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The Introduced Green Alga Caulerpa Taxifolia Continues to Spread in the Mediterranean

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The Introduced Green Alga Caulerpa Taxifolia Continues to Spread in the Mediterranean Biological Invasions 3: 201–210, 2001. © 2002 Kluwer Academic Publishers. Printed in the Netherlands. Invasion note The introduced green alga Caulerpa taxifolia continues to spread in the Mediterranean Alexandre Meinesz1,∗, Thomas Belsher2, Thierry Thibaut1, Boris Antolic3, Karim Ben Mustapha4, Charles-Franc¸ois Boudouresque5, Daniele` Chiaverini1, Francesco Cinelli6, Jean-Michel Cottalorda1, Aslam Djellouli7, Amor El Abed3, Carla Orestano8, Antoni M. Grau9, Ljiljana Ivesa10, Andrej Jaklin10, Habib Langar6, Enric Massuti-Pascual9, Andrea Peirano11, Leonardo Tunesi12, Jean de Vaugelas1, Nevenka Zavodnik10 & Ante Zuljevic3 1Laboratoire Environnement Marin Littoral, Universite´ de Nice-Sophia Antipolis, 06108 Nice Cedex 2, France; 2IFREMER, Centre de Brest, Departement´ d’Ecologie cotiˆ ere,` BP 70, 29280 Plouzane´ Cedex, France; 3Laboratory of Benthos, Institute of Oceanography and Fisheries, I. Mestrovica 63, 21000 Split, P.P. 500, Croatia; 4Institut National des Sciences et des Technologies de la mer (INSTM) 2025 Salammbo,ˆ Tunisia; 5Centre d’Oceanologie´ de Marseille, UMR CNRS 6540, Campus de Luminy, 13288 Marseille Cedex 9, France; 6Dipartimento di Scienze dell’Uomo e dell’Ambiente, Universita` di Pisa, Via A. Volta, 6, 56121 Pisa, Italy; 7Faculte´ des Sciences de Tunis, Campus Universitaire, 1060 Tunis, Tunisia; 8Laboratorio di Ecologia Acquatica, Dipartimento di Scienze Botaniche, Universita` degli studi di Palermo, Via Archirafi, 38, 90123, Palermo, Italy; 9Conselleria d’Agricultura i Pesca, C/. dels Foners, 10, 07006 Palma de Mallorca, Spain; 10Laboratory for Ecology and Systematics, Center for Marine Research, Obala Giordano Paliaga 5, 52210 Rovinj, Croatia; 11ENEA Ente per le Nuove Technologie, l’Energia e l’Ambiente, Centro Ricerche Ambiente Marino, C.P. 224, 19100 La Spezia, Italy; 12ICRAM Central Institute for Applied Marine Research, via di Casalotti, 300, 00166 Rome, Italy; ∗Author for correspondence (e-mail: [email protected]; fax: +33-4-92076849) Received 3 April 2001; accepted in revised form 27 September 2001 Key words: benthic survey, Caulerpa taxifolia, introduced species, invasive species, Mediterranean Sea Abstract The tropical green alga Caulerpa taxifolia in the Mediterranean has spread steadily since its introduction in 1984. At the end of 2000, approximately 131 km2 of benthos had been colonized in 103 independent areas along 191 km of coastline in six countries (Spain, France, Monaco, Italy, Croatia and Tunisia). Large regions neighboring the invaded areas appear favorable to further colonization, and there is thus no reason to believe that spreading will slow down in the years to come. Abbreviations: ENEA – Ente per le Nuove Technologie, l’Energia e l’Ambiente (National-Italian-Committee for Research and Development of New Technologies and Environment); ICRAM – Istituto Centrale per la Ricerca Scientifica e Technologica Applicata al Mare (Central Institute for Scientific and Technological Research on Sea); IFREMER – Institut Franc¸ais de Recherches pour l’Exploitation de la Mer (French Research Institute for Marine Development); rDNA ITS – Internal Transcribed Spacer (ITS) of ribosomal DNA 202 Introduction of the world. In order to reduce the risks of additional invasions, it is now illegal to import or be in possession Marine algal invasions have played important roles of this alga in France, Australia, the USA and certain in community structure around the world (Ribera and regions of Spain. Boudouresque 1995). A major algal invasion was first In light of the discovery of invasive strains of detected in the Mediterranean Sea in 1984 when the C. taxifolia in several non-Mediterranean localities, tropical green alga Caulerpa taxifolia (Vahl)C. Agardh and considering the global threat it may constitute for was observed a few meters from the public aquarium temperate and tropical littoral communities, several in Monaco, where it was used as a decorative alga and authors have recently attempted to describe the current from where it was accidentally released (Meinesz and status of this alga in the Mediterranean Sea. The use of Hesse 1991). qualitative adjectives, such as ‘carpeted’ or ‘infested’, Genetic studies based on sequence analysis of the and older quantitative data, has resulted in confusion rDNA ITS region in a large number of Caulerpa sam- regarding the history of the spread of C. taxifolia in the ples collected both from the Mediterranean and public Mediterranean Sea (Kaiser 2000; Dalton 2000; Gili aquaria (including samples originating from the algal 2000; Chisholm et al. 2000). In the present paper, we cultures cultivated in Monaco) have revealed the exten- clarify the current