Hostname: page-component-586b7cd67f-2brh9 Total loading time: 0 Render date: 2024-11-28T00:17:39.278Z Has data issue: false hasContentIssue false
  • English
  • Français

Natural egg mass deposition by the Humboldt squid (Dosidicus gigas) in the Gulf of California and characteristics of hatchlings and paralarvae

Published online by Cambridge University Press:  25 June 2008

Danna J. Staaf ,
Susana Camarillo-Coop ,
Steven H.D. Haddock ,
Al C. Nyack ,
John Payne ,
Cesar A. Salinas-Zavala ,
Brad A. Seibel ,
Lloyd Trueblood ,
Chad Widmer  and
William F. Gilly
Danna J. Staaf*
Affiliation:
Hopkins Marine Station of Stanford University, Oceanview Boulevard, Pacific Grove, CA 93950USA
Susana Camarillo-Coop
Affiliation:
Centro de Investigaciones Biológicas del Noroeste, SC Unidad Sonora. Mar Bermejo # 195 Col. Playa Palo de Santa Rita. La Paz, B.C.S.Mexico
Steven H.D. Haddock
Affiliation:
Monterey Bay Aquarium Research Institute, 7700 Sandholdt Rd., Moss Landing, CA 95039USA
Al C. Nyack
Affiliation:
Department of Biological Sciences, University of Rhode Island, 100 Flagg Road, Kingston, RI 02881USA
John Payne
Affiliation:
POST project, 13639 SW 224th Street, Vashon, WA 98070USA
Cesar A. Salinas-Zavala
Affiliation:
Centro de Investigaciones Biológicas del Noroeste, SC Unidad Sonora. Mar Bermejo # 195 Col. Playa Palo de Santa Rita. La Paz, B.C.S.Mexico
Brad A. Seibel
Affiliation:
Department of Biological Sciences, University of Rhode Island, 100 Flagg Road, Kingston, RI 02881USA
Lloyd Trueblood
Affiliation:
Department of Biological Sciences, University of Rhode Island, 100 Flagg Road, Kingston, RI 02881USA
Chad Widmer
Affiliation:
Monterey Bay Aquarium, 886 Cannery Row, Monterey, CA 93940USA
William F. Gilly
Affiliation:
Hopkins Marine Station of Stanford University, Oceanview Boulevard, Pacific Grove, CA 93950USA
*
Correspondence should be addressed to: Danna J. StaafHopkins Marine Station of Stanford UniversityOceanview Boulevard, Pacific Grove, CA 93950USA email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The jumbo or Humboldt squid, Dosidicus gigas, is an important fisheries resource and a significant participant in regional ecologies as both predator and prey. It is the largest species in the oceanic squid family Ommastrephidae and has the largest known potential fecundity of any cephalopod, yet little is understood about its reproductive biology. We report the first discovery of a naturally deposited egg mass of Dosidicus gigas, as well as the first spawning of eggs in captivity. The egg mass was found in warm water (25–27°C) at a depth of 16 m and was far larger than the egg masses of any squid species previously reported. Eggs were embedded in a watery, gelatinous matrix and were individually surrounded by a unique envelope external to the chorion. This envelope was present in both wild and captive-spawned egg masses, but it was not present in artificially fertilized eggs. The wild egg mass appeared to be resistant to microbial infection, unlike the incomplete and damaged egg masses spawned in captivity, suggesting that the intact egg mass protects the eggs within. Chorion expansion was also more extensive in the wild egg mass. Hatchling behaviours included proboscis extension, chromatophore activity, and a range of swimming speeds that may allow them to exercise some control over their distribution in the wild.

