Advertisement

Marine Biology

, Volume 156, Issue 3, pp 355–372 | Cite as

Feeding current characteristics of three morphologically different bivalve suspension feeders, Crassostrea gigas, Mytilus edulis and Cerastoderma edule, in relation to food competition

  • Karin TroostEmail author
  • Eize J. Stamhuis
  • Luca A. van Duren
  • Wim J. Wolff
Original Paper

Abstract

Introduced Pacific oysters (Crassostrea gigas) have shown rapid expansion in the Oosterschelde estuary, while stocks of native bivalves declined slightly or remained stable. This indicates that they might have an advantage over native bivalve filter feeders. Hence, at the scale of individual bivalves, we studied whether this advantage occurs in optimizing food intake over native bivalves. We investigated feeding current characteristics, in which potential differences may ultimately lead to a differential food intake. We compared feeding currents of the invasive epibenthic non-siphonate Pacific oyster to those of two native bivalve suspension feeders: the epibenthic siphonate blue mussel Mytilus edulis and the endobenthic siphonate common cockle Cerastoderma edule. Inhalant flow fields were studied empirically using digital particle image velocimetry and particle tracking velocimetry. Exhalant jet speeds were modelled for a range of exhalant-aperture cross-sectional areas as determined in the laboratory and a range of filtration rates derived from literature. Significant differences were found in inhalant and exhalant current velocities and properties of the inhalant flow field (acceleration and distance of influence). At comparable body weight, inhalant current velocities were lower in C. gigas than in the other species. Modelled exhalant jets were higher in C. gigas, but oriented horizontally instead of vertically as in the other species. Despite these significant differences and apparent morphological differences between the three species, absolute differences in feeding current characteristics were small and are not expected to lead to significant differences in feeding efficiency.

Keywords

Bivalve Shell Length Pacific Oyster Particle Tracking Velocimetry Oyster Reef 

Notes

Acknowledgments

We are grateful to D. B. Blok, E. Brummelhuis, A. van Gool, J. J. de Wiljes and the crews of MS ‘Valk’ and MS ‘Krukel’ for their practical assistance. We thank P. Kamermans and anonymous reviewers for providing valuable comments on the manuscript. This project was funded by the Netherlands Organization for Scientific Research—Earth and Life Sciences (NWO-ALW) (project number 812.03.003). The experiments comply with the current Dutch laws.

Open Access

This article is distributed under the terms of the Creative Commons Attribution Noncommercial License which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.

