Biological Invasions

, 12:15 | Cite as

Recently established Crassostrea-reefs versus native Mytilus-beds: differences in ecosystem engineering affects the macrofaunal communities (Wadden Sea of Lower Saxony, southern German Bight)

  • Alexandra Markert
  • Achim Wehrmann
  • Ingrid Kröncke
Original Paper


Since 1998 the non-indigenous Pacific oyster Crassostrea gigas (Thunberg 1793) has been invading the Wadden Sea of Lower Saxony, southern German Bight. C. gigas settles predominantly on intertidal Mytilus-beds (M. edulis L.) and subsequently create rigid reef-like structures. Both bivalve species are ecosystem engineers in sedimentary tidal flats. They provide hard substrate for sessile species, mobile organisms find refuge within the habitat matrix of dense suspension feeders, and biodeposits enrich the sediments with organic matter. The transformation of Mytilus-beds into Crassostrea-reefs gives rise to the question whether the invader may affect the native community. We investigated two parts of a changing bivalve bed in the backbarrier area of the island of Juist in March 2005. One part was still dominated by M. edulis whereas the other part was already densely colonized by C. gigas. Crassostrea-reefs compensate for the conceivable loss of Mytilus-beds in the intertidal of the Wadden Sea by replacing the ecological function of M. edulis. There was no indication of a suppression of indigenous species. This even applied to M. edulis, which persisted at the site invaded by C. gigas. The associated macrofaunal community showed increased species richness, abundance, biomass, and diversity in the Crassostrea-reef. The latter particularly favored sessile species like anthozoans, hydrozoans, and barnacles. Higher abundance and biomass for vagile epizoic species like the shore crab Carcinus maenas and the periwinkle Littorina littorea also occurred among oysters. Abundance of deposit feeding oligochaetes was enhanced by oysters as well. More opportunistic, facultative filter-feeding polychaetes occurred in the Crassostrea-reef.


Bioinvasion Biozoenosis Crassostrea gigas Diversity Ecosystem engineering Macrofauna Mytilus edulis Neozoa North Sea 



The study was carried out within the framework of the project “Bioinvasion” which is financially supported by the SNG Senckenbergische Naturforschende Gesellschaft and the Niedersächsische Wattenmeer Stiftung. Thanks are due to Torsten Janßen for helping during field work. We are grateful to Norbert Dankers, Frouke Fey and Karsten Reise for valuable remarks which considerably improved an earlier version of the manuscript. The paper benefits essentially from constructive comments of two anonymous reviewers. Thanks to Charles Ver Straeten (New York State Museum) for correcting the English.


