Advertisement

Marine Biology

, Volume 161, Issue 1, pp 89–99 | Cite as

Looking for the clock mechanism responsible for circatidal behavior in the oyster Crassostrea gigas

  • Audrey M. Mat
  • Jean-Charles Massabuau
  • Pierre Ciret
  • Damien TranEmail author
Original Paper

Abstract

Valve activity rhythm of the oyster Crassostrea gigas is mainly driven by tides in the field, but in the laboratory, only a circadian clock mechanism has been demonstrated. In an attempt to reconcile these results, the mechanisms underlying the circatidal rhythm were studied in the laboratory under different entrainment or free-running regimes and in the field at Arcachon (44°39′N/1°09′W) in February–April 2011). Results confirm the existence of a circadian clock in C. gigas. Under entrainment regimes (12-h dark/12-h light photoperiod and tidal cycles simulated by a reversing current flow), oysters exhibited both circadian and circatidal cycles. Under free-running conditions (e.g., continuous darkness), the endogenous rhythm appeared to be circadian. There was no experimental evidence for an endogenous circatidal rhythm, even in oysters just transferred from the field, where a clear tidal cycle was expressed. There are two possible mechanisms to explain tidal behavior in C. gigas: an exogenous tidal cue that drives tidal activity and masks the circadian rhythm and an endogenous circatidal clock that is sensitive to tidal zeitgebers and runs at tidal frequency.

Keywords

Circadian Rhythm Circadian Clock Tidal Cycle Circadian Oscillator Tidal Period 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This work was supported by a ministerial scholarship to A.M. and the projects EC2CO-Cytrix and OSQUAR, Région Aquitaine. The authors thank Dr. Katherine Flynn for editing and English corrections.

