Klein_Review Caulerpa Racemosa Invasion_2008

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Marine Pollution Bulletin 56 (2008) 205–225

Review

The Caulerpa racemosa invasion: A critical review

Judith Klein *, Marc Verlaque

Universite de la Mediterranee, Centre d’Oceanologie 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 eventcan be considered as one of the most serious in the history of species introduced into the Mediterranean Sea, C. racemosa has not trig-gered as much attention as the famous ‘‘killer alga’’ Caulerpa taxifolia. The aim of the present study was: (i) to summarize the currentstate of knowledge with regard to the distribution, the various biological and ecological characteristics of the introduced C. racemosa andits impact on the Mediterranean coastal environment; (ii) to discuss the various hypotheses regarding the explanation for its rapid andsuccessful spread; (iii) to investigate the disparity in the treatment of C. racemosa and Caulerpa taxifolia invasions; and (iv) to outlinefuture research needs.� 2007 Elsevier Ltd. All rights reserved.

Keywords: Biological invasions; Impact; Marine macrophytes; Mediterranean Sea; Review; Species introduction

1. Introduction

The Mediterranean Sea harbours around 600 intro-duced species representing 5% of the known flora andfauna (Boudouresque and Verlaque, 2005; Boudouresqueet al., 2005; Zenetos et al., 2005). It can be considered asone of the regions most severely affected by marine speciesinvasions along with the Bay of San Francisco, the Balticand the Black Sea. Around 100 macrophyte species areconsidered as having been introduced into the Mediterra-nean Sea (Ribera Siguan, 2002).

The eradication and control of invasive marine species isa difficult task that is mainly feasible in a restricted areasuch as in bays and harbours (Kuris and Culver, 1999;Bax et al., 2001; Anderson, 2005). Attempts at manage-ment of invasive marine species in the Mediterranean Searemain rare. Caulerpa taxifolia (Vahl) C. Agardh was thefirst macrophyte invasion to draw widespread public atten-tion. Consequently, the authorities in some Mediterraneancountries (Spain, France) tried to eradicate and control

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* Corresponding author. Tel.: +33 491 829 067; fax: +33 491 411 265.E-mail address: [email protected] (J. Klein).

invaded areas and prohibited the aquarium trade for thespecies. However, this attempt at management was notrepeated when a second introduced Caulerpa belongingto the Caulerpa racemosa complex, which is widely distrib-uted in warm temperate and tropical seas (see Fig. 17 inVerlaque et al., 2000), was found to have invaded the Med-iterranean Sea.

Is it unnecessary to worry about the invasion of C. race-

mosa? Is it impossible to do anything about it or do we notknow enough? To answer these questions, the present studyaims to survey all studies dealing with this recently intro-duced C. racemosa (description of the species, sightings,impact studies, population dynamic studies) and to sum-marize the current state of knowledge. In addition, gapsin current knowledge are identified and recommendationsfor future lines of research are offered.

2. Materials and methods

In order to identify all relevant studies for the presentsurvey, the databases Web of Science (http://portal.isi-knowledge.com/), Science Direct (http://www.sciencedi-rect.com) and Aquatic Sciences and Fisheries Abstracts

http://portal.isiknowledge.com/

http://portal.isiknowledge.com/

http://www.sciencedirect.com

http://www.sciencedirect.com

mailto:[email protected]

Table 1Number of articles included, excluded and total analyzed

Evaluation Number of articles

Includeda Pertinent 150Excluded Redundant 19

Total 169

a Thereof two partially excluded due to serious bias andmisidentification.

206 J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225

(http://www.csa.com/factsheets/aquclust-set-c.php) havebeen searched for articles dealing with the recently intro-duced C. racemosa, frequently referred to as ‘‘invasive C.

racemosa’’. The search was conducted using ‘‘Caulerpa’’,‘‘racemosa’’ and ‘‘invasive’’ in different combinations.For the ‘grey’ literature and literature not indexed in stan-dard databases, the library of the laboratory of the Ocean-ology Centre of Marseille was searched for MediterraneanConference proceedings, Mediterranean journals, non-gov-ernmental and governmental publications. Furthermorethe search engine Caulerpa On Line (http://www.unice.fr/LEML) was consulted in order to complete recorded pres-ence data. Special attention was paid to the identificationof the species; due to identification difficulties several‘‘false’’ sightings have been published.

The following criteria were used to select relevant publi-cations to include in the present survey. The complete pub-lication list can be requested from the authors. The criteriafor inclusion were:

– Identity: if the recently introduced C. racemosa was mis-identified as another taxon and recorded under a differ-ent name, it was nevertheless taken into account.

The criteria for exclusion were:

– Redundancy: if a study was published several times (e.g.in conference proceedings, national journals and inter-national journals) the article in the journal with highestimpact factor or with best accessibility was considered.For sightings the first date was chosen regardless ofimpact factor or accessibility. Articles not adding anynew information were excluded.

– Serious bias.– Identity: if a species was incorrectly identified as C. race-

mosa var. cylindracea or invasive C. racemosa it was nottaken into account. Misidentifications were revealedbased on the descriptions and photos.

The results were summarized using major key-words.

1 Lessepsian migrant: species introduced into the Mediterranean Seafrom the Red Sea via the Suez Canal after its opening in 1869.

3. Results

Overall, 169 articles have been examined; thereof 19articles have been excluded due to redundancy and partsof two publications because of serious bias and misidentifi-cation (Table 1). The articles dealing with the recentlyintroduced C. racemosa have mostly been published innational journals or Mediterranean conference proceedings(around 63%), which are not all indexed in the standarddatabases (e.g. Web of Science, Science Direct). Far fewerarticles have been published in international peer-reviewedjournals (around 37%). The high percentage of difficult toaccess ‘grey’ literature hinders the circulation of informa-tion and requires extensive networking for informationexchange.

3.1. Taxonomy

Caulerpa racemosa (Forsskal) J. Agardh is a Chloro-phyta of the order Bryopsidales belonging to the familyCaulerpaceae. The genus Caulerpa includes approximately85 species (Guiry and Guiry, 2007). There is much confu-sion in the literature regarding the taxonomic classificationof several Caulerpa species complexes (including the C.racemosa complex), within which different undetected spe-cies are certainly confused. The C. racemosa complex is dis-tinguished from the flat feather-like Caulerpa taxifolia byspherical, club-shaped or mushroom- to disc-shapedbranchlets. A high number of infraspecific taxa have beendescribed inside the C. racemosa complex. However, highmorphological plasticity induced by environmental param-eters renders the validity of numerous taxa questionable(Ohba and Enomoto, 1987; Prud’homme van Reineet al., 1996).

In the Mediterranean Sea, three infra-specific taxa of C.

racemosa have been identified (Verlaque et al., 2000, 2003):

– a taxon corresponding to the two varieties C. racemosa

var. turbinata (J. Agardh) Eubank and var. uvifera (C.Agardh) J. Agardh,

– C. racemosa var. lamourouxii (Turner) Weber-van Bossef. requienii (Montagne) Weber-van Bosse,

– the recently introduced C. racemosa.