Keywords

Humboldt squidjumbo squidDosidicus gigasommastrephidegg massrhynchoteuthion paralarvae
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 88 , Issue 4 , August 2008 , pp. 759 - 770
Copyright
Copyright © Marine Biological Association of the United Kingdom 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abitía-Cárdenas, L., Muhlia-Melo, A., Cruz-Escalona, V. and Galván-Magaña, F. (2002) Trophic dynamics and seasonal energetics of striped marlin Tetrapturus audax in the southern Gulf of California, Mexico. Fisheries Research 57, 287–295.CrossRefGoogle Scholar
Arnold, J.M. and O'Dor, R.K. (1990) In vitro fertilization and embryonic development of oceanic squid. Journal of Cephalopod Biology 1, 21–36.Google Scholar
Atkinson, B. (1973) Squid nidamental gland extract: isolation of a factor inhibiting ciliary activity. Journal of Experimental Zoology 184, 335–340.CrossRefGoogle ScholarPubMed
Balch, N., O'Dor, R.K. and Helm, P. (1985) Laboratory rearing of rhynchoteuthions of the ommastrephid squid Illex illecebrosus (Mollusca: Cephalopoda). Vie et Milieu 35, 243–246.Google Scholar
Bazzino, G., Salinas-Zavala, C. and Markaida, U. (2007) Variability in the population structure of jumbo squid (Dosidicus gigas) in Santa Rosalía, central Gulf of California. Ciencias Marinas 33, 173–186.CrossRefGoogle Scholar
Biggs, J. and Epel, D. (1991) Egg capsule sheath of Loligo opalescens Berry: structure and association with bacteria. Journal of Experimental Zoology 259, 263–267.CrossRefGoogle Scholar
Boletzky, S.V. (1994) Embryonic development of cephalopods at low temperatures. Antarctic Science 6, 139–142.CrossRefGoogle Scholar
Boletzky, S.V. (2003) Biology of early life stages in cephalopod molluscs. Advances in Marine Biology 44, 143–293.CrossRefGoogle Scholar
Bower, J.R. and Sakurai, Y. (1996) Laboratory observations on Todarodes pacificus (Cephalopoda: Ommastrephidae) egg masses. American Malacological Bulletin 13, 65–71.Google Scholar
Boyle, P.R. (1991) The UFAW Handbook on the care and management of cephalopods in the laboratory. Potters Bar, UKUniversities Federation for Animal Welfare, 64 p.Google Scholar
Brunetti, N.E. (1990) Description of rhynchoteuthion larvae of Illex argentinus from the summer spawning subpopulation. Journal of Plankton Research 12, 1045–1057.CrossRefGoogle Scholar
Chen, D.S., Dykhuizen, G.V., Hodge, J. and Gilly, W.F. (1996) Ontogeny of copepod predation in juvenile squid (Loligo opalescens). Biological Bulletin. Marine Biological Laboratory, Woods Hole 190, 69–71.CrossRefGoogle ScholarPubMed
Clarke, M.R. (1966) A review of the systematics and ecology of oceanic squids. Advances in Marine Biology 4, 91–300.CrossRefGoogle Scholar
Cosgrove, J.A. (2005) The first specimens of Humboldt squid in British Columbia. PICES Press 13, 30–31.Google 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
Field, J.C., Baltz, K., Phillips, A.J. and Walker, W.A. (2007) Range expansion and trophic interactions of the jumbo squid, Dosidicus gigas, in the California Current. CalCOFI Reports 48, 131–144.Google Scholar
Gilbert, D.L., Adelman, W.J. and Arnold, J.M. (eds) (1990) Squid as experimental animals. New York: Plenum Press, 516 pp.CrossRefGoogle Scholar
Gilly, W.F., Elliger, C.A., Salinas-Zavala, C.A., Camarillo-Coop, S., Bazzino, G. and Beman, M. (2006a) Spawning by jumbo squid Dosidicus gigas in the San Pedro Mártir Basin, Gulf of California, Mexico. Marine Ecology Progress Series 313, 125–133.CrossRefGoogle Scholar
Gilly, W.F. and Markaida, U. (2007) Perspectives on Dosidicus gigas in a changing world. In Olson, R.W. and Young, J. (eds) GLOBEC Report: The ecological role of squids in pelagic ecosystems, CLIOTOP workshop, 16–17 November, 2006, Honolulu, HI, pp. 81–90.Google Scholar