References

  1. Anayiotos AS, Perry GJ, Myers JG, Green DW, Fan PH, Nanda NC (1995) A numerical and experimental investigation of the flow acceleration region proximal to an orifice. Ultrasound Med Biol 21:501–516. doi: https://doi.org/10.1016/0301-5629(94)00141-Y CrossRefGoogle Scholar
  2. Anayiotos AS, Elmahdi AM, Newman BE, Perry GJ, Costa F, Agrawal D, Agrawal G, DeCarvalho CT, Nanda NC (1997) An improved flow evaluation scheme in orifices of different aspect ratios. Ultrasound Med Biol 23:231–244. doi: https://doi.org/10.1016/S0301-5629(96)00228-1 CrossRefGoogle Scholar
  3. André C, Jonsson PR, Lindegarth M (1993) Predation on settling bivalve larvae by benthic suspension feeders: the role of hydrodynamics and larval behaviour. Mar Ecol Prog Ser 97:183–192. doi: https://doi.org/10.3354/meps097183 CrossRefGoogle Scholar
  4. Bayne BL (1976) Marine mussels: their ecology and physiology. Cambridge University Press, CambridgeGoogle Scholar
  5. Bougrier S, Geairon P, Deslous-Paoli JM, Bacher C, Jonquières G (1995) Allometric relationships and effects of temperature on clearance and oxygen consumption rates of Crassostrea gigas (Thunberg). Aquaculture 134:143–154. doi: https://doi.org/10.1016/0044-8486(95)00036-2 CrossRefGoogle Scholar
  6. Butman CA, Fréchette M, Geyer WR, Starczak VR (1994) Flume experiments on food supply to the blue mussel Mytilus edulis L. as a function of boundary-layer flow. Limnol Oceanogr 39:1755–1768CrossRefGoogle Scholar
  7. Ciutat A, Widdows J, Pope ND (2007) Effect of Cerastoderma edule density on near-bed hydrodynamics and stability of cohesive muddy sediments. J Exp Mar Biol Ecol 346:114–126. doi: https://doi.org/10.1016/j.jembe.2007.03.005 CrossRefGoogle Scholar
  8. Dame RF (1996) Ecology of marine bivalves: an ecosystem approach. CRC Press, Boca RatonCrossRefGoogle Scholar
  9. Dankers N, Meijboom A, de Jong M, Dijkman E, Cremer J, Fey F, Smaal A, Craeymeersch J, Brummelhuis E, Steenbergen J, Baars D (2006) De ontwikkeling van de Japanse Oester in Nederland. Wageningen IMARES, Report C040/06, YersekeGoogle Scholar
  10. Dolmer P (2000) Algal concentration profiles above mussel beds. J Sea Res 43:113–119. doi: https://doi.org/10.1016/S1385-1101(00)00005-8 CrossRefGoogle Scholar
  11. Drinkwaard AC (1999a) History of cupped oyster in european coastal waters. Aquac Eur 15:7–14 +41Google Scholar
  12. Drinkwaard AC (1999b) Introductions and developments of oysters in the North Sea area: a review. Helgol Meersunters 52:301–308. doi: https://doi.org/10.1007/BF02908904 CrossRefGoogle Scholar
  13. Dupuy C, Vaquer A, Lam-Höai T, Rougier C, Mazouni N, Lautier J, Collos Y, Le Gall S (2000) Feeding rate of the oyster Crassostrea gigas in a natural planktonic community of the Mediterranean Thau Lagoon. Mar Ecol Prog Ser 205:171–184. doi: https://doi.org/10.3354/meps205171 CrossRefGoogle Scholar
  14. Ertman SC, Jumars PA (1988) Effects of bivalve siphonal currents on the settlement of inert particles and larvae. J Mar Res 46:797–813. doi: https://doi.org/10.1357/002224088785113342 CrossRefGoogle Scholar
  15. Famme P, Riisgård HU, Jørgensen CB (1986) On direct measurement of pumping rates in the mussel Mytilus edulis. Mar Biol (Berl) 92:323–327. doi: https://doi.org/10.1007/BF00392672 CrossRefGoogle Scholar
  16. Fernandes S, Sobral P, Van Duren L (2007) Clearance rates of Cerastoderma edule under increasing current velocity. Cont Shelf Res 27:1104–1115. doi: https://doi.org/10.1016/j.csr.2006.08.010 CrossRefGoogle Scholar
  17. Foster-Smith RL (1975) The effect of concentration of suspension on the filtration rates and pseudofaecal production for Mytilus edulis L., Cerastoderma edule (L.) and Venerupis pullastra (Montagu). J Exp Mar Biol Ecol 17:1–22. doi: https://doi.org/10.1016/0022-0981(75)90075-1 CrossRefGoogle Scholar
  18. Frank DM, Ward JE, Shumway SE, Holohan BA, Gray C (2008) Application of particle image velocimetry to the study of suspension feeding in marine invertebrates. Mar Freshw Behav Physiol 41:1–18. doi: https://doi.org/10.1080/10236240801896207 CrossRefGoogle Scholar
