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In situ long-term monitoring of cardiac activity of two bivalve species from the White Sea, the blue mussel Mytilus edulis and horse mussel Modiolus modiolus

Published online by Cambridge University Press:  24 October 2018

Igor N. Bakhmet ,
Andrey Sazhin ,
Nikolay Maximovich  and
Dmitry Ekimov
Igor N. Bakhmet*
Affiliation:
Institute of Biology, Karelian Research Centre of RAS, 186005 Petrozavodsk, Russia
Andrey Sazhin
Affiliation:
Shirshov Institute of Oceanology, Russian Academy of Sciences, Moscow, Russia
Nikolay Maximovich
Affiliation:
Saint-Petersburg State University, Faculty of Biology, Saint Petersburg, Russia
Dmitry Ekimov
Affiliation:
Department of Information Measuring Systems and Physical Electronics, Petrozavodsk State University, Lenin str. 33, 185910, Petrozavodsk, Russia
*
Author for correspondence: Igor N. Bakhmet, E-mail: [email protected]
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Abstract

Cardiac activity of two White Sea Bivalvia species – Mytilus edulis and Modiolus modiolus – was monitored in situ for one full calendar year every 4 days. During the year, we also assessed the temperature and salinity of the ambient seawater (at intervals of 1 min), measured phytoplankton concentration (every 4 days) and checked the reproductive status of the molluscs (every 2 weeks). Our field study showed a significant linear correlation between the molluscs’ heart rates and the temperature of the ambient seawater. However, during specific periods of the year, we observed that phytoplankton composition or reproductive status became the dominant influence over cardiac activity. Phytoplankton concentrations were generally found to be low throughout the entire year, but two peak periods of drastically elevated phytoplankton concentration were found (April and May), and during April the peak heart rates of the blue mussels significantly increased. Spawning time took place in the middle of June, and at this time the cardiac activity of the molluscs did not change in spite of a 4°C temperature increase in the ambient seawater. Monitoring of the heart rates of the real intertidal blue mussels (animals located at the middle part of intertidal) revealed periodic fluctuations in cardiac activity that correlated strongly with tidal fluctuations. Cardiac activity in M. modiolus was significantly lower than in M. edulis from 9 May to 25 November. On the basis of our data, we concluded that the molluscs’ cardiac activity can serve not only as an indicator of the animals’ physiological conditions, but also as an indicator of changes in ambient factors.

Keywords

Cardiac activityin situModiolus modiolusmonitoringMytilus edulisphytoplanktonreproductive statusWhite Sea
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 4 , June 2019 , pp. 833 - 840
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

