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Advances in defining the life histories of myopsid squid

George D. Jackson
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Institute of Antarctic and Southern Ocean Studies, University of Tasmania, Private Bag 77, Hobart, Tasmania 7001, Australia. Email: george.jackson@utas.edu.au

Marine and Freshwater Research 55(4) 357-365 https://doi.org/10.1071/MF03152
Submitted: 26 September 2003  Accepted: 19 March 2004   Published: 22 June 2004

Abstract

Recent years have seen the emergence of extensive studies of myopsid squid growth of the family Loliginidae. This has greatly advanced our understanding of their life histories. Growth data have accumulated from both statolith-based field studies and culture work. Validation studies on loliginids continue to support that statolith increments are laid down daily. Ageing work has also revealed that short lifespans are typical, with nine of the 21 species studied having lifespans <200 days, eight species with lifespans between 200 days and about 1 year and only three species with lifespans >1 year. While growth is continuous and non-asymptotic, the marked plasticity in size-at-age has hindered the development of a general model to describe squid growth. Many loliginids are multiple spawners that continue to feed while growing and reproducing, although there has been some documented loss of conditon in mature individuals. An exception is Loligo opalescens, which has a terminal spawning strategy with a marked loss of condition and post-spawning mortality. Quantification of the cost of living and the energetics of loliginids are likely to be best achieved by combining field and culture studies on a species such as the Indo-Pacific squid Sepioteuthis lessoniana.

Extra keywords: growth rates, Loliginidae, statolith age, validation.


Acknowledgments

I would like to thank the many participants of the 2003 Cephalopod International Advisory Council growth workshop who provided an interesting forum to discuss cephalopod growth. Thanks to two anonymous reviewers for comments on an earlier draft of this manuscript, and to C. Jackson for preparing tables and assisting with earlier drafts.


References

Alford, R. A. , and Jackson, G. D. (1993). Do cephalopods and larvae of other taxa grow asymptotically? American Naturalist 141, 717–728.
Crossref | GoogleScholarGoogle Scholar |

Arkhipkin, A. I. (1993). Statolith microstructure and maximum age of Loligo gahi (Myopsida: Loliginidae) on the Patagonian shelf. Journal of Marine Biological Association of the United Kingdom 73, 979–982.


Arkhipkin, A. (1995). Age, growth and maturation of the European squid Loligo vulgaris (Myopsida, Loliginidae) on the West Saharan Shelf. Journal of the Marine Biological Association of the United Kingdom 75, 593–604.


Arkhipkin, A. (2004). Diversity in growth and longevity in short-lived animals: squid of the suborder Oegopsina. Marine and Freshwater Research 55, 341–351.


Arkhipkin, A. I. , and Nekludova, N. (1993). Age, growth and maturation of the loliginid squids Alloteuthis africana and A. subulata on the West Africa Shelf. Journal of the Marine Biological Association of the United Kingdom 73, 949–961.


Balgos, M. C. , and Pauly, D. (1998). Age and growth of the squid Sepioteuthis lessoniana in NW Luzon, Philippines. South African Journal of Marine Science 20, 449–452.


Bettencourt, V. , Coelho, L. , Andrade, J. P. , and Guerra, A. (1996). Age and growth of the squid Loligo vulgaris off the south coast of Portugal, using statolith analysis. The Journal of Molluscan Studies 62, 359–366.


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


Brodziak, J. K. T. , and Macy, W. K. (1996). Growth of long-finned squid, Loligo pealeii, in the northwest Atlantic. Fishery Bulletin 94, 212–236.


Butler, J. , Fuller, D. , and Yaremko, M. (1999). Age and growth of market squid (Loligo opalescens) off California during 1998. CalCOFI Reports 40, 191–195.


Chotiyaputta, C. (1997). Distribution, abundance, reproductive biology, age and growth of Loligo chinensis and Loligo duvauceli in the western Gulf of Thailand. In ‘Developing and Sustaining World Fisheries Resources, the State of Science and Management’. (Eds. D. A. Hancock, D. C. Smith, A. Grant and J. P. Beumer)  pp. 614–619. (CSIRO: Melbourne, Australia.)

