Spawning pattern of the neon flying squid Ommastrephes bartramii (Cephalopoda: Oegopsida) around the Hawaiian Islands
DOI:
https://doi.org/10.3989/scimar.04112.27BKeywords:
North Pacific, squid, Ommastrephes bartramii, reproductive strategy, spawning patternAbstract
The neon flying squid, Ommastrephes bartramii, is an oceanic squid species that is widely distributed in the North Pacific, with the winter-spring cohort spawning around the Hawaiian Islands. Here, we investigated the spawning characteristics of O. bartramii by analyzing various reproductive parameters of individuals (622 males, 108 females) collected in this region. Female spawning status was determined from the somatic indices and histological characteristics of the ovaries. At all developmental stages, the ovaries of spawned females contained oocytes, and oviduct fullness was not correlated with body size. Thus, because the eggs mature asynchronously, with multiple filling and evacuation events, this species is considered an intermittent spawner. Mature males with developed accessory glands were also present within the distribution range of healthy spawned females, indicating that mating occurs between spawning events. Our data indicate that the first spawning event occurs at a mantle length of ~520-540 mm for Hawaiian O. bartramii. Subsequently, the squid forage and grow, and refill the oviducts, before the second spawning event occurs.
Downloads
References
Arkhipkin A.I., Laptikhovsky V.V., Nigmatullin Ch.M., et al. 1998. Growth, reproduction and feeding of the tropical squid Ornithoteuthis antillarum (Cephalopoda: Ommastrephidae) from the central - east Atlantic. Sci. Mar. 62: 273-288. http://dx.doi.org/10.3989/scimar.1998.62n3273
Bigelow K., Landgraph K. 1993. Hatch dates and growth of Ommastrephes bartramii paralarvae from Hawaiian waters as determined from statolith analysis. In: Okutani T., O'Dor R.K., Kubodera T. (eds), Recent Advances in Cephalopod Fisheries Biology. Tokai University Press, Tokyo, pp. 15-24.
Bower J.R., Ichii T. 2005. The red flying squid (Ommastrephes bartramii): A review of recent research and the fishery in Japan. Fish. Res. 76: 39-55. http://dx.doi.org/10.1016/j.fishres.2005.05.009
Bower J.R., Sakurai Y. 1996. Laboratory observations on Todarodes pacificus (Cephalopoda: Ommastrephidae) egg masses. Am. Malacol. Bull. 13: 65-71.
Boyle P. 1983. Cephalopod Life Cycles: Species Accounts. Academic Press, London.
Boyle P., Rodhouse P. 2005. Cephalopods: Ecology and Fisheries, Vol. 1. Blackwell Science Ltd., Oxford. http://dx.doi.org/10.1002/9780470995310 PMid:17012863
Brunetti N., Ivanovic M., Aubone A., et al. 2006. Reproductive biology of red squid (Ommastrephes bartramii) in the Southwest Atlantic. Revista de Investigación y Desarrollo Pesquero 18: 5-19.
Calow P. 1987. Fact and theory - an overview. In: Boyle, P. (ed.), Cephalopod Life Cycles, Vol. 2. Comparative reviews. Academic Press, London, pp. 351-365.
Chen C.S., Chiu T.S. 2003. Variations of life history parameters in two geographical groups of the neon flying squid, Ommastrephes bartramii, from the North Pacific. Fish. Res. 63: 349-366. http://dx.doi.org/10.1016/S0165-7836(03)00101-2
Cullen J. 1982. The deep chlorophyll maximum: comparing vertical profiles of chlorophyll a. Can. J. Fish. Aquat. Sci. 39: 791-803 http://dx.doi.org/10.1139/f82-108
Durward R.D., Amaratunga T., O'Dor R.K. 1979. Maturation index and fecundity for female squid Illex illecebrosus (Leseue, 1821). ICNAF Res. Bull. 14: 67-72.
Eppley R., Peterson E. 1979. Particulate organic matter flux and planktonic new production in the deep ocean. Nature 282: 677-680. http://dx.doi.org/10.1038/282677a0
González Á.F., Guerra Á., 1996. Reproductive biology of the short-finned squid Illex coindetii (Cephalopoda, Ommastrephidae) of the northeastern Atlantic. Sarsia 81: 107-118.
