des côtes tunisiennes. I. Scyliorhinus canicula (Linné, 1758): répartition géographique et bathymétrique, sexualité, reproduction, fécondité. Bulletin de l’Office National des Pêches de Tunisie 1, 83–101.

Capapé, C., Tomasini, J. A., and Bouchereau, J. L. (1991). Observations sur la biologie de la reproduction de la petite rousett Scyliorhinus canicula (Linnaeus, 1758) (Pisces, Scyliorhinidae) du Golfe du Lion (France Méridionale). Ichtyophysiologica Acta 14, 87–109.

Capapé, C., Guélorget, O., Siau, Y., Vergne, Y., and Quignard, J. P. (2007). Reproductive biology of the thornback ray Raja clavata L., 1758, (Chondrichthyes: Rajidae) from the coast of Languedoc (Southern France, Northern Mediterranean). Vie et Milieu 57, 83–90.

Capapé, C., Vergne, Y., Reynaud, C., Guélorget, O., and Quignard, J. P. (2008a). Maturity, fecundity and occurrence of the smallspotted catshark, Scyliorhinus canicula (Chondrichthyes: Scyliorhinidae) off the Languedocian coast (Southern France, North-Western Mediterranean). Vie et Milieu 58, 47–55.

Capapé, C., Reynaud, C., Vergne, Y., and Quignard, J. P. (2008b). Biological observations on the small-spotted catshark Scyliorhinus canicula (Chondrichthyes: Scyliorhinidae) off the Languedocian coast (southern France, northern Mediterranean). Pan-American Journal of Aquatic Sciences 3, 282–289.

Capapé, C., Mnasri-Sioudi, N., El Kamel-Moutalibibi, O., Boumaïza, M., Ben Amor, M. M., and Reynaud, C. (2014). Production, maturity, reproductive cycle and fecundity of small-spotted catshark, Scyliorhinus canicula (Chondrichthyes: Scyliorhinidae) from the Northern Coast of Tunisia (Central Mediterranean). Journal of Ichthyology 54, 111–126.
Production, maturity, reproductive cycle and fecundity of small-spotted catshark, Scyliorhinus canicula (Chondrichthyes: Scyliorhinidae) from the Northern Coast of Tunisia (Central Mediterranean).Crossref | GoogleScholarGoogle Scholar |

Cardinale, M., and Osio, G. C. (2013). State of fish stocks and fisheries in European waters: status of Mediterranean and Black Sea resources in European waters in 2013. European Commission, Ispra, Italy.

Carrier, J. C., Pratt, H. L. Jr, and Castro, J. I. (2004). Reproductive biology of elasmobranchs. In ‘Biology of Sharks and Their Relatives’. (Eds J. C. Carrier, J. A. Musick, and M. R. Heithaus.) pp. 269–286. (CRC Press: Boca Raton, FL, USA.)

Castro, J. I., Bubucis, P. M., and Overstrom, N. A. (1988). The reproductive biology of the chain dogfish, Scyliorhinus retifer. Copeia 1988, 740–746.
The reproductive biology of the chain dogfish, Scyliorhinus retifer.Crossref | GoogleScholarGoogle Scholar |

Cavanagh, R. D., and Gibson, C. (2007). Overview of the conservation status of cartilaginous fishes (chondrichthyans) in the Mediterranean Sea. (International Union for Conservation of Nature.) Available at https://www.iucn.org/content/overview-conservation-status-cartilaginous-fishes-chondrichthyans-mediterranean-sea [Verified 23 July 2019].

Collenot, G. (1966). Observations relatives au développment au laboratoire d’embryons et d’individus juvéniles de Scyliorhinus canicula L. Cahiers de Biologie Marine 7, 319–330.

Compagno, L. J. V. (1984). FAO species catalogue. Sharks of the world. An annotated and illustrated catalogue of shark species known to date. Part 2. Carchariniformes. FAO Fisheries Synopsis 4, 251–265.

