Marine Biology

, Volume 152, Issue 6, pp 1293–1307 | Cite as

Relationship between filtration activity and food availability in the Mediterranean mussel Mytilus galloprovincialis

  • Olivier Maire
  • Jean-Michel Amouroux
  • Jean-Claude Duchêne
  • Antoine Grémare
Research Article


The filtration activity of the Mediterranean mussel, Mytilus galloprovincialis, was assessed under different concentrations and compositions of seston by using a new automated image acquisition and analysis system. This approach allowed for frequent and simultaneous measurements of valve gape and exhalant siphon area. Filtration rates were measured through clearance measurements whereas pumping rates were measured using hot-film probes. The average filtration rate (17.5 l g h−1 DW−1 for a 0.36 g DW mussel) recorded during the present study was higher than those available for Mytilus edulis when standardized to flesh dry weight but almost equivalent (17.5 l h−1 g DW−1 for a 53 mm shell length mussel) to those rates when standardized to shell length. Immediately after the addition of algal cells (Isochrysis galbana; 4.5 μm in size), valve gape, exhalant siphon area and filtration rate increased quickly as mussels reached their maximum filtration activity. These three parameters then gradually decreased until complete closure of the shell. The algal cell concentration inducing this transition was close to 800 cells ml−1 and 0.5 μg Chl a l−1. When algal concentration was maintained above this threshold by successive algal additions, both valve gape and exhalant siphon area remained maximal. Temporal changes in the exhalant siphon area were continuous as opposed to those of valve gape. Therefore, despite the significant correlation between these two parameters, valves and siphon were sometimes dissociated due to a reduction of the area or even a closure of the exhalant siphon while the valves remained open. The velocity of exhaled water tended to be constant irrespective of exhalant siphon area and thus pumping rates were a linear function of exhalant siphon area. Consequently, reductions in exhalant siphon area and pumping rate were almost similar in M. galloprovincialis. Our results thus clearly support the hypothesis that exhalant siphon area constitutes a better proxy of pumping rate than valve gape as already suggested for Mytilus edulis. Finally, the high filtration rates measured during the present study together with the high concentrations of inorganic matter (> 40 mg DW l−1) requested to alter those rates suggest that the studied mussels were well adapted to oligotrophic waters featuring strong hydrodynamism and frequent sediment resuspension events.


Mytilus galloprovincialis Exhalant siphon area Valve gape Filtration rate Pumping rate Food availability Image analysis 



The authors gratefully acknowledge Martin Desmalades, Gilles Vétion, Béatrice Rivière and Karine Escoubeyrou for their help during the experiments. Olivier Maire was supported by a grant from the French Ministry of Education, Research and Technology. This work was in partial fulfillment of the doctoral thesis of Olivier Maire at the University Pierre et Marie Curie. This study complied with the legal requirements in France.


  1. Amouroux JM (1976) Ethology and filtration of Mactra glauca (Born). Vie Mileu 26:21–30Google Scholar
  2. Amouroux JM, Revault d’Allones M, Rouault C (1975) Rate of flow of the filtration-current in Lamellibranch molluscs. Vie Milieu 25:339–346Google Scholar
  3. Bayne BL (1998) The physiology of suspension feeding by bivalve molluscs: an introduction to the Plymouth “TROPHEE” workshop. J Exp Mar Biol Ecol 219:1–19CrossRefGoogle Scholar
  4. Bayne BL (2001) Reply to comment by H.U. Riisgård. Ophelia 54:211CrossRefGoogle Scholar
