Biological Invasions

, Volume 12, Issue 9, pp 3171–3186 | Cite as

Does larval supply explain the low proliferation of the invasive gastropod Crepidula fornicata in a tidal estuary?

  • François Rigal
  • Frédérique Viard
  • Sakina-Dorothée Ayata
  • Thierry Comtet
Original Paper

Abstract

Human-mediated transport and aquaculture have promoted the establishment of non-indigenous species in many estuaries around the world over the last century. This phenomenon has been demonstrated as a major cause of biodiversity alterations, which has prompted scientists to provide explanations for the success or failure of biological invasions. Crepidula fornicata is a gastropod native from the East coast of North America which has successfully invaded many European bays and estuaries since the 19th century, with some noticeable exceptions. Its spread over Europe has been explained by a combination of human-mediated transport and natural dispersal through its long-lived planktonic larva. We here investigated whether larval supply may explain the failure in the proliferation of this species within a particular bay, the Bay of Morlaix (France). Patterns of larval distribution and larval size structure were analysed over ten sites sampled three times (20 July, 4 August and 21 August 2006), regarding characteristics of the adult population and environmental features. Our results evidenced a strong spatial structure in both larval abundance and size at the bay scale, even if larval abundances were low. In this scheme, the location of spawning adults played a critical role, with high numbers of early larvae above the main spawning location. The larval size structure further showed that settlement-stage larvae were rare, which suggested that released larvae might have been exported out of the bay. The use of an analytical model aimed to study the effect of tidal currents on the potential for larval exportation confirmed that larval retention within the bay might be low. The limitation in larval supply resulting from the interactions between spawning location and local hydrodynamics may thus impede the proliferation of this species which is well established for more than 50 years. This study provided an example of factors which may explain the failure of the transition between two major steps of biological invasions, i.e. sustainable establishment and proliferation.

Keywords

Crepidula fornicata Spatial distribution Propagule supply Larval dispersal Bentho–pelagic cycle 

Supplementary material

10530_2010_9708_MOESM1_ESM.pdf (22 kb)
Supplementary material 1 (PDF 21 kb)
10530_2010_9708_MOESM2_ESM.pdf (153 kb)
Supplementary material 2 (PDF 154 kb)

