Marine Biology

, Volume 159, Issue 9, pp 2091–2103 | Cite as

The invasive gastropod Crepidula fornicata: reproduction and recruitment in the intertidal at its northernmost range in Wales, UK, and implications for its secondary spread

  • Katrin Bohn
  • Christopher Richardson
  • Stuart Jenkins
Original Paper


The establishment and spread of a non-native species in an introduced range depends to a large extent on the performance of the species under the prevailing environmental conditions. The spawning, larval and spatfall periods of the invasive gastropod Crepidula fornicata were monitored in the intertidal zone at its northernmost range in Wales, UK, between February 2010 and January 2011. The duration of the reproductive season was similar to that recorded from more southerly European populations. Spawning and larval release occurred throughout most of the year even at low seawater temperatures of <7 °C, but benthic recruitment was observed over a much shorter period at seawater temperatures >16 °C. Recruitment was low and likely controlled by post-settlement mortality. These observations suggest that C. fornicata’s northwards spread in Welsh waters will not be limited by seawater temperature negatively affecting reproduction, but by processes acting after larval release. These data show the importance of incorporating settlement and post-settlement processes into studies on recruitment success when aiming to predict the potential spread of a potentially harmful invader such as C. fornicata.


Seawater Temperature Larval Release Competent Larva Northern Range Limit Maximum Shell Length 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank the SMNR Team from the Countryside Council for Wales and Mr. Ian Pritchard from the School of Ocean Sciences, Bangor University, for the provision of temperature data from the SMNR and the Menai Strait, respectively. We are thankful to Prof. Jan Pechenik and Dr. Thierry Comtet for the confirmation of our larval ID. We are grateful to Mr. Mark Burton and Mr. Phil Newman from the SMNR team and Mr. John Warneford from the Milford Haven Port Authority for the provision of boat time and support during plankton sampling. Dr. Alice Ramsay, Mr. Rodrigo Reis and Dr. Nick Jones provided valuable assistance during the intertidal field sampling. KB acknowledges her PhD scholarship provided by the Countryside Council for Wales and the Bangor Mussel Producers Ltd.

Supplementary material

227_2012_1997_MOESM1_ESM.docx (75 kb)
Supplementary material 1 (DOCX 76 kb)


