Abstract
The reproduction of Crepidula fornicata was studied in the Bay of Brest in order to characterise the first step of the reproductive cycle of this invasive species. The survey was carried out from 2000 to 2003 and different parameters were measured, namely, the percentage of the different sexual stages, the straight length of the shell and the percentage of brooding females using a survey of the embryonic development and the fecundity. The juvenile frequency increases generally from mid-June or mid-August, depending on the year. In 2001 and 2003, a first peak was observed as early as May, but it was followed by a rapid disappearance of the individuals. The sex-ratio female/male increased from 0.22 to 0.46 between 2001 and 2003. The sex change between intermediates and females took place mainly in summer and was well marked in 2001 and 2003. The survey of the embryonic development in the egg capsules brooded by the females provided an annual phenology of the laying and hatching processes. The laying period extends from February to September with three to four major periods of egg-laying per year and corresponding hatching periods about 1 month later. Each female lays two to four times per year on average. The first egg-laying concerned fewer females than subsequent ones, except in 2003, and exhibited a higher fecundity. The annual mean of the number of eggs for each stage was not significantly different, thus indicating no significant mortality rate during embryonic development. For the C. fornicata population in the Bay of Brest, several reproductive characteristics tend to highlight its invasive capacity: (1) a long reproductive period, (2) reproduction in a ‘multi-trials’ process equivalent to a spreading out of the risks and (3) a relatively high fecundity.
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References
Baker HG (1965) Characteristics and modes of origin of weeds. In: Baker HG (ed) The genetics of colonizing species. Academic, New York, NY, pp 147–169
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 40:253–275
Blanchard M (1997) Spread of the slipper limpet Crepidula fornicata (L. 1758) in Europe. Current state and consequences. Sci Mar 61(Suppl 2):109–118
Brown AHD, Burdon JJ (1987) Mating systems and colonizing success in plants. In: Gray AJ, Crawley MJ, Edwards PJ (eds) Colonization, succession and stability. Blackwell Scientific, Oxford, pp 115–131
Carlton JT (1985) Transoceanic and interoceanic dispersal of coastal marine organisms, the biology of ballast water. Oceanogr Mar Biol 23:313–371
Carlton JT (2001) Introduced species in US coastal waters: environmental impacts and management priorities. Pew Oceans Commission, Arlington, VA
Chaparro OR, Paschke KA (1990) Nurse egg feeding and energy balance in embryos of Crepidula dilatata (Gastropoda: Calyptraeidae) during intracapsular development. Mar Ecol Prog Ser 65(2):183–191
Charnov AL (1982) The theory of sex allocation. Princeton University Press, Princeton, NJ
Chauvaud L (1998) La coquille Saint-Jacques en rade de Brest: un modèle biologique d’étude des réponses de la faune benthique aux fluctuations de l’environnement. Thèse de doctorat, Université Bretagne Occidentale, Brest
Chauvaud L, Jean F, Ragueneau O, Thouzeau G (2000) Long-term variation of the Bay of Brest ecosystem: benthic-pelagic coupling revisited. Mar Ecol Prog Ser 200:35–48
Chauvaud L, Thouzeau G, Grall J (2003a) La coquille Saint-Jacques et la crépidule, deux modèles biologiques d’étude des réponses de la faune benthique aux fluctuations de l’environnement en rade de Brest. In: ‘Zones côtières et questions d’environnement: réflexions méthodologiques’. Institut Océanographique Editeur, Rapport sur la Science et la Technologie Ingénierie des Territoires, atelier ‘Science et aménagement des zones côtières, réflexions méthodologiques’, Institut de France, Académie des Sciences, Paris, 23 novembre 2001. Océanis 27(2):215–238
Chauvaud L, Thouzeau G, Grall J, Paulet Y-M (2003b) La crépidule en rade de Brest: un paradoxe pour le devenir de la coquille Saint-Jacques. In: ‘Exploitation et surexploitation des ressources marines vivantes’, Tec & Doc Editeurs, Rapport sur la Science et la Technologie Ingénierie des Territoires, Institut de France, Académie des Sciences, Paris, 3 octobre 2001. Rapport sur la Science et la Technologie no. 17, décembre 2003, Paris, pp 307–318
Chipperfield PNJ (1951) The breeding of Crepidula fornicata (L) in the river Blackwater, Essex. J Mar Biol Assoc UK 30:49–71
Coe WR (1935) Sexual phases in prosobranch mollusks of the genus Crepidula. Science 81(2110):570–571
Coe WR (1936) Sexual phases in Crepidula. J Exp Zool 72(3):455–477
Coe WR (1938a) Conditions influencing change of sex in mollusks of the genus Crepidula. J Exp Zool 77(3):401–424
