Skip to main content
Log in

Responses of common SE Australian herbivores to three suspected invasive Caulerpa spp.

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

We sought to determine whether common intertidal and shallow subtidal zone grazers would consume extracts or fronds of three invasive Caulerpa spp., all of which are now resident in southern New South Wales, Australia. We examined the responses of herbivorous fishes, echinoderms and molluscs to C. filiformis. A subset of these organisms was tested with extracts of C. scalpelliformis and C. taxifolia. Polar (seawater) extracts of C. filiformis deterred a single herbivore, Aplysia sydneyensis, but confirmed that the biological activity reported from some Caulerpa spp. is not restricted to the lipophilic fractions. The large turbinid Turbo torquatus was deterred by an ethanol extract of C. filiformis, while the small congener T. undulatus demonstrated a significant preference for palatable agar discs containing ethanol extracts of C. filiformis. However, when T. undulatus were offered a choice of fronds from five algal species in the laboratory, they readily consumed Ulva spp. and Sargassum sp., showing the lowest preference for C. filiformis. Solvent extracts of C. scalpelliformis and C. taxifolia did not significantly deter any grazers. However, the overall trend was for reduced consumption of discs containing solvent extracts of these seaweeds. Indeed, for the large urchin Centrostephanus rodgersii and in the fish trials these effects were very near significant (P<0.06). We conclude that common herbivores associated with hard substrata are highly unlikely to intercede in the spread or control of these invasive algae.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7A, B

Similar content being viewed by others

References

  • Agrawal AA, Kotanen PM (2003) Herbivores and the success of exotic plants: a phylogenetically controlled experiment. Ecol Lett 6:712–715

    Article  Google Scholar 

  • Andrew NL (1993) Spatial heterogeneity, sea urchin grazing, and habitat structure on reefs in temperate Australia. Ecology 74:292–302

    Google Scholar 

  • Andrew NL, Jones GP (1990) Patch formation by herbivorous fish in a temperate Australian kelp forest. Oecologia 85:57–68

    Article  Google Scholar 

  • Ayling AL (1978) The relation of food availability and food preferences to field diet of an echinoid Evechinus chloroticus (Valenciennes). J Exp Mar Biol Ecol 33:223–235

    Article  Google Scholar 

  • Boudouresque CF, Lemee R, Mari X, Meinesz A (1996) The invasive algae Caulerpa taxifolia is not a suitable diet for the sea urchin Paracentrotus lividus. Aquat Bot 53:245–250

    Article  Google Scholar 

  • Calvert HE, Dawes CJ, Borowitzka MA (1976) Phylogenetic relationships of Caulerpa (Chlorophyta) based on comparative chloroplast ultrastructure. J Phycol 12:149–162

    Google Scholar 

  • Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82

    Google Scholar 

  • Chang GC, Kareiva P (1999) The case of indigenous generalists in biological control. In: Hawkins BA, Cornell HV (eds) Theoretical approaches to biological control. Cambridge University Press, Cambridge, pp 13–115

  • Clarke B, Murray J, Johnson MS (1984) The extinction of endemic species by a program of biological control. Pacif Sci 38:97–104

    Google Scholar 

  • Conover WJ (1999) Practical nonparametric statistics. Wiley, New York

  • Crawley MJ (1996) Plant ecology. Blackwell, Oxford

  • Creese RG, Davis AR, Glasby TM (2004) Eradicating and preventing the spread of the invasive alga Caulerpa taxifolia in NSW. Final report to the Natural Heritage Trust’s coast and clean seas introduced marine pests program, project no. 35593. NSW Fisheries Final Report no. 64 (available at http://www.fisheries.nsw.gov.au/sci/outputs/aqua_sust/466_Crease.htm)

  • Cronin G, Hay ME (1996) Susceptibility to herbivores depends on recent history of both the plant and aninmal. Ecology 77:1531–1543

