Hostname: page-component-cd9895bd7-gvvz8 Total loading time: 0 Render date: 2024-12-22T12:56:35.610Z Has data issue: false hasContentIssue false
  • English
  • Français

First description of spawning in a deep water loliginid squid, Loligo forbesi (Cephalopoda: Myopsida)

Published online by Cambridge University Press:  08 September 2008

Christopher K. Pham ,
Gilberto P. Carreira ,
Filipe M. Porteiro ,
João M. Gonçalves ,
Frederico Cardigos  and
Helen R. Martins
Christopher K. Pham*
Affiliation:
Departamento de Oceanografia e Pescas, Universidade dos Açores, PT 9900 Horta, Açores, Portugal
Gilberto P. Carreira
Affiliation:
Departamento de Oceanografia e Pescas, Universidade dos Açores, PT 9900 Horta, Açores, Portugal
Filipe M. Porteiro
Affiliation:
Departamento de Oceanografia e Pescas, Universidade dos Açores, PT 9900 Horta, Açores, Portugal
João M. Gonçalves
Affiliation:
Departamento de Oceanografia e Pescas, Universidade dos Açores, PT 9900 Horta, Açores, Portugal
Frederico Cardigos
Affiliation:
Departamento de Oceanografia e Pescas, Universidade dos Açores, PT 9900 Horta, Açores, Portugal
Helen R. Martins
Affiliation:
Departamento de Oceanografia e Pescas, Universidade dos Açores, PT 9900 Horta, Açores, Portugal
*
Correspondence should be addressed to: Christopher K. Pham, Departamento de Oceanografia e Pescas, Universidade dos Açores, PT 9900 Horta, Açores, Portugal email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Despite being an exploited and economically important species, little is known about the reproductive behaviour of Loligo forbesi. During a captive trial performed in a closed seawater system in the Azores, three spawning events were directly witnessed. An account of their main behavioural aspects is given. A number of behavioural components are described for the first time in this species: ‘pair formation’, ‘mate guarding’, ‘egg holding’, ‘egg touching’, ‘white arms’, ‘red accessory nidamental glands’, ‘accentuated testis’, and ‘jockeying and parrying’. The chromatic, locomotor and postural components were very similar to other coastal loliginids observed on spawning grounds. From egg masses recovered on octopus traps, we show that in the Azores spawning activity occurs at least between 25 and 144 m, but greater depths might be expected. We suggest that this squid preferentially deposits egg masses on hard structures probably hiding them in cracks and crevices of volcanic substrata. The existence of spawning aggregations is supported by several factors: (i) these spawning grounds may coincide with the fishing spots, where the exploitation seasonally takes place, given that most individuals caught by fishermen are usually mature (more than 80%); and (ii) mate guarding and jockeying/parrying by males was observed, which is a common feature of spawning aggregation areas, where sperm competition occurs. Furthermore, our results, combined with available published and non-published data further confirm L. forbesi as an intermittent spawner. We estimate that throughout their short life cycle, females of L. forbesi are able to perform up to six spawning events, each composed of an average of ≈2300 eggs.

Keywords

cephalopodssquidspawning rangeembryosmate guardingcaptivityAzores
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 89 , Issue 1 , February 2009 , pp. 171 - 177
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

