Available online at www.sciencedirect.com
Marine Pollution Bulletin 56 (2008) 205–225
www.elsevier.com/locate/marpolbul
Review
The Caulerpa racemosa invasion: A critical review
Judith Klein *, Marc Verlaque
Université de la Méditerranée, Centre d’Océanologie 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
The Mediterranean Sea harbours around 600 introduced species representing 5% of the known flora and
fauna (Boudouresque and Verlaque, 2005; Boudouresque
et al., 2005; Zenetos et al., 2005). It can be considered as
one of the regions most severely affected by marine species
invasions along with the Bay of San Francisco, the Baltic
and the Black Sea. Around 100 macrophyte species are
considered as having been introduced into the Mediterranean Sea (Ribera Siguan, 2002).
The eradication and control of invasive marine species is
a difficult task that is mainly feasible in a restricted area
such as in bays and harbours (Kuris and Culver, 1999;
Bax et al., 2001; Anderson, 2005). Attempts at management of invasive marine species in the Mediterranean Sea
remain rare. Caulerpa taxifolia (Vahl) C. Agardh was the
first macrophyte invasion to draw widespread public attention. Consequently, the authorities in some Mediterranean
countries (Spain, France) tried to eradicate and control
*
Corresponding author. Tel.: +33 491 829 067; fax: +33 491 411 265.
E-mail address: [email protected] (J. Klein).
0025-326X/$ - see front matter 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.marpolbul.2007.09.043
invaded areas and prohibited the aquarium trade for the
species. However, this attempt at management was not
repeated when a second introduced Caulerpa belonging
to the Caulerpa racemosa complex, which is widely distributed in warm temperate and tropical seas (see Fig. 17 in
Verlaque et al., 2000), was found to have invaded the Mediterranean Sea.
Is it unnecessary to worry about the invasion of C. racemosa? Is it impossible to do anything about it or do we not
know enough? To answer these questions, the present study
aims to survey all studies dealing with this recently introduced C. racemosa (description of the species, sightings,
impact studies, population dynamic studies) and to summarize the current state of knowledge. In addition, gaps
in current knowledge are identified and recommendations
for future lines of research are offered.
2. Materials and methods
In order to identify all relevant studies for the present
survey, the databases Web of Science (http://portal.isiknowledge.com/), Science Direct (http://www.sciencedirect.com) and Aquatic Sciences and Fisheries Abstracts
206
J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225
(http://www.csa.com/factsheets/aquclust-set-c.php) have
been searched for articles dealing with the recently introduced 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 standard databases, the library of the laboratory of the Oceanology Centre of Marseille was searched for Mediterranean
Conference proceedings, Mediterranean journals, non-governmental and governmental publications. Furthermore
the search engine Caulerpa On Line (http://www.unice.fr/
LEML) was consulted in order to complete recorded presence data. Special attention was paid to the identification
of the species; due to identification difficulties several
‘‘false’’ sightings have been published.
The following criteria were used to select relevant publications to include in the present survey. The complete publication list can be requested from the authors. The criteria
for inclusion were:
– Identity: if the recently introduced C. racemosa was misidentified as another taxon and recorded under a different 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 international journals) the article in the journal with highest
impact factor or with best accessibility was considered.
For sightings the first date was chosen regardless of
impact factor or accessibility. Articles not adding any
new information were excluded.
– Serious bias.
– Identity: if a species was incorrectly identified as C. racemosa var. cylindracea or invasive C. racemosa it was not
taken into account. Misidentifications were revealed
based on the descriptions and photos.
The results were summarized using major key-words.
3. Results
Overall, 169 articles have been examined; thereof 19
articles have been excluded due to redundancy and parts
of two publications because of serious bias and misidentification (Table 1). The articles dealing with the recently
introduced C. racemosa have mostly been published in
national journals or Mediterranean conference proceedings
(around 63%), which are not all indexed in the standard
databases (e.g. Web of Science, Science Direct). Far fewer
articles have been published in international peer-reviewed
journals (around 37%). The high percentage of difficult to
access ‘grey’ literature hinders the circulation of information and requires extensive networking for information
exchange.
Table 1
Number of articles included, excluded and total analyzed
a
Included
Excluded
Evaluation
Number of articles
Pertinent
Redundant
150
19
Total
a
Thereof two
misidentification.
169
partially
excluded
due
to
serious
bias
and
3.1. Taxonomy
Caulerpa racemosa (Forsskål) J. Agardh is a Chlorophyta of the order Bryopsidales belonging to the family
Caulerpaceae. The genus Caulerpa includes approximately
85 species (Guiry and Guiry, 2007). There is much confusion in the literature regarding the taxonomic classification
of several Caulerpa species complexes (including the C.
racemosa complex), within which different undetected species are certainly confused. The C. racemosa complex is distinguished from the flat feather-like Caulerpa taxifolia by
spherical, club-shaped or mushroom- to disc-shaped
branchlets. A high number of infraspecific taxa have been
described inside the C. racemosa complex. However, high
morphological plasticity induced by environmental parameters renders the validity of numerous taxa questionable
(Ohba and Enomoto, 1987; Prud’homme van Reine
et 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 Bosse
f. 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 for
one decade. Various scenarios have been proposed to
explain the sudden spread of C. racemosa in the Mediterranean Sea. First it was speculated that C. racemosa was a
Lessepsian migrant1 from the Red Sea (Alongi et al.,
1993; Giaccone and Di Martino, 1995a). However, morphological examination and bibliographical analysis ruled
out the idea of a lessepsian migration while supporting
the hypothesis of the species having been introduced (Verlaque et al., 2000). Molecular data confirmed the morphological findings and suggested a hybrid origin for the
species (Durand et al., 2002). Finally, Caulerpa cylindracea
Sonder (1845) endemic from south-western Australia and
more specifically from the region between Perth and Hope-
1
Lessepsian migrant: species introduced into the Mediterranean Sea
from the Red Sea via the Suez Canal after its opening in 1869.
J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225
toun (Harvey, 1858; Womersley, 1984) was recognized as
the taxon that was recently introduced into the Mediterranean Sea (Famà 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 (Famà 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 (Famà et al., 2000,
2001; Jousson et al., 2001).
3.2. Morphology
Caulerpa species have a uniaxial siphonous2 thallus
mostly divided into a creeping axis (stolon) with rhizoids
and erect shoots (fronds) either nude, leaf-like or with
grape- or feather-like ramuli. There are outgrowths of the
cell wall called trabeculae that function as buttress.
Caulerpa racemosa has erect fronds up to 11 cm (exceptionally 19 cm) high bearing un-crowded vesiculate ramuli
that are radially or distichously arranged (Fig. 1). Fronds
are slightly inflated above the attachment to the stolon
which is fixed to the substrate by thin short rhizoids (Verlaque et al., 2003).
Morphometric data of C. racemosa in the Mediterranean Sea may vary according to region, depth and season
(Table 2).
3.3. Distribution and spread
In Australia, C. racemosa var. cylindracea has been
introduced to Adelaide in 2001 from its native range
between Perth and Hopetoun (Womersley, 2003; Collings
et al., 2004) (Fig. 2).
