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Experimental removal of the invasive Caulerpa racemosa triggers partial assemblage recovery

Published online by Cambridge University Press:  05 July 2010

J.C. Klein  and
M. Verlaque
J.C. Klein*
Affiliation:
Centre d'Océanologie de Marseille, Université de la Méditerranée, DIMAR UMR 6540, Parc Scientifique et Technologique de Luminy, case 901, 13288 Marseille cedex 9, France
M. Verlaque
Affiliation:
Centre d'Océanologie de Marseille, Université de la Méditerranée, DIMAR UMR 6540, Parc Scientifique et Technologique de Luminy, case 901, 13288 Marseille cedex 9, France
*
Correspondence should be addressed to: J.C. Klein, Centre for Research on Ecological Impacts of Coastal Cities, Marine Ecology Laboratories A11, School of Biological Sciences, University of Sydney, New South Wales 2006, Australia email: [email protected]
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Abstract

The invasive species Caulerpa racemosa var. cylindracea represents a serious threat to the diversity of benthic assemblages in the Mediterranean Sea. In the present study, a removal experiment was carried out to test whether, after 18 months of C. racemosa var. cylindracea exclusion, the macrophyte assemblage resembled a non-invaded assemblage. The results show that in the assemblage invaded by C. racemosa var. cylindracea the number of species, macrophyte cover, Shannon diversity and Pielou's evenness were lower than in the non-invaded assemblage. Erect perennial species were particularly affected and other introduced species were significantly reduced or completely excluded. After 18 months of removal/exclusion of C. racemosa var. cylindracea, only partial recovery of the macrophyte assemblage could be observed. Species numbers, total cover and erect perennial species cover were still significantly lower than in the non-invaded plots. However Shannon diversity and Pielou's evenness had reached comparable levels. In contrast to native macrophytes, the total cover of other introduced species reached a level comparable to the non-invaded plots. In summary, the present study revealed that after 18 months of C. racemosa var. cylindracea exclusion: (i) only partial recovery of the macrophyte assemblage occurred; and (ii) the development of other invasive species was favoured by the absence of C. racemosa var. cylindracea (Sisyphus effect).

Keywords

biological invasionsdead Posidonia oceanica ‘matte’invasion impactmarine macrophytesMediterranean Seaspecies introductions
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Issue 1 , February 2011 , pp. 117 - 125
Copyright
Copyright © Marine Biological Association of the United Kingdom 2010

