The Caulerpa Racemosa Invasion: a Critical Review

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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´diterraneé, Centre d’Oceánologie 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 triggered 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. 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

(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-governmental 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 species 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 information 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 morphological 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). High intra-population genetic variability has been observed in the recently introduced C. racemosa (Fama` et al., 2000, Fig. 1. Thallus of the invasive Caulerpa racemosa from the Gulf of 2001; Jousson et al., 2001). Marseille (À30 m). Herbarium specimen, J. Klein.

3.2. Morphology (Belkhiria, 1999), Croatia (Zˇ uljevic´ et al., 2003), and recently from Algeria (Ould-Ahmed and Meinesz, 2007). Caulerpa species have a uniaxial siphonous2 thallus Within the Mediterranean Sea, dispersal mechanisms of mostly divided into a creeping axis (stolon) with rhizoids C. racemosa as zygotes, fragments or propagules, by ship- and erect shoots (fronds) either nude, leaf-like or with ping (ballast water, anchor gear), fishing (dredging, trawl- grape- or feather-like ramuli. There are outgrowths of the ing, bottom nets and traps) and/or currents may play a cell wall called trabeculae that function as buttress. major role in the dispersion of the species (Piazzi et al., Caulerpa racemosa has erect fronds up to 11 cm (excep- 1997a; Gambi and Terlizzi, 1998; Serio and Pizzuto, tionally 19 cm) high bearing un-crowded vesiculate ramuli 1998; Relini et al., 2001; Verlaque et al., 2003, 2004; Zˇ ulj- that are radially or distichously arranged (Fig. 1). Fronds evic´ et al., 2004; Ruitton et al., 2005a). are slightly inflated above the attachment to the stolon Only 17 years after its first observation, C. racemosa has which is fixed to the substrate by thin short rhizoids (Verl- colonized 12 countries and all major islands in the Mediter- aque et al., 2003). ranean Sea as well as the Canary Islands in the Atlantic Morphometric data of C. racemosa in the Mediterra- Ocean (Fama` et al., 2000; Verlaque et al., 2004)(Fig. 3, nean Sea may vary according to region, depth and season Appendix A). (Table 2). Records of C. racemosa in the literature are often impre- cise and no estimation of the total surface area covered in 3.3. Distribution and spread the Mediterranean Sea can be made. Only simple maps indicating the presence of the species have been compiled, In Australia, C. racemosa var. cylindracea has been and coastlines affected were roughly estimated (Piazzi introduced to Adelaide in 2001 from its native range et al., 2005a). It seems from the literature that the country between Perth and Hopetoun (Womersley, 2003; Collings most heavily affected is Italy (500 km of coastline), fol- et al., 2004)(Fig. 2). lowed by the Balearic Islands (120 km), France (83 km) Caulerpa racemosa was observed for the first time in the and Croatia (15 km) (Piazzi et al., 2005a). However, these Mediterranean Sea in Libya in 1990 (Nizamuddin, 1991). estimations have only been obtained in the four regions The primary introduction of C. racemosa into the Mediter- cited above without a standardized method, therefore they ranean Sea remains speculative. Ship traffic (ballast water, have to be considered with great caution. In France, the ship hull fouling) and aquaria can be considered as possible estimated surface area covered doubled within two years vectors. In fact, C. racemosa has been found in aquarium (early 2004: 4000–5000 ha; end of 2005: 8000 ha) (Ruitton stores and various Caulerpa species are sold by internet et al., 2005a; Javel and Meinesz, 2006). retailers and through auctions (Frisch Zaleski and Murray, 2006; Stam et al., 2006; Walters et al., 2006; J. Huisman 3.4. Population stability pers. comm.). Subsequently, C. racemosa was reported from Italy In most of the invaded Mediterranean areas, no (Alongi et al., 1993), then from Greece (Panayotidis and decrease in colonized surfaces has been reported after 17 Montesanto, 1994), Albania (Di Martino and Giaccone, years. However, a sudden collapse of certain C. racemosa 1995), Cyprus (Hadjichristophorou et al., 1997), France meadows has been observed in south-eastern France (A. (Jousson et al., 1998), Turkey (Cirik, 1999), Malta Meinesz pers. comm.) and Turkey (Kas – U¨ ç Adalar, B. (Stevens, 1999), Spain (Ballesteros et al., 1999), Tunisia Yokes pers. comm.). These disappearances may be due to unfavourable conditions, such as extreme temperatures, sediment abrasion or high hydrodynamism, but massive 2 Siphonous: consisting of large multinucleate cells without cross walls. reproduction (see: Section 3.6) or natural decline may also 208 J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225