  1. Barnes RSK, Coughlan J, Holmes NJ (1973) A preliminary survey of the macroscopic bottom fauna of the Solent, with particular reference to Crepidula fornicata and Ostrea edulis. Proc Malacol Soc Lon 40:253–275Google Scholar
  2. Beninger PG, Valdizan A, Decottignies P, Cognie B (2010a) Field reproductive dynamics of the invasive slipper limpet, Crepidula fornicata. J Exp Mar Biol Ecol 390:179–187Google Scholar
  3. Beninger PG, Valdizan A, Decottignies P, Cognie B (2010b) Corrigendum to ‘Field reproductive dynamics of the invasive slipper limpet, Crepidula fornicata’. J Exp Mar Biol Ecol 390:179–187Google Scholar
  4. Blanchard M (1997) Spread of the slipper limpet Crepidula fornicata (L. 1758) in Europe. Current state and consequences. Sci Mar 61(2):109–118Google Scholar
  5. Blanchard M (2009) Recent expansion of the slipper limpet population (Crepidula fornicata) in the Bay of Mont-Saint-Michel (Western Channel, France). Aquat Living Resour 22:11–19Google Scholar
  6. Brante A, Fernández M, Viard F (2009) Limiting factors to encapsulation: the combined effects of dissolved protein and oxygen availability on embryonic growth and survival of species with contrasting feeding strategies. J Exp Biol 212:2287–2295Google Scholar
  7. Büttger H, Nehls G, Witte S (2011) High mortality of Pacific oysters in a cold winter in the North-Frisian Wadden Sea. Helgol Mar Res. doi: 10.1007/s10152-011-0272-1 Google Scholar
  8. Canning-Clode J, Fowler AE, Byers JE, Carlton JT, Ruiz GM (2011) ‘Caribbean creep’ chills out: climate change and marine invasive species. PLoS One 6(12):e29657. doi: 10.1371/journal.pone.0029657 Google Scholar
  9. Chapman JW (2000) Climate effects on the geography of nonindigenous peracaridan crustacean introductions in estuaries. In: Pederson J (ed) First national conference on marine bioinvasions. Massachusetts Institute of Technology, Massachusetts, pp 66–80Google Scholar
  10. Child AR, Laing I (1998) Comparative low temperature tolerance of small juvenile European, Ostrea edulis L., and Pacific oysters, Crassostrea gigas Thunberg. Aquac Res 29:102–113Google Scholar
  11. Chipperfield PNJ (1951) The breeding of Crepidula fornicata in the River Blackwater, Essex. J Mar Biol Assoc UK 30:49–71Google Scholar
  12. Colautti RI, MacIsaac HJ (2004) A neutral terminology to define ‘invasive’ species. Divers Distrib 10:143–146Google Scholar
  13. Cole HA, Baird RH (1953) The American slipper limpet (Crepidula fomicata) in Milford Haven. Nat 172:687Google Scholar
  14. Collin R (1995) Sex, size, and position: a test of models predicting size at sex change in the protandrous gastropod Crepidula fornicata. Am Nat 146:815–831Google Scholar
  15. Collin R (2006) Sex ratio, life history invariants, and patterns of sex change in a family of protandrous gastropods. Evol 60:735–745Google Scholar
  16. Crisp DJ (1964) The effects of the severe winter of 1962–1963 on marine life in Britain. J Anim Ecol 33:165–210Google Scholar
  17. Crothers JH (1966) Dale Fort Marine Fauna, second edition. Field Studies 2, supplementGoogle Scholar
  18. de Rivera CE, Hitchcock NG, Teck SJ, Steves BP, Hines AH, Ruiz GM (2007) Larval development rate predicts range expansion of an introduced crab. Mar Biol 150:1275–1288Google Scholar
  19. Diederich S, Nehls G, van Beusekom JEE, Reise K (2005) Introduced Pacific oysters (Crassostrea gigas) in the northern Wadden Sea: invasion accelerated by warm summers? Helgol Mar Res 59:97–106Google Scholar
  20. Dupont L, Richard J, Paulet YM, Thouzeau G, Viard F (2006) Gregariousness and protandry promote reproductive insurance in the invasive gastropod Crepidula fornicata: evidence from assignment of larval paternity. Mol Ecol 15:3009–3021Google Scholar
  21. Dupont L, Bernas D, Viard F (2007a) Sex and genetic structure across age groups in populations of the European marine invasive mollusc, Crepidula fornicata L. (Gastropoda). Biol J Linn Soc 90:365–374Google Scholar
  22. Dupont L, Ellien C, Viard F (2007b) Limits to gene flow in the slipper limpet Crepidula fornicata as revealed by microsatellite data and a larval dispersal model. Mar Ecol Prog Ser 349:125–128Google Scholar
  23. Dutertre M, Beninger PG, Barillé L, Papin M, Haure J (2010) Rising water temperatures, reproduction and recruitment of an invasive oyster, Crassostrea gigas, on the French Atlantic coast. Mar Environ Res 69:1–9Google Scholar