Gilly, W.F., Markaida, U., Baxter, C.H., Block, B.A., Boustany, A., Zeidberg, L., Reisenbichler, K., Robison, B., Bazzino, G. and Salinas-Zavala, C. (2006b) Vertical and horizontal migrations by the jumbo squid Dosidicus gigas revealed by electronic tagging. Marine Ecology Progress Series 324, 1–17.CrossRefGoogle Scholar
Guerra, A. and Rocha, F. (1997) On a floating egg mass of the diamond shaped squid Thysanoteuthis rhombus (Cephalopoda: Thysanoteuthidae) in the western Mediterranean. Iberus 15, 125–130.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
Haddock, S.H.D. and Heine, J.N. (2005) Scientific blue-water diving. La Jolla: California Sea Grant, 49 pp.Google Scholar
Harman, R.F., Young, R.E., Mangold, K.M., Suzuki, T. and Hixon, R.F. (1989) Evidence of multiple spawning in the tropical oceanic squid Sthenoteuthis oualaniensis (Teuthoidea: Ommastrephidae). Marine Biology 101, 513–519.CrossRefGoogle Scholar
Hurley, A.C. (1976) Feeding behavior, food consumption, growth, and respiration of the squid Loligo opalescens raised in the laboratory. Fishery Bulletin 74, 176–l82.Google Scholar
Ikeda, Y., Sakurai, Y. and Shimazaki, K. (1993a) Maturation process of the Japanese common squid Todarodes pacificus in captivity. In Okutani, T., O'Dor, R.K. and Kubodera, T. (eds) Recent advances in cephalopod fisheries biology. Tokyo: Tokai University Press, pp. 179–187.Google Scholar
Ikeda, Y., Sakurai, Y. and Shimazaki, K. (1993b) Fertilizing capacity of squid (Todarodes pacificus) spermatozoa collected from various sperm storage sites, with special reference to the role of gelatinous substance from oviducal gland in fertilization and embryonic development. Invertebrate Reproduction and Development 23, 39–44.CrossRefGoogle Scholar
Klimley, A.P., Caberera-Mancilla, I. and Castillo-Geniz, J.L. (1993) Horizontal and vertical movements of the scalloped hammerhead shark, Sphyrna lewini, in the southern Gulf of California, Mexico. Ciencias Marinas 19, 95–115.CrossRefGoogle Scholar
Laptikhovsky, V.V. (1991) Mathematical model for the study of duration of embryogenesis in cephalopods. Biologicheskiye Nauki 3, 37–48 [In Russian, English summary.]Google Scholar
Laptikhovsky, V.V. (1999) Improved mathematical model to study the duration of embryogenesis in cephalopod molluscs. Ruthenica 9, 141–146.Google Scholar
Laptikhovsky, V.V. and Murzov, S.A. (1990) A catch of the epipelagic egg mass of the squid Stenoteuthis pteropus in Eastern Tropical Atlantic. Biologiya Morya 3, 62–63 [In Russian, English summary.]Google Scholar
Laptikhovsky, V.V. and Nigmatullin, C.M. (1993) Egg size, fecundity, and spawning in females of the genus Illex (Cephalopoda: Ommastrephidae). ICES Journal of Marine Science 50, 393–403.CrossRefGoogle Scholar
Lipiński, M.R. and Underhill, L.G. (1995) Sexual maturation in squid: quantum or continuum? South African Journal of Marine Science 15, 207–223.CrossRefGoogle Scholar
Markaida, U. and Sosa-Nishizaki, O. (2003) Food and feeding habits of jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae) from the Gulf of California, Mexico. Journal of the Marine Biological Association of the UK 83, 507–522.CrossRefGoogle Scholar
Miyahara, K., Fukui, K., Ota, T. and Minami, T. (2006) Laboratory observations on the early life stages of the diamond squid Thysanoteuthis rhombus. Journal of Molluscan Studies 72, 199–205.CrossRefGoogle Scholar
Miyanaga, S. and Sakurai, Y. (2006) Effect of temperature on the swimming behavior of Japanese common squid (Todarodes pacificus) paralarvae. In Proceedings of the Cephalopod International Advisory Council Symposium 2006, Cephalopod Life Cycles, 6–10 February 2006, Hotel Grand Chancellor, Hobart, Tasmania, p. 89.Google Scholar