  1. Arakawa KY (1990) Natural spat collecting in the Pacific oyster Crassostrea gigas (Thunberg). Mar Behav Physiol 17:95–128CrossRefGoogle Scholar
  2. Asmus H (1987) Secondary production of an intertidal mussel bed community related to its storage and turnover compartments. Mar Ecol Prog Ser 39:251–266. doi: 10.3354/meps039251 CrossRefGoogle Scholar
  3. Bell WJ (1991) Searching behaviour. The behavioural ecology of finding resources. Chapman and Hall, New YorkGoogle Scholar
  4. Bergfeld C (1999) Macrofaunal community pattern in an intertidal sandflat: effects of organic enrichment via biodeposition by mussel beds. First results. Senckenbergiana marit 29(suppl):23–27CrossRefGoogle Scholar
  5. Böttger R, Schnack D (1986) On the effect of formaldehyde fixation on the dry weight of copepods. Meeresforschung/reports on marine research. Sonderdruck 31:141–152Google Scholar
  6. Brandt G, Wehrmann A, Wirtz KW (2008) Rapid invasion of Crassostrea gigas into the German Wadden Sea by larval supply. J Sea Res 59:279–296. doi: 10.1016/j.seares.2008.03.004 CrossRefGoogle Scholar
  7. Bray JR, Curtis JT (1957) An ordination of the upland forest communities of Southern Wisconsin. Ecol Monogr 27:325–349. doi: 10.2307/1942268 CrossRefGoogle Scholar
  8. Brey T (1986) Formalin and formaldehyde depot chemicals: effects on dry weight and ash free dry weight of two marine bivalve species. Meeresforsch./reports on marine res. Sonderdruck 31:52–57Google Scholar
  9. Brey T (2001) Population dynamics in benthic invertebrates—a virtual handbook. Version 01.2. Alfred Wegener Institute for Polar and Marine Research, Germany
  10. Buschbaum C, Nehls G (2003) Effekte der Miesmuschel- und Garnelenfischerei. In: Lozán JL, Rachor E, Reise K, Sündermann J, von Westernhagen H (eds) Warnsignale aus Nordsee & Wattenmeer. Hamburg. Wissenschaftliche Auswertungen, pp 250–255Google Scholar
  11. Carlton JT (1987) Patterns of transoceanic marine biological invasions in the Pacific ocean. Bull Mar Sci 41:452–465Google Scholar
  12. Carlton JT, Geller JB (1993) Ecological roulette. The transport of nonindigenous marine organisms. Science 261:78–82. doi: 10.1126/science.261.5117.78 CrossRefGoogle Scholar
  13. Crooks JA (1998) Habitat alteration and community-level effects of an exotic mussel, Musculista senhousia. Mar Ecol Prog Ser 162:137–152. doi: 10.3354/meps162137 CrossRefGoogle Scholar
  14. Dankers NMJA, Dijkman EM, de Jong JL, de Kort G, Meijboom A (2004) De verspreiding en uitbreiding van de Japanese Oester en de Nederlandse Waddenzee. Alterra-rapport 909, Alterra, WageningenGoogle Scholar
  15. Deslous-Paoli JM, Heral M, Goulletquer P, Boromthanarat W, Razet D, Granier J, Prou J, Barille L (1987) Evolution saisonniere de la filtration de bivalves intertideaux dans des conditions naturelles. Oceanis 13(4–5):575–579Google Scholar
  16. Diederich S (2005) Invasion of Pacific oysters (Crassostrea gigas) in the Wadden Sea: competitive advantage over native mussels. Dissertation, Universität KielGoogle Scholar
  17. Dittmann S (1987) Die Bedeutung der Biodeposite für die Benthosgemeinschaft der Wattsedimente. Unter besonderer Berücksichtigung der Miesmuschel Mytilus edulis L. Dissertation, Universität GöttingenGoogle Scholar
  18. Dittmann S (1990) Mussel beds – amensalism or amelioration for intertidal fauna? Helgoländer Meeresunters 44:335–352. doi: 10.1007/BF02365471 CrossRefGoogle Scholar
  19. Dörjes J (1978) Das Watt als Lebensraum. In: Reineck HE (ed) Das Watt. Ablagerungs- und Lebensraum. Verlag W Kramer, Frankfurt a.M.Google Scholar
  20. Dörjes J (1992) Langzeitentwicklung makrobenthischer Tierarten im Jadebusen (Nordsee) während der Jahre 1974 bis 1987. Senckenbergiana marit 22:37–57Google Scholar
  21. Drinkwaard AC (1999) Introductions and developments of oysters in the North Sea area: a review. Helgoländer Meeresunters 52:301–308. doi: 10.1007/BF02908904 CrossRefGoogle Scholar
  22. Fauchald K, Jumars PA (1979) The diet of worms: a study of polychaete feeding guilds. Oceanogr Mar Biol Ann Rev 17:193–284Google Scholar
  23. Gollasch S (2002) The importance of ship hull fouling as a vector of species introductions into the North Sea. Biofouling 18:105–121. doi: 10.1080/08927010290011361 CrossRefGoogle Scholar