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


Dimmlich, W. F. , and Hoedt, F. E. (1998). Age and growth of the myopsid squid Loliolus noctiluca in Western Port, Victoria, determined from statolith microstructure analysis. Journal of the Marine Biological Association of the United Kingdom 78, 577–586.


Durholtz, M. D. , Lipinski, M. R. , and Field, J. G. (2002). Laboratory validation of periodicity of incrementation in statoliths of the South African chokka squid Loligo vulgaris reynaudii (d’Orbigny, 1845): a reevaluation. Journal of Experimental Marine Biology and Ecology 279, 41–59.
Crossref | GoogleScholarGoogle Scholar |

Fields, W. G. (1965). The structure, development, food relations, reproduction and life history of the squid, Loligo opalescens Berry. California Department of Fish and Game Fishery Bulletin 131, 1–108.


Forsythe, J. W. (1993). A working hypothesis of how seasonal temperature change may impact the field growth of young cephalopods. In ‘Recent Advances in Cephalopod Fisheries Biology’. (Eds. T. Okutani, R. K. O’Dor and T. Kubodera)  pp. 133–143. (Tokai University Press: Tokyo, Japan.)

Forsythe, J. W. (2004). Accounting for the effect of temperature on squid growth in nature: from hypothesis to practice. Marine and Freshwater Research 55, 331–339.


Forsythe, J. W. , and Hanlon, R. T. (1989). Growth of the eastern Atlantic Squid, Loligo forbesi Steenstrup (Mollusca: Cephalopoda). Aquaculture and Fisheries Management 20, 1–14.


Forsythe, J. W. , Walsh, L. S. , Turk, P. E. , and Lee, P. G. (2001). Impact of temperature on juvenile growth and age at first egg-laying of the Pacific reef squid Sepioteuthis lessoniana reared in captivity. Marine Biology 138, 103–112.
Crossref | GoogleScholarGoogle Scholar |

González, A. F. , Macy, W. K. , and Guerra, A. (1998). Validation of a semi-automatic image analysis system to age squids and its application to age Illex coindetii statoliths. ICES Journal of Marine Science 55, 535–544.
Crossref | GoogleScholarGoogle Scholar |

González, A. F. , Dawe, E. , Beck, P. , and Perez, J. (2000). Bias associated with statolith-based methodologies for ageing squid: a comparative study on Illex illecebrosus (Cephalopoda: Ommastrephidae). Journal of Experimental Marine Biology and Ecology 244, 161–180.
Crossref | GoogleScholarGoogle Scholar |

Grist, E. P. M. , and des Clers, (1998). How seasonal temperature variations may influence the structure of annual squid populations. IMA Journal of Mathematics Applied in Medicine and Biology 15, 187.


Grist, E. P. M. , and des Clers, (1999). Seasonal and genotypic influences on life cycle synchronisation: further insights from annual squid. Ecological Modelling 115, 149.


Grist, E. P. M. , and Jackson, G. D. (2004). Energy balance as a determinant of two-phase growth in cephalopods. Marine and Freshwater Research 55, 395–401.


Hatfield, E. M. C. (1991). Post-recruit of the Patagonian squid Loligo gahi (D’Orbigny). Bulletin of Marine Science 49, 349–361.


Hatfield, E. (2000). Do some like it hot? Temperature as a possible determinant of variability in the growth of the Patagonian squid, Loligo gahi (Cephalopoda: Loliginidae). Fisheries Research 47, 27–40.
Crossref | GoogleScholarGoogle Scholar |

Hatfield, E. M. C. , and Cadrin, S. X. (2002). Geographic and temporal patterns in size and maturity of the longfin inshore squid (Loligo pealeii) off the northeastern United States. Fishery Bulletin 100, 200–213.


Hatfield, E. M. C. , Hanlon, R. T. , Forsythe, J. W. , and Grist, E. P. M. (2001). Laboratory testing of a growth hypothesis for juvenile squid Loligo pealeii (Cephalopoda: Loliginidae). Canadian Journal of Fisheries and Aquatic Sciences 58, 845–857.
Crossref | GoogleScholarGoogle Scholar |

Herke, S. W. , and Foltz, D. W. (2002). Phylogeography of two squid (Loligo pealei and L. plei) in the Gulf of Mexico and northwestern Atlantic Ocean. Marine Biology 140, 103–115.
Crossref | GoogleScholarGoogle Scholar |

Hixon, R. F. , and Villoch, M. R. (1984). Growth rings in the statoliths of young laboratory cultured squids (Loligo opalescens). American Malacological Bulletin 2, 93.


