Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences

Limited grazing pressure by native herbivores on the invasive seaweed Caulerpa taxifolia in a temperate Australian estuary

John R. Gollan A B C and Jeffrey T. Wright A

A Institute for Conservation Biology and Department Biological Science, University of Wollongong, Northfields Avenue, Wollongong, NSW 2522, Australia.

B Present address: Australian Museum, College Street, Sydney, NSW 2010, Australia.

C Corresponding author. Email:

Marine and Freshwater Research 57(7) 685-694
Submitted: 19 December 2005  Accepted: 2 August 2006   Published: 13 October 2006


Caulerpa taxifolia is an invasive alga threatening biodiversity in invaded regions. Its proliferation in recipient communities will be due to several factors including limited grazing effects by native herbivores. However, little is known about grazing pressure exerted by native herbivores on C. taxifolia relative to native macrophytes or its attractiveness to them as habitat. The present study determined which herbivores co-occurred with invasive C. taxifolia in a temperate Australian estuary and documented their abundance, relative grazing effects, habitat preference and survivorship on C. taxifolia compared with native macrophytes. Four herbivores co-occurred with C. taxifolia and their densities were often low or zero at the sites studied. Feeding experiments showed that compared with C. taxifolia: the fish, Girella tricuspidata, preferred Ulva sp.; the sea-hare, Aplysia dactylomela, preferred Laurencia sp.; whereas the mesograzers, Cymadusa setosa and Platynereis dumerilii antipoda, both consumed Cystoseira trinodus and Sargassum sp. at higher rates. The two mesograzers also showed strong habitat preference for C. trinodus and Sargassum sp. Cymadusa setosa had poor survivorship on Caulerpa taxifolia whereas P. dumerilii antipoda had 100% survivorship on C. taxifolia after 41 days. We consider that the low diversity and abundance of native herbivores, their weak grazing pressure on C. taxifolia and its low attractiveness as habitat may facilitate further local spread in this estuary, and potentially in other invaded locations.

Extra keywords: enemy-release, exotic, generalist, herbivory, Lake Conjola, New South Wales.


Adolph S.Jung V.Rattke J.Pohnert G.2005Wound closure in the invasive green alga Caulerpa taxifolia by enzymatic activation of a protein cross-linker.Angewandte Chemie International Edition4428062808doi:10.1002/ANIE.200462276

Amade P.Lemée R.1998Chemical defense of the Mediterranean alga Caulerpa taxifolia: variation in caulerpenyne production.Aquatic Toxicology43287290doi:10.1016/S0166-445X(98)00054-X

Bellan-Santini D.Arnaud P. M.Bellan G.Verlaque M.1996The influence of the introduced tropical alga Caulerpa taxifolia, on the biodiversity of the Mediterranean marine biota.Journal of the Marine Biological Association of the UK76235237

Boudouresque C. F.Lemée R.Mari X.Meinesz A.1996The invasive alga Caulerpa taxifolia is not a suitable diet for the sea urchin Paracentrotus lividus.Aquatic Botany53245250

Ceccherelli G.Cinelli F.1998Habitat effect on spatiotemporal variability in size and density of the introduced alga Caulerpa taxifolia.Marine Ecology Progress Series163289294

Ceccherelli G.Cinelli F.1999The role of vegetative fragmentation in dispersal of the invasive alga Caulerpa taxifolia in the Mediterranean.Marine Ecology Progress Series182299303

Chisholm J. R. M.Fernex F. E.Methieuand D.Jaubert J. M.1997Wastewater discharge, seagrass decline and algal proliferation on the Côte d’Azur.Marine Pollution Bulletin347884

Clements K. D.Choat J. H.1997Comparison of herbivory in the closely-related marine fish genera Girella and Kyphosus.Marine Biology127579586doi:10.1007/S002270050048

Colautti R. I.Ricciardi A.Grigorovich I. A.MacIsaac H. J.2004Is invasion success explained by the enemy release hypothesis?Ecology Letters7615622

Creese R. G., Davis A. R., and Glasby T. (2004). Eradicating and preventing the spread of the invasive alga Caulerpa taxifolia in NSW. NSW Fisheries Final Report Series No. 64, p. 110. NSW Fisheries: Sydney.

