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(Caulerpales, Chlorophyta) in the Mediterranean Cryptogamie,Algol., 2005, 26 (2): 189-202 ©2005 Adac.Tous droits réservés Invasion of Caulerpa racemosa var. cylindracea (Caulerpales,Chlorophyta) in the Mediterranean Sea: an assessment of the spread Luigi PIAZZI a * ,Alexandre MEINESZ b ,Marc VERLAQUE c ,Baris AKÇALI d , Boris ANTOLIĆ e ,Marina ARGYROU f ,David BALATA a , Enric BALLESTEROS g ,Sebastiano CALVO h ,Francesco CINELLI a , Sukran CIRIKd ,Andrea COSSU j ,Roberta D’ARCHINO k , Aslam Sami DJELLOULI l ,Fabrice JAVELb ,Edwin LANFRANCO m , Carmen MIFSUD m ,David PALA j ,Panayotis PANAYOTIDIS n , Andrea PEIRANO o ,Gérard PERGENT p ,Antonella PETROCELLI q , Sandrine RUITTON c ,Ante Ž ULJEVIĆ e ,Giulia CECCHERELLI j a Dipartimento di Scienze dell’Uomo e dell’Ambiente,Università di Pisa, Via A. Volta 6, 56126 Pisa, Italy b Laboratoire Environnement Marin Littoral, EA 3156 Université de Nice-Sophia Antipolis,06108 Nice Cedex 2, France c UMR6540-COM, Université de la Méditerranée,Parc de Luminy, 13288 Marseille Cedex 9, France d Institute of Marine Sciences and Technology,University of Dokuz Eylül, 35340 Izmir,Turkey e Institute of Oceanography and Fisheries, š et. I. Meš trović a 63, 21000 Split, Croatia f Department of Fisheries and Marine Research, Ministry of Agriculture, Natural Resources and Environment. 13, Aeolou Str.1416 Nicosia, Cyprus g Centre d’Estudis Avançats de Blanes,CSIC,Acc.Cala Sant Francesc 14, 17300 Blanes,Girona, Spain h Dipartimento di Scienze Botaniche,Università di Palermo,Via Archirafi 38, 90123 Palermo,Italy j Dipartimento di Botanica ed Ecologia vegetale,Università di Sassari, Via F. Muroni 25, I-07100 Sassari (Italy) k Dipartimento di Biologia Vegetale,Università “La Sapienza”, Piazzale A. Moro 5, 00185 Roma, Italy l Département de Biologie,Faculté de Sciences de Tunis,1002 Tunis,Tunisie m Malta Environment and Planning Authority,P.O.box 200, CMR 01 St. F. Ramlin, Valletta, Malta n Institute of Oceanography,Hellenic Center of Marine Research. POB 712. 19013 Anavissos,Athens,Greece o ENEA, Centro Ricerche Ambiente Marino,C.P.224, 19100 La Spezia, Italy p Equipe « Ecosystèmes Littoraux », Université de Corse,B.P.52, 20250 Corte,France q Istituto Ambiente Marino Costiero-C.N.R., Talassografico “A.Cerruti”, V. Roma 3, 74100 Taranto,Italy (Received 15 February 2004, accepted 19 July 2004) * Correspondence and reprints: [email protected] Communicating editor: Fabio Rindi 190 L. Piazzi et al. Abstract – The aim of this paper is to evaluate the colonization of the green alga Caulerpa racemosa var. cylindracea thirteen years after it was signalled in the Mediterranean Sea. The alga has been recorded along the coasts of 11 nations,developing on all kind of sub- strata, both in polluted and in unpolluted areas,between 0 and 70 m depth. The length of coastline affected by the invasion of C. racemosa var. cylindracea in Spain, France,Italy and Croatia ranged from 700 to 750 km at the end of 2003. The main aspects of the ecology of the species in the Mediterranean Sea and the effects of the invasion on human activities in coastal areas are also discussed. Biological invasion / Caulerpa racemosa / distribution / ecology / Mediterranean Sea Résumé – Invasion de l’algue Caulerpa racemosa (Caulerpales,Chlorophyta) en Mer Méditerranée :le bilan de treize années de colonisation. L’article a comme objet de pré- senter un bilan de la colonisation de la Méditerranée par l’algue verte introduite Caulerpa racemosa var. cylindracea,treize années après le début de son expansion. L’algue a été signalée le long des côtes de 11 états.Elle pousse entre 0 et 70 mètres de profondeur sur tous les types de substrats,aussi bien en zones polluées qu’en zones non polluées.Le linéaire de côte concernée par l’invasion de C. racemosa var. cylindracea entre l’Espagne, la France,l’Italie et la Croatie a été estimé entre 700 et 750 km fin 2003. Les aspects majeurs de l’écologie de l’espèce en Méditerranée les conséquences de son expansion sur les activités humaines en zone côtière sont également discutés. Caulerpa racemosa / distribution / écologie / invasion / Mer Méditerranée INTRODUCTION Biological invasions represent an important aspect of human-induced global change and a serious ecological problem (Carlton, 1989; Abrams,1996; Vitouseck et al., 1997; Harris & Tyrrell, 2001). Alien species are widely studied by ecologists and environmental managers.In fact, knowledge of ecological traits of invaders and assessment of damage are fundamental for predicting the conse- quences of invasions and finding effective methods to control and mitigate this form of pollution (Bax et al., 2001; Allendorf & Lundquist, 2003). Species of macroalgae have been responsible for some of the most dra- matic invasions in marine habitats (Carlton & Scanlon, 1985; Rueness,1989; Verlaque,1994; Meinesz et al., 2001; Silva et al., 2002). In the Mediterranean Sea, more than 90 taxa of red, brown and green algae have been introduced and at least 8 of them are considered invasive (Boudouresque & Verlaque,2002). Among these latter,two species of