The identity and origin of the recently introduced C.

racemosa in the Mediterranean Sea remained obscure forone decade. Various scenarios have been proposed toexplain the sudden spread of C. racemosa in the Mediterra-nean Sea. First it was speculated that C. racemosa was aLessepsian migrant1 from the Red Sea (Alongi et al.,1993; Giaccone and Di Martino, 1995a). However, mor-phological examination and bibliographical analysis ruledout the idea of a lessepsian migration while supportingthe hypothesis of the species having been introduced (Verl-aque et al., 2000). Molecular data confirmed the morpho-logical findings and suggested a hybrid origin for thespecies (Durand et al., 2002). Finally, Caulerpa cylindracea

Sonder (1845) endemic from south-western Australia andmore specifically from the region between Perth and Hope-

http://www.csa.com/factsheets/aquclust-set-c.php

http://www.unice.fr/LEML

http://www.unice.fr/LEML

Fig. 1. Thallus of the invasive Caulerpa racemosa from the Gulf ofMarseille (�30 m). Herbarium specimen, J. Klein.

J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225 207

toun (Harvey, 1858; Womersley, 1984) was recognized asthe taxon that was recently introduced into the Mediterra-nean Sea (Fama et al., 2000; Verlaque et al., 2003). A mor-phological and genetic study classified this taxon as C.

racemosa var. cylindracea (Sonder) Verlaque, Huismanand Boudouresque (hereafter C. racemosa) (Verlaqueet al., 2003). The identity of specimens from Croatia,Cyprus, France, Greece, Italy, Turkey and the CanaryIslands has been proved by genetic studies (Fama et al.,2000; Verlaque et al., 2000, 2003; Nuber et al., 2007). Highintra-population genetic variability has been observed inthe recently introduced C. racemosa (Fama et al., 2000,2001; Jousson et al., 2001).

3.2. Morphology

Caulerpa species have a uniaxial siphonous2 thallusmostly divided into a creeping axis (stolon) with rhizoidsand erect shoots (fronds) either nude, leaf-like or withgrape- or feather-like ramuli. There are outgrowths of thecell wall called trabeculae that function as buttress.

Caulerpa racemosa has erect fronds up to 11 cm (excep-tionally 19 cm) high bearing un-crowded vesiculate ramulithat are radially or distichously arranged (Fig. 1). Frondsare slightly inflated above the attachment to the stolonwhich is fixed to the substrate by thin short rhizoids (Verl-aque et al., 2003).

Morphometric data of C. racemosa in the Mediterra-nean Sea may vary according to region, depth and season(Table 2).

3.3. Distribution and spread

In Australia, C. racemosa var. cylindracea has beenintroduced to Adelaide in 2001 from its native rangebetween Perth and Hopetoun (Womersley, 2003; Collingset al., 2004) (Fig. 2).

Caulerpa racemosa was observed for the first time in theMediterranean Sea in Libya in 1990 (Nizamuddin, 1991).The primary introduction of C. racemosa into the Mediter-ranean Sea remains speculative. Ship traffic (ballast water,ship hull fouling) and aquaria can be considered as possiblevectors. In fact, C. racemosa has been found in aquariumstores and various Caulerpa species are sold by internetretailers and through auctions (Frisch Zaleski and Murray,2006; Stam et al., 2006; Walters et al., 2006; J. Huismanpers. comm.).

Subsequently, C. racemosa was reported from Italy(Alongi et al., 1993), then from Greece (Panayotidis andMontesanto, 1994), Albania (Di Martino and Giaccone,1995), Cyprus (Hadjichristophorou et al., 1997), France(Jousson et al., 1998), Turkey (Cirik, 1999), Malta(Stevens, 1999), Spain (Ballesteros et al., 1999), Tunisia

2 Siphonous: consisting of large multinucleate cells without cross walls.

(Belkhiria, 1999), Croatia (Zuljevic et al., 2003), andrecently from Algeria (Ould-Ahmed and Meinesz, 2007).Within the Mediterranean Sea, dispersal mechanisms ofC. racemosa as zygotes, fragments or propagules, by ship-ping (ballast water, anchor gear), fishing (dredging, trawl-ing, bottom nets and traps) and/or currents may play amajor role in the dispersion of the species (Piazzi et al.,1997a; Gambi and Terlizzi, 1998; Serio and Pizzuto,1998; Relini et al., 2001; Verlaque et al., 2003, 2004; Zulj-evic et al., 2004; Ruitton et al., 2005a).

Only 17 years after its first observation, C. racemosa hascolonized 12 countries and all major islands in the Mediter-ranean Sea as well as the Canary Islands in the AtlanticOcean (Fama et al., 2000; Verlaque et al., 2004) (Fig. 3,Appendix A).

Records of C. racemosa in the literature are often impre-cise and no estimation of the total surface area covered inthe Mediterranean Sea can be made. Only simple mapsindicating the presence of the species have been compiled,and coastlines affected were roughly estimated (Piazziet al., 2005a). It seems from the literature that the countrymost heavily affected is Italy (500 km of coastline), fol-lowed by the Balearic Islands (120 km), France (83 km)and Croatia (15 km) (Piazzi et al., 2005a). However, theseestimations have only been obtained in the four regionscited above without a standardized method, therefore theyhave to be considered with great caution. In France, theestimated surface area covered doubled within two years(early 2004: 4000–5000 ha; end of 2005: 8000 ha) (Ruittonet al., 2005a; Javel and Meinesz, 2006).

3.4. Population stability

In most of the invaded Mediterranean areas, nodecrease in colonized surfaces has been reported after 17years. However, a sudden collapse of certain C. racemosa

meadows has been observed in south-eastern France (A.Meinesz pers. comm.) and Turkey (Kas – Uc Adalar, B.Yokes pers. comm.). These disappearances may be due tounfavourable conditions, such as extreme temperatures,sediment abrasion or high hydrodynamism, but massivereproduction (see: Section 3.6) or natural decline may also

Table 2Morphometric data for the invasive Caulerpa racemosa from different localities in the Mediterranean Sea

Stolon width(mm)

Frond height(cm)

Branchlet width(mm)

Region Country Depth Date Authors

2 up to 19 2 Tajura, Tripoli Libya – February, November,December-1990

Nizamuddin (1991)

2.0–3 3.0–10 2.0–3 Zakynthos, PylosBay

Greece 25–35 m

Summer/autumn 93 Panayotidis andMontesanto (1994)

0.9–1.1 (2) 2–3 (5) 4.0–5 Leghorn Italy 4 m September-1993 toJanuary-1994

Piazzi et al. (1994)

– 3.0–5.0 0.3 Eastern Sicily Italy 5, 10 m 1994 Giaccone and DiMartino (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–

20 mFebruary-1997 Gambi and Terlizzi

(1998)0.9–2 0.39–6.9 0.7–1.5 Gulf of Salerno Italy 13–

20 mMay-1997 Gambi and Terlizzi

(1998)2.0–3 3.0–10 2.0–3 Nissoros Island/

Cape SounionGreece Shallow Summer 95 and 96 Panayotidis and

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–

23 mOctober-1997 Verlaque et al. (2000)

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–

40 m– Verlaque et al. (2000)

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 Gokova Turkey 25–

50 mNovember-1997 Verlaque et al. (2000)

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

99Cantasano (2001)

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 Martın 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 areasin France (e.g. Marseille, Hyeres, Toulon) have notextended their range for several years. It is unclear if thisis due to unfavourable conditions in the surrounding areas,a lack of dispersal or other unknown factors.

