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Ovarian development in Argentinean shortfin squid Illex argentinus: group-synchrony for corroboration of intermittent spawning strategy

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Abstract

Modern living cephalopod species have evolved a wide phenotypic diversity and flexibility of reproductive strategies, which is closely linked to the pattern of oogenesis and oocytes ovulation of species. Although it has been suggested that Argentinean shortfin squid Illex argentinus lay eggs intermittently, there is still little evidence for the mode of oocyte production and development. In this study, the ovarian development of I. argentinus was investigated by using histological analysis of ovaries, and six distinct histological stages of ovarian development were found among the ovaries. For each histological stage of the ovary, the frequency distribution of both number and occupied areas by each oogenesis stage was unimodal, and that gradually progressed along with ovarian development. The oocyte size distribution in ovaries before reaching vitellogenic stage was unimodal, bimodal in vitellogenic ovaries, and polymodal in ripe and partially spent ovaries. This evidence indicates that I. argentinus undergoes group-synchronous ovarian development, with a single dominant oocyte stock being produced to develop in several batches for a multiple-batch group-synchronous ovulation and confirms the intermittent spawning strategy of this species.

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References

  • Acha, E. M., H. W. Mianzan, R. A. Guerrero, M. Favero & J. Bava, 2004. Marine fronts at the continental shelves of austral South America: physical and ecological processes. Journal of Marine Systems 44: 83–105.

    Article  Google Scholar 

  • Adcock, G. J., P. W. Shaw, P. G. Rodhouse & G. R. Carvalho, 1999. Microsatellite analysis of genetic diversity in the squid Illex argentinus during a period of intensive fishing. Marine Ecology Progress Series 187: 171–178.

    Article  Google Scholar 

  • Anderson, C. I. & P. G. Rodhouse, 2001. Life cycles, oceanography and variability: ommastrephid squid in variable oceanographic environments. Fisheries Research 54: 133–143.

    Article  Google Scholar 

  • Arizmendi-Rodríguez, D. I., C. Rodríguez-Jaramillo, C. Quiñonez-Velázquez & C. A. Salinas-Zavala, 2012. Reproductive indicators and gonad development of the Panama brief squid Lolliguncula panamensis (Berry 1911) in the Gulf of California, Mexico. Journal of Shellfish Research 31: 817–826.

    Article  Google Scholar 

  • Arkhipkin, A., 1993. Age, growth, stock structure and migratory rate of pre-spawning short-finned squid Illex argentinus based on statolith ageing investigations. Fisheries Research 16: 313–338.

    Article  Google Scholar 

  • Arkhipkin, A. I., 2012. Squid as nutrient vectors linking Southwest Atlantic marine ecosystems. Deep-Sea Research Part II: Topical Studies in Oceanography 95: 7–20.

    Article  Google Scholar 

  • Arkhipkin, A. & V. Laptikhovsky, 1994. Seasonal and interannual variability in growth and maturation of winter-spawning Illex argentinus (Cephalopoda, Ommastrephidae) in the Southwest Atlantic. Aquatic Living Resources 7: 221–232.

    Article  Google Scholar 

  • Asturiano, J. F., L. A. Sorbera, J. Ramos, D. E. Kime, M. Carrillo & S. Zanuy, 2002. Group-synchronous ovarian development, spawning and spermiation in the European sea bass (Dicentrarchus labrax L.) could be regulated by shifts in gonadal steroidogenesis. Scientia Marina 66: 273–282.

    Article  Google Scholar 

  • Bainy, M. C. R. S. & M. Haimovici, 2012. Seasonality in Growth and Hatching of the Argentine Short-Finned Squid Illex argentinus (Cephalopoda: Ommastrephidae) Inferred from Aging on Statoliths in Southern Brazil. Journal of Shellfish Research 31: 135–143.

    Article  Google Scholar 

  • Bolognari, A., M. P. A. Carmignani & G. Zaccone, 1976. A cytochemical analysis of the follicular cells and the yolk in the growing oocytes of Octopus vulgaris (Cephalopoda, Mollusca). Acta Histochemica 55: 167–175.