Table 2 Morphometric data for the invasive Caulerpa racemosa from diﬀerent localities in the Mediterranean Sea Stolon width Frond height Branchlet width Region Country Depth Date Authors (mm) (cm) (mm) 2 up to 19 2 Tajura, Tripoli Libya – February, November, Nizamuddin (1991) December-1990 2.0–3 3.0–10 2.0–3 Zakynthos, Pylos Greece 25– Summer/autumn 93 Panayotidis and Bay 35 m Montesanto (1994) 0.9–1.1 (2) 2–3 (5) 4.0–5 Leghorn Italy 4 m September-1993 to Piazzi et al. (1994) January-1994 – 3.0–5.0 0.3 Eastern Sicily Italy 5, 10 m 1994 Giaccone and Di Martino (1995b) 1.52 1 2.15 Genova Italy 9 m October, December-1995 Bussotti et al. (1996) 0.12 3.17 0.1 Gulf of Taranto Italy 6, 9 m October-1996 Buia et al. (1998) 3.14 3.16 0.12 Gulf of Taranto Italy 6, 9 m January-1997 Buia et al. (1998) 0.28 3.38 0.13 Gulf of Taranto Italy 6, 9 m May-1997 Buia et al. (1998) 1–2.5 0.96–8.8 1.1–3 Gulf of Salerno Italy 13– February-1997 Gambi and Terlizzi 20 m (1998) 0.9–2 0.39–6.9 0.7–1.5 Gulf of Salerno Italy 13– May-1997 Gambi and Terlizzi 20 m (1998) 2.0–3 3.0–10 2.0–3 Nissoros Island/ Greece Shallow Summer 95 and 96 Panayotidis and Cape Sounion Montesanto (1998) – 6.1 – Leghorn Italy 0–3 m October-1996 Piazzi and Cinelli (1999) – 0.7 – Leghorn Italy 0–3 m April-1996, April-1997 Piazzi and Cinelli (1999) 1.3 2 2 Varazze, Genova Italy 5–7 m August-1998 Modena et al. (2000) – – 2.0–3 Varazze, Genova Italy 5–7 m Winter 98 Modena et al. (2000) – – 2.0–7 Varazze, Genova Italy 5–7 m Summer 99 Modena et al. (2000) – 4.5–5.5 1.6 Sturla, Genova Italy 5 m September-1998 Modena et al. (2000) 0.9–1.0 <2 Nervi, Genova Italy 0.1–1 m March-1999 Modena et al. (2000) 1.5–2.0 1.2–8.7 1.3–3.0 Marseille France 14– October-1997 Verlaque et al. (2000) 23 m 1.0–2.0 5.7–16.0 3.8–7.0 Acitreza, Sicily Italy – October-1998 Verlaque et al. (2000) 1.3–1.8 2.5–5.0 2.0–4.5 Saronikos Greece – 98 Verlaque et al. (2000) 2.0–3.0 3.0–15.0 3.0–3.5 Castellorizo Island Greece 35– – Verlaque et al. (2000) 40 m 1.0–1.5 0.85–2.0 2.5–4.0 Kalimnos Island Greece – November-1997 Verlaque et al. (2000) 1.0–1.5 0.5–1.2 3.0–6.0 Samos Island Greece – September-1998 Verlaque et al. (2000) 0.5–1.8 2.2–11.0 2.5–5.0 Go¨kova Turkey 25– November-1997 Verlaque et al. (2000) 50 m 1.5–2.0 2.2–19.2 – Famagusta harbour Cyprus 8 m November-1998 Verlaque et al. (2000) 0.9–2.0 0.39–6.90 0.7–1.5 Gulf of Salerno Italy 15 m May-1998 Buia et al. (2001) 0.8–2.1 0.6–3.38 1.1–1.8 Gulf of Salerno Italy 1 m May-1998 Buia et al. (2001) 1.0–1.7 0.48–7.55 1.2–2.2 Gulf of Naples Italy 5 m May-1998 Buia et al. (2001) 0.1–2.5 0.64–4.10 0.7–1.2 Gulf of Taranto Italy 6 m May-1998 Buia et al. (2001) 0.7–0.8 7.0–8.0 1.2–1.5 Calabria Italy 1–2 m September and October Cantasano (2001) 99 1.46 1.18 – Liguria Italy – December-1995 Matricardi and Piatti (2001) 2.1 0.79 – Liguria Italy – March-1996 Matricardi and Piatti (2001) 1.52 1.05 – Liguria Italy – June-1996 Matricardi and Piatti (2001) 1.84 0.98 – Liguria Italy – August-1996 Matricardi and Piatti (2001) 1.66 1.15 – Leghorn Italy 2 m October-1998 Piazzi et al. (2001c) 1–1.5 1.5 2 Cap Bon Tunisia – – Langar et al. (2002) 1–1.5 3.5 (5) 2.0–3 Santa Pola, Alicante Spain 0–2 m – Pena Martı´n et al. (2003) 1.5–2 2–7 1–1.5 Vlora Bay Albania 5 m Summer 2005 Xhulaj and Kashta (2007) be implied. On the other hand, some large colonized areas 3.5. Seasonal dynamics in France (e.g. Marseille, Hye`res, Toulon) have not extended their range for several years. It is unclear if this There are more or less pronounced seasonal variations is due to unfavourable conditions in the surrounding areas, in C. racemosa stolon and erect axis length, growth rate, a lack of dispersal or other unknown factors. cover and biomass (Figs. 4–6). In France at 17 m depth J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225 209

Fig. 2. Map indicating the native range of Caulerpa racemosa var. cylindracea in south-western Australia (grey surface) and its introduction in Adelaide (• + arrowhead) (from Verlaque et al., 2003; amended). and in Tunisia at 1 m depth, a more or less pronounced variations during the summer in Marseille, France in rela- winter regression was observed (Ruitton et al., 2005b; Cap- tion with the fluctuations of temperature due to violent iomont et al., 2005; Mezgui et al., 2007). In northern Italy northern wind periods with two peaks, one in June and at 2 m depth, a reduction of the fronds was observed in the other in October (Ruitton et al., 2005b)(Fig. 5). Stolon winter with persistence of the stolons all year round (Piazzi growth was almost double at Leghorn, Italy (1.26 cm et al., 2001a). In contrast in southern Italy, C. racemosa dayÀ1) compared to Marseille, France (0.75 cm dayÀ1). does not show a clear winter regression (Giaccone and Di The highest number of fronds and stolon length per m2 Martino, 1995b). of C. racemosa have been observed in Croatia (Zˇ uljevic´ The longest stolon lengths were observed from June to et al., 2003)(Table 3). It is worth noting that there are wide December with a maximum in September and November. differences between the two French localities, Marseille and Mean maximum values were lower at Villefranche-sur- Villefranche-sur-Mer (Capiomont et al., 2005; Ruitton Mer than at Marseille (Fig. 4). et al., 2005b)(Table 3). This might be due to the depth dif- A clear summer peak in mean frond height was recorded ferences (Marseille: 17 m; Villefranche-sur-Mer: 22 m). De at Leghorn, Italy with fronds reaching 6 cm in October at Biasi et al. (1999) observed a decrease in the C. racemosa 0–3 m depth (Piazzi and Cinelli, 1999). In the deeper site cover from 5–10 m to 15–20 m depth. at Marseille in France (À17 m) maximum mean frond The highest C. racemosa biomass has been observed in height was only 2 cm during the summer months, and no Italy at Leghorn, where up to 237.5 g dw mÀ2 on rock clear summer peak could be distinguished, but rather an and up to 447 g dw mÀ2 on dead Posidonia oceanica alternation of several peaks and drops (Ruitton et al., ‘‘matte’’ have been recorded in October at a depth of 2 m 2005b). However, it should be pointed out that the study (Piazzi et al., 2001c). Much lower values, a maximum of in France took into account all erect fronds present in a 74.32 g dw mÀ2, were recorded on the Liberata coast 20 cm · 20 cm plot, whereas in Italy five randomly chosen (180 km south of Leghorn) between 1 and 5 m depth in erect fronds were measured. July 2006 (Lenzi et al., 2007). In France between 17 and Similarly, stolon growth had a clear peak in August at 30 m depth, values were comparable to the Liberata coast Leghorn, Italy (Piazzi and Cinelli, 1999), whereas it showed in Italy, with maxima ranging from 40.1 to 81.6 g dw 210 J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225

Fig. 3. First sighting of Caulerpa racemosa in Libya in 1991 (• + arrowhead) and subsequently observed colonies (•) in the Mediterranean Sea and the Canary Islands (from Verlaque et al., 2004; Piazzi et al., 2005a, amended).

