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Invasion dynamics: interactions between the European Green Crab Carcinus maenas and the Asian Shore Crab Hemigrapsus sanguineus

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Abstract

As ecosystems are increasingly inhabited by multiple invasive species, interactions among exotic species have the potential to negatively impact native communities and habitats, often in counterintuitive ways. In rocky intertidal habitats along southern New England, the recently introduced Asian Shore Crab, Hemigrapsus sanguineus, has been implicated in the displacement of the more established invasive European Green Crab, Carcinus maenas. We coupled faunal sampling with two field experiments to examine whether H. sanguineus is also displacing C. maenas in the Gulf of Maine. First, we investigated natural recruitment of the two species across an elevation gradient, using cage exclusion units to manipulate predator access. Excluding H. sanguineus adults significantly increased the density of C. maenas recruits, but not conspecific recruit density. Next, to simulate the transition that occurred from pre-invasion to the establishment of H. sanguineus, we conducted a predator inclusion experiment manipulating the density of adult H. sanguineus to examine the effects on C. maenas and conspecific recruit densities. In contrast to the previous experiment, we found that the density of H. sanguineus included in cages negatively affected conspecific recruit density but had no effect on C. maenas recruit density. We hypothesize that juxtaposing results from the two experiments may be a consequence of the considerably greater abundance of C. maenas recruits relative to H. sanguineus recruits during the first experiment. Our work highlights the importance of considering the multitude of factors that influence competitive and intraguild predation interactions, including density-dependent effects, ontogeny and life history characteristics.

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References

  • Abrams PA, Fung SR (2010) Prey persistence and abundance in systems with intraguild predation and type-2 functional responses. J Theor Biol 264:1033–1042

    Article  PubMed  Google Scholar 

  • Amarasekare P (2008) Coexistence of intraguild predators and prey in resource-rich environments. Ecology 89:2786–2797

    Article  PubMed  Google Scholar 

  • Arim M, Marquet PA (2004) Intraguild predation: a widespread interaction related to species biology. Ecol Lett 7:557–564

    Article  Google Scholar 

  • Baillie CJ, Grabowski JH (2018) Competitive and agonistic interactions between the invasive Asian shore crab and juvenile American lobster. Ecology 99:2067–2079

    Article  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2014) lme4: linear mixed-effects models using Eigen and S4. R package version 1

  • Bretz F, Hothorn T, Westfall P (2010) Multiple comparisons using R. CRC Press, London

    Book  Google Scholar 

  • Briggs CJ, Borer ET (2005) Why short-term experiments may not allow long-term predictions about intraguild predation. Ecol Appl 15:1111–1117

    Article  Google Scholar 

  • Brönmark C, Hansson LA (2000) Chemical communication in aquatic systems: an introduction. Oikos 88:103–109

    Article  Google Scholar 

  • Byers JE (2000) Competition between two estuarine snails: implications for invasions of exotic species. Ecology 81:1225–1239

    Article  Google Scholar 

  • Carlton JT (1989) Man’s role in changing the face of the ocean: biological invasions and implications for conservation of near-shore environments. Conserv Lett 3:265–273

    Google Scholar 

  • Delaney DG, Griffen BD, Leung B (2011) Does consumer injury modify invasion impact? Biol Invasions 13:2935–2945

    Article  Google Scholar 

  • Drake JM, Lodge DM (2007) Hull fouling is a risk factor for intercontinental species exchange in aquatic ecosystems. Aquat Invasions 2:121–131

    Article  Google Scholar 

  • Ebling FJ, Kitching JA, Muntz L, Taylor CM (1964) The ecology of lough ine. J Anim Ecol 33:73–82

    Article  Google Scholar 

  • Ehrenfeld JG (2003) Effects of exotic plant invasions on soil nutrient cycling processes. Ecosystems 6:503–523

    Article  CAS  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 

  • Fox LR (1975) Cannibalism in natural populations. Annu Rev Ecol Syst 6:87–106

    Article  Google Scholar 

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

    Google Scholar 

  • Gilman M, Grace SP (2009) Use of subtidal habitat by the Asian shore crab Hemigrapsus sanguineus in Long Island Sound. Northeast Nat 16:481–487

