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Brooding and sperm storage by the deep-sea squid Bathyteuthis berryi (Cephalopoda: Decapodiformes)

Published online by Cambridge University Press:  23 February 2012

Stephanie L. Bush ,
Hendrik J. T. Hoving ,
Christine L. Huffard ,
Bruce H. Robison  and
Louis D. Zeidberg
Stephanie L. Bush*
Affiliation:
University of Rhode Island, Department of Biological Sciences, 120 Flagg Road, Kingston, RI 02881 Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039
Hendrik J. T. Hoving
Affiliation:
Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039
Christine L. Huffard
Affiliation:
Conservation International, 2011 Crystal Drive, Suite 500, Arlington, VA 22202
Bruce H. Robison
Affiliation:
Monterey Bay Aquarium Research Institute, 7700 Sandholdt Road, Moss Landing, CA 95039
Louis D. Zeidberg
Affiliation:
California Department of Fish and Game, Marine Region, 20 Lower Ragsdale Drive, Suite 100, Monterey, CA 93940, USA
*
Correspondence should be addressed to: S.L. Bush, University of Rhode Island, Department of Biological Sciences, 120 Flagg Road, Kingston, RI 02881 email: [email protected]
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Abstract

Squids of the family Bathyteuthidae have generally been infrequently encountered in their deep-sea habitat. Remotely operated vehicles were used to observe seven individuals in situ in the Monterey Submarine Canyon, CA, USA. One of these was a female Bathyteuthis berryi holding a sheet with approximately 360 embedded embryos. Examination of this female after collection revealed the presence of a seminal receptacle on the buccal membrane. We present some potential costs and benefits of post-spawning egg care, a strategy that is now known for two families of deep-dwelling squids, but may turn out to be more common with the increasing exploration of the deep sea.

Keywords

Bathyteuthisbroodingdeep seareproductionseminal receptaclesperm storagesquid
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 92 , Issue 7 , November 2012 , pp. 1629 - 1636
Copyright
Copyright © Marine Biological Association of the United Kingdom 2012