À2 Fig. 4. Mean Caulerpa racemosa stolon length (mmÀ2) from December Fig. 6. Mean Caulerpa racemosa biomass (g dw m ) from December 2001 2001 to June 2003 at Villefranche-sur-Mer, France À22 m () and to June 2003 at Villefranche-sur-Mer, France À22 m () and Marseille, Marseille, France À17 m (•)(Capiomont et al., 2005; Ruitton et al., France À17 m (•)(Capiomont et al., 2005; Ruitton et al., 2005b amended). 2005b amended). The regional variations observed between studies are difficult to interpret, due to the differences in methodology and experimental conditions (depth, exposition, substrate). There has been speculation regarding seawater temperature and light conditions. Water motion in contrast has never been taken into account. Moreover, general conclusions cannot be drawn on the basis of studies carried out over a period of a single year, because fluctuations may occur at greater temporal scales.

3.6. Reproduction and vegetative multiplication

Fig. 5. Mean Caulerpa racemosa stolon growth (cm dayÀ1) from April Like many other species, C. racemosa is capable of repro- 1996 to April 1997 at Leghorn, Italy 0–3 m () and from March 2002 to ducing sexually and vegetatively. Sexual reproduction is 3 June 2003 at Marseille, France À17 m (•)(Piazzi and Cinelli, 1999; holocarpic , the entire cytoplasm of the cell forms anisoga- Ruitton et al., 2005b amended). metes4 which are liberated simultaneously, resulting in the subsequent death of the individual. C. racemosa like Caul- À2 m (Capiomont et al., 2005; Ruitton et al., 2005b; Klein, erpa taxifolia is monoecious (Goldstein and Morall, 1970; 2007). High values were found from July to November Panayotidis and Zˇ uljevic´, 2001). However, in the Mediterra- (Fig. 6). A study in the Bay of Bizerte, Tunisia, recorded the lowest values (biomass, stolon length and frond height) 3 Holocarpy: transformation of the entire cytoplasm in reproductive of all studies, however only single measurements at one site cells, their release causes the death of the individual. were taken and no mean values were available (Mezgui 4 Anisogamy: sexual reproduction including two diﬀerent types of et al., 2007). gametes (reproductive cells). J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225 211

Table 3 cells possess an antioxidant system with enzymes, superoxide 2 Stolon length and number of fronds of Caulerpa racemosa per m dismutase (SOD), catalase (CAT) and glutathione peroxi- Country Mean Authors dase, which transform the oxygen radical into water and Stolon length Frond numbers molecular oxygen. In C. racemosa higher levels of enzyme (mmÀ2) (mÀ2) activity (SOD, CAT) have been observed compared to Med- Croatia 2600 27,000 Zˇ uljevic´ et al. iterranean macrophytes, thus indicating higher capability to (2003) cope with environmental stress (Cavas and Yurdakoc, Marseille, France 1162 20,955 Ruitton et al. 2005a). Furthermore, the enzyme activity changed seasonally, (2005b) while no clear correlation with temperature or solar radiation Villefranche, France 348 5005 Capiomont et al. (2005) could be revealed (Cavas and Yurdakoc, 2005b).

3.8. Natural defences nean Sea, in contrast to Caulerpa taxifolia, where only male ˇ gametes have been observed (Zuljevic´ and Antolic´, 2000), After physical injury and grazing, wound healing in C. racemosa produces both sexual gametes (Panayotidis Caulerpa species is very effective and occurs within seconds ˇ and Zuljevic´, 2001). The gamete release process is preceded by deposition of a proteinaceous plug and retraction of the by the appearance of small papillae and the transformation cytoplasm away from the wound (Dreher et al., 1978). of the cytoplasm into a light green and brownish orange net- Moreover, C. racemosa produces secondary metabolites work. Approximately 14 min before sunrise gametes are that may be involved in chemical defence against herbi- released within a few minutes forming a green cloud (Panay- vores and in competition with other species. Antiprolifera- ˇ otidis and Zuljevic´, 2001). After gamete release, the emptied tive and apoptotic effects of C. racemosa crude extracts and thallus decomposes rapidly within a few hours (A. Meinesz Caulerpenyne have been shown on different cell lines pers. comm.). An interesting finding was made in the labora- (Cavas et al., 2006). In addition, C. racemosa Caulerpenyne tory: the fusion of very few gametes to form zygotes (Panay- extracts, directly applied onto the leaves of the seagrass ˇ otidis and Zuljevic´, 2001). Mass spawning events were Cymodocea nodosa, triggered alterations in photosynthesis observed in the early morning hours in summer in Greece (Raniello et al., 2007). Caulerpenyne varies seasonally and ˇ and France (Panayotidis and Zuljevic´, 2001; A. Meinesz between different parts of the thallus. Constrasting results and T. Thibaut pers. comm.). This phenomenon might have been obtained for the amount of Caulerpenyne in explain the patchy distribution of C. racemosa meadows. C. racemosa. In the first study, in contrast with the invasive While some light is shed on the reproduction process, the Caulerpa taxifolia and the native Mediterranean Caulerpa cues triggering sexual reproduction remain unknown. prolifera (Forsska˚l) J.V. Lamouroux which contained Vegetative multiplication may occur in three forms, equally high amounts of Caulerpenyne (6 mg gÀ1 of fresh growth pattern, fragmentation and formation of propagules. weight), the content in C. racemosa was half as low (3 mg The particular growth pattern of Caulerpa species, where one gÀ1 of fresh weight) (Jung et al., 2002). In the second study, end of the ramified stolon decomposes while the apices keep C. racemosa always had 35–80 times less Caulerpenyne per growing, results in rapid multiplication of individuals. Frag- g of dry weight than Caulerpa taxifolia (Dumay et al., mentation of the thallus can be caused by disturbances 2002a). These two studies are not comparable, because of (water movements, grazing, human activities). The resulting very different experimental approaches and different units fragments are able to survive several days of transport and employed. The first study used material collected from may re-establish on a suitable substrate (Ceccherelli and southern France during summer after an acclimation in Piazzi, 2001a). Drifting C. racemosa fragments have fre- an aquarium (Jung et al., 2002), whereas the second study quently been observed in the water column in Italy and seem directly analyzed material collected in Leghorn, Italy under to be a highly effective multiplication mechanism especially different levels of interspecific competition and at different in summer (Ceccherelli et al., 2000; Ceccherelli and Piazzi, seasons (Dumay et al., 2002a). 2001a). Attachment of these C. racemosa fragments to the Despite the secondary metabolites produced by C. race- substratum occurs within a few days (Carruthers et al., mosa, several herbivores are encountered in the meadows. 1993). Propagule formation has been observed in the labora- The fish species observed to graze on C. racemosa were tory on C. racemosa collected at Villefranche, France Boops boops (Linnaeus, 1758), Pagellus acarne (Risso, (Renoncourt and Meinesz, 2002). Propagules consisted in 1827) and Sarpa salpa (Linnaeus, 1758) (Nizamuddin, detached ramuli that produced chlorophyllous filaments, 1991; Ruitton et al., 2006; G. Cadiou pers. comm.) and growing after only 5 days into a new individual. the lessepsian species Siganus luridus (Ru¨ppell, 1829) in the central and eastern Mediterranean Sea (Lundberg 3.7. Resistance to stress et al., 1999; Azzurro et al., 2004). The two sea urchins, Paracentrotus lividus (Lamarck, 1816) and Sphaerechinus Under environmental stress conditions, normal production granularis (Lamarck, 1816), consume C. racemosa (Ruitton of reactive oxygen species (ROS) is increased to levels where et al., 2006). Furthermore, several herbivorous molluscs cells can be severely damaged. In order to cope with ROS, have been encountered on C. racemosa: Aplysia sp., 212 J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225

