Spread of the introduced tropical green alga Caulerpa taxifolia in northern Mediterranean waters

The first report of Caulerpa taxifolia in the Mediterranean is from 1984. The alga was found on the rocky shore at Monaco, below the Oceanographic Museum, where it had been on display in tropical aquaria. Within five years, there was an abundance of C. taxifolia on the shores around the first point of observation. In 1987, C. taxifolia appeared on the French coast, 3 km east of Monaco, at Cap Martin. By late 1991, 30 ha of shore in the vicinity of Monaco was covered with the alga. New points of colonization were in Livorno, Italy, 240 km east of Monaco, and to the west at Agay, Le Lavandou, Hyères, Toulon, Les Lecques, Saint Cyprien, 50 to 370 km from Monaco. The westernmost point of colonization, noted in September 1992, was 600 km from Monaco, at Majorca (Balearic island, Spain). Most types of substrata, between 0 and 50 m depth, are susceptible to colonization by C. taxifolia. Seaweed and seagrass populations on the coasts of Monaco and Cap Martin have been significantly reduced or destroyed because of invasion by C. taxifolia.     

Genetic polymorphism in Caulerpa taxifolia (Ulvophyceae) chloroplast DNA revealed by a PCR‐based assay of the invasive Mediterranean strain

Abstract An invasive, cold‐tolerant strain of the tropical green alga Caulerpa taxifolia was introduced recently in the Mediterranean Sea and along the Californian coast. We screened 50 aquarium and open‐sea C. taxifolia specimens for the presence/absence of an intron located in the rbcL gene of chloroplast DNA. We also reanalysed a total of 229 sequences of the Internal Transcribed Spacer (ITS) of ribosomal DNA, combining previously published sequences from different studies with 68 new sequences to complement rbcL data. The introduced Mediterranean strain was found to be characterized by the absence of the rbcL intron and by the occurrence of a particular monomorphic ITS type. A PCR assay based on rbcL gene was developed to detect new introductions of the invasive strain of C. taxifolia. This rapid and inexpensive test could be useful to assist environment managers in the preservation of coastal marine ecosystems.     

Molecular data suggest a hybrid origin for the invasive Caulerpa racemosa (Caulerpales,Chlorophyta) in the Mediterranean Sea

Morphological data has provided a basis for the hypothesis that three taxa belonging to the Caulerpa racemosa complex occur in the Mediterranean Sea: var. turbinata–uvifera, var. lamourouxi, and the `invasive variety'. In order to test this hypothesis and to determine the origin of the `invasive variety', the transcribed spacer ITS1–ITS2 and an 18S ribosomal DNA (rDNA) intron were analysed from 16 isolates of Caulerpa racemosa. The `invasive variety' shows intraindividual polymorphism for both types of sequences. The ITS1–ITS2 data confirm that the three morphological varieties of C. racemosa from the Mediterranean Sea are distinct taxonomic units. The 18S intron data suggest that the new `invasive variety' could be a recent hybrid between var. turbinata–uvifera and an unknown tropical strain. Incongruence between the phylogenetic tree computed from ITS1–ITS2 regions and the 18S intron indicates that homogenization processes of concerted evolution have run at different rates.     

The Introduced Green Alga Caulerpa Taxifolia Continues to Spread in the Mediterranean

The tropical green alga Caulerpa taxifolia in the Mediterranean has spread steadily since its introduction in 1984. At the end of 2000, approximately 131km² of benthos had been colonized in 103 independent areas along 191km of coastline in six countries (Spain, France, Monaco, Italy, Croatia and Tunisia). Large regions neighboring the invaded areas appear favorable to further colonization, and there is thus no reason to believe that spreading will slow down in the years to come.     