Craik, J. C. A. (1978). An annual cycle of vitellogenesis in the elasmobranch Scyliorhinus canicula. Journal of the Marine Biological Association of the United Kingdom 58, 719–726.
An annual cycle of vitellogenesis in the elasmobranch Scyliorhinus canicula.Crossref | GoogleScholarGoogle Scholar |

D’Onghia, G., Matarrese, A., Tursi, A., and Sion, L. (1995). Observations on the depth distribution pattern of the small-spotted catshark in the North Aegean Sea. Journal of Fish Biology 47, 421–426.
Observations on the depth distribution pattern of the small-spotted catshark in the North Aegean Sea.Crossref | GoogleScholarGoogle Scholar |

Dodd, M. H. I., and Duggan, R. T. (1982). Trawl stress ovulation in the dogfish Scyliorhinus canicula. General and Comparative Endocrinology 46, 392.

Dulvy, N. K., Baum, J. K., Clarke, S., Compagno, L. J., Cortés, E., Domingo, A., Fordham, S., Fowler, S., Francis, M. P., Gibson, C., Martínez, J., Musick, J. A., Soldo, A., Stevens, J. D., and Valenti, S. (2008). You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks and rays. Aquatic Conservation 18, 459–482.
You can swim but you can’t hide: the global status and conservation of oceanic pelagic sharks and rays.Crossref | GoogleScholarGoogle Scholar |

Dulvy, N. K., Fowler, S. L., Musick, J. A., Cavanagh, R. D., Kyne, P. M., Harrison, L. R., Carlson, J. K., Davidson, L. N. K., Fordham, S. V., Francis, M. P., Pollock, C. M., Simpfendorfer, C. A., Burgess, G. H., Carpenter, K. E., Compagno, L. J., Ebert, D. A., Gibson, C., Heupel, M. R., Livingstone, S. R., Sanciangco, J. C., Stevens, J. D., Valenti, S., and White, W. T. (2014). Extinction risk and conservation of the world’s sharks and rays. eLife 3, e00590.
Extinction risk and conservation of the world’s sharks and rays.Crossref | GoogleScholarGoogle Scholar | 24448405PubMed |

Ellis, J. R., and Shackley, S. E. (1997). The reproductive biology of Scyliorhinus canicula in the Bristol Channel, U.K. Journal of Fish Biology 51, 361–372.
The reproductive biology of Scyliorhinus canicula in the Bristol Channel, U.K.Crossref | GoogleScholarGoogle Scholar |

Ellis, J., Mancusi, C., Serena, F., Haka, F., Guallart, J., Ungaro, N., Coelho, R., Schembri, T., and MacKenzie, K. (2009). Small spotted catshark Scyliorhinus canicula. In ‘The IUCN Red List of Threatened Species’, 2009 edn. e.T161399A5415204. (International Union for Conservation of Nature.) Available at https://www.iucnredlist.org/species/161399/5415204 [Verified 28 August 2019].

Fänge, R., and Pulsford, A. (1983). Structural studies on lymphomyeloid tissues of the dogfish, Scyliorhinus canicula L. Cell and Tissue Research 230, 337–351.
Structural studies on lymphomyeloid tissues of the dogfish, Scyliorhinus canicula L.Crossref | GoogleScholarGoogle Scholar | 6850771PubMed |

Fauré-Fremiet, E. (1942). Notes sur la biologie sexuelle de Scyliorhinus canicula. Bulletin Biologique de la France et de la Belgique 76, 244–249.

Fawcett, D. W., Ito, S., and Slautterback, S. (1959). The occurrence of intercellular bridges in groups of cells exhibiting synchronous differentiation. The Journal of Biophysical and Biochemical Cytology 5, 453–460.
The occurrence of intercellular bridges in groups of cells exhibiting synchronous differentiation.Crossref | GoogleScholarGoogle Scholar | 13664686PubMed |

Ferretti, F., Osio, G. C., Jenkins, C. J., Rosenberg, A. A., and Lotze, H. K. (2013). Long-term change in a meso-predator community in response to prolonged and heterogeneous human impact. Scientific Reports 3, 1057.
Long-term change in a meso-predator community in response to prolonged and heterogeneous human impact.Crossref | GoogleScholarGoogle Scholar | 23308344PubMed |

