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The Caulerpa Racemosa Invasion: a Critical Review

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The Caulerpa Racemosa Invasion: a Critical Review Available online at www.sciencedirect.com Marine Pollution Bulletin 56 (2008) 205–225 www.elsevier.com/locate/marpolbul Review The Caulerpa racemosa invasion: A critical review Judith Klein *, Marc Verlaque Universite´ de la Me´diterrane´e, Centre d’Oce´anologie de Marseille, DIMAR UMR 6540, Parc Scientifique et Technologique de Luminy, Case 901, 13288 Marseille Cedex 9, France Abstract Caulerpa racemosa var. cylindracea is a marine Chlorophyta introduced into the Mediterranean Sea from south-western Australia. Since 1990, it has been invading the Mediterranean Sea and the Canary Islands, raising ecological problems. Although this invasion event can be considered as one of the most serious in the history of species introduced into the Mediterranean Sea, C. racemosa has not trig- gered as much attention as the famous ‘‘killer alga’’ Caulerpa taxifolia. The aim of the present study was: (i) to summarize the current state of knowledge with regard to the distribution, the various biological and ecological characteristics of the introduced C. racemosa and its impact on the Mediterranean coastal environment; (ii) to discuss the various hypotheses regarding the explanation for its rapid and successful spread; (iii) to investigate the disparity in the treatment of C. racemosa and Caulerpa taxifolia invasions; and (iv) to outline future research needs. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Biological invasions; Impact; Marine macrophytes; Mediterranean Sea; Review; Species introduction 1. Introduction invaded areas and prohibited the aquarium trade for the species. However, this attempt at management was not The Mediterranean Sea harbours around 600 intro- repeated when a second introduced Caulerpa belonging duced species representing 5% of the known flora and to the Caulerpa racemosa complex, which is widely distrib- fauna (Boudouresque and Verlaque, 2005; Boudouresque uted in warm temperate and tropical seas (see Fig. 17 in et al., 2005; Zenetos et al., 2005). It can be considered as Verlaque et al., 2000), was found to have invaded the Med- one of the regions most severely affected by marine species iterranean Sea. invasions along with the Bay of San Francisco, the Baltic Is it unnecessary to worry about the invasion of C. race- and the Black Sea. Around 100 macrophyte species are mosa? Is it impossible to do anything about it or do we not considered as having been introduced into the Mediterra- know enough? To answer these questions, the present study nean Sea (Ribera Siguan, 2002). aims to survey all studies dealing with this recently intro- The eradication and control of invasive marine species is duced C. racemosa (description of the species, sightings, a difficult task that is mainly feasible in a restricted area impact studies, population dynamic studies) and to sum- such as in bays and harbours (Kuris and Culver, 1999; marize the current state of knowledge. In addition, gaps Bax et al., 2001; Anderson, 2005). Attempts at manage- in current knowledge are identified and recommendations ment of invasive marine species in the Mediterranean Sea for future lines of research are offered. remain rare. Caulerpa taxifolia (Vahl) C. Agardh was the first macrophyte invasion to draw widespread public atten- 2. Materials and methods tion. Consequently, the authorities in some Mediterranean countries (Spain, France) tried to eradicate and control In order to identify all relevant studies for the present survey, the databases Web of Science (http://portal.isi- * Corresponding author. Tel.: +33 491 829 067; fax: +33 491 411 265. knowledge.com/), Science Direct (http://www.sciencedi- E-mail address: [email protected] (J. Klein). rect.com) and Aquatic Sciences and Fisheries Abstracts 0025-326X/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.marpolbul.2007.09.043 206 J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225 (http://www.csa.com/factsheets/aquclust-set-c.php) have Table 1 been searched for articles dealing with the recently intro- Number of articles included, excluded and total analyzed duced C. racemosa, frequently referred to as ‘‘invasive C. Evaluation Number of articles racemosa’’. The search was conducted using ‘‘Caulerpa’’, Includeda Pertinent 150 ‘‘racemosa’’ and ‘‘invasive’’ in different combinations. Excluded Redundant 19 For the ‘grey’ literature and literature not indexed in stan- Total 169 dard databases, the library of the laboratory of the Ocean- a Thereof two partially excluded due to serious bias and ology Centre of Marseille was searched for Mediterranean misidentification. Conference proceedings, Mediterranean journals, non-gov- ernmental and governmental publications. Furthermore the search engine