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References

REFERENCES

Arkhipkin, A.I. and Bjorke, H. (1999) Ontogenetic changes in morphometric and reproductive indices of the squid Gonatus fabricii (Oegopsida, Gonatidae) in the Norwegian Sea. Polar Biology 22, 357–365.CrossRefGoogle Scholar
Bagenal, T.B. (1978) Aspects of fish fecundity. In Gerking, S.D. (ed.) Ecology of freshwater fish production. Ambleside, UK: FBA, Windermere Laboratory, pp. 75–101.Google Scholar
Boletzky, S.v. (1994) Embryonic development of cephalopods at low temperatures. Antarctic Science 6, 139–142.CrossRefGoogle Scholar
Boletzky, S.v. (2003) A lower limit to adult size in coleoid cephalopods: elements of a discussion. Berliner Paläobiologische Abhandlungen 3, 19–28.Google Scholar
Boyle, P.R. and Rodhouse, P.G. (2005) Cephalopods: ecology and fisheries. Oxford: Blackwell Science.CrossRefGoogle Scholar
Bush, S.L. and Robison, B.H. (2007) Ink utilization by mesopelagic squid. Marine Biology 152, 485–494.CrossRefGoogle Scholar
Bush, S.L., Robison, B.H. and Caldwell, R.L. (2009) Behaving in the dark: locomotor, chromatic, postural, and bioluminescent behaviors of the deep-sea squid Octopoteuthis deletron Young 1972. Biological Bulletin. Marine Biological Laboratory, Woods Hole 216, 7–22.CrossRefGoogle ScholarPubMed
Calow, P. (1987) Fact and theory—an overview. In Boyle, P.R. (ed.) Cepholopod life cycles. Volume 2. London: Academic Press, pp. 351–365.Google Scholar
Childress, J.J. (1995) Are there phyiological and biochemical adaptations of metabolism in deep-sea animals? Trends in Ecolology and Evolution 10, 30–36.CrossRefGoogle Scholar
Durward, R.D., Vessey, E., O'Dor, R.K. and Amaratunga, T. (1980) Reproduction in the squid Illex illecebrosus: first observations in captivity and implications for the life cycle. International Commission for the Northwest Atlantic Fisheries Selected Papers 6, 7–13.Google Scholar
Guerra, A., González, A.F., Rocha, F.J., Sagarminaga, R. and Cañadas, A. (2002) Planktonic egg masses of the diamond-shaped squid Thysanoteuthis rhombus in the eastern Atlantic and the Mediterranean Sea. Journal of Plankton Research 24, 333–338.CrossRefGoogle Scholar
Hanlon, R.T. and Messenger, J.B. (1996) Cephalopod behaviour. New York: Cambridge University Press.Google Scholar
Hayashi, S. (1989) Spawning behavior and embryonic development of the firefly squid, Watasenia scintillans. Bulletin of Toyama Prefectural Fisheries Experiment Institute 1, 1–14.Google Scholar
Hixon, R.F. (1983) Loligo opalescens. Cephalopod Life Cycles 1, 95–114.Google Scholar
Hoving, H.J.T., Laptikhovsky, V., Piatkowski, U. and Onsoy, B. (2008) Reproduction in Heteroteuthis dispar (Rüppell, 1844) (Mollusca: Cephalopoda): a sepiolid reproductive adaptation to an oceanic lifestyle. Marine Biology 154, 219–230.CrossRefGoogle Scholar
Hoving, H.J.T. and Lipinski, M.R. (2009) Female reproductive biology, and age of deep-sea squid Histioteuthis miranda from southern Africa. ICES Journal of Marine Science 66, 1868–1872.CrossRefGoogle Scholar
Hoving, H.J.T., Lipinski, M.R., Videler, J.J. and Bolstad, K.S.R. (2010) Sperm storage and mating in the deep-sea squid Taningia danae Joubin, 1931 (Oegopsida: Octopoteuthidae). Marine Biology 157, 393–400.CrossRefGoogle ScholarPubMed
Hoving, H.J.T., Roeleveld, M.A.C., Lipinski, M.R. and Malo, Y. (2004) Reproductive system of the giant squid Architeuthis in South African waters. Journal of Zoology, London 264, 153–169.CrossRefGoogle Scholar
Hoyle, W.E. (1885) Narrative of the voyage of the Challenger Expedition: the Cephalopoda. In Report on the voyage of the HMS Challenger (1873–1876), pp. 269–274.Google Scholar
