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Distribution of Chelidonura fulvipunctata in the Mediterranean Sea and Red Sea. Dates refer to the years when specimens were observed and/or collected.
Source publication
The number of tropical species established in the Mediterranean Sea has risen at an unprecedented rate in the last 40–50 years, often entering the basin from the Red Sea and to a lesser extent by shipping or mariculture. The taxonomic identity of these alien species can be difficult to determine and DNA barcoding can help to clarify the status of q...
Contexts in source publication
Context 1
... first observations in the central Mediterranean Sea date from 1993 and 1998 in Malta and we now report it from Sicily, Italy. It was only in 2014 and 2015 that the species was found in the western Mediterranean, namely off the coast of France and in the Spanish Balearic Islands (Figure 4; Table 3). ...
Context 2
... first reports of C. fulvipunctata in the Medi- terranean Sea were from the eastern basin (Turkey and Israel) and recent observations confirm that the species is slowly expanding westwards (Figure 4, Table 3), which is consistent with a Lessepsian introduction. However, Gofas and Zenetos (2003) have drawn attention to the fact that several Indo- Pacific molluscan immigrants not known in the Red Sea were reported first in the Mediterranean from the southern coast of Turkey and from Cyprus, and only later were observed and eventually become established in the Levantine coast and Egypt. ...
Similar publications
In recent years, shellfish farming of Haliotis tuberculata, the European abalone, has started in Ireland and France. In general, cold waters protect the gastropod from bacterial and parasitic diseases but the shell colonization by boring polychaetes is an important problem causing a reduction of marketability and growth rate. During this study cond...
Citations
... This area experiences intense maritime traffic, and is undergoing a period of rapid demographic growth and urban development (e.g., Chalastani et al., 2020;NEOM, 2024). Since the opening of the Suez Canal, this basin has been a transit area between the Indo-Pacific basin and the Mediterranean Sea (e.g., Goren and Klausewitz, 1978;Malaquias et al., 2016;Fernandez et al., 2022). Despite this, research specifically focused on NIS in the Red Sea remains considerably scarce (Aylagas et al., 2024). ...
Introduction
Maritime traffic and coastal urbanisation significantly contribute to the introduction and proliferation of non-indigenous species (NIS). However, the lack of information might prevent effective monitoring in data-limited regions, particularly in areas experiencing demographic growth, where monitoring biofouling communities could offer crucial insights into the dynamics of NIS invasions. This study represents a baseline characterization of the biofouling communities in the northern Saudi Arabian Red Sea (NEOM region) prior to extensive urban, industrial, and commercial development.
Methods
Samples were collected in November 2023 and February 2024 from seven sites within the region. At each site and time, three settlement structures, each with a PVC panel attached to a brick and rope, were sampled after 3-months deployment. Panels were analysed with photo quadrat analysis (PhQd), examined to manually collect sessile macroinvertebrate specimens for taxonomic identification using morphological and DNA barcoding analysis, and scraped for bulk DNA analyses using DNA metabarcoding. Five water samples were also collected for environmental DNA (eDNA) analysis. The environmental characteristics of each site were obtained by deploying temperature data loggers and through an environmental risk assessment.
Results
Community patterns observed from the PhQd and bulk DNA datasets revealed a clear separation of two sites within Sharma lagoon from the remaining sites. The eDNA analysis of seawater confirmed these spatial differences, also detecting a variation between sampling times that was not observed with the other approaches. A total of 20 NIS and 18 cryptogenic species were recorded, from which 12 were identified morphologically and the remaining detected with molecular methods only. The generally low NIS coverage confirms that the NEOM region is less affected by marine biological invasions compared to other anthropized habitats within the Red Sea. However, sites in the Sharma lagoon showed high human pressure levels and comparatively higher coverage of cryptogenic bryozoans on panels.
Discussion
This study provides the first detailed assessment of biofouling communities in NEOM, establishing a baseline and contributing to a regional species reference library for non-indigenous and cryptogenic species. As coastal development spreads, it presents both challenges and opportunities, highlighting the need for sustainable, ecosystem-based approaches to protect valuable natural areas. This baseline is essential for future monitoring of biofouling dynamics as the region develops.