Caulerpa J.V. Lamouroux, Caulerpa taxifolia (Vahl) C. Agardh and C. racemosa (Forsskål) J. Agardh, have caused serious biological pollution. Invasions of Caulerpa species are particularly threatening because of (1) their ability to spread rapidly over all kind of substrata, (2) their high rates of vegetative dispersal and (3) their high competitiveness related to overgrowth capabilities,production of allelopathic substances and pseudo-perennial habit (Meinesz & Hesse,1991; Lemée et al., 1993; Verlaque & Fritayre,1994; Smith & Walters,1999, Ceccherelli & Piazzi, 2001). Caulerpa racemosa is considered a Lessepsian migrant (migrated from the Red Sea to the Mediterranean through the Suez Canal) (Lipkin, 1972) that Caulerpa racemosa in the Mediterranean Sea 191 colonized the eastern part of the Mediterranean Sea since the 1920s (Hamel, 1926; Rayss,1941). Two varieties are recognized in the Mediterranean: an intermediate between var. turbinata (J.Agardh) Eubank and var. uvifera (C.Agardh) J. Agardh termed “ turbinata-uvifera”and var. lamourouxii (Turner) Weber-van Bosse f. requienii (Montagne) Weber-van Bosse (Verlaque et al., 2000). Since the early 1990s,a new invasive variety of C. racemosa has been spreading rapidly in the Mediterranean Sea. On the basis of a morphological study,Verlaque et al.(2000) considered this latter as a new introduced taxon close to C. racemosa var. occi- dentalis (J.Agardh) Børgesen. Molecular studies confirmed the presence of three different varieties of C. racemosa in the Mediterranean Sea and the introduction hypothesis for the invasive variety.Famà et al.(2000) found that invasive Mediterranean plants and Western Australian specimens were closely related. Durand et al.(2002) suggested that the invasive variety could be a hybrid between var. turbinata-uvifera and an unknown tropical strain. Nevertheless,Verlaque et al. (2003) disproved this hypothesis and demonstrated that the invasive event that has affected the Mediterranean since the early 1990s resulted from a recent intro- duction from south-western Australia. The invasive variety was identified as a poorly known taxon described from the Perth region as Caulerpa cylindracea Sonder (= C. racemosa var. laetevirens f. cylindracea (Sonder) Weber-van Bosse). Verlaque et al.(2003) proposed the new combination C. racemosa var. cylindracea (Sonder) Verlaque,Huisman et Boudouresque. Recorded for the first time in the Mediterranean in the early 1990s in Libya (Nizamuddin, 1991), C. racemosa var. cylindracea was almost immediately found in other parts of the basin (Alongi et al., 1993; Panayotidis & Montesanto, 1994; Piazzi et al., 1994) and showed traits of invasiveness right from its first phases of spread (Piazzi et al., 1997a). Thirteen years later,nearly the whole Medi- terranean basin is colonized and the Canary Islands have just been reached (Verlaque et al.,2004). Although highly invasive, C. racemosa var.cylindracea has not been the subject of large-scale research projects to describe its expansion. Several studies have been carried out on the ecology of this alga, but its spread was not quantified at a Mediterranean level. The aim of this paper is to assess the colonization of C. racemosa var. cylindracea thirteen years after the first record in the Mediterranean Sea. Furthermore,by means of available references,data of the web site Caulerpa on line (LEML-ENSA, 2003) and unpublished data, we try both to assess the scale of its invasion and to review the main aspects of the ecology of the alga. RESULTS Mediterranean distribution at the end of 2003 The colonization of Caulerpa racemosa var. cylindracea (hereafter: “ C. racemosa”) has been documented along the coasts of 11 nations throughout the Mediterranean basin (Verlaque et al., 2004) (Tab.1;Figs 1, 2, 3). The alga develops on all kind of substrata, both in polluted and unpolluted areas,between 0 and more than 50 m depth, down to 70 m depth in Cyprus (Argyrou, unpub- lished data) and in Southern Italy (Piazzi, unpublished data). In France there are large populations in the Gulf of Marseille and in the Bays of Toulon, Hyères and Villefranche-sur-Mer (Verlaque et al., 2000; Belsher et 192 L. Piazzi et al. Table 1. Mediterranean localities of Caulerpa racemosa var. cylindracea (Sonder) Verlaque, Huisman et Boudouresque (Situation December 2003). See reference localities in Figs 1-3. Nations and regions Localities concerned FRANCE Provence-Alpes- Bay of Marseille (01), Bay of Toulon (02), Gulf of Giens (03), Bay of Hyères (03), Côte d’Azur Porquerolles Island (03) Port-Cros Island (03), Saint-Tropez (04), Bay of Villefranche- sur-Mer (05), Nice (05) Corsica Coast of Bastia (06), East of Bonifacio (07) ITALY Liguria Bergeggi Island (08), Varazze (08), Genova (08), Bay of Monterosso (09), Palmaria Island (09), Gulf of La Spezia (09) Tuscany Meloria Shoals (10), Livorno (10), Vada Shoals (10), Capraia Island (11), Elba Island (12), Giglio Island (13) Sardinia Gulf of Asinara (14), Asinara Island (15), Bay of Malfatano (16), Gulf of Cagliari (16), Serpentera Island (17) Latium S.
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