Antioxidant response and caulerpenyne production of the alien Caulerpa taxifolia (Vahl) epiphytized by the invasive algae Lophocladia lallemandii (Montagne)

Invasive algae alter the structure and function of ecosystems. The red algae Lophocladia lallemandii grows in the West Mediterranean epiphyting the green algae Caulerpa taxifolia, another invasive alga. Our aim was to determine whether the invasive algae Lophocladia, recently introduced in the West Mediterranean, induces oxidative stress and an antioxidant response in Caulerpa taxifolia. We measured the caulerpenyne production, the activities of antioxidant enzymes and the levels of markers of lipid peroxidation in Caulerpa taxifolia. Caulerpenyne concentration was significantly higher in Caulerpa taxifolia epiphytized by Lophocladia. End-products of lipid peroxidation -malondialdehyde (MDA) and 4-hydroxinonenal (4-HNE)- were significantly increased in Caulerpa taxifolia samples from the station with Lophocladia. Antioxidant enzyme activities -catalase and superoxide dismutase (SOD)-, as well as H₂O₂ production significantly increased in the Lophocladia station compared to the control station. The activities of catalase and SOD determined in Lophocladia lallemandii showed no significant differences between Lophocladia living alone and Lophocladia epiphytating Caulerpa taxifolia. Caulerpa taxifolia epiphytized by Lophocladia lallemandii responded by increasing the caulerpenyne and H₂O₂ production and the antioxidant enzymes activities as a defensive mechanism against the new invasive algae.     

Preliminary survey of toxicity of the green algaCaulerpa taxifolia introduced into the Mediterranean

Caulerpa taxifolia (Vahl) C. Agardh (Ulvophyceae, Caulerpales) is an alga of tropical origin that was accidentally introduced into the Mediterranean sea in 1984, where this species can reach an abundance that has never been described in tropical endemic regions. It is known that caulerpacean algae can develop an efficient strategy against grazers consisting of the synthesis of repulsive of toxic secondary metabolites: we report here the first study of the toxicity of purified secondary metabolites and raw extracts fromC. taxifolia from the Mediterranean.Toxicity was evaluated on three models: mice (lethality), mammalian cells in culture (cytotoxicity) and sea urchin eggs (disturbance of cell proliferation). Aqueous extracts are only active on fibroblasts and mice. In the three toxicity models a seasonal variation of toxicity is observed for the crude methanol extract as well as a decrease of this activity whenC. taxifolia from the Mediterranean is kept in aquaria. Pure compounds exhibit different toxicity depending on the assay. 10,11-epoxycaulerpenyne is the most active substance on mice and fibroblasts whereas taxifolial A and D are inactive or only weakly toxic. Among the four tested compounds caulerpenyne, the major metabolite ofC. taxifolia, is the most active on sea urchin eggs. Caulerpenyne may therefore represent an ecological risk for microorganisms and the eggs of multicellular animals living close to this alga. The ecological impact of this toxicity on marine organisms and the interaction of this alga with the herbivorous fauna are discussed.     

Dinucleotide microsatellite markers in the genus <Emphasis Type="Italic">Caulerpa</Emphasis>

Caulerpa spp. are clonal green marine algae which often act as invasive species when growing outside their native biogeographical borders. Over the two past decades, Caulerpa taxifolia has spread along the Mediterranean coast, presently occurring at 70 sites and covering nearly 3,000 ha of subtidal area. New genetic markers (microsatellites) have been developed to assess clonal structure and genetic diversity of recently established populations of the invasive species C. taxifolia and Caulerpa racemosa in comparison with populations of the native Caulerpa prolifera in the Mediterranean. Our results show that nine polymorphic markers have been developed for C. prolifera, seven for C. taxifolia, and three for C. racemosa. Genetic diversity in Caulerpa was assessed in two geographical scales: one at a population scale where 40 thalli units were collected from C. prolifera in Cala d’Or, Mallorca, Spain, and another at a species scale, where 30 sample units were analyzed for C. prolifera, 24 for C. taxifolia, and 24 for C. racemosa from different sites in the Mediterranean, Atlantic, and Pacific Ocean. Number of alleles, expected heterozygosity, and marker amplification success are provided in each case.     

How an invasive alga species (<Emphasis Type="Italic">Caulerpa taxifolia</Emphasis>) induces changes in foraging strategies of the benthivorous fish <Emphasis Type="Italic">Mullus surmuletus</Emphasis> in coastal Mediterranean ecosystems