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References

REFERENCES

Alpert, P., Bone, E. and Holzapfel, C. (2000) Invasiveness, invasibility and the role of environmental stress in the spread of non-native plants. Perspectives in Plant Ecology, Evolution and Systematics 3, 52–66.CrossRefGoogle Scholar
Augier, H. and Boudouresque, C.F. (1967) Végétation marine de l'île de Port-Cros (Parc National). I. La Baie de la Palu. Bulletin du Muséum d'Histoire Naturelle de Marseille 27, 149–168.Google Scholar
Balata, D., Piazzi, L. and Cinelli, F. (2004) A comparison among assemblages in areas invaded by Caulerpa taxifolia and C. racemosa on a subtidal Mediterranean rocky bottom. Marine Ecology—PSZNI 25, 1–13.CrossRefGoogle Scholar
Ballesteros, E. (1984) Els vegetals i la zonació litoral: espècies, comunitats i factors que influeixen en la seva distribució. PhD thesis. University of Barcelona, Spain.Google Scholar
Bando, K.J. (2006) The roles of competition and disturbance in a marine invasion. Biological Invasions 8, 755–763.CrossRefGoogle Scholar
Boudouresque, C.F. (1971) Méthodes d'étude qualitative et quantitative du benthos (en particulier du phytobenthos). Téthys 3, 79–104.Google Scholar
Boudouresque, C.F. (1974) Aire minima et peuplements algaux marins. Bulletin de la Société Phycologique de France 19, 141–157.Google Scholar
Boudouresque, C.F. and Belsher, T. (1979a) Le peuplement algal du port de Port-Vendres: recherches sur l'aire minimale qualitative. Cahiers de Biologie Marine, France 20, 259–269.Google Scholar
Boudouresque, C.F. and Belsher, T. (1979b) Une méthode et determination de l'aire minimale qualitative. Rapport de la Commission Internationale pour l'Exploration Scientifique de la Mer Méditerranée 25/26, 273–275.Google Scholar
Boudouresque, C.F. and Verlaque, M. (2002) Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Marine Pollution Bulletin 44, 32–38.CrossRefGoogle ScholarPubMed
Boudouresque, C.F. and Verlaque, M. (2005) Nature conservation, marine protected areas, sustainable development and the flow of invasive species to the Mediterranean Sea. Scientific Reports of the Port-Cros National Park, France 21, 29–54.Google Scholar
Boudouresque, C.F., Ruitton, S. and Verlaque, M. (2005) Large-scale disturbances, regime shift and recovery in littoral systems subject to biological invasions. In Velikova, V. and Chipev, N. (eds) Large-scale disturbances (regime shifts) and recovery in aquatic ecosystems: challenges for management towards sustainability. Rome: UNESCO, pp. 85–101.Google Scholar
Branch, G.M. and Steffani, C.N. (2004) Can we predict the effects of alien species? A case-history of the invasion of South Africa by Mytilus galloprovincialis (Lamarck). Journal of Experimental Marine Biology and Ecology 300, 189–215.CrossRefGoogle Scholar
Brown, B.J., Mitchell, R.J. and Graham, S.A. (2002) Competition for pollination between an invasive species (purple loosestrife) and a native congener. Ecology 83, 2328–2336.CrossRefGoogle Scholar
Buia, M.C., Gambi, M.C., Terlizzi, A. and Mazzella, L. (2001) Colonization of Caulerpa racemosa along the southern Italian coasts: I. Distribution, phenological variability and ecological role. In Gravez, V., Ruitton, S., Boudouresque, C.F., Le Direac'h, L., Meinesz, A., Scabbia, G. and Verlaque, M. (eds) Fourth International Workshop on Caulerpa taxifolia. Marseille: GIS Posidonie Publication, pp. 352–360.Google Scholar
Capiomont, A., Breugnot, E., Den Haan, M. and Meinesz, A. (2005) Phenology of a deep-water population of Caulerpa racemosa var. cylindracea in the northwestern Mediterranean Sea. Botanica Marina 48, 80–83.CrossRefGoogle Scholar
Carriglio, D., Sandulli, R., Deastis, S., Gallo d'Addabbo, M. and Grimaldi de Zio, S. (2003) Caulerpa racemosa spread effects on the meiofauna of the Gulf of Taranto. Biologia Marina Mediterranea 10, 509–511.Google Scholar
Casu, D., Ceccherelli, G., Palomba, D., Curini-Gelletti, M. and Castelli, A. (2005) Effetto immediato della rimozione di Caulerpa racemosa sullo zoobenthos dell'infralittorale superficiale roccioso di Porto Torres (Nord Sardegna). XV Meeting of the Italian Society of Ecology, pp. 1–3.Google Scholar
Cinelli, F. and Salghetti-Drioli, U. (1983–1984) I popolamenti algali di una ‘matte’ morta di Posidonia oceanica (L.) Delile di Capo S. Andrea (Isola d'Elba). Nova Thalassia 6, 547–554.Google Scholar