... However, in marine ecosystems there have been an increasing number of cases of species belonging to various taxa dispersing from higher and/or lower latitudes into warmer waters (Lima et al. 2007;Chang et al. 2020). Among invertebrates, for example, the copepods Paracartia latisetosa (Kriczaguin, 1873) and Acartia (Acartiura) clausi (Giesbrecht, 1889), the giant squid Dosidicus gigas (d'Orbigny, 1835), the sea slug Chelidonura fulvipunctata (Baba, 1938), the cushion star Parvulastra exigua (Lamarck, 1816), and the ascidians Ciona robusta (Hoshino & Tokioka, 1967) and Corella inflata (Huntsman, 1912), are currently being recorded in warmer regions than those previously known (Belmonte and Potenza 2001;Malaquias et al. 2016;Shenkar et al. 2017;Chang et al. 2020;Pinsky et al. 2020). In addition, various species of fish, including the spotted seabass Dicentrarchus punctatus, the meagre Argyrosomus regius (Asso, 1801), the golden grey mullet Chelon auratus (Risso, 1810), as well as the giant goby Gobius cobitis Pallas, 1814, and the rock goby G. paganellus Linnaeus, 1758, have been found to disperse into the northern part of the Red Sea from the Mediterranean Sea (Tiralongo et al. 2021). ...
The number of species dispersing to higher and/or lower latitudes, in association with temperature warming, is growing exponentially with only a few described opposite cases of dispersal to warmer regions. Here we describe the dispersal of the solitary ascidian Ascidia virginea, considered native to the seas of North Europe, to disperse to warmer regions: the Eastern Mediterranean and a Red Sea marina. This case highlights an emerging trend of taxa being introduced by marine vessels and successfully establishing populations in unfavourable environmental conditions by opportunistically utilizing niche areas. We provide molecular and morphological data that facilitate the identification of A. virginea in regions in which it may have previously been overlooked. We also employ ecological-niche modeling to project habitat suitability for this species, predicting the coasts of North America, South America, the northwest Pacific, and the Red Sea as moderately and highly suitable habitats. Phylogenetic analyses based on the mitochondrial COI gene reveal that the A. virginea sequences obtained in this work belong to a well-supported clade, including previously published sequences of A. virginea from California and Florida, localities where its presence was not predicted by our model. Furthermore, publicly available COI sequences of A. malaca and A. sydneiensis are assigned to the same A. virginea clade, implying a case of synonymy or misidentification. Our results provide useful data for the accurate identification of this species when expanding into other areas in which it may become a nuisance, and highlight the need to further explore the potential of cold-water species to establish in ports and niche areas in warmer regions.
... Recently C. africana has been reported in the Adriatic Sea (Turk and Furlan 2011 Biuve fulvipunctata was originally described from Kii Peninsula, Japan (Baba 1938), and is currently widespread in the Indo-Pacific Ocean (Gosliner 1987, Gosliner et al. 2015. The sequence of Mediterranean findings of B. fulvipunctata was first reconstructed and updated by Malaquias et al. (2016b) and more recently by Lombardo and Marletta (2020b). The first and to date only one finding in the Adriatic Sea took place in 2018 (Petani and Crocetta 2019). ...
... Regarding the Atlantic area, within June and October 2016, many B. fulvipunctata individuals were found in six different localities of the Canary Islands expanding the distribution range of this species to NE Atlantic Ocean (Herrero- Barrencua et al. 2016). In the same year and before the publication of these last findings, a controversy arose regarding the possible anti-Lessepsian migration of the species from the Mediterranean Sea to the Red Sea (Malaquias et al. 2016b;Galil et al. 2016). However, understanding the dispersal pathway of a species is a challenging field of research which cannot be separated from a massive sampling effort throughout the geographic range of the species and possibly corroborated by a haplotype network analysis. ...
