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Increase in density of genetically diverse invasive Asian shore crab (Hemigrapsus sanguineus) populations in the Gulf of Maine

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Abstract

Hemigrapsus sanguineus, the Asian shore crab, has rapidly replaced Carcinus maenas, the green crab, as the most abundant crab on rocky shores in the northwest Atlantic since its introduction to the United States (USA) in 1988. The northern edge of this progressing invasion is the Gulf of Maine, where Asian shore crabs are only abundant in the south. We compared H. sanguineus population densities to those from published 2005 surveys and quantified genetic variation using the cytochrome c oxidase subunit I gene. We found that the range of H. sanguineus had extended northward since 2005, that population density had increased substantially (at least 10-fold at all sites), and that Asian shore crabs had become the dominant intertidal crab species in New Hampshire and southern Maine. Despite the significant increase in population density of H. sanguineus, populations only increased by a factor of 14 in Maine compared to 70 in southern New England, possibly due to cooler temperatures in the Gulf of Maine. Genetically, populations were predominantly composed of a single haplotype of Japanese, Korean, or Taiwanese origin, although an additional seven haplotypes were found. Six of these haplotypes were of Asian origin, while two are newly described. Large increases in population sizes of genetically diverse individuals in Maine will likely have a large ecological impact, causing a reduction in populations of mussels, barnacles, snails, and other crabs, similar to what has occurred at southern sites with large populations of this invasive crab species.

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References

  • Albins MA (2013) Effects of invasive Pacific red lionfish Pterois volitans versus a native predator on Bahamian coral-reef fish communities. Biol Invasions 15:29–43

    Article  Google Scholar 

  • Audet D, Davis D, Miron G, Moriyasu M (2003) Geographical 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

    Google Scholar 

  • Blakeslee A, McKenzie C, Darling J, Byers JE, Darling J, Pringle J, 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

    Article  Google Scholar 

  • Blasi JC, O’Connor NJ (2016) Amphipods as potential prey of the Asian shore crab Hemigrapsus sanguineus: laboratory and field experiments. J Exp Mar Biol Ecol 474:18–22

    Article  Google Scholar 

  • Bourdeau P, O’Connor N (2003) Predation by the nonindigenous Asian shore crab Hemigrapsus sanguineus on macroalgae and molluscs. Northeast Nat 10:319–334

    Article  Google Scholar 

  • Breton G, Faasse M, Noel P, Vincent T (2002) A new alien crab in Europe: Hemigrapsus sanguineus (Decapoda: Brachyura: Grapsidae). J Crustac Biol 22:184–189

    Article  Google Scholar 

  • Brousseau DJ, Filipowicz A, Baglivo JA (2001) Laboratory investigations of the effects of predator sex and size on prey selection by the Asian crab, Hemigrapsus sanguineus. J Exp Mar Biol Ecol 262:199–210

    Article  PubMed  Google Scholar 

  • Brousseau DJ, Goldberg R, Garza C (2014) Impact of predation by the invasive crab Hemigrapsus sanguineus on survival of juvenile blue mussels in western Long Island Sound. Northeast Nat 21:119–133

    Article  Google Scholar 

  • 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 30:1809–1820

    Article  Google Scholar 

  • Carlton J, Geller J (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82

    Article  Google Scholar 

  • Clavero M, García-Berthou E (2005) Invasive species are a leading cause of animal extinctions. Trends Ecol Evol 20:110

    Article  PubMed  Google Scholar 

  • Clement M, Posada D, Krandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9(10):1657–1659

    Article  PubMed  CAS  Google Scholar 

  • Darling J (2011) Interspecific hybridization and mitochondrial introgression in invasive Carcinus shore crabs. PLoS ONE 6(3):e17828

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 17:4992–5007

    Article  PubMed  CAS  Google Scholar 

  • Darling J, Tsai Y-H, Blakeslee A, Roman J (2014) Are genes faster than crabs? Mitochondrial introgression exceeds larval dispersal during population expansion of the invasive crab Carcinus maenas. R Soc Open Sci 1(2):140202

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • DeGraaf J, Tyrrell M (2004) Comparison of the feeding rates of two introduced crab species, Carcinus maenas and Hemigrapsus sanguineus, on the blue mussel, Mytilus edulis. Northeast Nat 11:163–166

    Article  Google Scholar 

  • Demeo A, Riley JG (2006) Hemigrapsus sanguineus (Asian Shore Crab) as predator of juvenile Homarus americanus (American Lobster). Tech Bull Maine Agric For Exp Stn 194:1–7

    Google Scholar 

  • Epifanio CE (2013) Invasion biology of the Asian shore crab Hemigrapsus sanguineus: a review. J Exp Mar Biol Ecol 441:33–49