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References

Antsulevich, AE, Maximovich, NV and Vuorinen, I (1999) Population structure, growth and reproduction of the common mussel (Mytilus edulis L.) of the Island of Seili (South-eastern Gulf of Bothnia, Sw, Finland). Boreal Environment Research 4, 3–19.Google Scholar
Bakhmet, IN (2017) Cardiac activity and oxygen consumption of blue mussels (Mytilus edulis) from the White Sea in relation to body mass, ambient temperature and food availability. Polar Biology 40, 1959–1964.Google Scholar
Bayne, BL (1973) Physiological changes in Mytilus edulis L. induced by temperature and nutritive stress. Journal of the Marine Biological Association of the United Kingdom 53, 39–58.Google Scholar
Bayne, BL (2004) Phenotypic flexibility and physiological tradeoffs in the feeding and growth of marine bivalve mollusks. Integrative and Comparative Biology 44, 425–432.Google Scholar
Bayne, BL and Widdows, J (1978) Physiological ecology of 2 populations of Mytilus edulis L. Oecologia 37, 137–162.Google Scholar
Вауnе, ВL, Widdows, J and Newell, RI (1978) Physiological Measurements on Estuarine Bivalve Molluscs in the Field. Oxford: Pergamon Press.Google Scholar
Campbell, HA, Fraser, KPP, Peck, LS, Bishop, CM and Egginton, S (2007) Life in the fast lane: the free-ranging activity, heart rate and metabolism of an Antarctic fish tracked in temperate waters. Journal of Experimental Marine Biology and Ecology 349, 142–151.Google Scholar
Chipperfield, PN (1953) Observation on the breeding and settlement of Mytilus edulis (L.) in British waters. Journal of the Marine Biological Association of the United Kingdom 32, 449–476.Google Scholar
Coleman, N and Trueman, ER (1971) The effect of aerial exposure on the activity of the mussels Mytilus edulis L. and Modiolus modiolus (L.). Journal of Experimental Marine Biology and Ecology 7, 295–304.Google Scholar
Dahlhoff, EP and Menge, BA (1996) Influence of phytoplankton concentration and wave exposure on the ecophysiology of Mytilus californianus. Marine Ecology Progress Series 144, 97–107.Google Scholar
De Pirro, M, Santini, G and Chelazzi, G (1999) Cardiac responses to salinity variations in two differently zoned Mediterranean limpets. Journal of Comparative Physiology B 169, 501–506.Google Scholar
Depledge, MH and Andersen, BB (1990) A computer-aided physiological monitoring system for continuous, long-term recording of cardiac activity in selected invertebrates. Comparative Biochemistry and Physiology 96A, 473–477.Google Scholar
DeVooys, CGN (1976) The influence of temperature and time of year on the oxygen uptake of the sea mussel Mytilus edulis. Marine Biology 36, 25–30.Google Scholar
Diamond, JM (1986) Overview: Laboratory experiments, field experiments, and natural experiments. In Diamond, J and Case, TJ (eds), Community Ecology. New York, NY: Harper and Row, pp. 3–22.Google Scholar
Green, JA (2011) The heart rate method for estimating metabolic rate: review and recommendations. Comparative Biochemistry and Physiology A 158, 287–304.Google Scholar
Hatcher, A, Grant, J and Schofield, B (1997) Seasonal changes in the metabolism of cultured mussels (Mytilus edulis l.) from a Nova Scotian inlet: the effects of winter ice cover and nutritive stress. Journal of Experimental Marine Biology and Ecology 217, 63–78.Google Scholar
Humason, GL (1967) Animal Tissue Techniques, 2nd Edn. San Francisco, CA: W.H. Freeman Co.Google Scholar
Jansen, JM, Pronker, AE, Kube, S, Sokolowski, A, Sola, JC, Marquiegui, MA, Schiedek, D, Bonga, SW, Wolowicz, M and Hummel, H (2007) Geographic and seasonal patterns and limits on the adaptive response to temperature of European Mytilus spp. and Macoma balthica populations. Oecologia 154, 23–34.Google Scholar
Jeffrey, SW, Wright, SW, Zapata, M (2011) Microalgal classes and their signature pigments. In Roy, S, Llewellyn, CA, Egeland, ES and Johnsen, G. (ed.), Phytoplankton Pigments: Characterization, Chemotaxonomy and Applications in Oceanography. Cambridge: Cambridge University Press, pp. 3–77.Google Scholar
Jeong, HJ, Yoo, YD, Kim, JS, Seong, KA, Nam Kang, NS and Kim, TH (2010) Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Science Journal 45, 65–91.Google Scholar
Jokumsen, A and Fyhn, HJ (1982) The influence of aerial exposure upon respiratory and osmotic properties of haemolymph from two intertidal mussels, Mytilus edulis L. and Modiolus modiolus L. Journal of Experimental Marine Biology and Ecology 61, 189–203.Google Scholar
Jones, HD (1983) The circulatory systems of gastropods and bivalves. In Saleuddin, ASM and Wilbur, KM (eds), The Mollusca, vol. 5. New York, NY: Academic Press, pp. 189–238.Google Scholar
Joosse, J and Geraerts, WPM (1983) Endocrinology. In Saleuddin, ASM (ed.), The Mollusca, vol. 4. Physiology. Part I. London: Academic Press, pp. 317–385.Google Scholar
Kamenos, NA, Calosi, P and Moore, PG (2006) Substratum-mediated heart rate responses of an invertebrate to predation threat. Animal Behaviour 71, 809–813.Google Scholar
Kholodkevich, SV, Ivanov, AV, Kuznetsova, TV, Kurakin, AS, Kornienko, EL, Pan'kov, SL and Khalatov, AN (2009) Ultradian rhythms in cardiac activity of Bivalvia. Doklady Biological Sciences, Physiology 426, 216–218.Google Scholar
Lesser, MP and Kruse, VA (2004) Seasonal temperature compensation in the horse mussel, Modiolus modiolus: metabolic enzymes, oxidative stress and heat shock proteins. Comparative Biochemistry and Physiology A 137, 495–504.Google Scholar
Lesser, MP, Witman, JD and Sebens, KP (1994) Effects of flow and seston availability on scope for growth of benthic suspension-feeding invertebrates from the Gulf of Maine. Biological Bulletin 187, 319–335.Google Scholar
