Abstract
Gaping activity of bivalve molluscs is closely related to physiological process such as breathing, nutrition, responses to environmental stimuli and follows rhythmic cycles in many species. Although the alternation of Sun and Moon is the major entraining agent for the daily living clock-driven rhythms, cyclic extrinsic environmental factors can also modulate gaping activity. Therefore, laboratory experimental conditions can alter the natural behaviour of bivalves, hindering the interpretation of observations. Many features of Pinna nobilis physiology are poorly known, gaping activity not being an exception. To reduce the knowledge gap on this regard, we performed a study on the species gaping activity. The research was designed to be carried out in situ, in order to avoid the interference of laboratory conditions in the observations. To this end, we designed and fabricated a new electronic system composed by a data logger and a sensor formed by multiple reed switches activated by a single magnet. The system is autonomous and can record gaping activity of subtidal bivalves in potentially any type of subtidal environment. Furthermore, it requires little framework for the installation. With this system, we monitored 10 individuals in periods ranging between 3 and 21 days, for up to a total of 98 days. The records have shown that far from being all day open, as previously suggested, P. nobilis follows marked circadian and circalunar rhythms of gaping activity. Individuals usually close the valves during night, sometimes for more than 12 h. The repetition of patterns observed made it possible to distinguish between two main behaviours: (1) night-closing related with sunset and (2) night-opening related with the Moon visible in the sky with the disc illuminated more than 50%. Another two less common trends were also observed: (3) day-closing and (4) night-opening with no visible Moon.
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References
Abell PI, Amegashitsi L, Ochumba PBO (1996) The shells of Etheria elliptica as recorders of seasonality at Lake Victoria. Palaeogeogr Palaeoclimatol Palaeoecol 119(3–4):215–219
Bayne B (1998) The physiology of suspension feeding bivalve molluscs: an introduction to the Plymouth ‘TROPHEE’ workshop. J Exp Mar Biol Ecol 219:1–19
Borcherding J (2006) Ten years of practical experience with the Dreissena-Monitor, a biological early warning system for continuous water quality monitoring. Hydrobiologia 556:417–426
Borcherding J, Volpers M (1994) The Dreissena-monitor—1st results on the application of this biological early warning system in the continuous monitoring of water quality. Water Sci Technol 29:199–201
Burnett LE (1988) Physiological responses to air exposure: acid-base balance and the role of branchial water stores. Am Zool 28(1):125–135
Butler A, Vicente N, De Gaulejac B (1993) Ecology of de Pterioid bivalves Pinna bicolor Gmelin and Pinna nobilis L. Life 3(1–2):37–45
Catsiki VA, Catsikieri CH (1992) Presence of chromium in P. nobilis collected from a polluted area. Fresenius Environ Bull 1:644–649
Cheung SG, Shin PKS (2005) Size effects of suspended particles on gill damage in green-lipped mussel Perna viridis. Mar Pollut Bull 51(8–12):801–810
Coco G, Thrush SF, Green MO, Hewitt JE (2006) Feedbacks between bivalve density, flow, and suspended sediment concentration on patch stable states. Ecology 87(11):2862–2870
Czihak G, Dierl W (1961) Pinna nobilis L. eine prëparationsanleitung. Gustav Fisher Verlag, Stuttgart
De Gaulejac B, Vicente N (1990) Ecologie de Pinna nobilis (L.) mollusque bivalve sur les côtes de Corse. Essais de transplantation et expériences en milieu contrôlé. Haliotis 10:83–100
De Gaulejac B, Medioni E, Vicente N (2003) Essais de captage de Pinna nobilis et autres mollusques sur les côtes méditerranéennes françaises. Mem Inst Oceanogr Paul Ricard 9:57–62
Demers A, Guderley H (1994) Acclimatization to intertidal conditions modifies the physiological response to prolonged air exposure in Mytilus edulis. Mar Biol 118(1):115–122
Duffet-Smith P (1988) Practical astronomy with your calculator, 3rd edn. Cambridge University Press, Cambridge
Ellis J, Cummings V, Hewitt J, Thrush S, Norkko A (2002) Determining effects of suspended sediment on condition of a suspension feeding bivalve (Atrina zelandica): results of a survey, a laboratory experiment and a field transplant experiment. J Exp Mar Biol Ecol 267:147–174
El-Shenawy NS (2004) Heavy-metal and microbial depuration of the clam Ruditapes decussatus and its effect on bivalve behavior and physiology. Environ Toxicol 19(2):143–153
Englund V, Heino M (1994) Valve movement of Anodonta anatina and Unio tumidus (Bivalvia, Unionidae) in a eutrophic lake. Ann Zool Fenn 31(2):257–262
Englund V, Heino M (1996) Valve movement of the freshwater mussel Anodonta anatina: a reciprocal transplant experiment between lake and river. Hydrobiologia 328:49–56
García-March JR (2003) Contribution to the knowledge of the status of Pinna nobilis (L.) 1758 in Spanish coasts. Mem Inst Oceanogr Paul Ricard 9:29–41
García-March JR, Garcia-Carrascosa AM, Perez-Rojas L (2007a) Influence of hydrodynamic forces on population structure of Pinna nobilis L., 1758 (Mollusca: Bivalvia): the critical combination of drag force, water depth shell size and orientation. J Exp Mar Biol Ecol 342:202–212