    Article  Google Scholar 

  • Griffen BD (2011) Ecological impacts of replacing one invasive species with another in rocky intertidal areas. In: Galil B, Clark P, Carlton J (eds) In the wrong place-alien marine crustaceans: distribution, biology and impacts. Invading nature-springer series in invasion ecology, vol 6. Springer, Dordrecht

    Google Scholar 

  • Griffen BD (2016) Scaling the consequences of interactions between invaders from the individual to the population level. Ecol Evol 6:1769–1777

    Article  PubMed  PubMed Central  Google Scholar 

  • Griffen BD, Byers JE (2006) Intraguild predation reduces redundancy of predator species in multiple predator assemblage. J Anim Ecol 75:959–966

    Article  PubMed  Google Scholar 

  • Griffen BD, Delaney DG (2007) Species invasion shifts the importance of predator dependence. Ecology 88:3012–3021

    Article  PubMed  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 

  • Griffen BD, Altman I, Hurley J, Mosblack H (2011) Reduced fecundity by one invader in the presence of another: a potential mechanism leading to species replacement. J Exp Mar Biol Ecol 406:6–13

    Article  Google Scholar 

  • Grosholz ED (2005) Recent biological invasion may hasten invasional meltdown by accelerating historical introductions. Proc Natl Acad Sci USA 102:1088–1091

    Article  PubMed  CAS  Google Scholar 

  • Hart DR (2002) Intraguild predation, invertebrate predators, and trophic cascades in lake food webs. J Theor Biol 218:111–128

    Article  PubMed  Google Scholar 

  • Holt RD, Polis GA (1997) A theoretical framework for intraguild predation. Am Nat 149:745–764

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P, Heiberger R, Schuetzenmeister A, Scheibe S (2013) Multcomp: simultaneous inference in general parametric models. Version 1.3-0

  • Jensen GC, McDonald PS, Armstrong DA (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 

  • Juliano SA, O’Meara GF, Morrill JR, Cutwa MM (2002) Desiccation and thermal tolerance of eggs and the coexistence of competing mosquitoes. Oecologia 130:458–469

    Article  PubMed  PubMed Central  Google Scholar 

  • Kitchell JF, Schindler DE, Ogutu-Ohwayo R, Reinthal PN (1997) The Nile perch in Lake Victoria: interactions between predation and fisheries. Ecol Appl 7:653–664

    Article  Google Scholar 

  • Klassen GJ, Locke A (2007) A biological synopsis of the European green crab, Carcinus maenas. Can Manuscr Rep Fish Aquat Sci no. 2818: vii-75

  • Kraemer GP, 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 

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

    Article  Google Scholar 

  • Lodge DM (1993) Biological invasions: lessons for ecology. Trends Ecol Evol 8:133–137

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Lohrer AM, Whitlatch RB (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 

  • McDermott JJ (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 JJ (1998) The western Pacific brachyuran (Hemigrapsus sanguineus: Grapsidae), in its new habitat along the Atlantic coast of the United States: geographic distribution and ecology. ICES J Mar Sci 55:289–298

    Article  Google Scholar 

  • Menge BA (1983) Components of predation intensity in the low zone of the New England rocky intertidal region. Oecologia 58:141–155

    Article  PubMed  Google Scholar 

  • Moksnes PO (2004) Interference competition for space in nursery habitats: density-dependent effects on growth and dispersal in juvenile shore crabs Carcinus maenas. Mar Ecol Prog Ser 281:181–191

    Article  Google Scholar 

  • Moksnes P, Pihl L, Van Montfrans J (1998) Predation on postlarvae and juveniles of the shore crab Carcinus maenas: importance of shelter, size and cannibalism. Mar Ecol Prog Ser 166:211–225

    Article  Google Scholar 

  • Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Environ 6:485–492

    Article  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 

  • Polis GA, Holt RD (1992) Intraguild predation: the dynamics of complex trophic interactions. Trends Ecol Evol 7:151–154