  24. Grabowski JH, Powers SP (2004) Habitat complexity mitigates trophic transfer on Crassostrea-reefs. Mar Ecol Prog Ser 277:291–295. doi: 10.3354/meps277291 CrossRefGoogle Scholar
  25. Grotjahn M (1987) Sedimente und Makrofauna der Watten bei der Insel Spiekeroog. Untersuchungen im Rahmen des „Sensitivitätsrasters Deutsche Nordseeküste. Forschungsstelle Küste: pp 97–119Google Scholar
  26. Hamilton S, Kingston PF (1985) The effects of the preservatives alcohol, formalin and propylene phenoxetol on the wet weights of some marine animals. ICES Benthos working GroupGoogle Scholar
  27. Hartmann-Schröder G (1996) Polychaeta. In: Dahl F (ed) Die Tierwelt Deutschlands und der angrenzenden Meeresteile nach ihren Merkmalen und nach ihrer Lebensweise. 58. Teil, 2. Auflage. Gustav Fischer Verlag, JenaGoogle Scholar
  28. Herlyn M, Michaelis H (1996) Untersuchung zur Entwicklung von Miesmuschelbänken der niedersächsischen Watten, unter besonderer Berücksichtigung der Miesmuschelfischerei. Abschlussbericht der A-Hauptphase, Teilprojekt A 3.3 des Teilvorhabens ÖSF Nds. WattenmeerGoogle Scholar
  29. Herlyn M, Millat G (2004) Wissenschaftliche Begleituntersuchungen zur Aufbauphase des Miesmuschelmanagements im Nationalpark „Niedersächsisches Wattenmeer”. Forschungsprojekt der Niedersächsischen Wattenmeerstiftung, Abschlussbericht MärzGoogle Scholar
  30. Hertweck G, Liebezeit G (1996) Biogenic and geochemical properties of intertidal biosedimentary deposits related to Mytilus beds. Mar Ecol 17(1–3):131–141Google Scholar
  31. Hild A, Günther C-P (1999) Ecosystem engineers: Mytilus edulis and Lanice conchilega. In: Dittmann S (ed) The Wadden Sea ecosystem – stability properties and mechanisms. Berlin. S, Springer, pp 43–49Google Scholar
  32. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69(3):373–386. doi: 10.2307/3545850 CrossRefGoogle Scholar
  33. Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16(4):199–204. doi: 10.1016/S0169-5347(01)02101-2 CrossRefPubMedGoogle Scholar
  34. Kristensen E (2000) Organic matter diagenesis at the oxic/anoxic interface in costal marine sediments, with emphasis on the role of burrowing animals. In: Liebezeit G, Dittmann S, Kröncke I (eds) Life at Interfaces and Under Extreme Conditions. Kluwer Dordrecht. Hydrobiologia 426:1–24Google Scholar
  35. Kröncke I (1996) Impact of Biodeposition on Macrofaunal Communities in Intertidal Sandflats. P.S.Z.N.I. Mar Ecol 17(1–3):159–174. doi: 10.1111/j.1439-0485.1996.tb00497.x CrossRefGoogle Scholar
  36. Kröncke I, Bergfeld C (1996) Makrofaunauntersuchungen auf der Swinnplate. In: Bartholomä A, Boysen-Ennen E, Delafontaine MT, Flemming BW, Hertweck G, Kröncke I, Wolf F, Bergfeld C (eds) Zur Elastizität makrofaunistischer biosedimentärer Systeme im Spiekerooger Watt: Wechselwirkungen zwischen Organismen, Sediment und Wasserkörper. Ökosystemforschung Niedersächsisches Wattenmeer (ELAWAT), Abschlussbericht des Teilprojektes B6, pp 117–152Google Scholar
  37. Kruskal JB, Wish M (1978) Multidimensional scaling. Sage Publishers, Berverly HillsGoogle Scholar
  38. Lenihan HS (1999) Physical-biological coupling on Crassostrea-reefs: how habitat structure influences individual performance. Ecol Monogr 69(3):251–275Google Scholar
  39. Lenihan HS, Peterson CH, Allen JM (1996) Does flow speed also have a direct effect on growth of active suspension-feeders: an experimental test on oysters. Limnol Oceanogr 41(6):1359–1366Google Scholar
  40. Linke O (1954) Die Bedeutung der Miesmuscheln für die Landgewinnung im Wattenmeer. Natur Volk 84(8):253–261Google Scholar
  41. Little-Gadow S (1978) Sedimente und Chemismus. In: Reineck HE (ed) Das Watt – Ablagerungs- und Lebensraum. 2. neubearb. Auflage. Dr Waldemar Kramer, Frankfurt a. MGoogle Scholar
  42. MacArther RH, MacArther JW (1961) On species diversity. Ecology 42:594–598. doi: 10.2307/1932254 CrossRefGoogle Scholar
  43. May P (2006) Nahrungskonkurrenz zwischen Crassostrea gigas (Thunberg 1793) und Mytilus edulis Linnaeus, 1758. Master thesis, Universität OldenburgGoogle Scholar
  44. Meire PM (1996) Using optimal foraging theory to determine the density of Mussels Mytilus edulis that can be harvested by hammering oystercatchers Haematopus ostralegus. Ardea 84A:141–152Google Scholar
