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Temperature regulates the switch between light-synchronized and unsynchronized activity patterns in the subtidal bivalve Pinna nobilis

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The present study reports new knowledge into the biological rhythms of subtidal bivalves using the fan mussel Pinna nobilis as model. The objective was determining which factor(s) provoke the change between two different patterns observed in the annual cycle of this species: P1, characterized by the individuals opening and closing their valves following the presence and absence of ambient light and P2, characterised by a behaviour independent of the presence of light. Magnetoresistive sensors were installed on 8 fan mussels to record gaping activity in laboratory conditions. Different temperature and light treatments were applied. Results showed temperature as the factor modulating the change between behavioural patterns. The individuals switched to P1 when temperature reached 24.5º C. In this pattern, individuals are entrained by light showing a circadian rhythm linked to the daily light treatments. During P2, the circadian rhythm was missing or very weak, contrary to in situ observations. The results of the present study contribute to understand the biology of the species in order to plan new conservation strategies. Furthermore, the observed relationship between temperature and P1 is of interest to develop captive breeding of fan mussels. Altogether, this information is especially relevant in view of the recent mass mortality of P. nobilis occurred in the western Mediterranean.


Pinnidae; Biomonitoring; Daily rhythm; Marine ecology; Biological rhythm; Fan mussel; Climate change

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Andrade, H., Massabuau, J.-C., Cochrane, S., Ciret, P., Tran, D. et al., 2016. High frequency non-invasive (HFNI) bio-sensors as a potential tool for marine monitoring and assessments. Frontiers in Marine Science 3 (187).

Bae, M.-J., Park, Y.-S., 2014. Biological early warning system based on the responses of aquatic organisms to disturbances: A review. Science of the Total Environment 466, 635-649.

Basso, L., Vazquez-Luis, M., Garcia-March, J.R., Deudero, S., Alvarez, E. et al., 2015. The Pen Shell, Pinna nobilis: A review of population status and recommended research priorities in the Mediterranean Sea. Advances in Marine Biology, Vol 71 71, 109-160.

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.

Cabanellas-Reboredo, M., Deudero, S., Alos, J., Valencia, J.M., March, D. et al., 2009. Recruitment of Pinna nobilis (Mollusca: Bivalvia) on artificial structures. Marine Biodiversity Records 2 (e126), 1-5.

Darriba, S., 2017. First haplosporidan parasite reported infecting a member of the Superfamily Pinnoidea (Pinna nobilis) during a mortality event in Alicante (Spain, Western Mediterranean). Journal of invertebrate pathology.

Deudero, S., Grau, A., Vazquez-Luis, M., Alvarez, E., Alomar, C. et al., 2017. Reproductive investment of the pen shell Pinna nobilis (Bivalvia, Pinnidae) Linnaeus, 1758 in Cabrera National Park, Spain. Mediterranean Marine Science 18 (2), 271-284.

Fournier, E., Tran, D., Denison, F., Massabuau, J.C., Garnier-Laplace, J., 2004. Valve closure response to uranium exposure for a freshwater bivalve (Corbicula fluminea): Quantification of the influence of pH. Environmental Toxicology and Chemistry 23 (5), 1108-1114.

Garcia-March, J.R., Jiménez, S., Sanchis, M.A., Monleon, S., Lees, J. et al., 2016. In situ biomonitoring shows seasonal patterns and environmentally mediated gaping activity in the bivalve, Pinna nobilis. Marine Biology 163 (2), 1-12.

Garcia-March, J.R., Marquez-Aliaga, A., Wang, Y.G., Surge, D., Kersting, D.K., 2011. Study of Pinna nobilis growth from inner record: How biased are posterior adductor muscle scars estimates? Journal of Experimental Marine Biology and Ecology 407 (2), 337-344.

Garcia-March, J.R., Solsona, M.A.S., Garcia-Carrascosa, A.M., 2008. Shell gaping behaviour of Pinna nobilis L., 1758: circadian and circalunar rhythms revealed by in situ monitoring. Marine Biology 153 (4), 689-698.

Kersting, D.K., Garcia-March, J.R., 2017. Long-term assessment of recruitment, early stages and population dynamics of the endangered Mediterranean fan mussel Pinna nobilis in the Columbretes Islands (NW Mediterranean). Marine Environmental Research 130, 282-292.