3.5. Seasonal dynamics

There are more or less pronounced seasonal variationsin C. racemosa stolon and erect axis length, growth rate,cover and biomass (Figs. 4–6). In France at 17 m depth

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 pronouncedwinter regression was observed (Ruitton et al., 2005b; Cap-iomont et al., 2005; Mezgui et al., 2007). In northern Italyat 2 m depth, a reduction of the fronds was observed inwinter with persistence of the stolons all year round (Piazziet al., 2001a). In contrast in southern Italy, C. racemosa

does not show a clear winter regression (Giaccone and DiMartino, 1995b).

The longest stolon lengths were observed from June toDecember with a maximum in September and November.Mean maximum values were lower at Villefranche-sur-Mer than at Marseille (Fig. 4).

A clear summer peak in mean frond height was recordedat Leghorn, Italy with fronds reaching 6 cm in October at0–3 m depth (Piazzi and Cinelli, 1999). In the deeper siteat Marseille in France (�17 m) maximum mean frondheight was only 2 cm during the summer months, and noclear summer peak could be distinguished, but rather analternation of several peaks and drops (Ruitton et al.,2005b). However, it should be pointed out that the studyin France took into account all erect fronds present in a20 cm · 20 cm plot, whereas in Italy five randomly chosenerect fronds were measured.

Similarly, stolon growth had a clear peak in August atLeghorn, Italy (Piazzi and Cinelli, 1999), whereas it showed

variations during the summer in Marseille, France in rela-tion with the fluctuations of temperature due to violentnorthern wind periods with two peaks, one in June andthe other in October (Ruitton et al., 2005b) (Fig. 5). Stolongrowth was almost double at Leghorn, Italy (1.26 cmday�1) compared to Marseille, France (0.75 cm day�1).

The highest number of fronds and stolon length per m2

of C. racemosa have been observed in Croatia (Zuljevicet al., 2003) (Table 3). It is worth noting that there are widedifferences between the two French localities, Marseille andVillefranche-sur-Mer (Capiomont et al., 2005; Ruittonet al., 2005b) (Table 3). This might be due to the depth dif-ferences (Marseille: 17 m; Villefranche-sur-Mer: 22 m). DeBiasi et al. (1999) observed a decrease in the C. racemosa

cover from 5–10 m to 15–20 m depth.The highest C. racemosa biomass has been observed in

Italy at Leghorn, where up to 237.5 g dw m�2 on rockand up to 447 g dw m�2 on dead Posidonia oceanica

‘‘matte’’ have been recorded in October at a depth of 2 m(Piazzi et al., 2001c). Much lower values, a maximum of74.32 g dw m�2, were recorded on the Liberata coast(180 km south of Leghorn) between 1 and 5 m depth inJuly 2006 (Lenzi et al., 2007). In France between 17 and30 m depth, values were comparable to the Liberata coastin Italy, with maxima ranging from 40.1 to 81.6 g dw

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

Fig. 4. Mean Caulerpa racemosa stolon length (mm�2) from December2001 to June 2003 at Villefranche-sur-Mer, France �22 m (�) andMarseille, France �17 m (•) (Capiomont et al., 2005; Ruitton et al.,2005b amended).

Fig. 5. Mean Caulerpa racemosa stolon growth (cm day�1) from April1996 to April 1997 at Leghorn, Italy 0–3 m (�) and from March 2002 toJune 2003 at Marseille, France �17 m (•) (Piazzi and Cinelli, 1999;Ruitton et al., 2005b amended).

Fig. 6. Mean Caulerpa racemosa biomass (g dw m�2) from December 2001to June 2003 at Villefranche-sur-Mer, France �22 m (�) and Marseille,France�17 m (•) (Capiomont et al., 2005; Ruitton et al., 2005b amended).

3 Holocarpy: transformation of the entire cytoplasm in reproductivecells, their release causes the death of the individual.

4 Anisogamy: sexual reproduction including two different types ofgametes (reproductive cells).


m�2 (Capiomont et al., 2005; Ruitton et al., 2005b; Klein,2007). High values were found from July to November(Fig. 6). A study in the Bay of Bizerte, Tunisia, recordedthe lowest values (biomass, stolon length and frond height)of all studies, however only single measurements at one sitewere taken and no mean values were available (Mezguiet al., 2007).

The regional variations observed between studies aredifficult to interpret, due to the differences in methodologyand experimental conditions (depth, exposition, substrate).There has been speculation regarding seawater temperatureand light conditions. Water motion in contrast has neverbeen taken into account. Moreover, general conclusionscannot be drawn on the basis of studies carried out overa period of a single year, because fluctuations may occurat greater temporal scales.

3.6. Reproduction and vegetative multiplication

Like many other species, C. racemosa is capable of repro-ducing sexually and vegetatively. Sexual reproduction isholocarpic3, the entire cytoplasm of the cell forms anisoga-metes4 which are liberated simultaneously, resulting in thesubsequent death of the individual. C. racemosa like Caul-

erpa taxifolia is monoecious (Goldstein and Morall, 1970;Panayotidis and Zuljevic, 2001). However, in the Mediterra-

Table 3Stolon length and number of fronds of Caulerpa racemosa per m2

Country Mean Authors

Stolon length(mm�2)

Frond numbers(m�2)

Croatia 2600 27,000 Zuljevic et al.(2003)

Marseille, France 1162 20,955 Ruitton et al.(2005b)

Villefranche, France 348 5005 Capiomont et al.(2005)


nean Sea, in contrast to Caulerpa taxifolia, where only malegametes have been observed (Zuljevic and Antolic, 2000),C. racemosa produces both sexual gametes (Panayotidisand Zuljevic, 2001). The gamete release process is precededby the appearance of small papillae and the transformationof the cytoplasm into a light green and brownish orange net-work. Approximately 14 min before sunrise gametes arereleased within a few minutes forming a green cloud (Panay-otidis and Zuljevic, 2001). After gamete release, the emptiedthallus decomposes rapidly within a few hours (A. Meineszpers. comm.). An interesting finding was made in the labora-tory: the fusion of very few gametes to form zygotes (Panay-otidis and Zuljevic, 2001). Mass spawning events wereobserved in the early morning hours in summer in Greeceand France (Panayotidis and Zuljevic, 2001; A. Meineszand T. Thibaut pers. comm.). This phenomenon mightexplain the patchy distribution of C. racemosa meadows.While some light is shed on the reproduction process, thecues triggering sexual reproduction remain unknown.