Arnold, J.M. (1990) Squid mating behavior. In Gilbert, D.L., Adelman, W.J. and Arnold, J.M. (eds) Squid as experimental animals. New York: Plenum Press, pp. 65–75.CrossRefGoogle Scholar
Boyle, P.R. and Pierce, G.J. (1994) Fishery biology of Northeast Atlantic squid: an overview. Fisheries Research 21, 1–15.CrossRefGoogle Scholar
Boyle, P.R., Pierce, G.J. and Hastie, L.C. (1995) Flexible reproductive strategies in the squid Loligo forbesi. Marine Biology 121, 201–508.CrossRefGoogle Scholar
Brierley, A.S., Thorpe, J.P., Clarke, M.R. and Martins, H.R. (1993) A preliminary biochemical genetic investigation of population structure of Loligo forbesi Steenstrup, 1856 from British Isles and the Azores. In Okutani, T., O'Dor, R.K. and Kubodera, T. (eds) Recent advances in cephalopod fisheries biology. Tokyo: Tokai University Press, pp. 61–69.Google Scholar
Brierley, A.S., Thorpe, J., Pierce, G.J., Clarke, M.R. and Boyle, P.R. (1995) Genetic variation in the neritic squid Loligo forbesi (Myopsidae: Loliginidae) in the northeast Atlantic Ocean. Marine Biology 122, 79–86.CrossRefGoogle Scholar
Carreira, G.P. (2000) Octopus vulgaris Cuvier, 1797 (Mollusca: Cephalopoda) dos Açores: biologia populacional e exploração. Tese de Mestrado. Universidade do Porto, Porto, Portugal.Google Scholar
Collins, M.A., Burnell, G.M. and Rodhouse, P.G. (1995a) Reproductive strategies of male and female Loligo forbesi. Journal of the Marine Biological Association of the United Kingdom 75, 621–634.CrossRefGoogle Scholar
Collins, M.A., Burnell, G.M. and Rodhouse, P.G. (1995b) Recruitment, maturation and spawning of Loligo forbesi Steenstrup (Cephalopoda: Loliginidae) in Irish waters. ICES Journal of Marine Science 52, 127–137.CrossRefGoogle Scholar
Craig, S. and Overnell, J. (2003) Metals in squid, Loligo forbesi, adults, eggs and hatchlings. No evidence for a role for Cu- or Zn-metallothionein. Comparative Biochemistry and Physiology Part C 134, 311–317.Google ScholarPubMed
DiMarco, F.P. and Hanlon, R.T. (1997) Agonistic behavior in the squid Loligo plei (Loliginidae, Teuthoidea): fighting tactics and the effects of size and resource value. Ethology 103, 89–108.CrossRefGoogle Scholar
Gonçalves, J.M., Porteiro, F.M., Cardigos, F. and Martins, H.R. (1995) Adult squid Loligo forbesi (Cephalopoda: Loliginidae) in captivity: maintenance and transport. International Council for the Exploration of the Sea (CM Papers and Reports) CM 1995/F: 14, 12 pp.Google Scholar
Hanlon, R.T. (1982) The functional organization of chromatophores and iridescent cells in the body patterning of Loligo plei (Cephalopoda: Myopsida). Malacologia 23, 89–119.Google Scholar
Hanlon, R.T. (1988) Behavioral and body patterning characters useful in taxonomy and field identification of cephalopods. Malacologia, 29, 247–264.Google Scholar
Hanlon, R.T. (1998) Mating systems and sexual selection in the squid Loligo: how might commercial fishing and spawning squid affect them? CalCOFI 39, 92–100.Google Scholar
Hanlon, R.T. and Messenger, J.B. (1996) Cephalopod behaviour. Cambridge: Cambridge University Press.Google Scholar
Hanlon, R.T., Yang, W.T., Turk, P.E., Lee, P.G. and Hixon, R.F. (1989) Laboratory culture and estimated life span of the Eastern Atlantic squid, Loligo forbesi Steenstrup, 1856 (Mollusca: Cephalopoda). Aquaculture and Fisheries Management 20, 15–34.Google Scholar
Hanlon, R.T., Smale, M.J. and Sauer, W.H.H. (1994) An ethogram of body patterning behavior in the squid Loligo vulgaris reynaudii on spawning grounds in South Africa. Biological Bulletin. Marine Biological Laboratory, Woods Hole 187, 363–372.CrossRefGoogle ScholarPubMed
Hanlon, R.T., Maxwell, M.R., Shashar, N., Loew, E.R. and Boyle, K.L. (1999) An ethogram of body patterning behaviour in the biomedically and commercially valuable squid Loligo pealei off Cape Cod, Massachusetts. Biological Bulletin. Marine Biological Laboratory, Woods Hole 197, 49–62.CrossRefGoogle ScholarPubMed
Hanlon, R.T., Naud, M.J., Shaw, P.W. and Havenhand, J.N. (2005) Transient sexual mimicry leads to fertilisation. Nature 430, 212.CrossRefGoogle Scholar
Holme, N.A. (1974) The biology of Loligo forbesi Steenstrup (Mollusca: Cephalopoda) in the Plymouth area. Journal of the Marine Biological Association of the United Kingdom 54, 481–503.CrossRefGoogle Scholar
Hurley, A.C. (1977) Mating behavior of the squid Loligo opalescens. Marine Behaviour and Physiology 4, 195–203.CrossRefGoogle Scholar
Jantzen, T.M. and Havenhand, J. (2003) Reproductive behaviour in the squid Sepitoteuthis australis from South Australia: ethogram of reproductive body patterns. Biological Bulletin. Marine Biological Laboratory, Woods Hole 204, 290–304.CrossRefGoogle ScholarPubMed