Caulerpa racemosa was observed for the first time in the
Mediterranean Sea in Libya in 1990 (Nizamuddin, 1991).
The primary introduction of C. racemosa into the Mediterranean Sea remains speculative. Ship traffic (ballast water,
ship hull fouling) and aquaria can be considered as possible
vectors. In fact, C. racemosa has been found in aquarium
stores and various Caulerpa species are sold by internet
retailers and through auctions (Frisch Zaleski and Murray,
2006; Stam et al., 2006; Walters et al., 2006; J. Huisman
pers. comm.).
Subsequently, C. racemosa was reported from Italy
(Alongi et al., 1993), then from Greece (Panayotidis and
Montesanto, 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.
207
Fig. 1. Thallus of the invasive Caulerpa racemosa from the Gulf of
Marseille ( 30 m). Herbarium specimen, J. Klein.
(Belkhiria, 1999), Croatia (Žuljević et al., 2003), and
recently from Algeria (Ould-Ahmed and Meinesz, 2007).
Within the Mediterranean Sea, dispersal mechanisms of
C. racemosa as zygotes, fragments or propagules, by shipping (ballast water, anchor gear), fishing (dredging, trawling, bottom nets and traps) and/or currents may play a
major 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; Žuljević et al., 2004; Ruitton et al., 2005a).
Only 17 years after its first observation, C. racemosa has
colonized 12 countries and all major islands in the Mediterranean Sea as well as the Canary Islands in the Atlantic
Ocean (Famà et al., 2000; Verlaque et al., 2004) (Fig. 3,
Appendix A).
Records of C. racemosa in the literature are often imprecise and no estimation of the total surface area covered in
the Mediterranean Sea can be made. Only simple maps
indicating the presence of the species have been compiled,
and coastlines affected were roughly estimated (Piazzi
et al., 2005a). It seems from the literature that the country
most heavily affected is Italy (500 km of coastline), followed by the Balearic Islands (120 km), France (83 km)
and Croatia (15 km) (Piazzi et al., 2005a). However, these
estimations have only been obtained in the four regions
cited above without a standardized method, therefore they
have to be considered with great caution. In France, the
estimated surface area covered doubled within two years
(early 2004: 4000–5000 ha; end of 2005: 8000 ha) (Ruitton
et al., 2005a; Javel and Meinesz, 2006).
3.4. Population stability
In most of the invaded Mediterranean areas, no
decrease in colonized surfaces has been reported after 17
years. However, a sudden collapse of certain C. racemosa
meadows has been observed in south-eastern France (A.
Meinesz pers. comm.) and Turkey (Kas – Üç Adalar, B.
Yokes pers. comm.). These disappearances may be due to
unfavourable conditions, such as extreme temperatures,
sediment abrasion or high hydrodynamism, but massive
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
(mm)
Frond height
(cm)
Branchlet width
(mm)
Region
Country
Depth
Date
Authors
2
up to 19
2
Tajura, Tripoli
Libya
–
Nizamuddin (1991)
2.0–3
3.0–10
2.0–3
Greece
0.9–1.1 (2)
2–3 (5)
4.0–5
Zakynthos, Pylos
Bay
Leghorn
Italy
25–
35 m
4m
February, November,
December-1990
Summer/autumn 93
–
3.0–5.0
0.3
Eastern Sicily
Italy
5, 10 m
1.52
0.12
3.14
0.28
1–2.5
1
3.17
3.16
3.38
0.96–8.8
2.15
0.1
0.12
0.13
1.1–3
Genova
Gulf of Taranto
Gulf of Taranto
Gulf of Taranto
Gulf of Salerno
Italy
Italy
Italy
Italy
Italy
October, December-1995
October-1996
January-1997
May-1997
February-1997
0.9–2
0.39–6.9
0.7–1.5
Gulf of Salerno
Italy
2.0–3
3.0–10
2.0–3
Greece
–
–
1.3
–
–
–
0.9–1.0
1.5–2.0
6.1
0.7
2
–
–
4.5–5.5
<2
1.2–8.7
–
–
2
2.0–3
2.0–7
1.6
1.3–3.0
Nissoros Island/
Cape Sounion
Leghorn
Leghorn
Varazze, Genova
Varazze, Genova
Varazze, Genova
Sturla, Genova
Nervi, Genova
Marseille
9m
6, 9 m
6, 9 m
6, 9 m
13–
20 m
13–
20 m
Shallow
Italy
Italy
Italy
Italy
Italy
Italy
Italy
France
October-1996
April-1996, April-1997
August-1998
Winter 98
Summer 99
September-1998
March-1999
October-1997
1.0–2.0
1.3–1.8
2.0–3.0
5.7–16.0
2.5–5.0
3.0–15.0
3.8–7.0
2.0–4.5
3.0–3.5
Acitreza, Sicily
Saronikos
Castellorizo Island
Italy
Greece
Greece
October-1998
98
–
Verlaque et al. (2000)
Verlaque et al. (2000)
Verlaque et al. (2000)
1.0–1.5
1.0–1.5
0.5–1.8
0.85–2.0
0.5–1.2
2.2–11.0
2.5–4.0
3.0–6.0
2.5–5.0
Kalimnos Island
Samos Island
Gökova
Greece
Greece
Turkey
November-1997
September-1998
November-1997
Verlaque et al. (2000)
Verlaque et al. (2000)
Verlaque et al. (2000)
1.5–2.0
0.9–2.0
0.8–2.1
1.0–1.7
0.1–2.5
0.7–0.8
2.2–19.2
0.39–6.90
0.6–3.38
0.48–7.55
0.64–4.10
7.0–8.0
–
0.7–1.5
1.1–1.8
1.2–2.2
0.7–1.2
1.2–1.5
Famagusta harbour
Gulf of Salerno
Gulf of Salerno
Gulf of Naples
Gulf of Taranto
Calabria
Cyprus
Italy
Italy
Italy
Italy
Italy
0–3 m
0–3 m
5–7 m
5–7 m
5–7 m
5m
0.1–1 m
14–
23 m
–
–
35–
40 m
–
–
25–
50 m
8m
15 m
1m
5m
6m
1–2 m
Giaccone and Di
Martino (1995b)
Bussotti et al. (1996)
Buia et al. (1998)
Buia et al. (1998)
Buia et al. (1998)
Gambi and Terlizzi
(1998)
Gambi and Terlizzi
(1998)
Panayotidis and
Montesanto (1998)
Piazzi and Cinelli (1999)
Piazzi and Cinelli (1999)
Modena et al. (2000)
Modena et al. (2000)
Modena et al. (2000)
Modena et al. (2000)
Modena et al. (2000)
Verlaque et al. (2000)
Verlaque et al. (2000)
Buia et al. (2001)
Buia et al. (2001)
Buia et al. (2001)
Buia et al. (2001)
Cantasano (2001)
1.46
1.18
–
Liguria
Italy
–
November-1998
May-1998
May-1998
May-1998
May-1998
September and October
99
December-1995
2.1
0.79
–
Liguria
Italy
–
March-1996
1.52
1.05
–
Liguria
Italy
–
June-1996
1.84
0.98
–
Liguria
Italy
–
August-1996
1.66
1–1.5
1–1.5
1.5–2
1.15
1.5
3.5 (5)
2–7
–
2
2.0–3
1–1.5
Leghorn
Cap Bon
Santa Pola, Alicante
Vlora Bay
Italy
Tunisia
Spain
Albania
2m
–
0–2 m
5m
October-1998
–
–
Summer 2005
be implied. On the other hand, some large colonized areas
in France (e.g. Marseille, Hyères, Toulon) have not
extended their range for several years. It is unclear if this
is due to unfavourable conditions in the surrounding areas,
a lack of dispersal or other unknown factors.