  19. Fréchette M, Butman CA, Geyer WR (1989) The importance of boundary-layer flows in supplying phytoplankton to the benthic suspension feeder, Mytilus edulis L. Limnol Oceanogr 34:19–36CrossRefGoogle Scholar
  20. Gerdes D (1983) The Pacific oyster Crassostrea gigas. Part I. Feeding behaviour of larvae and adults. Aquaculture 31:195–219. doi: https://doi.org/10.1016/0044-8486(83)90313-7 CrossRefGoogle Scholar
  21. Geurts van Kessel AJM, Kater BJ, Prins TC (2003) Veranderende draagkracht van de Oosterschelde voor kokkels. National Institute for Coastal and Marine Management (RIKZ) & Netherlands Institute for Fisheries Research (RIVO), Report RIKZ/2003.043/RIVO C062/03, Middelburg, the NetherlandsGoogle Scholar
  22. Gosling E (2003) Bivalve molluscs. Biology, ecology and culture. Blackwell, OxfordCrossRefGoogle Scholar
  23. Green S, Visser AW, Titelman J, Kiørboe T (2003) Escape responses of copepod nauplii in the flow field of the blue mussel, Mytilus edulis. Mar Biol (Berl) 142:727–733CrossRefGoogle Scholar
  24. Hawkins AJS, Fang JG, Pascoe PL, Zhang JH, Zhang XL, Zhu MY (2001) Modelling short-term responsive adjustments in particle clearance rate among bivalve suspension-feeders: separate unimodal effects of seston volume and composition in the scallop Chlamys farreri. J Exp Mar Biol Ecol 262:61–73CrossRefGoogle Scholar
  25. Helm MM, Bourne N, Lovatelli A (2004) Hatchery culture of bivalves—a practical manual. In: Lovatelli A (ed) FAO fisheries technical paper, Rome, p 177Google Scholar
  26. Hinsch KD (1993) Particle image velocimetry. In: Sirohi RS (ed) Speckle metrology. Marcel Dekker, New York, pp 235–324Google Scholar
  27. Jones HD, Richards OG, Southern TA (1992) Gill dimensions, water pumping rate and body size in the mussel Mytilus edulis L. J Exp Mar Biol Ecol 155:213–237. doi: https://doi.org/10.1016/0022-0981(92)90064-H CrossRefGoogle Scholar
  28. Jonsson PR, Petersen JK, Karlsson Ö, Loo L-O, Nilsson S (2005) Particle depletion above experimental bivalve beds: in situ measurements and numerical modelling of bivalve filtration in the boundary layer. Limnol Oceanogr 50:1989–1998CrossRefGoogle Scholar
  29. Kamermans P (1993) Food limitation in cockles (Cerastoderma edule (L.)): influences of location on tidal flat and of nearby presence of mussel beds. Neth J Sea Res 31:71–81. doi: https://doi.org/10.1016/0077-7579(93)90019-O CrossRefGoogle Scholar
  30. Kiørboe T, Visser AW (1999) Predator and prey perception in copepods due to hydromechanical signals. Mar Ecol Prog Ser 179:81–95. doi: https://doi.org/10.3354/meps179081 CrossRefGoogle Scholar
  31. Kiørboe T, Saiz E, Visser AW (1999) Hydrodynamic signal perception in the copepod Acartia tonsa. Mar Ecol Prog Ser 179:97–111. doi: https://doi.org/10.3354/meps179097 CrossRefGoogle Scholar
  32. Larsen PS, Riisgård HU (1997) Biomixing generated by benthic filter feeders: a diffusion model for near-bottom phytoplankton depletion. J Sea Res 37:81–90. doi: https://doi.org/10.1016/S1385-1101(97)00009-9 CrossRefGoogle Scholar
  33. Lassen J, Kortegård M, Riisgård HU, Friedrichs M, Graf G, Larsen PS (2006) Down-mixing of phytoplankton above filter-feeding mussels—interplay between water flow and biomixing. Mar Ecol Prog Ser 314:77–88. doi: https://doi.org/10.3354/meps314077 CrossRefGoogle Scholar
  34. Lehane C, Davenport J (2002) Ingestion of mesozooplankton by three species of bivalve; Mytilus edulis, Cerastoderma edule and Aequipecten opercularis. J Mar Biol Assoc U K 82:615–619. doi: https://doi.org/10.1017/S0025315402005957 CrossRefGoogle Scholar
  35. Maar M, Nielsen TG, Bolding K, Burchard H, Visser AW (2007) Grazing effects of blue mussel Mytilus edulis on the pelagic food web under different turbulence conditions. Mar Ecol Prog Ser 339:199–213. doi: https://doi.org/10.3354/meps339199 CrossRefGoogle Scholar
  36. Maas Geesteranus RA (1942) On the formation of banks by Mytilus edulis L. Arch Neerl Zool 6:283–326CrossRefGoogle Scholar
  37. Møhlenberg F, Riisgård HU (1978) Efficiency of particle retention in 13 species of suspension feeding bivalves. Ophelia 17:239–246CrossRefGoogle Scholar
  38. Møhlenberg F, Riisgård HU (1979) Filtration rate, using a new indirect technique, in thirteen species of suspension-feeding bivalves. Mar Biol (Berl) 54:143–147. doi: https://doi.org/10.1007/BF00386593 CrossRefGoogle Scholar
