Skip to main content
Log in

Native species behaviour mitigates the impact of habitat-forming invasive seaweed

  • Global change ecology - Original Paper
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Habitat-forming invasive species cause large, novel changes to the abiotic environment. These changes may elicit important behavioural responses in native fauna, yet little is known about mechanisms driving this behaviour and how such trait-mediated responses influence the fitness of native species. Low dissolved oxygen is a key abiotic change created by the habitat-forming invasive seaweed, Caulerpa taxifolia, which influences an important behavioural response (burrowing depth) in the native infaunal bivalve Anadara trapezia. In Caulerpa-colonised areas, Anadara often emerged completely from the sediment, and we experimentally demonstrate that water column hypoxia beneath the Caulerpa canopy is the mechanism instigating this “pop-up” behaviour. Importantly, pop-up in Caulerpa allowed similar survivorship to that in unvegetated sediment; however, when we prevented Anadara from popping-up, they suffered >50% mortality in just 1 month. Our findings not only highlight the substantial environmental alteration by Caulerpa, but also an important role for the behaviour of native species in mitigating the effects of habitat-forming invasive species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Altieri AH (2008) Dead zones enhance key fisheries species by providing predation refuge. Ecology 89:2808–2818

    Article  PubMed  Google Scholar 

  • Byers JE (2002) Physical habitat attribute mediates biotic resistance to non-indigenous species invasion. Oecologia 130:146–156

    Google Scholar 

  • Byers JE, Wright JT, Gribben PE (2010) Variable direct and indirect effects of a habitat-modifying invasive species on mortality of native fauna. Ecology 91:1787–1798

    PubMed  Google Scholar 

  • Castilla JC, Lagos NA, Cerda M (2004) Marine ecosystem engineering by the alien ascidian Pyura praeputialis on a mid-intertidal rocky shore. Mar Ecol Prog Ser 268:119–130

    Article  Google Scholar 

  • Chisholm JRM, Moulin P (2003) Stimulation of nitrogen fixation in refractory organic sediments by Caulerpa taxifolia (Chlorophyta). Limnol Oceanogr 48:787–794

    Article  CAS  Google Scholar 

  • Creese RG, Davis AR, Glasby TM (2004) Eradicating and preventing the spread of Caulerpa taxifolia in NSW. NSW Fish Final Rep Ser 64:110 http://www.dpi.nsw.gov.au/_data/assets/pdf_file/0003/137487/output-466.pdf

  • Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Mar Ecol Prog Ser 97:153–166

    Google Scholar 

  • D’Avanzo C, Kremer JN (1994) Diel oxygen dynamics and anoxic events in an eutrophic estuary of Waquoit Bay, Massachusetts. Estuaries 17:131–139

    Article  Google Scholar 

  • Dayton PK (1972) Toward an understanding of community resilience and the potential effects of enrichment to the benthos of McMurdo Sound, Antarctica. In: Parker BC (ed) Proceedings of the colloquium on conservation problems in Antarctica. Allen Press, Lawrence, pp 81–95

    Google Scholar 

  • Deegan LA, Wright A, Ayvazian SG, Finn JT, Golden H, Rand Merson R, Harrison J (2002) Nitrogen loading alters seagrass ecosystem structure and support of higher trophic levels. Aquat Conserv Mar Freshw Ecosyst 12:193–212

    Article  Google Scholar 

  • Diaz RJ, Rosenberg R (1995) Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceanogr Mar Biol Annu Rev 33:245–303

    Google Scholar 

  • Freeman AS, Byers JE (2006) Divergent induced responses to an invasive predator in marine mussel populations. Science 313:831–833

    Article  CAS  PubMed  Google Scholar 

  • Glasby TM, Creese RG (2007) Invasive marine species management and research. In: Connell SD, Gillanders BM (eds) Marine ecology. Oxford University Press, Melbourne, pp 569–594

    Google Scholar 

  • Gribben PE, Wright JT (2006) Invasive seaweed enhances recruitment of a native bivalve: roles of refuge from predation and the habitat choice of recruits. Mar Ecol Prog Ser 318:177–185

    Article  Google Scholar 

  • Gribben PE, Wright JT, O’Connor WA, Doblin MA, Eyre B, Steinberg PD (2009a) Reduced performance of native infauna following recruitment to a habitat-forming invasive marine alga. Oecologia 158:733–745

    Article  PubMed  Google Scholar 

  • Gribben PE, Byers JE, Clements M, McKenzie LA, Steinberg PD, Wright JT (2009b) Behavioural interactions between ecosystems engineers control community species richness. Ecol Lett 12:1127–1136

    Article  PubMed  Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386

    Article  Google Scholar 

  • Jones CG, Lawton JH, Shachak M (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78:1946–1957

    Article  Google Scholar 

  • Kennish MJ (2001) Coastal salt marsh systems in the US: a review of anthropogenic impacts. J Coast Res 17:731–748

    Google Scholar 

  • Kiesecker JM, Blaustein AR (1997) Population differences in responses of red-legged frogs (Rana aurora) to introduced bullfrogs. Ecology 78:1752–1760