September-1993 to
January-1994
1994
May-1997
Summer 95 and 96
Panayotidis and
Montesanto (1994)
Piazzi et al. (1994)
Matricardi and Piatti
(2001)
Matricardi and Piatti
(2001)
Matricardi and Piatti
(2001)
Matricardi and Piatti
(2001)
Piazzi et al. (2001c)
Langar et al. (2002)
Pena Martı́n et al. (2003)
Xhulaj and Kashta
(2007)
3.5. Seasonal dynamics
There are more or less pronounced seasonal variations
in C. racemosa stolon and erect axis length, growth rate,
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
winter regression was observed (Ruitton et al., 2005b; Capiomont et al., 2005; Mezgui et al., 2007). In northern Italy
at 2 m depth, a reduction of the fronds was observed in
winter with persistence of the stolons all year round (Piazzi
et al., 2001a). In contrast in southern Italy, C. racemosa
does not show a clear winter regression (Giaccone and Di
Martino, 1995b).
The longest stolon lengths were observed from June to
December with a maximum in September and November.
Mean maximum values were lower at Villefranche-surMer than at Marseille (Fig. 4).
A clear summer peak in mean frond height was recorded
at Leghorn, Italy with fronds reaching 6 cm in October at
0–3 m depth (Piazzi and Cinelli, 1999). In the deeper site
at Marseille in France ( 17 m) maximum mean frond
height was only 2 cm during the summer months, and no
clear summer peak could be distinguished, but rather an
alternation of several peaks and drops (Ruitton et al.,
2005b). However, it should be pointed out that the study
in France took into account all erect fronds present in a
20 cm · 20 cm plot, whereas in Italy five randomly chosen
erect fronds were measured.
Similarly, stolon growth had a clear peak in August at
Leghorn, Italy (Piazzi and Cinelli, 1999), whereas it showed
variations during the summer in Marseille, France in relation with the fluctuations of temperature due to violent
northern wind periods with two peaks, one in June and
the other in October (Ruitton et al., 2005b) (Fig. 5). Stolon
growth was almost double at Leghorn, Italy (1.26 cm
day 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 (Žuljević
et al., 2003) (Table 3). It is worth noting that there are wide
differences between the two French localities, Marseille and
Villefranche-sur-Mer (Capiomont et al., 2005; Ruitton
et al., 2005b) (Table 3). This might be due to the depth differences (Marseille: 17 m; Villefranche-sur-Mer: 22 m). De
Biasi 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 rock
and 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 of
74.32 g dw m 2, were recorded on the Liberata coast
(180 km south of Leghorn) between 1 and 5 m depth in
July 2006 (Lenzi et al., 2007). In France between 17 and
30 m depth, values were comparable to the Liberata coast
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).
Fig. 4. Mean Caulerpa racemosa stolon length (mm 2) from December
2001 to June 2003 at Villefranche-sur-Mer, France 22 m () and
Marseille, France 17 m (•) (Capiomont et al., 2005; Ruitton et al.,
2005b amended).
Fig. 6. Mean Caulerpa racemosa biomass (g dw m 2) from December 2001
to June 2003 at Villefranche-sur-Mer, France 22 m () and Marseille,
France 17 m (•) (Capiomont et al., 2005; Ruitton et al., 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 day 1) from April
1996 to April 1997 at Leghorn, Italy 0–3 m () and from March 2002 to
June 2003 at Marseille, France 17 m (•) (Piazzi and Cinelli, 1999;
Ruitton et al., 2005b amended).
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, recorded
the lowest values (biomass, stolon length and frond height)
of all studies, however only single measurements at one site
were taken and no mean values were available (Mezgui
et al., 2007).
Like many other species, C. racemosa is capable of reproducing sexually and vegetatively. Sexual reproduction is
holocarpic3, the entire cytoplasm of the cell forms anisogametes4 which are liberated simultaneously, resulting in the
subsequent death of the individual. C. racemosa like Caulerpa taxifolia is monoecious (Goldstein and Morall, 1970;
Panayotidis and Žuljević, 2001). However, in the Mediterra3
Holocarpy: transformation of the entire cytoplasm in reproductive
cells, their release causes the death of the individual.
4
Anisogamy: sexual reproduction including two different types of
gametes (reproductive cells).
J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225
Table 3
Stolon 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
Marseille, France
1162
20,955
Villefranche, France
348
5005
Žuljević et al.
(2003)
Ruitton et al.
(2005b)
Capiomont et al.
(2005)
nean Sea, in contrast to Caulerpa taxifolia, where only male
gametes have been observed (Žuljević and Antolić, 2000),
C. racemosa produces both sexual gametes (Panayotidis
and Žuljević, 2001). The gamete release process is preceded
by the appearance of small papillae and the transformation
of the cytoplasm into a light green and brownish orange network. Approximately 14 min before sunrise gametes are
released within a few minutes forming a green cloud (Panayotidis and Žuljević, 2001). After gamete release, the emptied
thallus decomposes rapidly within a few hours (A. Meinesz
pers. comm.). An interesting finding was made in the laboratory: the fusion of very few gametes to form zygotes (Panayotidis and Žuljević, 2001). Mass spawning events were
observed in the early morning hours in summer in Greece
and France (Panayotidis and Žuljević, 2001; A. Meinesz
and T. Thibaut pers. comm.). This phenomenon might
explain the patchy distribution of C. racemosa meadows.
While some light is shed on the reproduction process, the
cues 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 one
end of the ramified stolon decomposes while the apices keep
growing, results in rapid multiplication of individuals. Fragmentation of the thallus can be caused by disturbances
(water movements, grazing, human activities). The resulting
fragments are able to survive several days of transport and
may re-establish on a suitable substrate (Ceccherelli and
Piazzi, 2001a). Drifting C. racemosa fragments have frequently been observed in the water column in Italy and seem
to be a highly effective multiplication mechanism especially
in summer (Ceccherelli et al., 2000; Ceccherelli and Piazzi,
2001a). Attachment of these C. racemosa fragments to the
substratum occurs within a few days (Carruthers et al.,
1993). Propagule formation has been observed in the laboratory on C. racemosa collected at Villefranche, France
(Renoncourt and Meinesz, 2002). Propagules consisted in
detached ramuli that produced chlorophyllous filaments,
growing after only 5 days into a new individual.