Coe WR (1938b) Influence of association on the sexual phases of gastropods having protandric consecutive sexuality. Biol Bull 75:274–285
Coe WR (1948) Nutrition and sexuality in protandric gastropods of the genus Crepidula. Biol Bull 94(3):158–160
Coe WR (1953) Influences of association, isolation, and nutrition on the sexuality of snails of the genus Crepidula. J Exp Zool 122:5–19
Collin R (1995) Sex, size, and position: a test of models predicting size at sex change in the protandrous gastropod Crepidula fornicata. Am Nat 146:815–831
Conklin EG (1897) Environmental and sexual dimorphism in Crepidula. Proc Acad Nat Sci Philadelphia 435–444
Connor DW, Dalkin MJ, Hill TO, Holt RHF, Sanderson WG (1997) Marine nature conservation review, marine biotope classification for Britain and Ireland, vol 2 Sublittoral biotopes. Version 97.06.JNCC Report, No 230
Coum A (1979) La population de crépidules Crepidula fornicata (L.) en rade de Brest: écologie et dynamique. Thèse de doctorat, Université Bretagne Occidentale, Brest
Cronin TM, Dwyer GS, Kamiya T, Schwede S, Willard DA (2003) Medieval Warm Period, Little Ice Age and 20th century temperature variability from Chesapeake Bay. Glob Planet Change 36:17–29
Cushing DH (1982) Climate and fisheries. Academic, Bury St Edmunds, Suffolk
Degobbis D (1989) Increased eutrophication of the Northern Adriatic Sea. Mar Pollut Bull 20:452–457
Deslous-Paoli JM (1985) Crepidula fornicata L (gastéropode) dans le bassin de Marennes-Oléron: structure, dynamique et production d’une population. Oceanol Acta 8(4):453–460
Deslous-Paoli JM, Héral M (1986) Crepidula fornicata L (Gastéropode, Calyptraeidae) dans le bassin de Marennes-Oléron: composition et valeur énergétique des individus et des pontes. Oceanol Acta 9(3):305–311
Delmas R (1981) Etude de l’évolution saisonnière des sels nutritifs dans la rade de Brest en fonction des apports fluviaux et des échanges avec l’Iroise. Thèse de doctorat, Université Bretagne Occidentale, Brest
Delmas R, Tréguer P (1983) Evolution saisonnière des nutriments dans un écosystème eutrophe d’Europe occidentale (la rade de Brest). Interactions marines et terrestres. Oceanol Acta 6:345–355
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 Paris VI, Paris
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 253:183–195
Erhold 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 (Earth Planet Sci) 327:583–588
Gaffney PM, McGee B (1992) Multiple paternity in Crepidula fornicata (Linnaeus). Veliger 35(1):12–15
Gallardo CS (1996) Reproduction in Crepidula philippiana (Gastropoda, Calyptraeidae) from Southern Chile. Stud Neotrop Fauna Environ 31:117–122
Guérin L (2004) La crépidule en rade de Brest: un modèle biologique d’espèce introduite proliférante en réponse aux fluctuations de l’environnement. Thèse de doctorat, Université Bretagne Occidentale, Brest
Hoagland KE (1978) Protandry and the evolution of environmentally mediated sex-change: a study of the Mollusca. Malacologia 17(2):365–391
Hoagland KE (1979) The behaviour of three sympatric species of Crepidula (Gastropoda: Prosobranchia) from the Atlantic, with implications for evolutionary ecology. Nautilus 94(4):143–148
Hoagland KE (1985) Genetic relationships between one British and several North American populations of Crepidula fornicata based on allozyme studies (Gastropoda: Calyptraeidae). J Molluscan Stud 51:177–182
Korringa P (1951) Crepidula fornicata as an oyster pest. Cons Perm Int Explor Mer Part II 128:55–59
Le Gall P (1980) Etude expérimentale d’association en chaîne et de son influence sur la croissance et la sexualité chez la crépidule (Crepidula fornicata Linné 1758). Thèse de doctorat, Université Caen, Caen
Levin J, Vilà M, D’Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlaying the impact of exotic plant invasions. Proc R Soc Lond B 270:775–781
Lodge DM (1993) Biological invasions—lessons for ecology. Trends Ecol Evol 8:133–137
Lorrain A (2002) Utilisation de la coquille Saint-Jacques comme traceur environnemental: approches biologique et biogéochimique. Thèse de doctorat, Université Bretagne Occidentale, Brest
Lubet P, Le Gall P (1972) Recherches préliminaires sur la structure des populations de Crepidula fornicata Philb., Mollusque Mésogastéropode. Bull Soc Zool 97(2):211–222
MacGinitie N, MacGinitie GE (1964) Habitats and breeding seasons of the shelf limpet Crepidula norrisiarum Williamson. Veliger 7(1):34
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz A (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710
de Montaudouin X, Sauriau PG (1999) The proliferating Gastropoda Crepidula fornicata may stimulate macrozoobenthic diversity. J Mar Biol Assoc UK 79:1069–1077
