Population dynamics and life cycle of the introduced ascidian Microcosmus squamiger in the Mediterranean Sea

Marine introductions are a serious threat for biodiversity, especially in seas where shipping is intensive. Microcosmus squamiger is a widespread marine invader that can alter native biota and it is therefore imperative to understand its biology and ecology. We studied the population dynamics and reproductive cycles of M. squamiger over a 2-year period, as well as its settlement and colonization patterns, in a north-western Mediterranean (NE Spain) locality where M. squamiger has been introduced. All biological parameters showed a strong seasonal pattern that peaked in summer with a major spawning episode at the end of summer. Size-frequency histograms indicated a 2-year cycle. Colonization experiments suggested that M. squamiger recruitment mortality is high and requires a well structured community. In addition, we monitored the abundance of the native predator Thais haemastoma, which showed a significant positive correlation with M. squamiger biomass, indicating its potential usefulness as a biological control.     

Phylogeography of the widespread marine invader Microcosmus squamiger (Ascidiacea) reveals high genetic diversity of introduced populations and non-independent colonizations

The spread of non-indigenous species into new marine habitats represents an increasing threat to global diversity. Genetic techniques provide basic understanding of the invasion processes. The ascidian Microcosmus squamiger is considered to be native to Australia, having been spread worldwide via transoceanic vessels. It has successfully invaded artificial and natural habitats where it has become a pest. We studied phylogeography and genetic structure of 12 M. squamiger populations, including samples from its native range (Australia) and introduced populations from the Indian, Pacific, and Atlantic oceans, as well as the Mediterranean Sea. We amplified 574 bp of the mitochondrial COI gene in 258 individuals and found a total of 52 haplotypes. A haplotype tree revealed two main groups of haplotypes. The relative frequency of each group of haplotypes, multidimensional scaling, and analysis of molecular variance showed important differences between the western Australia localities and the remaining ones (eastern Australia and introduced populations). Furthermore, we found that the colonization of the different areas by M. squamiger has not occurred independently, as many introduced populations shared some low frequency alleles. A nested clade analysis showed a global pattern of restricted gene flow with isolation by distance, although we found episodes of long-distance dispersal in some clades. A contiguous range expansion was detected between Australian populations. We conclude that M. squamiger is native to Australia and has most likely expanded its range of distribution sequentially through worldwide shipping, especially from the harbours of the more populated eastern Australia. In introduced populations, we found a high genetic diversity which suggests enhanced invasive potential. Consequently, there is a need to control this species, as it outcompetes local biota and is an economic threat.     

Invasion Pathway of the Ctenophore Mnemiopsis leidyi in the Mediterranean Sea

Gelatinous zooplankton outbreaks have increased globally owing to a number of human-mediated factors, including food web alterations and species introductions. The invasive ctenophore Mnemiopsis leidyi entered the Black Sea in the early 1980s. The invasion was followed by the Azov, Caspian, Baltic and North Seas, and, most recently, the Mediterranean Sea. Previous studies identified two distinct invasion pathways of M. leidyi from its native range in the western Atlantic Ocean to Eurasia. However, the source of newly established populations in the Mediterranean Sea remains unclear. Here we build upon our previous study and investigate sequence variation in both mitochondrial (Cytochrome c Oxidase subunit I) and nuclear (Internal Transcribed Spacer) markers in M. leidyi, encompassing five native and 11 introduced populations, including four from the Mediterranean Sea. Extant genetic diversity in Mediterranean populations (n = 8, N _a = 10) preclude the occurrence of a severe genetic bottleneck or founder effects in the initial colonizing population. Our mitochondrial and nuclear marker surveys revealed two possible pathways of introduction into Mediterranean Sea. In total, 17 haplotypes and 18 alleles were recovered from all surveyed populations. Haplotype and allelic diversity of Mediterranean populations were comparable to populations from which they were likely drawn. The distribution of genetic diversity and pattern of genetic differentiation suggest initial colonization of the Mediterranean from the Black-Azov Seas (pairwise F _ST = 0.001–0.028). However, some haplotypes and alleles from the Mediterranean Sea were not detected from the well-sampled Black Sea, although they were found in Gulf of Mexico populations that were also genetically similar to those in the Mediterranean Sea (pairwise F _ST = 0.010–0.032), raising the possibility of multiple invasion sources. Multiple introductions from a combination of Black Sea and native region sources could be facilitated by intense local and transcontinental shipping activity, respectively.     