Moltschaniwskyj, N.A., Hall, K., Lipinski, M., Marian, J.E.A.R., Nishiguchi, M., Sakai, M., Shulman, D.J., Sinclair, B., Sinn, D.L., Staudinger, M., Van Gelderen, R., Villanueva, R. and Warnke, K. (2007) Ethical considerations when using cephalopods as experimental animals. Reviews in Fish Biology and Fisheries 17, 455–476.CrossRefGoogle Scholar
Nigmatullin, C.M. and Arkhipkin, A.I. (1998) A review of the biology of the diamondback squid, Thysanoteuthis rhombus (Oegopsida: Thysanoteuthidae). In Okutani, T. (ed.) Large pelagic squids. Tokyo: Japan Marine Fishery Resource Research Center, p. 155–181.Google Scholar
Nigmatullin, C.M. and Laptikhovsky, V.V. (1994) Reproductive strategies in the squids of the family Ommastrephidae (preliminary report). Ruthenica 4, 79–82.Google Scholar
Nigmatullin, C.M. and Markaida, U. (2002) Oocyte development, egg size, and fecundity of the large size females of jumbo squid Dosidicus gigas. Second International Symposium on Pacific Squid (November 25–29, 2002), La Paz, Baja California Sur, Mexico. Abstracts book, IPN–CICIMAR, La Paz, p. 9.Google Scholar
Nigmatullin, C.M., Arkhipkin, A.I. and Sabirov, R.M. (1995) Age, growth and reproductive biology of diamond-shaped squid Thysanoteuthis rhombus (Oegopsida: Thysanoteuthidae). Marine Ecology Progress Series 124, 73–87.CrossRefGoogle Scholar
Nigmatullin, C.M., Laptikhovsky, V.V., Mokrin, N., Sabirov, R. and Markaida, U. (1999) On life history traits of the jumbo squid Dosidicus gigas. In Tresierra Aguilar, A.E. and Culquichicon, Z.G. (eds) VIII Congreso Latinoamericano sobre Ciencias del Mar (COLACMAR), Trujillo, Peru, 17–21 October 1999. Libro de Resúmenes Ampliados, Tomo I, p. 291.Google Scholar
Nigmatullin, C.M., Nesis, K.N. and Arkhipkin, A.I. (2001) A review of the biology of the jumbo squid Dosidicus gigas (Cephalopoda: Ommastrephidae). Fisheries Research 54, 9–19.CrossRefGoogle Scholar
O'Dor, R.K. and Balch, N. (1985) Properties of Illex illecebrosus egg masses potentially influencing larval oceanographic distribution. Northwest Atlantic Fisheries Organization Scientific Council Studies 9, 69–76.Google Scholar
O'Dor, R.K., Balch, N. and Amaratunga, T. (1982a) Laboratory observations of midwater spawning by Illex illecebrosus. Northwest Atlantic Fisheries Organization Scientific Council Studies 6, 5–8.Google Scholar
O'Dor, R.K., Balch, N., Foy, E.A., Hirtle, R.W.M., Johnston, D.A. and Amaratunga, T. (1982b) Embryonic development of the squid, Illex illecebrosus, and effect of temperature on developmental rates. Journal of Northwest Atlantic Fisheries Science 3, 41–45.CrossRefGoogle Scholar
O'Dor, R.K., Helm, P. and Balch, N. (1985) Can rhynchoteuthions suspension feed? (Mollusca: Cephalopoda). Vie et Milieu 35, 267–271.Google 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
Piatkowski, U., Welsch, W. and Röpke, A. (1993) Distribution patterns of the early life stages of pelagic cephalopods in three geographically different regions of the Arabian Sea. In Okutani, T., O'Dor, R.K. and Kubodera, T. (eds) Recent advances in cephalopod fisheries biology. Tokyo: Tokai University Press, pp. 179–187.Google Scholar
Preuss, T., Lebaric, Z.N. and Gilly, W.F. (1997) Post-hatching development of circular mantle muscles in the squid Loligo opalescens. Biological Bulletin. Marine Biological Laboratory, Woods Hole 192, 375–387.CrossRefGoogle ScholarPubMed
Rocha, F., Guerra, A. and González, A.F. (2001) A review of reproductive strategies in cephalopods. Biological Reviews 76, 291–304.CrossRefGoogle ScholarPubMed
Rosas-Aloya, J., Hernández-Herrera, A., Galván-Magaña, F., Abitía-Cárdenas, L. and Muhlia-Melo, A. (2002) Diet composition of sailfish (Istiophorus platypterus) from the southern Gulf of California, Mexico. Fisheries Research 57, 185–195.CrossRefGoogle Scholar
