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

A decline in the abundance and condition of a native bivalve associated with Caulerpa taxifolia invasion

Jeffrey T. Wright A C , Louise A. McKenzie B and Paul E. Gribben B

A Institute for Conservation Biology and School of Biological Sciences, University of Wollongong, Wollongong, NSW 2522, Australia.

B Centre for Marine Biofouling and Bio-Innovation and School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia.

C Corresponding author. Email: jeffw@uow.edu.au

Marine and Freshwater Research 58(3) 263-272 http://dx.doi.org/10.1071/MF06150
Submitted: 18 August 2006  Accepted: 10 January 2007   Published: 9 March 2007

Abstract

Caulerpa taxifolia is a fast-spreading invasive seaweed that threatens biodiversity in temperate Australian estuaries. To date, little is known about its effects on infauna. In the present study, we describe variation in demographic and life-history traits of the abundant infaunal bivalve, Anadara trapezia, in C. taxifolia and uninvaded habitats (seagrass and unvegetated sediments) at multiple sites across three estuaries in south-eastern New South Wales. Densities of A. trapezia were always lower in C. taxifolia than on unvegetated sediment, and lower in C. taxifolia than in seagrass at three out of four sites where they were compared. Dry tissue weight of A. trapezia was also lower in C. taxifolia than on unvegetated sediment at most sites, but was only lower in C. taxifolia than in seagrass at one of four sites. Populations were dominated by larger individuals (>45 mm length), but smaller individuals (35–45 mm length) were more common in C. taxifolia and seagrass. A. trapezia shell weight and morphology was variable and appeared weakly affected by invasion. Generally, our findings are consistent with the hypothesis that A. trapezia is negatively affected by C. taxifolia. However, C. taxifolia invasion appears complex and, at some places, its effects may not differ from those of native seagrass. There is a need for manipulative studies to understand the mechanisms underlying the effects of C. taxifolia on infauna.

Additional keywords: Anadara trapezia, infauna, invasive species.


References

Allen B. J.Williams S. L.2003Native eelgrass Zostera marina controls growth and reproduction of an invasive mussel through food limitation.Marine Ecology Progress Series2545767

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 United Kingdom76235237


Bolam S. G.Fernandes T. F.2002The effects of macroalgal cover on the spatial distribution of macrobenthic invertebrates: the effects of macroalgal morphology.Hydrobiologia475–476437448
doi:10.1023/A:1020307929624

Bulleri F.Airoldi L.Branca G. M.Abbiati M.2006Positive effects of the introduced green alga, Codium fragile ssp. tomentosoides, on recruitment and survival of mussels.Marine Biology14812131220doi:10.1007/S00227-005-0181-4

Carmichael R. H.Shriver A. C.Valiela I.2004Changes in shell and soft tissue growth, tissue composition, and survival of quahogs, Mercenaria mercenaria, and soft shell clams, Mya arenaria, in response to eutrophic-driven changes in food supply and habitat.Journal of Experimental Marine Biology and Ecology31375104doi:10.1016/J.JEMBE.2004.08.006

Ceccherelli G.Cinelli F.1997Short term effects of nutrient enrichment of the sediment and interactions between the seagrasses Cymodocea nodosa and the introduced green alga Caulerpa taxifolia in a Mediterranean bay.Journal of Experimental Marine Biology and Ecology217165177doi:10.1016/S0022-0981(97)00050-6

Chisholm J. R. M.Moulin P.2003Stimulation of nitrogen fixation in refractory organic sediments by Caulerpa taxifolia (Chlorophyta).Limnology and Oceanography48787794

Constable A. J.1999Ecology of benthic macro-invertebrates in soft-sediment environments: a review of progress towards quantitative models and predictions.Australian Journal of Ecology24452476
doi:10.1046/J.1442-9993.1999.00977.X

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. (NSW Fisheries: Cronulla.)

Crenshaw M. A.Neff J. M.1969Decalcification at the mantle-shell interface in molluscs.American Zoologist9881885

Crooks J. A.1998Habitat alteration and community-level effects of an exotic mussel, Musculista senhousia.Marine Ecology Progress Series162137152


Crooks J. A.2001Assessing invader roles within changing ecosystems: historical and experimental perspectives on an exotic mussel in an urbanized lagoon.Biological Invasions32336
doi:10.1023/A:1011404914338

Crooks J. A.2002Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers.Oikos97153166doi:10.1034/J.1600-0706.2002.970201.X

Crooks J. A.Khim H. S.1999Architectural vs. biological effects of a habitat-altering, exotic mussel, Musculista senhousia.Journal of Experimental Marine Biology and Ecology2405375doi:10.1016/S0022-0981(99)00041-6

DeVille W.Verlaque M.1995Changes and degradation in a Posidonia oceanica bed invaded by the introduced tropical alga Caulerpa taxifolia in the north western Mediterranean.Aquatic Botany583741

Edgar G. J. (2000). ‘Australian Marine Life: the Plants and Animals of Temperate Waters.’ (Reed New Holland: Sydney.)

