Advertisement

Biological Invasions

, Volume 18, Issue 6, pp 1653–1665 | Cite as

Estuarine fouling communities are dominated by nonindigenous species in the presence of an invasive crab

  • Aaren S. Freeman
  • Alejandro Frischeisen
  • April MH. Blakeslee
Original Paper

Abstract

Interactions between anthropogenic disturbances and introduced and native species can shift ecological communities, potentially leading to the successful establishment of additional invaders. Since its discovery in New Jersey in 1988, the Asian shore crab (Hemigrapsus sanguineus) has continued to expand its range, invading estuarine and coastal habitats in eastern North America. In estuarine environments, H. sanguineus occupies similar habitats to native, panopeid mud crabs. These crabs, and a variety of fouling organisms (both NIS and native), often inhabit man-made substrates (like piers and riprap) and anthropogenic debris. In a series of in situ experiments at a closed dock in southwestern Long Island (New York, USA), we documented the impacts of these native and introduced crabs on hard-substrate fouling communities. We found that while the presence of native mud crabs did not significantly influence the succession of fouling communities compared to caged and uncaged controls, the presence of introduced H. sanguineus reduced the biomass of native tunicates (particularly Molgula manhattensis), relative to caged controls. Moreover, the presence of H. sanguineus favored fouling communities dominated by introduced tunicates (especially Botrylloides violaceous and Diplosoma listerianum). Altogether, our results suggest that H. sanguineus could help facilitate introduced fouling tunicates in the region, particularly in locations where additional solid substrates have created novel habitats.

Keywords

Fouling community Mud crabs Invasion meltdown Tunicates Anthropogenic habitats Panopeus herbstii Hemigrapsus sanguineus Botrylloides violaceous Molgulamanhattensis Diplosoma listerianum 

Notes

Acknowledgments

For assistance with field work we would like to thank: Westley Blakeslee, Melanie Bram, James Brown, Steve Harstein, Zack Holmes, Isabela Kernin, Sara Kulins, Jaclyn Onufrey, and the Town of Hempstead Marina and Bay Constables. Comments from James T. Carlton and two anonymous reviewers improved this manuscript.

