Coming and going – Historical distributions of the European oyster Ostrea edulis Linnaeus, 1758 and the introduced slipper limpet Crepidula fornicata Linnaeus, 1758 in the North Sea

Autoři: Sarah Hayer aff001;  Andreas Bick aff002;  Angelika Brandt aff003;  Christine Ewers-Saucedo aff001;  Dieter Fiege aff003;  Susanne Füting aff005;  Ben Krause-Kyora aff006;  Peter Michalik aff007;  Götz-Bodo Reinicke aff008;  Dirk Brandis aff001
Působiště autorů: Zoological Museum, Christian-Albrechts-University, Kiel, Schleswig-Holstein, Germany aff001;  Zoological Collections of the University Rostock, Institut for Biosciences, General and Systematic Zoology, Rostock, Mecklenburg-Vorpommern, Germany aff002;  Senckenberg Research Institute and Natural History Museum, Frankfurt am Main, Hessen, Germany aff003;  Evolution and Diversity, Institut for Ecology, Goethe-University of Frankfurt, Frankfurt am Main, Hessen, Germany aff004;  Museum for Nature and Environment, Lübeck, Schleswig-Holstein, Germany aff005;  Institut of Clinical Molecular Biology (IKMB), Christian-Albrechts-University, Kiel, Schleswig-Holstein, Germany aff006;  Zoological Museum of the University Greifswald, Greifswald, Mecklenburg-Vorpommern, Germany aff007;  German Oceanographic Museum, Stralsund, Mecklenburg-Vorpommern, Germany aff008
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article


Natural history collections are fundamental for biodiversity research as well as for any applied environment-related research. These collections can be seen as archives of earth´s life providing the basis to address highly relevant scientific questions such as how biodiversity changes in certain environments, either through evolutionary processes in a geological timescale, or by man-made transformation of habitats throughout the last decades and/or centuries. A prominent example is the decline of the European flat oyster Ostrea edulis Linneaus, 1758 in the North Sea and the concomitant invasion of the common limpet slipper Crepidula fornicata, which has been implicated to have negative effects on O. edulis. We used collections to analyse population changes in both species in the North Sea. In order to reconstruct the change in distribution and diversity over the past 200 years, we combined the temporal and spatial information recorded with the collected specimens contained in several European natural history collections. Our data recover the decline of O. edulis in the North Sea from the 19th century to the present and the process of invasion of C. fornicata. Importantly, the decline of O. edulis was nearly completed before C. fornicata appeared in the North Sea, suggesting that the latter had nothing to do with the local extinction of O. edulis in the North Sea.

Klíčová slova:

Europe – German people – Invasive species – Museum collections – Oysters – Species extinction – Zoology – Oyster farming


1. Lüttschwager J. Studien an vorgeschichtlichen Wirbeltieren Schleswig-Holsteins. Schr d Naturw Ver f Schleswig-Holstein. 1954; 27.

2. Yonge CM. Oysters. London, Collins. 1960; 209: 104.

3. Neudecker T. The history of the former German oyster fishery and mariculture: 400 years of Crown Law on oyster (4.2.1587). Deutsche Hydrografische Zeitschrift, Ergänzungsheft Reihe B. 1990; 22: 518.

4. Thüry GE. Römische Austernfunde in der Schweiz, im rechtsrheinischen Süddeutschland und in Österreich. Helbing & Lichtenhahn. 1990.

5. Gercken J, Schmidt A. Aktueller Status der europäischen Auster (Ostrea edulis) und Möglichkeiten einer Wiederansiedlung in der deutschen Nordsee. 2014.

6. Lotze HK (2007). Rise and fall of fishing and marine resource use in the Wadden Sea, southern Nord Sea. Fish Res. 2007; 87: 208–218.

7. Möbius KA. Die Auster und die Austernwirtschaft. Berlin, Verlag von Wiegandt, Hempel und Parey. 1877.

8. Schümer K. Die Schichte der Sylter Auster. Dittmeyer’s Austern-Campagnie, Sylter Royale. ca. 1990.

9. Thieltges DW. Erfolgreiche Einwanderin aus Übersee–Die Amerikanische Pantoffel-schnecke Crepidula fornicata im Wattenmeer. Natur u Museum. 2003; 133: 110–114.