3.7. Resistance to stress
Under environmental stress conditions, normal production
of reactive oxygen species (ROS) is increased to levels where
cells can be severely damaged. In order to cope with ROS,
211
cells possess an antioxidant system with enzymes, superoxide
dismutase (SOD), catalase (CAT) and glutathione peroxidase, which transform the oxygen radical into water and
molecular oxygen. In C. racemosa higher levels of enzyme
activity (SOD, CAT) have been observed compared to Mediterranean macrophytes, thus indicating higher capability to
cope with environmental stress (Cavas and Yurdakoc,
2005a). Furthermore, the enzyme activity changed seasonally,
while no clear correlation with temperature or solar radiation
could be revealed (Cavas and Yurdakoc, 2005b).
3.8. Natural defences
After physical injury and grazing, wound healing in
Caulerpa species is very effective and occurs within seconds
by deposition of a proteinaceous plug and retraction of the
cytoplasm away from the wound (Dreher et al., 1978).
Moreover, C. racemosa produces secondary metabolites
that may be involved in chemical defence against herbivores and in competition with other species. Antiproliferative and apoptotic effects of C. racemosa crude extracts and
Caulerpenyne have been shown on different cell lines
(Cavas et al., 2006). In addition, C. racemosa Caulerpenyne
extracts, directly applied onto the leaves of the seagrass
Cymodocea nodosa, triggered alterations in photosynthesis
(Raniello et al., 2007). Caulerpenyne varies seasonally and
between different parts of the thallus. Constrasting results
have been obtained for the amount of Caulerpenyne in
C. racemosa. In the first study, in contrast with the invasive
Caulerpa taxifolia and the native Mediterranean Caulerpa
prolifera (Forsskål) J.V. Lamouroux which contained
equally high amounts of Caulerpenyne (6 mg g 1 of fresh
weight), the content in C. racemosa was half as low (3 mg
g 1 of fresh weight) (Jung et al., 2002). In the second study,
C. racemosa always had 35–80 times less Caulerpenyne per
g of dry weight than Caulerpa taxifolia (Dumay et al.,
2002a). These two studies are not comparable, because of
very different experimental approaches and different units
employed. The first study used material collected from
southern France during summer after an acclimation in
an aquarium (Jung et al., 2002), whereas the second study
directly analyzed material collected in Leghorn, Italy under
different levels of interspecific competition and at different
seasons (Dumay et al., 2002a).
Despite the secondary metabolites produced by C. racemosa, several herbivores are encountered in the meadows.
The fish species observed to graze on C. racemosa were
Boops boops (Linnaeus, 1758), Pagellus acarne (Risso,
1827) and Sarpa salpa (Linnaeus, 1758) (Nizamuddin,
1991; Ruitton et al., 2006; G. Cadiou pers. comm.) and
the lessepsian species Siganus luridus (Rüppell, 1829) in
the central and eastern Mediterranean Sea (Lundberg
et al., 1999; Azzurro et al., 2004). The two sea urchins,
Paracentrotus lividus (Lamarck, 1816) and Sphaerechinus
granularis (Lamarck, 1816), consume C. racemosa (Ruitton
et al., 2006). Furthermore, several herbivorous molluscs
have been encountered on C. racemosa: Aplysia sp.,
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J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225
Ascobulla fragilis (Jeffreys, 1856), Bittium latreillei (Payraudeau, 1826), Elysia tomentosa (Jensen, 1997), Lobiger serradifalci (Calcara, 1840), Oxynoe olivacea (Rafinesque, 1814)
(Gianguzza et al., 2001, 2002; Yokes and Rudman, 2004;
Cavas and Yurdakoc, 2005a; Djellouli et al., 2006; J. Klein
pers. observ.).
3.9. Ecology
In its native range in south-western Australia, C. racemosa is a common and opportunistic species that grows
from the intertidal down to only 6 m depth on reef flats
and in intertidal pools (Womersley, 1984; Carruthers
et al., 1993). In contrast, in the Mediterranean Sea, it
thrives under a large array of environmental conditions.
It is found on all kinds of soft and hard substrata such
as in tide pools, on pebbles, rock, dead Posidonia oceanica
‘‘matte’’, sand, mud, detritic and coralligenous assemblages
in depths ranging from 0 to 70 m, with highest abundance
between 0 and 30 m (Appendix A).
Mean sea surface temperatures in south-western Australian waters range from 14.0 to 16.0 C in winter and 22.5 C
in summer (Verlaque et al., 2003). In the Mediterranean
Sea, C. racemosa is exposed to a wider temperature range
down to 8 C in Croatia (Žuljević, 2005) and up to an average of 28 C in the Eastern basin (Cyprus, Libya, Turkey).
Experimental manipulation of light and salinity conditions in the laboratory showed that C. racemosa from coastal
waters of south-western Australia (intertidal/subtidal reef)
had highest growth rates at salinity levels of 30–40 and light
intensities of 20–60 lE m 2 s 1 (Carruthers et al., 1993).
There have been no such experiments conducted on the Mediterranean populations. Salinity ranges from 35.27 to
37.00 in south-western Australian waters and around 38.50
in Mediterranean waters. C. racemosa was found in two
Mediterranean coastal lagoons, Mar Piccolo and Mar
Grande di Taranto (Mastrototaro et al., 2004), where salinity ranges from 34.3 to 37.7 (Alabiso et al., 1997).
In the Mediterranean Sea, the observation of deep populations (up to 70 m of depth) attests to the high tolerance
of C. racemosa to low light conditions. Caulerpa racemosa
is capable of performing photoacclimation. Acclimation
takes place both at increasing depth and during a seasonal
cycle. Firstly, the number of reaction centres can be changed according to irradiance levels to maintain constant
photosynthetic efficiency; and secondly, photosynthetic
efficiency itself can be increased under low irradiance levels
while 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 as
in sheltered areas with the exception of unstable soft-bottom substrates. However, on wave-exposed coasts the
C. racemosa meadows may be damaged by sand scour
(unpubl. data). It seems that C. racemosa is relatively resistant to burial by sediments (Piazzi et al., 2005b). The species is found in polluted as well as relatively pristine
areas (Ballesteros et al., 1999; Žuljević et al., 2004; Ruitton
et al., 2005a; Mifsud and Lanfranco, 2007). The increased
occurrence of C. racemosa in the proximity of large cities
and industrial, cargo, passenger, fishing and recreational
boating harbours does not necessarily demonstrate an
affinity for polluted areas but may be an artefact due to
the secondary dispersal mechanisms via ship traffic and
fishing activities (Appendix A). At least it attests to the tolerance of C. racemosa of high levels of pollution.
3.10. Caulerpa racemosa assemblages
In south-western Australia, C. racemosa occurs intermixed with other algae without forming monospecific
meadows (Carruthers et al., 1993; Verlaque et al., 2003).