status and dynamics of the spread of sive homogeneity of this invasive strain, which is now Caulerpa in the Mediterranean. available worldwide in the aquarist trade (Jousson et al. Centralized monitoring efforts, within the frame- 1998; Olsen et al. 1998). These genetic studies, in addi- work of two European programs (Life DGXI), led to the tion to morphological, biogeographical and taxonomic regular surveying of the C. taxifolia invasion until 1997 considerations (Meinesz et al. 1994; Meinesz and (Meinesz et al. 1997, 1998). Since then, the spread of Boudouresque 1996) confirm the identity of this alga as the alga has been monitored independently, by means C. taxifolia. It is not a cryptic species that has developed of standardized methods, by national organizations from the warming of Mediterranean waters involving and/or research institutes. The observations, emanating the subsequent ‘metamorphosis’ of Caulerpa mexicana from six Mediterranean countries concerned with the (Sonder) J. Agardh (located in Israel and Lebanon, C. taxifolia invasion, have been brought together here eastern Mediterranean) as proposed by Chisholm et al. in an effort to assess current invasion status. (1995). The worldwide availability of the invasive strain of Methods C. taxifolia through the aquarium trade forewarned of additional aquarium-related introductions around the Several international groups are involved in monitoring world. In June 2000 an invasive strain of C. taxifolia the spread of C. taxifolia in the Mediterranean Sea. was discovered in San Diego and Los Angeles on the Consequently, standardized methods were established southern California coast. C. taxifolia had not pre- to measure the spread of this alga consistently on both viously been reported from the Pacific coast of the spatial and temporal scales (Vaugelas et al. 1999). Americas (Dalton 2000; Kaiser 2000). Millar (2001) Regional or global status can thus be described and observed a proliferation of C. taxifolia near Sydney, compared from one year to the next. The standard- Australia, approximately 600 km south of the known ization of colonization characteristics has led to the range of autochthonous populations. identification of three levels of colonization (Table 1 Sequence analysis (rDNA ITS region) and DNA fin- and Figure 1): gerprints of invasive, aquarium and natural worldwide strains of C. taxifolia, and sequence analysis of 16S Level I is the first stages of colonization, in which rDNA of bacteria associated with C. taxifolia, revealed one to several colonies occurring less than 100 m that the California strains are identical to those found apart occupy a total surface area less than 1000 m2. in the Mediterranean and in many aquaria, and are very Under these conditions it is relatively easy to esti- similar to those collected from Australia (Jousson et al. mate the surface area covered by the alga (referred 2000; Wiedenmann et al. 2001; Meusnier et al. 2001). to as the covered area) and to delimit the exact These results support the hypothesis that the invasive perimeter of the area of dispersal by SCUBA strain originated in southern Australia and has been diving. The area included by the perimeter of the disseminated via the aquarium trade to several parts established colonies is called the ‘affected area’. 203 Table 1. Descriptive parameters for each level of colonization of C. taxifolia. Levels of Descriptive parameters colonization Covered Affected Concerned Number of surface Surace Coastline Surface Coastline colonies I Threshold <1000 m2 Parameters + ++−−+ II Threshold >1000 m2 <10 ha Parameters − ++−−− III Threshold >1000 m2 >10 ha Parameters − −−++− +: applicable, − : not applicable (after Vaugelas et al. 1999). Figure 1. Theoretical configuration of the three levels of colonization of C. taxifolia. In level III the position of the dozen or hundred main colonies, involving more than 100 ha and covering much more than 1000 m2, is not presented (after Vaugelas et al. 1999). Level II refers to the next step of spreading. It is area less than 10 ha. During this stage of the inva- characterized by several colonies that occur within sion it is both time-consuming and futile to measure 250 m of each other, that cover a total area of more the covered area as the alga grows and spreads very than 1000 m2, and that are dispersed over a surface quickly. The best method to estimate the extent of 204 coverage is to delimit the perimeter that incorpo- France and Monaco rates all of the colonies. We refer to this value again as ‘affected area’. The first discovery of C. taxifolia occurred in 1984 in Level III is attained when dozens or hundreds of Monaco. Six years later, it was observed in France, colonies of various sizes are dispersed over a sur- 6 km east of Monaco (Meinesz and Hesse 1991). By face area greater than 10 ha, with a total cov- the end of 2000, 76 independent
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