Liao, C.M., Jau, S.F., Lin, C.M., Jou, L.J., Liu, C.W. et al., 2009. Valve movement response of the freshwater clam Corbicula fluminea following exposure to waterborne arsenic. Ecotoxicology 18 (5), 567-576.

Mat, A.M., Massabuau, J.C., Ciret, P., Tran, D., 2012. Evidence for a plastic dual circadian rhythm in the oyster Crassostrea gigas. Chronobiology International 29(7), 857-867.

Ortmann, C., Grieshaber, M.K., 2003. Energy metabolism and valve closure behaviour in the Asian clam Corbicula fluminea. Journal of Experimental Biology 206 (22), 4167-4178.

Palmer, J.D., 2000. The clocks controlling the tide-associated rhythms of intertidal animals. Bioessays 22 (1), 32-37.

Rensing, L., Meyer-Grahle, U., Ruoff, P., 2001. Biological timing and the clock metaphor: Oscillatory and hourglass mechanisms. Chronobiology International 18 (3), 329-369.

Robson, A.A., De Leaniz, C.G., Wilson, R.P., Halsey, L.G., 2010a. Behavioural adaptations of mussels to varying levels of food availability and predation risk. Journal of Molluscan Studies 76, 348-353.

Robson, A.A., de Leaniz, C.G., Wilson, R.P., Halsey, L.G., 2010b. Effect of anthropogenic feeding regimes on activity rhythms of laboratory mussels exposed to natural light. Hydrobiologia 655 (1), 197-204.

Rodland, D.L., Schone, B.R., Baier, S., Zhang, Z.J., Dreyer, W. et al., 2009. Changes in gape frequency, siphon activity and thermal response in the freshwater bivalves Anodonta cygnea and Margaritifera falcata. Journal of Molluscan Studies 75, 51-57.

Schwartzmann, C., Durrieu, G., Sow, M., Ciret, P., Lazareth, C.E. et al., 2011. In situ giant clam growth rate behavior in relation to temperature: A one-year coupled study of high-frequency noninvasive valvometry and sclerochronology. Limnology and Oceanography 56 (5), 1940-1951.

Sluyts, H., VanHoof, F., Cornet, A., Paulussen, J., 1996. A dynamic new alarm system for use in biological early warning systems. Environmental Toxicology and Chemistry 15 (8), 1317-1323.

Sobrino-Figueroa, A., Caceres-Martinez, C., 2009. Alterations of valve closing behavior in juvenile Catarina scallops (Argopecten ventricosus Sowerby, 1842) exposed to toxic metals. Ecotoxicology 18 (8), 983-987.

Sow, M., Durrieu, G., Briollais, L., Ciret, P., Massabuau, J.C., 2011. Water quality assessment by means of HFNI valvometry and high-frequency data modeling. Environmental Monitoring and Assessment 182 (1-4), 155-170.

Tran, D., Fournier, E., Durrieu, G., Massabuau, J.-C., 2007. Inorganic mercury detection by valve closure response in the freshwater clam Corbicula fluminea: Integration of time and water metal concentration changes. Environmental Toxicology and Chemistry 26 (7), 1545-1551.

Tran, D., Nadau, A., Durrieu, G., Ciret, P., Parisot, J.P. et al., 2011. Field chronobiology of a molluscan bivalve: How the moon and sun cycles interact to drive oyster activity rhythms. Chronobiology International 28 (4), 307-317.

Trigos, S., 2016. Estudio de la ecofiología y ensayo de cultivo de la nacra Pinna nobilis Linnaeus, 1758. Tesis Título Doctoral, Universidad Católica de Valencia San Vicente mártir, Valencia, España.

Trigos, S., Garcia-March, J.R., Vicente, N., Tena, J., Torres, J., 2014. Utilization of muddy detritus as organic matter source by the fan mussel Pinna nobilis. Mediterranean Marine Science 15 (3), 667-674.

Vaze, K.M., Sharma, V.K., 2013. On the adaptive significance of circadian clocks for their owners. Chronobiology International 30 (4), 413-433.

Vázquez-Luis, M., Álvarez, E., Barrajón, A., García-March, J.R., Grau, A. et al. 2017. S.O.S. Pinna nobilis: a mass mortality rvent in western Mediterranean Sea. Frontiers in Marine Science 4 (220).

Williams, B.G., Pilditch, C.A., 1997. The entrainment of persistent tidal rhythmicity in a filter-feeding bivalve using cycles of food availability. Journal of Biological Rhythms 12 (2), 173-181.


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