More than One Way to Invade: Lessons from Genetic Studies of Carcinus Shore Crabs

Chapter
First Online:
Part of the Invading Nature - Springer Series in Invasion Ecology book series (INNA, volume 6)

Abstract

The European green crab Carcinus maenas is one of the world’s most widely recognized marine invaders. The success of this species has provided opportunities to explore genetic patterns associated with establishment and population expansion following independent introduction events to widely different recipient ecosystems. Recent studies have revealed an extraordinary diversity of such patterns. Globally, genetic reconstruction of invasion histories suggests complicated scenarios comprising multiple introductions to some regions as well as secondary introductions deriving from previously established invasive populations. In addition, detailed genetic analyses of several introduced populations indicate that successful invasion may involve rapid expansion from single low diversity founder populations, multiple introductions from genetically distinct sources with subsequent intraspecific admixture, or even interspecific hybridization between C. maenas and its sibling species C. aestuarii. The complexity of this global picture highlights the contingent nature of individual biological invasion events. Nevertheless, genetic study of non-native Carcinus populations provides crucial insights into invasion dynamics relevant to green crab management and control, and offers an unusually rich system within which to explore the genetic consequences of colonizations and range expansions in coastal marine ecosystems.

Keywords

Ballast Water Invasive Population Larval Dispersal Green Crab Multiple Introduction 
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.
This is a preview of subscription content, log in to check access.