Harman R.F., Young R.E., Reid S.B., et al. 1989. Evidence for multiple spawning in the tropical oceanic squid Stenoteuthis oualaniensis (Teuthoidea: Ommastrephidae). Mar. Biol. 101: 513-519. http://dx.doi.org/10.1007/BF00541653
Ichii T., Mahapatra K., Sakai M., et al. 2009. Life history of the neon flying squid: effect of the oceanographic regime in the North Pacific Ocean. Mar. Ecol. Prog. Ser. 378: 1-11. http://dx.doi.org/10.3354/meps07873
Ikeda Y., Sakurai Y., Shimazaki K. 1993. Maturation process of the Japanese common squid Todarodes pacificus in captivity. In: Okutani T., O'Dor R.K., Kubodera T. (eds), Recent Advances in Cephalopod Fisheries Biology. Tokai University Press, Tokyo, pp. 179-187. PMid:8325065
Jereb P., Roper C.F.E. 2010. Myopsid and Oegopsid Squids, in Cephalopods of the World: An Annotated and Illustrated Catalogue of Cephalopods Species Known to Date. FAO Species Catalogue for Fisheries Purposes No 4 Vol 2.
Kidokoro H., Sakurai Y. 2008. Effect of water temperature on gonadal development and emaciation of Japanese common squid Todarodes pacificus. Fish. Sci. 74: 553-561. http://dx.doi.org/10.1111/j.1444-2906.2008.01558.x
Li S.L., Liu B.L., Chen X.J., et al. 2011. Reproductive biology of neon flying squid (Ommastrephes bartramii) in Northwest Pacific ocean. Oceanol. Limnol. Sinica 42: 179-185.
Laptikhovsky V. 2011. Ecology of Cephalopod reproduction. LAP Lambert Academic Publishing GmBH & Co. Saarbru.chen, Germany. 233 pp. (In Russian).
Laptikhovsky V.V., Murzoy S.A. 1990. Epipelagic egg mass of the squid Sthenoteuthis pteropus collected in the tropical eastern Atlantic. Biologya Morya 3: 62-63.
Laptikhovsky V.V., Nigmatullin Ch.M. 1992. Caracteristicas reproductivas de machos y hembras de calamar (Illex argentinus). Frente Maritimo 12: 23-37.
Laptikhovsky V.V., Nigmatullin Ch.M. 1993. Egg size, fecundity, and spawning in females of the genus Illex (Cephalopoda, Ommastrephidae). ICES J. Mar. Sci. 50: 393-403. http://dx.doi.org/10.1006/jmsc.1993.1044
Laptikhovsky V.V., Nigmatullin Ch.M. 1999. Egg size and fecundity in females of the subfamilies Todaropsinae and Todarodinae (Cephalopoda: Ommastrephidae). J. Mar. Biol. Assoc. UK. 79: 569-570. http://dx.doi.org/10.1017/S002531549800071X
Laptikhovsky V.V., Nigmatullin Ch.M. 2005. Female reproductive biology of the orange-back squid, Sthenoteuthis pteropus (Steenstup) (Ommastrephidae: Oegopsidae) in the eastern tropical Atlantic. Sci. Mar. 69: 383-390.
Laptikhovsky V., Collins M.A., Arkhipkin A. 2013. First case of possible iteroparity among coleoid cephalopods: the giant warty squid Kondakovia longimana. J. Molluscan Stud. 79: 270-272. http://dx.doi.org/10.1093/mollus/eyt014
Moltschaniwskyj N.A. 1995. Multiple spawning in the tropical squid Photololigo sp.: what is the cost in somatic growth? Mar. Biol. 124: 127-135. http://dx.doi.org/10.1007/BF00349154
Murata M., Hayase S. 1993. Life history and biological information on flying squid (Ommastrephes bartramii) in the North Pacific Ocean. Int. North Pac. Fish. Comm. Bull. 53: 147-182.