Vegetative multiplication may occur in three forms,growth pattern, fragmentation and formation of propagules.The particular growth pattern of Caulerpa species, where oneend of the ramified stolon decomposes while the apices keepgrowing, results in rapid multiplication of individuals. Frag-mentation of the thallus can be caused by disturbances(water movements, grazing, human activities). The resultingfragments are able to survive several days of transport andmay re-establish on a suitable substrate (Ceccherelli andPiazzi, 2001a). Drifting C. racemosa fragments have fre-quently been observed in the water column in Italy and seemto be a highly effective multiplication mechanism especiallyin summer (Ceccherelli et al., 2000; Ceccherelli and Piazzi,2001a). Attachment of these C. racemosa fragments to thesubstratum occurs within a few days (Carruthers et al.,1993). Propagule formation has been observed in the labora-tory on C. racemosa collected at Villefranche, France(Renoncourt and Meinesz, 2002). Propagules consisted indetached ramuli that produced chlorophyllous filaments,growing after only 5 days into a new individual.

3.7. Resistance to stress

Under environmental stress conditions, normal productionof reactive oxygen species (ROS) is increased to levels wherecells can be severely damaged. In order to cope with ROS,

cells possess an antioxidant system with enzymes, superoxidedismutase (SOD), catalase (CAT) and glutathione peroxi-dase, which transform the oxygen radical into water andmolecular oxygen. In C. racemosa higher levels of enzymeactivity (SOD, CAT) have been observed compared to Med-iterranean macrophytes, thus indicating higher capability tocope with environmental stress (Cavas and Yurdakoc,2005a). Furthermore, the enzyme activity changed seasonally,while no clear correlation with temperature or solar radiationcould be revealed (Cavas and Yurdakoc, 2005b).

3.8. Natural defences

After physical injury and grazing, wound healing inCaulerpa species is very effective and occurs within secondsby deposition of a proteinaceous plug and retraction of thecytoplasm away from the wound (Dreher et al., 1978).Moreover, C. racemosa produces secondary metabolitesthat may be involved in chemical defence against herbi-vores and in competition with other species. Antiprolifera-tive and apoptotic effects of C. racemosa crude extracts andCaulerpenyne have been shown on different cell lines(Cavas et al., 2006). In addition, C. racemosa Caulerpenyneextracts, directly applied onto the leaves of the seagrassCymodocea nodosa, triggered alterations in photosynthesis(Raniello et al., 2007). Caulerpenyne varies seasonally andbetween different parts of the thallus. Constrasting resultshave been obtained for the amount of Caulerpenyne inC. racemosa. In the first study, in contrast with the invasiveCaulerpa taxifolia and the native Mediterranean Caulerpa

prolifera (Forsskal) J.V. Lamouroux which containedequally high amounts of Caulerpenyne (6 mg g�1 of freshweight), the content in C. racemosa was half as low (3 mgg�1 of fresh weight) (Jung et al., 2002). In the second study,C. racemosa always had 35–80 times less Caulerpenyne perg of dry weight than Caulerpa taxifolia (Dumay et al.,2002a). These two studies are not comparable, because ofvery different experimental approaches and different unitsemployed. The first study used material collected fromsouthern France during summer after an acclimation inan aquarium (Jung et al., 2002), whereas the second studydirectly analyzed material collected in Leghorn, Italy underdifferent levels of interspecific competition and at differentseasons (Dumay et al., 2002a).

Despite the secondary metabolites produced by C. race-

mosa, several herbivores are encountered in the meadows.The fish species observed to graze on C. racemosa wereBoops boops (Linnaeus, 1758), Pagellus acarne (Risso,1827) and Sarpa salpa (Linnaeus, 1758) (Nizamuddin,1991; Ruitton et al., 2006; G. Cadiou pers. comm.) andthe lessepsian species Siganus luridus (Ruppell, 1829) inthe central and eastern Mediterranean Sea (Lundberget al., 1999; Azzurro et al., 2004). The two sea urchins,Paracentrotus lividus (Lamarck, 1816) and Sphaerechinus

granularis (Lamarck, 1816), consume C. racemosa (Ruittonet al., 2006). Furthermore, several herbivorous molluscshave been encountered on C. racemosa: Aplysia sp.,


Ascobulla fragilis (Jeffreys, 1856), Bittium latreillei (Payrau-deau, 1826), Elysia tomentosa (Jensen, 1997), Lobiger serra-

difalci (Calcara, 1840), Oxynoe olivacea (Rafinesque, 1814)(Gianguzza et al., 2001, 2002; Yokes and Rudman, 2004;Cavas and Yurdakoc, 2005a; Djellouli et al., 2006; J. Kleinpers. observ.).

3.9. Ecology

In its native range in south-western Australia, C. race-

mosa is a common and opportunistic species that growsfrom the intertidal down to only 6 m depth on reef flatsand in intertidal pools (Womersley, 1984; Carrutherset al., 1993). In contrast, in the Mediterranean Sea, itthrives under a large array of environmental conditions.It is found on all kinds of soft and hard substrata suchas in tide pools, on pebbles, rock, dead Posidonia oceanica

‘‘matte’’, sand, mud, detritic and coralligenous assemblagesin depths ranging from 0 to 70 m, with highest abundancebetween 0 and 30 m (Appendix A).

Mean sea surface temperatures in south-western Austra-lian waters range from 14.0 to 16.0 �C in winter and 22.5 �Cin summer (Verlaque et al., 2003). In the MediterraneanSea, C. racemosa is exposed to a wider temperature rangedown to 8 �C in Croatia (Zuljevic, 2005) and up to an aver-age of 28 �C in the Eastern basin (Cyprus, Libya, Turkey).

Experimental manipulation of light and salinity condi-tions in the laboratory showed that C. racemosa from coastalwaters of south-western Australia (intertidal/subtidal reef)had highest growth rates at salinity levels of 30–40 and lightintensities of 20–60 lE m�2 s�1 (Carruthers et al., 1993).There have been no such experiments conducted on the Med-iterranean populations. Salinity ranges from 35.27 to37.00 in south-western Australian waters and around 38.50in Mediterranean waters. C. racemosa was found in twoMediterranean coastal lagoons, Mar Piccolo and MarGrande di Taranto (Mastrototaro et al., 2004), where salin-ity ranges from 34.3 to 37.7 (Alabiso et al., 1997).

In the Mediterranean Sea, the observation of deep pop-ulations (up to 70 m of depth) attests to the high toleranceof C. racemosa to low light conditions. Caulerpa racemosa

is capable of performing photoacclimation. Acclimationtakes place both at increasing depth and during a seasonalcycle. Firstly, the number of reaction centres can be chan-ged according to irradiance levels to maintain constantphotosynthetic efficiency; and secondly, photosyntheticefficiency itself can be increased under low irradiance levelswhile keeping the number of reaction centres constant(Raniello et al., 2004, 2006).