During underwater monitoring, one specimen of Camachoaglaja africana and one of Biuve fulvipunctata were found at the ‘Tavolara Punta Coda Cavallo’ Marine Protected Area, allowing to expand the known Mediterranean range of distribution of these two species. The finding of both species constitutes the first report for NE Sardinia and the whole Tyrrhenian Sea. By coupling data obtained from the analysis of social media and those present in the bibliography it was also possible to speculate on alternative pattern of distribution of these two species at a global scale. Finally, it is also confirmed the importance of repeated monitoring activities over time on the mooring buoys which act as steppingstone habitats for epifauna or for larval settlement and that are capable to provide important additional information on local biodiversity.
... Native and widely distributed in the Indo-West Pacific, B. fulvipunctata was first recorded as an alien species in the Mediterranean Sea in 1959. Soon after its first record in Turkey, it colonized almost the entire basin, with subsequent records in both the easternmost parts (Israel, Cyprus) and in central (Malta, Italy) and western parts (France, Spain) (review in Malaquias et al., 2016). However, no records of this taxon were known from the Adriatic Sea. ...
The Collective Article on "New Mediterranean Biodiversity Records" offers the means to publish biodiversity records in the Med-iterranean Sea. The current article presents new biodiversity data information on 18 taxa (14 alien, 3 native and 1 cryptogenic species) belonging to 5 Phyla that are reported for 11 different countries listed according to their geographic position from the western to the eastern Mediterranean Sea. Algeria: the alien green alga Caulerpa taxifolia var. distichophylla and the heterobranchs Aplysia dacty-lomeda and Aplysia punctata are first reported from the entire country. France: a new record of the alien hydroid Porpita porpita is reported from the Corsican Sea, representing the second record of the species in the western Mediterranean Sea. Tunisia: the alien fish Scatophagus argus is reported from the Gulf of Gabès, probably representing an aquarium release. Italy: the well-established Mediterranean alien bivalve Malleus regula is first reported from the entire country. Slovenia: the alien marine bivalve Xenostrobus securis is reported for the first time from the entire country. Croatia: the alien gastropod Biuve fulvipunctata is reported for the first time from the country but also from the entire Adriatic Sea. Montenegro: the alien bivalve Rapana venosa is reported for the first time from the Montenegrin waters. Albania: the well-established alien fish Lagocephalus sceleratus and the rare native shark Rhizoprionodon acutus are reported for the first from the entire country. Greece: the rare native ray Leucoraja circularis is reported for the first time from the Argolikos Gulf and for the first time for the entire country its identification is confirmed morphologically and molecularly; additional records of the alien nomad jellyfish Rhopilema nomadic document its expanding distribution, while the occurrence and the alien fishes Sillago suezensis and Pomadasys stridens are reported for the first time from Hellenic waters. Turkey: additional records of the Egyptian Prawn Metapenaeopsis aegyptia are reported with some biological information. Cyprus: the alien fish Variola louti is reported for the first time for the entire Mediterranean Sea, probably released from an aquarium, while the alien moon crab Matuta victor is reported for the first time from the entire country.
... Native and widely distributed in the Indo-West Pacific, B. fulvipunctata was first recorded as an alien species in the Mediterranean Sea in 1959. Soon after its first record in Turkey, it colonized almost the entire basin, with subsequent records in both the easternmost parts (Israel, Cyprus) and in central (Malta, Italy) and western parts (France, Spain) (review in Malaquias et al., 2016). However, no records of this taxon were known from the Adriatic Sea. ...