Finotto, L., Michele, C., Garofalo, G., Riginella, E., and Mazzoldi, C. (2015). Contrasting life history and reproductive traits in two populations of Scyliorhinus canicula. Marine Biology 162, 1175–1186.
Contrasting life history and reproductive traits in two populations of Scyliorhinus canicula.Crossref | GoogleScholarGoogle Scholar |

Ford, E. (1921). A contribution to our knowledge of the life-histories of the dogfishes landed at Plymouth. Journal of the Marine Biological Association of the United Kingdom 12, 468–505.
A contribution to our knowledge of the life-histories of the dogfishes landed at Plymouth.Crossref | GoogleScholarGoogle Scholar |

Foulley, M. M., and Mellinger, J. (1980). Etude chronologique, structurale et biométrique de l’oeuf et de son développement chez la petite roussette (Scyliorhinus canicula) élevée en eau de mer artificielle. Reproduction, Nutrition, Development 20, 1835–1848.
Etude chronologique, structurale et biométrique de l’oeuf et de son développement chez la petite roussette (Scyliorhinus canicula) élevée en eau de mer artificielle.Crossref | GoogleScholarGoogle Scholar |

García-Garrido, L., Múñoz-Chápuli, R., and De Andres, A. V. (1990). Serum cholesterol and triglyceride levels in Scyliorhinus canicula (L.) during sexual maturation. Journal of Fish Biology 36, 499–509.
Serum cholesterol and triglyceride levels in Scyliorhinus canicula (L.) during sexual maturation.Crossref | GoogleScholarGoogle Scholar |

Gibson, C., Valenti, S. V., Fowler, S. L., and Fordham, S. V. (2006). The conservation status of Northeast Atlantic chondrichthyans. Report of the IUCN Shark Specialist Group, Northeast Atlantic Regional Red List Workshop VIII. IUCN SSC Shark Specialist Group, Peterborough, UK.

Girard, M., Rivalan, P., and Sinquin, G. (2000). Testis and sperm morphology in two deep-water squaloid sharks, Centroscymnus coelolepis and Centrophorus squamosus. Journal of Fish Biology 57, 1575–1589.
Testis and sperm morphology in two deep-water squaloid sharks, Centroscymnus coelolepis and Centrophorus squamosus.Crossref | GoogleScholarGoogle Scholar |

Hamlett, W. C. (1999). Male reproductive system. In ‘Sharks, Skates and Rays: The Biology of Elasmobranch Fishes’. (Ed. W. C. Hamlett.) pp. 444–470. (The Johns Hopkins University Press: Baltimore, MD, USA.)

Hamlett, W. C., Knight, D. P., Koob, T. J., Jezior, M., Luong, T., Rozycki, T., Brunette, N., and Hysell, M. K. (1998). Survey of oviducal gland structure and function in elasmobranchs. The Journal of Experimental Zoology 282, 399–420.
Survey of oviducal gland structure and function in elasmobranchs.Crossref | GoogleScholarGoogle Scholar |

Hamlett, W. C., Knight, D. P., Pereira, F. T. V., Steele, J., and Sever, D. M. (2005). Oviducal glands in chondrichthyans. In ‘Reproductive Biology and Phylogeny of Chondrichthyes Sharks, Batoids and Chimaeras’. Volume 3. (Ed. W. C. Hamlett.) pp. 301–335. (Science Publishers: Enfield, NH, USA.)

Harris, J. E. (1952). A note of the breeding season, sex ratio and embryonic development of the dogfish Scyliorhinus canicula (L.). Journal of the Marine Biological Association of the United Kingdom 31, 269–275.
A note of the breeding season, sex ratio and embryonic development of the dogfish Scyliorhinus canicula (L.).Crossref | GoogleScholarGoogle Scholar |

Henderson, A., and Casey, Ã. (2001). Reproduction and growth in the lesser-spotted dogfish Scyliorhinus canicula (Elasmobranchii; Scyliorhinidae), from the west coast of Ireland. Cahiers de Biologie Marine 42, 397–405.

