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Assessment of sperm storage across different reproductive modes in the elasmobranch fishes

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Abstract

The oviducal gland is a specialised region of the elasmobranch oviduct that is thought to be a site of sperm storage, among other functions. The phenomenon of female sperm storage in elasmobranchs has implications for the understanding of their reproductive ecology and the management of exploited populations, but relatively little information exists on its taxonomic extent. In the present study, oviducal glands from 29 different species, of varying reproductive modes, from the northern Indian and North East Atlantic oceans were examined using light microscopy for the presence of sperm. The organisation of the gland into four fundamental zones; club, papillary, baffle and terminal, was conserved across all species, with slight variations in relative zone volume due to reproductive mode. Spermatozoa observed within the oviducal gland were not limited to a particular reproductive mode or maturity stage. Although spermatozoa were most commonly encountered in the terminal zone tubules, in some species they were also encountered elsewhere in the gland. The storage of sperm may be a vital reproductive strategy for many species and furthering our taxonomic understanding of which species employ this strategy will help to better inform fisheries managers and protect exploited low reproductive species.

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References

  • Ba A, Ba CT, Diouf K, Ndiaye PI, Panfili J (2013) Reproductive biology of the milk shark Rhizoprionodon acutus (Carcharhinidae) off the coast of Senegal. Afr J Mar Sci 35(2):223–232

    Article  Google Scholar 

  • Bancroft JD, Layton C (2012) The hematoxylins and eosin. Bancroft’s theory and practice of histological techniques:173–186

  • Bernal MA, Sinai NL, Rocha C, Gaither MR, Dunker F, Rocha LA (2015) Long-term sperm storage in the brownbanded bamboo shark Chiloscyllium punctatum. J Fish Biol 86(3):1171–1176

  • Birkhead TR, Møller AP (1992) Numbers and size of sperm storage tubules and the duration of sperm storage in birds: a comparative study. Biol J Linn Soc 45(4):363–372

    Article  Google Scholar 

  • Birkhead TR, Møller AP (1993) Sexual selection and the temporal separation of reproductive events: sperm storage data from reptiles, birds and mammals. Biol J Linn Soc 50(4):295–311

    Article  Google Scholar 

  • Birkhead TR, Pizzari T (2002) Postcopulatory sexual selection. Nat Rev Genet 3(4):262–273

    Article  CAS  Google Scholar 

  • Castro JI, Bubucis PM, Overstrom NA (1988) The reproductive biology of the chain dogfish, Scyliorhinus retifer. Copeia 1988(3):740–746

    Article  Google Scholar 

  • Clark RS (1922) Rays and Skates (Raiœ) No. 1.—Egg-Capsules and Young. J Mar Biol Assoc U K 12(4):578–643

    Article  Google Scholar 

  • Conrath CL, Musick JA (2012) Reproductive biology of elasmobranchs. Biology of Sharks and their Relatives:291–312

  • Dean MD, Ardlie KG, Nachman MW (2006) The frequency of multiple paternity suggests that sperm competition is common in house mice (Mus domesticus). Mol Ecol 15(13):4141–4151

    Article  CAS  Google Scholar 

  • Ellis JR, Shackley SE (1995) Observations on egg-laying in the thornback ray. J Fish Biol 46(5):903–904

    Article  Google Scholar 

  • Farrell ED, Mariani S, Clarke MW (2010) Reproductive biology of the starry smooth-hound shark Mustelus asterias: geographic variation and implications for sustainable exploitation. J Fish Biol 77(7):1505–1525

    Article  CAS  Google Scholar 

  • Ferretti F, Worm B, Britten GL, Heithaus MR, Lotze HK (2010) Patterns and ecosystem consequences of shark declines in the ocean. Ecol Lett 13(8):1055–1071

    PubMed  Google Scholar 

  • Frisk MG, Miller TJ, Fogarty MJ (2001) Estimation and analysis of biological parameters in elasmobranch fishes: a comparative life history study. Can J Fish Aquat Sci 58(5):969–981

    Article  Google Scholar 

  • Gaskin DE (1970) Composition of schools of sperm whales Physeter catodon Linn. east of New Zealand. N Z J Mar Freshwater Res 4(4):456–471

    Article  Google Scholar 

  • Gist DH, Jones JM (1989) Sperm storage within the oviduct of turtles. J Morphol 199(3):379–384

    Article  Google Scholar 

  • Goetz JE, McFarland KP, Rimmer CC (2003) Multiple paternity and multiple male feeders in Bicknell's Thrush (Catharus bicknelli). Auk 120(4):1044–1053

    Article  Google Scholar 

  • Halpert AP, Garstka WR, Crews D (1982) Sperm transport and storage and its relation to the annual sexual cycle of the female red-sided garter snake, Thamnophis sirtalis parietalis. J Morphol 174(2):149–159

    Article  Google Scholar 

  • Hamlett WC (1999) Sharks, skates, and rays: the biology of elasmobranch fishes. JHU Press

  • Hamlett WC, Hysell MK, Jezior M, Rozycki T, Brunette N, Tumilty K (1997) Fundamental zonation in elasmobranch oviducal glands. In: Proceedings of the 5th Indo-Pacific Fish Conference, Nouméa. Society of French Ichthyology, France, Paris, pp 271–280

  • Hamlett WC, Knight DP, Koob TJ, Jezior M, Luong T, Rozycki T, Brunette N, Hysell MK (1998) Survey of oviducal gland structure and function in elasmobranchs. J Exp Zool 282(4–5):399–420

    Article  Google Scholar 

  • Hamlett WC, Fishelson L, Baranes A, Hysell CK, Sever DM (2002) Ultrastructural analysis of sperm storage and morphology of the oviducal gland in the Oman shark, Iago omanensis (Triakidae). Mar Freshw Res 53(2):601–613