References

  1. Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell Publishing, MaldenGoogle Scholar
  2. Anderson LWJ (2005) California’s reaction to Caulerpa taxifolia: a model for invasive species rapid response. Biol Invas 7:1003–1016CrossRefGoogle Scholar
  3. Audet D, Davis DS, Miron G, Moriyasu M, Benhalima K, Campbell R (2003) Geographical expansion of a nonindigenous crab, Carcinus maenas (L.), along the Nova Scotian shore into the southeastern Gulf of St. Lawrence, Canada. J Shell Res 22:255–262CrossRefGoogle Scholar
  4. Austerlitz F, JungMuller B, Godelle B, Gouyon PH (1997) Evolution of coalescence times, genetic diversity and structure during colonization. Theor Popul Biol 51:148–164CrossRefGoogle Scholar
  5. Bagley MJ, Geller JB (2000) Microsatellite analysis of native and invading populations of European green crabs. In: Pederson J (ed) Marine bioinvasions: proceedings of the first national conference, Cambridge MA. MIT Seagrant, Cambridge, pp 241–243Google Scholar
  6. Bax N, Hayes K, Marshall A, Parry D (2002) Man-made marinas as sheltered islands for alien marine organisms: establishment and eradication of an alien invasive marine species. In: Veitch CR, Clout MN (eds) Turning the tide: the eradication of invasive species. IUCN SSC, Gland/Cambridge, pp 26–39Google Scholar
  7. Bazin E, Glémin S, Galtier N (2006) Population size does not influence mitochondrial genetic diversity in animals. Science NY 312:570–572Google Scholar
  8. Blakeslee AMH, McKenzie C, Darling JA, Byers J, Pringle J, Roman J (2010) A hitchhiker’s guide to the Maritimes: Anthropogenic transport facilitates long-distance dispersal of a marine crab to Newfoundland. Diver Distrib 16:879–891Google Scholar
  9. Browne JM, Boudjelas S (2000) 100 of the World’s worst invasive alien species IUCN/SSC invasive species specialist group (ISSG), AucklandGoogle Scholar
  10. Bulnheim HP, Bahns S (1996) Genetic variation and divergence in the genus Carcinus (Crustacea, Decapoda). Int Rev Ges Hydrobiol Hydrogr 81:611–619CrossRefGoogle Scholar
  11. 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
  12. Byers JE, Pringle JM (2008) Going against the flow: how marine invasions spread and persist in the face of advection. ICES J Mar Sci 65:723–724CrossRefGoogle Scholar
  13. Carlton JT, Cohen AN (2003) Episodic global dispersal in shallow water marine organisms: the case history of the European shore crabs Carcinus maenas and C. aestuarii. J Biogeogr 30:1809–1820CrossRefGoogle Scholar
  14. Chen RB, Watanabe S, Yokota M (2004) Feeding habits of an exotic species, the Mediterranean green crab Carcinus aestuarii, in Tokyo Bay. Fish Sci 70:430–435CrossRefGoogle Scholar
  15. Clark PF, Neale M, Rainbow PS (2001) A morphometric analysis of regional variation in Carcinus Leach, 1814 (Brachyura: Portunidae: Carcininae) with particular reference to the status of the two species C. maenas (Linnaeus, 1758) and C. aestuarii Nardo, 1847. J Crust Biol 21:288–303CrossRefGoogle Scholar
  16. Cohen AN, Carlton JT, Fountain MC (1995) Introduction, dispersal and potential impacts of the green crab Carcinus maenas in San Francisco Bay, California. Mar Biol 122:225–238Google Scholar
  17. Colautti RI, Grigorovich IA, MacIsaac HJ (2007) Propagule pressure: a null model for biological invasions. Biol Invas 9:885–885CrossRefGoogle Scholar
  18. Culver CS, Kuris AM (2000) The apparent eradication of a locally established introduced marine pest. Biol Invas 2:245–253CrossRefGoogle Scholar
  19. Currat M, Ruedi M, Petit RJ, Excoffier L (2008) The hidden side of invasions: massive introgression by local genes. Evolution 62:1908–1920Google Scholar
  20. Darling JA, Bagley MJ, Roman J, Tepolt CK, Geller JB (2008) Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus. Mol Ecol 17:4992–5007CrossRefGoogle Scholar
  21. Darling JA (in press). Interspecific hybridization and mitochondrial introgression in invasive Carcinus shore crabs. PLoS ONEGoogle Scholar
  22. Davies N, Villablanca FX, Roderick GK (1999) Determining the source of individuals: multilocus genotyping in nonequilibrium population genetics. Trends Ecol Evol 14:17–21CrossRefGoogle Scholar
  23. Demeusy N, Veillet A (1953) Sur l’existence de deux populations de Carcinus maenas Pennant et sur les caractères morphologiques qui les distinguent. C r hebd Séanc Acad Sci Paris 236:1088–1090Google Scholar