  5. Bayne BL, Hawkins AJS (1992) Ecological and physiological aspects of herbivory in benthic suspension-feeding molluscs. In: Hawkins JDM, Price SJ (eds) Plant-animal interactions in the marine benthos. Systematics Association, Special. Clarendon Press, Oxford, pp 265–288Google Scholar
  6. Bayne BL, Iglesias JIP, Hawkins AJS, Navarro E, Heral M, Deslous-Paoli JM (1993) Feeding behaviour of the mussel, Mytilus edulis: responses to variations in quantity and organic content of the seston. J Mar Biol Assoc UK 73:813–829CrossRefGoogle Scholar
  7. Bodin N, Burgeot T, Stanisière JY, Bocquené G, Menard D, Minier C, Boutet I, Amat A, Cherel Y, Budzinski H (2004) Seasonal variations of a battery of biomarkers and physiological indices for the mussel Mytilus galloprovincialis transplanted into the northwest Mediterranean Sea. Comp Biochem Physiol C 138:411–427Google Scholar
  8. Charles F, Lopez-legentil S, Grémare A, Amouroux JM, Desmalades M, Vétion G, Escoubeyrou K (2005) Does sediment resuspension by storms affect the fate of polychlorobiphenyls (PCBs) in the benthic food chain? Interactions between changes in POM characteristics, adsorption and absorption by the mussel Mytilus galloprovincialis. Cont Shelf Res 25:2533–2553CrossRefGoogle Scholar
  9. Clausen I, Riisgård HU (1996) Growth, filtration and respiration in the mussel Mytilus edulis: No evidence for physiological regulation of the filter-pump to nutritional needs. Mar Ecol Prog Ser 141:37–45CrossRefGoogle Scholar
  10. Cloern JE (1982) Does the benthos control phytoplankton biomass in south San Francisco bay? Mar Ecol Prog Ser 9:191–202CrossRefGoogle Scholar
  11. Coughlan J (1969) The estimation of filtering rate from the clearance suspensions. Mar Biol 8:356–358CrossRefGoogle Scholar
  12. Curtis TM, Williamson R, Depledge MH (2000) Simultaneous, long-term monitoring of valve and cardiac activity in the blue mussel Mytilus edulis exposed to copper. Mar Biol 136:837–846CrossRefGoogle Scholar
  13. Dare PJ (1976) Settlement, growth and production of the mussel, Mytilus edulis L., in Morecambe Bay, England. Fish Invest Ser II 28, No. 1, London, p 1–25Google Scholar
  14. Davenport J (1979) The isolation response of mussels (Mytilus edulis L.) exposed to falling sea-water conentrations. J Mar Biol Assoc UK 59:123–132CrossRefGoogle Scholar
  15. Davenport J, Manley A (1978) The detection of heightened sea-water copper concentrations by the mussel Mytilus edulis. J Mar Biol Assoc UK 58:843–850CrossRefGoogle Scholar
  16. Dolmer P (2000a) Algal concentration profiles above mussel beds. J Sea Res 43:113–119CrossRefGoogle Scholar
  17. Dolmer P (2000b) Feeding activity of mussels Mytilus edulis related to near-bed currents and phytoplankton biomass. J Sea Res 44:221–231CrossRefGoogle Scholar
  18. Duchêne JC (2004) Early recognition of sediment during settlement of Eupolymnia nebulosa (Polychaeta: Terebellidae) larvae. Mar Biol 145:79–85CrossRefGoogle Scholar
  19. Duchêne JC, Nozais C (1994) Light influence on larval emission and vertical swimming in the terebellid worm Eupolymnia nebulosa (Montagu, 1818). Mem Mus Natl Hist Nat Zool 162:405–412Google Scholar
  20. Duchêne JC, Queiroga H (2001) Use of an intelligent CCD camera for the study of endogenous vertical migration rhythms in first zoeae of the crab Carcinus maenas. Mar Biol 139:901–909CrossRefGoogle Scholar
  21. Duchêne JC, Jordana E, Charles F, Grémare A, Amouroux JM (2000) Experimental study of filtration activity in Ditrupa arietina (Annelida Polychaeta) using an automated image analysis system. Oceanol Acta 23:805–817CrossRefGoogle Scholar
  22. Famme P, Riisgård HU, Jørgensen CB (1986) On direct measurement of pumping rates in the mussel Mytilus edulis. Mar Biol 92:323–327CrossRefGoogle Scholar
