Evidence for multiple year classes of the giant Australian cuttlefish Sepia apama in northern Spencer Gulf, South Australia

  • Karina C. Hall
  • Anthony J. Fowler
  • Michael C. Geddes
Original Paper

Abstract

Giant Australian cuttlefish form a mass spawning aggregation at a single site in northern Spencer Gulf (NSG) in South Australia every austral winter. Samples of cuttlefish were collected from this region over three consecutive years. Analysis of regular growth increments in the cuttlebones of these individuals, revealed a polymorphism in growth pattern for both sexes. Three distinct “bone patterns” were identified based on the variation in increment widths over the lengths of the bones. All bones analysed conformed to one of the three bone patterns, and the increment width patterns were consistent between years. Interpretation of the patterns, suggested that Sepia apama have two alternative life cycles. The first involves rapid juvenile growth during the first summer after hatching, with maturity reached within 7–8 months. These individuals return to spawn in their first year as small individuals. The second life cycle involves much slower juvenile growth during the first summer, with maturity deferred until their second year, when they return to spawn as much larger individuals. Thus, the age compositions of populations of S. apama in the NSG appear to consist of two year classes for both sexes.

Keywords

Cuttlefish Sepia apama Life history Ageing Cuttlebone Growth increments Phenotypic plasticity 