References

  1. Abello P, Reid DG, Naylor E (1991) Comparative locomotor activity patterns in the portunid crab Liocarcinus holsatus and L. depurator. J Mar Biol Assoc UK 71:1–10CrossRefGoogle Scholar
  2. Akiyama T (1995) Circatidal swimming activity rhythm in a subtidal cumacean Dimorphostylis asiatica (Crustacea). Mar Biol 123:251–255CrossRefGoogle Scholar
  3. Akiyama T (1997) Tidal adaptation of a circadian clock controlling a crustacean swimming behavior. Zool Sci 14:901–906CrossRefGoogle Scholar
  4. Al-Adhub AHY, Naylor E (1975) Emergence rhythms and tidal migrations in the brown shrimp Crangon crangon (L.). J Mar Biol Assoc UK 55:801–810CrossRefGoogle Scholar
  5. Beentjes MP, Williams BG (1986) Endogenous circatidal rhythmicity in the New Zealand cockle Chione stutchburyi (Bivalvia, Veneridae). Mar Behav Physiol 12:171–180Google Scholar
  6. Bingham C, Arbogast B, Cornélissen G, Lee J-K, Halberg F (1982) Inferential statistical methods for estimating and comparing cosinor parameters. Chronobiologia 9:397–439Google Scholar
  7. Box GEP, Jenkins GM, Reinsel GC (1994) Time series analysis: forecasting and control, 3rd edn. Prentice Hall, New YorkGoogle Scholar
  8. Chabot CC, Skinner SJ, Watson WH III (2008) Rhythms of locomotion expressed by Limulus polyphemus, the American horseshoe crab: I. Synchronization by artificial tides. Biol Bull 215:34–45CrossRefGoogle Scholar
  9. Chambon C, Legeay A, Durrieu G, Gonzalez P, Ciret P, Massabuau JC (2007) Influence of the parasite worm Polydora sp. on the behavior of the oyster Crassostrea gigas: a study of the respiratory impact and associated oxidative stress. Mar Biol 152:329–338CrossRefGoogle Scholar
  10. Connor KM, Gracey AY (2011) Circadian cycles are the dominant transcriptional rhythm in the intertidal mussel Mytilus californianus. Proc Natl Acad Sci USA 108:16110–16115CrossRefGoogle Scholar
  11. De la Iglesia HO, Rodriguez EM, Dezi RE (1994) Burrow plugging in the crab Uca uruguayensis and its synchronization with photoperiod and tides. Physiol Behav 55:913–919CrossRefGoogle Scholar
  12. Enright JT (1976a) Resetting a tidal clock: a phase-response curve for Excirolana. In: DeCoursey DJ (ed) Biological rhythms in the marine environment. University of South Carolina Press, Columbia, pp 103–114Google Scholar
  13. Enright JT (1976b) Plasticity in an isopod’s clockworks: shaking shapes form and affects phase and frequency. J Comp Physiol 107:13–37CrossRefGoogle Scholar
  14. Gibson RN (1973) Tidal and circadian activity rhythms in juvenile plaice, Pleuronectes platessa. Mar Biol 22:379–386CrossRefGoogle Scholar
  15. Gibson RN (1992) Tidally-synchronized behaviour in marine fishes. In: Ali MA (ed) Rhythms in fishes. Plenum Press, London, pp 63–82CrossRefGoogle Scholar
  16. Gouthière L, Mauvieux B (2004) Étapes essentielles dans l’analyse des rythmes: qualité des données expérimentales, recherche de périodes par analyses spectrales de principes divers, modélisation. XXXVème Congrès de la Société Francophone de Chronobiologie, Université de Saint Etienne, France du 10 au 12 Juin 2003. Quelques aspects sur la Chronobiologie. Presses Universitaires de Saint EtienneGoogle Scholar
  17. Gouthière L, Claustrat B, Brun J, Mauvieux B (2005a) Complementary methodological steps in the analysis of rhythms: search of periods, modelling. Examples of plasma melatonin and temperature curves. Pathol Biol 53:285–289CrossRefGoogle Scholar
  18. Gouthière L, Mauvieux B, Davenne D, Waterhouse J (2005b) Complementary methodology in the analysis of rhythmic data, using examples from a complex situation, the rhythmicity of temperature in night shift workers. Biol Rhythm Res 36:177–193CrossRefGoogle Scholar
  19. Halberg F (1969) Chronobiology. Annu Rev Physiol 31:675–725CrossRefGoogle Scholar
  20. Hastings JW (2001) Keeping in tune with time: entrainments of circadian rhythms. In: Lebert M, Häder DP (eds) Photomovement. ESP review series, (D-P Häder and B Jori, series editors) BerlinGoogle Scholar