The effect of water motion on C. racemosa is unclear.The species has been found on exposed shores as well asin sheltered areas with the exception of unstable soft-bot-tom substrates. However, on wave-exposed coasts theC. racemosa meadows may be damaged by sand scour(unpubl. data). It seems that C. racemosa is relatively resis-tant to burial by sediments (Piazzi et al., 2005b). The spe-cies is found in polluted as well as relatively pristine

areas (Ballesteros et al., 1999; Zuljevic et al., 2004; Ruittonet al., 2005a; Mifsud and Lanfranco, 2007). The increasedoccurrence of C. racemosa in the proximity of large citiesand industrial, cargo, passenger, fishing and recreationalboating harbours does not necessarily demonstrate anaffinity for polluted areas but may be an artefact due tothe secondary dispersal mechanisms via ship traffic andfishing activities (Appendix A). At least it attests to the tol-erance of C. racemosa of high levels of pollution.

3.10. Caulerpa racemosa assemblages

In south-western Australia, C. racemosa occurs inter-mixed with other algae without forming monospecificmeadows (Carruthers et al., 1993; Verlaque et al., 2003).

In contrast, in the Mediterranean Sea, C. racemosa iscapable of forming continuous dense meadows in differentphotophilic and sciaphilic benthic assemblages dominatedby different species such as Caulerpa prolifera, crustose Cor-allinaceae and other encrusting species, Cymodocea nodosa,Cystoseira spp., Halophila stipulacea, red algal turfs, rhodo-liths, Zostera noltii and sessile macrofauna such as bryozo-ans, sponges, gorgonian corals and anemones. Caulerparacemosa does not seem to be able to penetrate into densePosidonia oceanica meadows, while it has often been foundcreeping on the rhizomes at the margins or in sparse mead-ows (Panayotidis and Montesanto, 1994; Piazzi et al.,1997a,b; Serio and Pizzuto, 1998; Ceccherelli and Piazzi,1999; Piazzi and Cinelli, 1999; Ceccherelli et al., 2000,2001a; Zuljevic et al., 2004; Tsirika and Haritonidis,2005). It is interesting to note that the introduced benthicIndo-Pacific ctenophore Coeloplana willeyi was reportedfor the first time in the Mediterranean on Turkish C. race-

mosa meadows (Cavas and Yurdakoc, 2005b).At Leghorn Italy, the invasion success of C. racemosa in

benthic habitats appeared to be dependent on the vegeta-tion layers (encrusting, filamentous, erect) present and noton the diversity of the assemblages. The spread of C. race-

mosa was most facilitated in assemblages composed of turfand encrusting species, to a lesser degree in assemblageswith only encrusting species and the assemblage least inva-sible was an assemblage constituted of erect, turf andencrusting species (Ceccherelli et al., 2002). Similarly, C.

racemosa colonized algal turf faster than bare rock (Piazziet al., 2003a). Furthermore the health of seagrass meadowsinfluenced the invasion success of C. racemosa. At low shootdensity of Posidonia oceanica, relatively high C. racemosagrowth rate was observed, whereas higher shoot densityreduced C. racemosa growth (Ceccherelli et al., 2000).

Analogous to the seasonal fluctuations observed inC. racemosa, its associated flora vary during the course ofthe year. In order to characterize in detail the new assem-blage constituted of C. racemosa meadows on soft-bottomsubstrates, a new phytosociological association, Caulerpe-

tum racemosae Giaccone and Di Martino, was describedin southern Italy (Giaccone and Di Martino, 1995b; DiMartino and Giaccone, 1996).

Table 4Comparison of species characteristics between Caulerpa racemosa (R) andCaulerpa taxifolia (T)

Characteristics Comparison Authors

Biomass T > R Capiomont et al. (2005)Frond numbers T > R Capiomont et al. (2005)Frond size T > R Capiomont et al. (2005)Patch number R > T Piazzi et al. (2001e)Propagation capacity R > T Piazzi et al. (2001b)Ramification R > T Piazzi et al. (2001e)

T > R Capiomont et al. (2005)Rhizoidal pillars R > T Capiomont et al. (2005)Spread R > T Piazzi et al. (2001e)Stolon growth R > T Piazzi et al. (2001e)Stolon length R > T Capiomont et al. (2005)Stolon numbers R > T Piazzi et al. (2001b)Surface area increase R > T Piazzi et al. (2001e)


3.11. Impacts

Under certain conditions, C. racemosa may form com-pact multilayered mats up to 15 cm thick that trap sedimentthereby possibly contributing to the siltation of the assem-blages (Pandolfo and Chemello, 1995; Piazzi et al., 1997a,2007a; Argyrou et al., 1999a; Zuljevic et al., 2003). Under-neath, an anoxic layer has been observed (Piazzi et al.,1997a; A. Zuljevic pers. comm.; J. Klein pers. observ.).

It was found that, compared to other Mediterraneanrhizophytic macrophytes, other Caulerpa spp. and seagrass-es, the number of macrophyte species of the epiphyticassemblage was highest in C. racemosa meadows (Di Mar-tino and Giaccone, 1996). The studies of the impact of C.racemosa on macrophyte assemblages (rocky substrate,dead Posidonia oceanica ‘matte’, coralligenous and detriticassemblages) have been conducted in Italy (Leghorn)mostly at depths of 2–10 m and 30 m, and in France (Mar-seille) at 17 m and 30 m (Ceccherelli et al., 2001b; Piazziet al., 2001c,d, 2005b, 2007b; Piazzi and Cinelli, 2003;Balata et al., 2004; Piazzi and Ceccherelli, 2006; Cinelliet al., 2007; Klein, 2007; Klein and Verlaque, 2007). Thestudies indicate a decrease in the total number of speciesand total macrophyte cover in presence of C. racemosa.All layers were concerned, with the encrusting layer beingparticularly reduced on rocky substrate. Furthermore theeffect of C. racemosa colonization and sedimentation stresswere found to be similar, indicating that the impact on mac-rophytes could be mainly caused by accumulation and bur-ial by sediments induced by the mat (Piazzi et al., 2005b).

In presence of C. racemosa the biomass of the intro-duced Acrothamnion preissii, Asparagopsis armata andWomersleyella setacea is reduced (Piazzi and Cinelli,2003; Klein, 2007).

The two introduced species Caulerpa taxifolia and C.

racemosa co-occur in certain areas of the MediterraneanSea (Italy, France, Croatia, Spain). In some cases highercompetitive ability was hypothesized for C. racemosa (Piaz-zi and Ceccherelli, 2002; Piazzi et al., 2003b) and in othercases the contrary (Renoncourt, 2001; Ceccherelli andPiazzi, 2001b, Ceccherelli et al., 2002). In Table 4 the char-acteristics of the two species are compared.

As far as seagrasses are concerned, the impact on shootdensity and flowering has been evaluated through manualeradication of C. racemosa at Leghorn, Italy at 1 m depth(Ceccherelli and Campo, 2002). The study showed thatshoot density of Cymodocea nodosa (Ucria) Aschersondecreased in presence of C. racemosa whereas it increasedfor Zostera noltii Hornemann; in both seagrasses the fre-quency of flowering shoots increased. At the same site,the effect of C. racemosa on the vegetative cycle and pheno-lic compounds of Posidonia oceanica was assessed.Reduced leaf length and leaf area index was found in pres-ence of C. racemosa and at the same time an increase in pri-mary foliar production and in the number of leavesproduced annually was observed, leading to a higher turn-over rate (Dumay et al., 2002b). No change in the mean

phenolic compound content of Posidonia oceanica leaveswas detected and the number of tannin cells was not signif-icantly modified in the presence of C. racemosa. However,estimation was difficult at high interaction levels due tonecrosis of the leaves (Dumay et al., 2004).