Enríquez S.Marbà N.Duarte C. M.van Tussenbroek B. I.Reyes-Zavala G.2001Effects of seagrass Thalassia testudinum on sediment redox.Marine Ecology Progress Series219149158


Freeman A. S.Byers J. E.2006Divergent induced responses to an invasive predator in marine mussel populations.Science313831833
doi:10.1126/SCIENCE.1125485

Gollan J. R.Wright J. T.2006Limited grazing pressure by native herbivores on the invasive seaweed Caulerpa taxifolia in a temperate Australian estuary.Marine and Freshwater Research57685694doi:10.1071/MF05253

Gordon J.Carriker M. R.1978Growth lines in a bivalve mollusk: subtidal patterns and dissolution of the shell.Science202519521doi:10.1126/SCIENCE.202.4367.519

Gribben P. E.Wright J. T.2006aInvasive seaweed enhances recruitment of a native bivalve: roles of refuge predation and habitat choice.Marine Ecology Progress Series318177185

Gribben P. E.Wright J. T.2006bSublethal effects on reproduction in native fauna: are females more vulnerable to biological invasion?Oecologia149352361
doi:10.1007/S00442-006-0452-X

Gribben P. E.Helson J.Millar R.2004Population abundance estimates of the New Zealand geoduck clam, Panopea zelandica, using North American methodology: is the technology transferable.Journal of Shellfish Research23683691

Grosholz E. D.Ruiz G. M.Dean C. A.Shirley K. A.Maron J. L.Conners P. G.2000The impacts of a nonindigenous marine predator in a California bay.Ecology8112061224
doi:10.2307/177202

Hadfield A. J.Anderson D. T.1988Reproductive cycles of the bivalve molluscs Anadara trapezia (Deshayes), Venerupis crenata Lamarck and Anomia descripta Iredale in the Sydney region.Australian Journal of Marine and Freshwater Research39649660doi:10.1071/MF9880649

Irlandi E. A.Peterson C. H.1991Modification of animal habitat by large plants: mechanisms by which seagrasses influence clam growth.Oecologia87307318doi:10.1007/BF00634584

Jousson O.Pawlowski J.Zaninetti L.Zechman F. W.Dini F.Di Guiseppe G.Woodfield R.Millar A. J. K.Meinesz A.2000Invasive alga reaches California.Nature408157158doi:10.1038/35041623

Keck R. T.Maurer D.Lind H.1975A comparative study of the hard clam gonad development cycle.The Biological Bulletin148243258

Lenihan H. S., and Micheli F. (2001). Soft sediment communities. In ‘Marine Community Ecology’. (Eds M. D. Bertness, S. D. Gaines and M. E. Hay.) pp. 253–288. (Sinuaer Associates: Sunderland, MA.)

Les D. H.Moody M. L.Jacobs S. W. L.Bayer R. J.2002Systematics of seagrasses (Zosteraceae) in Australia and New Zealand.Systematic Botany27468484


Levi F.Francour P.2004Behavioural response of Mullus surmuletus to habitat modification by the invasive macroalga Caulerpa taxifolia.Journal of Fish Biology645564
doi:10.1111/J.1095-8649.2004.00280.X

Levine J. M.Vila M.D'Antonio C. M.Dukes J. S.Grigulis K.Lavorel S.2003Mechanisms underlying the impacts of exotic plant invasions.Proceedings of the Royal Society of London B: Biological Sciences270775781doi:10.1098/RSPB.2002.2299

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

Meinesz A.Benichou L.Blachier J.Komatsu T.Lemee R.Molenaar H.Mari X.1995Variations in the structure, morphology and biomass of Caulerpa taxifolia in the Mediterranean Sea.Botanica Marina38499508


Meinesz A.Belsher T.Thibaut T.Antolic B.Ben Mustapha K.et al.2001The introduced green alga Caulerpa taxifolia continues to spread in the Mediterranean.Biological Invasions3201210
doi:10.1023/A:1014549500678

Micheli F.Peterson C. H.1999Estuarine vegetated habitats as corridors for predator movement.Conservation Biology13869881doi:10.1046/J.1523-1739.1999.98233.X

Neira C.Levin L. A.Grosholz E. D.2005Benthic macrofaunal communities of three sites in San Francisco Bay invaded by hybrid Spartina, with comparison to uninvaded habitats.Marine Ecology Progress Series292111126

Neira C.Grosholz E. D.Levin L. A.Blake R.2006Mechanisms generating modification of benthos following tidal flat invasion by a Spartina hybrid.Ecological Applications1613911404


NSW DPI (2006). ‘Maps of Caulerpa Distribution.’ Available at
www.fisheries.nsw.gov.au/threatened_species/general/species/caulerpa_distribution [Verified 15 January 2007].

