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Biological Invasions

, Volume 19, Issue 3, pp 765–772 | Cite as

Conspecific tolerance and heterospecific competition as mechanisms for overcoming resistance to invasion by an intertidal crab

  • Niels-Viggo S. HobbsEmail author
  • J. Stanley Cobb
  • Carol S. Thornber
Original Paper

Abstract

The success of the invasive Asian shore crab, Hemigrapsus sanguineus, stems partly from its ability to exclude established crab species from preferred rocky and cobble intertidal habitat. Here, we assessed preference and competition for habitat types (cobble vs. sand) for H. sanguineus and two competitor species; the previous invasive green crab, Carcinus maenas, and the native rock crab, Cancer irroratus, in New England. In simple laboratory experiments, we paired similarly sized heterospecifics and conspecifics from each species, and also grouped combinations of C. maenas and H. sanguineus in a series of four-individual sets in order to dissect the outcome of intra- and inter-specific competition at different densities. Individually, all three species preferred cobble substrate. With paired conspecifics, H. sanguineus individuals would cohabitate in cobble, whereas C. maenas and C. irroratus individuals each excluded conspecifics from cobble. In heterospecific pairs, H. sanguineus excluded both C. maenas and C. irroratus from cobble. C. maenas and C. irroratus, were equally likely to exclude the other species, but rarely excluded H. sanguineus. In larger assemblages, H. sanguineus preferentially grouped under cobble, whereas C. maenas were more evenly distributed among habitat types. These observations demonstrate that conspecific tolerance and heterospecific competition can be effective, complementary mechanisms for overcoming invasion resistance. Such mechanisms help explain the well-studied success of H. sanguineus following its introduction into New England coastal habitats, and the resulting exclusion of preexisting crab species.

Keywords

Habitat competition Conspecific tolerance Invasion resistance Hemigrapsus sanguineus Carcinus maenas Cancer irroratus Rocky intertidal 

Notes

Acknowledgments

We thank D. Bengtson, J. Kolbe, S. Menden-Deuer, E. Preisser, and G. Puggioni for invaluable feedback and constructive guidance. Thanks, too, to two anonymous reviewers whose thorough comments greatly improved this manuscript. D. Corideo, D. Hudson, R. Stadnick and D. Wieczorek helped greatly with crab collection, and set-up and maintenance of the experiments. Funding was provided by a graduate research Grant from the College of Arts and Sciences at the University of Rhode Island.