    Article  CAS  PubMed  Google Scholar 

  • Bottke, W., 1974. The fine structure of the ovarian follicle of Alloteuthis subulata Lam. (Mollusca, Cephalopoda). Cell and Tissue Research 150: 463–479.

    Article  CAS  PubMed  Google Scholar 

  • Boyle, P. & P. Rodhouse, 2005. Cephalopods: Ecology and Fisheries. Wiley-Blackwell, Oxford.

    Book  Google Scholar 

  • Boyle, P. R., G. J. Pierce & L. C. Hastie, 1995. Flexible reproductive strategies in the squid Loligo forbesi. Marine Biology 121: 501–508.

    Article  Google Scholar 

  • Brunetti, N., M. Ivanovic, E. Louge & H. Christiansen, 1991. Estudio de la biología reproductiva y de la fecundidad en dos subpoblaciones del calamar (Illex argentinus) [Reproductive biology and fecundity of two stocks of the squid (Illex argentinus)]. Frente Marítimo 8: 73–84.

    Google Scholar 

  • Brunetti, N. E., B. Elena, G. R. Rossi, M. L. Ivanovic, A. Aubone, R. Guerrero & H. Benavides, 1998a. Summer distribution, abundance and population structure of Illex argentinus on the Argentine shelf in relation to environmental features. South African Journal of Marine Science 20: 175–186.

    Article  Google Scholar 

  • Brunetti, N. E., M. Ivanovic, G. Rossi, B. Elena & S. Pineda, 1998b. Fishery biology and life history of Illex argentinus. In Okutani, T. (ed.), Contributed Papers to International Symposium on Large Pelagic Squids, July 18–19, 1996, for JAMARC’s 25th Anniversary of Its Foundation. Japan Marine Fishery Resources Research Center (JAMARC), Tokyo: 217–231.

    Google Scholar 

  • Carvalho, G. R., A. Thompson & A. L. Stoner, 1992. Genetic diversity and population differentiation of the shortfin squid Illex argentinus in the south-west Atlantic. Journal of Experimental Marine Biology and Ecology 158: 105–121.

    Article  Google Scholar 

  • Collins, M. A., G. M. Burnell & P. G. Rodhouse, 1995. Reproductive strategies of male and female Loligo forbesi (Cephalopoda: Loliginidae). Journal of the Marine Biological Association of the United Kingdom 75: 621–634.

    Article  Google Scholar 

  • Cornwell, R. E., M. J. Law Smith, L. G. Boothroyd, F. R. Moore, H. P. Davis, M. Stirrat, B. Tiddeman & D. I. Perrett, 2006. Reproductive strategy, sexual development and attraction to facial characteristics. Philosophical Transactions of the Royal Society of London B: Biological Sciences 361: 2143–2154.

    Article  PubMed  PubMed Central  Google Scholar 

  • Crespi-Abril, A. C., E. M. Morsan, G. N. Williams & D. A. Gagliardini, 2013. Spatial distribution of Illex argentinus in San Matias Gulf (Northern Patagonia, Argentina) in relation to environmental variables: a contribution to the new interpretation of the population structuring. Journal of Sea Research 77: 22–31.

    Article  Google Scholar 

  • FAO, 2014. The State of World Fisheries and Aquaculture 2014. Opportunities and Challenges. FAO, Rome.

    Google Scholar 

  • Gan, J., L. A. Mysak & D. N. Straub, 1998. Simulation of the South Atlantic Ocean circulation and its seasonal variability. Journal of Geophysical Research: Oceans 103: 10241–10251.

    Article  Google Scholar 

  • Haimovici, M., N. Brunetti, P. Rodhouse, J. Csirke & R. Leta, 1998. Illex argentinus. In Rodhouse, P. G., E. G. Dawe & R. K. O’Dor (eds), Squid Recruitment Dynamics: The Genus Illex as A model, The Commercial Illex Species and Influences on Variability, Vol. 376. FAO, Rome: 27–58.

    Google Scholar 

  • Hanlon, R. T., N. Kangas & J. W. Forsythe, 2004. Egg-capsule deposition and how behavioral interactions influence spawning rate in the squid Loligo opalescens in Monterey Bay, California. Marine Biology 145: 923–930.