The foraging behaviour variability of three striped red mullet (Mullus surmuletus L. 1758) populations with respect to the vegetation cover was examined along the French Mediterranean coasts. We tested both the carrying capacity of different habitats and the hypothesis of a food segregation by the invasive alga Caulerpa taxifolia (Vahl) C. Agardh, on the functioning of benthic fish populations. The results indicated a significant site effect on M. surmuletus foraging behaviour and movements. The vegetation cover may play an important role in modifying the striped red mullet cost of foraging (sampling effort) and thus its strategy of prey capture. As long as the cover of marine phanerogams and/or macrophyte algae (Caulerpaceae) increases, the foraging budget and the distances covered in search of prey decrease significantly. Similarly, the striped red mullet increases the prospected sample periods to augment its foraging success, swimming above the bottom. These changes are related to the development of a dense superficial network of plagiotropic rhizomes and stolons, and to the reduction of space between fronds that limits the accessibility to resources and may increase intra-specific food competition. The role of C. taxifolia does not differ from that of other marine phanerogams but induces significant changes in the structure of Mullidae populations at the local level. The rapid expansion of Caulerpaceae in the Mediterranean Sea could constitute a real threat for the balance of the marine coastal biodiversity and the ecology of M. surmuletus, which is considered a flagship species for coastal Mediterranean demersal fisheries.     

Genetic evidence for the identity of Caulerpa racemosa (Forsskål) J. Agardh (Caulerpales,Chlorophyta) in the Adriatic Sea

Three taxa of Caulerpa racemosa that differ morphologically and genetically have been reported in the Mediterranean Sea. The ‘invasive variety’ was recorded for the first time in the early 1990s in Libya. In less than 10 years, it was found in almost all parts of the Mediterranean. The first record of C. racemosa in the Croatian part of the Adriatic Sea was in 2000 and as many as 35 different localities were established by the end of 2004. In terms of morphology, the specimens from the Adriatic Sea resemble the ‘invasive variety’. To confirm this, we analysed populations from two different localities (the island of Mljet and the peninsula of Pelje?ac) using the ITS1-5.8S-ITS2 region of 18S-5.8S-26S rDNA unit as a molecular marker. The ITS1-5.8S-ITS2 region from nine individual plants was amplified by PCR, cloned in a pCR 2.1 vector and sequenced. Phylogenetic comparison of sequences from specimens found in the Adriatic Sea with specimens of the same and similar taxa, found both inside and outside the Mediterranean, provided genetic evidence that C. racemosa populating the Adriatic Sea corresponds to the Mediterranean C. racemosa var. cylindracea (Sonder) Verlaque, Huisman?&?Boudouresque, i.e. to the ‘invasive variety’.     

Predicting risks of invasion of macroalgae in the genus Caulerpa in Florida

There is worldwide concern about the aquarium strain of the green alga Caulerpa taxifolia (Vahl) C. Agardh that was introduced to the Mediterranean Sea in 1984. Since that time, it has flourished and now covers thousands of hectares of near-shore waters. More recently, aquarium strains of C. taxifolia invaded southern California and Australian waters. Our goal was to evaluate potential invasion of C. taxifolia to Florida’s coastal waters. We looked for evidence of C. taxifolia—aquarium strain, as well as the present distribution of all species of Caulerpa, in Florida’s near-shore waters. We surveyed 24 areas in six zones along the Floridian coastline, and evaluated the association of potential indicators for the presence of Caulerpa. Latitude, presence of seagrass beds, human population density, and proximity to marinas were the four variables simultaneously considered. Caulerpa taxifolia—aquarium strain was not found at any of our survey locations. However, 14 species of Caulerpa were found at 31 of the 132 sites visited. Percent correct for our model was 61.5% for presence and 98.1% for absence. There was a positive correlation between Caulerpa spp. and seagrass beds and proximity to marinas. There was a negative correlation with latitude and human population density. The parameters in the logistic regression model assessing the association of Caulerpa occurrence with the measured variables were then used to predict current and future probabilities of Caulerpa spp. presence throughout the state. This prediction model will allow resource managers to focus their efforts in future surveys.     