References

  1. Aguilera MA, Navarrete SA (2012) Interspecific competition for shelters in territorial and gregarious intertidal grazers: consequences for individual behaviour. PLoS One 7(9):e46205. doi: 10.1371/journal.pone.0046205 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alexander RD (1974) The evolution of social behavior. Annu Rev Ecol Syst 5:325–383CrossRefGoogle Scholar
  3. Best RJ, Caulk NC, Stachowicz JJ (2013) Trait vs. phylogenetic diversity as predictors of competition and community composition in herbivorous marine amphipods. Ecol Lett 16:72–80. doi: 10.1111/ele.12016 CrossRefPubMedGoogle Scholar
  4. Boulangeat I, Gravel D, Thuiller W (2012) Accounting for dispersal and biotic interactions to disentangle the drivers of species distributions and their abundances. Ecol Lett 15:584–593. doi: 10.1111/j.1461-0248.2012.01772.x CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125. doi: 10.1016/S0169-5347(02)00045-9 CrossRefGoogle Scholar
  6. Bruno JE, Fridley JD, Bromberg KD, Bertness MD (2005) Insights into biotic interactions from studies of species invasions. In: Sax DF, Stachowicz JJ, Gaines SD (eds) Species invasions: insights into ecology, evolution, and biogeography. Sinauer, Sunderland, p 495Google Scholar
  7. Carlton JT (2011) The global dispersal of marine and estuarine crustaceans. In: Galil BS, Clark PF, Carlton JT (eds) In the wrong place–alien marine crustaceans: distribution, biology and impacts. Springer, New York. doi: 10.1007/978-94-007-0591-3_1 Google Scholar
  8. Carlton JT, Cohen AN (2003) Episodic global dispersal in shallow water marine organisms: the case history of the European shore crabs Carcinus maenas and Carcinus aestuarii. J Biogeogr 30:1809–1820. doi: 10.1111/j.1365-2699.2003.00962.x CrossRefGoogle Scholar
  9. Caut S, Casanovas JG, Virgos E, Lozano J, Witmer GW, Courchamp F (2007) Rats dying for mice: modelling the competitor release effect. Austral Ecol 32:858–868. doi: 10.1111/j.1442-9993.2007.01770.x CrossRefGoogle Scholar
  10. Connell JH (1961) The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42:710–723. doi: 10.2307/1933500 CrossRefGoogle Scholar
  11. DeGoursey RE, Auster PJ (1992) A mating aggregation of the spider crab (Libinia emarginata). J Northwest Atl Fish Sci 13:77–82CrossRefGoogle Scholar
  12. Dijkstra JA, Boudreau J, Dionne M (2012) Species-specific mediation of temperature and community interactions by multiple foundation species. Oikos 121:646–654. doi: 10.1111/j.1600-0706.2011.19712.x CrossRefGoogle Scholar
  13. Dubuc C, Hughes KD, Cascio J, Santos LR (2012) Social tolerance in a despotic primate: co-feeding between consortship partners in rhesus macaques. Am J Phys Anthropol 148:73–80. doi: 10.1002/ajpa.22043 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Elton C (1958) The ecology of invasions by animals and plants. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  15. Epifanio CE (2013) Invasion biology of the Asian shore crab Hemigrapsus sanguineus: a review. J Exp Mar Biol Ecol 441:33–49. doi: 10.1016/j.jembe.2013.01.010 CrossRefGoogle Scholar
  16. Foster WA, Treherne JE (1981) Evidence for the dilution effect in the selfish herd from fish predation on a marine insect. Nature 293:466–467. doi: 10.1038/293466a0 CrossRefGoogle Scholar
  17. Freeman GH, Halton JH (1951) Note on an exact treatment of contingency, goodness of fit and other problems of significance. Biometrika 38:141–149CrossRefPubMedGoogle Scholar
  18. Griffen BD, Byers JE (2009) Community impacts of two invasive crabs: the interactive roles of density, prey recruitment, and indirect effects. Biol Invasions 11:927–940. doi: 10.1007/s10530-008-9305-3 CrossRefGoogle Scholar
  19. Griffen BD, Delaney DG (2007) Species invasion shifts the importance of predator dependence. Ecology 88:3012–3021. doi: 10.1890/07-0172.1 CrossRefPubMedGoogle Scholar