Davis A. R.Benkendorff K.Ward D. W.2005Responses of common SE Australian herbivores to three suspected invasive Caulerpa spp.Marine Biology146859868

Duffy J. E., and Hay M. E. (2001). The ecology and evolution of marine consumer-prey interactions. In ‘Marine Community Ecology’. (Eds M. D. Bertness, S. D. Gaines and M. E. Hay.) pp. 131–157. (Sinauar Associates: Sunderland, MA.)

Francour P.Harmelin-Vivien M.Harmelin J. G.Duclerc J.1995Impact of Caulerpa taxifolia colonization on the littoral ichthyofauna of north-western Mediterranean Sea: Preliminary results.Hydrobiologia300–301345353doi:10.1007/BF00024475

Glasby T. M.Creese R. G.Gibson P. T.2005Experimental use of salt to control the invasive marine alga Caulerpa taxifolia in New South Wales, Australia.Biological Conservation122573580doi:10.1016/J.BIOCON.2004.09.012

Hay M. E., and Steinberg P. D. (1992). The chemical ecology of plant-herbivore interactions in marine versus terrestrial communities. In ‘Herbivores: their Interaction with Secondary Plant Metabolites’. (Eds G. A. Rosenthal and M. R. Berenbaum.) pp. 371–413. (Academic Press Inc.: San Diego, CA.)

Hutchings M. J.Booth K. D.Waite S.1991Comparison of survivorship by log rank test: criticisms and alternatives.Ecology7222902293doi:10.2307/1941579

Keane R. M.Crawley M. J.2002Exotic plant invasions and the enemy release hypothesis.Trends in Ecology & Evolution17164170doi:10.1016/S0169-5347(02)02499-0

Kingsford M. J. (1998). Reef fishes. In ‘Studying Temperate Marine Environments: A Handbook for Ecologists’. (Eds M. J. Kingsford and C. Battershill.) pp. 132–166. (Canturbury University Press: Christchurch.)

Lemee R.Pesando D.Issanchou C.Amade P.1997Microalgae: a model to investigate the ecotoxicity of the green alga Caulerpa taxifolia from the Mediterranean Sea.Marine Environmental Research441325doi:10.1016/S0141-1136(96)00099-2

Levin P. S.Coyer J. A.Petrik R.Good T. P.2002Community-wide effects of nonindigenous species on temperate rocky reefs.Ecology8331823193

Longepierre S.Robert A.Levi F.Francour P.2005How an invasive alga species (Caulerpa taxifolia) induces changes in foraging strategies of the benthivorous fish Mullus surmuletus in coastal Mediterranean ecosystems.Biodiversity and Conservation14365376

Mack R. N.Simberloff D.Lonsdale W. M.Evans H.Clout M.Bazzaz F. A.2000Biotic invasions: causes, epidemiology, global consequences, and control.Ecological Applications10689710

McConnell O. J.Hughes P. A.Targett N. M.Daley J.1982Effects of secondary metabolites from marine algae on feeding by the sea urchin Lytechinus variegates.Journal of Chemical Ecology814371453doi:10.1007/BF00989101

Meinesz A.Belsher T.Thibaut T.Antolic B.Ben Mustapha K.2001The introduced green alga Caulerpa taxifolia continues to spread in the Mediterranean.Biological Invasions3201210doi:10.1023/A:1014549500678

Meyer K. D.Paul V. J.1992Intraplant variation in secondary metabolite concentration in three Caulerpa (Chlorophyta: Caulerpales) and its effects on herbivorous fishes.Marine Ecology Progress Series82249257

Pennings S. C.Paul V. J.1992Effect of plant toughness, calcification and chemistry on herbivory by Dolabella auriculata.Ecology7316061619

Peterson C. H.Renaud P. E.1989Analysis of feeding preference experiments.Oecologia808286doi:10.1007/BF00789935

Phillips J. A.Price I. R.2002How different is Mediterranean Caulerpa taxifolia (Caulerpales: Chlorophyta) to other populations of the species?Marine Ecology Progress Series2386172

Poore A. G. B.Steinberg P. D.1999Preference-performance relationships and effects of host plant choice in an herbivorous marine amphipod.Ecological Monographs69443464

Poore A. G. B.Watson M. Nys R.Lowry J. K.Steinberg P. D.2000Patterns of host use in alga- and sponge-associated amphipods.Marine Ecology Progress Series208183196