Hunt, J.C. and Seibel, B.A. (2000) Life history of Gonatus onyx (Cephalopoda: Teuthoidea): ontogenetic changes in habitat, behavior and physiology. Marine Biology 136, 543–552.CrossRefGoogle Scholar
Hunt, J.C., Zeidberg, L.D., Hamner, W.M. and Robison, B.H. (2000) The behavior of Loligo opalescens (Mollusca: Cephalopoda) as observed by a remotely operated vehicle. Journal of the Marine Biological Association of the United Kingdom 80, 873–883.CrossRefGoogle Scholar
Hunter, J.R. and Macewicz, B.J. (1985) Measurement of spawning frequency in multiple spawning fishes. In Lasker, R. (ed.) An egg production method for spawning biomass of pelagic fish: application to the northern anchovy, Engraulis mordax. NOAA Technical Report NMFS 36, pp. 79–93.Google Scholar
Jackson, G.D. (1997) Age, growth and maturation of the deepwater squid Moroteuthis ingens (Cephalopoda: Onychoteuthidae) in New Zealand waters. Polar Biology 17, 268–274.CrossRefGoogle Scholar
Kaufman, M.R., Ikeda, Y., Patton, C., Van Dykhuizen, G. and Epel, D. (1998) Bacterial symbionts colonize the accessory nidamental gland of the squid Loligo opalescens via horizontal transmission. Biological Bulletin. Marine Biological Laboratory, Woods Hole 194, 36–43.CrossRefGoogle ScholarPubMed
Laptikhovsky, V.V. (1999) Fecundity and spawning in squid of families Enoploteuthidae and Ancistrocheiridae (Cephalopoda: Oegopsida). Scientia Marina 63, 1–7.CrossRefGoogle Scholar
Laptikhovsky, V.V., Arkhipkin, A.I. and Hoving, H.J.T. (2007) Reproductive biology in two species of deep-sea squids. Marine Biology 152, 981–990.CrossRefGoogle Scholar
Lindgren, A.R. and Daly, M. (2007) The impact of length-variable data and alignment criterion on the phylogeny of Decapodiformes (Mollusca: Cephalopoda). Cladistics 23, 464–476.CrossRefGoogle Scholar
Lu, C.C. and Williams, R. (1994) Contribution to the biology of squid in the Prydz Bay region, Antarctica. Antarctic Science 6, 223–229.CrossRefGoogle Scholar
Madan, J.J. and Wells, M.J. (1996) Why squid can breathe easy. Nature 380, 590.CrossRefGoogle Scholar
Melo, Y. and Sauer, W.H.H. (1998) Ovarian atresia in cephalopods. South African Journal of Marine Science 20, 143–151.CrossRefGoogle Scholar
Nesis, K.N. (1995) Mating, spawning and death in oceanic cephalopds: a review. Ruthenica 6, 23–64.Google Scholar
Nesis, K.N., Nigmatullin, Ch.M. and Nikitina, I.V. (1998) Spent females of deepwater squid Galiteuthis glacialis under the ice at the surface of the Weddell Sea (Antarctic). Journal of Zoology, London 244, 185–200.CrossRefGoogle Scholar
O'Shea, S., Bolstad, K.S. and Ritchie, P.A. (2004) First records of egg masses of Nototodarus gouldi McCoy, 1888 (Mollusca: Cephalopoda: Ommastrephidae), with comments on egg-mass susceptibility to damage by fisheries trawl. New Zealand Journal of Zoology 31, 161–166.CrossRefGoogle Scholar
Okutani, T., Nakamura, I. and Seki, K. (1995) An unusual egg-brooding behavior of an oceanic squid in the Okhotsk Sea. Venus 54, 237–239.Google Scholar
Robison, B.H., Reisenbichler, K.R., Hunt, J.C. and Haddock, S.H.D. (2003) Light production by the arm tips of the deep-sea cephalopod Vampyroteuthis infernalis. Biological Bulletin . Marine Biological Laboratory, Woods Hole 205, 102–109.CrossRefGoogle Scholar
Robison, B.H., Sherlock, R.E. and Reisenbicher, K.R. (2010) The bathypelagic community of Monterey Canyon. Deep-Sea Research II 57, 1551–1556.CrossRefGoogle Scholar
Rocha, F., Guerra, A. and Gonzalez, A.F. (2001) A review of reproductive strategies in cephalopods. Biological Reviews 76, 291–304.CrossRefGoogle ScholarPubMed
Roper, C.F.E. (1968) Preliminary descriptions of two new species of the bathypelagic squid Bathyteuthis (Cephalopoda: Oegopsida). Proceedings of the Biological Society of Washington 81, 261–272.Google Scholar
