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Abiotic influences on embryo growth: statoliths as experimental tools in the squid early life history

  • Roger VillanuevaEmail author
  • Natalie A. Moltschaniwskyj
  • Anna Bozzano
Original paper

Abstract

Statolith size and growth was used to determine the influence of abiotic factors on the growth of Loligo vulgaris and Sepioteuthis australis embryos. Recently spawned egg masses collected from the field were incubated in the laboratory under different levels of light intensity, photoperiod, or short periods of low salinity (30‰). Double tetracycline staining was used to follow statolith growth. In L. vulgaris constant light conditions produced significantly slower growth in the embryonic statoliths and embryos held at summer photoperiod had slower statolith growth than those held at winter photoperiods. However once they hatched out there was no evidence that photoperiod affected statolith growth. After hatching, in all photoperiods statolith growth rates decreased in comparison with late embryonic rates. In S. australis embryos, differences between the high and medium light intensities for summer and intermediate photoperiods were found, suggesting that under summer incubation temperature, longer daylengths at medium light intensity favoured higher statolith growth for this species. In comparison to controls, slower statolith growth in S. australis embryos due to low salinity only occurred when exposed for 72 h. Comparison with previous studies indicates that temperature seems to be the main abiotic factor influencing statolith growth during early stages, however, interactions among all abiotic factors needs to be determined as well as the unknown influence of other isolated factors, e.g., oxygen concentration within the egg mass.

Keywords

Early life Loliginidae Embryo Growth Statolith 

Notes

Acknowledgements

The work undertaken by RV and AB at the University of Tasmania was supported by the Spanish Ministry of Science (Programa para Movilidad de Investigadores and postdoctoral fellowship, respectively). This work was supported by grants from the European Commission (Cephstock Concerted Action) and the University of Tasmania Merit Grants Scheme.