  24. Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449CrossRefGoogle Scholar
  25. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci USA 97:7043–7050CrossRefGoogle Scholar
  26. Estoup A, Beaumont M, Sennedot F, Moritz C, Cornuet JM (2004) Genetic analysis of complex demographic scenarios: spatially expanding populations of the cane toad, Bufo marinus. Evolution 58:2021–2036Google Scholar
  27. Excoffier L, Foll M, Petit RJ (2009) Genetic consequences of range expansions. Annu Rev Ecol Evol Syst 40:481–501CrossRefGoogle Scholar
  28. Facon B, Pointier JP, Jarne P, Sarda V, David P (2008) High genetic variance in life-history strategies within invasive populations by way of multiple introductions. Curr Biol 18:363–367CrossRefGoogle Scholar
  29. Frankham R (2005) Invasion biology – resolving the genetic paradox in invasive species. Heredity 94:385CrossRefGoogle Scholar
  30. Geller JB, Walton ED, Grosholz ED, Ruiz GM (1997) Cryptic invasions of the crab Carcinus detected by molecular phylogeography. Mol Ecol 6:901–906CrossRefGoogle Scholar
  31. Geller JB, Darling JA, Carlton JT (2010) Genetic perspectives on marine bioinvasions. Annu Rev Mar Sci 2:367–393CrossRefGoogle Scholar
  32. Gillespie GE, Phillips AC, Paltzat DL, Therriault TW (2007) Status of the European green crab, Carcinus maenas, in British Columbia, 2006 Canada FaO (ed). Canadian technical report of fisheries and aquatic sciences, NanaimoGoogle Scholar
  33. Grosholz ED, Ruiz GM (1995) Spread and potential impact of the recently introduced European green crab, Carcinus maenas, in central California. Mar Biol 122:239–247Google Scholar
  34. Grosholz ED, Ruiz GM, Dean CA, Shirley KA, Maron JL, Connors PG (2000) The impacts of a nonindigenous marine predator in a California bay. Ecology 81:1206–1224CrossRefGoogle Scholar
  35. Hampton SL, Griffiths CL (2007) Why Carcinus maenas cannot get a grip on South Africa’s wave-exposed coastline. Afr J Mar Sci 29:123–126CrossRefGoogle Scholar
  36. Hanfling B (2007) Understanding the establishment success of non-indigenous fishes: lessons from population genetics. J Fish Biol 71:115–135CrossRefGoogle Scholar
  37. Hidalgo FJ, Baron PJ, Orensanz JM (2005) A prediction come true: the green crab invades the Patagonian coast. Biol Invas 7:547–552CrossRefGoogle Scholar
  38. Hierro JL, Maron JL, Callaway RM (2005) A biogeographical approach to plant invasions: the importance of studying exotics in their introduced and native range. J Ecol 93:5–15CrossRefGoogle Scholar
  39. Ho SYW, Phillips MJ, Cooper A, Drummond AJ (2005) Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol Biol Evol 22:1561–1568CrossRefGoogle Scholar
  40. Holthuis LB, Gottlieb E (1958) An annotated list of the decapod Crustacea of the Mediterranean coast of Israel, with an appendix listing the Decapoda of the eastern Mediterranean. Bull Res Counc Isr Zool 7B:1–85Google Scholar
  41. Huyer A, Barth JA, Fleischbein J, Kosro PM, Smith RL (1998) The coastal ocean off Oregon and northern California during the 1997/1998 El Niño, Part 1: temperature, salinity, and geostrophic velocity fields. Trans Am Geophys Union 79:F485Google Scholar
  42. Ibrahim K, Nichols R, Hewitt G (1996) Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77:282–291CrossRefGoogle Scholar
  43. Kimbro DL, Grosholz ED, Baukus AJ, Nesbitt N, Travis N, Attoe S, Coleman_Hulbert C (2009) Invasive species cause large-scale loss of native California oyster habitat by disrupting trophic cascades. Oecologia 160:563–575CrossRefGoogle Scholar
  44. Klassen G, Locke A (2007) A biological synopsis of the European green crab, Carcinus maenas (ed. Gulf Fisheries Center DoFaOC). Canadian manuscript report of fisheries and aquatic sciencesGoogle Scholar
  45. Kolbe JJ, Larson A, Losos JB (2007) Differential admixture shapes morphological variation among invasive populations of the lizard Anolis sagrei. Mol Ecol 16:1579–1591CrossRefGoogle Scholar
  46. Leach WE (1814) Crustaceology. In: Brewster D (ed) The Edinburgh encyclopaedia. Edinburgh, BlackwoodGoogle Scholar
  47. Leroux PJ, Branch GM, Joska MAP (1990) On the distribution, diet and possible impact of the invasive European shore crab Carcinus maenas (L) along the South African coast. S Afr J Mar Sci 9:85–93Google Scholar
