Biological Invasions 3: 201–210, 2001. © 2002 Kluwer Academic Publishers. Printed in the Netherlands.

Invasion note

The introduced green alga 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,

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, , 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 colonized areas were ered area of more than 1000 m2. At this stage, inventoried off the coast of these two countries, repre- it becomes impossible to map with precision the senting a concerned area of 3184 ha. Two regions are location of each colony and to measure the cov- impacted with this invasion: the Languedoc-Roussillon ered areas. Rather, the suggested method is to region (with one area (>5000 m2) in the harbor of estimate the boundary by identifying the periph- Saint-Cyprien located 30 km from the Spanish bor- eral colonies. The surface area of this large zone der), and the Provence-Alpes-Coteˆ d’Azur region (with that incorporates all of the colonies is called the the remaining areas dispersed along about 300 km of ‘concerned area’. coastline between the Italian border and Six-Fours-les- Plages, 20 km west of Toulon). By summing the ‘affected’ (levels I and II) and Mapping efforts (by SCUBA diving) have been ‘concerned’ areas (level III), we obtain an evaluation of made yearly since 1990 and annual mapping cam- the overall status for a given region in terms of surface paigns using towed video cameras have been performed area impacted by the colonization of C. taxifolia. by IFREMER in an attempt to assess the spread The linear extent of coastline adjacent to each of the alga in those areas deemed to be vulnera- affected or concerned area constitutes an alternative ble to high amplitude spread (Belsher et al. 1994). means to measure algal spread. Finally, the num- During 1999–2000 a national Caulerpa survey pro- ber of independent area of colonization (each area gram was implemented by the French government, has one of the three levels of colonization) also rep- which included public awareness campaigns and sur- resents an important means of assessing population veys. Since the beginning of these surveys all of status. the information generated has been compiled at the Using the methods outlined above, we have University of Nice-Sophia Antipolis and has been compiled standardized yearly monitoring surveys the subject of a number of publications and reports based on SCUBA diving and towed video transects describing the dynamics of the invasion (Meinesz et al. since C. taxifolia was first observed in each 1998). of six affected countries in the Mediterranean. All information gathered since 1990 for France has Because public-awareness campaigns (distribution of been incorporated into a searchable database avail- pamphlets and posters) resulted in some inaccurate able on the Internet (http://www.caulerpa.org). Reg- reports of C. taxifolia, only those reports that have been ular control of the algae only occurs in the waters of verified by scientific divers are included in the results. the National Park of Port-Cros (under the aegis of the Finally, a brief description of the monitoring program Ministry of the Environment) where surveys and eradi- is given for each country. cation efforts such as manual removal or the application of a cloth soaked in copper salts, have been performed annually since 1994 (Cottalorda et al. 1996; Robert Results 1996; Robert and Gravez 1998). In addition, 15 isolated colonies measuring less than 5 m2 have been eradi- At the end of 2000, six countries were affected by cated successfully since the beginning of the invasion the invasion of C. taxifolia: Spain, France, Monaco, through private initiatives. Italy, Croatia and Tunisia (Table 2 and Figure 2). The characteristic situation in each country, the changes Spain in surface area, the number of independent colonized areas, the linear extent of coastline adjacent to the C. taxifolia was first observed in Spain in 1992 at colonies, the organization of the monitoring efforts and Mallorca. At this site, 250 m2 were covered by the alga the local eradication measures taken (if any) that may at an anchoring site located in the vicinity of a port. have affected the spread are described here. By the end of 2000, 62.8 ha were colonized in four 205

Table 2. Status of C. taxifolia invasion in the Mediterranean Sea.

Year Spain France and Monaco Italy Croatia Tunisia Total ACLACL A CL ACLACLA C L ha n km ha n km ha n km ha n km ha n km ha n km 1989 0 0 0 1 1 0.2 0 0 0 0 0 0 0 0 0 1 1 0.2 1991 0 0 0 30 9 3.5 0 0 0 0 0 0 0 0 0 30 9 3.5 1994 2 1 0.1 1383 13 21.7 153 9 8.9 0 0 0 0 0 0 1538 23 30.7 1997 30 2 2.6 1882 52 34 2704 17 43.6 13 8 2 0 0 0 4629 79 82.2 2000 63 4 9.4 3184 76 70.8 9415 14 103.7 41 8 5.4 350 1 2 13053 103 191.3 A – concerned areas (ha); C – number of colonies (n); L – concerned linear coastline (km)0–nodata available.