Ascobulla fragilis (Jeffreys, 1856), Bittium latreillei (Payrau- areas (Ballesteros et al., 1999; Zˇ uljevic´ et al., 2004; Ruitton deau, 1826), Elysia tomentosa (Jensen, 1997), Lobiger serra- et al., 2005a; Mifsud and Lanfranco, 2007). The increased difalci (Calcara, 1840), Oxynoe olivacea (Rafinesque, 1814) occurrence of C. racemosa in the proximity of large cities (Gianguzza et al., 2001, 2002; Yokes and Rudman, 2004; and industrial, cargo, passenger, fishing and recreational Cavas and Yurdakoc, 2005a; Djellouli et al., 2006; J. Klein boating harbours does not necessarily demonstrate an pers. observ.). affinity for polluted areas but may be an artefact due to the secondary dispersal mechanisms via ship traffic and 3.9. Ecology fishing activities (Appendix A). At least it attests to the tolerance of C. racemosa of high levels of pollution. In its native range in south-western Australia, C. racemosa is a common and opportunistic species that grows 3.10. Caulerpa racemosa assemblages from the intertidal down to only 6 m depth on reef flats and in intertidal pools (Womersley, 1984; Carruthers In south-western Australia, C. racemosa occurs inter- et al., 1993). In contrast, in the Mediterranean Sea, it mixed with other algae without forming monospecific thrives under a large array of environmental conditions. meadows (Carruthers et al., 1993; Verlaque et al., 2003). It is found on all kinds of soft and hard substrata such In contrast, in the Mediterranean Sea, C. racemosa is as in tide pools, on pebbles, rock, dead Posidonia oceanica capable of forming continuous dense meadows in different ‘‘matte’’, sand, mud, detritic and coralligenous assemblages photophilic and sciaphilic benthic assemblages dominated in depths ranging from 0 to 70 m, with highest abundance by different species such as Caulerpa prolifera, crustose Cor- between 0 and 30 m (Appendix A). allinaceae and other encrusting species, Cymodocea nodosa, Mean sea surface temperatures in south-western Austra- Cystoseira spp., Halophila stipulacea, red algal turfs, rhodo- lian waters range from 14.0 to 16.0 C in winter and 22.5 C liths, Zostera noltii and sessile macrofauna such as bryozo- in summer (Verlaque et al., 2003). In the Mediterranean ans, sponges, gorgonian corals and anemones. Caulerpa Sea, C. racemosa is exposed to a wider temperature range racemosa does not seem to be able to penetrate into dense down to 8 C in Croatia (Zˇ uljevic´, 2005) and up to an aver- Posidonia oceanica meadows, while it has often been found age of 28 C in the Eastern basin (Cyprus, Libya, Turkey). creeping on the rhizomes at the margins or in sparse mead- Experimental manipulation of light and salinity condi- ows (Panayotidis and Montesanto, 1994; Piazzi et al., tions in the laboratory showed that C. racemosa from coastal 1997a,b; Serio and Pizzuto, 1998; Ceccherelli and Piazzi, waters of south-western Australia (intertidal/subtidal reef) 1999; Piazzi and Cinelli, 1999; Ceccherelli et al., 2000, had highest growth rates at salinity levels of 30–40 and light 2001a; Zˇ uljevic´ et al., 2004; Tsirika and Haritonidis, intensities of 20–60 lEmÀ2 sÀ1 (Carruthers et al., 1993). 2005). It is interesting to note that the introduced benthic There have been no such experiments conducted on the Med- Indo-Pacific ctenophore Coeloplana willeyi was reported iterranean populations. Salinity ranges from 35.27 to for the first time in the Mediterranean on Turkish C. race- 37.00 in south-western Australian waters and around 38.50 mosa meadows (Cavas and Yurdakoc, 2005b). in Mediterranean waters. C. racemosa was found in two At Leghorn Italy, the invasion success of C. racemosa in Mediterranean coastal lagoons, Mar Piccolo and Mar benthic habitats appeared to be dependent on the vegeta- Grande di Taranto (Mastrototaro et al., 2004), where salin- tion layers (encrusting, filamentous, erect) present and not ity ranges from 34.3 to 37.7 (Alabiso et al., 1997). on the diversity of the assemblages. The spread of C. race- In the Mediterranean Sea, the observation of deep pop- mosa was most facilitated in assemblages composed of turf ulations (up to 70 m of depth) attests to the high tolerance and encrusting species, to a lesser degree in assemblages of C. racemosa to low light conditions. Caulerpa racemosa with only encrusting species and the assemblage least inva- is capable of performing photoacclimation. Acclimation sible was an assemblage constituted of erect, turf and takes place both at increasing depth and during a seasonal encrusting species (Ceccherelli et al., 2002). Similarly, C. cycle. Firstly, the number of reaction centres can be chan- racemosa colonized algal turf faster than bare rock (Piazzi ged according to irradiance levels to maintain constant et al., 2003a). Furthermore the health of seagrass meadows photosynthetic efficiency; and secondly, photosynthetic influenced the invasion success of C. racemosa. At low shoot efficiency itself can be increased under low irradiance levels density of Posidonia oceanica, relatively high C. racemosa while keeping the number of reaction centres constant growth rate was observed, whereas higher shoot density (Raniello et al., 2004, 2006). reduced C. racemosa growth (Ceccherelli et al., 2000). The effect of water motion on C. racemosa is unclear. Analogous to the seasonal fluctuations observed in The species has been found on exposed shores as well as C. racemosa, its associated flora vary during the course of in sheltered areas with the exception of unstable soft-bot- the year. In order to characterize in detail the new assem- tom substrates. However, on wave-exposed coasts the blage constituted of C. racemosa meadows on soft-bottom C. racemosa meadows may be damaged by sand scour substrates, a new phytosociological association, Caulerpe- (unpubl. data). It seems that C. racemosa is relatively resis- tum racemosae Giaccone and Di Martino, was described tant to burial by sediments (Piazzi et al., 2005b). The spe- in southern Italy (Giaccone and Di Martino, 1995b; Di cies is found in polluted as well as relatively pristine Martino and Giaccone, 1996). J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225 213

