Skip to main content

Advertisement

SpringerLink
Log in

Premature refutation of a human-mediated marine species introduction: the case history of the marine snail Littorina littorea in the Northwestern Atlantic

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The closely documented spread of the European periwinkle snail, Littorina littorea from Pictou, Nova Scotia in 1840 to New Jersey by 1870, its near absence in pre-European fossil deposits, and its close association with human mechanisms of transport from Europe, are among the clearest evidence of a human-mediated marine introduction ever reported. Genetic data were recently proposed as evidence that North American L. littorea predate European contact and thus, are not introduced. Review of these genetic data and all other data reveals that the simplest explanation of the modern occurrence of this snail in North America is by human introduction.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

COI:

Cytochrome oxydase I

cytb:

Cytochrome b

ITS:

Internal transcribed spacer region

References

  • Adkins RM, Gelke EL, Rowe D, Honeycutt RL (2001) Molecular phylogeny and divergence time estimates for major rodent groups: evidence from multiple genes. Mol Biol Evol 18:777–791

    PubMed  CAS  Google Scholar 

  • Ballard JWO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744

    Article  PubMed  Google Scholar 

  • Berger EM (1977) Gene-enzyme variation in three sympatric species of Littorina. II. The Roscoff population, with a note on the origin of North American L. littorea. Biol Bull 153:255–264

    Article  Google Scholar 

  • Bird JB (1968) Littorina littorea: occurrence in a northern Newfoundland beach terrace, predating Norse settlements. Science 159:114

    Article  CAS  Google Scholar 

  • Brenchley GA, Carlton JT (1983). Competitive displacement of native mud snails by introduced periwinkles in the New England intertidal zone. Biol Bull 165:543–558

    Article  Google Scholar 

  • Carlton JT (1979) History, biogeography, and ecology of the introduced marine and estuarine invertebrates of the Pacific coast of North America. Ph.D. Dissertation, University of California, Davis

  • Carlton JT (1982) The historical biogeography of Littorina littorea on the Atlantic coast of North America, and implications for the interpretation of the structure of New England intertidal communities. Malacol Rev 15:146

    Google Scholar 

  • Carlton JT (1992) Introduced marine and estuarine mollusks of North America: an end-of-the-20th-century perspective. J Shellfish Res 11:489–505

    Google Scholar 

  • Carlton JT (1999). The scale and ecological consequences of biological invasions in the world’s oceans. In: Sandlund OT, Schei PJ, Åuslaug V (eds) Invasive species and biodiversity management. Kluwer Academic Publishers, Dordrecht, The Netherlands pp 195–212

  • Carlton JT (2000) Global change and biological invasions in the oceans. In: Mooney HA, Hobbs RJ (eds) Invasive species in a changing world. Island Press, Washington, D.C, pp 31–52

    Google Scholar 

  • Carlton JT (2002) Bioinvasion ecology: assessing invasion impact and scale. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe. Distribution, impacts, and management. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 7–19

    Google Scholar 

  • Carlton JT (2003) Community assembly and historical biogeography in the North Atlantic Ocean: the potential role of human-mediated dispersal vectors. Hydrobiologia 503:1–8

    Article  Google Scholar 

  • Chapman JW (1988) Invasions of the northeast Pacific by Asian and Atlantic gammaridean amphipods crustaceans, including a new species of Corophium. J Crustacean Biol 8:364–382

    Article  Google Scholar 

  • Chapman JW, Carlton JT (1991) A test of criteria for introduced species: the global invasion by the isopod Synidotea laevidorsalis (Miers, 1881). J Crustacean Biol 11:386–400

    Article  Google Scholar 

  • Chapman JW, Carlton JT (1994) Predicted discoveries of the introduced isopod, Synidotea laevidorsalis (Miers, 1881). J Crustacean Biol 14:700–714

    Article  Google Scholar 

  • Clarke AH (1963a) Supplementary notes on pre-Columbian Littorina littorea in Nova Scotia. Nautilus 77:8–11

    Google Scholar 

  • Clarke AH (1963b) Littorina littorea as an indicator of Norse settlements. Science 142:1022

    Article  PubMed  Google Scholar 

  • Clarke AH (1971) Littorina littorea, native or introduced? Biologist 53:160–162

    Google Scholar 

  • Clarke AH, Erskine JS (1961) Pre-Columbian Littorina littorea in Nova Scotia. Science 134:393–394

    Article  PubMed  Google Scholar 

  • Cosby AW (1993) Ecological imperialism: the biological expansion of Europe, 900–1900. Cambridge University Press, New York