Surprisingly, few reliable studies have been undertakento quantify the impact of C. racemosa and its competitionwith the Mediterranean fauna. Benthic invertebrates werestudied in Cyprus, but the impact of C. racemosa on thisassemblage could not be dissociated from other fluctuatingdisturbances in the study area (sewage outfall, fish farming)(Argyrou et al., 1999a,b). In Sardinia (Italy), no effect ofthe presence of C. racemosa on zoobenthic assemblagesof the rocky infralittoral zone could be detected (Casuet al., 2005). Two studies in Italy on the malacofauna asso-ciated with C. racemosa have produced contrasting results.In the first, low species richness (14 species) was observedand the two dominant species were Ascobulla fragilis (Jeff-reys, 1856) and Bittium latreillei (Payraudeau, 1826), twospecies that are usually found associated with Caulerpa pro-

lifera and high sedimentation stress (Pandolfo and Chem-ello, 1995). The second study found high species richness(42 species) comparable to Cymodocea nodosa meadows,which fluctuated according to the seasonal biomass cycleof C. racemosa (Buia et al., 2001). In Sicily, 52 species ofpolychaeta have been found in a C. racemosa meadowand soft-bottom species such as Laonome kroyeri (Malm-gren, 1866), Scolaricia typica (Eisig, 1914) and Jasmineira

elegans (Saint-Joseph, 1884) were dominant (Cantone,1999). In the Gulf of Taranto, an increase in densities,diversity and evenness of meiofauna was found in assem-blages invaded by C. racemosa compared to Controls.The percentage composition was slightly changed, showingincreased percentages of crustaceans and annelids (Carri-glio et al., 2003). Caulerpa racemosa has frequently beenobserved creeping on various kinds of macrobenthic ani-mals such as sponges, gorgonian corals and sea anemones(Zuljevic et al., 2004; Tsirika et al., 2006; J. Klein pers.observ.) and dead sponges completely overgrown by C.racemosa have been found in Croatia (A. Zuljevic pers.comm. and unpubl. video data).


The economic impact of C. racemosa has never beenquantified. However, there has been some speculation onthe basis of observations by fisherman in Italy who foundtheir fishing nets clogged with C. racemosa (Magri et al.,2001). Although no studies are available, the large-scalemodification of landscapes induced by C. racemosa withthe overgrowth of benthic assemblages by a more or lessdense and continuous web-like green meadow (A. Zuljevicunpubl. data) may reduce the attractiveness of the biota forunderwater tourism (spearfishing, scuba and free diving).

3.12. Management attempts

Experimental eradication studies concerning C. racemo-

sa remain an exception and limited to small surfaces (400–1000 cm2). After a period of 2 and 18 months of regularmanual eradication at a 3–4 week interval, C. racemosa

fragments were still found in eradicated plots (Ceccherelliand Piazzi, 2005; Klein, 2007).

Recovery of macrophyte assemblages after eradicationof C. racemosa has been studied in Italy and France (Piazziand Ceccherelli, 2006; Klein, 2007). After 12 and 18months, respectively, only partial recovery of the assem-blages could be observed.

4. Discussion

4.1. Caulerpa racemosa, a new Mediterranean keystone

species

Possible consequences of the C. racemosa invasion eventinclude modifications of physical and chemical conditions(water movement, sediment deposition, substrate charac-teristics) and the underwater landscape, as well as pro-found modifications of benthic assemblages. On the basisof its rapid spread and ecological impact C. racemosa isregarded as an invasive introduced species (sensu Richard-son et al., 2000; Boudouresque and Verlaque, 2002). Due toits impact mainly on habitat architecture and sediments,C. racemosa can be considered as a habitat modifier (sensuWallentinus and Nyberg, 2007). In addition, the differenti-ation of extensive meadows in the Mediterranean Sea clas-sifies C. racemosa as a new keystone species (=ecosystemengineer) (sensu Crooks, 2002).

4.2. Why is Caulerpa racemosa so successful?

In the Mediterranean Sea the following 10 introducedmacrophyte species can be considered as invasive species(on the basis of the criteria elaborated by Boudouresqueand Verlaque, 2002): Acrothamnion preissii (Sonder)E.M.Wollaston, Asparagopsis armata Harvey, Asparagopsis

taxiformis (Delile) Trevisan de Saint-Leon with their ‘‘Fal-

kenbergia’’ tetrasporophytic phases, Caulerpa racemosa

var. cylindracea (Sonder) Verlaque, Huisman and Boudour-esque, Caulerpa taxifolia (M. Vahl) C. Agardh, Codium frag-

ile subsp. tomentosoides (van Goor) P.C. Silva, Halophila

stipulacea (Forsskal) Ascherson, Lophocladia lallemandii

(Montagne) F. Schmitz, Stypopodium schimperi (Buchingerex Kutzing) Verlaque & Boudouresque and Womersleyella

setacea (Hollenberg) R.E. Norris. Some of them are locatedexclusively in the south-eastern basin (e.g. Stypopodium

schimperi) others are restricted to the western basin (e.g.Acrothamnion preissii). Only Asparagopsis armata and C.

racemosa, which are the most abundant introduced species,have achieved colonization of the entire Mediterranean Sea.

Caulerpa racemosa has experienced an impressive speedof spread during the last 17 years. Verlaque et al. (2004)analyzed the distribution (latitudinal and longitudinal) ofseveral introduced species 15 years after their first observa-tion and concluded that the rapid spread of C. racemosawas comparable only to that of Asparagopsis armata andWomersleyella setacea. Consequently, C. racemosa seemsto be particularly successful compared to most other intro-duced species (Verlaque et al., 2004).

Several general hypotheses have been proposed toexplain the success of invasive species. Escape from special-ist predators and pathogens and the possession of novelweapons have been put forward to explain the high inva-sive capacity of certain introduced species (Keane andCrawley, 2002; Torchin et al., 2003; Callaway and Ride-nour, 2004). Indeed, few herbivores have been observedon C. racemosa meadows in the Mediterranean Sea.

The presence of effective vegetative propagation mecha-nisms in addition to sexual reproduction may explain inpart the prolific development. In addition, the very rapidspread of C. racemosa may also be due to the effectivenessof the secondary dispersal mechanisms, which is illustratedby the occurrence of the species near harbours and in fish-ing areas in particular.

4.3. Differential attitude towards the two invasive Caulerpa

species

Despite the fact that Caulerpa racemosa is comparableto Caulerpa taxifolia in terms of capacity to colonize andalter native assemblages, there is a wide disparity in theeffort and means mobilised to attempt to cope with thesetwo invasive Caulerpa species.