  21. Higuera-Ruiz R, Elorza J (2009) Biometric, microstructural, and high-resolution trace element studies in Crassostrea gigas of Cantabria (Bay of Biscay, Spain): anthropogenic and seasonal influences. Estuar Coast Shelf Sci 82:201–213CrossRefGoogle Scholar
  22. Jenkins GM, Watts DG (1968) Spectral analysis and its applications. Holden Day, San FranciscoGoogle Scholar
  23. Kim WS, Huh HT, Lee JH, Rumohr H, Koh CH (1999) Endogenous circatidal rhythm in the Manila clam Ruditapes philippinarum (Bivalvia: Veneridae). Mar Biol 134:107–112CrossRefGoogle Scholar
  24. Kim WS, Huh HT, Je JG, Han KN (2003) Evidence of two-clock control of endogenous rhythm in the Washington clam, Saxidomus purpuratus. Mar Biol 142:305–309Google Scholar
  25. Klapow LA (1972) Natural and artificial rephasing of a tidal rhythm. J Comp Physiol 79:233–258CrossRefGoogle Scholar
  26. Koukkari WL, Sothern RB (2006) Introducing biological rhythms: a primer on the temporal organization of life, with implications for health, society, reproduction and the natural environment. Springer, New YorkGoogle Scholar
  27. Last KS, Bailhache T, Kramer C, Kyriacou CP, Rosato E, Olive PJW (2009) Tidal, daily, and lunar-day activity cycles in the marine polychaete Nereis virens. Chronobiol Int 26:167–183CrossRefGoogle Scholar
  28. Massabuau JC, Forgue J (1996) A field versus laboratory study of blood oxygen status in normoxic crabs at different temperatures. Can J Zool 74:423–430CrossRefGoogle Scholar
  29. Mat AM, Massabuau JC, Ciret P, Tran D (2012) Evidence for a plastic dual circadian rhythm in the oyster Crassostrea gigas. Chronobiol Int 29:857–867CrossRefGoogle Scholar
  30. Mehta TS, Lewis RD (2000) Quantitative tests of a dual circalunidian clock model for tidal rhythmicity in the sand beach isopod Cirolana cookii. Chronobiol Int 17:29–41CrossRefGoogle Scholar
  31. Morton BS (1977) The tidal rhythm of feeding and digestion in the Pacific oyster, Crassostrea gigas (Thunberg). J Exp Mar Biol Ecol 26:135–151CrossRefGoogle Scholar
  32. Mrosovsky N (1999) Masking: history, definitions, and measurement. Chronobiol Int 16:415–429CrossRefGoogle Scholar
  33. Naylor E (1958) Tidal and diurnal rhythms of locomotory activity in Carcinus maenas (L.). J Exp Biol 35:602–610Google Scholar
  34. Naylor E (2001) Marine animal behaviour in relation to lunar phase. Earth Moon Planets 85–86:291–302Google Scholar
  35. Naylor E (2010) Chronobiology of marine organisms. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  36. Nelson W, Tong YL, Lee JK, Halber F (1979) Methods for cosinor-rhythmometry. Chronobiologia 6:305–323Google Scholar
  37. Palmer JD (1990) The rhythmic lives of crabs. Bioscience 40:352–358CrossRefGoogle Scholar
  38. Palmer JD (1995a) The biological rhythms and clocks of intertidal animals. Oxford University Press, New YorkGoogle Scholar
  39. Palmer JD (1995b) Review of the dual-clock control of tidal rhythms and the hypothesis that the same clock governs both circatidal and circadian rhythms. Chronobiol Int 12:299–310CrossRefGoogle Scholar
  40. Palmer JD (1997) Dueling hypotheses: circatidal versus circalunidian battle basics. Chronobiol Int 14:337–346CrossRefGoogle Scholar
  41. Palmer JD (2000) The clocks controlling the tide-associated rhythms of intertidal animals. BioEssays 22:32–37CrossRefGoogle Scholar
  42. Poulain C, Lorrain A, Flye-Sainte-Marie J, Amice E, Morize E, Paulet YM (2011) An environmentally induced tidal periodicity of microgrowth increment formation in subtidal populations of the clam Ruditapes philippinarum. J Exp Mar Biol Ecol 397:58–64CrossRefGoogle Scholar
  43. Redfern P, Minors D, Waterhouse J (1994) Circadian rhythms, jet lag, and chronobiotics: an overview. Chronobiol Int 11:253–265CrossRefGoogle Scholar
  44. Reid DG, Naylor E (1989) Are there separate circatidal and circadian clocks in the shore crab Carcinus maenas? Mar Ecol Prog Ser 52:1–6CrossRefGoogle Scholar
  45. Reid DG, Naylor E (1990) Entrainment of bimodal circatidal rhythms in the shore crab Carcinus maenas. J Biol Rhythms 5:333–347CrossRefGoogle Scholar