    Article  Google Scholar 

  • Epifanio CE, Tilburg CE, Dittel AI (2013) Abundance of invasive and native crab larvae in the mouth of Delaware Bay: Hemigrapsus sanguineus and Uca Pugnax. J Shellfish Res 32:543–550

    Article  Google Scholar 

  • Floyd T, Williams J (2004) Impact of green crab (Carcinus maenas L.) predation on a population of softshell clams (Mya arenaria L.) in the southern Gulf of St. Lawrence. J Shellfish Res 23:457–462

    Google Scholar 

  • 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 Biotechnol 3(5):294–299

    PubMed  CAS  Google Scholar 

  • Griffen BD, Guy T, Buck JC (2008) Inhibition between invasives: a newly introduced predator moderates the impacts of a previously established invasive predator. J Anim Ecol 77:32–40

    Article  PubMed  Google Scholar 

  • Grosholz E, Ruiz G (1996) Predicting the impact of introduced marine species: lessons from the multiple invasions of the European green crab Carcinus maenas. Biol Conserv 3207:59–66

    Article  Google Scholar 

  • Hong S-E, Kim J-K, Yu J-N, Yoon M (2012) Genetic variation in the Asian shore crab Hemigrapsis sanguineus in Korean coastal waters as inferred from mitochondrial DNA sequences. Fish Aquat Sci 15(1):49–56

    CAS  Google Scholar 

  • Incze LS, Naimie CE (2000) Modelling the transport of lobster (Homarus americanus) larvae and postlarvae in the Gulf of Maine. Fish Oceanogr 9:99–113

    Article  Google Scholar 

  • Jensen G, McDonald P, Armstrong D (2002) East meets west: competitive interactions between green crab Carcinus maenas, and native and introduced shore crab Hemigrapsus spp. Mar Ecol Prog Ser 225:251–262

    Article  Google Scholar 

  • Kolber Z, Wyman KV, Falkowski PG (1990) Natural variability in photosynthetic energy conversion efficiency: a field study in the Gulf of Maine. Limnol Oceanogr 35:72–79

    Article  CAS  Google Scholar 

  • Kraemer G, Sellberg M, Gordon A, Main J (2007) Eight-year record of Hemigrapsus sanguineus (Asian shore crab) invasion in western Long Island sound estuary. Northeast Nat 14:207–224

    Article  Google Scholar 

  • Larkin M, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Ledesma M, O’Connor N (2001) Habitat and diet of the non-native crab Hemigrapsus sanguineus in southeastern New England. Northeast Nat 8:63–78

    Article  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452

    Article  PubMed  CAS  Google Scholar 

  • Lohrer A, Whitlatch R (2002a) Interactions among aliens: apparent replacement of one exotic species by another. Ecology 83:719–732

    Article  Google Scholar 

  • Lohrer A, Whitlatch R (2002b) Relative impacts of two exotic brachyuran species on blue mussel populations in Long Island Sound. Mar Ecol Prog Ser 227:135–144

    Article  Google Scholar 

  • Lohrer A, Fuikui Y, Wada K, Whitlatch R (2000) Structural complexity and vertical zonation of intertidal crabs, with focus on habitat requirements of the invasive Asian shore crab, Hemigrapsus sanguineus (de Haan). J Exp Mar Biol Ecol 244:203–217

    Article  Google Scholar 

  • Lord J, Dalvano B (2015) Differential response of the American lobster Homarus americanus to the invasive Asian shore crab Hemigrapsus sanguineus and green crab Carcinus maenas. J Shell Res 34:1091–1096

    Article  Google Scholar 

  • Lubchenco J (1978) Plant species diversity in a marine intertidal community: importance of herbivore food preference and algal competitive abilities. Am Nat 112:23–39

    Article  Google Scholar 

  • McDermott J (1991) A breeding population of the western Pacific crab Hemigrapsus sanguineus (Crustacea: Decapoda: Grapsidae) established on the Atlantic coast of North America. Biol Bull 181:195–198

    Article  PubMed  CAS  Google Scholar 

  • McDermott J (1998) The western Pacific brachyuran Hemigrapsus sanguineus (Grapsidae) in its new habitat along the Atlantic coast of the United States: reproduction. J Crustac Biol 18:308–316

    Article  Google Scholar 

  • Micu D, Niţă V, Todorova V (2010) First record of the Japanese shore crab Hemigrapsus sanguineus (de Haan, 1835) (Brachyura: Grapsoidea: Varunidae) from the Black Sea. Aquat Invasions 5:S1–S4

    Article  Google Scholar 

  • Mooney HA, Cleland EE (2001) The evolutionary impact of invasive species. Proc Natl Acad Sci 98(10):5446–5451

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York

    Book  Google Scholar 

  • O’Connor NJ (2014) Invasion dynamics on a temperate rocky shore: from early invasion to establishment of a marine invader. Biol Invasions 16:73–87