Roper, C.F.E. (1969) Systematics and zoogeography of the worldwide bathypelagic squid Bathyteuthis (Cephalopoda: Oegopsida). Bulletin of the United States National Museum 291, 1–210.CrossRefGoogle Scholar
Sato, N., Kasugai, T., Ikeda, Y. and Munehara, H. (2010) Structure of the seminal receptacle and sperm storage in the Japanese pygmy squid. Journal of Zoology, London 282, 151–156.CrossRefGoogle Scholar
Seibel, B.A., Goffredi, S.K., Thuesen, E.V., Childress, J.J. and Robison, B.H. (2004) Ammonium content and buoyancy in midwater cephalopods. Journal of Experimental Marine Biology and Ecology 313, 375–387.CrossRefGoogle Scholar
Seibel, B.A., Hochberg, F.G. and Carlini, D.B. (2000) Life history of Gonatus onyx (Cephalopoda: Teuthoidea): deep-sea spawning and post-spawning egg care. Marine Biology 137, 519–526.CrossRefGoogle Scholar
Seibel, B.A., Robison, B.H. and Haddock, S.H.D. (2005) Post-spawning egg care by a squid. Nature 438, 929.CrossRefGoogle ScholarPubMed
Staaf, D.S., Camarillo-Coop, S., Haddock, S.H.D., Nyack, A., Payne, J., Salinas-Zavala, C., Seibel, B.A., Trueblood, L., Widmer, C. and Gilly, W.F. (2008) Natural egg mass deposition by the Humboldt squid (Dosidicus gigas) in the Gulf of California and characteristics of hatchlings and paralarvae. Journal of the Marine Biological Association of the United Kingdom 88, 759–770.CrossRefGoogle Scholar
Vecchione, M., Young, R.E. and Piatkowski, U. (2010) Cephalopods of the northern Mid-Atlantic Ridge. Marine Biology Research 6, 25–52.CrossRefGoogle Scholar
Voss, G.L. (1956) A review of the cephalopods of the Gulf of Mexico. Bulletin of Marine Science of the Gulf and Caribbean 6, 85–178.Google Scholar
Watanabe, K., Sakurai, Y., Segawa, S. and Okutani, T. (1996) Development of the ommastrephid squid Todarodes pacificus, from fertilized egg to the rhynchoteuthion paralarva. American Malacological Bulletin 13, 73–88.Google Scholar
Young, R.E. (1972a) The systematics and areal distribution of pelagic cephalopods from the seas off Southern California. Smithsonian Contributions to Zoology 97, 1–159.CrossRefGoogle Scholar
Young, R.E. (1972b) Brooding in a bathypelagic octopus. Pacific Science 26, 400–404.Google Scholar
Young, R.E. (1995) Aspects of the natural history of pelagic cephalopods of the Hawaiian mesopelagic-boundary region. Pacific Science 49, 143–155.Google Scholar
Young, R.E. (2008a) Bolitaena pygmaea (Verrill 1884). Bolitaena Steenstrup 1859. Version 28 April 2008. The Tree of Life Web Project. http://tolweb.org, 2011.Google Scholar
Young, R.E. (2008b) Japetella diaphana Hoyle 1885. Version 28 April 2008 (under construction). The Tree of Life Web Project. http://tolweb.org, 2011.Google Scholar
Young, R.E., Mangold, K. and Vecchione, M. (2010) Vitreledonellidae Robson, 1932. Vitreledonella richardi Joubin, 1918. Version 4 March 2010 (under construction). Tree of Life Web Project. http://tolweb.org, 2011.Google Scholar
Young, R.E. and Vecchione, M. (2008) Bathyteuthoidea Vecchione, Young and Sweeney, 2004. Version 21 October 2008 (under construction). The Tree of Life Web Project. http://tolweb.org, 2011.Google Scholar
Zeidberg, L.D. (2004) Allometry measurements can determine the size and swimming speeds of juvenile and adult Loligo opalescens (Cephalopoda: Myopsida) squid from in situ video. Journal of Experimental Biology 207, 4195–4203.CrossRefGoogle ScholarPubMed

Bush et al. supplementary movie

Supplemental Video 1. Female Bathyteuthis berryi maintaining neutral bouyancy and undulating the fins while brooding a sheet of approximately 360 embryos at 1350 m depth.

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