  46. Richardson CA (1988) Exogenous and endogenous rhythms of band formation in the shell of the clam Tapes philippinarum (Adams et Reeve, 1850). J Exp Mar Biol Ecol 122:105–126CrossRefGoogle Scholar
  47. Richardson CA, Crisp DJ, Runham NW, Gruffydd LD (1980) The use of tidal growth bands in the shell of Cerastoderma edule to measure seasonal growth rates under cool temperate and sub-arctic conditions. J Mar Biol Ass UK 60:977–989Google Scholar
  48. Rodriguez G, Naylor E (1972) Behavioural rhythms in littoral prawns. J Mar Biol Assoc UK 52:81–95CrossRefGoogle Scholar
  49. Saigusa M (1992) Phase shift of a tidal rhythm by light-dark cycles in the semi-terrestrial crab Sesarma pictum. Biol Bull 182:257–264CrossRefGoogle Scholar
  50. Saigusa M, Oishi K (2000) Emergence rhythms of subtidal small invertebrates in the subtropical sea: nocturnal patterns and variety in the synchrony with tidal and lunar cycles. Zool Sci 17:241–251CrossRefGoogle Scholar
  51. Saurel C, Gascoigne JC, Palmer MR, Kaiser MJ (2007) In situ mussel feeding behavior in relation to multiple environmental factors: regulation through food concentration and tidal conditions. Limnol Oceanogr 52:1919–1929CrossRefGoogle Scholar
  52. Scargle JD (1982) Studies in astronomical time series analysis. II. Statistical aspects of spectral analysis of unevenly spaced data. Astrophys J 263:835–853CrossRefGoogle Scholar
  53. Sheeba V, Kaneko M, Sharma VK, Holmes TC (2008) The Drosophila circadian pacemaker circuit: pas de deux or tarantella? Crit Rev Biochem Mol Biol 43:37–61CrossRefGoogle Scholar
  54. Southward AJ, Crisp DJ (1965) Activity rhythms of barnacles in relation to respiration and feeding. J Mar Biol Assoc UK 45:161–185CrossRefGoogle Scholar
  55. Taylor AC, Naylor E (1977) Entrainment of the locomotor rhythm of Carcinus by cycles of salinity change. J Mar Biol Assoc UK 57:273–277CrossRefGoogle Scholar
  56. Tessmar-Raible K, Raible F, Arboleda E (2011) Another place, another timer: marine species and the rhythms of life. BioEssays 33:165–172CrossRefGoogle Scholar
  57. Tran D, Ciret P, Ciutat A, Durrieu G, Massabuau JC (2003) Estimation of potential and limits of bivalve closure response to detect contaminants: application to cadmium. Environ Toxicol Chem 22:116–122CrossRefGoogle Scholar
  58. Tran D, Nadau A, Durrieu G, Ciret P, Parisot JP, Massabuau JC (2011) Field chronobiology of a molluscan bivalve: how the Moon and Sun cycles interact to drive Oyster activity Rhythms. Chronobiol Int 28:307–317CrossRefGoogle Scholar
  59. Warman CG, Naylor E (1995) Evidence for multiple, cue-specific circatidal clocks in the shore crab Carcinus maenas. J Exp Mar Biol Ecol 189:93–101CrossRefGoogle Scholar
  60. Webb HM (1976) Interactions of daily and tidal rhythms. In: DeCoursey DJ (ed) Biological rhythms in the marine environment. University of South Carolina Press, Columbia, pp 129–135Google Scholar
  61. Wilcockson D, Zhang L (2008) Circatidal clocks. Curr Biol 18:753–755CrossRefGoogle Scholar
  62. Williams BG (1998) The lack of circadian timing in two intertidal invertebrates and its significance in the circatidal/circalunidian debate. Chronobiol Int 15:205–218CrossRefGoogle Scholar
  63. Williams BG, Naylor E (1969) Synchronization of the locomotor tidal rhythm of Carcinus. J Exp Biol 51:715–725Google Scholar
  64. Williams BG, Pilditch CA (1997) The entrainment of persistent tidal rhythmicity in a filter-feeding bivalve, using cycles of food availability. J Biol Rhythms 12:173–181CrossRefGoogle Scholar
  65. Williams BG, Palmer JD, Hutchinson DN (1992) Comparative studies of tidal rhythms XIII Is a clam clock similar to those of other intertidal animals? Mar Behav Physiol 24:1–14Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Audrey M. Mat
    • 1
  • Jean-Charles Massabuau
    • 1
    • 2
  • Pierre Ciret
    • 1
    • 2
  • Damien Tran
    • 1
    • 2
    Email author
  1. 1.Université BordeauxArcachonFrance
  2. 2.CNRSArcachonFrance

Personalised recommendations