Abstract
Reconstructing the invasion history of aquatic invasive species can enhance understanding of invasion risks by recognizing areas most susceptible to invasion and forecasting future spread based on past patterns of population expansion. Here we reconstruct the invasion history of the Japanese amphipod Grandidierella japonica Stephensen 1938 combining information from historical collection data with molecular genetic data to better understand post-invasion range expansion and anthropogenic connectivity across the Pacific coast of North America. Compilation of collection data from bays and estuaries of the Pacific North American coast show many new localities have been colonized in the last two decades, moving outward from harbors and bays with high commercial traffic into smaller coastal locations dominated by local recreational traffic. DNA barcode sequence data for G. japonica reveals two distinct clades: one found in San Francisco Bay and sites to the north, and one also found in San Francisco Bay and sites to the south. The two clades differ by an average 7.28 % genetic distance, large enough to consider these invasive amphipods two separate species. Both northern and southern clades exhibit low levels of genetic diversity, suggesting a single introduction event for each. The presence of cryptic diversity within this invasive amphipod highlights the need for more extensive study of the invasive and native populations of aquatic invasive invertebrates to address questions of taxonomy, diversity, and invasion history.
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References
Audet D, Davis DS, Miron G, Moriyasu M, Benhalima K, Campbell R (2003) Geographic expansion of a nonindigenous crab, Carcinus maenas (L.), along the Nova Scotian shore into the southeastern Gulf of St. Lawrence, Canada. J Shellfish Res 22:255–262
Barnard JL, Sanved K, Thomas JD (1991) Tube-building behavior in Grandidierella, and 2 species of Cerapus. Hydrobiologia 223:239–254
Bastrop R, Jurss K, Sturmbauer C (1998) Cryptic species in a marine polychaete and their independent introduction from North America to Europe. Mol Biol Evol 15:97–103
Blakeslee AMH, McKenzie CH, Darling JA, Byers JE, Pringle JM, Roman J (2010) A hitchhiker’s guide to the Maritimes: anthropogenic transport facilitates long-distance dispersal of an invasive marine crab to Newfoundland. Divers Distrib 16:879–891
Blum MJ, Bando KJ, Katz M, Strong DR (2007) Geographic structure, genetic diversity and source tracking Spartina alterniflora. J Biogeog 34:2055–2069
Byers JE (1999) The distribution of an introduced mollusc and its role in the long-term demise of a native confamilial species. Biol Invasions 1:339–352
Carlton JT (1996) Pattern, process, and prediction in marine invasion ecology. Biol Conserv 78:97–106
Carlton JT (2009) Deep invasion ecology and the assembly of communities in historical time. In: Rilov G, Crooks JA (eds) Biological invasion in marine ecosystems: ecological, management, and geographic perspectives. Springer, Berlin
Carlton JT, Geller JB (1993) Ecological roulette: the global transport and invasion of nonindigenous marine organisms. Science 261:78–82
Castillo GC (2000) Benthic biological invasions in two temperate estuaries and their effects on trophic relations of native fish and community stability. PhD dissertation, Oregon State University, Corvallis, OR
Chapman JW (2007) Gammaridea. In: Carlton JT (ed) The light and smith manual: intertidal invertebrates from Central California to Oregon, 4th edn. University of California Press, Berkeley
Chapman JW, Dorman JA (1975) Diagnosis, systematics, and notes on Grandidierella japonica (Amphipoda: Gammaridae) and its introduction to the Pacific coast of the United States. Bull Southern California Acad Sci 74:104–108
Cohen AN, Carlton JT (1995) Nonindigenous aquatic species in a United States Estuary: a case study of the biological invasions of the San Francisco Bay and delta. Report for the US Fish Wildlife Ser, Wash., DC, and Nat Sea Grant College Program Connecticut Sea Grant
Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558
Colautti RI, Manca M, Viljanen M, Ketelaars HAM, Burgi H, MacIsaac HJ, Heath DD (2005) Invasion genetics of the Eurasian spiny waterflea: evidence for bottlenecks and gene flow using microsatellites. Mol Ecol 14:1869–1879