    Article  Google Scholar 

  • Harman, R. F., R. E. Young, S. B. Reid, K. M. Mangold, T. Suzuki & R. F. Hixon, 1989. Evidence for multiple spawning in the tropical oceanic squid Stenoteuthis oualaniensis (Teuthoidea: Ommastrephidae). Marine Biology 101: 513–519.

    Article  Google Scholar 

  • Hernández-Muñoz, A. T., C. Rodríguez-Jaramillo, A. Mejía-Rebollo & C. A. Salinas-Zavala, 2016. Reproductive strategy in jumbo squid Dosidicus gigas (D’Orbigny, 1835): a new perspective. Fisheries Research 173: 145–150.

    Article  Google Scholar 

  • Hoving, H. J. T. & M. R. Lipiński, 2009. Female reproductive biology, and age of deep-sea squid Histioteuthis miranda from southern Africa. ICES Journal of Marine Science: Journal du Conseil 66: 1868–1872.

    Article  Google Scholar 

  • Hoving, H. J. T., V. V. Laptikhovsky, M. R. Lipinski & E. Jürgens, 2014. Fecundity, oogenesis, and ovulation pattern of southern African Lycoteuthis lorigera (Steenstrup, 1875). Hydrobiologia 725: 23–32.

    Article  CAS  Google Scholar 

  • ICES, 2010. Report of the Workshop on Sexual Maturity Staging of Cephalopods, 8–11 November 2010, Livorno, Italy. ICES CM 2010/ACOM: 49.

  • Jackson, G. D. & P. V. Mladenov, 1994. Terminal spawning in the deepwater squid Moroteuthis ingens (Cephalopoda: Onychoteuthidae). Journal of Zoology 234: 189–201.

    Article  Google Scholar 

  • Jereb, P. & C. Roper, 2005. Cephalopods of the World, an Annotated and Illustrated Catalogue of Cephalopod Species Known to Date. Chambered Nautiluses and Sepioids (Nautilidae, Sepiidae, Sepiolidae, Sepiadariidae, Idiosepiidae and Spirulidae), Vol. 1. FAO, Rome.

  • Jereb, P. & C. F. E. Roper, 2010. Cephalopods of the World. An Annotated and Illustrated Catalogue of Cephalopod Species Known to Date. Myopsid and Oegopsid Squids, Vol. 2. FAO, Rome.

  • Jiang, X. M., F. Y. Fu, Z. Li & X. D. Feng, 2007. Study on the oogenesis and ovarial development of Sepiella maindroni. Journal of Fisheries of China 31: 607–617.

    Google Scholar 

  • Laptikhovsky, V., 2001. First data on ovary maturation and fecundity in the squid family Histioteuthidae. Scientia Marina 65: 127–129.

    Article  Google Scholar 

  • Laptikhovsky, V. V. & A. I. Arkhipkin, 2001. Oogenesis and gonad development in the cold water loliginid squid Loligo gahi (Cephalopoda: Myopsida) on the Falkland shelf. Journal of Molluscan Studies 67: 475–482.

    Article  Google Scholar 

  • Laptikhovsky, V. & C. M. Nigmatullin, 1992. Caracteristicas reproductivas de machos y hembras del calamar (Illex argentinus). Frente Marítimo 12: 23–37.

    Google Scholar 

  • Laptikhovsky, V. V. & C. M. Nigmatullin, 1993. Egg size, fecundity, and spawning in females of the genus Illex (Cephalopoda: Ommastrephidae). ICES Journal of Marine Science: Journal du Conseil 50: 393–403.

    Article  Google Scholar 

  • Laptikhovsky, V. V. & C. M. Nigmatullin, 1999. Egg size and fecundity in females of the subfamilies Todaropsinae and Todarodinae (Cephalopoda: Ommastrephidae). Journal of the Marine Biological Association of the United Kingdom 79: 569–570.

    Article  Google Scholar 

  • Laptikhovsky, V. V. & C. M. Nigmatullin, 2005. Aspects of female reproductive biology of the orange-back squid, Sthenoteuthis pteropus (Steenstup) (Oegopsina: Ommastrephidae) in the eastern tropical Atlantic. Scientia Marina 69: 383–390.