Ivory, P., Jeal, F., and Nolan, C. P. (2005). Age determination, growth and reproduction in the lesser-spotted dogfish, Scyliorhinus canicula (L.). Journal of Northwest Atlantic Fishery Science 35, 89–106.
Age determination, growth and reproduction in the lesser-spotted dogfish, Scyliorhinus canicula (L.).Crossref | GoogleScholarGoogle Scholar |

Jardas, I. (1979). Morphological, biological and ecological characteristics of the lesser spotted dogfish, Scyliorhinus canicula (Linnaeus, 1758) population in the Adriatic Sea. Izvješća Reports 4, 1–104.

Jennings, S., Greenstreet, S. P. R., and Reynolds, J. D. (1999). Structural change in an exploited fish community: a consequence of differential fishing effects on species with contrasting life histories. Journal of Animal Ecology 68, 617–627.
Structural change in an exploited fish community: a consequence of differential fishing effects on species with contrasting life histories.Crossref | GoogleScholarGoogle Scholar |

Knight, D. P., Feng, D., and Stewart, M. (1996). Structure and function of the Selachian egg case. Biological Reviews of the Cambridge Philosophical Society 71, 81–111.
Structure and function of the Selachian egg case.Crossref | GoogleScholarGoogle Scholar |

Kollmann, M., Van Gaver, F., and Timon-David, J. (1929). Le développement du foie et son rendement en huile chez Scyllium canicula L. dans leurs rapports avec l’état sexuel de l’animal. Comptes Rendus des Seances de la Société de Biologie et de ses Filiales 100, 355–358.

Koob, T. J., and Callard, I. P. (1999). Reproductive endocrinology of female elasmobranchs: lessons from the little skate (Raja erinacea) and spiny dogfish (Squalus acanthias). The Journal of Experimental Zoology 284, 557–574.
Reproductive endocrinology of female elasmobranchs: lessons from the little skate (Raja erinacea) and spiny dogfish (Squalus acanthias).Crossref | GoogleScholarGoogle Scholar | 10469994PubMed |

Kousteni, V. (2015). Population characteristics and heavy metal concentrations in benthic sharks from the eastern Mediterranean Sea. Ph.D. Thesis, National and Kapodistrian University of Athens, Athens, Greece.

Kousteni, V., Kontopoulou, M., and Megalofonou, P. (2010). Sexual maturity and fecundity of Scylliorhinus canicula (Linnaeus, 1758) in the Aegean Sea. Marine Biology Research 6, 390–398.
Sexual maturity and fecundity of Scylliorhinus canicula (Linnaeus, 1758) in the Aegean Sea.Crossref | GoogleScholarGoogle Scholar |

Kousteni, V., Kasapidis, P., Kotoulas, G., and Megalofonou, P. (2015). Strong population genetic structure and contrasting demographic histories for the small-spotted catshark (Scyliorhinus canicula) in the Mediterranean Sea. Heredity 114, 333–343.
Strong population genetic structure and contrasting demographic histories for the small-spotted catshark (Scyliorhinus canicula) in the Mediterranean Sea.Crossref | GoogleScholarGoogle Scholar | 25469687PubMed |

Le Cren, E. D. (1951). The length–weight relationship and seasonal cycle in gonadal weight and condition of perch (Perca fluviatilis). Journal of Animal Ecology 20, 201–219.
The length–weight relationship and seasonal cycle in gonadal weight and condition of perch (Perca fluviatilis).Crossref | GoogleScholarGoogle Scholar |

Leloup, J., and Olivereau, M. (1951). Données biométriques comparatives sur la rousette (Scyllium canicula L.) de la Manche et de la Méditerranée. Vie et Milieu 2, 182–209.