  39. Newell CR, Wildish DJ, MacDonald BA (2001) The effects of velocity and seston concentration on the exhalant siphon area, valve gape and filtration rate of the mussel Mytilus edulis. J Exp Mar Biol Ecol 262:91–111. doi: https://doi.org/10.1016/S0022-0981(01)00285-4 CrossRefGoogle Scholar
  40. Nikora V, Green MO, Thrush SF, Hume TM, Goring D (2002) Structure of the internal boundary layer over a patch of pinnid bivalves (Atrina zelandica) in an estuary. J Mar Res 60:121–150. doi: https://doi.org/10.1357/002224002762341276 CrossRefGoogle Scholar
  41. Norušis MJ (2008) SPSS 16.0 statistical procedures companion. Prentice Hall, Upper Saddle River. ISBN-13: 978-0-13-606139-7Google Scholar
  42. O’Riordan CA, Monismith SG, Koseff JR (1995) The effect of bivalve excurrent jet dynamics on mass transfer in a benthic boundary layer. Limnol Oceanogr 40:330–344CrossRefGoogle Scholar
  43. Petersen JK, Bougrier S, Smaal AC, Garen P, Robert S, Larsen JEN, Brummelhuis EBM (2004) Intercalibration of mussel Mytilus edulis clearance rate measurements. Mar Ecol Prog Ser 267:187–194. doi: https://doi.org/10.3354/meps267187 CrossRefGoogle Scholar
  44. Porter ET, Cornwell JC, Sanford LP (2004) Effect of oysters Crassostrea virginica and bottom shear velocity on benthic-pelagic coupling and estuarine water quality. Mar Ecol Prog Ser 271:61–75. doi: https://doi.org/10.3354/meps271061 CrossRefGoogle Scholar
  45. Prins TC, Smaal AC, Pouwer AJ, Dankers N (1996) Filtration and resuspension of particulate matter and phytoplankton on an intertidal mussel bed in the Oosterschelde estuary (SW Netherlands). Mar Ecol Prog Ser 142:121–134. doi: https://doi.org/10.3354/meps142121 CrossRefGoogle Scholar
  46. Riisgård HU (1977) On measurements of the filtration rates of suspension feeding bivalves in a flow system. Ophelia 16:167–173CrossRefGoogle Scholar
  47. Riisgård HU (2001) On measurement of filtration rates in bivalves—the stony road to reliable data: review and interpretation. Mar Ecol Prog Ser 211:275–291. doi: https://doi.org/10.3354/meps211275 CrossRefGoogle Scholar
  48. Riisgård HU, Larsen PS (2000) Comparative ecophysiology of active zoobenthic filter feeding, essence of current knowledge. J Sea Res 44:169–193. doi: https://doi.org/10.1016/S1385-1101(00)00054-X CrossRefGoogle Scholar
  49. Riisgård HU, Randløv A (1981) Energy budgets, growth and filtration rates in Mytilus edulis at different algal concentrations. Mar Biol (Berl) 61:227–234. doi: https://doi.org/10.1007/BF00386664 CrossRefGoogle Scholar
  50. Riisgård HU, Kittner C, Seerup DF (2003) Regulation of opening state and filtration rate in filter-feeding bivalves (Cardium edule, Mytilus edulis, Mya arenaria) in response to low algal concentrations. J Exp Mar Biol Ecol 284:105–127. doi: https://doi.org/10.1016/S0022-0981(02)00496-3 CrossRefGoogle Scholar
  51. Singarajah KV (1969) Escape reactions of zooplankton: the avoidance of a pursuing siphon tube. J Exp Mar Biol Ecol 3:171–178. doi: https://doi.org/10.1016/0022-0981(69)90015-X CrossRefGoogle Scholar
  52. Singarajah KV (1975) Escape reactions of zooplankton: effects of light and turbulence. J Mar Biol Assoc U K 55:627–639CrossRefGoogle Scholar
  53. Smaal AC, Twisk F (1997) Filtration and absorption of Phaecystis cf. globosa by the mussel Mytilus edulis L. J Exp Mar Biol Ecol 209:33–46. doi: https://doi.org/10.1016/S0022-0981(96)02695-0 CrossRefGoogle Scholar
  54. Spedding GR, Rignot EJM (1993) Performance analysis and application of grid interpolation techniques for fluid flows. Exp Fluids 15:417–430. doi: https://doi.org/10.1007/BF00191784 CrossRefGoogle Scholar
  55. Stamhuis EJ (2006) Basics and principles of particle image velocimetry (PIV) for mapping biogenic and biologically relevant flows. Aquat Ecol 40:463–479. doi: https://doi.org/10.1007/s10452-005-6567-z CrossRefGoogle Scholar
  56. Stamhuis EJ, Videler JJ, Duren LAV, Müller UK (2002) Applying digital particle image velocimetry to animal-generated flows: Traps, hurdles and cures in mapping steady and unsteady flows in Re regimes between 10–2 and 105. Exp Fluids 33:801–813CrossRefGoogle Scholar