Murata M., Nakamura Y. 1998. Seasonal migration and diel migration of the neon flying squid, (Ommastrephes bartramii), in the North Pacific. In: Okutani, T. (ed.), International Symposium on Large Pelagic Squids. Japan Marine Fishery Resources Research Center, Tokyo, pp. 1330. PMid:9703820
Nesis K. 1996. Mating, spawning, and death in oceanic cephalopods: a review. Ruthenica 6: 23-64.
Nigmatullin Ch.M. 1989. Las especies de calamar mas abundates del Atlantico Sudoeste y sinopsis sobre la ecologia del calamar (Illex argentinus). Frente Maritimo 5: 71-81.
Nigmatullin Ch.M. 1997. Egg size, fecundity, vitelline oocyte resorption, and spawning in the Gonatid squid, Berryteuthis magister (Gonatidae). In: 63rd Annual Meeting American Malacological Union (21-27 June 1997, Santa Barbara, California). Abstracts. pp. 46.
Nigmatullin Ch.M. 2002. Ovary development, potential and actual fecundity and oocyte resorption in coleoid cephalopods: a review. In: International Symposium "Coleoid cephalopods through time" (17-19 September 2002, Berlin). Berliner Palabiologische Abhandlungen. Bd. pp. 82-84.
Nigmatullin Ch.M. 2011. Two spawning patterns in ommastrephid squids and other cephalopods. 4th International symposium "Coleoid cephalopods through time" (6-9 September 2011, Stuttgart, Germany). Abstract volume. Stuttgart: Museum fur Naturkunde Stuttgart. pp. 48.
Nigmatullin C.M., Laptikhovsky V.V. 1994. Reproductive strategies in the squids of the family Ommastrephidae (preliminary report). Ruthenica 4: 79-82.
Nigmatullin Ch.M., Laptikhovsky V.V. 1999. Reproductive biology in females of the subfamilies Todaropsinae and Todarodinae (Cephalopoda: Ommastrephidae). Ruthenica 9: 63-75.
Nigmatullin C.M., Markaida U. 2009. Oocyte development, fecundity and spawning strategy of large sized jumbo squid Dosidicus gigas. J. Mar. Biol. Assoc. UK. 89:789-801. http://dx.doi.org/10.1017/S0025315408002853
Nigmatullin C.M., Arkhipkin A.I., Sabirov R.M. 1995. Age, growth and reproductive-biology of diamond-shaped squid Thysanoteuthis rhombus (Oegopsida, Thysanoteuthidae). Mar. Ecol. Prog. Ser. 124: 73-87. http://dx.doi.org/10.3354/meps124073
Nigmatullin C.M., Laptikhovsky V.V., Sabirov R.M. 1996. Reproductive biology of commander squid. In: Jelizarov A.A. (ed.), "Commercial aspects of biology of commander squid Berryteuthis magister and of fishes of slope communities in the westrn part of the Bering Sea". Moscow: VNIRO Publ. pp. 101-124 (In Russian).
Nigmatullin C.M., Sabirov R.M., Zalygalin V.P. 2003. Ontogenetic aspects of morphology, size structure and production of spermatophores in ommmastrephid squids: an overview. In: Warnke K., Keupp H., Boletzky S.v. (eds), Coleoid cephalopods through time. Berliner Palabiologische Abhandlungen. Bd. pp. 225-240.
Nixon M. 1983. Teuthowenia megalops. In: Boyle, P. (ed.), Cephalopod Life Cycles, Vol. 1. Academic Press, pp. 233-247
O'Dor R.K. 1983. Illex illecebrosus. In: Boyle P. (ed.), Cephalopod Life Cycles, Vol. 1. Academic Press, pp. 175-199
O'Dor R.K., Dawe E. 1998. Illex illecebrosus. In: Rodhouse P., Dawe E.G., O'Dor R.K. (eds), Squid Recruitment Dynamics FAO Fish. Tech. Pap. 376. FAO, Rome, pp. 77-104
Okutani T., Tung I.H. 1978. Review of biology of commercially important squids in Japanese and adjacent waters. Symplectoteuthis oualaniensis (Lesson). Veliger 21: 87-95.
R Core Development Team 2013. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.r-project.org/
Rasero M., González Á.F., Guerra Á. 1995. Spawning pattern and fecundity of the Ommastrephid squid Todaropsis eblanae in northeastern Atlantic waters. ICES CM1995/K9 1-18.