Lombardi-Carlson, L. A., Cortés, E., Parsons, G. R., and Manire, C. A. (2003). Latitudinal variation in life history traits of bonnethead sharks, Sphyrna tiburo (Carchariniformes: Sphyrnidae), from the Eastern Gulf of Mexico. Marine and Freshwater Research 54, 875–883.
Latitudinal variation in life history traits of bonnethead sharks, Sphyrna tiburo (Carchariniformes: Sphyrnidae), from the Eastern Gulf of Mexico.Crossref | GoogleScholarGoogle Scholar |

Lutton, B. V., St George, J., Murrin, C. R., Fileti, L. A., and Callard, I. P. (2005). The elasmobranch ovary. In ‘Reproductive Biology and Phylogeny of Chondrichthyes Sharks, Batoids and Chimaeras, Volume 3’. (Ed. W. C. Hamlett.) pp. 237–282. (Science Publishers: Enfield, NH, USA.)

Magrabaña, E., Lucifora, L. O., and Massa, A. M. (2002). The reproductive ecology and abundance of Sympterygia bonapartii endemic to the south-west Atlantic. Journal of Fish Biology 60, 951–967.

Maravelias, C. D., Tserpes, G., Pantazi, M., and Peristeraki, P. (2012). Habitat selection and temporal abundance fluctuations of demersal cartilaginous species in the Aegean Sea (Eastern Mediterranean). PLoS One 7, e35474.
Habitat selection and temporal abundance fluctuations of demersal cartilaginous species in the Aegean Sea (Eastern Mediterranean).Crossref | GoogleScholarGoogle Scholar | 22536389PubMed |

Mellinger, J. (1983). Egg-case diversity among dogfish, Scyliorhinus canicula (L.): a study of egg-laying rate and nidamental gland secretory activity. Journal of Fish Biology 22, 83–90.
Egg-case diversity among dogfish, Scyliorhinus canicula (L.): a study of egg-laying rate and nidamental gland secretory activity.Crossref | GoogleScholarGoogle Scholar |

Mellinger, J., Wrisez, J., and Alluchon Gérard, M. J. (1984). Caractères biométriques distinctifs de l’embryon et de ses annexes chez la roussette (Scyliorhinus canicula) de la Manche comparée à celle de la Méditerranée et détermination précise du stade d’éclosion. Cahiers de Biologie Marine 25, 305–317.

Metten, H. (1939). Studies on the reproduction of the dogfish. Proceedings of the Royal Society of London. Series B, Biological Sciences 230, 217–238.

Múñoz-Chápuli, R. (1984). Ethologie de la reproduction chez quelques requins d l’Atlantique Nord-Est. Cybium 8, 1–14.

Musick, J. A., and Ellis, J. K. (2005). Reproductive evolution of chondrichthyans. In ‘Reproductive Biology and Phylogeny of Chondrichthyes Sharks, Batoids and Chimaeras, Volume 3’. (Ed. W. C. Hamlett.) pp. 1–10. (Science Publishers: Enfield, NH, USA.)

Myers, R. A., and Worm, B. (2005). Extinction, survival or recovery of large predatory fishes. Philosophical Transactions of the Royal Society of London – B. Biological Sciences 360, 13–20.
Extinction, survival or recovery of large predatory fishes.Crossref | GoogleScholarGoogle Scholar | 15713586PubMed |

Navarro, J., Cardador, L., Fernandez, A. M., Bellido, J. M., and Coll, M. (2016). Differences in the relative roles of environment, prey availability and human activity in the spatial distribution of two marine mesopredators living in highly exploited ecosystems. Journal of Biogeography 43, 440–450.
Differences in the relative roles of environment, prey availability and human activity in the spatial distribution of two marine mesopredators living in highly exploited ecosystems.Crossref | GoogleScholarGoogle Scholar |

Oddone, M. C., and Vooren, C. M. (2005). Reproductive biology of Atlantoraja cyclophora (Regan 1903) (Elasmobrachii: Rajidae) off southern Brazil. ICES Journal of Marine Science 62, 1095–1103.
Reproductive biology of Atlantoraja cyclophora (Regan 1903) (Elasmobrachii: Rajidae) off southern Brazil.Crossref | GoogleScholarGoogle Scholar |