Impact of Caulerpa taxifolia colonization on the littoral ichthyofauna of North-Western Mediterranean sea: preliminary results

After its accidental introduction in the French waters of the Mediterranean, the green seaweed Caulerpa taxifolia is now spreading along the coast of the Alpes-Maritimes, invading various biotopes (rock, sand and Posidonia oceanica seagrass beds). During the spring and fall of 1992, we evaluated the impact of C. taxifolia on the infralittoral ichthyofauna of Cap Martin (Menton) and compared invaded and reference sites, in shallow (3–8 m) and deep (11–25 m) stations. Caulerpa taxifolia apparently does not have any effect on the composition and global species richness of the ichthyofauna. Therefore, no exclusion phenomenon has been observed and fish behavior has remained normal (feeding habits, reproduction, recruitment). However, fish density and biomass are slightly lower in the colonized sites. Negative regression was observed, in shallow sites during the spring season, between the percentage of substrate invaded by C. taxifolia and the average density of fish assemblages (slope= –0.13, r=0.26, p<0.01). Despite these observations, C. taxifolia meadows seem to be a favorable environment for the recruitment of some species of Labridae (Coris julis, Symphodus ocellatus), Sparidae (Diplodus annularis) and Serranidae (Serranus cabrilla) in the fall.The relative importance of C. taxifolia as environmental parameter and of other habitat characteristics (structural complexity, substrate slope, hydrodynamism, depth, fishing pressure) is discussed to explain these differences. The results of this first study indicate that there exists no simple relation between the presence of C. taxifolia and fish assemblages.     

Grazing rates of Elysia tomentosa on native and introduced Caulerpa taxifolia

The marine alga Caulerpa taxifolia Vahl (C. Agardh), recognized globally as one of the most prolific non-native species introductions, has been introduced to several temperate locations from where it has since rapidly expanded. C. taxifolia is protected by a toxin (terpenoid) in its tissues that limits grazing by native herbivores. Sacoglossan molluscs of the genus Elysia are among the few organisms that graze C. taxifolia; however, little is known about their feeding ecology. In the current study, we quantified the grazing rates of Elysia tomentosa on native C. taxifolia (Moreton Bay, Queensland) and introduced C. taxifolia (Botany Bay and Lake Conjola, New South Wales). Grazing rates were similar at Moreton Bay sites and Botany Bay; however, they were significantly lower in Lake Conjola. At the maximum observed grazing rate, slugs ate their body weight in C. taxifolia (dry weight) every 18–24 h. Differences in grazing rates between locations may be explained by differences in C. taxifolia morphology rather than native or introduced origin. Handling editor: J. Padisak     

Tracking the origin of the invading Caulerpa (Caulerpales, Chlorophyta) with Geographic Profiling, a criminological technique for a killer alga

The application of the Geographic Profiling technique (with the “Rossmo formula”) proved to be effective in assessing the spreading origin of invading species of Caulerpa in the Mediterranean. Geoprofiling is a technique more frequently used in criminology. We applied this method to an algal invasion for the first time. The method was calibrated with the distribution data of Caulerpa taxifolia, whose spreading in the Mediterranean Sea started from the aquarium of Monaco. This is the first time that Geographic Profiling is calibrated on a data set of sites of presence of a biological invader, of which the spreading origin is known. The application on Caulerpa racemosa var. cylindracea showed that the probable spreading center of the alga should be located in Western Sicily for the Mediterranean and in the southern part of Tenerife for the Canary Islands (Las Galletas, a fishing village). The spreading centers correspond to areas with ports, indicating that the spreading of this alga should be related to (fishing) boats. This result confirmed the opinion of other authors. The parameters used in the Rossmo Formula, obtained through calibration with the known origin of C. taxifolia invasion for identifying the origin of the spread of C. racemosa var. cylindracea may be extended to other algae with similar propagation mode and similar habitat requirements.     

Nutrient availability in the sediment and the reciprocal effects between the native seagrass Cymodocea nodosa and the introduced rhizophytic alga Caulerpa taxifolia

Two reciprocal experiments testing for the effects of nutrient addition in the sediment and competitive interactions between the native seagrass Cymodocea nodosa (Ucria) Ascherson and the introduced alga Caulerpa taxifolia (Vahl) C. Agardh were performed. This study was conducted for 13 months (August 1995 until September 1996) in a bay on the south coast of Elba Island (Italy). Each experiment consisted of the manipulation of the level of nutrients (addition vs. control) and the manipulation of the neighbours (presence vs. removal). Response variables were blade density and size for one experiment and shoot density and leaf length of seagrass in the other. Results indicated that the presence of Caulerpa taxifolia did not affect significantly Cymodocea nodosa shoot density and the increased nutrient availability in the sediment did not alter this pattern. Neither the removal of the canopy of the seagrass nor the fertilization of the sediment has influenced significantly the density of the alga. Both species, where co-occurring, show larger size than where the neighbour is removed. Hence, results of this study suggest that the two species on the long term are likely to coexist and that the high nutrient supply of the sediment would not enhance the probability of success neither of the seagrass nor of the alga. Predictions made on the basis of short-term results, that high nutrient loads of the substratum would have represented an even more suitable condition for C. taxifolia to colonize C. nodosa beds and that on the long-term the alga has a high probability of success, did not occur.     