  57. Tamburri MN, Zimmer RK, Zimmer CA (2007) Mechanisms reconciling gregarious larval settlement with adult cannibalism. Ecol Monogr 77:255–268. doi: https://doi.org/10.1890/06-1074 CrossRefGoogle Scholar
  58. Titelman J, Kiørboe T (2003) Predator avoidance by nauplii. Mar Ecol Prog Ser 247:137–149. doi: https://doi.org/10.3354/meps247137 CrossRefGoogle Scholar
  59. Tritton DJ (1988) Physical fluid dynamics. Oxford University Press, New YorkGoogle Scholar
  60. Troost K, Kamermans P, Smaal AC, Wolff WJ (submitted) The effect of bivalve filter feeders on bivalve larval abundance in the Oosterschelde estuary (SW Netherlands) at different spatial scales. Submitted for publication in the Journal of Sea ResearchGoogle Scholar
  61. Vahl O (1972) Porosity of the gill, oxygen consumption and pumping rate in Cardium edule (L.) (Bivalvia). Ophelia 10:109–118CrossRefGoogle Scholar
  62. Van Duren L, Herman PMJ, Sandee AJJ, Heip CHR (2006) Effects of mussel filtering activity on boundary layer structure. J Sea Res 55:3–14. doi: https://doi.org/10.1016/j.seares.2005.08.001 CrossRefGoogle Scholar
  63. Visser AW (2001) Hydromechanical signals in the plankton. Mar Ecol Prog Ser 222:1–24. doi: https://doi.org/10.3354/meps222001 CrossRefGoogle Scholar
  64. Walne PR (1972) The influence of current speed, body size and water temperature on the filtration rate of five species of bivalves. J Mar Biol Assoc U K 52:345–374CrossRefGoogle Scholar
  65. Widdows J, Navarro JM (2007) Influence of current speed on clearance rate, algal cell depletion in the water column and resuspension of biodeposits of cockles (Cerastoderma edule). J Exp Mar Biol Ecol 343:44–51. doi: https://doi.org/10.1016/j.jembe.2006.11.011 CrossRefGoogle Scholar
  66. Wildish D, Kristmanson D (1997) Benthic suspension feeders and flow. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  67. Wiles PJ, Van Duren LA, Häse C, Larsen J, Simpson JH (2006) Stratification and mixing in the Limfjorden in relation to mussel culture. J Mar Syst 60:129–143. doi: https://doi.org/10.1016/j.jmarsys.2005.09.009 CrossRefGoogle Scholar
  68. Winter JE (1973) The filtration rate of Mytilus edulis and its dependence on algal concentration, measured by a continuous automatic recording apparatus. Mar Biol (Berl) 22:137–328. doi: https://doi.org/10.1007/BF00391388 CrossRefGoogle Scholar
  69. Wolff WJ, Reise K (2002) Oyster imports as a vector for the introduction of alien species into northern and western European coastal waters. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe. Distribution, impacts and management. Kluwer, Dordrecht, pp 193–205CrossRefGoogle Scholar
  70. Wong WH, Levinton JS (2004) Culture of the blue mussel Mytilus edulis (Linnaeus, 1758) fed both phytoplankton and zooplankton: a microcosm experiment. Aquacult Res 35:965–969. doi: https://doi.org/10.1111/j.1365-2109.2004.01107.x CrossRefGoogle Scholar
  71. Wong WH, Levinton JS (2006) The trophic linkage between zooplankton and benthic suspension feeders: direct evidence from analyses of bivalve faecal pellets. Mar Biol (Berl) 148:799–805. doi: https://doi.org/10.1007/s00227-005-0096-0 CrossRefGoogle Scholar
  72. Wright LD, Friedrichs CT, Hepworth DA (1997) Effects of benthic biology on bottom boundary layer processes, dry Tortugas Bank, Florida Keys. Geo-Mar Lett 17:291–298. doi: https://doi.org/10.1007/s003670050040 CrossRefGoogle Scholar

Copyright information

© The Author(s) 2008

Open AccessThis is an open access article distributed under the terms of the Creative Commons Attribution Noncommercial License (https://doi.org/creativecommons.org/licenses/by-nc/2.0), which permits any noncommercial use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.

Authors and Affiliations

  • Karin Troost
    • 1
    • 3
    Email author
  • Eize J. Stamhuis
    • 2
  • Luca A. van Duren
    • 4
  • Wim J. Wolff
    • 1
  1. 1.Marine Benthic Ecology and EvolutionUniversity of GroningenHarenThe Netherlands
  2. 2.Ocean EcosystemsUniversity of GroningenHarenThe Netherlands
  3. 3.Wageningen IMARES, YersekeYersekeThe Netherlands
  4. 4.DELTARESDelftThe Netherlands

Personalised recommendations