Figure 2. Overall status of C. taxifolia in the Mediterranean Sea at the end of 2000. different areas along the eastern coast of the island of vacuum and exposure to copper ions (Pou et al. 1993; Mallorca, between Portocolom and Portopetro (these Riera et al. 1994; Grau et al. 1998). two localities being separated by 15 km). These areas are regularly surveyed, and all information concerning Italy the spread is kept in a centralized database (Conselle- ria d’Agricultura i Pesca). Since the first discovery in In Italy the first discovery of C. taxifolia was made 1992, regional authorities have led operations to slow in 1992 in a port of Imperia, located 40 km east of down the rate of spread through both the use of a benthic Monaco (Relini and Torchia 1992). By the end of 206

2000 the alga had spread to five regions: Liguria of Oceanography and Fisheries of Split (for the areas (eastern, 10 m2; western, 8623 ha), Toscania (south of colonized on Hvar island). At the end of 2000 the total Livorno, 500 m2; Island of Elba, 51 ha), Sicily (Strait concerned area was 40 ha for Hvar Island and 1.3 ha of Messina, 480 ha), and Calabria (Strait of Messina, for Krk Island. 260 ha), for a total of 9415 ha concerned area. Since 1992, mapping data have been gathered and Tunisia verified by laboratories or institutions according to their field of expertise (Liguria: Morucci et al. 1996; Torchia In Tunisia the alga has recently been detected (January et al. 2001, Belsher et al. 2001; Toscania: Cinelli and 2000) in front of the port of Sousse, where a large num- Lavelli 1994, Piazzi et al. 2001; Sicilia and Calabria: ber of boats anchor before entering the port (Langar Frada` Orestano et al. 1994; Frada` Orestano and Calvo et al. 2000). Divers from the Tunisian ‘Institut National 1995; Orestano 1998; Orestano et al. 2001; Di Martino des Sciences et des Techniques’, estimated the perime- 2001). The frequency of these efforts is quite sporadic ter of the concerned area as 350 ha, in depths of and the degree of precision in the estimates made by 15–18 m. No control strategies have been implemented the divers is variable. A few compilations of these data to date. have been published (Morucci et al. 1994; Sandulli et al. 1995). In 1999 an international mapping effort was mounted using towed video cameras (Belsher et al. Discussion and conclusion 2001). This allowed a more accurate appraisal of the situation prevailing in western Liguria (IFREMER for The status of C. taxifolia in the Mediterranean at the France, ICRAM and ENEA for Italy). With the excep- end of 2000 can be described as follows. C. taxifolia tion of a few eradication attempts at Messina, Elba, is present in 6 countries with 103 independent areas Chiavari and Livorno made at the onset of the invasion of colonization, involving 131 km2 of concerned area (removal by hand of the alga by a few academics), no along 191 km of coastline. In the Mediterranean control strategy has been set up by either the state or C. taxifolia continues to spread and at the present the regions concerned. time it is still in the expansion phase (Ribera and Boudouresque 1995). Croatia It is remarkable that 90% of the concerned areas and 80% of the areas colonized are found along 500 km of In Croatia C. taxifolia was observed for the first time coastline between Toulon (France) and Genoa (Italy). in 1994 close to a mooring dock in Stari Grad (Hvar This distribution, in addition to the earlier historical Island). In 1995 it was discovered again in a port spreading in this region, further supports the hypothesis at Malinska (Krk Island) (Span et al. 1998; Zuljevic that the origin of the introduction is in the center of this et al. 1998; Zavodnik 1995; Zavodnik et al. 1998a,b, region (Monaco). 