Caulerpa taxifolia is introduced in seven countries in theMediterranean Sea (Croatia, France, Italy, Monaco, Spain,Tunisia, Turkey) and in Australia. The populations intro-duced into California (USA) have successfully been eradi-cated (Anderson, 2005). In 2005 in France, C. taxifoliacovered around 8842.3 ha corresponding to 143.8 km ofcoastline. Currently, C. racemosa is introduced in 12 Med-iterranean countries and all major islands as well as insouth-eastern Australia. In 2005, despite having been dis-covered 6 years after C. taxifolia, C. racemosa alreadyaffected a comparable surface area (8070 ha) and coastline(163.4 km) (Javel and Meinesz, 2006).

Caulerpa taxifolia has been extensively covered in themedia, seven congresses and workshops have been orga-nized, one book, 361 journal articles (including articles in


Nature, Science, Ecology) and hundreds newspaper articleshave been published, two European programmes have beenconducted, eradication campaigns have been carried outand biological control programmes launched. There arelaws regarding C. taxifolia in Australia, the USA, andSpain. The French Ministry for the Environment issued abanning order on the trade in and sale of C. taxifolia,but this order was not prolonged after its expiration. Con-sequently no legislation exists currently in France on intro-duced or invasive marine species.

Although research is being conducted on C. racemosa inseveral Mediterranean countries and an improvement inthe public awareness of the problem may be noted, thereis a wide disparity in the management of the two invasiveCaulerpa species. Caulerpa racemosa has only been dis-cussed within conferences on C. taxifolia, no Europeanprogramme has been conducted and only 150 journal arti-cles have been published only two of them on the results ofa short-term manual eradication (Ceccherelli and Piazzi,2005; Klein, 2007).

4.4. Future research needs and management

Overall, in-depth rigorous studies are lacking, particu-larly on the impact, and much of the speculation remainsto be tested. Several authors have reported the species’occurrence, often with a serious lack of detailed informa-tion (depth, substrate, illustrations, morphometric data)and the impact has often been inferred solely on the basisof point observations or mere speculation. Furthermorestudies have often been restricted in space and time (1 yearat most). Many meso- and large scale spatial and temporalfluctuations have possibly been missed.

In the current state of knowledge, no meta-analysis canbe carried out on the effects of C. racemosa on Mediterra-nean ecosystems. This is due to wide differences in experi-mental approaches, sampling depths (0–22 m), substratesand invaded macrophyte assemblages (sand, seagrasses,dead ‘‘matte’’, rocks), other disturbances (presence of otherintroduced species, nutrient input, sedimentation rate, pol-

Appendix A

Presence of Caulerpa racemosa in the Mediterranean Sea and

Country Site Authors

Albania – Di Martino anGiaccone (199

– Cinelli unpublin Piazzi et al.(2005a)

Dherm, Porto Palermo Piazzi et al. (2Vlora Bay, Himara (PortoPalermo), Saranda, Ksamil, Ftelea

Xhulaj and Ka(2007)

lution) and the insufficient number of localities studied. Infact, an important bias in the knowledge of the C. racemosa

invasion arises from the choice of the sites and assemblagesstudied. 55% of all studies have been carried out in Italyand 26% at the same locality (Leghorn).

As far as experimental design is concerned, there is anurgent need for more rigorous and comparable studies.The impact of C. racemosa needs to be evaluated in differ-ent habitats, at different depths, in different regions of theMediterranean and at different time scales (in particularlong-term studies are essential).

To limit the impact of the C. racemosa invasion in theMediterranean Sea, management strategies need to be putinto action encompassing all countries affected by the prob-lem. A manual and/or chemical control of C. racemosa

similar to the local attempts currently conducted onC. taxifolia is not a realistic solution considering the extentand the more diffuse limits of the meadows, the difficultiesto locate individuals, the high capacity of regeneration andthe constraints resulting from the underwater environment.Studies in the home range of the species (SW Australia) onthe natural predators, diseases and parasites as well ascompetition with other macrophytes could provide a basisfor understanding the biology of C. racemosa and to helpto find a possible control mechanism (e.g. biological con-trol). Finally, after Caulerpa taxifolia the disastrous conse-quences of the introduction of Caulerpa racemosa into theMediterranean Sea highlight the urgent necessity to informthe public and to prohibit all Caulerpa species from theinternational aquarium trade.

Acknowledgements

The authors would like to thank an anonymous refereefor useful comments on the manuscript and Michael Paulfor revising the English text. The study was supported bya grant from the Agence de l’Eau Rhone-Mediterranee-Corse, the Conseil General 13 and the Ville de Marseilleto J.K.

Australia

Substrate Depth Indust Fish Recr

d5)

– –

. data –

005a) + +shta Sand, mud, rocks,

dead ‘‘matte’’1–25 m

+ +

(continued on next page)

Appendix (continued)

Country Site Authors Substrate Depth Indust Fish Recr

Algeria Bou-Ismail Beach, Tamenfoust,Sidi-Fredj (Algiers)

Ould-Ahmed andMeinesz (2007)

– 0.5–3 m

+ + +

Australia Perth to Hopetoun (native) Womersley (1984) +Perth to Hopetoun (native) Verlaque et al.

(2003)Epilithic to 6 m + +

Port River Estuary, Adelaide Womersley (2003) Artifical substrate 2–3 m +Port River Estuary, Adelaide Collings et al.

(2004)– – +

Croatia Marinkovac Islet (Hvar Island) Zuljevic et al.(2003)

Sand, rock 5–15 m

+ + +

Pakleni Islands, Cesminova cove,Marculeti Bay, Mirca, Cape Pusti,Vela Garska cove, Bisevo Island(Mezuporat cove), Cavtat, CapeOsti (Dubrovnik), Dubrovnik,Goli Islet

Zuljevic et al.(2004)

Rock, sand, mud,Posidonia oceanica,Cymodocea nodosa,benthic fauna

0.5–50 m

+

Mljet Island (Sobra), Glavat Islet,Peljesak Peninsula (Prije ba Cove,Mirce, Cape Loviste)

Piazzi et al. (2005a) – –

Komiza (Vis), Ravnik (Vis),Zavala (Hvar), Korcula, Susak,Lokrum, Orsula, Prolaz Harpoti,Prapratno, Okuklje, V. jezero,Soline, Gonoturska, Blaca

Nuber et al. (2007) – –

Cyprus – Bianchi et al. (1996) – –Episkopi, Limassol, Larnaca,Moni, Morfou, Pafos

Hadjichristophorouet al. (1997)

– –

Famagusta harbour Verlaque et al.(2000); Verlaquepers. observ.