The Collective Article on “New Mediterranean Biodiversity Records” offers the means to publish biodiversity records in the Mediterranean
Sea. The current article presents new biodiversity data information on 18 taxa (14 alien, 3 native and 1 cryptogenic species)
belonging to 5 Phyla that are reported for 11 different countries listed according to their geographic position from the western to the
eastern Mediterranean Sea. Algeria: the alien green alga Caulerpa taxifolia var. distichophylla and the heterobranchs Aplysia dactylomeda
and Aplysia punctata are first reported from the entire country. France: a new record of the alien hydroid Porpita porpita is
reported from the Corsican Sea, representing the second record of the species in the western Mediterranean Sea. Tunisia: the alien
fish Scatophagus argus is reported from the Gulf of Gabès, probably representing an aquarium release. Italy: the well-established
Mediterranean alien bivalve Malleus regula is first reported from the entire country. Slovenia: the alien marine bivalve Xenostrobus
securis is reported for the first time from the entire country. Croatia: the alien gastropod Biuve fulvipunctata is reported for the
first time from the country but also from the entire Adriatic Sea. Montenegro: the alien bivalve Rapana venosa is reported for the
first time from the Montenegrin waters. Albania: the well-established alien fish Lagocephalus sceleratus and the rare native shark
Rhizoprionodon acutus are reported for the first from the entire country. Greece: the rare native ray Leucoraja circularis is reported
for the first time from the Argolikos Gulf and for the first time for the entire country its identification is confirmed morphologically
and molecularly; additional records of the alien nomad jellyfish Rhopilema nomadic document its expanding distribution, while the
occurrence and the alien fishes Sillago suezensis and Pomadasys stridens are reported for the first time from Hellenic waters. Turkey:
additional records of the Egyptian Prawn Metapenaeopsis aegyptia are reported with some biological information. Cyprus: the alien
fish Variola louti is reported for the first time for the entire Mediterranean Sea, probably released from an aquarium, while the alien
moon crab Matuta victor is reported for the first time from the entire country.
... Brachidontes pharaonis, a species of Indo-Pacific origin, was recorded for the first time in Italy from Vendicari (Siracusa, Sicily) (Di Geronimo, 1971). Among the latest findings, the gastropod Biuve fulvipunctata (described from the Indian Ocean and W Pacific) was reported from Lake Faro (Malaquias et al., 2016), where it has already formed self-sustaining populations. The first Mediterranean records include the alien limpet Lottia sp., whose native distribution is yet to be determined, found in 2015 in the Ionian Sea (Scuderi & Eernisse, 2016), with permanent populations already established in Catania harbour and nearby areas, and the circumtropical gastropod Syphonota geographica, found in 1999 in Reggio Calabria (Turano & Neto, 2001). ...
The re-examination of marine alien species or Non-indigenous species (NIS) reported in Italian Seas by December 2018, is here provided, particularly focusing on establishment success, year of first record, origin, potential invasiveness, and likely pathways. Furthermore, their distribution is assessed according to marine subregions outlined by the European Union (EU) Marine Strategy Framework Directive: Adriatic Sea (ADRIA), Ionian Sea and Central Mediterranean Sea (CMED), and Western Mediterranean Sea (WMED). In Italy, 265 NIS have been detected with the highest number of species being recorded in the CMED (154 species) and the WMED (151 species), followed by the ADRIA (143). Most of these species were recorded in more than one subregion. The NIS that have established stable populations in Italian Seas are 180 (68%), among which 26 have exhibited invasive traits.Among taxa involved, Macrophyta rank first with 65 taxa. Fifty-five of them are established in at least one subregion, mostly in the ADRIA and the CMED. Crustacea rank second with 48 taxa, followed by Polychaeta with 43 taxa, Mollusca with 29 taxa, and Pisces with 28 taxa, which were mainly reported from the CMED. In the period 2012-2017, 44 new alien species were recorded, resulting in approximately one new entry every two months. Approximately half of the NIS (~52%) recorded in Italy have most likely arrived through the transport-stowaway pathway related to shipping traffic (~28% as biofoulers, ~22% in ballast waters, and ~2% as hitchhikers). The second most common pathway is the unaided movement with currents (~19%), followed by the transport-contaminant on farmed shellfishes pathway (~18%). Unaided is the most common pathway for alien Fisshes, especially in CMED. Escapes from confinement account for ~3% and release in nature for ~2% of the NIS. The present NIS distribution hotspots for new introductions were defined on the first recipient area/location in Italy. In ADRIA the hotspot is Venice which accounts for the highest number of alien taxa introduced in Italy, with 50 newly recorded taxa. In the CMED, hotspots of introduction are the Taranto and Catania Gulfs, hosting 21 first records each. The Strait of Sicily represents a crossroad between the alien taxa from the Atlantic Ocean and the Indo-Pacific area. In the WMED, hotspots of bioinvasions include the Gulfs of Naples, Genoa and Livorno.This review can serve as an updated baseline for future coordination and harmonization of monitoring initiatives under international, EU and regional policies, for the compilation of new data from established monitoring programs, and for rapid assessment surveys.