    Article  Google Scholar 

  • Laptikhovsky, V. V., A. I. Arkhipkin & H. J. T. Hoving, 2007. Reproductive biology in two species of deep-sea squids. Marine Biology 152: 981–990.

    Article  Google Scholar 

  • Laptikhovsky, V., C. M. Nigmatullin, H. Hoving, B. Onsoy, A. Salman, K. Zumholz & G. Shevtsov, 2008. Reproductive strategies in female polar and deep-sea bobtail squid genera Rossia and Neorossia (Cephalopoda: Sepiolidae). Polar Biology 31: 1499–1507.

    Article  Google Scholar 

  • Lu, H. J. & X. J. Chen, 2012. Age, growth and population structure of Illex argentinus based on statolith microstructure in Southwest Atlantic Ocean. Journal of Fisheries of China 36: 1049–1056.

    Article  Google Scholar 

  • Mackie, M. & P. Lewis, 2001. Assessment of gonad staging systems and other methods used in the study of the reproductive biology of narrow-barred Spanish mackerel, Scomberomorus commerson, in Western Australia. Department of Fisheries Perth, Western Australia 136: 1–32.

  • McBride, R. S., S. Somarakis, G. R. Fitzhugh, A. Albert, N. A. Yaragina, M. J. Wuenschel, A. Alonso-Fernández & G. Basilone, 2013. Energy acquisition and allocation to egg production in relation to fish reproductive strategies. Fish and Fisheries 15: 1–35.

    Google Scholar 

  • McBride, R. S., R. Ferreri, E. K. Towle, J. M. Boucher & G. Basilone, 2016. Yolked oocyte dynamics support agreement between determinate- and indeterminate-method estimates of annual fecundity for a northeastern United States Population of American Shad. PLoS ONE 11: e0164203.

    Article  PubMed  PubMed Central  Google Scholar 

  • Melo, Y. C. & W. H. H. Sauer, 1998. Ovarian atresia in cephalopods. South African Journal of Marine Science 20: 143–151.

    Article  Google Scholar 

  • Melo, Y. C. & W. H. H. Sauer, 1999. Confirmation of serial spawning in the chokka squid Loligo vulgaris reynaudii off the coast of South Africa. Marine Biology 135: 307–313.

    Article  Google Scholar 

  • Mendo, T., J. M. Semmens, J. M. Lyle, S. R. Tracey & N. Moltschaniwskyj, 2016. Reproductive strategies and energy sources fuelling reproductive growth in a protracted spawner. Marine Biology 163: 1–11.

    Article  Google Scholar 

  • Murua, H. & F. Saborido-Rey, 2003. Female reproductive strategies of marine fish species of the North Atlantic. Journal of Northwest Atlantic Fishery Science 31: 23–31.

    Article  Google Scholar 

  • Mylonas, C. & Y. Zohar, 2007. Promoting oocyte maturation, ovulation and spawning in farmed fish. In Babin, P., J. Cerdà & E. Lubzens (eds), The Fish Oocyte: From Basic Studies to Biotechnological Applications. Springer Netherlands, Dordrecht: 437–474.

    Chapter  Google Scholar 

  • Nigmatullin, C. M., 2011. Two spawning patterns in ommastrephid squids and other cephalopods. In 4th International Symposium “Coleoid Cephalopods Through Time”. Museum fur Naturkunde Stuttgart, Stuttgart, Abstract volume: 48.

  • Nigmatullin, C. M. & V. Laptikhovsky, 1994. Reproductive strategies in the squids of the family Ommastrephidae (preliminary report). Ruthenica 4: 79–82.

    Google Scholar 

  • Nigmatullin, C. M. & U. Markaida, 2009. Oocyte development, fecundity and spawning strategy of large sized jumbo squid Dosidicus gigas (Oegopsida: Ommastrephinae). Journal of the Marine Biological Association of the United Kingdom 89: 789–801.

    Article  Google Scholar 

  • Nigmatullin, C. M., A. Arkhipkin & R. Sabirov, 1995. Age, growth and reproductive biology of diamond-shaped squid Thysanoteuthis rhombus (Oegopsida: Thysanoteuthidae). Marine Ecology Progress Series 43: 73–87.