Oddone, M. C., Amorim, A. F., Mancini, P. L., Norbis, W., and Velazco, G. (2007). The reproductive biology and the cycle of Rioraja agassizi (Müller and Henle, 1841) (Chondrichthyes: Rajidae) in southeastern Brazil, SW Atlantic Ocean. Scientia Marina 71, 593–604.
The reproductive biology and the cycle of Rioraja agassizi (Müller and Henle, 1841) (Chondrichthyes: Rajidae) in southeastern Brazil, SW Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |

Parsons, G. R., and Grier, H. J. (1992). Seasonal changes in shark testicular structure and spermatogenesis. The Journal of Experimental Zoology 261, 173–184.
Seasonal changes in shark testicular structure and spermatogenesis.Crossref | GoogleScholarGoogle Scholar |

Por, F. D. (1989). ‘The Legacy of Tethys. An Aquatic Zoogeography of the Levant.’ (Kluwer Academic Publishers: Dordrecht, Netherlands.)

Pratt, H. L. Jr, and Casey, J. G. (1990). Shark reproductive strategies as a limiting factor in directed fisheries, with a review of Holden’s method of estimating growth-parameters. In ‘Elasmobranchs as Living Resources: Advances in the Biology, Ecology, Systematics, and the Status of the Fisheries. Vol. 90’. (Eds H. L. Pratt Jr, S. Gruber, and T. Taniuchi.) NOAA Technical Report, pp. 97–109. (National Marine Fisheries Service: Washington, DC, USA.)

Prisco, M., Liguoro, A., Ricchiari, L., Del Giudice, G., and Andreuccetti, P. (2007). Oogenesis in the spotted ray Torpedo marmorata. Reviews in Fish Biology and Fisheries 17, 1–10.
Oogenesis in the spotted ray Torpedo marmorata.Crossref | GoogleScholarGoogle Scholar |

Prisco, M., Valiante, S., Maddalena Di Fiore, M., Raucci, F., Del Giudice, G., Romano, M., Laforgia, V., Limatola, E., and Andreuccetti, P. (2008). Effect of 17β-estradiol and progesterone on vitellogenesis in the spotted ray Torpedo marmorata Risso 1810 (Elasmobranchii: Torpediniformes): studies on females and on estrogen-treated males. General and Comparative Endocrinology 157, 125–132.
Effect of 17β-estradiol and progesterone on vitellogenesis in the spotted ray Torpedo marmorata Risso 1810 (Elasmobranchii: Torpediniformes): studies on females and on estrogen-treated males.Crossref | GoogleScholarGoogle Scholar | 18555067PubMed |

Ragonese, S., and Jereb, P. (1990). Egg-case of the dogfish Scyliorhinus canicula (L., 1758) from the Sicilian Channel (Mediterranean Sea). Rapport de la Commission Internationale pour la Mer Méditerrané 32, 264.

Rodríguez-Cabello, C., De La Gándara, F., and Sanchez, F. (1998). Preliminary results on growth and movements of dogfish Scyliorhinus canicula (Linnaeus, 1758) in the Cantabrian Sea. Oceanologica Acta 21, 363–370.
Preliminary results on growth and movements of dogfish Scyliorhinus canicula (Linnaeus, 1758) in the Cantabrian Sea.Crossref | GoogleScholarGoogle Scholar |

Rossouw, G. J. (1987). Function of the liver and hepatic lipids of the lesser sand shark, Rhinobatos annulatus (Müller and Henle). Comparative Biochemistry and Physiology – B. Comparative Biochemistry 86, 785–790.
Function of the liver and hepatic lipids of the lesser sand shark, Rhinobatos annulatus (Müller and Henle).Crossref | GoogleScholarGoogle Scholar | 3581802PubMed |

Serena, F., Abella, A., Baino, R., Carbonara, P., Facchini, M. T., Ferrari, A., Follesa, M. C., Gangitano, V., Garibaldi, F., Manfredi, C., Mancusi, C., Sartor, P., Sbrana, M., Sion, L., and Tinti, F. (2014). ‘Preliminary Considerations of the Status of Elasmobranchs in the Italian Waters.’ (Shark International: Durban, South Africa.)