Caulerpa On Line (http://www.unice.fr/ 3.1. Taxonomy LEML) was consulted in order to complete recorded pres- ˚ ence data. Special attention was paid to the identification Caulerpa racemosa (Forsskal) J. Agardh is a Chloro- of the species; due to identification difficulties several phyta of the order Bryopsidales belonging to the family ‘‘false’’ sightings have been published. Caulerpaceae. The genus Caulerpa includes approximately The following criteria were used to select relevant publi- 85 species (Guiry and Guiry, 2007). There is much confu- cations to include in the present survey. The complete pub- sion in the literature regarding the taxonomic classification lication list can be requested from the authors. The criteria of several Caulerpa species complexes (including the C. for inclusion were: racemosa complex), within which different undetected spe- cies are certainly confused. The C. racemosa complex is dis- – Identity: if the recently introduced C. racemosa was mis- tinguished from the flat feather-like Caulerpa taxifolia by identified as another taxon and recorded under a differ- spherical, club-shaped or mushroom- to disc-shaped ent name, it was nevertheless taken into account. branchlets. A high number of infraspecific taxa have been described inside the C. racemosa complex. However, high The criteria for exclusion were: morphological plasticity induced by environmental param- eters renders the validity of numerous taxa questionable – Redundancy: if a study was published several times (e.g. (Ohba and Enomoto, 1987; Prud’homme van Reine in conference proceedings, national journals and inter- et al., 1996). national journals) the article in the journal with highest In the Mediterranean Sea, three infra-specific taxa of C. impact factor or with best accessibility was considered. racemosa have been identified (Verlaque et al., 2000, 2003): For sightings the first date was chosen regardless of impact factor or accessibility. Articles not adding any – a taxon corresponding to the two varieties C. racemosa new information were excluded. var. turbinata (J. Agardh) Eubank and var. uvifera (C. – Serious bias. Agardh) J. Agardh, – Identity: if a species was incorrectly identified as C. race- – C. racemosa var. lamourouxii (Turner) Weber-van Bosse mosa var. cylindracea or invasive C. racemosa it was not f. requienii (Montagne) Weber-van Bosse, taken into account. Misidentifications were revealed – the recently introduced C. racemosa. based on the descriptions and photos. The identity and origin of the recently introduced C. The results were summarized using major key-words. racemosa in the Mediterranean Sea remained obscure for one decade. Various scenarios have been proposed to explain the sudden spread of C. racemosa in the Mediterra- 3. Results nean Sea. First it was speculated that C. racemosa was a Lessepsian migrant1 from the Red Sea (Alongi et al., Overall, 169 articles have been examined; thereof 19 1993; Giaccone and Di Martino, 1995a). However, mor- articles have been excluded due to redundancy and parts phological examination and bibliographical analysis ruled of two publications because of serious bias and misidentifi- out the idea of a lessepsian migration while supporting cation (Table 1). The articles dealing with the recently the hypothesis of the species having been introduced (Verl- introduced C. racemosa have mostly been published in aque et al., 2000). Molecular data confirmed the morpho- national journals or Mediterranean conference proceedings logical findings and suggested a hybrid origin for the (around 63%), which are not all indexed in the standard species (Durand et al., 2002). Finally, Caulerpa cylindracea databases (e.g. Web of Science, Science Direct). Far fewer Sonder (1845) endemic from south-western Australia and articles have been published in international peer-reviewed more specifically from the region between Perth and Hope- journals (around 37%). The high percentage of difficult to access ‘grey’ literature hinders the circulation of informa- tion and requires extensive networking for information 1 Lessepsian migrant: species introduced into the Mediterranean Sea exchange. from the Red Sea via the Suez Canal after its opening in 1869. J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225 207 toun (Harvey, 1858; Womersley, 1984) was recognized as the taxon that was recently introduced into the Mediterra- nean Sea (Fama` et al., 2000; Verlaque et al., 2003). A mor- phological and genetic study classified this taxon as C. racemosa var. cylindracea (Sonder) Verlaque, Huisman and Boudouresque (hereafter C. racemosa)(Verlaque et al., 2003). The identity of specimens from Croatia, Cyprus, France, Greece, Italy, Turkey and the Canary Islands has been proved by genetic studies (Fama` et al., 2000; Verlaque et al., 2000, 2003; Nuber et al., 2007).
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