    Google Scholar 

  • Davis AR, Roberts DE, Cummins SP (1997) Rapid invasion of a sponge-dominated deep-reef by Caulerpa scalpelliformis (Chlorophyta) in Botany Bay, New South Wales. Aust J Ecol 22:146–150

    Google Scholar 

  • Davis AR, Fyfe SK, Turon X, Uriz MJ (2003) Size matters sometimes: wall height and the structure of subtidal benthic invertebrate assemblages in southeastern Australia and Mediterranean Spain. J Biogeogr 30:1797–1807

    Article  Google Scholar 

  • de Villele X, Verlaque M (1995) Changes and degradation in a Posidonia oceanica bed invaded by the introduced tropical alga Caulerpa taxifolia in the north western Mediterranean. Bot Mar 38:79–87

    Google Scholar 

  • Dodd AP (1940) The biological campaign against prickly-pear in Australia. Commonwealth Prickly Pear Board, Brisbane

  • Dumay O, Pergent G, Pergent-Martini C, Amade P (2002) Variations in caulerpenyne contents in Caulerpa taxifolia and Caulerpa racemosa. J Chem Ecol 28:343–352

    Article  Google Scholar 

  • Edgar GJ (1997) Australian marine life: the plants and animals of temperate waters. Reed, Victoria, Australia

    Google Scholar 

  • Edwards A (2002) Fauna associated with Caulerpa spp.; potential biological control of C. taxifolia. Honours thesis, Department of Biological Sciences, University of Wollongong, Wollongong, Australia

  • Fletcher WJ (1987) Interactions among subtidal Australian sea urchins, gastropods and algae: effects of experimental removals. Ecol Monogr 57:89–109

    Google Scholar 

  • Guerriero A, Meinesz A, D’Ambrosio M, Pietra F (1992) Isolation of toxic and potentially toxic sesqui- and monoterpenes from the tropical green seaweed Caulerpa taxifolia which has invaded the region of Cap Martin and Monaco. Helv Chim Acta 75:689–695

    Article  Google Scholar 

  • Guerriero A, Marchetti F, D’Ambrosio M, Senesi S, Dini F, Pietra F (1993) New ecotoxicologically and biogenetically relevant terpenes of the tropical green seaweed Caulerpa taxifolia which is invading the Mediterranean. Helv Chim Acta 76:855–864

    Article  Google Scholar 

  • Hay ME (1984) Predictable spatial escapes from herbivory: How do these affect the evolution of herbivore resistance in tropical marine communities? Oecologia 64:396–407

    Article  Google Scholar 

  • Hay ME, Colburn T, Downing D (1983) Spatial and temporal patterns in herbivory on a Caribbean fringing reef: the effects on plant distribution. Oecologia 58:299–308

    Article  Google Scholar 

  • Jousson O, Pawlowski J, Zaninetti L, Zechman FW, Dini F, Di Guiseppe G, Woodfield R, Millar A, Meinesz A (2000) Invasive alga reaches California. Nature 408:157

    Article  Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Komatsu T, Ishikawa T, Yamaguchi N, Hori Y, Ohba H (2003) But next time? Unsuccessful establishment of the Mediterranean strain of the green seaweed Caulerpa taxifolia in the Sea of Japan. Biol Invasions 5:275–278

    Article  Google Scholar 

  • Lemée R, Pesando D, Durand-Clément M, Dubreuil A, Meinesz A, Guerriero A, Pietra F (1993) Preliminary survey of toxicity of the green alga Caulerpa taxifolia introduced into the Mediterranean. J Appl Phycol 5:485–493

    Google Scholar 

  • Lucas AHS (1927) Notes on the Australian marine algae. V. Proc Linn Soc NSW 52:555–562

    Google Scholar 

  • Maron JL, Vilà M (2001) When do herbivores affect plant invasion? Evidence for the natural enemies and biotic resistance hypotheses. Oikos 95:361–373