Myers JH, Simberloff D, Kuris AM, Carey JR (2000) Eradication revisited: dealing with exotic species. Trends Ecol Evol 15:316–320
Naylor R, Williams S, Strong D (2001) Aquaculture a gateway for exotic species. Science 294:1655–1656
Newell RIE, Hilbish TJ, Koehn RK, Newell CJ (1982) Temporal variation in the reproductive cycle of Mytilus edulis L. (Bivalvia, Mytilidae) from localities on the east coast of the United States. Biol Bull US 162:299–310
Nienhuis PH (1992) Ecology of coastal lagoons in the Netherlands (Veerse Meer and Grevelingen). Vie Milieu 42:59–72
Orton JH (1909) On the occurrence of protandric hermaphroditism in the mollusc Crepidula fornicata. Proc R Soc Lond B Biol Sci 81:468–484
Orton JH (1927) Is the American slipper limpet an oyster pest? Nautilus 40:102–103
Orton JH (1950) Recent breeding phenomena in the American slipper limpet, Crepidula fornicata. Nature 165(4194):433–434
Paulet YM, Lucas A, Gerard A (1988) Reproduction and larval development in two Pecten maximus (L.) populations from Brittany. J Exp Mar Biol Ecol 119:145–156
Ragueneau O, Chauvaud L, Leynaert A, Thouzeau G, Paulet YM, Bonnet S, Lorrain A, Grall J, Corvaisier R, Le Hir M, Jean F, Clavier J (2002) Direct evidence of a biologically active coastal silicate pump: ecological implications. Limnol Oceanogr 47(6):1849–1854
Ragueneau O, Chauvaud L, Moriceau B, Leynaert A, Thouzeau G, Donval A, Le Loc’h F, Jean F (2005) Biodeposition by an invasive suspension feeder impacts the biogeochemical cycle of Si in a coastal ecosystem (Bay of Brest, France). Biogeochemistry 75(1):19–41
Ruiz GM, Carlton JT, Grosholz E, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species, mechanisms, extent, and consequences. Am Zool 37:621–632
Ruiz GM, Fofonoff PW, Carlton JT, Wonham MJ, Hines AH (2000) Invasion of coastal marine communities in North America, apparent patterns, processes, and biases. Ann Rev Ecol Syst 31:481–531
Sala OE, Chapin FS III, Armesto JJ, Berlow E, Bloomfield J, Dirzo R, Huber-Sanwald E, Huenneke LF, Jackson RB, Kinzig A, Leemans R, Lodge DM, Mooney HA, Oesterheld M, Poff NL, Sykes MT, Walker BH, Walker M, Wall DH (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774
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(2):375–391
Thouzeau G, Chauvaud L, Grall J, Guérin L (2000) Rôle des interactions biotiques sur le devenir du pré-recrutement et la croissance de Pecten maximus (L.) en rade de Brest. C R Acad Sci, Ser III Sci Vie/Life Sci 323:815–825
Thouzeau G, Chauvaud L, Durand G, Patris T, Glémarec M (2003) Impact des polluants d’origine anthropique sur les organismes benthiques marins: notions d’indicateurs biologiques de perturbation et de réseaux de surveillance. In: ‘Zones côtières et questions d’environnement: réflexions méthodologiques’. Institut Océanographique (ed), Rapport sur la Science et la Technologie Ingénierie des Territoires, atelier ‘Science et aménagement des zones côtières, réflexions méthodologiques’, Institut de France, Académie des Sciences, Paris, 23 novembre 2001. Océanis 27(2):177–214
Vitousek PM, D’Antonio CM, Loppe LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478
Walne PR (1956) The biology and distribution of the Slipper Limpet Crepidula fornicata in Essex rivers. Fish Invest 20(6):1–50
Werner B (1948) Die amerikanische Pantoffelschneke Crepidula fornicata L. im nordfriesischen Wattenmeer. Zool Jahrb 77:449–488
Whittier JM, Limpus D (1996) Reproductive patterns of a biologically invasive species: the brown tree snake (Boiga irregularis) in eastern Australia. J Zool 238:591–597
Wilczynski JZ (1955) On sex behaviour and sex determination in Crepidula fornicata. Biol Bull 109:353–354
Williamson M, Fitter A (1996) The varying success of invaders. Ecology 77:1661–1665
Acknowledgements
We wish to thank anonymous referees for their helpful comments on the manuscript. This research was supported by the Programme National d’Environnement Côtier (PNEC) and the University of Geneva; the authors greatly acknowledge Professor Louisette Zaninetti. We thank the captains, officers and crew members of the INSU/CNRS research vessels for their technical assistance at sea, as well as Anne Donval, Alain Lemercier and Laurent Guérin. We are grateful to the students Elodie Coquard, Véronique Dupin and Patrick Ladiesse for their help. Thanks are also due to the staff of the SOMLIT network in Plouzané and to Sorcha Ni Longphuirt for the English corrections.
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Richard, J., Huet, M., Thouzeau, G. et al. Reproduction of the invasive slipper limpet, Crepidula fornicata, in the Bay of Brest, France. Mar Biol 149, 789–801 (2006). https://doi.org/10.1007/s00227-005-0157-4
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DOI: https://doi.org/10.1007/s00227-005-0157-4