  48. Lovell S, Besedin E, Grosholz E (2007) Modeling economic impacts of the European green crab. Paper presented at: American Agricultural Economics Association annual meeting, Portland, July 29–Aug 1 2007Google Scholar
  49. Manel S, Gaggiotti OE, Waples RS (2005) Assignment methods: matching biological questions techniques with appropriate. Trends Ecol Evol 20:136–142CrossRefGoogle Scholar
  50. Marino IAM, Barbisan F, Gennari M, Bisol PM, Zane L (2008) Isolation and characterization of microsatellite loci in the Mediterranean shore crab Carcinus aestuarii (Decapoda, Portunidae). Mol Ecol Res 8:370–372CrossRefGoogle Scholar
  51. Mergeay J, Verschuren D, De Meester L (2006) Invasion of an asexual American water flea clone throughout Africa and rapid displacement of a native sibling species. Proc R Soc Lond B Biol Sci 273:2839–2844CrossRefGoogle Scholar
  52. Miura O (2007) Molecular genetic approaches to elucidate the ecological and evolutionary issues associated with biological invasions. Ecol Res 22:876–883CrossRefGoogle Scholar
  53. Muirhead JR, Gray DK, Kelly DW, Ellis SM, MacIsaac HJ (2008) Identifying the source of species invasions: sampling intensity vs. genetic diversity. Mol Ecol 17:1020–1035CrossRefGoogle Scholar
  54. Rieseberg LH, Kim SC, Randell RA, Whitney KD, Gross BL, Lexer C, Clay K (2007) Hybridization and the colonization of novel habitats by annual sunflowers. Genetica 129:149–165CrossRefGoogle Scholar
  55. Rollins LA, Woolnough AP, Sherwin WB (2006) Population genetic tools for pest management: a review. Wildl Res 33:251–261CrossRefGoogle Scholar
  56. Roman J (2006) Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proc R Soc Lond B Biol Sci 273:2453–2459CrossRefGoogle Scholar
  57. Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464CrossRefGoogle Scholar
  58. Roman J, Palumbi SR (2004) A global invader at home: population structure of the green crab, Carcinus maenas, in Europe. Mol Ecol 13:2891–2898CrossRefGoogle Scholar
  59. Stepien CA, Brown JE, Neilson ME, Tumeo MA (2005) Genetic diversity of invasive species in the Great Lakes versus their Eurasian source populations: insights for risk analysis. Risk Anal 25:1043–1060CrossRefGoogle Scholar
  60. Tepolt CK, Bagley MJ, Geller JB, Blum MJ (2006) Characterization of microsatellite loci in the European green crab (Carcinus maenas). Mol Ecol Notes 6:343–345CrossRefGoogle Scholar
  61. Tepolt CK, Darling JA, Bagley MJ, Geller JB, Blum MJ, Grosholz ED (2009) European green crabs (Carcinus maenas) in the northeastern Pacific: genetic evidence for high population connectivity and current-mediated expansion from a single introduced source population. Diver Distrib 15:997–1009CrossRefGoogle Scholar
  62. Thresher RE, Kuris AM (2004) Options for managing invasive marine species. Biol Invas 6:295–300CrossRefGoogle Scholar
  63. Thresher R, Proctor C, Ruiz G, Gurney R, MacKinnon C, Walton W, Rodriguez L, Bax N (2003) Invasion dynamics of the European shore crab, Carcinus maenas, in Australia. Mar Biol 142:867–876Google Scholar
  64. Vellend M, Harmon LJ, Lockwood JL, Mayfield MM, Hughes AR, Wares JP, Sax DF (2007) Effects of exotic species on evolutionary diversification. Trends Ecol Evol 22:481–488CrossRefGoogle Scholar
  65. 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 102:5432–5437CrossRefGoogle Scholar
  66. Wares JP, Hughes AR, Grosberg RK (2005) Mechanisms that drive evolutionary change: insights from species introductions and invasions. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer Associates, SunderlandGoogle Scholar
  67. Yamada SB (2000) Global invader: the European green crab. Oregon Seagrant, CorvallisGoogle Scholar
  68. Yamada SB, Hauck L (2001) Field identification of the European green crab species: Carcinus maenas and Carcinus aestuarii. J Shell Fish Res 20:905–912Google Scholar
  69. Yamada S, Hunt C (2000) The arrival and spread of the European green crab, Carcinus maenas, in the Pacific Northwest. Dreissena 11:1–7Google Scholar
  70. Yamada SB, Kosro PM (in press) Linking ocean conditions to year class strength of the invasive European green crab, Carcinus maenas. Biol Invas 12:1791–1804 Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.National Exposure Research LaboratoryUS EPACincinnatiUSA

Personalised recommendations