Ho, J. D. , Moltschaniwskyj, N. A. , and Carter, C. G. (2004). The effect of variability in growth on somatic condition and reproductive status in the southern calamary Sepioteuthis australis. Marine and Freshwater Research 55, 423–428.


Izuka, T. , Segawa, S. , Okutani, T. , and Numachi, K. (1994). Evidence on the existence of three species in the oval squid Sepioteuthis lessoniana complex in Ishigaki Island, Okinawa, southwestern Japan, by isozyme analyses. Venus 53, 217–228.


Izuka, T. , Segawa, S. , and Okutani, T. (1996). Biochemical study of the population heterogeneity and distribution of the oval squid Sepioteuthis lessoniana complex in southwestern Japan. American Malacological Bulletin 12, 129–135.


Jackson, G. D. (1990). Age and growth of the tropical nearshore Loliginid squid Sepioteuthis lessoniana determined from statolith growth-ring analysis. Fishery Bulletin 88, 113–118.


Jackson, G. D. (1990). The use of tetracycline staining techniques to determine statolith growth ring periodicity in the tropical loliginid squids Loliolus noctiluca and Loligo chinensis.  The Veliger 33, 395–399.


Jackson, G. D. (1993). Seasonal variation in reproductive investment in the tropical loliginid squid Loligo chinensis and the small tropical sepioid Idiosepius pygmaeus.  Fishery Bulletin 91, 260–270.


Jackson, G. D. (1994). Application and future potential of statolith increment analysis in squids and sepioids. Canadian Journal of Fisheries and Aquatic Sciences 51, 2612–2625.


Jackson, G. D. (1994). Statolith age estimates of the loliginid squid Loligo opalescens (Mollusca: Cephalopoda), corroboration with culture data. Bulletin of Marine Science 54, 554–557.


Jackson, G. D. (1998). Research into the life history of Loligo opalescens: where to from here? CalCOFI Reports 39, 101–107.


Jackson, G. D. , and Choat, J. H. (1992). Growth in tropical cephalopods: an analysis based on statolith microstructure. Canadian Journal of Fisheries and Aquatic Sciences 49, 218–228.


Jackson, G. D. , and Forsythe, J. W. (2002). Statolith age validation and growth of Loligo plei (Cephalopoda: Loliginidae) in the north-west Gulf of Mexico during spring/summer. Journal of Marine Biological Association of the United Kingdom 82, 677–678.
Crossref | GoogleScholarGoogle Scholar |

Jackson, G. D. , and Domeier, M. L. (2003). The effects of an extraordinary El Niño/ La Niña event on the size and growth of the squid Loligo opalescens off Southern California. Marine Biology 142, 925–935.


Jackson, G. D. , and Moltschaniwskyj, N. A. (1999). Analysis of precision in statolith derived age estimates of the tropical squid Photololigo (Cephalopoda: Loliginidae). ICES Journal of Marine Science 56, 221–227.
Crossref | GoogleScholarGoogle Scholar |

Jackson, G. D. , and Moltschaniwskyj, N. A. (2001). Temporal variation in growth rates and reproductive parameters in the small near-shore tropical squid, Loliolus noctiluca; is cooler better? Marine Ecology Progress Series 218, 167–177.


Jackson, G. D. , and Moltschaniwskyj, N. A. (2001). The influence of ration level on growth and statolith increment width of the tropical squid Sepioteuthis lessoniana (Cephalopoda: Loliginidae): an experimental approach. Marine Biology 138, 819–825.
Crossref | GoogleScholarGoogle Scholar |

Jackson, G. D. , and Moltschaniwskyj, N. A. (2002). Spatial and temporal variation in growth rates and maturity in the Indo-Pacific squid Sepioteuthis lessoniana (Cephalopoda: Loliginidae). Marine Biology 140, 747–754.
Crossref | GoogleScholarGoogle Scholar |

Jackson, G. D. , and O’Dor, R. K. (2001). Time, space and the ecophysiology of squid growth, life in the fast lane. Vie Milieu 51, 205–215.