Reznik Y.I., Bessmertnaya N.B. 1993. Ripening, fecundity and spawning of neon flying squid (Ommastrephes bartramii) in the North West Pacific ocean. Bull. Int. North Pac. Fish. Comm. 53: part II: 205.
Rocha F., Guerra Á., González Á.F. 2001. A review of reproductive strategies in cephalopods. Biol. Rev. 76: 291-304. http://dx.doi.org/10.1017/S1464793101005681 PMid:11569786
Roden G. 1991. Subarctic-subtropical transition zone of the North Pacific: large-scale aspects and mesoscale structure. NOAA National Marine Fisheries Service Technical Report, pp. 105-138.
Rodhouse P. 1998. Physiological progenesis in cephalopod molluscs. Biol. Bull. 195: 17-20. http://dx.doi.org/10.2307/1542771
Roper C.F.E., Nigmatullin C., Jereb P. 2010. Family Ommastre phidae, In: Jereb, P., Roper, C.F.E. (eds), Cephalopods of the World: An Annotated and Illustrated Catalogue of Cephalopod Species Known to Date. Volume 2: Myopsid Oegopsid Squids. FAO Species Catalogue for Fisheries Purposes No. 4. Vol. 2. Rome, pp. 269-347.
Sakurai Y., Kiyofuji H., Saitoh S., et al. 2000. Changes in inferred spawning sites of Todarodes pacificus (Cephalopoda: Ommastrephidae) due to changing environmental conditions. ICES J. Mar. Sci. 57: 24-30. http://dx.doi.org/10.1006/jmsc.2000.0667
Staaf D.J., Camarillo-Coop S., Haddock S.H.D., et al. 2008. Natural egg mass deposition by the Humboldt squid (Dosidicus gigas) in the Gulf of California and characteristics of hatchlings and paralarvae. J. Mar. Biol. Assoc. UK. 88: 759-770. http://dx.doi.org/10.1017/S0025315408001422
Yatsu A., Tanaka H., Mori J. 1998. Population structure of the neon flying squid, Ommastrephes bartramii, in the North Pacific Ocean. In: Okutani, T. (ed.), International Symposium on Large Pelagic Squids. Japan Marine Fishery Resources Research Center: Tokyo, pp. 31-48
Young R.E., Hirota J., Parry M. 1997. Aspects of the ecology of the red squid Ommastrephes bartramii, a potential target for a major Hawaiian fishery. FY 1997 Progress Report. Pelagic Fisheries Research Program, JIMAR.
Zuyev G., Nigmatullin Ch., Chesalin M., et al. 2002. Main results of long-term worldwise studies on tropical nektonic oceanic squid genus Sthenoteuthis: An overview of the Soviet investigations. Bull. Mar. Sci. 71(2): 1019-1060.
Young R.E., Hirota J., Parry M. 1997. Aspects of the ecology of the red squid Ommastrephes bartramii, a potential target for a major Hawaiian fishery. FY 1997 Progress Report. Pelagic Fisheries Research Program, JIMAR.
Zuyev G., Nigmatullin Ch., Chesalin M., Nesis K. 2002. Main results of long-term worldwise studies on tropical nektonic oceanic squid genus Sthenoteuthis: An overview of the Soviet investigations. Bull. Mar. Sci. 71(2): 1019-1060.
Published
How to Cite
Issue
Section
License
Copyright (c) 2014 Consejo Superior de Investigaciones Científicas (CSIC)
This work is licensed under a Creative Commons Attribution 4.0 International License.
© CSIC. Manuscripts published in both the printed and online versions of this Journal are the property of Consejo Superior de Investigaciones Científicas, and quoting this source is a requirement for any partial or full reproduction.All contents of this electronic edition, except where otherwise noted, are distributed under a “Creative Commons Attribution 4.0 International” (CC BY 4.0) License. You may read here the basic information and the legal text of the license. The indication of the CC BY 4.0 License must be expressly stated in this way when necessary.
Self-archiving in repositories, personal webpages or similar, of any version other than the published by the Editor, is not allowed.