  24. Dytham C (2011) Choosing and using statistics: a biologist’s guide, 3rd edn. Blackwell Publishing, ChichesterGoogle Scholar
  25. Eyster LS, Pechenik JA (1988) Comparison of growth, respiration, and feeding of juvenile Crepidula fornicata (L.) following natural or KCl-triggered metamorphosis. J Exp Mar Biol Ecol 118:269–279Google Scholar
  26. Firth LB, Knights AM, Bell SS (2011) Air temperature and winter mortality: implications for the persistence of the invasive mussel, Perna viridis in the intertidal zone of the south-eastern United States. J Exp Mar Biol Ecol 400:250–256Google Scholar
  27. Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27Google Scholar
  28. Hawkins SJ, Moore P, Burrows MT, Poloczanska E, Mieszkowska N, Jenkins SR, Thompson RC, Genner MJ, Southward AJ (2008) Complex interactions in a rapidly changing world: responses of rocky shore communities to recent climate change. Clim Res 37:123–133Google Scholar
  29. Hinz H, Capasso E, Lilley M, Frost M, Jenkins SR (2011) Temporal differences across a bio-geographical boundary reveal slow response of sub-littoral benthos to climate change. Mar Ecol Prog Ser 423:69–82Google Scholar
  30. Hiscock K, Southward AJ, Tittley I, Hawkins SJ (2004) Effects of changing temperature on benthic marine life in Britain and Ireland. Aquat Conserv Mar Freshwat Ecosyst 14:333–362Google Scholar
  31. Hoagland KE (1978) Protandry and the evolution of environmentally-mediated sex change: a study of the mollusca. Malacol 17:365–391Google Scholar
  32. Hoagland KE (1979) The behaviour of three sympatric species of Crepidula (Gastropoda, Prosobranchia) from the Atlantic, with implications for evolutionary ecology. Nautil 94:143–149Google Scholar
  33. Hoch JM, Cahill AE (2012) Variation in size at sex-change among natural populations of the protandrous hermaphrodite, Crepidula fornicata (Gastropoda, Calyptraeidae). Mar Biol. doi: 10.1007/s00227-011-1867-4 Google Scholar
  34. Hunt HL, Scheibling RE (1997) Role of early post-settlement mortality in recruitment of benthic marine invertebrates. Mar Ecol Prog Ser 155:269–301Google Scholar
  35. Jenkins SR (2005) Larval habitat selection, not larval supply, determines settlement patterns and adult distribution in two chthamalid barnacles. J Anim Ecol 74:893–904Google Scholar
  36. Maeda-Martínez A (2008) Osmotic and ionic concentration of the egg capsule fluid of Crepidula fornicata in relation to embryonic development. Mar Biol 154:643–648Google Scholar
  37. Masuda R (2008) Seasonal and interannual variation of subtidal fish assemblages in Wakasa Bay with reference to the warming trend in the Sea of Japan. Environ Biol Fish 82:387–399Google Scholar
  38. McGee BL, Targett NM (1989) Larval habitat selection in Crepidula (L.) and its effect on adult distribution patterns. J Exp Mar Biol Ecol 131:195–214Google Scholar
  39. McNeill G, Nunn J, Minchin D (2010) The slipper limpet Crepidula fornicata Linnaeus, 1758 becomes established in Ireland. Aquat Invasions 5(Suppl. 1):21–25Google Scholar
  40. Mettam C (1979) Faunal changes in the Severn Estuary over several decades. Mar Pollut Bull 10:133–136Google Scholar
  41. Mieszkowska N, Leaper R, Moore P, Kendall MA, Burrows MT, Lear D, Poloczanska E, Hiscock K, Moschella PS, Thompson RC, Herbert RJ, Laffoley D, Baxter J, Southward AJ, Hawkins SJ (2005) Marine biodiversity and climate change: assessing and predicting the influence of climatic change using intertidal rocky shore biota. Final report for United Kingdom funders. Mar Biol Assoc Occas Publ 20:1–53Google Scholar
  42. Mieszkowska N, Kendall MA, Hawkins SJ, Leaper R, Williamson P, Hardman-Mountford NJ, Southward AJ (2006) Changes in the range of some common rocky shore species in Britain: a response to climate change? Hydrobiolog 555:241–251Google Scholar
  43. Moore PJ, Thompson RC, Hawkins SJ (2011) Phenological changes in intertidal con-specific gastropods in response to climate warming. Global Chang Biol 17:709–719Google Scholar
  44. Nehls G, Diederich S, Thieltges DW, Strasser M (2006) Wadden Sea mussel beds invaded by oysters and slipper limpets: competition or climate control? Helgol Mar Res 60:135–143Google Scholar
  45. Nelson-Smith A (1965) Marine biology of Milford Haven: the physical environment. Field Stud 2:155–188Google Scholar