    Article  Google Scholar 

  • May V (1976) Changing dominance of an algal species (Caulerpa filiformis (Suhr) Hering). Telopea 1:135–138

    Google Scholar 

  • Meinesz A (1999) Killer algae. University of Chicago Press, Chicago

  • Meinesz A, de Vaugelas J, Hesse B, Mari X (1993) Spread of the introduced tropical green alga Caulerpa taxifolia in northern Mediterranean waters. J Appl Phycol 5:141–147

    Google Scholar 

  • Meinesz A, Belsher T, Thibaut T, Antolic B, Mustapha KB, Boudouresque CF, Chiaverini D, Cinelli F, Cottalorda J-M, Djellouli A, El Abed A, Orestano C, Grau Antoni M, Ivesa L, Jaklin A, Langar H, Massuti-Pascual E, Peirano A, Tunesi L, de Vaugelas J, Zavodnik N, Zuljevic A (2001) The introduced green alga Caulerpa taxifolia continues to spread in the Mediterranean. Biol Invasions 3:201–210

    Article  Google Scholar 

  • Meyer KD, Paul VJ (1992) Intraplant variation in secondary metabolite concentration in three species of Caulerpa (Chlorophyta: Caulerpales) and its effects on herbivorous fishes. Mar Ecol Prog Ser 82:249–257

    Google Scholar 

  • Paul VJ, Fenical W (1986) Chemical defense in tropical green algae, order Caulerpales. Mar Ecol Prog Ser 34:157–169

    Google Scholar 

  • Paul VJ, Fenical W (1987) Natural products chemistry and chemical defence in tropical marine algae of the phylum Chlorophyta. In: Scheuer PJ (ed) Bioorganic marine chemistry. Springer, Berlin, pp 1–29

  • Paul VJ, Hay ME (1986) Seaweed susceptibility to herbivory, chemical and morphological correlates. Mar Ecol Prog Ser 33:255–264

    Google Scholar 

  • Paul VJ, Littler MM, Littler DS, Fenical W (1987) Evidence for chemical defense in tropical green algae Caulerpa ashmeadii (Caulerpaceae: Chlorophyta): isolation of bioactive sesquiterpenoids. J Chem Ecol 13:1171–1185

    CAS  Google Scholar 

  • Paul VJ, Cruz-Rivera E, Thacker RW (2001) Chemical mediation of macroalgal–herbivore interactions: ecological and evolutionary perspectives. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, Fla., USA, pp 227–265

  • Peterson CH, Renaud PE (1989) Analysis of feeding preference experiments. Oecologia 80:82–86

    Article  Google Scholar 

  • Piazzi L, Balestri E, Cinelli F (1994) Presence of Caulerpa racemosa in the north-western Mediterranean. Cryptogam Algol 15:183–189

    Google Scholar 

  • Pillman A, Woolcott GW, Olsen JL, Stam WT, King RJ (1997) Inter- and intraspecific genetic variation in Caulerpa (Chlorophyta) based on nuclear rDNA ITS sequences. Eur J Phycol 32:379–386

    Article  Google Scholar 

  • Roa R (1992) Design and analysis of multiple-choice feeding-preference experiments. Oecologia 89:509–515

    Google Scholar 

  • Sanderson JC (1997) Subtidal macroalgal assemblages in temperate Australian coastal waters, Australia. State of the Environment Technical Paper Series (Estuaries and the Sea), Department of the Environment, Canberra

  • Sant N, Delgado O, Rodriguez-Prieto C, Ballesteros E (1996) The spreading of the introduced seaweed Caulerpa taxifolia (Vahl) C. Agardh in the Mediterranean Sea: testing the boat transportation hypothesis. Bot Mar 39:427–430

    Google Scholar 

  • Secord D (2003) Biological control of marine invasive species: cautionary tales and land-based lessons. Biol Invasions 5:117–131