References

  1. Barnay AS, Ellien C, Gentil F, Thiébaut E (2003) A model study on variations in larval supply: are populations of the polychaete Owenia fusiformis in the English Channel open or closed? Helgol Mar Res 56:229–237Google Scholar
  2. 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 Lond 40:253–275Google Scholar
  3. Bhaud M (2000) Two contradictory elements determine invertebrates recruitment: dispersion of larvae and spatial restrictions on adults. Oceanol Acta 23:409–422CrossRefGoogle Scholar
  4. Black KP, Gay SL, Andrews JC (1990) Residence times of neutrally-buoyant matter such as larvae, sewage or nutrients on coral reefs. Coral Reefs 9:105–114CrossRefGoogle Scholar
  5. Blanchard M (1995) Origine et état de la population de Crepidula fornicata (Gastropoda Prosobranchia) sur le littoral français. Haliotis 24:75–86Google Scholar
  6. Blanchard M (1997) Spread of the slipper limpet Crepidula fornicata (L.1758) in Europe: current state and consequences. Sci Mar 61:109–118Google Scholar
  7. 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 22:11–19CrossRefGoogle Scholar
  8. Blanchet FG, Legendre P, Borcard D (2008) Forward selection of explanatory variables. Ecology 89:2623–2632CrossRefPubMedGoogle Scholar
  9. Byers JE, Pringle JM (2006) Going against the flow: retention, range limits and invasions in advective environments. Mar Ecol Prog Ser 313:27–41CrossRefGoogle Scholar
  10. Cabioch L (1968) Contribution à la connaissance des peuplements benthiques de la Manche occidentale. Cah Biol Mar 9:493–720Google Scholar
  11. Cabioch L, Douvillé JL (1979) La circulation des eaux dans la baie de Morlaix et ses abords: premières données obtenues par suivis de flotteurs dérivants. Trav St Biol Roscoff 26:11–20Google Scholar
  12. Cameron B, Metaxas A (2005) Invasive green crab, Carcinus maenas, on the Atlantic coast and in the Bras d’Or Lakes of Nova Scotia, Canada: larval supply and recruitment. J Mar Biol Ass U K 85:847–855CrossRefGoogle Scholar
  13. Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82CrossRefGoogle Scholar
  14. Chipperfield PNJ (1951) The breeding of Crepidula fornicata (L.) in the river Blackwater, Essex. J Mar Biol Ass U K 30:49–71CrossRefGoogle Scholar
  15. Coe WR (1936) Sexual phases in Crepidula. J Exp Zool 72:455–477CrossRefGoogle Scholar
  16. Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558CrossRefPubMedGoogle Scholar
  17. Conq C, Dauvin JC, Lorgeré JC (1998) Température et salinité de l’eau de mer au large de Roscoff de 1991 à 1997. Cah Biol Mar 39:207–212Google Scholar
  18. Coum A (1979) La population de crépidules Crepidula fornicata (L. 1758) en rade de Brest: écologie et dynamique. Thèse de doctorat, Université de Bretagne Occidentale, Brest, FranceGoogle Scholar
  19. Dame RF, Allen DM (1996) Between estuaries and the sea. J Exp Mar Biol Ecol 200:169–185CrossRefGoogle Scholar
  20. de Montaudouin X, Sauriau PG (1999) The proliferating Gastropoda Crepidula fornicata may stimulate macrozoobenthic diversity. J Mar Biol Ass U K 79:1069–1077CrossRefGoogle Scholar
  21. de Montaudouin X, Labarraque D, Giraud K, Bachelet G (2001) Why does the introduced gastropod Crepidula fornicata fail to invade Arcachon Bay (France)? J Mar Biol Ass U K 81:97–104CrossRefGoogle Scholar
  22. deRivera CE, Hitchcock NG, Teck SJ, Hines AH, Ruiz GM (2007) Larval development rate predicts range expansion of an introduced crab. Mar Biol 150:1275–1288CrossRefGoogle Scholar
  23. Deslous-Paoli JM (1985) Crepidula fornicata L. (gastéropode) dans le bassin de Marennes-Oléron: structure, dynamique et production d’une population. Oceanol Acta 8:453–460Google Scholar
  24. Drake JM, Lodge DM (2006) Allee effect, propagule pressure and the probability of the establishment: risk analysis for biological invasions. Biol Invasions 8:365–375CrossRefGoogle Scholar
  25. Dubois S, Comtet T, Retière C, Thiébaut E (2007) Distribution and retention of Sabellaria alveolata larvae (Polychaeta: Sabellariidae) in the Bay of Mont-Saint-Michel, France. Mar Ecol Prog Ser 346:243–254CrossRefGoogle Scholar
  26. Dunstan PK, Bax NJ (2007) How far can marine species go? Influence of population biology and larval movement on future range limits. Mar Ecol Prog Ser 344:15–28CrossRefGoogle Scholar