    Article  Google Scholar 

  • Ortiz, N., 2013. Validation of macroscopic maturity stages of the Patagonian red octopus Enteroctopus megalocyathus. Journal of the Marine Biological Association of the United Kingdom 93: 833–842.

    Article  Google Scholar 

  • Pecl, G., 2001. Flexible reproductive strategies in tropical and temperate Sepioteuthis squids. Marine Biology 138: 93–101.

    Article  Google Scholar 

  • Rocha, F. & A. Guerra, 1996. Signs of an extended and intermittent terminal spawning in the squids Loligo vulgaris Lamarck and Loligo forbesi Steenstrup (Cephalopoda: Loliginidae). Journal of Experimental Marine Biology and Ecology 207: 177–189.

    Article  Google Scholar 

  • Rocha, F., Á. Guerra & Á. F. González, 2001. A review of reproductive strategies in cephalopods. Biological Reviews 76: 291–304.

    Article  CAS  PubMed  Google Scholar 

  • Rodrigues, M., M. Garcí, J. Troncoso & Á. Guerra, 2011. Spawning strategy in Atlantic bobtail squid Sepiola atlantica (Cephalopoda: Sepiolidae). Helgoland Marine Research 65: 43–49.

    Article  Google Scholar 

  • Rodrigues, M., Á. Guerra & J. S. Troncoso, 2012. Reproduction of the Atlantic bobtail squid Sepiola atlantica (Cephalopoda: Sepiolidae) in northwest Spain. Invertebrate Biology 131: 30–39.

    Article  Google Scholar 

  • Sauer, W. H. & M. R. Lipiński, 1990. Histological validation of morphological stages of sexual maturity in chokker squid Loligo vulgaris reynaudii D’Orb (Cephalopoda: Loliginidae). South African Journal of Marine Science 9: 189–200.

    Article  Google Scholar 

  • Schwarz, R. & J. A. A. Perez, 2013. Age structure and life cycles of the Argentine shortfin squid Illex argentinus (Cephalopoda: Ommastrephidae) in southern Brazil. Journal of the Marine Biological Association of the United Kingdom 93: 557–565.

    Article  Google Scholar 

  • Selman, K. & J. M. Arnold, 1977. An ultrastructural and cytochemical analysis of oogenesis in the squid, Loligo pealei. Journal of Morphology 152: 381–400.

    Article  CAS  PubMed  Google Scholar 

  • Sieiro, P., J. Otero & Á. Guerra, 2014. Contrasting macroscopic maturity staging with histological characteristics of the gonads in female Octopus vulgaris. Hydrobiologia 730: 113–125.

    Article  Google Scholar 

  • Wallace, R. A. & K. Selman, 1981. Cellular and dynamic aspects of oocyte growth in Teleosts. American Zoologist 21: 325–343.

    Article  Google Scholar 

  • Wright, P. J., 1992. Ovarian development, spawning frequency and batch fecundity in Encrasicholina heteroloba (Ruppell, 1858). Journal of Fish Biology 40: 833–844.

    Article  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China under Grant NSFC41306127; Natural Science Foundation of Shanghai under Grant 16ZR1415400; and the Innovation Program of Shanghai Municipal Education Commission under Grant 13YZ091. This work was under the protocol of Shanghai Ocean University’s postdoctoral science foundation (A2-0203-00-100325) and Shanghai Ocean University’s Sci-Tech foundation (A2-0203-00-100213). The involvement of Y. Chen was supported by SHOU International Center for Marine Studies and Shanghai 1000 Talent Program. Thanks to Cheng Zhou, Fengying Li, Hao Tang, Guancha Lan, Yue Jin, Guanyu Hu, Miao Zhang, Hang Su, and Min Jiao for the biological data collected in the laboratory; Dr. Chingis Nigmatullin, Dr. Iacopo Bertocci, and other anonymous reviewers for providing valuable comments and suggestions on the manuscript; and Mr. Deepan Selvaraj and Ms. Pauline Lichtveld for assistance.

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Lin, D., Chen, X., Chen, Y. et al. Ovarian development in Argentinean shortfin squid Illex argentinus: group-synchrony for corroboration of intermittent spawning strategy. Hydrobiologia 795, 327–339 (2017). https://doi.org/10.1007/s10750-017-3154-y

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