In contrast, in the Mediterranean Sea, C. racemosa is
capable of forming continuous dense meadows in different
photophilic and sciaphilic benthic assemblages dominated
by different species such as Caulerpa prolifera, crustose Corallinaceae and other encrusting species, Cymodocea nodosa,
Cystoseira spp., Halophila stipulacea, red algal turfs, rhodoliths, Zostera noltii and sessile macrofauna such as bryozoans, sponges, gorgonian corals and anemones. Caulerpa
racemosa does not seem to be able to penetrate into dense
Posidonia oceanica meadows, while it has often been found
creeping on the rhizomes at the margins or in sparse meadows (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; Žuljević et al., 2004; Tsirika and Haritonidis,
2005). It is interesting to note that the introduced benthic
Indo-Pacific ctenophore Coeloplana willeyi was reported
for the first time in the Mediterranean on Turkish C. racemosa meadows (Cavas and Yurdakoc, 2005b).
At Leghorn Italy, the invasion success of C. racemosa in
benthic habitats appeared to be dependent on the vegetation layers (encrusting, filamentous, erect) present and not
on the diversity of the assemblages. The spread of C. racemosa was most facilitated in assemblages composed of turf
and encrusting species, to a lesser degree in assemblages
with only encrusting species and the assemblage least invasible was an assemblage constituted of erect, turf and
encrusting species (Ceccherelli et al., 2002). Similarly, C.
racemosa colonized algal turf faster than bare rock (Piazzi
et al., 2003a). Furthermore the health of seagrass meadows
influenced the invasion success of C. racemosa. At low shoot
density of Posidonia oceanica, relatively high C. racemosa
growth rate was observed, whereas higher shoot density
reduced C. racemosa growth (Ceccherelli et al., 2000).
Analogous to the seasonal fluctuations observed in
C. racemosa, its associated flora vary during the course of
the year. In order to characterize in detail the new assemblage constituted of C. racemosa meadows on soft-bottom
substrates, a new phytosociological association, Caulerpetum racemosae Giaccone and Di Martino, was described
in southern Italy (Giaccone and Di Martino, 1995b; Di
Martino and Giaccone, 1996).
J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225
3.11. Impacts
Under certain conditions, C. racemosa may form compact multilayered mats up to 15 cm thick that trap sediment
thereby possibly contributing to the siltation of the assemblages (Pandolfo and Chemello, 1995; Piazzi et al., 1997a,
2007a; Argyrou et al., 1999a; Žuljević et al., 2003). Underneath, an anoxic layer has been observed (Piazzi et al.,
1997a; A. Žuljević pers. comm.; J. Klein pers. observ.).
It was found that, compared to other Mediterranean
rhizophytic macrophytes, other Caulerpa spp. and seagrasses, the number of macrophyte species of the epiphytic
assemblage was highest in C. racemosa meadows (Di Martino and Giaccone, 1996). The studies of the impact of C.
racemosa on macrophyte assemblages (rocky substrate,
dead Posidonia oceanica ‘matte’, coralligenous and detritic
assemblages) have been conducted in Italy (Leghorn)
mostly at depths of 2–10 m and 30 m, and in France (Marseille) at 17 m and 30 m (Ceccherelli et al., 2001b; Piazzi
et al., 2001c,d, 2005b, 2007b; Piazzi and Cinelli, 2003;
Balata et al., 2004; Piazzi and Ceccherelli, 2006; Cinelli
et al., 2007; Klein, 2007; Klein and Verlaque, 2007). The
studies indicate a decrease in the total number of species
and total macrophyte cover in presence of C. racemosa.
All layers were concerned, with the encrusting layer being
particularly reduced on rocky substrate. Furthermore the
effect of C. racemosa colonization and sedimentation stress
were found to be similar, indicating that the impact on macrophytes could be mainly caused by accumulation and burial by sediments induced by the mat (Piazzi et al., 2005b).
In presence of C. racemosa the biomass of the introduced Acrothamnion preissii, Asparagopsis armata and
Womersleyella 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 Mediterranean
Sea (Italy, France, Croatia, Spain). In some cases higher
competitive ability was hypothesized for C. racemosa (Piazzi and Ceccherelli, 2002; Piazzi et al., 2003b) and in other
cases the contrary (Renoncourt, 2001; Ceccherelli and
Piazzi, 2001b, Ceccherelli et al., 2002). In Table 4 the characteristics of the two species are compared.
As far as seagrasses are concerned, the impact on shoot
density and flowering has been evaluated through manual
eradication of C. racemosa at Leghorn, Italy at 1 m depth
(Ceccherelli and Campo, 2002). The study showed that
shoot density of Cymodocea nodosa (Ucria) Ascherson
decreased in presence of C. racemosa whereas it increased
for Zostera noltii Hornemann; in both seagrasses the frequency of flowering shoots increased. At the same site,
the effect of C. racemosa on the vegetative cycle and phenolic compounds of Posidonia oceanica was assessed.
Reduced leaf length and leaf area index was found in presence of C. racemosa and at the same time an increase in primary foliar production and in the number of leaves
produced annually was observed, leading to a higher turnover rate (Dumay et al., 2002b). No change in the mean
213
Table 4
Comparison of species characteristics between Caulerpa racemosa (R) and
Caulerpa taxifolia (T)
Characteristics
Comparison
Authors
Biomass
Frond numbers
Frond size
Patch number
Propagation capacity
Ramification
T>R
T>R
T>R
R>T
R>T
R>T
T>R
R>T
R>T
R>T
R>T
R>T
R>T
Capiomont et al. (2005)
Capiomont et al. (2005)
Capiomont et al. (2005)
Piazzi et al. (2001e)
Piazzi et al. (2001b)
Piazzi et al. (2001e)
Capiomont et al. (2005)
Capiomont et al. (2005)
Piazzi et al. (2001e)
Piazzi et al. (2001e)
Capiomont et al. (2005)
Piazzi et al. (2001b)
Piazzi et al. (2001e)
Rhizoidal pillars
Spread
Stolon growth
Stolon length
Stolon numbers
Surface area increase
phenolic compound content of Posidonia oceanica leaves
was detected and the number of tannin cells was not significantly modified in the presence of C. racemosa. However,
estimation was difficult at high interaction levels due to
necrosis of the leaves (Dumay et al., 2004).
Surprisingly, few reliable studies have been undertaken
to quantify the impact of C. racemosa and its competition
with the Mediterranean fauna. Benthic invertebrates were
studied in Cyprus, but the impact of C. racemosa on this
assemblage could not be dissociated from other fluctuating
disturbances in the study area (sewage outfall, fish farming)
(Argyrou et al., 1999a,b). In Sardinia (Italy), no effect of
the presence of C. racemosa on zoobenthic assemblages
of the rocky infralittoral zone could be detected (Casu
et al., 2005). Two studies in Italy on the malacofauna associated with C. racemosa have produced contrasting results.