Jackson, G. D. , and Pecl, G. (2003). The dynamics of the summer-spawning population of the loliginid squid (Sepioteuthis australis) in Tasmania, Australia – a conveyor belt of recruits. ICES Journal of Marine Science 60, 290–296.
Crossref | GoogleScholarGoogle Scholar |

Jackson, G. D. , and Yeatman, J. (1996). Variation in size and age at maturity in Photololigo (Mollusca: Cephalopoda) from the northwest shelf of Australia. Fishery Bulletin 94, 59–65.


Jackson, G. D., Arkhipkin, A. I., Bizikov, V. A. and  Hanlon, R. T. (1993). Laboratory and field corroboration of age and growth from statoliths and gladii of the loliginid squid Sepioteuthis lessoniana (Mollusca: Cephalopoda). In ‘Recent Advances in Cephalopod Fisheries Biology’. (Eds. T. Okutani, R. K. O’Dor and T. Kubodera)  pp. 189–199. (Tokai University Press: Tokyo, Japan.)

Jackson, G. D. , Forsythe, J. W. , Hixon, R. F. , and Hanlon, R. T. (1997). Age, growth, and maturation of Lolliguncula brevis (Cephalopoda: Loliginidae) in the northwestern Gulf of Mexico with a comparison of length–frequency versus statolith age analysis. Canadian Journal of Fisheries and Aquatic Sciences 54, 2907–2919.
Crossref | GoogleScholarGoogle Scholar |

Jackson, G. D. , Alford, R. A. , and Choat, J. H. (2000). Can squid populations be analyzed using standard fishery length-based techniques? ICES Journal of Marine Science 57, 948–954.
Crossref | GoogleScholarGoogle Scholar |

Karnik, N. S. , Chakraborty, S. K. , Jaiswar, A. K. , Swamy, R. P. , Rajaprasad, R. , Boomireddy, S. , and Rizvi, A. F. (2003). Growth and mortality of Indian squid, Loligo duvauceli (d’Orbigny) (Mollusca/Cephalopoda/Teuthoidea) from Mumbai waters, India. Indian Journal of Marine Sciences 32, 67–70.


Kinoshita, A. (1989). Age and growth of the loliginid squid, Heterloligo bleekeri.  Bulletin of the Seikai Regional Fisheries Research Laboratory 67, 59–69.


Lee, P. G. , Turk, P. E. , Yang, W. T. , and Hanlon, R. T. (1994). Biological characteristics and biomedical applications of the squid Sepioteuthis lessoniana cultured through multiple generations. The Biological Bulletin 186, 328–341.


Lipinski, M. R. (1986). Methods for the validation of squid age from statoliths. Journal of the Marine Biological Association of the United Kingdom 66, 505–524.


Lipinski, M. R. (1991). Scanning electron microscopy (SEM) and chemical treatment. Squid age determination using statoliths. In ‘Proceedings of an International Workshop, 9–14 Oct. 1989, Mazara del Vallo, Italy. N.T.R. – I.T.P.P. Spec. Publ. 1’. (Eds. P. Jereb, S. Ragonese and S. V. Boletzky)  pp. 97–112. (Istituto di Tecnologia della Pesca e del Pescato: Mazara del Vallo, Italy.)

Lipinski, M. R. , and Durholtz, M. D. (1994). Growth of Loligo vulgaris reynaudii d’Orb., 1845 (Cephalopoda: Loliginidae) statoliths from South African waters. Antarctic Science 6, 215–222.


Lipinski, M. R. , Durholtz, M. D. , and Underhill, L. G. (1998). Field validation of age readings from the statoliths of chokka squid (Loligo vulgaris reynaudii d'Orbigny, 1845) and an assessment of associated errors. ICES Journal of Marine Science 55, 240–257.
Crossref | GoogleScholarGoogle Scholar |

Macy, W. K. (1995). The application of digital image processing to the aging of long-finned squid, Loligo pealei, using the statolith. In ‘Recent Developments in Fish Otolith Research’. (Eds. D. H. Secor, J. M. Dean and S. E. Campana)  pp. 283–301. (University of South Carolina Press: Columbia, USA.)