    Article  Google Scholar 

  • Smith CM, Walters LJ (1999) Fragmentation as a strategy for Caulerpa species: fates of fragments and implications for management of an invasive weed. Mar Ecol 2:307–319

    Article  Google Scholar 

  • Steinberg PD (1988) Effects of quantitative and qualitative variation in phenolic compounds of feeding in three species of marine invertebrate herbivores. J Exp Mar Biol Ecol 120:221–237

    Article  Google Scholar 

  • Steinberg PD, van Altena I (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol Monogr 62:189–222

    Google Scholar 

  • Thibaut T, Meinesz A (2000) Are the Mediterranean ascoglossan molluscs Oxynoe olivacea and Lobiger serradifalci suitable agents for a biological control against the invading tropical alga Caulerpa taxifolia? C R Acad Sci Ser III Life Sci 323:477–488

    Google Scholar 

  • Thibaut T, Meinesz A, Amade P, Charrier S, DeAngelis K, Ierardi S, Mangialajo L, Melneck J, Vidal V (2001) Elysia subornata (Mollusca) a potential control agent of the alga Caulerpa taxifolia (Chlorophyta) in the Mediterranean Sea. J Mar Biol Assoc UK 81:497–504

    Google Scholar 

  • Trowbridge CD (1995) Establishment of the green alga Codium fragile ssp. tomentosoides on New Zealand rocky shores: current distribution and invertebrate grazers. J Ecol 83:949–965

    Google Scholar 

  • Trowbridge CD (2004) Emerging associations on marine rocky shores: specialist herbivores on introduced macroalgae. J Anim Ecol 73:294–308

    Article  Google Scholar 

  • Trowbridge CD, Todd CD (2001) Host–plant change in marine specialist herbivores: ascoglossan sea slugs on introduced macroalgae. Ecol Monogr 71:219–243

    Google Scholar 

  • Van Driesche RG, Bellows Jr TS (1996) Biological control. Chapman and Hall, New York

  • Williamson M (1996) Biological invasions. Chapman and Hall, New York

  • Worthington DG, Fairweather PG (1989) Shelter and food interactions between Turbo undulatum (Archaeogastropoda, Turbinidae) and coralline algae on rocky seashores in New South Wales, Australia. J Exp Mar Biol Ecol 129:61–80

    Article  Google Scholar 

  • Wright JT, Benkendorff K, Davis AR (1997) Habitat associated differences in temperate sponge assemblages: the importance of chemical defence. J Exp Mar Biol Ecol 213:199–213

    Article  Google Scholar 

  • Wright JT, de Nys R, Steinberg PD (2000) Geographic variation in halogenated furanones from the red alga Delisea pulchra and associated herbivores and epiphytes. Mar Ecol Prog Ser 207:227–241

    Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Engelwood Cliffs, N.J., USA

  • Zuljevic A, Thibaut T, Elloukal H, Meinesz A (2001) Sea slug disperses the invasive Caulerpa taxifolia. J Mar Biol Assoc UK 81:343–344

    Google Scholar 

Download references

Acknowledgements

We acknowledge the assistance of D. Barker at NSW Fisheries for allowing access to their seawater facility. S. Fyfe and J. Wright improved early drafts of this manuscript. All algae and invertebrates for this study were collected under NSW Fisheries permit F265. This work was undertaken with financial assistance from the Institute for Conservation Biology, University of Wollongong. This is contribution number 252 from the Ecology and Genetics Group, University of Wollongong.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. R. Davis.

Additional information

Communicated by M.S. Johnson, Crawley

Rights and permissions

Reprints and permissions

About this article

Cite this article

Davis, A.R., Benkendorff, K. & Ward, D.W. Responses of common SE Australian herbivores to three suspected invasive Caulerpa spp.. Marine Biology 146, 859–868 (2005). https://doi.org/10.1007/s00227-004-1499-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-004-1499-z

Keywords

Navigation