References

  1. Bandel K, von Boletzky S (1979) A comparative study of the structure, development and morphological relationship of chambered cephalopod shells. Veliger 21:313–354Google Scholar
  2. Beamish RJ, McFarlane GA (1983) The forgotten requirement for age validation in fisheries biology. Trans Am Fish Soc 112:735–743CrossRefGoogle Scholar
  3. Bettencourt V, Guerra A (2000) Growth increments and biomineralization process in cephalopod statoliths. J Exp Mar Biol Ecol 248:191–205PubMedCrossRefGoogle Scholar
  4. Bettencourt V, Guerra A (2001) Age studies based on daily growth increments in statoliths and growth lamellae in cuttlebone of cultured Sepia officinalis. Mar Biol 139:327–334CrossRefGoogle Scholar
  5. Brodziak JKT, Macy WK (1996) Growth of long-finned squid, Loligo pealei, in the northwest Atlantic. Fish Bull 94:212–236Google Scholar
  6. Caddy JF (1991) Death rates and time intervals: is there an alternative to the constant natural mortality axiom? Rev Fish Biol Fish 1:109–138CrossRefGoogle Scholar
  7. Campana SE (1999) Chemistry and composition of fish otoliths: pathways, mechanisms and applications. Mar Ecol Prog Ser 188:263–297Google Scholar
  8. Campana SE (2001) Accuracy, precision and quality control in age determination, including a review of the use and abuse of age validation methods. J Fish Biol 59:197–242CrossRefGoogle Scholar
  9. Campana SE, Neilson JD (1985) Microstructure of fish otoliths. Can J Fish Aquat Sci 42:1014–1032Google Scholar
  10. Campana SE, Thorrold SR (2001) Otoliths, increments, and elements: keys to a comprehensive understanding of fish populations? Can J Fish Aquat Sci 58:30–38CrossRefGoogle Scholar
  11. Carrick NA (1997) A preliminary assessment of the by-catch from the Spencer Gulf prawn fishery, South Australian Fisheries Assessment Series 97/02. SARDI Aquatic Sciences, AdelaideGoogle Scholar
  12. Challier L, Royer J, Robin JP (2002) Variability in age-at-recruitment and early growth in English Channel Sepia officinalis described with statolith analysis. Aquat Living Resour 15:303–311CrossRefGoogle Scholar
  13. Challier L, Dunn MR, Robin JP (2005) Trends in age-at-recruitment and juvenile growth of cuttlefish, Sepia officinalis, from the English Channel. ICES J Mar Sci 62:1671–1682CrossRefGoogle Scholar
  14. Choe S (1963) Daily age markings on the shell of cuttlefishes. Nature 197:306–307CrossRefGoogle Scholar
  15. Denton EJ, Gilpin-Brown JB (1961) The buoyancy of the cuttlefish, Sepia officinalis (L.). J Mar Biol Assoc UK 41: 319–342CrossRefGoogle Scholar
  16. Gales R, Pemberton D, Lu CC, Clarke MR (1993) Cephalopod diet of the Australian fur seal: variation due to location, season and sample type. Aust J Mar Freshw Res 44:657–671CrossRefGoogle Scholar
  17. Hall KC, Fowler AJ (eds) (2003) The fisheries biology of the cuttlefish Sepia apama Gray, in South Australian waters. Final Report to FRDC (Project No. 98/151). SARDI Aquatic Sciences, Adelaide, p 277Google Scholar
  18. Hatfield EMC, Rodhouse PG (1994) Migration as a source of bias in the measurement of cephalopod growth. Antarct Sci 6:179–184Google Scholar
  19. Hewitt RA, Stait B (1988) Seasonal variation in septal spacing of Sepia officinalis and some Ordovician actinocerid nautiloids. Lethaia 21:383–394Google Scholar
  20. Jackson GD, Alford RA, Choat JH (2000) Can length frequency analysis be used to determine squid growth?—an assessment of ELEFAN. ICES J Mar Sci 57:948–954CrossRefGoogle Scholar
  21. Kim ZG, Hong BQ (1991) Study on possible group separation of cuttlefish Sepia esculenta Hoyle in Korean waters. Bull Natl Fish Res Dev Agency (Korea) 45:71–84Google Scholar
  22. Le Goff R, Gauvrit E, Du Sel GP, Daguzan J (1998) Age group determination by analysis of the cuttlebone of the cuttlefish Sepia officinalis L. in reproduction in the Bay of Biscay. J Molluscan Stud 64:183–193CrossRefGoogle Scholar
  23. Lipinski MR (1998) Cephalopod life cycles: patterns and exceptions. In: Payne AIL, Lipinski MR, Clarke MR, Roeleveld MAC (eds) Cephalopod biodiversity, ecology and evolution. S Afr J Mar Sci 15:439–447Google Scholar
  24. Lu CC (1998) A synopsis of Sepiidae in Australian waters (Cephalopoda: Sepioidea). In: Voss NA, Vecchione M, Toll RB, Sweeney MJ (eds) Systematics and biogeography of cephalopods. Smiths Contr Zool 586:159–190Google Scholar
  25. Macy WK III (1995) The application of digital image processing to the aging of long-finned squid, Loligo pealei, using the statolith. In: Secor DH, Dean JM, Campana SE (eds) Recent developments in fish otolith research. South Carolina Press, USA, pp 283–302Google Scholar
  26. Macy WK, Brodziak JKT (2001) Seasonal maturity and size at age of Loligo pealeii in waters of southern New England. ICES J Mar Sci 58:852–864CrossRefGoogle Scholar
  27. Natsukari Y, Hirata S, Washizake M (1991) Growth and seasonal change of the cuttlebone characters of Sepia esculenta. In: Boucaud-Camou E (ed) La seiche, The cuttlefish. 1st international symposium on the cuttlefish, Sepia. Centre de Publications de L’Université de Caen, Caen, France, pp 49–67Google Scholar
  28. Nunes RA, Lennon GW (1986) Physical property distributions and seasonal trends in Spencer Gulf, South Australia: an inverse estuary. Aust J Mar Freshw Res 37:39–53CrossRefGoogle Scholar
  29. Nunes Vaz RA, Lennon GW, Bowers DG (1990) Physical behaviour of a large, negative or inverse estuary. Cont Shelf Res 10:277–304CrossRefGoogle Scholar
  30. Packard A (1972) Cephalopods and fish: the limits of convergence. Biol Rev 47:241–307CrossRefGoogle Scholar
  31. Pannella G (1971) Fish otoliths: daily growth layers and periodical patterns. Science 173:1124–1127CrossRefGoogle Scholar
  32. Pierce GJ, Guerra A (1994) Stock assessment methods used for cephalopod fisheries. Fish Res 21:255–285CrossRefGoogle Scholar
  33. Ré P, Narciso L (1994) Growth and cuttlebone microstructure of juvenile cuttlefish, Sepia officinalis L., under controlled conditions. J Exp Mar Biol Ecol 177:73–78CrossRefGoogle Scholar
  34. Richard A (1969) The part played by temperature in the rhythm of formation of markings on the shell of cuttlefish (Sepia officinalis L.) (Cephalopoda, Mollusca). Experientia 25:1051–1052PubMedCrossRefGoogle Scholar
  35. Rodhouse PG, Hatfield EMC (1990) Age determination in squid using statolith growth increment. Fish Res 8:323–334CrossRefGoogle Scholar
  36. Tabachnick BG, Fidell LS (2001) Using multivariate statistics. Allyn & Bacon, Needham Heights, p. 966Google Scholar
  37. von Boletzky S (1974) Effets de la sous-nutrition prolongée sur le développement de la coquille de Sepia officinalis L. (Mollusca, Cephalopoda). Bull Soc Zool Fr 99:667–673Google Scholar
  38. von Boletzky S (1983) Sepia officinalis. In: Boyle PR (ed) Cephalopod life cycles, vol. I: species accounts. Academic, London, pp 31–52Google Scholar
  39. von Boletzky S, Overath H (1991) Shell fracture and repair in the cuttlefish Sepia officinalis. In: Boucaud-Camou E (ed) La seiche, The cuttlefish. 1st international symposium on the cuttlefish, Sepia. Centre de Publications de L’Université de Caen, Caen, France, pp 69–78Google Scholar
  40. Voss NA (1983) A review of cephalopod fisheries biology. Mem Mus Vic 44:229–241Google Scholar
  41. Zar JH (1999) Biostatistical analysis. Prentice-Hall, Upper Saddle River, p 663Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  • Karina C. Hall
    • 1
    • 2
  • Anthony J. Fowler
    • 1
  • Michael C. Geddes
    • 2
  1. 1.South Australian Research and Development InstituteHenley Beach, AdelaideAustralia
  2. 2.Department of Environmental BiologyUniversity of AdelaideAdelaideAustralia

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