Serra-Pereira, B., Figueiredo, I., and Serrano Gordo, L. (2011). Maturation of the gonads and reproductive tracts of the thornback ray Raja clavata, with comments on the development of a standardized reproductive terminology for oviparous elasmobranchs. Marine and Coastal Fisheries 3, 160–175.
Maturation of the gonads and reproductive tracts of the thornback ray Raja clavata, with comments on the development of a standardized reproductive terminology for oviparous elasmobranchs.Crossref | GoogleScholarGoogle Scholar |

Stanley, H. P. (1966). The structure and development of the seminiferous follicle in Scyliorhinus caniculus and Torpedo marmorata (Elasmobranchii). Zeitschrift für Zellforschung und Mikroskopische Anatomie 75, 453–468.
The structure and development of the seminiferous follicle in Scyliorhinus caniculus and Torpedo marmorata (Elasmobranchii).Crossref | GoogleScholarGoogle Scholar | 4860880PubMed |

Sulikowski, J. A., Tsang, P. C. W., and Howell, W. H. (2005). Age and size at sexual maturityfor the winter skate, Leucoraja ocellata, in the western Gulf of Maine based onmorphological, histological and steroid hormone analyses. Environmental Biology of Fishes 72, 429–441.
Age and size at sexual maturityfor the winter skate, Leucoraja ocellata, in the western Gulf of Maine based onmorphological, histological and steroid hormone analyses.Crossref | GoogleScholarGoogle Scholar |

Taleb-Bendiab, A. A., Mouffok, S., and Boutiba, Z. (2012). Reproductive biology and growth of lesser spotted dogfish Scyliorhinus canicula (Linnaeus, 1758) in western Algerian coasts (Chondrichthyes, Scyliorhinidae). Journal of Biodiversity 3, 41–48.

Tambourgi, M. R. D., Hazin, F. H. V., Oliveira, P. G. V., Coelho, R., Burgess, G., and Roque, P. C. G. (2013). Reproductive aspects of the oceanic whitetip shark, Carcharhinus longimanus (Elasmobranchii: Carcharhinidae), in the equatorial and southwestern Atlantic Ocean. Brazilian Journal of Oceanography 61, 161–168.
Reproductive aspects of the oceanic whitetip shark, Carcharhinus longimanus (Elasmobranchii: Carcharhinidae), in the equatorial and southwestern Atlantic Ocean.Crossref | GoogleScholarGoogle Scholar |

Tortonese, E. (1950). Studi sui plagiostomi. III. La viviparità: un fondamentale carattere biologico degli Squali. Archivio Zoologico Italiano 1950, 101–155.

Walker, T. I. (2005). Reproduction in fisheries science. In ‘Reproductive Biology and Phylogeny of Chondrichthyes. Sharks, Batoids and Chimaeras’. (Ed. W. C. Hamlett.) pp. 81–127. (Science Publishers: Enfield, NH, USA.)

Wallace, R. A., and Selman, K. (1981). Cellular and dynamic aspects of oocyte growth in teleosts. Animal Zoology 21, 325–343.
Cellular and dynamic aspects of oocyte growth in teleosts.Crossref | GoogleScholarGoogle Scholar |

Wootton, R. J. (1990). ‘Ecology of Teleost Fishes’, 1st edn. (Chapman and Hall: London, UK.)

Wootton, R. J., Evans, G. W., and Mills, L. A. (1978). Annual cycle in female three spined stickleback (Gasterosteus aculeatus) from an upland and lowland population. Journal of Fish Biology 12, 331–343.
Annual cycle in female three spined stickleback (Gasterosteus aculeatus) from an upland and lowland population.Crossref | GoogleScholarGoogle Scholar |

Zar, J. H. (1999). ‘Biostatistical Analysis’, 4th edn. (Prentice Hall: Upper Saddle River, NJ, USA.)

Zupanovic, S. (1961). Contribution à la connaissance des poisons de l’Adriatique. Acta Adriatica 9, 1–84.