Loo, LO (1992) Filtration, assimilation, respiration and growth of Mytilus edulis L. at low temperatures. Ophelia 35, 123–131.Google Scholar
Lowe, GA and Trueman, ER (1972) The heart and water flow rates of Mya arenaria (Bivalvia: Mollusca) at different metabolic levels. Comparative Biochemistry and Physiology A 41, 487–494.Google Scholar
MacDonald, BA and Ward, JE (2009) Feeding activity of scallops and mussels measured simultaneously in the field: repeated measures sampling and implications for modelling. Journal of Experimental Marine Biology and Ecology 371, 42–50.Google Scholar
Marshall, DJ and McQuaid, CD (1992) Relationship between heart rate and oxygen consumption in the intertidal limpets Patella granularis and Siphonaria oculus. Comparative Biochemistry and Physiology A 103, 297–300.Google Scholar
Maximovich, NV (1985) Reproductive cycle of M. edulis in the Inlet of Chupa. In Lukanin, VV (ed.), Investigations of Mussels of the White Sea. Leningrad: ZIN AN SSSR, pp. 22–35. [In Russian.]Google Scholar
Melzner, F, Gobel, S, Langenbuch, M, Gutowska, MA, Portner, HO and Lucassen, M (2009) Swimming performance in Atlantic Cod (Gadus morhua) following long-term (4–12 months) acclimation to elevated seawater P(CO2). Aquatic Toxicology 92, 30–37.Google Scholar
Menden-Deuer, S and Lessard, EJ (2000) Carbon to volume relationship for dinoflagellates, diatoms and other protists plankton. Limnology and Oceanography 45, 569–579.Google Scholar
Naumov, AD (2006) Bivalve Molluscs of the White Sea. The Experience of Ecology-Faunistic Analyses. St Petersburg: ZIN. [In Russian.]Google Scholar
Navarro, JM and Thompson, RJ (1996) Physiological energetics of the horse mussel Modiolus modiolus in a cold ocean environment. Marine Ecology Progress Series 138, 135–148.Google Scholar
Newell, RIE and Thompson, RJ (1984) Reduced clearance rates associated with spawning in the mussel, Mytilus edulis (L.) (Bivalvia, Mytilidae). Marine Biology Letters 5, 21–33.Google Scholar
Petes, LE, Menge, BA and Harris, AL (2008) Intertidal mussels exhibit energetic trade-offs between reproduction and stress resistance. Ecological Monographs 78, 387–402.Google Scholar
Portaluppi, F, Smolensky, MH and Touitou, Y (2010) Ethics and methods for biological rhythm research on animals and human beings. Chronobiology International 27, 1911–1929.Google Scholar
Rizzatti, ACS and Romero, SMB (2001) Heart rate and body weight alterations in juvenile specimens of the tropical land snail Megalobulimus sanctipauli during dormancy. Brazilian Journal of Medical and Biological Research 34, 959–967.Google Scholar
Romero, SMB and Hoffmann, A (1991) Heart rate and behavioral patterns of Megalobulimus sanctipauli (Mollusca, Gastropoda, Pulmonata). Brazilian Journal of Medical and Biological Research 24, 223–227.Google Scholar
Romero, SMB and Hoffmann, A (1996) Heart rate and temperature in the snail Megalobulimus sanctipauli: role of the cardiac nerve. Canadian Journal of Physiology and Pharmacology 74, 1362–1365.Google Scholar
Rovero, F, Hughes, RN and Chelazzi, G (1999) Cardiac and behavioural responses of mussels to risk of predation by dogwhelks. Animal Behaviour 58, 707–714.Google Scholar
Santini, G, De Pirro, M and Chelazzi, G (1999) In situ and laboratory assessment of heart rate in a Mediterranean limpet using a noninvasive technique. Physiological and Biochemical Zoology 72, 198–204.Google Scholar
Santini, G, Williams, GA and Chelazzi, G (2000) Assessment of factors affecting heart rate of the limpet Patella vulgata on the natural shore. Marine Biology 137, 291–296.Google Scholar
Schweinitz, EH and Lutz, RA (1976) Larval development of the northern horse mussel Modiolus modiolus (L.), including a comparison with the larvae of Mytilus edulis L. as an aid in planktonic identification. Biological Bulletin 150, 348–360.Google Scholar
Seifert, AW and Chapman, LJ (2006) Respiratory allocation and standard rate of metabolism in the African lungfish, Protopterus aethiopicus. Comparative Biochemistry and Physiology A 143, 142–148.Google Scholar
Smaal, AC, Vonck, A and Bakker, M (1997) Seasonal variation in physiological energetic of Mytilus edulis and Cerastoderma edule of different size classes. Journal of the Marine Biological Association of the United Kingdom 77, 817–838.Google Scholar
Sokal, RR and Rohlf, FJ (1995) Biometry, 3rd Edn. New York, NY: W.H. Freeman.Google Scholar
Somero, GN (2002) Thermal physiology and vertical zonation of intertidal animals: optima, limits, and costs of living. Integrative and Comparative Biology 42, 780–789.Google Scholar
Sommerville, BA (1975) Factors affecting the heart activity and blood pressure of the swan mussel Anodonta cygnea. Journal of Experimental Biology 62, 341–355.Google Scholar
Stoecker, DK (1999) Mixotrophy among dinoflagellates. Journal of Eukaryotic Microbiology 46, 397–401.Google Scholar
Sukhotin, AA (1989) Size and weight characteristics and the ratio of parts of the body of the White Sea mussel Mytilus edulis L. in suspended culture and in natural habitats. Proceeding of the Zoological Institute, USSR AS 92, 45–55. [In Russian.]Google Scholar
Thompson, RJ (1984) The reproductive cycle and physiological ecology of mussel Mytilus edulis in subarctic, non-estuarine environment. Marine Biology 79, 277–288.Google Scholar
Toro, JE, Thompson, RJ and Innes, DJ (2002) Reproductive isolation and reproductive output in two sympatric mussel species (Mytilus edulis, M. trossulus) and their hybrids from Newfoundland. Marine Biology 141, 897–909.Google Scholar
Underwood, AJ and Peterson, CH (1988) Towards an ecological framework for investigating pollution. Marine Ecology Progress Series 46, 227–234.Google Scholar