Costa FO, Henzler CM, Lunt DH, Whiteley N, Rock J (2009) Probing marine Gammarus (Amphipoda) taxonomy with DNA barcodes. Syst Biodivers 7:365–379
Darling JA (2011) Interspecific hybridization and mitochondrial introgression in invasive Carcinus shore crabs. PLoS ONE 6(3):e17828
Darling JA, Herborg L-M, Davidson I (2012) Intracoastal shipping drives patterns of regional population expansion by an invasive marine invertebrate. Ecol Evol 2(10):2557–2566
Davidson SK, Haygood MG (1999) Identification of sibling species of the bryozoan Bugula neritina that produce different anticancer bryostatins and harbor distinct strains of the bacterial symbiont Candidatus endobugula sertula. Biol Bull 196:273–280
Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17:431–449
Dumbauld BR (1994) Thalassinid shrimp ecology and the use of carbaryl to control populations on oyster ground in Washington coastal estuaries. PhD dissertation, University of Washington, Seattle, WA
Dumbauld BR, Brooks KM, Posey MH (2001) Response of an estuarine benthic community to application of the pesticide carbaryl and cultivation of pacific oysters (Crassostrea gigas) in Willapa Bay, Washington. Mar Poll Bull 42:826–844
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1:47–50
Facon B, Pointier J-P, Jarne P, Sarda V, David P (2008) High genetic variance in life-history strategies within invasive populations by way of multiple introductions. Current Biol 18:363–367
Feldman KL, Armstrong DA, Dumbauld BR, DeWitt TH, Doty DC (2000) Oysters, crabs, and burrowing shrimp: review of an environmental conflict over aquatic resources and pesticide use in Washington State’s (USA) coastal estuaries. Estuaries 23:141–176
Ferraro SP, Cole FA (2004) Optimal benthic macrofaunal sampling protocol for detecting differences among four habitats in Willapa Bay, Washington, USA. Estuaries 27:1014–1025
Figuerola J, Green AJ (2002) Dispersal of aquatic organisms by waterbirds: a review of past research and priorities for future studies. Fresh Biol 47:483–494
Figuerola J, Green AJ, Michot TC (2005) Invertebrate eggs can fly: evidence of waterfowl-mediated gene flow in aquatic invertebrates. Am Nat 165:274–280
Fofonoff PW, Ruiz GM, Steves B, Carlton JT (2003) In ships or on ships? Mechanisms of transfer and invasion for nonnative species to the coasts of North America. In: Ruiz GM, Carlton JT (eds) Invasive species: vectors and management strategies. Island Press, Washington, DC)
Folino-Rorem NC, Darling JA, D’Ausilio CA (2009) Genetic analysis reveals multiple cryptic invasive speciesof the hydrozoan genus Cordylophora. Biol Invasions 11:1869–1882
Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3:294–297
Geller JB, Darling JA, Carlton JT (2010) Genetic perspectives on marine biological invasions. Ann Rev Mar Sci 2:401–427
Goloboff PA (1999) Nona, version 2. http://www.cladistics.com/aboutNona.htm. Accessed 19 Apr 2012
Greenstein D, Tienfenthaler L (1997) Reproduction and population dynamics of Grandidierella japonica in upper Newport Bay, California. Bull So Cal Acad Sci 96:34–42
Griffen BD, DeWitt TH, Langon C (2004) Particle removal rates by the mud shrimp Upogebia pugettensis, its burrow, and a commensal clam: effects on estuarine phytoplankton abundance. Mar Ecol Prog Ser 269:223–236
Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc Lond B 270:313–321
Hoos PM, Miller AW, Ruiz GM, Vrijenhoek RC, Geller JB (2010) Genetic and historical evidence disagree on likely sources of the Atlantic amethyst gem clam Gemma gemma (Totten, 1834) in California. Divers Distrib 16:582–592
Johnson JA (1998) Bay clam data series report. Oregon Department of Fish and Wildlife, Marine Resources Program, Newport, OR
Knox MA, Hogg IA, Pilditch CA (2011) The role of vicariance and dispersal on New Zealand’s estuarine biodiversity: the case of Paracorophium (Crustacea: Amphipoda). Biol J Linnean Soc 103:863–874
Kolbe JJ, Glor RE, Schettino LR, Lara AC, Larson A, Losos JB (2007) Multiple sources, admixture, and genetic variation in introduced Anolis Lizard populations. Conserv Biol 21:1612–1625
Kumar S, Tamura K, Nei M (2004) MEGA 3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220
Myers AA (1970) Taxonomic studies of the genus Grandidierella Coutiere (Crustacea: Amphipoda), with a description of G. dentimera, sp. nov. Bull Mar Sci 20:135–147