  23. Ferré B, Guizien K, Durrieu de Madron X, Palanques A, Guillen J, Grémare A (2005) Fine-grained sediment dynamics during a strong storm event in the inner-shelf of the Gulf of Lions (NW Mediterranean). Cont Shelf Res 25:2410–2427CrossRefGoogle Scholar
  24. Foster-Smith RL (1976) Some mechanisms for the control of pumping activity in bivalves. Mar Behav Physiol 4:41–59CrossRefGoogle Scholar
  25. Grémare A (1988) Feeding, tube-building and particle size selection in the terebellid polychaete Eupolymnia nebulosa. Mar Biol 97:243–252CrossRefGoogle Scholar
  26. Grémare A, Amouroux JM, Chaabeni Y, Charles F (1998) Experimental study of the effect of kaolinite on the ingestion and the absorption of monospecific suspensions of Pavlova lutheri by the filter-feeding bivalve Venus verrucosa. Vie Milieu 48:295–307Google Scholar
  27. Grémare A, Amouroux JM, Cauwet G, Charles F, Courties C, De Bovée F, Dinet A, Devenon JL, Durrieu De Madron X, Ferré B, Fraunié P, Joux F, Lantoine F, Lebaron P (2003) The effects of a strong winter storm on physical and biological variables at a shelf site in the Mediterranean. Oceanol Acta 26:407–419CrossRefGoogle Scholar
  28. Grémare A, Duchêne JC, Rosenberg R, David E, Desmalades M (2004) Feeding behaviour and functional response of Abra ovata and A. nitida compared by image analysis. Mar Ecol Prog Ser 267:195–208CrossRefGoogle Scholar
  29. Ham KD, Peterson MJ (1994) Effect of fluctuating low-level chlorine concentrations on valve-movement behavior of the Asiatic clam (Corbicula fluminea). Environ Toxicol Chem 13:493–498CrossRefGoogle Scholar
  30. Hatcher A, Grant J, Schofield B (1994) Effects of suspended mussel culture (Mytilus spp.) on sedimentation, benthic respiration and sediment nutrient dynamics in a coastal bay. Mar Ecol Prog Ser 115:219–235CrossRefGoogle Scholar
  31. Higgins PJ (1980) Effects of food availability on the valve movements and feeding behavior of juvenile Crassostrea virginica (Gmelin). I. Valve movements and periodic activity. J Exp Mar Biol Ecol 45:229–244CrossRefGoogle Scholar
  32. Hily C (1991) Is the activity of benthic suspension feeders a factor controlling water quality in the Bay of Brest? Mar Ecol Prog Ser 69:2179–2188CrossRefGoogle Scholar
  33. Hollertz K, Duchêne JC (2001) Burrowing behaviour and sediment reworking in the heart urchin Brissopsis lyrifera Forbes (Spatangoida). Mar Biol 139:951–957CrossRefGoogle Scholar
  34. Iglesias JIP, Urrutia MB, Navarro E, Alvarez-Jorna P, Larretxea X, Bougrier S, Héral M (1996) Variability of feeding processes in the cockle Cerastoderma edule (L.) in response to changes in seston concentration and composition. J Exp Mar Biol Ecol 197:121–143CrossRefGoogle Scholar
  35. Jacques G (1970) Aspects quantitatifs du phytoplancton de la région de Banyuls-sur-Mer (Golfe du Lion). IV. Biomasse et production, 1965–1969. Vie milieu 20:279–316Google Scholar
  36. Jordana E, Duchêne JC, Charles F, Grémare A, Amouroux JM (2000) Experimental study of suspension-feeding activity in the serpulid polychaete Ditrupa arietina. J Exp Mar Biol Ecol 252:57–74CrossRefGoogle Scholar
  37. Jørgensen CB (1996) Bivalve filter feeding revisited. Mar Ecol Prog Ser 142:287–302CrossRefGoogle Scholar
  38. Jørgensen CB, Ockelmann K (1991) Beat frequency of lateral cilia in intact filter feeding bivalves: Effect of temperature. Ophelia 33:67–70CrossRefGoogle Scholar
  39. Jørgensen CB, Larsen PS, Møhlenberg F, Riisgård HU (1988) The mussel pump: properties and modelling. Mar Ecol Prog Ser 45:205–216CrossRefGoogle Scholar
  40. Kiørboe T, Møhlenberg F (1981) Particle selection in suspension-seeding bivalves. Mar Ecol Prog Ser 5:291–296CrossRefGoogle Scholar