Grateloupia turuturu (Halymeniaceae,Rhodophyta) is the correct name of the non-native species in the Atlantic known as Grateloupia doryphora

Grateloupia doryphora (Montagne) Howe, originally described from Peru, has repeatedly been reported as an invasive species in Atlantic and Mediterranean waters. Various attempts to explain this species' route of introduction have been unsatisfactory. New evidence from comparative rbcL sequence analysis and morphology suggests that this adventive species in the NE and NW Atlantic corresponds with G. turuturu Yamada, originally described from Japan. This provenance follows a well-recognized trend of invasive marine organisms that have colonized the Atlantic Ocean and Mediterranean Sea from Pacific NE Asia.     

REPORT OF A NEW INVASIVE ALGA IN THE ATLANTIC UNITED STATES: “HETEROSIPHONIA” JAPONICA IN RHODE ISLAND1

Recent collections of tetrasporangiate “Heterosiphonia” japonica Yendo from Watch Hill to Point Judith, Rhode Island, represent the first report of this nonnative alga in the western Atlantic. Native to the Pacific Ocean, this species was unintentionally introduced into European waters by 1984 and has subsequently invaded the eastern Atlantic Ocean widely from France to Norway and south into the Mediterranean Sea. Thus far, all western Atlantic collections of this species are confined to the outer coast of Rhode Island, and at present are not found in Narragansett Bay or in Long Island Sound along the Connecticut coast. Molecular and morphological studies confirm the identity of this newly introduced invasive species.     

Sensory Structures in Tadpole Larvae of the Ascidians Microcosmus exasperatus Heller and Herdmania momus (Savigny)

In this paper we describe the larval morphology of two species from the ascidian family Pyuridae, Microcosmus exasperatus and Herdmania momus, with special emphasis on components of the cerebral vesicle. Larvae have not previously been described for any species in the large genus Microcosmus. Besides a difference in size (larvae of H. momus are about 40% larger than those of M. exasperatus), larvae of the two species differ primarily in the number and arrangement of sensory structures. Both species possess a well-developed statocyte but only H. momus has an ocellus. The absence of an ocellus in M. exasperatus is unique among pyurid ascidians. An auxiliary vesicle was found situated on the left side of the cerebral vesicle in both species. However, unlike the larvae of H. momus and other pyurid species, there is no apparent communication between the auxiliary and cerebral vesicles of M. exasperatus. Epithelial cells in the auxiliary vesicles of both species carry modified cilia about 2 μm in diameter; auxiliary vesicles of H. momus also have simple cilia with axonemes in a 9 + 0 microtubule configuration. In H. momus the membranes of the epithelial cells are highly convoluted and extend into the lumen of the auxiliary vesicle. Morphological arrangements of auxiliary vesicles and globular cilia reported so far in ascidian tadpoles are contrasted and discussed.     

Phylogenetic analysis of the north‐east Atlantic and Mediterranean species of the genus Stenosoma (Isopoda,Valvifera, Idoteidae)

Xavier, R., Santos, A. M., Harris, D. J., Sezgin, M., Machado, M., Branco, M. (2012). Phylogenetic analysis of the north‐east Atlantic and Mediterranean species of the genus Stenosoma (Isopoda, Valvifera, Idoteidae). —Zoologica Scripta, 41, 386–399. The marine isopod genus Stenosoma is widespread in the northern hemisphere. However, 12 of its 14 known species are found within the Mediterranean basin and adjacent regions of the north‐east Atlantic and the Black Sea. Such a high level of diversity confined to a limited region of a much larger circumglobal distribution suggests that the Mediterranean region may have played a crucial role in the evolutionary history of this genus. In the present work, the phylogeny of the genus Stenosoma was investigated on the basis of DNA sequencing data from one nuclear (28SrRNA) and two mitochondrial (COI, ND4) gene fragments obtained for nine of 12 Atlantic–Mediterranean species. Divergence time estimates point to a Tethyan origin of Stenosoma and suggest that the speciation events from which stem most of the extant species took place well before the Messinian Salinity Crisis. Stenosoma spinosum and Stenosoma appendiculatum are the only exceptions, as they apparently arose within the Mediterranean during the Pleistocene. Phylogenetic reconstruction agrees with current taxonomic status of most species. However, Stenosoma capito clustered in two distinct and well‐supported clades, one composed of eastern Mediterranean and Black Sea specimens and the other by western Mediterranean and Atlantic ones. Such polyphyly suggests the existence of a previously unrecognized species, Stenosoma sp., which so far has been confounded with S. capito.     