    Article  Google Scholar 

  • Payne A, Kraemer G (2013) Morphometry and claw strength of the non-native Asian shore crab, Hemigrapsus sanguineus. Northeast Nat 20:478–492

    Article  Google Scholar 

  • Pershing A, Alexander MA, Hernandez CM, Kerr LA, Le Bris A, Mills KE, Nye JA, Record NR, Scannell HA, Scott JD, Sherwood GD, Thomas AC (2015) Slow adaptation in the face of rapid warming leads to collapse of the Gulf of Maine cod fishery. Science 350:809–812

    Article  PubMed  CAS  Google Scholar 

  • Peterson BJ, Fournier AM, Furman BT, Carroll JM (2014) Hemigrapsus sanguineus in Long Island salt marshes: experimental evaluation of the interactions between an invasive crab and resident ecosystem engineers. PeerJ 2:e472

    Article  PubMed  PubMed Central  Google Scholar 

  • Raupach MJ, Barco A, Steinke D, Beermann J, Laakmann S, Mohrbeck I, Neumann H, Kihara TC, Pointner A, Segelken-Voigt A, Wesse C, Knebelsberger T (2015) The application of DNA barcodes for the identification of crustaceans from the North Sea and Adjacent Regions. PLoS ONE 10(9):e0139421

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Raymond M, Rousset F (1995) An exact test for population differentiation. Evolution 49(6):1280–1283

    Article  PubMed  Google Scholar 

  • Roman J (2006) Diluting the founder effect: cryptic invasions expand a marine invader’s range. Proc R Soc B 273:2453–2459

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruiz G, Carlton J (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632

    Article  Google Scholar 

  • Say T (1817) An account of the Crustacea of the United States. J Acad Nat Sci Phila 1:57–63

    Google Scholar 

  • Shiganova T (1998) Invasion of the Black Sea by the ctenophore Mnemiopsis leidyi and recent changes in pelagic community structure. Fish Oceanogr 7:305–310

    Article  Google Scholar 

  • Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47(1):264–279

    Article  PubMed  Google Scholar 

  • Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129(2):555–562

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Spilmont N, Gothland M, Seuront L (2015) Exogenous control of the feeding activity in the invasive Asian shore crab Hemigrapsus sanguineus (De Haan, 1835). Aquat Invasions 10:327–332

    Article  Google Scholar 

  • Steinberg, MK (2008) To be or not to be: the presence and absence of the Asian shore crab Hemigrapsus sanguineus in North America. Dissertation, University of Delaware

  • Stephenson EH, Steneck RS, Seeley RH (2009) Possible temperature limits to range expansion of non-native Asian shore crabs in Maine. J Exp Mar Biol Ecol 375:21–31

    Article  Google Scholar 

  • Tajima F (1983) Evolutionary relationship of DNA sequences in finite populations. Genetics 105(2):437–460

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tajima F, Nei M (1984) Estimation of evolutionary distance between nucleotide sequences. Mol Biol Evol 1(3):269–285

    PubMed  CAS  Google Scholar 

  • Tyrrell M, Guarino P, Harris L (2006) Predatory impacts of two introduced crab species: inferences from microcosms. Northeast Nat 13:375–390

    Article  Google Scholar 

  • Williams LM, Nivison CL, Ambrose WG, Dobbin R, Locke WL (2015) Lack of adult novel northern lineages of invasive green crab Carcinus maenas along much of the northern US Atlantic coast. Mar Ecol Prog Ser 532:153–159

    Article  PubMed  PubMed Central  Google Scholar 

  • Yoon M, Hong S-E, Nam Y, Kim D (2011) Genetic diversity of the Asian shore crab, Hemigrapsus sanguineus, in Korea and Japan inferred from mitochondrial cytochrome c oxidase subunit I gene. Anim Cells Syst 15(3):243–249

    Article  CAS  Google Scholar 

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Acknowledgements

Thanks to Brielle Dalvano and Dr. Zair Burris for assistance in the field and with measuring crabs in the laboratory, to Drs. Mia Steinberg, Charles Epifanio, and Shawn McCafferty for sharing their Hemigrapsus sanguineus COI sequences, and Alexandra Ulin for assistance with PCR. Additional thanks to the Bates College Biology Department for providing space and facilities for analysis. Funding provided by a Bates College startup fund 3457-2025 (to JPL), and a Bates College research reserve fund 3829-9155 (to LMW). Research reported in this project was supported by an Institutional Development Award (IDeA) from the National Institute of General Medical Sciences of the National Institutes of Health under Grant Number P20GM103423.

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Correspondence to Joshua P. Lord.

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Lord, J.P., Williams, L.M. Increase in density of genetically diverse invasive Asian shore crab (Hemigrapsus sanguineus) populations in the Gulf of Maine. Biol Invasions 19, 1153–1168 (2017). https://doi.org/10.1007/s10530-016-1304-1

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