... For example, more than 90 fishes have been introduced through the Lessepsian migration, a process of biological invasions from the Red Sea into the Mediterranean Sea [37][38][39]. However, only a handful of opposite-direction introductions from the Mediterranean to the Red Sea (anti-Lessepsian migration) have been recorded so far [40], mainly owing to harsh environmental conditions in the Red Sea, such as high salinity, high temperature and oligotrophic conditions [41,42]. For the Mediterranean C. robusta populations, the optimal temperature range was 14-23.4°C ...
... For newly established populations, gene flow and some events such as genetic bottleneck, genotype sorting and drift are likely to influence population genetic structure [46][47][48]. Given the increasing shipping activities, [16,41,49]. According to Shenkar et al. [35], mtDNA analyses of C. robusta samples from the same sampling site in 2015 suggested that the Red Sea population might be introduced from the Mediterranean Sea, where C. robusta were detected much earlier in the end of nineteenth century [31,44]. ...
Background: Adaptive evolution is one of the crucial mechanisms for organisms to survive and thrive in new environments. Recent studies suggest that adaptive evolution could rapidly occur in species to respond to novel environments or environmental challenges during range expansions. However, for environmental adaptation, many studies successfully detected phenotypic features associated with local environments, but did not provide ample genetic evidence on microevolutionary dynamics. It is therefore crucial to thoroughly investigate the genetic basis of rapid microevolution in response to environmental changes, in particular on what genes and associated variation are responsible for environmental challenges. Here, we genotyped genome-wide gene-associated microsatellites to detect genetic signatures of rapid microevolution of a marine tunicate invader, Ciona robusta, during recent range expansion to the harsh environment in the Red Sea.
Results: The Red Sea population was significantly differentiated from the other global populations. The genome-wide scan, as well as multiple analytical methods, successfully identified a set of adaptive genes. Interestingly, the allele frequency largely varied at several adaptive loci in the Red Sea population, and we found significant correlations between allele frequency and local environmental factors at these adaptive loci. Furthermore, a set of genes were annotated to get involved in local temperature and salinity adaptation, and the identified adaptive genes may largely contribute to the invasion success to harsh environments.
Conclusions: All the evidence obtained in this study clearly showed that environment-driven selection had left detectable signatures in the genome of Ciona robusta within a few generations. Such a rapid microevolutionary process is largely responsible for the harsh environmental adaptation and therefore contributes to invasion success in different aquatic ecosystems with largely varied environmental factors.
... This is particularly relevant at a time when the number of alien species reported in the Mediterranean Sea has been growing significantly, namely those migrating from the Red Sea, but also arriving via mariculture and shipping activities (e.g. Crocetta and Vazzana 2009;Malaquias et al. 2016;Micali et al. 2016). Therefore, caution is recommended when identifying Mediterranean species of the genus Atys based on shells alone. ...
Atys jeffreysi is a heterobranch Cephalaspidea gastropod belonging to the family Haminoeidae occurring in the Mediterranean Sea, Madeira and Canary archipelagos. Nearly nothing is known about the internal anatomical features of this species. In this paper we redescribe the species A. jeffreysi based on fine anatomical work and scanning electron microscopy. DNA barcodes are provided for the first time for A. jeffreysi and A. macandrewii, the only two species of the genus native in the Mediterranean Sea. The genetic distance (COI uncorrected p-distance) between them is estimate at 21.6%. A Bayesian molecular phylogeny based on the gene marker cytochrome c oxidase subunit I (COI) including all sequences available of the genera Aliculastrum, Liloa and Atys species did not support a sister relationship between the two Mediterranean species and suggests that they are more closely related to distinct Indo-West Pacific lineages. The complex systematics of the genus Atys is briefly discussed.