  27. Dupont L (2004) Invasion des côtes françaises par le mollusque exotique Crepidula fornicata: contribution de la dispersion larvaire et du système de reproduction au succès de la colonisation. Thèse de doctorat, Université Pierre et Marie Curie-Paris 6, ParisGoogle Scholar
  28. Dupont L, Jollivet D, Viard F (2003) High genetic diversity and ephemeral drift effects in a successful introduced mollusc (Crepidula fornicata: Gastropoda). Mar Ecol Prog Ser 253:183–195CrossRefGoogle Scholar
  29. Dupont L, Ellien C, Viard F (2007) Limits to gene flow in the slipper limpet Crepidula fornicata as revealed by microsatellite data and a larval dispersal model. Mar Ecol Prog Ser 349:125–138CrossRefGoogle Scholar
  30. Edwards KP, Hare JA, Werner FE, Seim H (2007) Using 2-dimensional dispersal kernels to identify the dominant influences on larval dispersal on continental shelves. Mar Ecol Prog Ser 352:77–87CrossRefGoogle Scholar
  31. Ehrhold A, Blanchard M, Auffret JP, Garlan T (1998) 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 Sci Terre Planet 327:583–588Google Scholar
  32. Frontier S, Pichod-Viale D (1991) Ecosystèmes: structure, fonctionnement, évolution. Masson, ParisGoogle Scholar
  33. Gaines S, Roughgarden J (1985) Larval settlement rate: a leading determinant of structure in an ecological community of the marine intertidal zone. Proc Natl Acad Sci USA 82:3707–3711CrossRefPubMedGoogle Scholar
  34. Geyer WR, Signell RP (1992) A reassessment of the role of tidal dispersion in estuaries and bays. Estuaries 15:97–108CrossRefGoogle Scholar
  35. Gros P, Cochard JC (1978) Biologie de Nyctiphanes couchii (Crustacea, euphasiacea) dans le secteur Nord du Golfe de Gascogne. Ann Inst Océanogr 54:25–46Google Scholar
  36. Jollivet D, Empis A, Baker MC, Hourdez S, Comtet T, Jouin-Toulmond C, Desbruyères D, Tyler PA (2000) Reproductive biology, sexual dimorphism, and population structure of the deep sea hydrothermal vent scale-worm, Branchipolynoe seepensis (Polychaeta: Polynoidae). J Mar Biol Ass U K 80:55–68CrossRefGoogle Scholar
  37. Kinlan BP, Gaines SD, Lester SE (2005) Propagule dispersal and the scales of marine community process. Diversity Distrib 11:139–148CrossRefGoogle Scholar
  38. Kutner MH, Nachtsheim CJ, Neter J, Li W (2004) Applied linear statistical models, 5th edn. McGraw-Hill Irwin, New YorkGoogle Scholar
  39. Le Cam S (2009) Modalités de la reproduction chez l’espèce hermaphrodite protandre Crepidula fornicata: paternité et changement de sexe. Thèse de doctorat, Université Pierre et Marie Curie-Paris 6, ParisGoogle Scholar
  40. Legendre P, Gallagher ED (2001) Ecologically meaningful transformations for ordination of species data. Oecologia 129:271–280CrossRefGoogle Scholar
  41. Legendre P, Legendre L (1998) Numerical ecology, 2nd edn. Elsevier, AmsterdamGoogle Scholar
  42. Leppäkoski E, Olenin S (2000) Non-native species and rates of spread: lessons from the brackish Baltic Sea. Biol Invasions 2:151–163CrossRefGoogle Scholar
  43. Loomis SH, Van Nieuwenhuyze W (1985) Sediment correlates to density of Crepidula fornicata Linnaeus in the Pataguanset River, Connecticut. Veliger 27:266–272Google Scholar
  44. Lorenzen CJ (1966) A method for the continuous measurement of in vivo chlorophyll a concentration. Deep-Sea Res 13:223–227Google Scholar
  45. Martin S, Thouzeau G, Chauvaud L, Jean F, Guérin L, Clavier J (2006) Respiration, calcification, and excretion of the invasive slipper limpet, Crepidula fornicata L.: implications for carbon, carbonate, and nitrogen fluxes in affected areas. Limnol Oceanogr 51:1996–2007CrossRefGoogle Scholar
  46. McGee BL, Targett NM (1989) Larval habitat selection in Crepidula (L.) and its effect on adult distribution patterns. J Exp Mar Biol Ecol 131:195–214CrossRefGoogle Scholar
  47. Naylor RL, Williams SL, Strong DR (2001) Aquaculture-a gateway for exotic species. Science 294:1655–1656CrossRefPubMedGoogle Scholar
  48. Nehring S (2006) Four arguments why so many alien species settle into estuaries, with special reference to the German river Elbe. Helgol Mar Res 60:127–134CrossRefGoogle Scholar
  49. Paavola M, Olenin S, Leppäkoski E (2005) Are invasive species most successful in habitats of low native species richness across European brackish water seas? Est Coast Shelf Sci 64:738–750CrossRefGoogle Scholar