2001). Control measures were implemented annually Hill et al. (1998) simulated the alga invasion on by covering isolated colonies with black plastic sheets several levels. The simulation utilized data collected in Stari Grad Bay and by using a benthic vacuum in by divers (natural dispersion around main colonies, Malinska (Zuljevic and Antolic 2001b; Zavodnik et al. growth rates of the stolons, behavior of C. taxifolia on 1998a,b, 2001). Despite these efforts it continues to different substrates, depth or hydrodynamic situation) spread, particularly in the Hvar region. and attempted to estimate accurate rates of spreading The last record of an isolated colony of C. taxifolia given certain known physical considerations (different in Croatia was in 1996 at Barbat Channel near Dolin substrates, and direction and velocity of the main cur- Island, an area subject to frequent moorings (Zuljevic rents). Results indicate that each area has its own rate of and Antolic 2001a). C. taxifolia was eradicated from spread, which can then be enhanced by anthropogenic this area in September 1996 by manual removal. activities (mooring or fishing), diminished by control However, it was recorded here again in June 2001. efforts (eradication of peripheral colonies) and always Since the initial discovery of C. taxifolia in 1994, limited by the depth boundaries (C. taxifolia colonizes its spread has been regularly mapped by scientists only to depths of 50 m). from the Oceanographic station of Rovinj (for the Some local examples indicate that from the first colonized areas of Malinska) and from the Institute stages of colonization to 8 years later, 50–500 ha are 207 colonized (concerned). Examples include the Island of the alga is estimated to be in the period between 1991 Elba (600 m2 in 1993 and 51 ha in 2000), the Straits to 1993. Three hypotheses may explain the long-range of Messina, where the dissemination is amplified by spread of the alga during this period, and the possible strong currents (10 m2 in 1993 and 480 ha in 2000), decrease in the number of new populations appearing Island of Hvar, where most of the peripheral colonies at long distances away from established populations: were eradicated (7 ha in 1995 and 40 ha in 2000), (i) the growing awareness of pleasure-boaters and fish- and the Island of Mallorca, where regular eradica- ermen to the problem, as the result of public aware- 2 tion efforts are made (250 m in 1992 and 65 ha in ness campaigns started in 1991, brought with it a 2000). In the region of Monaco (20 km west and east decrease in long-range spread; 2 of this principality), the alga spread from 1 m in 1984 (ii) some remote colonized areas, with a more recent to 30 ha at the end of 1991 and 427 ha by the end invasion date, and therefore a small surface area, of 1992. remain undiscovered, especially if they are located With the exception of new invasions via aquariums in regions rarely visited by SCUBA divers or where and in the absence of any sexual reproduction (Meinesz public awareness is low. The discovery in 2000 of et al. 1993; Carvalho et al. 1998; Zuljevic and Antolic an invaded area involving 350 ha in Tunisia fol- 2000), the invading strain of C. taxifolia spreads either lowing a local public awareness campaign is an as the result of small pieces of the plant (cuttings) that example of this; are transported over short distances along the bottoms (iii) long-range spread can be attributed to a few boats by hydrodynamics, or through the transport of cuttings sailing between 1991 and 1993 that contained by boat anchors or fishing nets, the latter over poten- clumps of C. taxifolia in their anchor locker (as tially great distances (Meinesz 1992; Sant et al. 1996; observed on occasion by some of us) originating Relini et al. 2000). from highly invaded areas at that time (Monaco, Sixteen years after the introduction of the alga in French and Italian Riviera). Accidental release Monaco, it is remarkable to note that all the first set- from a yacht possessing an onboard aquarium with tlements of the colonized areas at Mallorca, Saint- the alga may also be possible. Cyprien, Livorno, Elba, strait of Messina, Hvar, Krk, A continued monitoring of the spread of C. taxifolia Barbat and Sousse, other than the initial introduction in the Mediterranean should allow these different region (between Toulon and Genoa), are either ports hypotheses to be assessed. or frequently used anchoring sites. The geographic Large regions neighboring the areas now invaded by locations of these areas of colonization do not reveal a C. taxifolia appear favorable to further colonization. dissemination gradient between them and between the There is thus no reason to believe that spreading will initial colonized area. 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