Pease B. C.1999A spatially oriented analysis of estuaries and their associated commercial fisheries in New South Wales, Australia.Fisheries Research426786doi:10.1016/S0165-7836(99)00035-1

Posey M. H.1988Community changes associated with the spread of an introduced seagrass, Zostera japonica.Ecology69974983doi:10.2307/1941252

Quinn G. P., and Keough M. J. (2002). ‘Experimental Design and Data Analysis for Biologists.’ (Cambridge University Press: Cambridge.)

Reusch T. B. H.Williams S. L.1999Macrophyte canopy structure and the success of an invasive marine bivalve.Oikos84398416

Richardson C. A.Walker P.1991The age structure of a population of the hard-shell clam, Mercenaria mercenaria from Southampton Water, England, derived from acetate peels replicas of shell sections.ICES Journal of Marine Science48229236


Robertson B. A.Hutto R. L.2006A framework for understanding ecological traps and an evaluation of existing evidence.Ecology8710751085


Ross D. J.Johnson C. R.Hewitt C. L.2002Impact of introduced seastars Asterias amurensis on survivorship of juvenile commercial bivalves Fulvia tenuicostata.Marine Ecology Progress Series24199112


Schlaepfer M. A.Runge M. C.Sherman P. W.2002Ecological and evolutionary traps.Trends in Ecology & Evolution17474480
doi:10.1016/S0169-5347(02)02580-6

Schlaepfer M. A.Sherman P. W.Blossey B.Runge M. C.2005Introduced species as evolutionary traps.Ecology Letters8241246doi:10.1111/J.1461-0248.2005.00730.X

Schöne B.Tanabe K.Dettman D.Sato S.2003Environmental controls on shell growth rates and d18O of the shallow-marine bivalve mollusk Phacosoma japonicum in Japan.Marine Biology142473485

Shumway S. E.Scott T. M.Shick J. M.1983The effects of anoxia and hydrogen sulphide on survival, activity and metabolic rate in the coot clam, Mulinia lateralis (Say).Journal of Experimental Marine Biology and Ecology71135146
doi:10.1016/0022-0981(93)90069-Z

Skilleter G. A.1994Refuges from predation and the persistence of estuarine clam populations.Marine Ecology Progress Series1092942

Slattery J. P.Vrijenhoek R. C.Lutz R. A.1991Heterozygosity, growth, and survival of the hard clam, Mercenaria mercenaria, in seagrass vs. sandflat habitats.Marine Biology111335342
doi:10.1007/BF01319404

Talman S. G.Keough M. J.2001Impact of an exotic clam, Corbula gibba, on the commercial scallop Pecten fumatus in Port Phillip Bay, south-east Australia: evidence of resource-restricted growth in a subtidal environment.Marine Ecology Progress Series221135143

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

Underwood A. J.Chapman M. C.Connell S. D.2000Observations in ecology: you can’t make progress on process without understanding the patterns.Journal of Experimental Marine Biology and Ecology25097115
doi:10.1016/S0022-0981(00)00181-7

Wikström S. A.Kautsky L.2004Invasion of a habitat-forming seaweed: effects on associated biota.Biological Invasions6141150doi:10.1023/B:BINV.0000022132.00398.14

Williams S. L.Grosholz E. D.2002Preliminary reports from the Caulerpa taxifolia invasion in southern California.Marine Ecology Progress Series233307310

Williams S. L., and Heck K. L.,Jr (2001). Seagrass community ecology. In ‘Marine Community Ecology’. (Eds M. D. Bertness, S. D. Gaines and M. E. Hay.) pp. 317–337. (Sinuaer Associates: Sunderland, MA.)

Winberg P. C.Lynch T. P.Murray A.Jones A. R.Davis A. R.2007The importance of spatial scale for the conservation of tidal flat macrobenthos: an example from New South Wales, Australia.Biological Conservation134310320
doi:10.1016/J.BIOCON.2006.07.019

Wonham M. J.O’Connor M.Harley C. D. G.2005Positive effects of a dominant invader on introduced and native mudflat species.Marine Ecology Progress Series289109116

Wright J. T.2005Differences between native and invasive Caulerpa taxifolia: a link between asexual fragmentation and abundance in invasive populations.Marine Biology147559569
doi:10.1007/S00227-005-1561-5

Wright J. T.Davis A. R.2006Demographic feedback between clonal growth and fragmentation in an invasive seaweed.Ecology8717441754

York P. H.Booth D. J.Glasby T. M.Pease B. C.2006Fish assemblages in habitats dominated by Caulerpa taxifolia and native seagrasses in south-eastern Australia.Marine Ecology Progress Series312223234




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