  50. Pechenik JA (1999) On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles. Mar Ecol Prog Ser 177:269–297CrossRefGoogle Scholar
  51. Pechenik JA, Heyman WD (1987) Using KCl to determine size at competence for larvae of the marine gastropod Crepidula fornicata (L.). J Exp Mar Biol Ecol 112:27–38CrossRefGoogle Scholar
  52. 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 166:537–549CrossRefGoogle Scholar
  53. Pedersen TM, Hansen JLS, Josefson AB, Hansen BW (2008) Mortality through ontogeny of soft-bottom marine invertebrates with planktonic larvae. J Mar Syst 73:185–207CrossRefGoogle Scholar
  54. Plus M, Maurer D, Stanisière JY, Dumas F (2006) Caractérisation des composantes hydrodynamiques d’une lagune mésotidale, le Bassin d’Arcachon. Report RST/LER/AR/06.007. IFREMER, Arcachon, FranceGoogle Scholar
  55. Quiniou F, Blanchard M (1987) État de la prolifération de la crépidule (Crepidula fornicata L.) dans le secteur de Granville (golfe normano-breton). Haliotis 16:513–526Google Scholar
  56. Reise K, Olenin S, Thieltges DW (2006) Are aliens threatening European aquatic coastal ecosystems? Helgol Mar Res 60:77–83CrossRefGoogle Scholar
  57. 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 149:789–801CrossRefGoogle Scholar
  58. Rigal F (2009) Étude de la dynamique spatio-temporelle du nuage larvaire du gastéropode introduit Crepidula fornicata dans une baie mégatidale, la baie de Morlaix. Thèse de doctorat, Université Pierre et Marie Curie-Paris 6, ParisGoogle Scholar
  59. Roughgarden J, Gaines SD, Possingham H (1988) Recruitment dynamics in complex life cycles. Science 241:1460–1466CrossRefPubMedGoogle Scholar
  60. Rumrill SS (1990) Natural mortality of marine invertebrate larvae. Ophelia 32:163–198Google Scholar
  61. Salomon JC, Breton M (1991) Courants résiduels de marée dans la Manche. Oceanol Acta 11:47–53Google Scholar
  62. Sauriau PG, Pichocki-Seyfried C, Walker P, de Montaudouin X, Palud C, Héral M (1998) Crepidula fornicata L. (mollusque, gastéropode) en baie de Marennes-Oléron: cartographie des fonds par sonar à balayage latéral et estimation du stock. Oceanol Acta 21:353–362CrossRefGoogle Scholar
  63. Schneider DW, Stoeckel JA, Rehmann CR, Douglas Blodgett K, Sparks RE, Padilla DK (2003) A developmental bottleneck in dispersing larvae: implications for spatial population dynamics. Ecol Lett 6:352–360CrossRefGoogle Scholar
  64. Simberloff D (2009) The role of propagule pressure in biological invasions. Ann Rev Ecol Evol Syst 40:81–102CrossRefGoogle Scholar
  65. Simberloff D, Gibbons L (2004) Now you see them, now you don’t!—population crashes of established introduced species. Biol Invasions 6:161–172CrossRefGoogle Scholar
  66. Thiébaut E, Dauvin J-C, Lagadeuc Y (1992) Transport of Owenia fusiformis larvae (Annelida: Polychaeta) in the Bay of Seine. I. Vertical distribution in relation to water column stratification and ontogenic vertical migration. Mar Ecol Prog Ser 80:29–39CrossRefGoogle Scholar
  67. 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 311:375–391CrossRefGoogle Scholar
  68. Todd CD (1998) Larval supply and recruitment of benthic invertebrates: do larvae always disperse as much as we believe? Hydrobiologia 375(376):1–21CrossRefGoogle Scholar
  69. UNESCO (1968) Zooplankton sampling. Monographs on oceanographic methodology. UNESCO, Paris, p 174Google Scholar
  70. Viard F, Ellien C, Dupont L (2006) Dispersal ability and invasion success of Crepidula fornicata in a single gulf: insights from genetic markers and larval-dispersal model. Helgol Mar Res 60:144–152CrossRefGoogle Scholar
  71. Voisin M, Engel CR, Viard F (2005) Differential shuffling of native genetic diversity across introduced regions in a brown alga: aquaculture vs. maritime traffic effects. Proc Natl Acad Sci USA 102:5432–5437CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • François Rigal
    • 1
    • 2
  • Frédérique Viard
    • 1
    • 2
  • Sakina-Dorothée Ayata
    • 1
    • 2
  • Thierry Comtet
    • 1
    • 2
  1. 1.Equipe Div&Co, Station BiologiqueUniversité Pierre et Marie Curie-Paris 6, UMR 7144RoscoffFrance
  2. 2.Adaptation & Diversité en Milieu Marin, Station BiologiqueCNRS, UMR 7144Roscoff CedexFrance

Personalised recommendations