3.11. Impacts Table 4 Comparison of species characteristics between Caulerpa racemosa (R) and Under certain conditions, C. racemosa may form com- Caulerpa taxifolia (T) pact multilayered mats up to 15 cm thick that trap sediment Characteristics Comparison Authors thereby possibly contributing to the siltation of the assem- Biomass T > R Capiomont et al. (2005) blages (Pandolfo and Chemello, 1995; Piazzi et al., 1997a, Frond numbers T > R Capiomont et al. (2005) 2007a; Argyrou et al., 1999a; Zˇ uljevic´ et al., 2003). Under- Frond size T > R Capiomont et al. (2005) Patch number R > T Piazzi et al. (2001e) neath, an anoxic layer has been observed (Piazzi et al., Propagation capacity R > T Piazzi et al. (2001b) 1997a;A.Zˇ uljevic´ pers. comm.; J. Klein pers. observ.). Ramification R > T Piazzi et al. (2001e) It was found that, compared to other Mediterranean T > R Capiomont et al. (2005) rhizophytic macrophytes, other Caulerpa spp. and seagrass- Rhizoidal pillars R > T Capiomont et al. (2005) es, the number of macrophyte species of the epiphytic Spread R > T Piazzi et al. (2001e) Stolon growth R > T Piazzi et al. (2001e) assemblage was highest in C. racemosa meadows (Di Mar- Stolon length R > T Capiomont et al. (2005) tino and Giaccone, 1996). The studies of the impact of C. Stolon numbers R > T Piazzi et al. (2001b) racemosa on macrophyte assemblages (rocky substrate, Surface area increase R > T Piazzi et al. (2001e) dead Posidonia oceanica ‘matte’, coralligenous and detritic assemblages) have been conducted in Italy (Leghorn) phenolic compound content of Posidonia oceanica leaves mostly at depths of 2–10 m and 30 m, and in France (Mar- was detected and the number of tannin cells was not signif- seille) at 17 m and 30 m (Ceccherelli et al., 2001b; Piazzi icantly modified in the presence of C. racemosa. However, et al., 2001c,d, 2005b, 2007b; Piazzi and Cinelli, 2003; estimation was difficult at high interaction levels due to Balata et al., 2004; Piazzi and Ceccherelli, 2006; Cinelli necrosis of the leaves (Dumay et al., 2004). et al., 2007; Klein, 2007; Klein and Verlaque, 2007). The Surprisingly, few reliable studies have been undertaken studies indicate a decrease in the total number of species to quantify the impact of C. racemosa and its competition and total macrophyte cover in presence of C. racemosa. with the Mediterranean fauna. Benthic invertebrates were All layers were concerned, with the encrusting layer being studied in Cyprus, but the impact of C. racemosa on this particularly reduced on rocky substrate. Furthermore the assemblage could not be dissociated from other fluctuating effect of C. racemosa colonization and sedimentation stress disturbances in the study area (sewage outfall, fish farming) were found to be similar, indicating that the impact on mac- (Argyrou et al., 1999a,b). In Sardinia (Italy), no effect of rophytes could be mainly caused by accumulation and bur- the presence of C. racemosa on zoobenthic assemblages ial by sediments induced by the mat (Piazzi et al., 2005b). of the rocky infralittoral zone could be detected (Casu In presence of C. racemosa the biomass of the intro- et al., 2005). Two studies in Italy on the malacofauna asso- duced Acrothamnion preissii, Asparagopsis armata and ciated with C. racemosa have produced contrasting results. Womersleyella setacea is reduced (Piazzi and Cinelli, In the first, low species richness (14 species) was observed 2003; Klein, 2007). and the two dominant species were Ascobulla fragilis (Jeff- The two introduced species Caulerpa taxifolia and C. reys, 1856) and Bittium latreillei (Payraudeau, 1826), two racemosa co-occur in certain areas of the Mediterranean species that are usually found associated with Caulerpa pro- Sea (Italy, France, Croatia, Spain). In some cases higher lifera and high sedimentation stress (Pandolfo and Chem- competitive ability was hypothesized for C. racemosa (Piaz- ello, 1995). The second study found high species richness zi and Ceccherelli, 2002; Piazzi et al., 2003b) and in other (42 species) comparable to Cymodocea nodosa meadows, cases the contrary (Renoncourt, 2001; Ceccherelli and which fluctuated according to the seasonal biomass cycle Piazzi, 2001b, Ceccherelli et al., 2002). In Table 4 the char- of C. racemosa (Buia et al., 2001). In Sicily, 52 species of acteristics of the two species are compared. polychaeta have been found in a C. racemosa meadow As far as seagrasses are concerned, the impact on shoot and soft-bottom species such as Laonome kroyeri (Malm- density and flowering has been evaluated through manual gren, 1866), Scolaricia typica (Eisig, 1914) and Jasmineira eradication of C. racemosa at Leghorn, Italy at 1 m depth elegans (Saint-Joseph, 1884) were dominant (Cantone, (Ceccherelli and Campo, 2002). The study showed that 1999). In the Gulf of Taranto, an increase in densities, shoot density of Cymodocea nodosa (Ucria) Ascherson diversity and evenness of meiofauna was found in assem- decreased in presence of C. racemosa whereas it increased blages invaded by C. racemosa compared to Controls. for Zostera noltii Hornemann; in both seagrasses the fre- The percentage composition was slightly changed, showing quency of flowering shoots increased. At the same site, increased percentages of crustaceans and annelids (Carri- the effect of C. racemosa on the vegetative cycle and pheno- glio et al., 2003). Caulerpa racemosa has frequently been lic compounds of Posidonia oceanica was assessed. observed creeping on various kinds of macrobenthic ani- Reduced leaf length and leaf area index was found in pres- mals such as sponges, gorgonian corals and sea anemones ence of C. racemosa and at the same time an increase in pri- (Zˇ uljevic´ et al., 2004; Tsirika et al., 2006; J. Klein pers. mary foliar production and in the number of leaves observ.) and dead sponges completely overgrown by C. produced annually was observed, leading to a higher turn- racemosa have been found in Croatia (A. Zˇ uljevic´ pers. over rate (Dumay et al., 2002b). No change in the mean comm. and unpubl. video data). 214 J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225