García-March JR, García-Carrascosa AM, Peña AL, Wang YG (2007b) Study of the population structure, mortality and growth of Pinna nobilis in two populations located at different depths in Moraira bay. Mar Biol 150:861–871
Gibson RN (2003) Go with the flow: tidal migration in marine animals. Hydrobiologia 503(1–3):153–161
Hand SC, Hardewig I (1996) Downregulation of cellular metabolism during environmental stress: mechanisms and implications. Annu Rev Physiol 58:539–63
Higginns PJ (1980) Effects of food availability on the valve movements and feeding behaviour of juvenile Crassostrea virginica (Gmelin) I. Valve movements and periodic activity. J Exp Mar Biol Ecol 45:229–244
Jørgensen CB (1990) Bivalve filter feeding: hydrodynamics, bioenergetics, physiology and ecology. Olsen & Olsen, Fredensborg
Katsanevakis S (2005) Population ecology of the endangered fan mussel Pinna nobilis in a marine lake. Endang Species Res 1:1–9
Kim WS, Huh H-T, Je J-G, Han K-N (2003) Evidence of two-clock control of endogenous rhythm in the Washington clam, Saxidomus purpuratus. Mar Biol 142(2):305–309
Markich SJ, Brown PL, Jeffree RA, Lim RP (2000) Valve movement responses of Velesunio angasi (Bivalvia: Hyriidae) to manganese and uranium: An exception to the free ion activity model. Aquat Toxicol 51(2):155–175
Mcmahon RF (1988) Respiratory response to periodic emergence in intertidal Molluscs. Am Zool 28(1):97–114
Montenbruck O, Pfleger T (2000) Astronomy on the personal computer, 4th edn. Springer, Berlin
Newell RC, Branch GM (1980) The influence of temperature on the maintenance of metabolic energy balance in marine invertebrates. Adv Mar Biol 17:329–396
Ortmann C, Grieshaber MK (2003) Energy metabolism and valve closure behaviour in the Asian clam Corbicula Fluminea. J Exp Biol 206:4167–4178
Palmer JD (2000) The clocks controlling the tide-associated rhythms of intertidal animals. BioEssays 22(1):32–37
Richardson CA, Kennedy H, Duarte CM, Kennedy DP, Proud SV (1999) Age and growth of the fan mussel Pinna nobilis from south-east Spanish Mediterranean seagrass (Posidonia oceanica) meadows. Mar Biol 133:205–212
Richardson CA, Peharda M, Kennedy H, Kennedy P, Onofri V (2004) Age, growth rate and season of recruitment of Pinna nobilis (L) in the Croatian Adriatic determined from Mg:Ca and Sr:Ca shell profiles. J Exp Mar Biol Ecol 299:1–16
Riisgard H (2001) The stony road to reliable filtration rate measurements in bivalves: a reply. Mar Ecol Prog Ser 215:307–310
Riva A (2003) Approche méthodologique de quelques paramètres bioénergétiques chez Pinna nobilis. Mem Inst Oceanogr Paul Ricard 9:91–101
Rodland DL, Schöne R, Helama S, Nielsen JK, Baier S (2006) A clockwork mollusc: ultradian rhythms in bivalve activity revealed by digital photography. J Exp Mar Biol Ecol 334(2):316–323
Siletic T, Peharda M (2003) Population study of the fan shell Pinna nobilis L. in Malo and Veliko Jezero of the Mljet National Park (Adriatic Sea). Sci Mar 67(1):91–98
Sluyts H, Van Hoof F, Cornet A, Paulussen J (1996) A dynamic new alarm system for use in biological early warning systems. Environ Toxicol Chem 15(8):1317–1323
Sobral P, Widdows J (1997) Influence of hypoxia and anoxia on the physiological responses of the clam Ruditapes decussatus from southern Portugal. Mar Biol 127:455–461
Templado J, Calvo M, Garvía A, Luque AA, Maldonado M, Moro L (2004) Guía de invertebrados y peces Marinos protegidos por la legislación nacional e internacional. MMA–CSIC, Madrid
Vicente N (1990) Estudio ecológico y protección del molusco lamelibranquio Pinna nobilis L. 1758 en la costa mediterránea. Iberus 9(1–2):269–279
Vicente N, Moreteau JC (1991) Statut de Pinna nobilis L. en Mediterranee (mollusque eulamellibranche). In: Boudouresque CF, Avon M, Gravez V (eds) Les Espèces Marines à Protéger en Méditerranée. Gis Posidonie publication, Marseille, pp 159–168
Widdows J, Shick JM (1985) Physiological responses of Mytilus edulis and Cardium edule to aerial exposure. Mar Biol 85:217–232
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(2):173–181
Wilson R, Reuter P, Wahl M (2005) Muscling in on mussels: new insights into bivalve behaviour using vertebrate remote-sensing technology. Mar Biol 147:1165–1172
Zavodnik D, Hrs-Brenko M, Legac M (1991) Synopsis on the fan shell Pinna nobilis L. in the eastern Adriatic sea. In: Boudouresque CF, Avon M, Gravez V (eds) Les Espèces Marines à Protéger en Méditerranée. Gis Posidonie publication, Marseille, pp 169–178
Acknowledgments
Wave data was provided by “Puertos del Estado”, the Spanish State Port Authority, and illumination of the Moon was obtained from the Astronomical Applications Department of the United States Naval Observatory. We are grateful to Miguel Ángel García, Celia Agustí and Vicente Tasso for their help during the field surveys. The contribution of M. Goodstadt for the correction of the final version of the manuscript has been very valuable. These experiments complied with the current environmental laws of Spain and European Union.
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Communicated by J.-M. Gili.
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García-March, J.R., Sanchís Solsona, M.Á. & García-Carrascosa, A.M. Shell gaping behaviour of Pinna nobilis L., 1758: circadian and circalunar rhythms revealed by in situ monitoring. Mar Biol 153, 689–698 (2008). https://doi.org/10.1007/s00227-007-0842-6
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DOI: https://doi.org/10.1007/s00227-007-0842-6