References

  1. Bullard SG, Whitlatch RB, Osman RW (2004) Checking the landing zone: Do invertebrate larvae avoid settling near superior spatial competitors? Mar Ecol Prog Ser 280:239–247CrossRefGoogle Scholar
  2. Canning-Clode J, Fofonoff P, McCann L et al (2013) Marine invasions on a subtropical island: Fouling studies and new records in a recent marina on Madeira island (Eastern Atlantic Ocean). Aquat Invasions 8:261–270CrossRefGoogle Scholar
  3. Clarke Murray C, Therriault TW, Martone PT (2012) Adapted for invasion? Comparing attachment, drag and dislodgment of native and nonindigenous hull fouling species. Biol Invasions 14:1651–1663CrossRefGoogle Scholar
  4. Collin SB, Johnson LE (2014) Invasive species contribute to biotic resistance: negative effect of caprellid amphipods on an invasive tunicate. Biol Invasions 16:1–11CrossRefGoogle Scholar
  5. Dijkstra J, Harris LG, Westerman E (2007) Distribution and long-term temporal patterns of four invasive colonial ascidians in the Gulf of Maine. J Exp Mar Biol Ecol 342:61–68CrossRefGoogle Scholar
  6. Dijkstra JA, Westerman EL, Harris LG (2011) The effects of climate change on species composition, succession and phenology: a case study. Glob Change Biol 17:2360–2369CrossRefGoogle Scholar
  7. Dumont CP, Gaymer CF, Thiel M (2011) Predation contributes to invasion resistance of benthic communities against the non-indigenous tunicate Ciona intestinalis. Biol Invasions 13:2023–2034CrossRefGoogle Scholar
  8. Epifanio CE (2013) Invasion biology of the Asian shore crab Hemigrapsus sanguineus: a review. J Exp Mar Biol Ecol 441:33–49CrossRefGoogle Scholar
  9. Fehlauer-Ale KH, Winston JE, Tilbrook KJ et al (2015) Identifying monophyletic groups within Bugula sensu lato (Bryozoa, Buguloidea). Zool Scr 44:334–347CrossRefGoogle Scholar
  10. Fofonoff P, Ruiz G, Steves B, et al (2003) National Exotic Marine and Estuarine Species Information System. http://invasions.si.edu/nemesis/. Accessed on 30 Oct 2015
  11. Freestone AL, Ruiz GM, Torchin ME (2013) Stronger biotic resistance in tropics relative to temperate zone: effects of predation on marine invasion dynamics. Ecology 94:1370–1377CrossRefPubMedGoogle Scholar
  12. Glasby TM, Connell SD, Holloway MG et al (2007) Nonindigenous biota on artificial structures: could habitat creation facilitate biological invasions? Mar Biol 151:887–895CrossRefGoogle Scholar
  13. Griffen BD, Altman I, Hurley J et al (2011) Reduced fecundity by one invader in the presence of another: a potential mechanism leading to species replacement. J Exp Mar Biol Ecol 406:6–13CrossRefGoogle Scholar
  14. Griffen BD, Altman I, Bess BM et al (2012) The role of foraging in the success of invasive Asian shore crabs in New England. Biol Invasions 14:2545–2558CrossRefGoogle Scholar
  15. Griffen BD, Delaney DG (2007) Species invasion shifts the importance of predator dependence. Ecology 88:3012–3021CrossRefPubMedGoogle Scholar
  16. 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 77:32–40CrossRefPubMedGoogle Scholar
  17. Grosberg RK (1981) Competitive ability influences habitat choice in marineinvertebrates. Nature 290:700–702CrossRefGoogle Scholar
  18. Johnson LE, Strathmann RR (1989) Settling barnacle larvae avoid substrata previously occupied by a mobile predator. J Exp Mar Biol Ecol 128:87–103CrossRefGoogle Scholar
  19. Kimbro DL, Cheng BS, Grosholz ED (2013) Biotic resistance in marine environments. Ecol Lett 16:821–833CrossRefPubMedGoogle Scholar
  20. Lambert CC, Lambert G (2003) Persistence and differential distribution of nonindigenous ascidians in harbors of the Southern California Bight. Mar Ecol Prog Ser 259:145–161CrossRefGoogle Scholar
  21. Lohrer AM, Whitlatch RB (2002) Relative impacts of two exotic bracyuran species on blue mussel populations in Long Island Sound. Mar Ecol Prog Ser 227:135–144CrossRefGoogle Scholar
  22. Matassa CM, Trussell GC (2011) Landscape of fear influences the relative importance of consumptive and nonconsumptive predator effects. Ecology 92:2258–2266CrossRefPubMedGoogle Scholar
  23. 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 181:195–198CrossRefGoogle Scholar
  24. Osman RW, Whitlach RB (1995) Predation on early ontogenetic life stages and its effect on recruitment into a marine epifaunal community. Mar Ecol Prog Ser 117:111–126CrossRefGoogle Scholar
  25. Osman RW, Whitlatch RB (2004) The control of the development of a marine benthic community by predation on recruits. J Exp Mar Biol Ecol 311:117–145CrossRefGoogle Scholar
  26. Peterson CH (1979) The importance of predation and competition in organizing the intertidal epifaunal communities of Barnegat Inlet, New Jersey. Oecologia 39:1–24CrossRefGoogle Scholar
  27. Pollock L (1998) A practical guide to the marine animals of Northeastern North America. Rutgers University Press, New BrunswickGoogle Scholar
  28. Ricciardi A, Whoriskey FG (2004) Exotic species replacement: shifting dominance of dreissenid mussels in the Soulanges Canal, upper St. Lawrence River,Canada. J North Am Benthol Soc 23:507–514CrossRefGoogle Scholar
  29. Ruiz GM, Fofonoff PW, Carlton JT et al (2000) Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Ann Rev Ecol Syst 31:481–531CrossRefGoogle Scholar
  30. Ryland JS, Holt R, Loxton J (2014) First occurrence of the non-native bryozoan Schizoporella japonica Ortmann (1890) in Western Europe. Zootaxa 3780:481–502CrossRefPubMedGoogle Scholar
  31. Simberloff D (2006) Invasional meltdown 6 years later: Important phenomenon, unfortunate metaphor, or both? Ecol Lett 9:912–919CrossRefPubMedGoogle Scholar
  32. Simberloff D, Von Holle B (1999) Positive interactions of nonindigenous species: invasion meltdown? Biol Invasions 1:21–32CrossRefGoogle Scholar
  33. Simkanin C, Davidson IC, Dower JF et al (2012) Anthropogenic structures and the infiltration of natural benthos by invasive ascidians. Mar Ecol 33:499–511CrossRefGoogle Scholar
  34. Tyrrell MC, Byers JE (2007) Do artificial substrates favor nonindigenous fouling species over native species? J Exp Mar Biol Ecol 342:54–60CrossRefGoogle Scholar
  35. Wasson K, Fenn K, Pearse JS (2005) Habitat differences in marine invasions of central California. Biol Invasions 7:935–948CrossRefGoogle Scholar
  36. Williams SL, Davidson IC, Pasari JR et al (2013) Managing multiple vectors for marine invasions in an increasingly connected world. Bioscience 63:952–966CrossRefGoogle Scholar
  37. Winston JE, Hayward PJ (2012) The marine bryozoans of the northeast coast of the United States: maine to virginia. Virginia Museum Nat Hist Memoir 11:1–180Google Scholar
  38. Wonham MJ, O’Connor MI, Harley CDG (2005) Positive effects of a dominant invader on introduced and native mudflat species. Mar Ecol Prog Ser 289:109–116CrossRefGoogle Scholar
  39. Yund PO, Collins C, Johnson SL (2015) Evidence of a native Northwest Atlantic COI haplotype clade in the cryptogenic colonial ascidian Botryllus schlosseri. Biol Bull 228:201–216PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Aaren S. Freeman
    • 1
  • Alejandro Frischeisen
    • 1
    • 2
  • April MH. Blakeslee
    • 3
    • 4
  1. 1.Adelphi UniversityGarden CityUSA
  2. 2.Triumvirate EnvironmentalAstoriaUSA
  3. 3.East Carolina UniversityGreenvilleUSA
  4. 4.Smithsonian Environmental Research CenterEdgewaterUSA

Personalised recommendations