The economic impact of C. racemosa has never been stipulacea (Forsska˚l) Ascherson, Lophocladia lallemandii quantified. However, there has been some speculation on (Montagne) F. Schmitz, Stypopodium schimperi (Buchinger the basis of observations by fisherman in Italy who found ex Ku¨tzing) Verlaque & Boudouresque and Womersleyella their fishing nets clogged with C. racemosa (Magri et al., setacea (Hollenberg) R.E. Norris. Some of them are located 2001). Although no studies are available, the large-scale exclusively in the south-eastern basin (e.g. Stypopodium modification of landscapes induced by C. racemosa with schimperi) others are restricted to the western basin (e.g. the overgrowth of benthic assemblages by a more or less Acrothamnion preissii). Only Asparagopsis armata and C. dense and continuous web-like green meadow (A. Zˇ uljevic´ racemosa, which are the most abundant introduced species, unpubl. data) may reduce the attractiveness of the biota for have achieved colonization of the entire Mediterranean Sea. underwater tourism (spearfishing, scuba and free diving). Caulerpa racemosa has experienced an impressive speed of spread during the last 17 years. Verlaque et al. (2004) 3.12. Management attempts analyzed the distribution (latitudinal and longitudinal) of several introduced species 15 years after their first observa- Experimental eradication studies concerning C. racemo- tion and concluded that the rapid spread of C. racemosa sa remain an exception and limited to small surfaces (400– was comparable only to that of Asparagopsis armata and 1000 cm2). After a period of 2 and 18 months of regular Womersleyella setacea. Consequently, C. racemosa seems manual eradication at a 3–4 week interval, C. racemosa to be particularly successful compared to most other intro- fragments were still found in eradicated plots (Ceccherelli duced species (Verlaque et al., 2004). and Piazzi, 2005; Klein, 2007). Several general hypotheses have been proposed to Recovery of macrophyte assemblages after eradication explain the success of invasive species. Escape from special- of C. racemosa has been studied in Italy and France (Piazzi ist predators and pathogens and the possession of novel and Ceccherelli, 2006; Klein, 2007). After 12 and 18 weapons have been put forward to explain the high inva- months, respectively, only partial recovery of the assem- sive capacity of certain introduced species (Keane and blages could be observed. Crawley, 2002; Torchin et al., 2003; Callaway and Ride- nour, 2004). Indeed, few herbivores have been observed 4. Discussion on C. racemosa meadows in the Mediterranean Sea. The presence of effective vegetative propagation mecha- 4.1. Caulerpa racemosa, a new Mediterranean keystone nisms in addition to sexual reproduction may explain in species part the prolific development. In addition, the very rapid spread of C. racemosa may also be due to the effectiveness Possible consequences of the C. racemosa invasion event of the secondary dispersal mechanisms, which is illustrated include modifications of physical and chemical conditions by the occurrence of the species near harbours and in fish- (water movement, sediment deposition, substrate charac- ing areas in particular. teristics) and the underwater landscape, as well as pro- found modifications of benthic assemblages. On the basis 4.3. Differential attitude towards the two invasive Caulerpa of its rapid spread and ecological impact C. racemosa is species regarded as an invasive introduced species (sensu Richard- son et al., 2000; Boudouresque and Verlaque, 2002). Due to Despite the fact that Caulerpa racemosa is comparable its impact mainly on habitat architecture and sediments, to Caulerpa taxifolia in terms of capacity to colonize and C. racemosa can be considered as a habitat modifier (sensu alter native assemblages, there is a wide disparity in the Wallentinus and Nyberg, 2007). In addition, the differenti- effort and means mobilised to attempt to cope with these ation of extensive meadows in the Mediterranean Sea clas- two invasive Caulerpa species. sifies C. racemosa as a new keystone species (=ecosystem Caulerpa taxifolia is introduced in seven countries in the engineer) (sensu Crooks, 2002). Mediterranean Sea (Croatia, France, Italy, Monaco, Spain, Tunisia, Turkey) and in Australia. The populations intro- 4.2. Why is Caulerpa racemosa so successful? duced into California (USA) have successfully been eradicated (Anderson, 2005). In 2005 in France, C. taxifolia In the Mediterranean Sea the following 10 introduced covered around 8842.3 ha corresponding to 143.8 km of macrophyte species can be considered as invasive species coastline. Currently, C. racemosa is introduced in 12 Med- (on the basis of the criteria elaborated by Boudouresque iterranean countries and all major islands as well as in and Verlaque, 2002): Acrothamnion preissii (Sonder) south-eastern Australia. In 2005, despite having been dis- E.M.Wollaston, Asparagopsis armata Harvey, Asparagopsis covered 6 years after C. taxifolia, C. racemosa already taxiformis (Delile) Trevisan de Saint-León with their ‘‘Fal- affected a comparable surface area (8070 ha) and coastline kenbergia’’ tetrasporophytic phases, Caulerpa racemosa (163.4 km) (Javel and Meinesz, 2006). var. cylindracea (Sonder) Verlaque, Huisman and Boudour- Caulerpa taxifolia has been extensively covered in the esque, Caulerpa taxifolia (M. Vahl) C. Agardh, Codium frag- media, seven congresses and workshops have been orga- ile subsp. tomentosoides (van Goor) P.C. Silva, Halophila nized, one book, 361 journal articles (including articles in J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225 215

Nature, Science, Ecology) and hundreds newspaper articles lution) and the insufficient number of localities studied. In have been published, two European programmes have been fact, an important bias in the knowledge of the C. racemosa conducted, eradication campaigns have been carried out invasion arises from the choice of the sites and assemblages and biological control programmes launched. There are studied. 55% of all studies have been carried out in Italy laws regarding C. taxifolia in Australia, the USA, and and 26% at the same locality (Leghorn). Spain. The French Ministry for the Environment issued a As far as experimental design is concerned, there is an banning order on the trade in and sale of C. taxifolia, urgent need for more rigorous and comparable studies. but this order was not prolonged after its expiration. Con- The impact of C. racemosa needs to be evaluated in differ- sequently no legislation exists currently in France on intro- ent habitats, at different depths, in different regions of the duced or invasive marine species. Mediterranean and at different time scales (in particular Although research is being conducted on C. racemosa in long-term studies are essential). several Mediterranean countries and an improvement in To limit the impact of the C. racemosa invasion in the the public awareness of the problem may be noted, there Mediterranean Sea, management strategies need to be put is a wide disparity in the management of the two invasive into action encompassing all countries affected by the prob- Caulerpa species. Caulerpa racemosa has only been dis- lem. A manual and/or chemical control of C. racemosa cussed within conferences on C. taxifolia, no European similar to the local attempts currently conducted on programme has been conducted and only 150 journal arti- C. taxifolia is not a realistic solution considering the extent cles have been published only two of them on the results of and the more diffuse limits of the meadows, the difficulties a short-term manual eradication (Ceccherelli and Piazzi, to locate individuals, the high capacity of regeneration and 2005; Klein, 2007). the constraints resulting from the underwater environment. Studies in the home range of the species (SW Australia) on 4.4. Future research needs and management the natural predators, diseases and parasites as well as competition with other macrophytes could provide a basis Overall, in-depth rigorous studies are lacking, particu- for understanding the biology of C. racemosa and to help larly on the impact, and much of the speculation remains to find a possible control mechanism (e.g. biological con- to be tested. Several authors have reported the species’ trol). Finally, after Caulerpa taxifolia the disastrous conse- occurrence, often with a serious lack of detailed informa- quences of the introduction of Caulerpa racemosa into the tion (depth, substrate, illustrations, morphometric data) Mediterranean Sea highlight the urgent necessity to inform and the impact has often been inferred solely on the basis the public and to prohibit all Caulerpa species from the of point observations or mere speculation. Furthermore international aquarium trade. studies have often been restricted in space and time (1 year at most). Many meso- and large scale spatial and temporal fluctuations have possibly been missed. Acknowledgements In the current state of knowledge, no meta-analysis can be carried out on the effects of C. racemosa on Mediterra- The authors would like to thank an anonymous referee nean ecosystems. This is due to wide differences in experi- for useful comments on the manuscript and Michael Paul mental approaches, sampling depths (0–22 m), substrates for revising the English text. The study was supported by and invaded macrophyte assemblages (sand, seagrasses, a grant from the Agence de l’Eau Rhoˆne-Me´diterraneé- dead ‘‘matte’’, rocks), other disturbances (presence of other Corse, the Conseil Geńe´ral 13 and the Ville de Marseille introduced species, nutrient input, sedimentation rate, pol- to J.K.