Tracing the introduction history of the invasive swimming crab <Emphasis Type="Italic">Charybdis hellerii</Emphasis> (A. Milne-Edwards, 1867) in the Western Atlantic: evidences of high genetic diversity and multiple introductions

The swimming crab Charybdis hellerii is an invader with global distribution in warm waters. Native to the Indo-Pacific, this species invaded the eastern Mediterranean Sea after the Suez Canal opening. In 1987, it was first reported in the Western Atlantic, probably transported via ballast water of ships. Since then, it has been registered from many localities along the American coast from the USA to southern Brazil where it has rapidly established reproducing populations. Our main aim was to investigate the introduction history of this species along the American coast, using a phylogeographic approach. Additionally, we attempted to clarify the identity of this invasive species by molecular analyses and morphological assessment in order to provide a basis for our main investigation. C. hellerii was confirmed as a single species, but both cytochrome c oxidase subunit I and 16S rDNA revealed a genetic structure, splitting the potential source populations of American introductions into two groups: “western Indian Ocean and Mediterranean Sea” (WIO + MS) versus “eastern Indian + western Pacific oceans” (EIO + WPO). Most specimens from America clustered with the former group, supporting the hypothesis that the Mediterranean Sea represented the main source of Western Atlantic populations. However, the clustering of animals from southern Brazil with the latter group indicates that introductions from the eastern Indian or Pacific oceans must also have occurred. The existence of a third group, found exclusively within the American range and genetically related to EIO + WPO, also indicates an independent introduction from an unsampled locality from the native range. The haplotype and nucleotide diversities of American localities were comparable to those of source populations, contradicting a founder effect prediction. This finding might be related to the high propagule pressure associated with introductions via ballast water and the occurrence of multiple introductions from genetic distinct sources. The direct comparison of the haplotype numbers suggested no genetic bottleneck during introduction from the Mediterranean Sea, but a bottleneck might have occurred during introductions from the eastern Indian or Pacific oceans.     

Redescription of Fabriciola tonerella Banse, 1959, and a new record of Novafabricia infratorquata (Fitzhugh, 1983) from the Mediterranean Sea, with a key for the Fabriciinae (Annelida: Polychaeta) of the Mediterranean Sea and the north-east Atlantic

The fabriciin sabellid species Fabriciola tonerella Banse, 1959 living on gastropod shells inhabited by hermit crabs collected in the western Mediterranean Sea is redescribed. Another species of Fabriciinae, Novafabricia infratorquata (Fitzhugh, 1983), is recorded for the first time from the Mediterranean Sea and found in the same habitat is described as well. The variability of characters depending on size and geographical distribution is given for both species. Moreover, selected characters for all known species of Fabriciola and Novafabricia as well as a simple key for all Fabriciinae of the Mediterranean Sea and the north-east Atlantic are provided.     

Fortes différences des ADN mitochonclriaux de populations de Sardinella aurita de la mer Méditerranée et de l'Atlantique Est

Digestion by restriction enzymes has been carried out on polymerase chain reaction products of the mitochondrial DNA control region of round sardine (Sardinella aurita) samples coming from the Eastern Atlantic and the Mediterranean Sea. The results show i) that, though the habitat is continuous, there is no gene flow between the two basins where two genetically differentiated groups can be recognized, ii) that each basin is genetically homogeneous and, iii) that the haplotypic diversity in the Mediterranean is between two and three times smaller than that observed in the Atlantic. These results can hardly be explained by a recent colonization from the Eastern Atlantic. This suggests that, for S. aurita and some other species, the Mediterranean Sea is genetically little influenced by the Eastern Atlantic.     

Fickle or Faithful: The Roles of Host and Environmental Context in Determining Symbiont Composition in Two Bathymodioline Mussels

The Mediterranean Sea and adjoining East Atlantic Ocean host a diverse array of small-sized mussels that predominantly live on sunken, decomposing organic remains. At least two of these, Idas modiolaeformis and Idas simpsoni, are known to engage in gill-associated symbioses; however, the composition, diversity and variability of these symbioses with changing habitat and location is poorly defined. The current study presents bacterial symbiont assemblage data, derived from 454 pyrosequencing carried out on replicate specimens of these two host species, collected across seven sample sites found in three oceanographic regions in the Mediterranean and East Atlantic. The presence of several bacterial OTUs in both the Mediterranean Sea and eastern Atlantic suggests that similar symbiont candidates occur on both sides of the Strait of Gibraltar. The results reveal markedly different symbiotic modes in the two species. Idas modiolaeformis displays high symbiont diversity and flexibility, with strong variation in symbiont composition from the East Mediterranean to the East Atlantic. Idas simpsoni displays low symbiont diversity but high symbiont fidelity, with a single dominant OTU occurring in all specimens analysed. These differences are argued to be a function of the host species, where subtle differences in host evolution, life-history and behaviour could partially explain the observed patterns. The variability in symbiont compositions, particularly in Idas modiolaeformis, is thought to be a function of the nature, context and location of the habitat from which symbiont candidates are sourced.     