Cinelli, F., Boudouresque, C.F., Fresi, E., Marcot, J. and Mazzella, L. (1977a) L'aire minima du phytobenthos dans le port de Sant d'Angelo (Ischia, Italie). Rapport de la Commission Internationale pour l'Exploration Scientifique de la Mer Méditerranée 24, 149–152.Google Scholar
Cinelli, F., Fresi, E., Idato, E. and Mazzella, L. (1977b) L'aire minima du phytobenthos dans un peuplement à Cystoseira mediterranea de l'île d'Ischia (Golfe de Naples). Rapport de la Commission Internationale pour l'Exploration Scientifique de la Mer Méditerranée 24, 113–115.Google Scholar
Coppejans, E. (1980) Phytosociological studies on Mediterranean algal vegetation: rocky surfaces of the photophilic infralittoral zone. In Price, J.H., Irvine, D.E.G. and Farnham, W.F. (eds) The shore environment. Volume 2: ecosystems. London and New York: Academic Press, pp. 371–393.Google Scholar
Di Martino, V. and Giaccone, G. (1996) Biodiversità in associazioni dipendenti di epibionti vegetali in prati a Caulerpe nel Mediterraneo. Biologia Marina Mediterranea 3, 32–39.Google Scholar
Gray, J.S. (1997) Marine biodiversity: patterns, threats and conservation needs. Biodiversity Conservation 6, 153–175.CrossRefGoogle Scholar
Guiry, M.D. and Guiry, G.M. (2009) AlgaeBase version 4.2. World-wide electronic publication, National University of Ireland, Galway. http://www.algaebase.org; accessed 15 March 2009.Google Scholar
Hulme, P.E. and Bremner, E.T. (2006) Assessing the impact of Impatiens glandulifera on riparian habitats: partitioning diversity components following species removal. Journal of Applied Ecology 43, 43–50.CrossRefGoogle Scholar
Jousson, O., Pawlowski, J., Zaninetti, L., Meinesz, A. and Boudouresque, C.F. (1998) Molecular evidence for the aquarium origin of the green alga Caulerpa taxifolia introduced to the Mediterranea Sea. Marine Ecology Progress Series 172, 275–280.CrossRefGoogle Scholar
Klein, J. and Verlaque, M. (2008) The Caulerpa racemosa invasion: a critical review. Marine Pollution Bulletin 56, 205–225.CrossRefGoogle ScholarPubMed
Klein, J.C. and Verlaque, M. (2009a) Macroalgal assemblages of disturbed coastal detritic bottoms subject to invasive species. Estuarine, Coastal and Shelf Science 82, 461–468.CrossRefGoogle Scholar
Klein, J.C. and Verlaque, M. (2009b) Macrophyte assemblage associated with an invasive species exhibiting temporal variability in its development pattern. Hydrobiologia 636, 369–378.CrossRefGoogle Scholar
Levine, J.M., Vilà, M., D'Antonio, C.M., Dukes, J.S., Grigulis, K. and Lavorel, S. (2003) Mechanisms underlying the impacts of exotic plant invasions. Proceedings of the Royal Society London, B 270, 775–781.CrossRefGoogle ScholarPubMed
Littler, M.M. and Littler, D.S. (1980) The evolution of thallus form and survival strategies in benthic marine macroalgae—field and laboratory tests for a functional form model. American Naturalist 116, 25–44.CrossRefGoogle Scholar
Mack, M.C. and Lonsdale, W.M. (2002) Eradicating invasive plants: hard-won lessons for islands. In Veitch, C.R. and Clout, M.N. (eds) Turning the tide: the eradication of invasive species. IUCN, Gland, Switzerland and Cambridge, UK, pp. 164–172.Google Scholar
Morrison, L.W. (2000) Mechanisms of interspecific competition among an invasive and two native fire ants. Oikos 90, 238–252.CrossRefGoogle Scholar
Myers, J.H., Simberloff, D., Kuris, A.M. and Carey, J.R. (2000) Eradication revisited: dealing with exotic species. Trends in Ecology and Evolution 15, 316–320.CrossRefGoogle ScholarPubMed
Piazzi, L. and Ceccherelli, G. (2006) Persistence of biological invasion effects: recovery of macroalgal assemblages after removal of Caulerpa racemosa var. cylindracea. Estuarine, Coastal and Shelf Science 68, 455–461.CrossRefGoogle Scholar
Piazzi, L. and Cinelli, F. (2003) Evaluation of benthic macroalgal invasion in a harbour area of the western Mediterranean Sea. European Journal of Phycology 38, 223–231.CrossRefGoogle Scholar
Piazzi, L., Ceccherelli, G. and Cinelli, F. (2001) Threat to macroalgal diversity: effects of the introduced green alga Caulerpa racemosa in the Mediterranean. Marine Ecology Progress Series 210, 149–159.CrossRefGoogle Scholar
Piazzi, L., Balata, D., Cecchi, E. and Cinelli, F. (2003) Co-occurrence of Caulerpa taxifolia and C. racemosa in the Mediterranean Sea: interspecific interactions and influence on native macroalgal assemblages. Cryptogamie Algologie 24, 233–243.Google Scholar