Appendix A Presence of Caulerpa racemosa in the Mediterranean Sea and Australia Country Site Authors Substrate Depth Indust Fish Recr Albania – Di Martino and –– Giaccone (1995) – Cinelli unpubl. data – in Piazzi et al. (2005a) Dherm, Porto Palermo Piazzi et al. (2005a) ++ Vlora Bay, Himara (Porto Xhulaj and Kashta Sand, mud, rocks, 1– ++ Palermo), Saranda, Ksamil, Ftelea (2007) dead ‘‘matte’’ 25 m (continued on next page) 216 J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225

Appendix (continued) Country Site Authors Substrate Depth Indust Fish Recr Algeria Bou-Ismail Beach, Tamenfoust, Ould-Ahmed and – 0.5– +++ Sidi-Fredj (Algiers) Meinesz (2007) 3m Australia Perth to Hopetoun (native) Womersley (1984) + Perth to Hopetoun (native) Verlaque et al. Epilithic to 6 m + + (2003) Port River Estuary, Adelaide Womersley (2003) Artiﬁcal substrate 2–3 m + Port River Estuary, Adelaide Collings et al. ––+ (2004) Croatia Marinkovac Islet (Hvar Island) Zˇ uljevic´ et al. Sand, rock 5– +++ (2003) 15 m Pakleni Islands, Cesminova cove, Zˇ uljevic´ et al. Rock, sand, mud, 0.5– + Marcˇuleti Bay, Mirca, Cape Pusti, (2004) Posidonia oceanica, 50 m Vela Garsˇka cove, Bisˇevo Island Cymodocea nodosa, (Mezuporat cove), Cavtat, Cape benthic fauna Osti (Dubrovnik), Dubrovnik, Goli Islet Mljet Island (Sobra), Glavat Islet, Piazzi et al. (2005a) –– Peljesˇak Peninsula (Prije ba Cove, Mirce, Cape Lovisˇte) Komizˇa (Vis), Ravnik (Vis), Nuber et al. (2007) –– Zavala (Hvar), Korcˇula, Susˇak, Lokrum, Orsula, Prolaz Harpoti, Prapratno, Okuklje, V. jezero, Soline, Gonoturska, Blaca Cyprus – Bianchi et al. (1996) –– Episkopi, Limassol, Larnaca, Hadjichristophorou –– Moni, Morfou, Pafos et al. (1997) Famagusta harbour Verlaque et al. Mud, Halophila 1m + (2000); Verlaque stipulacea pers. observ. Capo Greco, Moulia rocks, Argyrou et al. Rock – Akamas peninsula (2006) France Marseille Jousson et al. ––+++ (1998) Marseille Verlaque et al. – 14.5– +++ (2000) 23 m Villefranche-sur-mer Renoncourt and Dead ‘‘matte’’, sand 16 m + + + Meinesz (2002) Bays of Toulon and Hye`res Belsher et al. (2003) – 20– +++ 30 m Villefranche-sur-mer Capiomont et al. Sand/mud, dead 22 m + + + (2005) ‘‘matte’’ Corsica (Bastia, Bonifacio, Ruitton et al. ––+++ Propriano), Porquerolles Island, (2005a) Port-Cros Island, St Tropez, Nice, Bay fo Giens Greece Laganas Bay (Zakynthos Island), Panayotidis and Posidonia oceanica 25– –++ Pylos Bay (w Greece) Montesanto (1994) 35 m Gulf of Saronikos Chryssovergis and +++ Panayotidis (1998) J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225 217

Appendix (continued) Country Site Authors Substrate Depth Indust Fish Recr Nissiros Island, Cape Sounion Panayotidis and Posidonia oceanica 25- Montesanto (1998) 35 m Crete Siakavara pers. –– com. in Panayotidis (1999) Rhodos Island Fama` et al. (2000) –– Kalimnos Island, Samos Island, Verlaque et al. –– Castellorizo Island (2000) Astypalea, Chalkidiki, Lesbos Orfanidis et al. –– Island, Chios Island, Corfu, Crete, (2005) Gulf of Korinth, Kalimnos, Karpathos, Kassos, Kerkyra Island, Milo, Rhodos, Santorin, Tilos Laganas Bay, Strofadia Island Tsirika and Rock, benthic 2–40 m (Zakynthos Island) Haritonidis (2005) ﬂora + fauna Messiniakos Gulf Tsirika et al. (2006) Rock, benthic 0–2 m; ﬂora + fauna 35– 40 m Italy Calabria Capo Rizzuto (Ionian Sea) Fama` et al. (2000) –– Capo Vaticano Cantasano (2001) Rock 1–2 m Stretto di Messina, Calabria Di Martino (2001) Caulerpa taxifolia –+ Vibo Marina, Palmi, Scilla Piazzi et al. (2005a) –– Campania Gulf of Salerno Gambi and Terlizzi Sand, Cymodocea 13– ++ (1998) nodosa 20 m Capo Miseno, Salerno Fama` et al. (2000) ––++ Naples Buia et al. (2001) Rock 2–7 m + + + Isola di Ischia, Procida, Vivara Dappiano et al. ––+++ (Gulf of Naples) (2001) Isole Flegree (Gulf of Naples) Gambi et al. (2001) ––+++ Isole Flegree (Gulf of Naples) Buia et al. (2003) ––+++ Capri Island, Sorrento Peninsula Russo et al. (2003) –4–+++ 30 m Capri Island, Point Campanella Piazzi et al. (2005a) ––+++ Gulf of Naples Guala et al. (2006) ––+++ Latium S. Agostino, S. Marinella, Piazzi et al. (2005a) –– Sperlonga, Ponza Island, Zannone Island, Ventotene Island Liguria Quinto (Genova) Bussotti et al. Rock, sand 9 m + + + (1996) Varazze, Sturla, Nervi (Genova) Modena et al. Dead ‘‘matte’’, rock 0– +++ (2000) 10 m Bergeggi Islands, Bay of Piazzi et al. (2005a) ––++ Monterosso, Palmaria Island, Gulf of La Spezia Foce, Quarto (Genova) Montefalcone et al. Rock, sand, dead 10– +++ (2007a) ‘‘matte’’ 20 m (continued on next page) 218 J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225