Occurrence of Diopatra marocensis (Annelida,Onuphidae) in the eastern Mediterranean

The present study deals with the presence of Diopatra marocensis in the eastern Mediterranean. This species is small-sized and inhabited muddy bottom near the opening of rivers or lagoons [salinity range: 33−39‰] in the Aegean and Levantine Seas, and reached a maximum density of 90 ind.m^-2 in Mersin Bay. This species might be an alien species that was introduced from the East Atlantic (near Gibraltar) to the eastern Mediterranean via ballast water of ships, as it has never been reported from the western Mediterranean Sea.     

Habitat utilization by an invasive herbivorous fish (<Emphasis Type="Italic">Siganus rivulatus</Emphasis>) in its native and invaded range

Movement is essential for understanding the distribution and abundance of animals. While it has been suggested that invasion success can be facilitated by species’ ability to adapt to novel environments, direct comparisons of movement patterns between native and invaded ranges of animals in their natural habitat are rare. The rivulated rabbitfish Siganus rivulatus was introduced from the Red Sea into the Mediterranean, where it is now found in extremely high abundances, and has overgrazed the coastal marine ecosystem in many locations. Through a continuous acoustic tracking system, we found that the movement of S. rivulatus individuals at a Mediterranean site differed substantially from those at a Red Sea site, with individuals in the Mediterranean having larger overall home ranges and lower site fidelity. However, no variation between sites was found in daily home range sizes. Results show that at the Mediterranean site S. rivulatus individuals have a larger spatial footprint, which may contribute to their impact and ability to expand their distribution. This study demonstrates a potential shift in individual movement of a marine invasive species between its native and invaded range, and highlights the role of movement in understanding biological invasions.     

Conservation genetics of the short-beaked common dolphin (<Emphasis Type="Italic">Delphinus delphis</Emphasis>) in the Mediterranean Sea and in the eastern North Atlantic Ocean

Mediterranean Sea common dolphins have recently been listed as ‘endangered’ in the IUCN Red list, due to their reported decline since the middle of the 20th century. However, little is know about the number or distribution of populations in this region. We analysed 118 samples from the Black Sea, Mediterranean Sea and eastern North Atlantic at nine microsatellite nuclear loci and for 428 bps of the mtDNA control region. We found small but significant population differentiation across the basin between the eastern and the western Mediterranean populations at both nuclear and mtDNA markers (microsatellite F _ST = 0.052, mtDNA F _ST = 0.107, P values ≤ 0.001). This matched the differential distribution and habitat use patterns exhibited by this species in the eastern and the western parts of the Mediterranean Sea. The assignment test of a small number of samples from the central Mediterranean could not exclude further population structure in the central area of the basin. No significant genetic differentiation at either marker was observed among the eastern north Atlantic populations, though the Alboran population (inhabiting the Mediterranean waters immediately adjacent the Atlantic ocean) showed significant mtDNA genetic differentiation compared to the Atlantic populations. Directional estimates of gene flow suggested movement of females out of the Mediterranean, which may be relevant to the population decline. Phylogenetic analysis suggested that the observed population structure evolved recently.     

An integrative systematic approach to species diversity and distribution in the genus Mesophyllum (Corallinales,Rhodophyta) in Atlantic and Mediterranean Europe

For the first time, a comprehensive assessment of Mesophyllum species diversity and their distribution in Atlantic Europe and the Mediterranean Sea is presented based on molecular (COI-5P, psbA) and morphological data. The distribution ranges were redefined for the four species collected in this study: M. alternans, M. expansum, M. macroblastum and M. sphaericum. Mesophyllum sphaericum, which was previously known only from a single maerl bed in Galicia (NW Spain), is reported from the Mediterranean Sea. The known range of M. expansum (Mediterranean and Macaronesia) was extended to the Atlantic Iberian Peninsula. The occurrence of M. alternans was confirmed along the Atlantic French coast south to Algarve (southern Portugal). Mesophyllum lichenoides was only recorded from the Atlantic, whereas M. macroblastum appears to be restricted to the Mediterranean Sea. A positive correlation was observed between maximum Sea Surface Temperature (SSTmax) and the depth at which M. expansum was collected, suggesting that this species may compensate for higher SST by growing in deeper habitats where the temperature is lower. The latter indicates that geographic shifts in the distribution of coastal species as a result of global warming can possibly be mitigated by changes in the depth profile at which these species occur. Mesophyllum expansum, an important builder of Mediterranean coralligenous habitats, may be a good target species to assess its response to climate change.     