Ruiz-Cooley, R.I., Gendron, D., Aguíñiga, S., Mesnick, S. and Carriquiry, J.D. (2004) Trophic relationships between sperm whales and jumbo squid using stable isotopes of C and N. Marine Ecology Progress Series 277, 275–283.CrossRefGoogle Scholar
Sabirov, R.M., Arkhipkin, A.I., Tsygankov, V.Y. and Schetinnikov, A.S. (1987) Egg laying and embryonal development of diamond-shaped squid, Thysanoteuthis rhombus (Oegopsida. Thysanoteuthidae). Zoologicheskii Zhurnal 66, 1155–1163.Google Scholar
Sakurai, Y. and Ikeda, Y. (1994) Laboratory rearing methods of Todarodes pacificus for the ecological study of life cycle. Report of 1992 Annual Meeting on Resources and Fisheries of Squids. National Institute for Far Sea Research, pp. 51–69. [In Japanese, with English title and abstract.]Google Scholar
Sakurai, Y., Young, R.E., Hirota, J. and Mangold, K. (1995) Artificial fertilization and development through hatching in the oceanic squids Ommastrephes bartramii and Sthenoteuthis oulaniensis (Cephalopod: Ommastrephidae). Veliger 38, 185–191.Google Scholar
Seibel, B.A. (2007) On the depth and scale of metabolic rate variation: scaling of oxygen consumption and enzymatic activity in the Class Cephalopoda (Mollusca). Journal of Experimental Biology 210, 1–11.CrossRefGoogle ScholarPubMed
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
Shea, E.K. (2005) Ontogeny of the fused tentacles in three species of ommastrephid squids (Cephalopoda, Ommastrephidae). Invertebrate Biology 124, 25–38.CrossRefGoogle Scholar
Shigeno, S., Kidokoro, H., Goto, T., Tsuchiya, K. and Segawa, S. (2001) Early ontogeny of the Japanese common squid Todarodes pacificus (Cephalopoda, Ommastrephidae) with special reference to its characteristic morphology and ecological significance. Zoological Science 18, 1011–1026.CrossRefGoogle Scholar
Strathmann, R.R. and Strathmann, M.F. (1995) Oxygen supply and limits on aggregation of embryos. Journal of the Marine Biological Association of the UK 75, 413–428.CrossRefGoogle Scholar
Vidal, E.A.G. and Haimovici, M. (1998) Feeding and the possible role of the proboscis and mucus cover in the ingestion of microorganisms by rhynchoteuthion paralarvae (Cephalopod: Ommastrephidae). Bulletin of Marine Science 63, 305–316.Google Scholar
Vecchione, M. (1999) Extraordinary abundance of squid paralarvae in the tropical eastern Pacific Ocean during El Niño of 1987. Fishery Bulletin 97, 1025–1030.Google Scholar
Watanabe, K., Sakurai, Y., Segawa, S. and Okutani, T. (1996) Development of the ommastrephid squid Todarodes pacificus, from fertilized egg through to rhynchoteuthion paralarva. American Malacological Bulletin 13, 73–88.Google Scholar
Watanabe, K., Ando, K., Tsuchiya, K. and Segawa, S. (1998) Late embryos and paralarvae of diamondback squid Thysanoteuthis rhombus Troschel, 1857. Venus, 57, 291–301.Google Scholar
Wing, B.L. (2006) Unusual invertebrates and fish observed in the Gulf of Alaska, 2004–2005. PICES Press 14, 26–28.Google Scholar
Yatsu, A., Tafur, R. and Maravi, C. (1999) Embryos and rhynchoteuthion paralarvae of the jumbo flying squid Dosidicus gigas (Cephalopoda) obtained through artificial fertilization from Peruvian waters. Fisheries Science 65, 904.CrossRefGoogle Scholar
Young, R.E., Harman, R.F. and Mangold, K.M. (1985a) The common occurrence of oegopsid squid eggs in near-surface oceanic waters. Pacific Science 39, 359–366.Google Scholar
Young, R.E., Harman, R.F. and Mangold, K.M. (1985b) The eggs and larvae of Brachioteuthis sp. (Cephalopoda: Teuthoidea) from Hawaiian waters. Vie et Milieu 35, 203–209.Google Scholar
Zeidberg, L.D. and Robison, B.H. (2007) Invasive range expansion by the Humboldt squid, Dosidicus gigas, in the eastern North Pacific. Proceedings of the National Academy of Sciences 104, 12948–12950.CrossRefGoogle ScholarPubMed