In the first, low species richness (14 species) was observed
and the two dominant species were Ascobulla fragilis (Jeffreys, 1856) and Bittium latreillei (Payraudeau, 1826), two
species that are usually found associated with Caulerpa prolifera and high sedimentation stress (Pandolfo and Chemello, 1995). The second study found high species richness
(42 species) comparable to Cymodocea nodosa meadows,
which fluctuated according to the seasonal biomass cycle
of C. racemosa (Buia et al., 2001). In Sicily, 52 species of
polychaeta have been found in a C. racemosa meadow
and soft-bottom species such as Laonome kroyeri (Malmgren, 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 assemblages invaded by C. racemosa compared to Controls.
The percentage composition was slightly changed, showing
increased percentages of crustaceans and annelids (Carriglio et al., 2003). Caulerpa racemosa has frequently been
observed creeping on various kinds of macrobenthic animals such as sponges, gorgonian corals and sea anemones
(Žuljević 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. Žuljević pers.
comm. and unpubl. video data).
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J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225
The economic impact of C. racemosa has never been
quantified. However, there has been some speculation on
the basis of observations by fisherman in Italy who found
their fishing nets clogged with C. racemosa (Magri et al.,
2001). Although no studies are available, the large-scale
modification of landscapes induced by C. racemosa with
the overgrowth of benthic assemblages by a more or less
dense and continuous web-like green meadow (A. Žuljević
unpubl. data) may reduce the attractiveness of the biota for
underwater tourism (spearfishing, scuba and free diving).
3.12. Management attempts
Experimental eradication studies concerning C. racemosa remain an exception and limited to small surfaces (400–
1000 cm2). After a period of 2 and 18 months of regular
manual eradication at a 3–4 week interval, C. racemosa
fragments were still found in eradicated plots (Ceccherelli
and Piazzi, 2005; Klein, 2007).
Recovery of macrophyte assemblages after eradication
of C. racemosa has been studied in Italy and France (Piazzi
and Ceccherelli, 2006; Klein, 2007). After 12 and 18
months, respectively, only partial recovery of the assemblages could be observed.
4. Discussion
4.1. Caulerpa racemosa, a new Mediterranean keystone
species
Possible consequences of the C. racemosa invasion event
include modifications of physical and chemical conditions
(water movement, sediment deposition, substrate characteristics) and the underwater landscape, as well as profound modifications of benthic assemblages. On the basis
of its rapid spread and ecological impact C. racemosa is
regarded as an invasive introduced species (sensu Richardson et al., 2000; Boudouresque and Verlaque, 2002). Due to
its impact mainly on habitat architecture and sediments,
C. racemosa can be considered as a habitat modifier (sensu
Wallentinus and Nyberg, 2007). In addition, the differentiation of extensive meadows in the Mediterranean Sea classifies C. racemosa as a new keystone species (=ecosystem
engineer) (sensu Crooks, 2002).
4.2. Why is Caulerpa racemosa so successful?
In the Mediterranean Sea the following 10 introduced
macrophyte species can be considered as invasive species
(on the basis of the criteria elaborated by Boudouresque
and Verlaque, 2002): Acrothamnion preissii (Sonder)
E.M.Wollaston, Asparagopsis armata Harvey, Asparagopsis
taxiformis (Delile) Trevisan de Saint-Léon with their ‘‘Falkenbergia’’ tetrasporophytic phases, Caulerpa racemosa
var. cylindracea (Sonder) Verlaque, Huisman and Boudouresque, Caulerpa taxifolia (M. Vahl) C. Agardh, Codium fragile subsp. tomentosoides (van Goor) P.C. Silva, Halophila
stipulacea (Forsskål) Ascherson, Lophocladia lallemandii
(Montagne) F. Schmitz, Stypopodium schimperi (Buchinger
ex Kützing) Verlaque & Boudouresque and Womersleyella
setacea (Hollenberg) R.E. Norris. Some of them are located
exclusively 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 speed
of spread during the last 17 years. Verlaque et al. (2004)
analyzed the distribution (latitudinal and longitudinal) of
several introduced species 15 years after their first observation and concluded that the rapid spread of C. racemosa
was comparable only to that of Asparagopsis armata and
Womersleyella setacea. Consequently, C. racemosa seems
to be particularly successful compared to most other introduced species (Verlaque et al., 2004).
Several general hypotheses have been proposed to
explain the success of invasive species. Escape from specialist predators and pathogens and the possession of novel
weapons have been put forward to explain the high invasive capacity of certain introduced species (Keane and
Crawley, 2002; Torchin et al., 2003; Callaway and Ridenour, 2004). Indeed, few herbivores have been observed
on C. racemosa meadows in the Mediterranean Sea.
The presence of effective vegetative propagation mechanisms in addition to sexual reproduction may explain in
part the prolific development. In addition, the very rapid
spread of C. racemosa may also be due to the effectiveness
of the secondary dispersal mechanisms, which is illustrated
by the occurrence of the species near harbours and in fishing areas in particular.
4.3. Differential attitude towards the two invasive Caulerpa
species
Despite the fact that Caulerpa racemosa is comparable
to Caulerpa taxifolia in terms of capacity to colonize and
alter native assemblages, there is a wide disparity in the
effort and means mobilised to attempt to cope with these
two invasive Caulerpa species.
Caulerpa taxifolia is introduced in seven countries in the
Mediterranean Sea (Croatia, France, Italy, Monaco, Spain,
Tunisia, Turkey) and in Australia. The populations introduced into California (USA) have successfully been eradicated (Anderson, 2005). In 2005 in France, C. taxifolia
covered around 8842.3 ha corresponding to 143.8 km of
coastline. Currently, C. racemosa is introduced in 12 Mediterranean countries and all major islands as well as in
south-eastern Australia. In 2005, despite having been discovered 6 years after C. taxifolia, C. racemosa already
affected a comparable surface area (8070 ha) and coastline
(163.4 km) (Javel and Meinesz, 2006).
Caulerpa taxifolia has been extensively covered in the
media, seven congresses and workshops have been organized, one book, 361 journal articles (including articles in
J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225
Nature, Science, Ecology) and hundreds newspaper articles
have been published, two European programmes have been
conducted, eradication campaigns have been carried out
and biological control programmes launched. There are
laws regarding C. taxifolia in Australia, the USA, and
Spain. The French Ministry for the Environment issued a
banning order on the trade in and sale of C. taxifolia,
but this order was not prolonged after its expiration. Consequently no legislation exists currently in France on introduced or invasive marine species.
Although research is being conducted on C. racemosa in
several Mediterranean countries and an improvement in
the public awareness of the problem may be noted, there
is a wide disparity in the management of the two invasive
Caulerpa species. Caulerpa racemosa has only been discussed within conferences on C. taxifolia, no European
programme has been conducted and only 150 journal articles have been published only two of them on the results of
a short-term manual eradication (Ceccherelli and Piazzi,
2005; Klein, 2007).
4.4. Future research needs and management
Overall, in-depth rigorous studies are lacking, particularly on the impact, and much of the speculation remains
to be tested. Several authors have reported the species’
occurrence, often with a serious lack of detailed information (depth, substrate, illustrations, morphometric data)
and the impact has often been inferred solely on the basis
of point observations or mere speculation. Furthermore
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.