Appendix (continued) Country Site Authors Substrate Depth Indust Fish Recr Cogoleto-Arenzano Montefalcone et al. Dead ‘‘matte’’ – (2007b) Gallinaria Island Tunesi et al. (2007) Dead ‘‘matte’’, 6– muddy detritic 25 m Puglia Gulf of Taranto Buia et al. (1998) Dead ‘‘matte’’ 6–9 m + + + Gulf of Taranto Cecere et al. (2000) Dead ‘‘matte’’ – + + + Cerano (Brindisi), Lecce Costantino et al. Dead ‘‘matte’’ – + (2002) Bari Bello et al. (2004) –– Lizzano, Maruggio, Monopoli, Piazzi et al. (2005a) –– Nardo, Otranto, Pulsano, S. Vito, Ugento Mar Piccolo, Mar Grande Mastrototaro et al. Caulerpa prolifera, +++ (2004) dead ‘‘matte’’, Posidonia meadow Sardinia Sarroch-Cagliari Marco Giani pers. –– com. in Di Martino and Giaccone (1995) Golfo di Cagliari Cossu and Gazale Dead ‘‘matte’’ – + + (1997) Golfo dell’Asinara Cossu et al. (2002) Dead ‘‘matte’’ – Serpentera Island, Golfo Cossu et al. (2004) Dead ‘‘matte’’ – dell’Asinara, Golfo di Cagliari Asinara Island, Bay of Malfatano Piazzi et al. (2005a) –– Sicily Baia di San Panagia (Syracuse) Alongi et al. (1993) Sand, Caulerpa 3– ++ prolifera 15 m Isola di Lampedusa (Pelagie Alongi et al. (1993) Sand/mud, 1m + Islands) Cymodocea nodosa Isola di Capo Passero (south of Di Martino and –1– Syracuse) Stancanelli (1998) 30 m Brucoli (Syracuse) Serio and Pizzuto Dead ‘‘matte’’ 2–6 m (1998) Capo Molini Fama` et al. (2000) –– Acitrezza (Catania) Verlaque et al. –– (2000) Isola di Pantelleria Picchetti & Morselli –– pers. com. in Di Martino (2001) Santa Maria La Scala to Capo Di Martino (2001) –1– Passero 30 m Capo Passero to Pozzallo (Ragusa) Di Martino (2001) Cymodocea nodosa – Peninsola Maddalena (Syracuse) Marino et al. (2001) ––+ Linosa Island (Pelagie Islands) – Azzurro et al. –– Sicily channel (2004) Straits of Messina Profeta et al. (2004) Rock 0.5– 1m Cape Feto, Marsala, Trapani, Gulf Piazzi et al. (2005a) –– of Castellammare, Termini Imerese, Favignana Island J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225 219

Appendix (continued) Country Site Authors Substrate Depth Indust Fish Recr Tuscany Meloria shoals (Livorno) Piazzi et al. (1994) Dead ‘‘matte’’ 4 m + + Livorno, Vada shoals Piazzi et al. (1997a) Dead ‘‘matte’’, rock 2– ++ 10 m Viareggio to Livorno Magri et al. (2001) Sand 5– ++ 20 m Livorno Piazzi et al. (2001a) Sand, dead ‘‘matte’’, 0– ++ rock 20 m Calafuria Piazzi et al. (2001b) Rock, sand 0– ++ 15 m Capraia Island, Elba Island, Giglio Piazzi et al. (2005a) –– Island Santa Liberata coast Lenzi et al. (2007) Dead ‘‘matte’’ 1–5 m Libya Tajura, Tripoli Nizamuddin (1991) Sand, rock – + Malta – Stevens (1999) Maerl, mud/sand, – rock Southern Malta Mifsud (2000) Maerl, mud/sand, rock Gozo Island (Dwejra, Xatt l- Piazzi et al. (2005a) –– Ahmar), Malta Island (St Georges’ Bay to Ghar Lapsi, Hard Bank) Marsascala Mifsud et al. (2006) Maerl, sand, rock 0– 10 m Hondoq ir-Rummien Mifsud and +0.05– Lanfranco (2007) 50 m Spain Balearic Islands Ballesteros et al. –– (1999) Gran Canaria (Canary Islands) Fama` et al. (2000) –– Alicante, Santa Pola, Tabarca Pena Martı´n et al. Rock, sand, dead 0– + Island (2003) ‘‘matte’’ 19 m Sagunto, Alicante, Castello de la Aranda (2004) Dead ‘‘matte’’ 15– + Plana 34 m Gran Canaria, Lanzarote, Tenerife Verlaque et al. Rock, sand with 21– + (Canary Islands) (2004) Caulerpa prolifera 30 m Mallorca (Dragonera, Bay of Piazzi et al. (2005a) –– Palma, Cap de Regana, Cap Blanc, Ses Fontanelles), Cabrera, Eivissa Tunisia – Belkhiria (1999) –– Cap Bon Djellouli (2000) ––+ – Djellouli et al. –– (2000) Cap Bon (Sidi Daoud, Ras Fartas, Langar et al. (2002) ––+ Korbous), Kerkennah harbour Rafraf, Metline, Beni Khiar, Piazzi et al. (2005a) –– Hammamet, Monastir, Madhia, Zarzis Bizerte Mezgui et al. (2007) Dead ‘‘matte’’ 0.8– 1.5 m Turkey Go¨kova Evirgen (1997) Sand, rock 25– + 51 m (continued on next page) 220 J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225

Appendix (continued) Country Site Authors Substrate Depth Indust Fish Recr Tasucu, Kas, Bodrum, Kusadasi Cirik (1999) –– Kemer, Tasucu, Kas, Kusadasi, Tolay et al. (2001) Rock, sand, mud, 0– Cesme, Marmaris, Go¨kova, dead ‘‘matte’’ 60 m Bodrum Odunluk Iskelesi Okudan et al. Sand, sand/mud 3–7 m (2002) Uc Adalar Yokes and –5– Rudman (2004) 24 m Seferihisar Cavas and –2m Yurdakoc (2005a,b) Bozcaada, Izmir (Eskifoça, Piazzi et al. (2005a) –– Karaburun), Didim Go¨kova bay, Gu¨llu¨k Cirik and Akçali Rock, sand, mud 0– (2006) 49 m Indust, industrial harbour; Fish, fishing activities; Recr, recreational boating.

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