Marine mites (Halacaroidea: Acari): a geographical and ecological survey

Halacarid mites (Acari), with almost 700 species described, inhabit marine and freshwater habitats. The majority of genera are recorded from at least two ocean basins or continents. There is no evidence of endemic genera, in either littoral faunal provinces or in deep-sea regions. Copidognathus, a genus comprising 1/4 of all species described, is found in almost all geographic regions, depths and habitats. Other genera dominate or are restricted to cold waters, to warm waters or to distinct habitats.Corresponding habitats on either side of the boreal Atlantic Ocean harbour congeneric, identical, sibling or morphologically similar species. The fauna in the western Atlantic is less diverse than that in the eastern. Amphiatlantics are restricted to certain genera. Transatlantic distribution is independent of the niche inhabited.Of the marine halacarid species recorded from the boreal western Atlantic, 41% are amphiatlantics, while only one species is recorded from both the Caribbean and the Mediterranean. The Caribbean and the Mediterranean faunas are dominated by genera in which amphiatlantics are unknown.Most of the Black Sea species of the genus Halacarellus also occur in the Baltic, North Sea or North Atlantic, whereas the Copidognathus fauna of the Black Sea is similar to that of the Mediterranean.Halacarids are thought to be an ancient taxon, with most genera probably having been present since the Mesozoic and with several species having an age of at least 50 million years. Evidence for their antiquity is found in the distributional pattern of marine and limnic genera and species, in the lack of endemic genera despite low fecundity and lack of dispersal stages, and in the fact that amphiatlantics are restricted to certain genera without relationships to the niches inhabited.     

Non-lethal effects of an invasive species in the marine environment: the importance of early life-history stages

Studies examining the effects of invasive species have focussed traditionally on the direct/lethal effects of the invasive on the native community but there is a growing recognition that invasive species may also have non-lethal effects. In terrestrial systems, non-lethal effects of invasive species can disrupt early life-history phases (such as fertilisation, dispersal and subsequent establishment) of native species, but in the marine environment most studies focus on adult rather than early life-history stages. Here, we examine the potential for an introduced sessile marine invertebrate (Styela plicata) to exert both lethal and non-lethal effects on a native species (Microcosmus squamiger) across multiple early life-history stages. We determined whether sperm from the invasive species interfered with the fertilisation of eggs from the native species and found no effect. However, we did find strong effects of the invasive species on the post-fertilisation performance of the native species. The invasive species inhibited the settlement of native larvae and, in the field, the presence of the invasive species was associated with a ten-fold increase in the post-settlement mortality of the native species, as well as an initial reduction of growth in the native. Our results suggest that larvae of the native species avoid settling near the invasive species due to reduced post-settlement survival in its presence. Overall, we found that invasive species can have complex and pervasive effects (both lethal and non-lethal) across the early life-history stages of the native species, which are likely to result in its displacement and to facilitate further invasion.     

Diagnostic features and taxonomy of the Mediterranean species of the big-scale sand smelts belonging to <Emphasis Type="Italic">Atherina boyeri</Emphasis> group (Atherinidae)

Morphological studies of the big-scale sand smelt from the group Atherina boyeri sensu lato were carried out using the materials of the museum collections from the Mediterranean Sea, the Black Sea, and the Sea of Azov. It has been shown that low-raker sand smelt belonging to the species A. boyeri sensu stricto, and multi-raker sand smelt, referred to the A. mochon species, are differentiated by a complex of morphological features: the number of gill rakers, the shape of scales, the length of the ascending process of praemaxillare, and the shape of the lower margin of maxillare. The key for their identification is presented. It is assumed that A. mochon is not a native Black Sea species but belongs to the invasive species originating from the Mediterranean Sea. The isolation of two cryptic species is discussed. The neotype of A. pontica is designated.     

Genetic validation of the unexpected presence of a tropical tuna,bigeye tuna (Thunnus obesus), in the Mediterranean

Bigeye tuna (Thunnus obesus, Lowe, 1839) is one of the eight recognized species of the genus Thunnus. It is considered a tropical species distributed in the Atlantic, Pacific and Indian Oceans. To date, no validated presence of this species has been reported inside the Mediterranean Sea. This study, however, confirms, for the first time, the presence of three young individuals of this species within the Mediterranean Sea.