Lordan, C. and Casey, J. (1999) The first evidence of offshore spawning in the squid species Loligo forbesi. Journal of the Marine Biological Association of the United Kingdom 79, 379–381.CrossRefGoogle Scholar
Lum-Kong, A., Pierce, G.J. and Yau, C. (1992) Timing of spawning and recruitment in Loligo forbesi (Cephalopoda: Loliginidae) in Scottish waters. Journal of the Marine Biological Association of the United Kingdom 72, 301–311.CrossRefGoogle Scholar
Mangold, K. (1987) Reproduction. In Boyle, P.R. (ed.) Cephalopod life cycles. Volume II. New York: Academic Press, pp. 157–200.Google 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.CrossRefGoogle Scholar
Martins, H.R. and Porteiro, F.M. (1988) The exploited stock of Loligo forbesi in the Azores: additional notes on biology and fisheries. International Council for the Exploration of the Sea. (CM Papers and Reports) CM 1988/K8: 7 pp.Google Scholar
Moynihan, M.H. (1985) Communication and non-communication by cephalopods. Bloomington: Indiana University Press.Google Scholar
O'Dor, R.K., Hoar, J.A., Webber, D.M., Carey, F.G., Tanaka, S., Martins, H.R. and Porteiro, F.M. (1994) Squid (Loligo forbesi) performance and metabolic rates in nature. Marine and Freshwater Behaviour and Physiology 25, 163–177.CrossRefGoogle Scholar
Pierce, G.J. and Boyle, P.R. (2003) Empirical modelling of interannual trends in abundance of squid (Loligo forbesi) in Scottish waters. Fisheries Research 59, 305–326.CrossRefGoogle Scholar
Pierce, G.J., Hastie, L.C., Guerra, A., Thorpe, R.S., Howard, F.G. and Boyle, P.R. (1994) Morphological variation in Loligo forbesi and Loligo vulgaris: regional, seasonal, sex, maturity and worker differences. Fisheries Research 21, 127–148.CrossRefGoogle Scholar
Pierce, G.J., Bailey, N., Stratoudakis, Y. and Newton, A. (1998) Distribution and abundance of the fished population of Loligo forbesi in Scottish waters: analysis of research cruise data. ICES Journal of Marine Science 55, 14–33.CrossRefGoogle Scholar
Porteiro, F.M. (1994) The present status of squid fishery (Loligo forbesi) in the Azores archipelago. Fisheries Research 21, 243–253.CrossRefGoogle Scholar
Porteiro, F.M. and Martins, H.R. (1992) First finding of natural laid eggs from Loligo forbesi Steenstup, 1856 (Mollusca: Cephalopoda) in the Azores. Arquipélago—Life and Earth Sciences 10, 119–120.Google Scholar
Porteiro, F.M. and Martins, H.R. (1994) Biology of Loligo forbesi Steenstrup, 1856 (Mollusca: Cephalopoda) in the Azores: sample composition and maturation of squid caught by jigging. Fisheries Research 21, 103–114.CrossRefGoogle Scholar
Porteiro, F.M., Martins, H.R. and Hanlon, R.T. (1990) Some observations on the behaviour of adult squid, Loligo forbesi in captivity. Journal of the Marine Biological Association of the United Kingdom 70, 459–472.CrossRefGoogle Scholar
Rocha, F. and Guerra, A. (1996) Signs of an extended and intermittent terminal spawning in the squids Loligo vulgaris Lamarck and L. forbesi Steenstrup (Cephalopoda: Loliginidae). Journal of Experimental Marine Biology and Ecology 207, 177–189.CrossRefGoogle Scholar
Roper, C.F.E., Sweeney, M.J. and Nauen, C.E. (1984) Cephalopods of the world. An annotated and illustrated catalogue of species of interest to fisheries. FAO fisheries Synopsis (125) 3, 277 pp.Google Scholar
Salman, A. and Laptikhovsky, V. (2002) First occurrence of egg masses of Loligo forbesi (Cephalopoda: Loliginidae) in deep waters of the Aegean Sea. Journal of the Marine Biological Association of the United Kingdom 82, 925–926.CrossRefGoogle Scholar
Santos, V.M.C. (1993) Fecundidade na espécie Loligo forbesi (Steenstrup, 1856). Tese de Licenciatura. Universidade do Algarve, Faro, Portugal.Google Scholar
Sauer, W.H.H., Smale, M.J. and Lipinski, M.R. (1992) The location of spawning grounds, spawning and schooling behaviour of the squid Loligo vulgaris reynaudii (Cephalopoda: Myopsidae) off the Eastern Cape Coast, South Africa. Marine Biology 114, 97–107.CrossRefGoogle Scholar
Segawa, S., Yang, W.T., Marthy, H.-J. and Hanlon, R.T. (1988) Illustrated embryonic stages of the eastern Atlantic squid Loligo forbesi. Veliger 30, 230–243.Google Scholar
Shaw, P.W. and Boyle, P.R. (1997) Multiple paternity within the brood of single females of Loligo forbesi (Cephalopoda: Loliginidae), demonstrated with microsatellite DNA markers. Marine Ecology Progress Series 160, 279–282.CrossRefGoogle Scholar
Shaw, P.W., Pierce, G.J. and Boyle, P.R. (1999) Subtle population structuring within a highly vagile marine invertebrate, the veined squid Loligo forbesi, demonstrated with microsatellite DNA markers. Molecular Ecology 8, 407–417.CrossRefGoogle Scholar
Zar, J.H. (1996) Biostatistical analysis. Third edition. Upper Saddle River, NJ: Prentice-Hall.Google Scholar
Wirtz, P. (1994) Underwater guide Madeira–Canary Islands–Azores: fish. Stuttgart: Naglschmid, 156p.Google Scholar