Mud, Halophila

stipulacea

1 m +

Capo Greco, Moulia rocks,Akamas peninsula

Argyrou et al.(2006)

Rock –

France Marseille Jousson et al.(1998)

– – + + +

Marseille Verlaque et al.(2000)

– 14.5–23 m

+ + +

Villefranche-sur-mer Renoncourt andMeinesz (2002)

Dead ‘‘matte’’, sand 16 m + + +

Bays of Toulon and Hyeres Belsher et al. (2003) – 20–30 m

+ + +

Villefranche-sur-mer Capiomont et al.(2005)

Sand/mud, dead‘‘matte’’

22 m + + +

Corsica (Bastia, Bonifacio,Propriano), Porquerolles Island,Port-Cros Island, St Tropez, Nice,Bay fo Giens

Ruitton et al.(2005a)

– – + + +

Greece Laganas Bay (Zakynthos Island),Pylos Bay (w Greece)

Panayotidis andMontesanto (1994)

Posidonia oceanica 25–35 m

– + +

Gulf of Saronikos Chryssovergis andPanayotidis (1998)

+ + +




Nissiros Island, Cape Sounion Panayotidis andMontesanto (1998)

Posidonia oceanica 25-35 m

Crete Siakavara pers.com. in Panayotidis(1999)

– –

Rhodos Island Fama et al. (2000) – –Kalimnos Island, Samos Island,Castellorizo Island

Verlaque et al.(2000)

– –

Astypalea, Chalkidiki, LesbosIsland, Chios Island, Corfu, Crete,Gulf of Korinth, Kalimnos,Karpathos, Kassos, KerkyraIsland, Milo, Rhodos, Santorin,Tilos

Orfanidis et al.(2005)

– –

Laganas Bay, Strofadia Island(Zakynthos Island)

Tsirika andHaritonidis (2005)

Rock, benthicflora + fauna

2–40 m

Messiniakos Gulf Tsirika et al. (2006) Rock, benthicflora + fauna

0–2 m;35–40 m

Italy Calabria

Capo Rizzuto (Ionian Sea) Fama et al. (2000) – –Capo Vaticano Cantasano (2001) Rock 1–2 mStretto di Messina, Calabria Di Martino (2001) Caulerpa taxifolia – +Vibo Marina, Palmi, Scilla Piazzi et al. (2005a) – –Campania

Gulf of Salerno Gambi and Terlizzi(1998)

Sand, Cymodocea

nodosa

13–20 m

+ +

Capo Miseno, Salerno Fama et al. (2000) – – + +Naples Buia et al. (2001) Rock 2–7 m + + +Isola di Ischia, Procida, Vivara(Gulf of Naples)

Dappiano et al.(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,Sperlonga, Ponza Island, ZannoneIsland, Ventotene Island


Liguria

Quinto (Genova) Bussotti et al.(1996)

Rock, sand 9 m + + +

Varazze, Sturla, Nervi (Genova) Modena et al.(2000)

Dead ‘‘matte’’, rock 0–10 m

+ + +

Bergeggi Islands, Bay ofMonterosso, Palmaria Island, Gulfof La Spezia

Piazzi et al. (2005a) – – + +

Foce, Quarto (Genova) Montefalcone et al.(2007a)

Rock, sand, dead‘‘matte’’

10–20 m

+ + +





Cogoleto-Arenzano Montefalcone et al.(2007b)

Dead ‘‘matte’’ –

Gallinaria Island Tunesi et al. (2007) Dead ‘‘matte’’,muddy detritic

6–25 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.

(2002)Dead ‘‘matte’’ – +

Bari Bello et al. (2004) – –Lizzano, Maruggio, Monopoli,Nardo, Otranto, Pulsano, S. Vito,Ugento


Mar Piccolo, Mar Grande Mastrototaro et al.(2004)

Caulerpa prolifera,dead ‘‘matte’’,Posidonia meadow

+ + +

Sardinia

Sarroch-Cagliari Marco Giani pers.com. in Di Martinoand Giaccone(1995)

– –

Golfo di Cagliari Cossu and Gazale(1997)

Dead ‘‘matte’’ – + +

Golfo dell’Asinara Cossu et al. (2002) Dead ‘‘matte’’ –Serpentera Island, Golfodell’Asinara, Golfo di Cagliari

Cossu et al. (2004) Dead ‘‘matte’’ –

Asinara Island, Bay of Malfatano Piazzi et al. (2005a) – –Sicily

Baia di San Panagia (Syracuse) Alongi et al. (1993) Sand, Caulerpa

prolifera

3–15 m

+ +

Isola di Lampedusa (PelagieIslands)

Alongi et al. (1993) Sand/mud,Cymodocea nodosa

1 m +

Isola di Capo Passero (south ofSyracuse)

Di Martino andStancanelli (1998)

– 1–30 m

Brucoli (Syracuse) Serio and Pizzuto(1998)

Dead ‘‘matte’’ 2–6 m

Capo Molini Fama et al. (2000) – –Acitrezza (Catania) Verlaque et al.

(2000)– –

Isola di Pantelleria Picchetti & Morsellipers. com. in DiMartino (2001)

– –

Santa Maria La Scala to CapoPassero

Di Martino (2001) – 1–30 m

Capo Passero to Pozzallo (Ragusa) Di Martino (2001) Cymodocea nodosa –Peninsola Maddalena (Syracuse) Marino et al. (2001) – – +Linosa Island (Pelagie Islands) –Sicily channel

Azzurro et al.(2004)

– –

Straits of Messina Profeta et al. (2004) Rock 0.5–1 m

Cape Feto, Marsala, Trapani, Gulfof Castellammare, TerminiImerese, Favignana Island





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’’,rock

0–20 m

+ +

Calafuria Piazzi et al. (2001b) Rock, sand 0–15 m

+ +

Capraia Island, Elba Island, GiglioIsland


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-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 andLanfranco (2007)

+0.05–50 m

Spain Balearic Islands Ballesteros et al.(1999)

– –

Gran Canaria (Canary Islands) Fama et al. (2000) – –Alicante, Santa Pola, TabarcaIsland

Pena Martın et al.(2003)

Rock, sand, dead‘‘matte’’

0–19 m

+

Sagunto, Alicante, Castello de laPlana

Aranda (2004) Dead ‘‘matte’’ 15–34 m

+

Gran Canaria, Lanzarote, Tenerife(Canary Islands)

Verlaque et al.(2004)

Rock, sand withCaulerpa prolifera

21–30 m

+

Mallorca (Dragonera, Bay ofPalma, 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,Korbous), Kerkennah harbour

Langar et al. (2002) – – +

Rafraf, Metline, Beni Khiar,Hammamet, Monastir, Madhia,Zarzis


Bizerte Mezgui et al. (2007) Dead ‘‘matte’’ 0.8–1.5 m

Turkey Gokova Evirgen (1997) Sand, rock 25–51 m

+





Tasucu, Kas, Bodrum, Kusadasi Cirik (1999) – –Kemer, Tasucu, Kas, Kusadasi,Cesme, Marmaris, Gokova,Bodrum

Tolay et al. (2001) Rock, sand, mud,dead ‘‘matte’’

0–60 m

Odunluk Iskelesi Okudan et al.(2002)

Sand, sand/mud 3–7 m

Uc Adalar Yokes andRudman (2004)

– 5–24 m

Seferihisar Cavas andYurdakoc(2005a,b)

– 2 m

Bozcaada, Izmir (Eskifoca,Karaburun), Didim


Gokova bay, Gulluk Cirik and Akcali(2006)

Rock, sand, mud 0–49 m

Indust, industrial harbour; Fish, fishing activities; Recr, recreational boating.


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