    Article  PubMed  CAS  Google Scholar 

  • R Core Team (2015) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Rossong M, Williams P, Comeau M, Mitchell S, Apaloo J (2006) Agonistic interactions between the invasive green crab, Carcinus maenas (Linnaeus), and juvenile American lobster, Homarus americanus (Milne Edwards). J Exp Mar Biol Ecol 329:281–288

    Article  Google Scholar 

  • Savaria MC, O’Connor NJ (2013) Predation of the non-native Asian shore crab Hemigrapsus sanguineus by a native fish species, the cunner (Tautogolabrus adspersus). J Exp Mar Biol Ecol 449:335–339

    Article  Google Scholar 

  • Say T (1969) An account of the Crustacea of the United States. J Acad Nat Sci Phila 1:445–458

    Google Scholar 

  • Scattergood LW (1952) The distribution of the green crab, Carcinus maenas (L.) in the northwestern Atlantic. Me. Department of Sea and Shore Fisheries

  • Schausberger P (1999) Predation preference of Typhlodromus pyri and Kampimodromus aberrans (Acari: Phytoseiidae) when offered con-and heterospecific immature life stages. Exp Appl Acarol 23:389–398

    Article  Google Scholar 

  • Simberloff D (2006) Invasional meltdown 6 years later: important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919

    Article  PubMed  Google Scholar 

  • Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasional meltdown? Biol Invasions 1:21–32

    Article  Google Scholar 

  • Strayer DL, Eviner VT, Jeschke JM, Pace ML (2006) Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–651

    Article  PubMed  Google Scholar 

  • Therneau TM, Atkinson B, Ripley B (2010) rpart: Recursive partitioning. R package version 3

  • Tilman D (1990) Constraints and tradeoffs: toward a predictive theory of competition and succession. Oikos 58:3–15

    Article  Google Scholar 

  • Trussell GC, Ewanchuk PJ, Bertness MD (2003) Trait-mediated effects in rocky intertidal food chains: predator risk cues alter prey feeding rates. Ecology 84:629–640

    Article  Google Scholar 

  • Vincent T, Scheel D, Brown J, Vincent T (1996) Trade-offs and coexistence in consumer-resource models: it all depends on what and where you eat. Am Nat 148:1038–1058

    Article  Google Scholar 

  • Wallentinus I, Nyberg CD (2007) Introduced marine organisms as habitat modifiers. Mar Pollut Bull 55:323–332

    Article  PubMed  CAS  Google Scholar 

  • Warman C, Reid D, Naylor E (1993) Variation in the tidal migratory behaviour and rhythmic light-responsiveness in the shore crab, Carcinus maenas. J Mar Biol Assoc UK 73:355–364

    Article  Google Scholar 

  • Wiles GJ, Bart J, Beck RE, Aguon CF (2003) Impacts of the brown tree snake: patterns of decline and species persistence in Guam’s avifauna. Conserv Biol 17:1350–1360

    Article  Google Scholar 

  • Williams P, Floyd T, Rossong M (2006) Agonistic interactions between invasive green crabs, Carcinus maenas (Linnaeus), and sub-adult American lobsters, Homarus americanus (Milne Edwards). J Exp Mar Biol Ecol 329:66–74

    Article  Google Scholar 

  • Wissinger SA (1992) Niche overlap and the potential for competition and intraguild predation between size-structured populations. Ecology 73:1431–1444

    Article  Google Scholar 

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Acknowledgements

We thank Allison Matzelle, Kelsey Schultz, and Lucy Harrington for their assistance with experimental setup and sampling. We thank Louise Cameron, Chris Conroy, Theresa Davenport, Marissa McMahan and Robert Murphy for their assistance with monthly field surveys.

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Correspondence to Christopher Baillie.

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Baillie, C., Grabowski, J.H. Invasion dynamics: interactions between the European Green Crab Carcinus maenas and the Asian Shore Crab Hemigrapsus sanguineus. Biol Invasions 21, 787–802 (2019). https://doi.org/10.1007/s10530-018-1858-1

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