Macy, W. K. , and Brodziak, J. K. T. (2001). Seasonal maturity and size at age of Loligo pealeii in waters of southern New England. ICES Journal of Marine Science 58, 852–864.
Crossref | GoogleScholarGoogle Scholar |

Martins, H. R. (1982). Biological studies of the exploited stock of Loligo forbesi (Mollusca: Cephalopoda) in the Azores. Journal of the Marine Biological Association of the United Kingdom 62, 799–808.


Maxwell, M. R. , and Hanlon, R. T. (2000). Female reproductive output in the squid Loligo pealeii: multiple egg clutches and implications for a spawning strategy. Marine Ecology Progress Series 199, 159–170.


Melo, Y. C. , and Sauer, W. H. H. (1999). Confirmation of serial spawning in the chokka squid Loligo vulgaris reynaudii off the coast of South Africa. Marine Biology 135, 307–313.
Crossref | GoogleScholarGoogle Scholar |

Moltschaniwskyj, N. A. (1994). Muscle tissue growth and muscle fibre dynamics in the tropical loliginid squid Photololigo sp. (Cephalopoda: Loliginidae). Canadian Journal of Fisheries and Aquatic Sciences 51, 830–835.


Moltschaniwskyj, N. A. (1995). Changes in shape associated with growth in the loliginid squid Photololigo sp.: a morphometric approach. Canadian Journal of Zoology 73, 1335–1343.


Moltschaniwskyj, N. A. , and Semmens, J. M. (2000). Limited use of stored energy reserves for reproduction by the tropical loliginid squid Photololigo sp. Journal of Zoology 251, 307–313.
Crossref | GoogleScholarGoogle Scholar |

Nabhitabhata, J. (1995). The culture of cephalopods: commercial scale attempts in Thailand. Aquaculture Towards the 21st Century. In ‘Proceedings of Infofish-Aquatech 94, International conference on aquaculture Colombo, Sri Lanka, 29–31 August 1994, Infofish 1995’. (Eds. K. P. P. Nambiar and T. Singh)  pp. 138–144. (INFOFISH: Kuala Lumpur, Malaysia.)

Nabhitabhata, J. (1996). Life cycle of cultured big fin squid, Sepioteuthis lessoniana Lesson. Phuket Marine Biological Centre Special Publication 16, 83–95.


Natsukari, Y. , and Komine, N. (1992). Age and growth estimation of the European squid, Loligo vulgaris, based on statolith microstructure. Journal of the Marine Biological Association of the United Kingdom 72, 271–280.


Natsukari, Y. , Nakanose, T. , and Oda, K. (1988). Age and growth of loliginid squid Photololigo edulis (Hoyle, 1885). Journal of Experimental Marine Biology and Ecology 116, 177–190.
Crossref | GoogleScholarGoogle Scholar |

O’Dor, R. K. , Adamo, J. P. , Andrade, Y. , Finn, J. , Hanlon, R. T. , and Jackson, G. D. (2002). Currents as environmental constraints on the behavior, energetics and distribution of cephalopods. Bulletin of Marine Science 71, 601–617.


Pecl, G. (2001). Flexible reproductive strategies in tropical and temperate Sepioteuthis squids. Marine Biology 138, 93–101.
Crossref | GoogleScholarGoogle Scholar |

Pecl, G. (2004). The in-situ relationship between season of hatching, growth and condition in the southern calamary, Sepioteuthis australis. Marine and Freshwater Research 55, 429–438.


Pecl, G. , and Moltschaniwskyj, N. (1999). Somatic growth processes: how are they altered in captivity? Proceedings of the Royal Society of London. Series B. Biological Sciences 266, 1133–1139.
Crossref | GoogleScholarGoogle Scholar |

Pecl, G. T. , Moltschaniwskyj, N. A. , Tracey, S. R. , and Jordan, A. R. (in press). Inter-annual plasticity of squid life-history and population structure: Ecological and management implications. Oecologia 139, 515–524.