  46. Nelson-Smith A (1967) Marine biology of Milford Haven: the distribution of littoral plants and animals. Field Stud 2:435–477Google Scholar
  47. Orton JH (1909) On the occurrence of protandric hermaphroditism in the mollusc Crepidula fornicata. Proc R Soc Lon B Biol Sci 81:468–484Google Scholar
  48. Pechenik JA (1980) Growth and energy balance during the larval life of three prosobranch gastropods. J Exp Mar Biol Ecol 44:1–28Google Scholar
  49. Pechenik JA (1984) The relationship between temperature, growth-rate, and duration of planktonic life for larvae of the gastropod Crepidula fornicata (L). J Exp Mar Biol Ecol 74:241–257Google Scholar
  50. Pechenik JA, Eyster LS (1989) Influence of delayed metamorphosis on the growth and metabolism of young Crepidula fornicata (Gastropoda) juveniles. Biol Bull 176:14–24Google Scholar
  51. Pechenik JA, Lima GM (1984) Relationship between growth, differentiation, and length of larval life for individually reared larvae of the marine gastropod, Crepidula fornicata. Biol Bull 166:537–549Google Scholar
  52. Rahel FJ, Olden JD (2008) Assessing the effects of climate change on aquatic invasive species. Conserv Biol 22:521–533Google Scholar
  53. Richard J, Huet M, Thouzeau G, Paulet YM (2006) Reproduction of the invasive slipper limpet, Crepidula fornicata, in the bay of Brest, France. Mar Biol 149:789–801Google Scholar
  54. Rigal F (2009) Etude de la dynamique spatio-temporelle du nuage larvaire du gasteropode introduit Crepidula fornicata dans une baie megatidale, la baie de Morlaix. These de doctorat, Universite Pierre et Marie Curie-Paris 6, ParisGoogle Scholar
  55. Rigal F, Viard F, Ayate S-D, Comtet T (2010) Does larval supply explain the low proliferation of the invasive gastropod Crepidula fornicata in a tidal estuary? Biol Invasions 12:3171–3186Google Scholar
  56. Spencer BE, Edwards DB, Kaiser MJ, Richardson CA (1994) Spatfalls of the non-native Pacific oyster, Crassostrea gigas, in British waters. Aquat Conserv 4:203–217Google Scholar
  57. Stachowicz JJ, Terwin JR, Whitlatch RB, Osman RW (2002) Linking climate change and biological invasions: ocean warming facilitates nonindigenous species invasions. Proc Natl Acad Sci 99:15497–15500Google Scholar
  58. Thieltges DW, Strasser M, Reise K (2003) The American slipper limpet Crepidula fornicata (L.) in the northern Wadden Sea 70 years after its introduction. Helgol Mar Res 57:27–33Google Scholar
  59. Thieltges DW, Strasser M, Van Beusekom JEE, Reise K (2004) Too cold to prosper: winter mortality prevents population increase of the introduced American slipper limpet Crepidula fornicata in northern Europe. J Exp Mar Biol Ecol 311:375–391Google Scholar
  60. Valdizan A, Beninger PG, Decottignies P, Chantrel M, Cognie B (2011) Evidence that rising coastal seawater temperatures increase reproductive output of the invasive gastropod Crepidula fornicata. Mar Ecol Prog Ser 438:153–165Google Scholar
  61. Walne PR (1956) The biology and distribution of the slipper limpet Crepidula fornicata in Essex Rivers. With notes on the distribution of larger epi-benthic invertebrates. Ministry of Agriculture, Fisheries and Food, Fishery Investigations, Series 2, 20(6):1–50Google Scholar
  62. Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nat 416:389–395Google Scholar
  63. Walther GR, Roques A, Hulme PE, Sykes MT, Pyšek P, Kuhn I, Zobel M, Bacher S, Botta-Dukát Z, Bugmann H, Czucz B, Dauber J, Hickler T, Jarošik V, Kenis M, Klotz S, Minchin D, Moora M, Nentwig W, Ott J, Panov VE, Reineking B, Robinet C, Semenchenko V, Solarz W, Thuiller W, Vilá M, Vohland K, Settele J (2009) Alien species in a warmer world: risks and opportunities. Trends Ecol Evol 24:686–693Google Scholar
  64. Werner B (1948) Die amerikanische Pantoffelschnecke Crepidula fornicata L. im nordfriesischen Wattenmeer. Zool Jahrb 77:449–488Google Scholar
  65. Wilczynski JZ (1955) On sex behaviour and sex determination in Crepidula fornicata. Biol Bull 109:353–354Google Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Katrin Bohn
    • 1
  • Christopher Richardson
    • 1
  • Stuart Jenkins
    • 1
  1. 1.School of Ocean Sciences, College of Natural SciencesBangor UniversityAnglesey, WalesUK

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