    Google Scholar 

  • Cunningham CW (2007) How to use genetic data to distinguish between natural and human-mediated introduction of Littorina littorea to North America. Biological Invasions doi:10.1007/s10530-007-9099-8

  • Dawson MN, Gupta AS, England MH (2005) Coupled biophysical global ocean model and molecular genetic analyses identify multiple introductions of cryptogenic species. Proc Natl Acad Sci 102:11968–11973

    Article  PubMed  CAS  Google Scholar 

  • Diamond J (1997) Guns, germs, and steel: the fates of human societies. W. W. Norton, New York

    Google Scholar 

  • Elton CS (1958) The ecology of invasions by plants and animals. John Wiley & Sons, New York

    Google Scholar 

  • Ganong WF (1886) Is Littorina littorea introduced or indigenous? Am Nat 20:931–940

    Article  Google Scholar 

  • Ganong WF (1887) Is Littorina littorea introduced or indigenous? Am Nat 21:287–288

    Google Scholar 

  • Gosner KL (1971) Guide to identification of marine and estuarine invertebrates, Cape Hatteras to the Bay of Fundy. Wiley-Interscience, John Wiley & Sons, Inc., New York

    Google Scholar 

  • Heltshe JF, Forrester NE (1983) Estimating species richness using the jackknife procedure. Biometrics 39:1–11

    Article  PubMed  CAS  Google Scholar 

  • Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760

    Article  PubMed  CAS  Google Scholar 

  • Johannesson K (1992) Genetic variability and large scale differentiation in two species of littorinid gastropods with planktotrophic development, Littorina littorea (L.) and Melarhaphe (Littorina) neritoides (L.) (Prosobranchia: Littorinacea), with notes on a mass occurrence of M. neritoides in Sweden. Biol J Linnaean Soc 47:285–299

    Google Scholar 

  • Kraeuter JN (1976) Offshore currents, larval transport, and establishment of southern populations of Littorina littorea Linne along the U.S. Atlantic coast. Thalassia Jugoslavica 10:159–170

    Google Scholar 

  • Krebs CJ (1989) Ecol Methodol. Harper Collins Publishers, New York

    Google Scholar 

  • Kumar S, Hedges SB (1998) A molecular timescale for vertebrate evolution. Nature 392:917–919

    Article  PubMed  CAS  Google Scholar 

  • Ledig FT, Conkle MT, Bermejo-Velazquez B, Eguiluz-Piedra T, Hodgskiss PD, Johnson DR, Dvorak WS (1999) Evidence for an extreme bottleneck in a rare Mexican pinyon: genetic diversity, disequilibrium, and the mating system in Pinus maximartinezii. Evolution 53:91–99

    Article  Google Scholar 

  • Lindroth CH (1957) The faunal connections between Europe and North America. John Wiley & Sons, New York, NY

    Google Scholar 

  • Medcof JC, Clarke AH, Erskine JS (1965) Ancient Canadian east-coast oyster and quahaug shells. J Fish Res Board of Canada 22:631–634

    Google Scholar 

  • Morris SR (1979) Genetic variation in the genus Littorina, Ph.D. dissertation. University College of Swansea, Wales, UK

  • Morse ES (1880) The gradual dispersion of certain mollusks in New England. Bull Essex Inst 12:171–176

    Google Scholar 

  • Nei M, Glazko GV (2002) Estimation of divergence times for a few mammalian and several primate species. J Hered 93:157–164

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Li W-H (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci 76:5269–5273

    Article  PubMed  CAS  Google Scholar 

  • Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885–896

    PubMed  CAS  Google Scholar 

  • Pederson J (ed) (2000). Marine Bioinvasions. National Conference on Marine Bioinvasions. Massachusetts Institute of Technology, Massachusetts Sea Grant, Cambridge, MA

  • Petersen KS, Rasmussen KL, Heinemeier J, Rud N (1992) Clams before Columbus? Nature 359:679

    Article  Google Scholar 

  • Powell JR (1991) Monophyly/paraphyly/polyphyly and gene/species trees: an example from Drosophila. Mol Biol Evol 8:892–896

    PubMed  CAS  Google Scholar 

  • Reid DG (1996) Systematics and evolution of Littorina. The Ray Society, The Dorset Press, Dorchester, Dorset, England

    Google Scholar 

  • Spjeldnaes N, Henningsmoen KE (1963a) Littorina littorea: an indicator of Norse settlement in North America? Science 141:275–276