Piazzi, L., Meinesz, A., Verlaque, M., Akçali, B., Antolić, B., Argyrou, M., Balata, D., Ballesteros, E., Calvo, S., Cinelli, F., Cirik, S., Cossu, A., D'Archino, R., Djellouli, A.S., Javel, F., Lanfranco, E., Mifsud, C., Pala, D., Panayotidis, P., Peirano, A., Pergent, G., Petrocelli, A., Ruitton, S., Žuljević, A. and Ceccherelli, G. (2005) Invasion of Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) in the Mediterranean Sea: an assessment of the spread. Cryptogamie Algologie 26, 189–202.Google Scholar
Piazzi, L., Balata, D. and Cinelli, F. (2007) Invasions of alien macroalgae in Mediterranean coralligenous assemblages. Cryptogamie Algologie 28, 289–301.Google Scholar
Ribera Siguan, M.A. (2003) Pathways of biological invasions of marine plants. In Ruiz, G.M. and Carlton, J.T. (eds) Invasive species: vectors and management strategies. Washington, DC: Island Press, pp. 183–226.Google Scholar
Richardson, D.M., Pyšek, P., Rejmánek, M., Barbour, M.G., Panetta, F.D. and West, C.J. (2000) Naturalization and invasion of alien plants: concepts and definitions. Diversity and Distributions 6, 93–107.CrossRefGoogle Scholar
Ruitton, S., Verlaque, M. and Boudouresque, C.F. (2005) Seasonal changes of the introduced Caulerpa racemosa var. cylindracea (Caulerpales, Chlorophyta) at the northwest limit of its Mediterranean range. Aquatic Botany 82, 55–70.CrossRefGoogle Scholar
Sala, O.E., Chapin, F.S. III, Armesto, J.J., Berlow, E., Bloomfield, J., Dirzo, R., Huber-Sanwald, E., Huenneke, L.F., Jackson, R.B., Kinzig, A., Leemans, R., Lodge, D.M., Mooney, H.A., Oesterheld, M., Poff, N.L., Sykes, M.T., Walker, B.H., Walker, M. and Wall, D.H. (2000) Global biodiversity scenarios for the year 2100. Science 287, 1770–1774.CrossRefGoogle ScholarPubMed
Salghetti-Drioli, U., Pardi, G. and Cinelli, F. (1985) Studio sull'epifitismo algale di un Thanato-Posidonietum oceanicae del litorale di Livorno. Bolletino dell'Accademia Gioenia di Scienze Naturali di Catania 18, 455–462.Google Scholar
Salghetti-Drioli, U., Pardi, G., Cinelli, F. and Della Pieta, F. (1989) I popolamenti fitobentonici di ‘intermatte’ in una ‘matte’ morta di Posidonia oceanica (Linnaeus) Delile a Livorno (Mar Tirreno, Italia). In Boudouresque, C.F., Meinesz, A., Fresi, E. and Gravez, V. (eds) International workshop on Posidonia beds. Marseille: GIS Posidonie Publication, pp. 115–125.Google Scholar
Simberloff, D., Parker, I. and Windle, P.N. (2005) Introduced species policy, management, and future research needs. Frontiers in Ecology and the Environment 3, 12–20.CrossRefGoogle Scholar
Soulé, M.E. (1990) The onslaught of alien species, and other challenges in the coming decades. Conservation Biology 4, 233–239.CrossRefGoogle Scholar
Steneck, R.S. and Dethier, M.N. (1994) A functional group approach to the structure of algal-dominated communities. Oikos 69, 476–498.CrossRefGoogle Scholar
Verlaque, M., Boudouresque, C.F., Meinesz, A. and Gravez, V. (2000) The Caulerpa racemosa complex (Caulerpales, Ulvophyceae) in the Mediterranean Sea. Botanica Marina 43, 49–68.CrossRefGoogle Scholar
Verlaque, M., Afonso-Carillo, J., Gil-Rodríguez, M.C., Durand, C., Boudouresque, C.F. and Le Parco, Y. (2004) Blitzkrieg in a marine invasion: Caulerpa racemosa var. cylindracea (Bryopsidales, Chlorophyta) reaches the Canary Islands (north-east Atlantic). Biological Invasions 6, 269–281.CrossRefGoogle Scholar
Vitousek, P.M., D'Antonio, C.M., Loope, L.L., Rejmánek, M. and Westbrooks, R. (1997) Introduced species: a significant component of human-caused global change. New Zealand Journal of Ecology 21, 1–16.Google Scholar
Wallentinus, I. (2002) Introduced marine algae and vascular plants in European aquatic environments. In Leppäkoski, E., Gollasch, S. and Olenin, S. (eds) Invasive aquatic species in Europe: distribution, impacts and management. Dordrecht, The Netherlands: Kluwer Academic Publisher, pp. 27–52.CrossRefGoogle Scholar
Zavaleta, E.S., Hobbs, R.J. and Mooney, H.A. (2001) Viewing invasive species removal in a whole-ecosystem context. Trends in Ecology and Evolution 16, 454–459.CrossRefGoogle Scholar
Zenetos, A., Çinar, M.E., Pancucci-Papadopoulou, M.A., Harmelin, J.G., Furnari, G., Andaloro, F., Bellou, N., Streftaris, N. and Zibrowius, H. (2005) Annotated list of marine alien species in the Mediterranean with records of the worst invasive species. Mediterranean Marine Science 6, 63–118.CrossRefGoogle Scholar