  45. Meire PM, Ervynck A (1986) Are oystercatchers (Haematopus ostralegus) selecting the most profitable mussels (Mytilus edulis)? Anim Behav 34:1427–1435. doi: 10.1016/S0003-3472(86)80213-5 CrossRefGoogle Scholar
  46. Möbius K (1877) Die Auster und die Austernwirthschaft. Verlag von Wiegandt, Hempel & Parey, BerlinGoogle Scholar
  47. Nehring S (1998) Neozoa an der Nordseeküste – Ein bislang wenig beachtetes Phänomen!. DGM-Mitteilungen 3:3–6Google Scholar
  48. Pearson TH, Rosenberg R (1978) Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr Mar Biol Ann Rev 16:229–311Google Scholar
  49. Pielou EC (1966) Shannon’s formula as a measurement of species diversity: it’s use and disuse. Am Nat 100:463–465. doi: 10.1086/282439 CrossRefGoogle Scholar
  50. Reise K (1998) Pacific oysters invade mussel beds in the European Wadden Sea. Senckenbergiana marit 28(4/6):167–175CrossRefGoogle Scholar
  51. Reise K (2002) Sediment mediated species interactions in costal waters. J Sea Res 48(2):127–140. doi: 10.1016/S1385-1101(02)00150-8 CrossRefGoogle Scholar
  52. Reise K, Dankers N, Essink K (2005) Quality Status Report Wadden Sea—introduced species. Int. Wadden Sea quality status report 2005. Wadden Sea ecosystem 19Google Scholar
  53. Ricciardi A, Bourget E (1998) Weight-to-weight conversion factors for marine benthic macroinvertebrates. Mar Ecol Prog Ser 163:245–251. doi: 10.3354/meps163245 CrossRefGoogle Scholar
  54. Ruesink JL, Lenihan HS, Trimble AC, Heiman KW, Micheli F, Byers JE, Kay MC (2005) Introduction of non-native oysters: ecosystem effects and restoration implications. Annu Rev Ecol Evol Syst 36:643–689. doi: 10.1146/annurev.ecolsys.36.102003.152638 CrossRefGoogle Scholar
  55. Rumohr H (1990) Soft bottom macrofauna: collection, treatment and quality assurance of samples. ICES Techniques in Marine Environmental Sciences, vol 8, 18 ppGoogle Scholar
  56. Soniat TM, Finelli CM, Ruiz JT (2004) Vertical structure and predator refuge mediate oyster reef development and community dynamics. J Exp Mar Biol Ecol 310:163–182CrossRefGoogle Scholar
  57. Troost K, Kamermans P, Stamhuis EJ, Wolff WJ (2004) Are introduced oysters (Crassostrea gigas) hampering the recruitment of indigenous bivalve filter feeders? ICES Council Meeting 2004/K: 10Google Scholar
  58. Tsuchiya M, Nishihira M (1986) Islands of Mytilus as a habitat for small intertidal animals: effects of Mytilus age structure on the species composition of the associated fauna and community organisation. Mar Ecol Prog Ser 31:171–178. doi: 10.3354/meps031171 CrossRefGoogle Scholar
  59. Villbrandt M, Hild A, Dittmann S (1999) Biogeochemical processes in tidal flat sediments and mutual interactions with macrobenthos. In: Dittmann S (ed) The Wadden Sea ecosystem. Springer, BerlinGoogle Scholar
  60. Walne PR (1972) The influence of current speed, body size and water temperature on the filtration rate of five species of bivalves. Mar Biol Assoc UK 52:345–374CrossRefGoogle Scholar
  61. Weaver W, Shannon CE (1949) The mathematical theory of communication. University of Illinois Press, Urbana, p 111Google Scholar
  62. Wehrmann A, Herlyn M, Bungenstock F, Hertweck G, Millat G (2000) The distribution gap is closed–first record of naturally settled Pacific oysters Crassostrea gigas in the East Frisian Wadden Sea, North Sea. Senckenbergiana marit 30(3/6):153–160CrossRefGoogle Scholar
  63. Wehrmann A, Markert A, May P, Schieck P, Schmidt A (2006) Gefährdungspotential der eulitoralen Miesmuschelbänke im Niedersächsischen Wattenmeer durch die Bioinvasion der Pazifischen Auster Crassostrea gigas. Abschlussbericht Projekt 7/02 der Niedersächsischen Wattenmeer-Stiftung, 110 ppGoogle Scholar
  64. Zens M, Michaelis H, Herlyn M, Reetz M (1997) Die Miesmuschelbestände der niedersächsischen Watten im Frühjahr 1994. Ber. Forschungsstelle Küste. Norderney 41:141–155Google Scholar
  65. Zwarts L, Cayford JT, Hulscher JB, Kersten M, Meire PM, Triplet P (1996) Prey size selection and intake rate. In: Goss-Custard JD (ed) The oystercatcher: from individuals to populations. Oxford University Press, OxfordGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Alexandra Markert
    • 1
  • Achim Wehrmann
    • 1
  • Ingrid Kröncke
    • 1
  1. 1.Department for Marine ResearchResearch Institute SenckenbergWilhelmshavenGermany

Personalised recommendations