... The Red Sea is typically regarded as a source of introduced fauna into the Mediterranean (Zenetos et al. 2012). However, oppositedirection introductions of fish and molluscs have also been recorded in the past (Goren and Klausewitz 1978;Golani and Bogorodsky 2010;Malaquias et al. 2016). The rapid expansion of maritime traffic via the Suez Canal increases the opportunities of opportunistic fouling organisms such as ascidians to establish populations in tropical regions. ...
... The rapid expansion of maritime traffic via the Suez Canal increases the opportunities of opportunistic fouling organisms such as ascidians to establish populations in tropical regions. As suggested by Malaquias et al. (2016), the Suez Canal may become a Brevolving door^, allowing not only organisms of Indo-Pacific origin to enter the Mediterranean but also allowing species established in the Mediterranean and resilient to tropical/subtropical environmental conditions to move into the Red Sea. Aside from potential damage as a fouling species within the marina, following a catastrophe in the coral reef adjacent to the Eilat marina, opportunistic species such as C. robusta could further contribute to habitat destruction by competing for space with reef-building corals, emphasizing the need to monitor its current status there, and to apply active management tools to control its population. ...
The solitary ascidian Ciona intestinalis is among the most damaging of invasive fouling species in the world. It is mostly known from cold-water or temperate environments, where it is able to form dense aggregations. We present the first record of C. intestinalis type-A, now recognized as C. robusta, from the Eilat marina, Israeli Red Sea coast. Several individuals found fouling the bottom of the floating docks in March 2015 were identified using both mitochondrial sequencing and morphological tools. Periodical surveys revealed some of them with full gonoducts, and small individuals appeared two months later, indicating a reproductive population. The extremely high salinity and temperature at the Eilat marina indicates the wide environmental tolerance of this species. Since the only other report from this region dates to 100 years ago, from a dredging vessel at the entrance to the Suez Canal, and it has not since been recorded from any natural substrates in the region, it should be considered a non-indigenous species in the Red Sea.
... Another example invoked by the authors is the colorful cephalaspid Haminoea cyanomarginata Heller and Thompson, 1983Thompson, described in 1983 from the Sudanese coast in the central part of the Red Sea (Heller and Thompson 1983) and reported later in the northern part of this basin at least seven times (Lederman 2005b, c, d;Koretz andKoretz 2005, 2006), therefore spread over a vast area of the Red Sea and known to be present in the Mediterranean since 2004 (Yokeş and Rudman 2004). It is difficult to understand how can this compare with the case of C. fulvipunctata, a species described from Japan (Baba 1938), and as mentioned earlier, widely distributed in the Indo-West Pacific and also in the Mediterranean Sea where it was first reported in 1961 (Swennen 1961;Malaquias et al. 2016), and yet only observed in the Red Sea twice during 2005 on the northernmost part of the realm (Gulf of Aqaba). Galil et al. (2016; point A of the Letter) have apparently misinterpreted the goal of our molecular phylogenetic analysis, which never intended to support or refute the Mediterranean origin of the Red Sea specimens of C. fulvipunctata, but only to yield evidence for the conspecificity of the Mediterranean and Indo-West Pacific specimens. ...
In this reply, we address the criticism directed recently to our work (Malaquias et al. 2016) by Galil et al. (2016) dismissing the hypothesis that the Suez Canal can act as a revolving door allowing marine species to move both ways between the Red Sea and the Mediterranean Sea. We reiterate that the presence in the Red Sea of the Indo-West Pacific sea slug Chelidonura fulvipunctata Baba, 1938 is most parsimoniously explained by an invasion from the Mediterranean and highlight several recent studies combing morphology and molecular phylogenetics where established views about the presence of alien Indo-Pacific / Red Sea species in the Mediterranean were proven wrong. Caution is suggested when assuming the conspecificity of species between these realms based solely on external features.