Feeding strategy of the sacoglossan opisthobranch <Emphasis Type="Italic">Oxynoe olivacea</Emphasis> on the tropical green alga <Emphasis Type="Italic">Caulerpa taxifolia</Emphasis>

The feeding behaviour of the shelled sacoglossan Oxynoe olivacea was investigated to better understand the role and importance of this species in influencing encroachments of the alien alga Caulerpa taxifolia in the Mediterranean sea. We tested whether this slug preferred, as preliminary field observations suggested, an aggregative feeding behaviour and which part of the algal thallus, phylloid vs rhizoid, it preferred. Results showed that O. olivacea fed in groups and actively selected phylloid. This outcome poses important questions regarding the possibility that this species, fragmenting the alga thallus, could enhance dispersion and regeneration of C. taxifolia.     

A FORENSIC AND PHYLOGENETIC SURVEY OF CAULERPA SPECIES (CAULERPALES,CHLOROPHYTA) FROM THE FLORIDA COAST,LOCAL AQUARIUM SHOPS,AND E‐COMMERCE: ESTABLISHING A PROACTIVE BASELINE FOR EARLY DETECTION1

Baseline genotypes were established for 256 individuals of Caulerpa collected from 27 field locations in Florida (including the Keys), the Bahamas, US Virgin Islands, and Honduras, nearly doubling the number of available GenBank sequences. On the basis of sequences from the nuclear rDNA‐ITS 1+2 and the chloroplast tufA regions, the phylogeny of Caulerpa was reassessed and the presence of invasive strains was determined. Surveys in central Florida and southern California of >100 saltwater aquarium shops and 90 internet sites revealed that >50% sold Caulerpa. Of the 14 Caulerpa species encountered, Caulerpa racemosa was the most common, followed by Caulerpa sertularioides, Caulerpa prolifera, Caulerpa mexicana, and Caulerpa serrulata. None of the >180 field‐collected individuals (representing 13 species) was the invasive strain of Caulerpa taxifolia or C. racemosa. With one exception (a sample of C. racemosa from a shop in southern California belonged to the invasive Clade III strain), no invasive strains were found in saltwater aquarium stores in Florida or on any of the internet sites. Although these results are encouraging, we recommend a ban on the sale of all Caulerpa species (including “live rock”) because: morphological identification of Caulerpa species is unreliable (>12% misidentification rate) and invasive strains can only be identified by their aligned DNA sequences, and because the potential capacity for invasive behavior in other Caulerpa species is far from clear. The addition of the Florida region to the genetic data base for Caulerpa provides a valuable proactive resource for invasion biologists as well as researchers interested in the evolution and speciation of Caulerpa.     

Lack of epifaunal response to the application of salt for managing the noxious green alga <Emphasis Type="Italic">Caulerpa taxifolia</Emphasis> in a coastal lake

Since the discovery of the green alga Caulerpa taxifolia in Lake Macquarie (New South Wales, Australia) in 2001, the New South Wales Department of Primary Industries (Fisheries) has attempted various control methods, including covering the alga with granulated sea salt to induce osmotic shock and cell lysis. In Lake Macquarie, C. taxifolia often occurs in patches within beds of the native seagrass Zostera capricorni. Although the effects of the salt treatment on blades of Z. capricorni and infauna have been shown to be minimal, there have been no tests of any effects on other native biota, including seagrass epifauna. In this study, we tested the general hypothesis that the abundance and diversity of epifauna would be reduced by salting. We used a ‘Beyond BACI’ experimental design whereby epifaunal invertebrates were sampled 3 months, 6 weeks and 6 days before and then again after salting. Epifaunal abundances at the putatively impacted (salted) location were compared to those at 4 control locations (where no salt was applied). Abundances of most organisms varied significantly among times and locations with no evidence of the consistent effect of salting on diversity or abundance of epifauna. The study represents an example of the use of large-scale managerial action as a scientific experiment. Electronic supplementary material Supplementary material is available for this article at <> and accessible for authorised users     