In the current state of knowledge, no meta-analysis can
be carried out on the effects of C. racemosa on Mediterranean ecosystems. This is due to wide differences in experimental approaches, sampling depths (0–22 m), substrates
and invaded macrophyte assemblages (sand, seagrasses,
dead ‘‘matte’’, rocks), other disturbances (presence of other
introduced species, nutrient input, sedimentation rate, pol-
215
lution) and the insufficient number of localities studied. In
fact, an important bias in the knowledge of the C. racemosa
invasion arises from the choice of the sites and assemblages
studied. 55% of all studies have been carried out in Italy
and 26% at the same locality (Leghorn).
As far as experimental design is concerned, there is an
urgent need for more rigorous and comparable studies.
The impact of C. racemosa needs to be evaluated in different habitats, at different depths, in different regions of the
Mediterranean and at different time scales (in particular
long-term studies are essential).
To limit the impact of the C. racemosa invasion in the
Mediterranean Sea, management strategies need to be put
into action encompassing all countries affected by the problem. A manual and/or chemical control of C. racemosa
similar to the local attempts currently conducted on
C. taxifolia is not a realistic solution considering the extent
and the more diffuse limits of the meadows, the difficulties
to locate individuals, the high capacity of regeneration and
the constraints resulting from the underwater environment.
Studies in the home range of the species (SW Australia) on
the natural predators, diseases and parasites as well as
competition with other macrophytes could provide a basis
for understanding the biology of C. racemosa and to help
to find a possible control mechanism (e.g. biological control). Finally, after Caulerpa taxifolia the disastrous consequences of the introduction of Caulerpa racemosa into the
Mediterranean Sea highlight the urgent necessity to inform
the public and to prohibit all Caulerpa species from the
international aquarium trade.
Acknowledgements
The authors would like to thank an anonymous referee
for useful comments on the manuscript and Michael Paul
for revising the English text. The study was supported by
a grant from the Agence de l’Eau Rhône-MéditerranéeCorse, the Conseil Général 13 and the Ville de Marseille
to J.K.
Appendix A
Presence of Caulerpa racemosa in the Mediterranean Sea and Australia
Country
Site
Albania
–
Authors
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
Palermo), Saranda, Ksamil, Ftelea (2007)
Substrate
Depth
–
–
Indust Fish Recr
–
Sand, mud, rocks,
dead ‘‘matte’’
+
+
1–
+
+
25 m
(continued on next page)
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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,
Sidi-Fredj (Algiers)
Ould-Ahmed and
Meinesz (2007)
–
0.5–
3m
+
Epilithic
to 6 m
+
+
Artifical substrate
–
2–3 m
–
+
+
Žuljević et al.
(2003)
Pakleni Islands, Cesminova cove, Žuljević et al.
Marčuleti Bay, Mirca, Cape Pusti, (2004)
Vela Garška cove, Biševo Island
(Mezuporat cove), Cavtat, Cape
Osti (Dubrovnik), Dubrovnik,
Goli Islet
Mljet Island (Sobra), Glavat Islet, Piazzi et al. (2005a)
Pelješak Peninsula (Prije ba Cove,
Mirce, Cape Lovište)
Komiža (Vis), Ravnik (Vis),
Nuber et al. (2007)
Zavala (Hvar), Korčula, Sušak,
Lokrum, Orsula, Prolaz Harpoti,
Prapratno, Okuklje, V. jezero,
Soline, Gonoturska, Blaca
Sand, rock
5–
15 m
0.5–
50 m
+
–
Episkopi, Limassol, Larnaca,
Moni, Morfou, Pafos
Famagusta harbour
Australia Perth to Hopetoun (native)
Perth to Hopetoun (native)
Port River Estuary, Adelaide
Port River Estuary, Adelaide
Croatia
Cyprus
Marinkovac Islet (Hvar Island)
Capo Greco, Moulia rocks,
Akamas peninsula
France
Marseille
Marseille
Villefranche-sur-mer
Bays of Toulon and Hyères
Villefranche-sur-mer
Corsica (Bastia, Bonifacio,
Propriano), Porquerolles Island,
Port-Cros Island, St Tropez, Nice,
Bay fo Giens
Greece
Womersley (1984)
Verlaque et al.
(2003)
Womersley (2003)
Collings et al.
(2004)
Laganas Bay (Zakynthos Island),
Pylos Bay (w Greece)
Gulf of Saronikos
Rock, sand, mud,
Posidonia oceanica,
Cymodocea nodosa,
benthic fauna
+
+
+
+
+
+
–
–
–
–
Bianchi et al. (1996)
Hadjichristophorou
et al. (1997)
Verlaque et al.
(2000); Verlaque
pers. observ.
Argyrou et al.
(2006)
–
–
–
–
Mud, Halophila
stipulacea
1m
Rock
–
Jousson et al.
(1998)
Verlaque et al.
(2000)
Renoncourt and
Meinesz (2002)
Belsher et al. (2003)
–
–
+
+
+
–
14.5–
23 m
16 m
+
+
+
+
+
+
Capiomont et al.
(2005)
Ruitton et al.
(2005a)
Sand/mud, dead
‘‘matte’’
–
Panayotidis and
Montesanto (1994)
Chryssovergis and
Panayotidis (1998)
Posidonia oceanica
Dead ‘‘matte’’, sand
–
+
20–
30 m
22 m
+
+
+
+
+
+
–
+
+
+
25–
35 m
–
+
+
+
+
+
J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225
217
Appendix (continued)
Country
Site
Authors
Substrate
Depth
Posidonia oceanica
–
2535 m
–
–
–
–
–
–
–
Rock, benthic
flora + fauna
Rock, benthic
flora + fauna
2–40 m
Famà et al. (2000)
Cantasano (2001)
Di Martino (2001)
Piazzi et al. (2005a)
–
Rock
Caulerpa taxifolia
–
–
1–2 m
–
–
Gambi and Terlizzi
(1998)
Famà et al. (2000)
Buia et al. (2001)
Dappiano et al.
(2001)
Gambi et al. (2001)
Buia et al. (2003)
Russo et al. (2003)
Sand, Cymodocea
nodosa
–
Rock
–
13–
20 m
–
2–7 m
–
–
–
–
Piazzi et al. (2005a) –
Guala et al. (2006) –
–
–
4–
30 m
–
–
Piazzi et al. (2005a) –
–
Bussotti et al.
Rock, sand
(1996)
Modena et al.