  41. Kiørboe T, Møhlenberg F, Nohr O (1980) Feeding, particle selection and carbon absorption in Mytilus edulis in different mixtures of algae and resuspended bottom material. Ophelia 19:193–205CrossRefGoogle Scholar
  42. Kittner C, Riisgård HU (2005) Effect of temperature on filtration rate in the mussel Mytilus edulis: No evidence for temperature compensation. Mar Ecol Prog Ser 305:147–152CrossRefGoogle Scholar
  43. Kramer KJM, Jenner HA, de Zwart D (1989) The valve movement response of mussels: a tool in biological monitoring. Hydrobiologia 188:433–443CrossRefGoogle Scholar
  44. Lantoine F (1995) Caractérisation et distribution des différentes populations du picoplancton (picoeucaryotes, Synechococcus spp., Prochlorococcus spp.) dans diverses situations trophiques (Atlantique tropical, Golfe du Lion). PhD dissertation, University Pierre et Marie Curie, ParisGoogle Scholar
  45. Maire O, Duchêne JC, Rosenberg R, Braga de Mendonça Jr J, Grémare A (2006) Effects of food availability on sediment reworking in Abra ovata and Abra nitida. Mar Ecol Prog Ser 319:135–153CrossRefGoogle Scholar
  46. Manley AR (1983) The effects of copper on the behavior, respiration, filtration and ventilation activity of Mytilus edulis. J Mar Biol Ass UK 63:205–222CrossRefGoogle Scholar
  47. Mølhenberg F, Riisgård HU (1978) Efficiency of particle retention in 13 species of suspension feeding bivalves. Ophelia 17(2):239–246CrossRefGoogle Scholar
  48. Mølhenberg F, Riisgård HU (1979) Filtration rate, using a new indirect technique, in thirteen species of suspension-feeding bivalves. Mar Biol 54:143–147CrossRefGoogle Scholar
  49. Neveux J, Lantoine F (1993) Spectrofluorometric assay of chlorophylls and phaeopigments using the least squares approximation technique. Deep Sea Res Part I 40:1747–1765CrossRefGoogle Scholar
  50. Newell CR, Campbell DE, Gallagher SM (1998) Development of the mussel aquaculture lease site model MUSMOD: a field program to calibrate model formulations. J Exp Mar Biol Ecol 219:143–169CrossRefGoogle Scholar
  51. Newell CR, Wildish DJ, MacDonald BA (2001) The effects of velocity and seston concentration on the exhalant siphon area, valve gapee and filtration rate of the mussel Mytilus edulis. J Exp Mar Biol Ecol 262:91–111CrossRefGoogle Scholar
  52. Newell CR, Pilskaln CH, Robinson SM, MacDonald BA (2005) The contribution of marine snow to the particle food supply of the benthic suspension feeder, Mytilus edulis. J Exp Mar Biol Ecol 321:109–124CrossRefGoogle Scholar
  53. Noren F, Haamer J, Lindahl O (1999) Changes in the plankton community passing a Mytilus edulis mussel bed. Mar Ecol Prog Ser 191:187–194CrossRefGoogle Scholar
  54. Officer CB, Smayda TJ, Mann R (1982) Benthic filter feeding: a natural eutrophication control. Mar Ecol Prog Ser 9:203–210CrossRefGoogle Scholar
  55. Orban E, Di Lena G, Nevigato T, Casini I, Marzetti A, Caproni R (2002) Seasonal changes in meat content, condition index and chemical composition of mussels (Mytilus galloprovincialis) cultured in two different Italian sites. Food Chem 77:57–65CrossRefGoogle Scholar
  56. Pearson TH, Rosenberg R (1987) Feast and famine: structuring factors in marine benthic communities. In: Gee JHR, Giller PS (eds) Organization of commutinies, past and present. Proc 27th Symp Br Ecol Soc, Aberystwyth. Blackwell, London, pp 373–395Google Scholar
  57. Pouvreau S, Jonquières G, Buestel D (1999) Filtration by the pearl oyster, Pinctada margaritifera, under conditions of low seston load and small particle size in a tropical lagoon habitat. Aquaculture 176:295–314CrossRefGoogle Scholar
  58. Pouvreau S, Bodoy A, Buestel D (2000) In situ suspension feeding behaviour of the pearl oyster, Pinctada margaritifera: combined effects of body size and weather-related seston composition. Aquaculture 181:91–113CrossRefGoogle Scholar