Relini G.Relini M.Torchia G.1998Fish biodiversity in a Caulerpa taxifolia meadow in the Ligurian Sea.The Italian Journal of Zoology65S465470

Rogers C. Nys R.Steinberg P. D.2003Ecology of the sea hare Aplysia parvula (Opisthobranchia) in New South Wales, Australia.Molluscan Research23185198

Ruesink J. L.2000Intertidal mesograzers in field microcosms: linking laboratory feeding rates to community dynamics.Journal of Experimental Marine Biology and Ecology248163176doi:10.1016/S0022-0981(00)00170-2

Ruiz G. M.Fofonoff P. W.Carlton J. T.Wonham M. J.Hines A. H.2000Invasion of coastal marine communities in North America: Apparent patterns, processes, and biases.Annual Review of Ecology and Systematics31481531doi:10.1146/ANNUREV.ECOLSYS.31.1.481

Schaffelke B.Evers D.Walhorn A.1995Selective grazing of the isopod Idotea baltica between Fucus evanescens and F. vesiculosus from Kiel Fjord (western Baltic).Marine Biology124215218doi:10.1007/BF00347125

Schaffelke B., Smith J. E., and Hewitt C. L. (in press). Introduced macroalgae – a growing concern. In ‘Proceedings of the 18th International Seaweed Symposium, Bergen, Norway’. (International Seaweed Association.)

Scheibling R. E.Anthony S. X.2001Feeding, growth and reproduction of sea urchins (Strongylocentrotus droebachiensis) on single and mixed diets of kelp (Laminaria spp.) and the invasive alga Codium fragile ssp. tomentosoides.Marine Biology139139146doi:10.1007/S002270100567

Steinberg P. D. (1992). Geographical variation in the interaction between marine herbivores and brown algal secondary metabolites. In ‘Ecological Roles for Marine Secondary Metabolites'. (Ed. V. J. Paul.) pp. 51–92. (Cornell University Press: New York.)

Strauss R. E.1979Reliability estimates for Ivlev’s electivity index, the forage ratio, and a proposed linear index of food selection.Transactions of the American Fisheries Society108344352doi:10.1577/1548-8659(1979)108<344:REFIEI>2.0.CO;2

Thibaut T.Meinesz A.2000Are the Mediterranean molluscs Oxynoe olivacea and Lobiger serradifalci suitable agents for a biological control against the invading tropical alga Caulerpa taxifolia.Comptes Rendus de l’Académie des Sciences, Sciences de la Vie, Paris323112

Thornber C. S.Kinlan B. P.Graham M. H.Stachowicz J. J.2004Population ecology of the invasive kelp Undaria pinnatifida in California: environmental and biological controls on demography.Marine Ecology Progress Series2686980

Trowbridge C. D.2004Emerging associations on marine rocky shores: specialist herbivores on introduced macroalgae.Journal of Animal Ecology73294308

Underwood A. J. (1997). ‘Experiments in Ecology.’ (Cambridge University Press: Cambridge.)

Underwood A. J.Kingsford M. J.Andrew N. L.1991Patterns in shallow subtidal marine assemblages along the coast of New South Wales.Australian Journal of Ecology6231249

Williams S. I.Walker D. I.1999Mesoherbivore-macroalgal interactions: feeding ecology of sacoglossan sea slugs (Mollusca, Opisthobranchia) and their effects on their food algae.Oceanography and Marine Biology: An Annual Review3787128

Wright J. T.2005Differences between native and invasive Caulerpa taxifolia: a link between asexual fragmentation and abundance in invasive populations.Marine Biology147559569

Wright J. T.Steinberg P. D.2001Effects of variable recruitment and post-recruitment herbivory on local population size of a marine alga.Ecology8222002215doi:10.2307/2680226

Wright J. Nys R.Steinberg P. D.2000Geographic variation in halogenated furanones from the red alga Delisea pulchra and associated herbivores and epiphytes.Marine Ecology Progress Series207227241

Zemke-White W.Clements K. D.1999Chlorophyte and rhodophyte starches as factors in diet choice by marine herbivorous fish.Journal of Experimental Marine Biology and Ecology240137149

Žuljevic A.Thibaut T.Elloukal H.Meinesz A.2001Sea slug disperses the invasive Caulerpa taxifolia.Journal of the Marine Biology Association of the UK81343344

Export Citation Cited By (31)