10. Ranson G. Ècologie et répartition géographique des Ostréidés vivants. La Revue scientifique. 1948; 86: 472.

11. Strauch F, Thüry GE. Austernfunde aus römischen Gebäuderesten in Tittmoning, Ldkr. Traunstein. Bayerische Vorgeschichtsblätter. 1985; 50: 341.

12. Lapègue S, Beaumont A, Boudry P, Goulletquer P. European flat oyster–Ostrea edulis. Genimpact–Final report. 2008; pp. 68.

13. Korringa P. Recent advances in oyster biology. Q Rev Biol. 1952; 27(3): 266–308. 13004275

14. Wilbur KM, Yonge CM (1966). Physiology of mollusca; volume 2. Academic Press.

15. Drinkwaard AC. Introductions and developments of oysters in the North Sea area: a review. Helgoländer Meeresuntersuchungen. 1998; 52(3): 301.

16. Hutchinson S, Hawkins LE. Quantification of the physiological responses of the European flat oyster Ostrea edulis L. to temperature and salinity. J Molluscan Stud. 1992; 58(2): 215–226.

17. Hagmeier A, Kändler R. Neue Untersuchungen im nordfriesischen Wattenmeer und auf den fiskalischen Austernbänken. Aus der Biologischen Anstalt auf Helgoland und deren Zweiglaboratorium in List a. Sylt. 1927; 16(6): 1–90.

18. Orton JH (1927). Is the American slipper-limpet an oyster pest? Nautilus. 1927; 40: 102–103.

19. Ankel WE. Die Pantoffelschnecke, ein Schädling der Auster. Natur u Volk. 1935; 65: 173–176.

20. Linke O. Die „Austern-Pest”auf den Muschelbänken des ostfriesischen Watts. Natur u. Volk. 1947; 77(1): 27–29.

21. Werner B. Die amerikanische Pantoffelschnecke Crepidula fornicata L. im nordfriesischen Wattenmeer. Zool Jahrb, Abt Syst Ökol Geogr Tiere. 1948; 77: 449–488.

22. Korringa P. Crepidula fornicata as an oyster-pest. Cons Per Internat Explor Mers, part II. 1951; 128: 55–59.

23. Schuster O. Zur Ausbreitung der Pantoffelschnecke (Crepidula fornicata) in der Nordsee. Natur u Mus. 1951; 81(10): 256–259.

24. Blanchard M. Spread of the slipper limpet Crepidula fornicata (L. 1758) in Europe. Current state and consequences. Sci mar. 1997; 61: 109–118.

25. Nehring S, Leuchs H. Neozoen im Makrozoobenthos der Brackgewässer an der deutschen Nordseeküste. Lauterbornia. 2000; 39: 73–116.

26. Ankel WE. Die Pantoffelschnecke auf deutschen Austernbänken. Natur u Volk. 1936; 66: 11–13.

27. Suarez AV, Tsutsui ND. The value of museum collections for research and society. Bioscience. 2004; 54(1): 66–74.

28. McCarthy MA (1998). Identifying declining and threatened species with museum data. Biol Conserv. 1998; 83: 9–17.

29. Shaffer HB, Fisher RN, Davidson C. The role of natural history collections in documenting species declines. Trends Ecol Evol. 1998; 13: 27–30. doi: 10.1016/s0169-5347(97)01177-4 21238186

30. Team RStudio. RStudio: Integrated Development for R. RStudio, Inc., Boston, MA. 2016.

31. Wickham H. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag, New York. 2009

32. Fullarton JH. The oyster fishery of Scotland. Proc Philos Soc Glasgow. 1891; 22: 110–127.

33. Guralnick R, Van Cleve J. Strengths and weaknesses of museum and national survey data sets for predicting regional species richness: comparative and combined approaches. Divers Distrib. 2005; 11(4): 349–359.