Preuss, T. , Lebaric, Z. N. , and Gilly, W. F. (1997). Post-hatching development of circular mantle muscles in the squid Loligo opalescens.  The Biological Bulletin 192, 375–387.


Raya, C. P. , Balguerías, E. , Fernández-Núñez, M. M. , and Pierce, G. J. (1999). On reproduction and age of the squid Loligo vulgaris from the Saharan Bank (north-west African coast). Journal of the Marine Biological Association of the United Kingdom 79, 111–120.
Crossref | GoogleScholarGoogle Scholar |

Reichow, D. , and Smith, M. J. (2001). Microsatellites reveal high levels of gene flow among populations of the California squid Loligo opalescens.  Molecular Ecology 10, 1101–1109.
Crossref | GoogleScholarGoogle Scholar |

Rocha, F. , and Guerra, A. (1999). Age and growth of two sympatric squid Loligo vulgaris and Loligo forbesi, in Galician waters (north-west Spain). Journal of the Marine Biological Association of the United Kingdom 79, 697–707.
Crossref | GoogleScholarGoogle Scholar |

Segawa, S. (1987). Life history of the oval squid, Sepioteuthis lessoniana in Kominato and adjacent waters Central Honshu, Japan. Journal of the Tokyo University of Fisheries 74, 67–105.


Segawa, S. (1990). Food consumption, food conversion and growth rates of the oval squid Sepioteuthis lessoniana by laboratory experiments. Nippon Suisan Gakkaishi 56, 217–222.


Segawa, S. (1995). Effect of temperature on oxygen consumption of juvenile oval squid Sepioteuthis lessoniana.  Fisheries Science 61, 743–746.


Semmens, J. (1998). An examination of the role of the digestive gland of two loliginid squids, with respect to lipid: storage or excretion?  Proceedings of the Royal Society of London. Series B. Biological Sciences 265, 1685–1690.
Crossref | GoogleScholarGoogle Scholar |

Semmens, J. M. , and Moltschaniwskyj, N. A. (2000). An examination of variable growth in the loliginid squid Sepioteuthis lessoniana: a whole animal and reductionist approach. Marine Ecology Progress Series 193, 135–141.


Sweeney, M. J. , and Roper, C. F. E. (1998). Classification, type localities, and type repositories of recent cephalopoda. Smithsonian Contributions to Zoology 586, 561–595.


Triantafillos, L. (2004). Effects of genetic and environmental factors on growth of southern calamary, Sepioteuthis australis, from southern Australia and northern New Zealand. Marine and Freshwater Research 55, 439–446.


Triantafillos, L. , and Adams, M. (2001). Allozyme analysis reveals a complex population structure in the southern calamary Sepioteuthis australis from Australia and New Zealand. Marine Ecology Progress Series 212, 193–209.


Tsuchiya, M. (1982). On the culture of the squid, Sepioteuthis lessoniana Lesson (Loliginidae), from hatching to the whole life in Iriomote Island, Okinawa. Bulletin of the Institute of Oceanic Research and Development 4, 49–70.


Vidal, E. A. G. , DiMarco, F. P. , Wormuth, J. H. , and Lee, P. G. (2002). Influence of temperature and food availability on survival, growth and yolk utilization in hatchling squid. Bulletin of Marine Science 71, 915–931.


Villanueva, R. (2000). Effect of temperature on statolith growth of the European squid Loligo vulgaris during early life. Marine Biology 136, 449–460.
Crossref | GoogleScholarGoogle Scholar |

Villanueva, R. (2000). Differential increment deposition rate in embryonic statoliths of the loliginid squid Loligo vulgaris.  Marine Biology 137, 161–168.
Crossref | GoogleScholarGoogle Scholar |

Yang, W. T. , Hixon, R. F. , Turk, P. E. , Krejci, M. E. , Hulet, W. H. , and Hanlon, R. T. (1986). Growth, behavior, and sexual maturation of the market squid, Loligo opalescens, cultured through the life cycle. Fishery Bulletin 84, 771–798.


Yeatman, J. , and Benzie, J. A. H. (1994). Genetic structure and distribution of Photololigo spp. in Australia. Marine Biology 118, 79–87.