References

  1. Boettcher KJ, Ruby EG, McFall-Ngai MJ (1996) Bioluminescence in the symbiotic squid Euprymna scolopes is controlled by a daily biological rhythm. J Comp Physiol Psychol 179:65–73Google Scholar
  2. Boletzky SV (1987) Embryonic phase. In: Boyle PR (ed) Cephalopod life cycles. Academic Press, London, pp 5–31Google Scholar
  3. Brown ER, Piscopo S, De Stefano R, Giuditta A (2006) Brain and behavioural evidence for rest-activity cycles in Octopus vulgaris. Behav Brain Res 172:355–359PubMedCrossRefGoogle Scholar
  4. Chung WS, Lu CC (2005) The influence of temperature and salinity on the statolith of the Oval squid Sepioteuthis lessoniana Lesson, 1830 during early developmental stages. Pukhet Mar Biol Cent Res Bull 66:175–185Google Scholar
  5. Cinti AB, Baron PJ, Rivas AL (2004) The effects of environmental factors on the embryonic survival of the Patagonian squid Loligo gahi. J Exp Mar Biol Ecol 313:225–240CrossRefGoogle Scholar
  6. Clarke MR (1978) The cephalopod statolith—an introduction to its form. J Mar Biol Assoc UK 58:701–712CrossRefGoogle Scholar
  7. Cobb CS, Pope SK, Williamson R (1995) Circadian rhythms to light-dark cycles in the lesser octopus, Eledone cirrhosa. Mar Fresh Behav Physiol 26:47–57Google Scholar
  8. D’Aniello A, D’Onofrio G, Pischetola M, Denucé JM (1989) Effect of pH, salinity and Ca2+, Mg2+, K+ and SO2+ 4 ions on hatching and viability of Loligo vulgaris embryo. Comp Biochem Physiol 94A:477–481CrossRefGoogle Scholar
  9. Durholtz MD, Lipinski MR (2000) Influence of temperature on the microstructure of statoliths of the thumbstall squid Lolliguncula brevis. Mar Biol 136:1029–1037CrossRefGoogle Scholar
  10. Forsythe JW (2004) Accounting for the effect of temperature on squid growth in nature: from hypothesis to practice. Mar Fresh Res 55:331–339CrossRefGoogle Scholar
  11. Gowland FC, Moltschaniwskyj NA, Steer MA (2002) Description and quantification of developmental abnormalities in a natural Sepioteuthis australis spawning population (Mollusca: Cephalopoda). Mar Ecol Prog Ser 243:133–141Google Scholar
  12. Ikeda I, Ito K, Matsumoto G (2004) Does light intensity affect embryonic development of squid (Heterololigo bleekeri)? J Mar Biol Ass UK 84:1215–1219CrossRefGoogle Scholar
  13. Jackson GD, Arkhipkin AI, Bizikov VA, Hanlon RT (1993) Laboratory and field corroboration of age and growth from statoliths and gladii of the loliginid squid Sepioteuthis lessoniana (Mollusca: Cephalopoda). In: Okutani T, O’Dor RK, Kubodera T (eds) Recent Advances in Cephalopod Fisheries Biology Tokai University Press, pp 189–200Google Scholar
  14. Jackson GD (1994) Application and future potential of statolith increment analysis in squids and sepioids. Can J Fish Aquat Sci 51:2612–2625CrossRefGoogle Scholar
  15. Jackson GD, Moltschaniwskyj NA (2001) The influence of ration level on growth and statolith increment width of the tropical squid Sepioteuthis lessoniana (Cephalopoda: Loliginidae): an experimental approach. Mar Biol 138:819–825CrossRefGoogle Scholar
  16. Mangold-Wirz K (1963) Biologie des céphalopodes benthiques et nectoniques de la Mer Catalane. Vie et Milieu 13:1–285Google Scholar
  17. Mugiya Y (1987) Effects of photoperiods on the formation of otolith Increments in the embryonic and larval rainbow trout Salmo gairdneri. Nipp Suis Gakk 53:1979–1984Google Scholar
  18. Nabhitabhata JA, Asawangkune P, Amornjaruchit S, Promboon P (2001) Tolerance of eggs and hatchlings of neritic cephalopods to salinity changes. Pukhet Mar Biol Cent 25(Special Publication):91–99Google Scholar
  19. O’Dor RK, Foy FA, Helm PL, Balch N (1986) The locomotion and energetics of hatchling squid Illex illecebrosus. Amer Malacol Bull 4:55–60Google Scholar
  20. Packard A (1969) Jet propulsion and the giant fibre response of Loligo. Nature 221:875–877PubMedCrossRefGoogle Scholar
  21. Palmegiano GB, D’Apote MP (1983) Combined effects of temperature and salinity on cuttlefish (Sepia officinalis L.) hatching. Aquaculture 35:259–264CrossRefGoogle Scholar
  22. Paulij WP, Herman PMJ, Van Hannen EJ, Denucé JM (1990a) The impact of photoperiodicity on hatching of Loligo vulgaris and Loligo forbesi. J Mar Biol Ass UK 70:597–610CrossRefGoogle Scholar
  23. Paulij WP, Bogaards RH, Denucé JM (1990b) Influence of salinity on embryonic development and the distribution of Sepia officinalis in the Delta Area (South Western part of The Netherlands). Mar Biol 107:17–23CrossRefGoogle Scholar
  24. Paulij WP, Herman PMJ, Roozen MEF, Denucé JM (1991) The influence of photoperiodicity on hatching of Sepia officinalis. J Mar Biol Ass UK 71:665–678Google Scholar
  25. Pecl GT, Steer MA, Hodgson KE (2004) The role of hatchling size in generating the intrinsic size-at-age variability of cephalopods: extending the Forsythe Hypothesis. Mar Fresh Res 55:387–394CrossRefGoogle Scholar
  26. Sakai M, Brunetti N, Ivanovic M, Elena B, Nakamura K (2004) Interpretation of statolith microstructure in reared hatchling paralarvae of the squid Illex argentinus. Mar Fresh Res 55:403–313CrossRefGoogle Scholar
  27. Sen H (2005) Incubation of European squid (Loligo vulgaris Lamarck, 1798) eggs at different salinities. Aquacult Res 36:876–881CrossRefGoogle Scholar
  28. Steer MA, Moltschaniwskyj NA, Gowland FC (2002) Temporal variability in embryonic development and mortality in the southern calamary Sepioteuthis australis: a field assessment. Mar Ecol Prog Ser 243:143–150Google Scholar
  29. Steer MP, Pecl GT, Moltschaniwskyj NA (2003a) Are bigger calamary Sepioteuthis australis hatchlings more likely to survive? A study based on statolith dimensions. Mar Ecol Prog Ser 261:175–182Google Scholar
  30. Steer MA, Moltschaniwskyj NA, Jordan AR (2003b) Embryonic development of southern calamary (Sepioteuthis australis) within the constraints of an aggregated egg mass. Mar Fresh Res 54:217–226CrossRefGoogle Scholar
  31. Vidal EAG, DiMarco FP, Wormuth JH, Lee PG (2002) Influence of temperature and food availability on survival, growth and yolk utilization in hatchling squid. Bull Mar Sci 71:915–931Google Scholar
  32. Vidal EAG, Roberts MJ, Martins RS (2005) Yolk utilization, metabolism and growth in reared Loligo vulgaris reynaudii paralarvae. Aquat Liv Res 18:385–393CrossRefGoogle Scholar
  33. Villanueva R (2000a) Effect of temperature on statolith growth of the European squid Loligo vulgaris during early life. Mar Biol 136:449–460CrossRefGoogle Scholar
  34. Villanueva R (2000b) Differential increment-deposition rate in embryonic statoliths of the loliginid squid Loligo vulgaris. Mar Biol 137:161–168CrossRefGoogle Scholar
  35. Villanueva R, Arkhipkin A, Jereb P, Lefkaditou E, Lipinski MR, Perales-Raya C, Riba J, Rocha F (2003) Embryonic life of the loliginid squid Loligo vulgaris: comparison between statoliths of Atlantic and Mediterranean populations. Mar Ecol Prog Ser 253:197–208Google Scholar
  36. Wells MJ, O’Dor RK, Mangold K, Wells J (1983) Diurnal changes in activity and metabolic rate in Octopus vulgaris. Mar Behav Physiol 9:275–287CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2006

Authors and Affiliations

  • Roger Villanueva
    • 1
    Email author
  • Natalie A. Moltschaniwskyj
    • 2
  • Anna Bozzano
    • 1
  1. 1.Institut de Ciències del MarCSICBarcelonaSpain
  2. 2.School of Aquaculture, Tasmanian Aquaculture and Fisheries InstituteUniversity of TasmaniaLauncestonAustralia

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