    Article  PubMed  Google Scholar 

  • Spjeldnaes N, Henningsmoen KE (1963b) Reply to A. H. Clarke. Science 142:1022

    Article  PubMed  Google Scholar 

  • Steneck RS, Carlton JT (2001) Human alteration of marine communities: students beware! In: Bertness MD, Gains SD, Hay ME (eds) Marine community ecology. Sinaur Associates, Inc., Sunderland, MA, pp 445–468

    Google Scholar 

  • Strasser M (1999) Mya arenaria—an ancient invader of the North Sea coast. Helgolander Meeresuntersuchungen 52:309–324

    Article  Google Scholar 

  • Sugden AM (2002) Origins of an invasion. Science 297:739

    Article  Google Scholar 

  • Turgeon DD, Quinn JF Jr, Bogan AE, Coan EV, Hochberg FG, Lyons WG (1998) Common and scientific names of aquatic invertebrates from the United States and Canada: Mollusks, 2nd ed. American Fisheries Society Special Publication, Bethesda, MD

    Google Scholar 

  • Vermeij GJ (1982) Environmental change and the evolutionary history of the periwinkle Littorina littorea in North America. Evolution 36:561–580

    Article  Google Scholar 

  • Vermeij GJ (1991) Anatomy of an invasion: the trans-Arctic interchange. Paleobiology 17:281–307

    Google Scholar 

  • Wagner FJE (1977) Palaeoecology of marine Pleistocene Mollusca, Nova Scotia. Can J Earth Sci 14:1305–1323

    Google Scholar 

  • Wares JP (2002) Community genetics in the northwestern Atlantic intertidal. Mol Evol 11:1131–1144

    Article  CAS  Google Scholar 

  • Wares JP, Goldwater DS, Kong BY, Cunningham CW (2002) Refuting a controversial case of a human-mediated marine species introduction. Ecol Lett 5:577–584

    Article  Google Scholar 

  • Webb DA (1985) What are the criteria for presuming native status? Watsonia 15:231–236

    Google Scholar 

  • Willis J (1863) On the occurrence of Littorina litorea on the coast of Nova Scotia. Trans NS Inst Nat Sci 1:88–90

    Google Scholar 

Download references

Acknowledgements

We are grateful to Mitch Cruzan (and students), Portland State University; Mike Behrenfeld, Mark Camara, Michael Banks, and Paul Lang, Oregon State University; George Mpitsos, OSU Hatfield Marine Science Center; Rasmus Nielsen, Cornell University; Jody Hey, Rutgers University; David Reid, The Natural History Museum; Bernd Schoene, Goethe University; Deniz Haydar, University of Groningen, The Netherlands; Amy Chapman, South Beach, Oregon; Katie Chapman, Bowdoin College, Maine; Anthony Ricciardi, Redpath Museum; and John Wares, University of Georgia, for invaluable information, materials and critical comments. We thank the curators of the museums noted above for access to their collections. Financial support for (AMHB) provided by NSF Award OCE 05–03932 to James E. Byers. Susan Gilmont, Judy Mullen, and Janet Webster, Guin Library, OSU, recovered difficult references. We thank the Coastal Ocean Experiment Station for use of their facilities by JWC and MRB. This paper is dedicated to Eliana Sabina Bellinger-Thomas and to Westley James Blakeslee, both born on 12 September 2005.

Author information

Authors and Affiliations

  1. Department of Fisheries and Wildlife, Oregon State University, Hatfield Marine Science Center, 2030 SE Marine Science Dr., Newport, OR, 97365-5296, USA

    John W. Chapman & M. Renee Bellinger

  2. Maritime Studies Program, Williams College—Mystic Seaport, 75 Greenmanville Ave., P.O. Box 6000, Mystic, CT, 06355, USA

    James T. Carlton

  3. Department of Zoology, University of New Hampshire, Rudman Hall, 46 College Road, Durham, NH, 03824, USA

    April M. H. Blakeslee

Authors
  1. John W. Chapman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. James T. Carlton
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Renee Bellinger
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. April M. H. Blakeslee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to John W. Chapman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chapman, J.W., Carlton, J.T., Bellinger, M.R. et al. Premature refutation of a human-mediated marine species introduction: the case history of the marine snail Littorina littorea in the Northwestern Atlantic. Biol Invasions 9, 995–1008 (2007). https://doi.org/10.1007/s10530-007-9098-9

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-007-9098-9

Keywords

Search

Navigation