Dead ‘‘matte’’, rock
(2000)
Piazzi et al. (2005a) –
Nissiros Island, Cape Sounion
Panayotidis and
Montesanto (1998)
Crete
Siakavara pers.
com. in Panayotidis
(1999)
Rhodos Island
Famà 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
(Zakynthos Island)
Haritonidis (2005)
Messiniakos Gulf
Tsirika et al. (2006)
Italy
Calabria
Capo Rizzuto (Ionian Sea)
Capo Vaticano
Stretto di Messina, Calabria
Vibo Marina, Palmi, Scilla
Campania
Gulf of Salerno
Capo Miseno, Salerno
Naples
Isola di Ischia, Procida, Vivara
(Gulf of Naples)
Isole Flegree (Gulf of Naples)
Isole Flegree (Gulf of Naples)
Capri Island, Sorrento Peninsula
Capri Island, Point Campanella
Gulf of Naples
Latium
S. Agostino, S. Marinella,
Sperlonga, Ponza Island, Zannone
Island, Ventotene Island
Liguria
Quinto (Genova)
Varazze, Sturla, Nervi (Genova)
Bergeggi Islands, Bay of
Monterosso, Palmaria Island, Gulf
of La Spezia
Foce, Quarto (Genova)
Montefalcone et al. Rock, sand, dead
(2007a)
‘‘matte’’
Indust Fish Recr
0–2 m;
35–
40 m
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
9m
+
+
+
0–
10 m
–
+
+
+
+
+
10–
+
+
+
20 m
(continued on next page)
218
J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225
Appendix (continued)
Country
Site
Authors
Cogoleto-Arenzano
Montefalcone et al. Dead ‘‘matte’’
(2007b)
Tunesi et al. (2007) Dead ‘‘matte’’,
muddy detritic
–
Buia et al. (1998)
Cecere et al. (2000)
Costantino et al.
(2002)
Bello et al. (2004)
Piazzi et al. (2005a)
Dead ‘‘matte’’
Dead ‘‘matte’’
Dead ‘‘matte’’
6–9 m
–
–
–
–
–
–
Mastrototaro et al.
(2004)
Caulerpa prolifera,
dead ‘‘matte’’,
Posidonia meadow
Marco Giani pers.
com. in Di Martino
and Giaccone
(1995)
Cossu and Gazale
(1997)
Cossu et al. (2002)
Cossu et al. (2004)
–
–
Dead ‘‘matte’’
–
Dead ‘‘matte’’
Dead ‘‘matte’’
–
–
Gallinaria Island
Puglia
Gulf of Taranto
Gulf of Taranto
Cerano (Brindisi), Lecce
Bari
Lizzano, Maruggio, Monopoli,
Nardo, Otranto, Pulsano, S. Vito,
Ugento
Mar Piccolo, Mar Grande
Sardinia
Sarroch-Cagliari
Golfo di Cagliari
Golfo dell’Asinara
Serpentera Island, Golfo
dell’Asinara, Golfo di Cagliari
Asinara Island, Bay of Malfatano
Sicily
Baia di San Panagia (Syracuse)
Isola di Lampedusa (Pelagie
Islands)
Isola di Capo Passero (south of
Syracuse)
Brucoli (Syracuse)
Capo Molini
Acitrezza (Catania)
Isola di Pantelleria
Santa Maria La Scala to Capo
Passero
Capo Passero to Pozzallo (Ragusa)
Peninsola Maddalena (Syracuse)
Linosa Island (Pelagie Islands) –
Sicily channel
Straits of Messina
Substrate
Depth
6–
25 m
Piazzi et al. (2005a) –
–
Alongi et al. (1993) Sand, Caulerpa
prolifera
Alongi et al. (1993) Sand/mud,
Cymodocea nodosa
Di Martino and
–
Stancanelli (1998)
Serio and Pizzuto
Dead ‘‘matte’’
(1998)
Famà et al. (2000) –
Verlaque et al.
–
(2000)
Picchetti & Morselli –
pers. com. in Di
Martino (2001)
Di Martino (2001) –
3–
15 m
1m
Di Martino (2001)
Marino et al. (2001)
Azzurro et al.
(2004)
Profeta et al. (2004)
Cymodocea nodosa
–
–
Rock
Cape Feto, Marsala, Trapani, Gulf Piazzi et al. (2005a) –
of Castellammare, Termini
Imerese, Favignana Island
Indust Fish Recr
+
+
+
+
+
+
+
+
+
+
+
+
+
+
+
1–
30 m
2–6 m
–
–
–
1–
30 m
–
–
–
0.5–
1m
–
+
J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225
219
Appendix (continued)
Country
Libya
Malta
Site
Authors
Substrate
Tuscany
Meloria shoals (Livorno)
Livorno, Vada shoals
Piazzi et al. (1994) Dead ‘‘matte’’
Piazzi et al. (1997a) Dead ‘‘matte’’, rock
+
+
+
+
+
+
+
+
+
+
Tajura, Tripoli
–
+
Nizamuddin (1991)
Stevens (1999)
Sand, rock
Maerl, mud/sand,
rock
Mifsud (2000)
Maerl, mud/sand,
rock
Piazzi et al. (2005a) –
–
Hondoq ir-Rummien
Mifsud and
Lanfranco (2007)
0–
10 m
+0.05–
50 m
Balearic Islands
Ballesteros et al.
(1999)
Famà et al. (2000)
Pena Martı́n et al.
(2003)
Aranda (2004)
Gozo Island (Dwejra, Xatt lAhmar), Malta Island (St Georges’
Bay to Ghar Lapsi, Hard Bank)
Marsascala
Mifsud et al. (2006) Maerl, sand, rock
Tunisia
Turkey
Indust Fish Recr
4m
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
Southern Malta
Spain
Depth
–
–
–
–
Gran Canaria (Canary Islands)
Alicante, Santa Pola, Tabarca
Island
Sagunto, Alicante, Castello de la
Plana
Gran Canaria, Lanzarote, Tenerife Verlaque et al.
(Canary Islands)
(2004)
Mallorca (Dragonera, Bay of
Piazzi et al. (2005a)
Palma, Cap de Regana, Cap Blanc,
Ses Fontanelles), Cabrera, Eivissa
–
Rock, sand, dead
‘‘matte’’
Dead ‘‘matte’’
Rock, sand with
Caulerpa prolifera
–
–
0–
19 m
15–
34 m
21–
30 m
–
–
Cap Bon
–
Belkhiria (1999)
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
Gökova
Sand, rock
25–
+
51 m
(continued on next page)
Evirgen (1997)
+
+
+
220
J. Klein, M. Verlaque / Marine Pollution Bulletin 56 (2008) 205–225
Appendix (continued)
Country
Site
Authors
Substrate
Depth
Tasucu, Kas, Bodrum, Kusadasi
Kemer, Tasucu, Kas, Kusadasi,
Cesme, Marmaris, Gökova,
Bodrum
Odunluk Iskelesi
Cirik (1999)
Tolay et al. (2001)
–
Rock, sand, mud,
dead ‘‘matte’’
–
0–
60 m
Okudan et al.
(2002)
Yokes and
Rudman (2004)
Cavas and
Yurdakoc
(2005a,b)
Piazzi et al. (2005a)
Sand, sand/mud
3–7 m
–
–
5–
24 m
2m
–
–
Cirik and Akçali
(2006)
Rock, sand, mud
0–
49 m
Uc Adalar
Seferihisar
Bozcaada, Izmir (Eskifoça,
Karaburun), Didim
Gökova bay, Güllük
Indust Fish Recr
Indust, industrial harbour; Fish, fishing activities; Recr, recreational boating.
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