  20. Griffen BD, Riley ME (2015) Potential impacts of invasive crabs on one life history strategy of native rock crabs in the Gulf of Maine. Biol Invasions 17:2533–2544. doi: 10.1007/s10530-015-0890-7 CrossRefGoogle Scholar
  21. Grosholz ED, Ruiz GM (1996) Predicting the impact of introduced marine species: lessons from the multiple invasions of the European green crab Carcinus maenas. Biol Conserv 78:59–66. doi: 10.1016/0006-3207(94)00018-2 CrossRefGoogle Scholar
  22. Hamilton WD (1971) Geometry for the selfish herd. J Theor Biol 31:295–311CrossRefPubMedGoogle Scholar
  23. Hare B, Melis AP, Woods V, Hastings S, Wrangham R (2007) Tolerance allows bonobos to outperform chimpanzees on a cooperative task. Curr Biol 17:619–623. doi: 10.1016/j.cub.2007.02.040 CrossRefPubMedGoogle Scholar
  24. He Q, Bertness MD (2014) Extreme stresses, niches, and positive species interactions along stress gradients. Ecology 95:1437–1443. doi: 10.1890/13-2226.1 CrossRefPubMedGoogle Scholar
  25. He Q, Bertness MD, Altieri AH (2013) Global shifts towards positive species interactions with increasing environmental stress. Ecol Lett 16:695–706. doi: 10.1111/ele.12080 CrossRefPubMedGoogle Scholar
  26. Hobbs NVS, Cobb JS, Thornber CS (2017) Injury, reproductive status, and distribution of Hemigrapsus sanguineus (De Haan, 1835) (Brachyura: Varunidae) on the rocky intertidal shores of Rhode Island, USA. J Crust Bio. doi: 10.1093/jcbiol/ruw002 Google Scholar
  27. Hunter E, Naylor E (1993) Intertidal migration by the shore crab Carcinus maenas. Mar Ecol Prog Ser 101:131CrossRefGoogle Scholar
  28. Jackson MC (2015) Interactions among multiple invasive animals. Ecology 96:2035–2041. doi: 10.1890/15-0171.1 CrossRefPubMedGoogle Scholar
  29. Januario SM, Navarrete SA (2013) Cannibalism and inter-specific predation in early stages of intertidal crab species that compete for refuges. J Exp Mar Biol Ecol 446:36–44. doi: 10.1016/j.jembe.2013.04.017 CrossRefGoogle Scholar
  30. 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. doi: 10.3354/meps225251 CrossRefGoogle Scholar
  31. Kennedy TA, Naeem S, Howe KM, Knops JM, Tilman D, Reich P (2002) Biodiversity as a barrier to ecological invasion. Nature 417:636–638. doi: 10.1038/nature00776 CrossRefPubMedGoogle Scholar
  32. Kintzing MD, Butler MJ IV (2014) The influence of shelter, conspecifics, and threat of predation on the behavior of the long-spined sea urchin (Diadema antillarum). J Shellfish Res 33:781–785. doi: 10.2983/035.033.0312 CrossRefGoogle Scholar
  33. Komdeur J, Schrama MJ, Meijer K, Moore AJ, Beukeboom LW (2013) Cobreeding in the burying beetle, Nicrophorus vespilloides: tolerance rather than cooperation. Ethology 119:1138–1148. doi: 10.1111/eth.12174 CrossRefGoogle Scholar
  34. 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. doi: 10.1656/1092-6194(2007)14%5B207:EROHSA%5D2.0.CO;2 CrossRefGoogle Scholar
  35. Landschoff J, Lackschewitz D, Kesy K, Reise K (2013) Globalization pressure and habitat change: pacific rocky shore crabs invade armored shorelines in the Atlantic Wadden Sea. Aquat Invasions 8:77–87. doi: 10.3391/ai.2013.8.1.09 CrossRefGoogle Scholar
  36. Lohrer AM, Whitlatch RB (2002) Interactions among aliens: apparent replacement of one exotic species by another. Ecology 83:719–732. doi: 10.1890/0012-9658(2002)083%5B0719:IAAARO%5D2.0.CO;2 CrossRefGoogle Scholar
  37. Lowry R (2015) Vassarstats: Website for statistical computation. http://vassarstats.net
  38. Marchetti MP, Moyle PB, Levine R (2004) Invasive species profiling? exploring the characteristics of non-native fishes across invasion stages in California. Freshw Biol 49:646–661. doi: 10.1111/j.1365-2427.2004.01202.x CrossRefGoogle Scholar