34. Olsen OT. The Piscatorial Atlas of the North Sea, English and St. George's Channels: Illustrating the Fishing Ports, Boats, Gear, Species of Fish (how, where and when Caught), and Other Information Concerning Fish and Fisheries. 1883.

35. Berghahn R, Ruth M. The disappearance of oysters from the Wadden Sea: a cautionary tale for no-take zones. Aquatic Conserv: Mar Freshw Ecosyst. 2005; 15: 91–104.

36. Herborg LM, Rushton SP, Clare AS, Bentley MG. Spread of the Chinese mitten crab (Eriocheir sinensis H. Milne Edwards) in Continental Europe: analysis of a historical data set. In: Migrations and Dispersal of Marine Organisms. Springer, Dordrecht. 2003; 21–28.

37. Thieltges D, Strasser M, Reise K. The American slipper limpet Crepidula fornicata (L.) in the northern Wadden Sea 70 years after its introduction. Helgol Mar Res. 2003; 57(1), 27.

38. Geburzi JC, McCarthy ML. How Do They Do It?–Understanding the Success of Marine Invasive Species. In: YOUMARES 8–Oceans Across Boundaries: Learning from each other. Springer, Cham. 2018; 109–124.

39. Boudouresque CF, Ruitton S, Verlaque M. Large-scale disturbances, regime shift and recovery in littoral systems subject to biological invasions. In UNESCO-Roste/BAS Workshop on regime shifts. 2005; 14–16.

40. Victoria DPI. Invasive plants and animals policy framework. Department of Primary Industries, Victoria. 2010.

41. Gothland M, Dauvin JC, Denis L, Dufossé F, Jobert S, Ovaert J, et al. Biological traits explain the distribution and colonisation ability of the invasive shore crab Hemigrapsus takanoi. Estuar Coast Shelf Sci. 2014; 142, 41–49.

42. Thieltges DW, Strasser M, Reise K. The American slipper-limpet Crepidula fornicata (L.) in the Northern Wadden Sea 70 years after its introduction. Helgol Mar Res. 2002; doi: 10.1007/s10152-002-0119-X

43. de Montaudouin X, Audemard C, Labourg PJ. Does the slipper limpet (Crepidula fornicata, L.) impair oyster growth and zoobenthos biodiversity? A revisited hypothesis. J Exp Mar Biol Ecol. 1999; 135: 105–124.

44. Thouzeau G, Chau-Vaud L, Grall J, Guérin L. Rôle des interactions biotiques sur le devenir du pré-recruitment et la croissance de Pecten maximus (L.) en rade de Brest. C R Acad Sci Paris, Sciences de la vie. 2000; 323: 815–825. 11072626

45. Pechenik JA, Blanchard M, Rotjan R. Susceptibility of larval Crepidula fornicata to predation by suspension-feeding adults. J Exp Mar Biol Ecol. 2004: 306.1: 75–94.

46. Ehrhold A, Blanchard M, Auffret JP, Garlan T. Conséquences de la prolifération de la crépidule (Crepidula fornicata) sur l'évolution sédimentaire de la baie du Mont-Saint-Michel (Manche, France). C R Acad Sci Paris, Earth & Planetary Sciences. 1998; 327: 583–588.

47. Vattenfall A, Skov-og N. Danish offshore wind-key environmental issues. DONG energy, 2006.

48. Bouma S, Lengkeek W. Benthic communities on hard substrates of the offshore wind farm Egmond aan Zee (OWEZ). Including results of samples collected in scour holes. OWEZ_R_266_ T1_20120206, Bureau Waardenburg report, 2012, Nr. 11–205, S. 80.

49. Rachor E, Bönsch R, Boos K, Gosselck F, Grotjahn M, Günther CP, et al. Rote Liste und Artenlisten der bodenlebenden wirbellosen Meerestiere. In: (Naturschutz und Biologische Vielfalt; 70, 2). Bundesamt für Naturschutz (BfN), 2013. S. 81–176.

50. Zettler ML, Beermann J, Dannheim J, Ebbe B, Grotjahn M, Günther CP, et al. An annotated checklist of macrozoobenthic species in German waters of the North and Baltic Seas. Helgol Mar Res. 2018; 72(1): 5.

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