Nelson WG, Lee II H, Lamberson JO, Engle V, Harwell L, Smith LM (2004) Condition of estuaries of the Western United States for 1999: a statistical summary. Office of Research and Development, National Health and Environmental Effects Research Laboratory, EPA/620/R-04/200
Nelson WG, Lee II H, Lamberson JO (2005) Condition of Estuaries of California for 1999: a statistical summary. Office of Research and Development, National Health and Environmental Effects Research Laboratory, EPA/620/R-05/004
Nixon KC (1999) Winclada (beta), version 0.9.9 published by the author, Ithaca, NY. http://www.cladistics.com/about_winc.htm. Accessed 19 Apr 2012
Peakall R, Smouse PE (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 1:288–295
Petersen CH, Black R (1987) Resource depletion by active suspension feeders on tidal flats: influence of local density and tidal elevation. Limnol Oceanogr 32:143–166
Pilgrim EM, Darling JA (2010) Genetic diversity in two introduced biofouling amphipods (Ampithoe valida & Jassa marmorata) along the Pacific North American coast: investigation into molecular identification and cryptic diversity. Divers Distrib 16:827–839
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256
Pringle JM, Blakeslee A, Byers J, Roman J (2011) Asymmetric dispersal allows an upstream region to control population structure throughout a species’ range. Proc Natl Acad Sci USA 108(37):15288–15293
Reusser DA, Lee II H, Hillman L, Kluza DA (2004) The “Pacific Coast Estuarine Information System”: creating a baseline for the future. Proceedings of the 13th international conference on aquatic invasive species
Roman J (2006) Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proc R Soc B Biol Sci 273:2453–2459
Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. Trends Ecol Evol 22:454–464
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574
Ruesink JL, Roegner GC, Dumbauld BR, Newton JA, Armstrong DA (2003) Contributions of coastal and watershed energy sources to secondary production in a Northeastern Pacific estuary. Estuaries 26:1079–1093
Ruiz GM, Carlton JT, Grosholz ED, 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
Schoenberg SA, Carlson RE (1984) Direct and indirect effects of zooplankton grazing on phytoplankton in a hypereutrophic lake. Oikos 42:291–302
Stachowicz JJ, Terwin JR, Whitlach RB, Osman RW (2002) Linking climate change and biological invasions: ocean warming facilitates non-indigenous species invasion. Proc Natl Acad Sci USA 99:15497–15500
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. Divers Distrib 15:997–1009
USGS (2004) Nonindigenous aquatic species database, Gainesville, FL. http://nas.er.usgs.gov. January 6, 2006 query
Wasson K, Zabin CJ, Bedinger L, Diaz MC, Pearse JS (2001) Biological invasions of estuaries without international shipping: the importance of intraregional transport. Biol Conserv 102:143–153
West JM, Cordrey M, Madon SP, Zedler JB (2002) Tijuana river national estuarine research reserve: annual report on ecosystem monitoring. Annual Report for Monitoring Conducted July 1, 2001–June 30, 2002. Report for NOAA National Ocean Service, Sanctuaries and Programs Division
Williams GD, West JM, Zedler JB (2001) Shifts in fish and invertebrate assemblages of two Southern California estuaries during the 1997–1998 El Niño. Bull So Calif Acad Sci 100:212–237
Witt JDS, Threloff DL, Hebert PDN (2006) DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: implications for desert spring conservation. Mol Ecol 15:3073–3082
Acknowledgments
We would like to thank Dr. Bruce Boese, Dr. John Chapman and Janet Lamberson for their insightful comments on an earlier manuscript and for collecting amphipods in Yaquina Bay, Oregon. We also would like to thank Jack Kelly, Florence Fulk, Mark Bagley, and two anonymous reviewers for their comments on this manuscript. The views expressed in this manuscript are those of the authors and do not necessarily reflect the views or policies of the US Environmental Protection Agency or the US Geological Survey.
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Pilgrim, E.M., Blum, M.J., Reusser, D.A. et al. Geographic range and structure of cryptic genetic diversity among Pacific North American populations of the non-native amphipod Grandidierella japonica . Biol Invasions 15, 2415–2428 (2013). https://doi.org/10.1007/s10530-013-0462-7
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DOI: https://doi.org/10.1007/s10530-013-0462-7