  39. Marraffini ML, Geller JB (2015) Species richness and interacting factors control invasibility of a marine community. Proc R Soc B 282:20150439. doi: 10.1098/rspb.2015.0439 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Menge BA (1995) Indirect effects in marine rocky intertidal interaction webs—patterns and importance. Ecol Mongr 65:21–74. doi: 10.2307/2937158 CrossRefGoogle Scholar
  41. Menge BA, Sutherland JP (1987) Community regulation: variation in disturbance, competition, and predation in relation to environmental stress and recruitment. Am Nat 130:730–757CrossRefGoogle Scholar
  42. Mittelbach GG, Schemske DW (2015) Ecological and evolutionary perspectives on community assembly. Trends Ecol Evol 30:241–247. doi: 10.1016/j.tree.2015.02.008 CrossRefPubMedGoogle Scholar
  43. O′Connor NJ (2014) Invasion dynamics on a temperate rocky shore: from early invasion to establishment of a marine invader. Biol Invasions 16(1):73–87. doi: 10.1007/s10530-013-0504-1 CrossRefGoogle Scholar
  44. Ory NC, Dudgeon D, Dumont CP, Miranda L, Thiel M (2012) Effects of predation and habitat structure on the abundance and population structure of the rock shrimp Rhynchocinetes typus (Caridea) on temperate rocky reefs. Mar Biol 159:2075–2089. doi: 10.1007/s00227-012-1994-6 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Parker JD, Torchin ME, Hufbauer RA, Lemoine NP, Alba C, Blumenthal DM, Bossdorf O, Byers JE, Dunn AM, Heckman RW, Hejda M (2013) Do invasive species perform better in their new ranges? Ecology 94:985–994. doi: 10.1890/12-1810.1 CrossRefPubMedGoogle Scholar
  46. Reilly PN, Saila SB (1978) Biology and ecology of the rock crab, Cancer irroratus Say, 1817, in southern New England waters (Decapoda, Brachyura). Crustaceana 34:121–140. doi: 10.1163/156854078X00709 CrossRefGoogle Scholar
  47. Ritz DA (1993) Social aggregation in pelagic invertebrates. Adv Mar Biol 30:155–216CrossRefGoogle Scholar
  48. Seeley B, Sewell J, Clark PF (2015) First GB records of the invasive Asian shore crab, Hemigrapsus sanguineus from Glamorgan, Wales and Kent, England. Mar Biodivers Rec 8:1–4. doi: 10.1017/S1755267215000809 CrossRefGoogle Scholar
  49. Snyder WE, Evans EW (2006) Ecological effects of invasive arthropod generalist predators. Annu Rev Ecol Evol Syst 37:95–122. doi: 10.1146/annurev.ecolsys.37.091305.110107 CrossRefGoogle Scholar
  50. Stachowicz JJ (2001) Mutualism, facilitation, and the structure of ecological communities. Bioscience 51:235–246. doi: 10.1641/0006-3568(2001)051[0235:MFATSO]2.0.CO;2 CrossRefGoogle Scholar
  51. Stachowicz JJ, Whitlatch RB, Osman RW (1999) Species diversity and invasion resistance in a marine ecosystem. Science 286:1577–1579. doi: 10.1126/science.286.5444.1577 CrossRefPubMedGoogle Scholar
  52. Steinberg MK, Epifanio CE (2011) Three’s a crowd: space competition among three species of intertidal shore crabs in the genus Hemigrapsus. J Exp Mar Biol Ecol 404:57–62. doi: 10.1016/j.jembe.2011.04.014 CrossRefGoogle Scholar
  53. Torchin ME, Lafferty KD, Kuris AM (2001) Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biol Invasions 3:333–345. doi: 10.1023/A:1015855019360 CrossRefGoogle Scholar
  54. Turner GF, Pitcher TJ (1986) Attack abatement: a model for group protection by combined avoidance and dilution. Am Nat 128:228–240CrossRefGoogle Scholar
  55. Wisz MS, Pottier J, Kissling WD et al (2013) The role of biotic interactions in shaping distributions and realised assemblages of species: implications for species distribution modelling. Biol Rev 88:15–30. doi: 10.1111/j.1469-185X.2012.00235.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Niels-Viggo S. Hobbs
    • 1
    Email author
  • J. Stanley Cobb
    • 2
  • Carol S. Thornber
    • 2
  1. 1.Graduate Program, Biological and Environmental SciencesUniversity of Rhode IslandKingstonUSA
  2. 2.Department of Biological SciencesUniversity of Rhode IslandKingstonUSA

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