    Article  Google Scholar 

  • Henderson AC, McIlwain JL, Al-Oufi HS, Ambu-Ali A (2006) Reproductive biology of the milk shark Rhizoprionodon acutus and the bigeye houndshark Iago omanensis in the coastal waters of Oman. J Fish Biol 68(6):1662–1678

    Article  Google Scholar 

  • Hobson AD (1930) A note on the formation of the egg case of the skate. J Mar Biol Assoc U K 16(2):577–581

    Article  Google Scholar 

  • Knight DP, Feng D (1994) Some observations on the collagen fibrils of the egg capsule of the dogfish, Scyliorhinus canicula. Tissue Cell 26(3):385–401

    Article  CAS  Google Scholar 

  • Knight DP, Feng D, Stewart M, King E (1993) Changes in macromolecular organization in collagen assemblies during secretion in the nidamental gland and formation of the egg capsule wall in the dogfish Scyliorhinus canicula. Philos Trans R Soc Lond B 341(1298):419–436

    Article  CAS  Google Scholar 

  • Knight DP, Feng D, Stewart M (1996) Structure and function of the salachian egg case. Biol Rev 71(1):81–111

    Article  Google Scholar 

  • Kobayashi H, Iwamatsu T (2002) Fine structure of the storage micropocket of spermatozoa in the ovary of the guppy Poecilia reticulata. Zool Sci 19(5):545–556

    Article  Google Scholar 

  • Kuehnel S, Kupfer A (2012) Sperm storage in caecilian amphibians. Front Zool 9(1):12

    Article  Google Scholar 

  • Last PR, Henderson AC, Naylor GJP (2016) Acroteriobatus omanensis (Batoidea: Rhinobatidae), a new guitarfish from the Gulf of Oman. Zootaxa 4144(2):276–286

    Article  Google Scholar 

  • McCracken GF, Burghardt GM, Houts SE (1999) Microsatellite markers and multiple paternity in the garter snake Thamnophis sirtalis. Mol Ecol 8(9):1475–1479

    Article  CAS  Google Scholar 

  • Metten H (1939) Studies on the reproduction of the dogfish. Philos Trans R Soc London, Ser B 230(569):217–238

    Article  Google Scholar 

  • Nalini MK (1940) Structure and function of the nidamental gland of Chiloscyllium griseum (Mull. and Henle). In: Proceedings of the Indian Academy of Sciences-Section B, vol 12, no 5. Springer India, pp 189–214

  • Pearse DE, Janzen FJ, Avise JC (2002) Multiple paternity, sperm storage, and reproductive success of female and male painted turtles (Chrysemys picta) in nature. Behav Ecol Sociobiol 51(2):164–171

    Article  Google Scholar 

  • Pratt HL (1993) The storage of spermatozoa in the oviducal glands of western North Atlantic sharks. In: The reproduction and development of sharks, skates, rays and ratfishes. Springer, pp 139–149

  • Serra-Pereira B, Afonso F, Farias I, Joyce P, Ellis M, Figueiredo I, Gordo LS (2011) The development of the oviducal gland in the Rajid thornback ray, Raja clavata. Helgol Mar Res 65(3):399

    Article  Google Scholar 

  • Smith RM, Walker TI, Hamlett WC (2004) Microscopic organisation of the oviducal gland of the holocephalan elephant fish, Callorhynchus milii. Mar Freshw Res 55(2):155–164

    Article  Google Scholar 

  • Storrie MT, Walker TI, Laurenson LJ, Hamlett WC (2008) Microscopic organization of the sperm storage tubules in the oviducal gland of the female gummy shark (Mustelus antarcticus), with observations on sperm distribution and storage. J Morphol 269(11):1308–1324

    Article  Google Scholar 

  • Waller GNH, Baranes A (1994) Food of Iago omanensis, a deep water shark from the northern Red Sea. J Fish Biol 45(1):37–45

    Article  Google Scholar 

  • Wearmouth VJ, Sims DW (2008) Sexual segregation in marine fish, reptiles, birds and mammals: behaviour patterns, mechanisms and conservation implications. Advances in marine biology 54:107–170

    Article  Google Scholar 

  • Weimerskirch H, Cherel Y, Cuenot-Chaillet F, Ridoux V (1997) Alternative foraging strategies and resource allocation by male and female wandering albatrosses. Ecology 78(7):2051–2063

    Article  Google Scholar 

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Acknowledgements

The authors would like to thank the many scientists and crew that contributed to the collection and processing of data during scientific surveys. The authors would also like to thank the two anonymous reviewers for their constructive feedback on a previous draft.

Funding

This project was funded by the Research & Innovation Strategic Endowment (RISE) scholarship provided by Galway-Mayo Institute of Technology (2016).

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Authors and Affiliations

  1. Marine and Freshwater Research Centre, Galway-Mayo Institute of Technology, Dublin Road, Galway, Ireland

    Robert P. Jordan, Conor T. Graham & Cóilín Minto

  2. Biology Department, College of Science, United Arab Emirates University, Al Ain, United Arab Emirates

    Aaron C. Henderson

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  1. Robert P. Jordan
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  2. Conor T. Graham
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  3. Cóilín Minto
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  4. Aaron C. Henderson
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Correspondence to Robert P. Jordan.

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All of the research undertaken herein was done so in accordance with the relevant national laws.

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Code used to produce maps available on https://github.com/elasmobranch23/Sperm-storage-maps

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Jordan, R.P., Graham, C.T., Minto, C. et al. Assessment of sperm storage across different reproductive modes in the elasmobranch fishes. Environ Biol Fish 104, 27–39 (2021). https://doi.org/10.1007/s10641-020-01051-x

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  • DOI: https://doi.org/10.1007/s10641-020-01051-x

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