But next time?: Unsuccessful Establishment of the Mediterranean Strain of the Green Seaweed Caulerpa taxifolia in the Sea of Japan

We conducted a survey of 63 public aquariums in Japan by means of a questionnaire asking if a green seaweed, Caulerpa taxifolia, was cultured or exhibited in aquariums under the network of the public aquarium association of Japan in 1997. Of 51 aquariums, 16 cultured or exhibited C. taxifolia. Most of the public aquariums possessing C. taxifolia purchased them from aquarium shops or received them from another public aquarium as a donation. Notojima aquarium reported temporal establishment of C. taxifolia in the Sea of Japan between the summer and autumn of 1992 and 1993. C. taxifolia was released into the sea from a 1 m³ cage that was submerged in an open pool. Two colonies with diameters less than 2 m were found near the mouth of a water outflow pipe in both years. Molecular analysis of the ITS rDNA gene of the aquarium strain of Notojima clarified that the seaweed is the same as the aquarium-Mediterranean and Californian invasive strain. Unsuccessful establishment of the invasive strain of C. taxifolia in the Sea of Japan is probably due to water temperatures in winter that are lethal for C. taxifolia. C. taxifolia remains present in many public and private aquariums. If C. taxifoliawere to be released in more temperate waters of Japan, there would be a high risk of establishment and, thus, impact on the marine ecosystem. This suggests that the trade, culture and exhibition of C. taxifolia should be strongly avoided to reduce the chances of accidental release of this harmful species.     

Habitat preference of three common fishes for seagrass, <Emphasis Type="Italic">Caulerpa taxifolia</Emphasis>, and unvegetated substrate in Moreton Bay,Australia

A decrease in seagrass cover and a commensurate increase in Caulerpa taxifolia distribution in Moreton Bay have prompted concern for the impact that habitat change may have on faunal communities. Therefore, it is important to understand the patterns of habitat use. We examined habitat selection of three common seagrass species: double-ended pipefish (Syngnathoides biaculeatus), eastern trumpeter (Pelates quadrilineatus), and fan-bellied leatherjacket (Monacanthus chinensis) using a mesocosm experiment. Fish were given three possible habitat pairings (1) seagrass and C. taxifolia, (2) seagrass and unvegetated, and (3) C. taxifolia and unvegetated. Observation trials were conducted during the day and night over two days. In all trials, fish preferred vegetated habitat (seagrass or C. taxifolia) over unvegetated habitat (sand). In seagrass and C. taxifolia trials, all species preferred seagrass significantly over C. taxifolia. Habitat use patterns did not differ between day and night trials. Caulerpa taxifolia provides a valuable structured habitat in the absence of seagrass; however, it is unclear if C. taxifolia meadows provide other resource benefits to fishes beyond that of shelter.     

Growth and survival of the invasive alga, <Emphasis Type="Italic">Caulerpa taxifolia</Emphasis>, in different salinities and temperatures: implications for coastal lake management

The alga Caulerpa taxifolia is an invasive pest species in many parts of the world and has recently become established in several estuaries in south eastern Australia. A major infestation has occurred in Lake Conjola, an intermittently open and closed coastal lagoon in southern NSW. Short term (1 week) laboratory experiments were carried out to investigate growth and survival of fragments of C. taxifolia collected from this outbreak, under a range of salinities (15–30 ppt) and water temperatures (15–30°C). Fronds, stolons and thalli of the alga all displayed similar responses. Many of the algal fragments doubled in size over the week and a maximum growth rate of 174 mm/week was recorded. Fragments showed good growth (> 20 mm/week) at salinities > 20 ppt and temperatures > 20°C. Almost total mortality occurred at salinities lower than 20 ppt and temperatures less than 20°C. Historical records of water quality demonstrate that prior to entrance manipulation in 2001, salinities in Lake Conjola had often dropped to below 17 ppt for extended periods (up to 2 years). This suggests that management of the alga may be improved if the lake was allowed to undergo its normal cycles of opening and closing to the ocean, and that entrance manipulation may be one factor that has influenced the success of this invasive species.