  59. Prins TC, Dankers N, Smaal AC (1994) Seasonal variation in the filtration rates of a semi-natural mussel bed in relation to seston composition. J Exp Mar Biol Ecol 176:69–86CrossRefGoogle Scholar
  60. Riisgård HU (1991) Filtration rate and growth in the blue mussel, Mytilus edulis Linnaeus, 1758: dependence on algal concentration. J Shellfish Res 10:29–35Google Scholar
  61. Riisgård HU (2001a) Physiological regulation versus autonomous filtration in filter feeding bivalves: starting points for progress. Ophelia 54:193–209CrossRefGoogle Scholar
  62. Riisgård HU (2001b) On measurement of filtration rates in bivalves—the stony road to reliable data: review and interpretation. Mar Ecol Prog Ser 211:275–291CrossRefGoogle Scholar
  63. Riisgård HU, Møhlenberg F (1979) An improved automatic recording apparatus for determining the filtration rate of Mytilus edulis as a function of size and algal concentration. Mar Biol 52:61–67CrossRefGoogle Scholar
  64. Riisgård HU, Randløv A (1981) Energy budget, growth and filtration rates in Mytilus edulis at different algal concentrations. Mar Biol 61:227–234CrossRefGoogle Scholar
  65. Riisgård HU, Kamermans P (2001) Switching between deposit and suspension feeding in coastal zoobenthos. In: Reise K (ed) Ecological comparisons of sedimentary shores. Springer, Berlin, pp 73–101CrossRefGoogle Scholar
  66. Riisgård HU, Larsen PS (2005) Water pumping and analysis of flow in burrowing zoobenthos: an overview. Aquat Ecol 39:237–258CrossRefGoogle Scholar
  67. Riisgård HU, Grémare A, Amouroux JM, Charles F, Vétion G, Rosenberg R, Nielsen C (2002) Comparative study of water-processing in two ciliary filter-feeding polychaetes (Ditrupa arietina and Euchone papillosa) from two different habitats. Mar Ecol Prog Ser 229:113–126CrossRefGoogle Scholar
  68. Riisgård HU, Kittner C, Seerup DF (2003) Regulation of opening state and filtration rate in filter-feeding bivalves (Cardium edule, Mytilus edulis, Mya arena) in response to low algal concentration. J Exp Mar Biol Ecol 284:105–127CrossRefGoogle Scholar
  69. Sejr MK, Petersen JK, Jensen KT, Rysgaard S (2004) Effects of food concentration on clearance rate and energy budget of the Arctic bivalve Hiatella arctica (L) at subzero temperature. J Exp Mar Biol Ecol 311:171–183CrossRefGoogle Scholar
  70. Staehr PA, Henriksen P, Markager S (2002) Photoacclimation of four marine phytoplankton species to irradiance and nutrient availability. Mar Ecol Prog Ser 238:47–59CrossRefGoogle Scholar
  71. Tran D, Fournier E, Durrieu G, Massabuau JC (2003) Copper detection in the Asiatic clam Corbicula fluminea: optimum valve closure response. Aquat Toxicol 65:317–327CrossRefGoogle Scholar
  72. Urban ER, Kirchman DL (1992) Effect of kaolinite clay on the feeding activity of the eastern oyster Crassostrea virginica (Gmelin). J Exp Mar Biol Ecol 160:47–60CrossRefGoogle Scholar
  73. Vogel S (1981) Life in moving fluids. Princetown University Press, 352 ppGoogle Scholar
  74. Wildish DJ, Miyares MP (1990) Filtration rate of blue mussels as a function of flow velocity: preliminary experiments. J Exp Mar Biol Ecol 142:213–219CrossRefGoogle Scholar
  75. Wong WH (1999) Feeding behaviour of the green mussel, Perna viridis: responses to variation in seston quantity and quality. J Exp Mar Biol Ecol 236:191–207CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Olivier Maire
    • 1
    • 2
  • Jean-Michel Amouroux
    • 1
    • 2
  • Jean-Claude Duchêne
    • 1
    • 2
  • Antoine Grémare
    • 1
    • 2
  1. 1.Laboratoire d’Océanographie Biologique de BanyulsUniversité Pierre et Marie Curie-Paris6, UMR7621Banyuls-sur-MerFrance
  2. 2.CNRS, UMR7621Banyuls-sur-MerFrance

Personalised recommendations