    Google Scholar 

  • Levine JM, Vila M, D’Antonio CM, Dukes JS, Grigulis K, Lavorel S (2003) Mechanisms underlying the impacts of exotic plant invasions. Proc R Soc Lond B 270:775–781

    Article  Google Scholar 

  • Lowe S, Browne M, Boudjelas S, De Poorter M (2000) 100 of the world’s worst invasive alien species. http://www.issg.org/database/species/search.asp?st=100ss

  • McKinnon JG, Gribben PE, Davis AR, Jolley DF, Wright JT (2009) Differences in soft-sediment macrobenthic assemblages invaded by Caulerpa taxifolia compared to uninvaded habitats. Mar Ecol Prog Ser 380:59–71

    Article  Google Scholar 

  • Meyer JF, Byers JE (2005) As good as dead? Sublethal predation facilitates lethal predation on an intertidal clam. Ecol Lett 8:160–166

    Article  Google Scholar 

  • Pearl CA, Adams MJ, Schuytema GS, Nebeker AV (2003) Behavioural responses of anuran larvae to chemical cues of native and introduced predators in the Pacific Northwestern United States. J Herpetol 37:572–576

    Article  Google Scholar 

  • Preisler A, de Beer D, Lichtschlag A, Lavik G, Boetius A, Jørgensen BB (2007) Biological and chemical sulfide oxidation in a Beggiatoa inhabited marine sediment. ISME J 1:341–353

    CAS  PubMed  Google Scholar 

  • SCC (2003) State of the environment report. Shoalhaven City Council, Nowra, Australia

  • Seitz RD, Marshall LS, Hines AH, Clark KL (2003) Effects of hypoxia on predator-prey dynamics of the blue crab Callinectes sapidus and the Baltic clam Macoma balthica in Chesapeake Bay. Mar Ecol Prog Ser 257:179–188

    Article  Google Scholar 

  • Strauss SY, Lau JA, Carroll SP (2006) Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Trends Ecol Evol 9:357–374

    Google Scholar 

  • Tallqvist M (2001) Burrowing behaviour of the Baltic clam Macoma balthica: effects of sediment type, hypoxia and predator presence. Mar Ecol Prog Ser 212:183–191

    Article  Google Scholar 

  • Taylor DL, Eggleston DB (2000) Effects of hypoxia on an estuarine predator-prey interaction: foraging behavior and mutual interference in the blue crab Callinectes sapidus and the infaunal clam prey Mya arenaria. Mar Ecol Prog Ser 196:221–237

    Article  Google Scholar 

  • Theel HJ, Dibble ED (2008) An experimental simulation of an exotic aquatic macrophyte invasion and its influence on foraging behaviour of bluegill. J Freshw Ecol 23:79–89

    Google Scholar 

  • Trammell MA, Butler JL (1995) Effects of exotic plants on native ungulate use of habitat. J Wildl Manag 59:808–816

    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 

  • Ulstrup KE, Hill R, Ralph PJ (2005) Photosynthetic impact of hypoxia on in hospite zooxanthellae in the scleractinian coral Pocillopora damicornis. Mar Ecol Prog Ser 286:125–132

    Article  Google Scholar 

  • Valentine LE (2006) Habitat avoidance of an introduced weed by native lizards. Austral Ecol 31:732–735

    Article  Google Scholar 

  • Valentine LE, Roberts B, Schwarzkopf L (2007) Mechanisms driving avoidance of non-native plants by lizards. J Appl Ecol 44:228–237

    Article  Google Scholar 

  • Whitlow WL, Rice NA, Sweeney C (2003) Native species vulnerability to introduced predators: testing an inducible defense and a refuge from predation. Biol Invasions 5:23–31

    Article  Google Scholar 

  • Wright JT (2005) Differences between native and invasive Caulerpa taxifolia: a link between asexual fragmentation and abundance in invasive populations. Mar Biol 147:559–569

    Article  Google Scholar 

  • Wright JT, Gribben PE (2008) Predicting the impact of an invasive seaweed on the fitness of native fauna. J Appl Ecol 45:1540–1549

    Article  Google Scholar 

  • Wright JT, McKenzie LA, Gribben PE (2007) A decline in the abundance and condition of a native bivalve associated with Caulerpa taxifolia invasion. Mar Freshw Res 58:263–272

    Article  Google Scholar 

  • Wu RSS (2002) Hypoxia: from molecular responses to ecosystem responses. Mar Pollut Bull 45:35–45

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Support was provided by the Institute for Conservation Biology, University of Wollongong to J.T.W., L.P.K. and J.E.B.; the National Geographic Society to J.E.B.; and the University of Technology-Sydney to P.E.G. Comments from Geoffrey Trussell and three anonymous reviewers greatly improved the previous draft of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jeffrey T. Wright.

Additional information

Communicated by Geoffrey Trussell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wright, J.T., Byers, J.E., Koukoumaftsis, L.P. et al. Native species behaviour mitigates the impact of habitat-forming invasive seaweed. Oecologia 163, 527–534 (2010). https://doi.org/10.1007/s00442-010-1608-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-010-1608-2

Keywords

Navigation