Comparative phylogeography of meroplanktonic species, <Emphasis Type="Italic">Aurelia</Emphasis> spp. and <Emphasis Type="Italic">Rhizostoma pulmo</Emphasis> (Cnidaria: Scyphozoa) in European Seas

Mass occurrences of scypozoan medusae have become increasingly common in recent decades in European seas, including species in the genera Aurelia and Rhizostoma. We inferred the phylogeographic patterns of metagenetic scyphozoa Aurelia spp. and Rhizostoma pulmo from mitochondrial COI and nuclear ITS regions. No genetic structure was detected in R. pulmo over the Mediterranean Sea. By contrast, the phylogeographic analyses confirmed the separation of Aurelia spp. to several proposed cryptic species. Our results do not support the null hypothesis that both genera have concordant phylogeographic patterns. The resolvable parsimony network of haplotypes was retrieved for Aurelia aurita, Aurelia sp. 5, and Aurelia sp. 8 without connectivity between them and no genetic structure were found within those groups. Even though evidence of hybridization was found between A. aurita and Aurelia sp. 5, that did not break down the phylogenetic separation among them. The lowest haplotype and nucleotide diversity were found in samples of Aurelia sp. 8 and R. pulmo from the northern Adriatic, which acts as a sink area due to strong genetic drift. These new findings will facilitate linking the phenotype of the organism and its ability to survive in a particular environment—which shapes phylogeographic patterns.     

Genetic characterization of the scyphozoan jellyfish Aurelia spp. in Chinese coastal waters using mitochondrial markers

Blooms of the moon jellyfish Aurelia spp. have occurred in the harbors and coastal waters around the world. The phylogenetic relationship and genetic characterization of Aurelia spp. was determined along the Chinese coastal waters based on sequences of the mitochondrial cytochrome c oxidase subunit I (COI) gene. The molecular analysis confirmed that all samples collected in Chinese coastal waters were Aurelia sp.1. We also analyzed the phylogenetic and population genetic structure of Aurelia sp.1 using the newly generated sequences supplemented with existing data from previous studies. The phylogenetic analyses of the COI regions did not support geographically restricted groups among the global samples of Aurelia sp.1. Analysis of molecular variance (AMOVA) indicated a complex genetic population structure and pattern of connectivity. Populations of Aurelia sp.1 were highly structured between most sampling sites over distances as small as 100 km (Rizhao and Qingdao) in certain cases. However, non-significant pairwise F_ST values were also observed between short geographic distances (Yantai, Rongcheng and Qingdao) and relatively distant sampling sites (Caofeidian, Rizhao and Japan). The life-cycle characteristics, together with the prevailing ocean currents in this region and possible anthropogenic introduction, were proposed and discussed as the main factors that determined the genetic patterns of Aurelia sp.1.     

Temperature effects on asexual reproduction rates of scyphozoan species from the northwest Mediterranean Sea

In recent decades, many areas worldwide have experienced mass occurrences of jellyfish. To determine how temperature may affect jellyfish populations in the northwest (NW) Mediterranean Sea, we maintained polyps of three scyphozoan species, Aurelia aurita, Rhizostoma pulmo, and Cotylorhiza tuberculata in the laboratory at three temperatures (14, 21, 28°C) to test effects on survival and production of new polyps and ephyrae. Temperature significantly affected survival of all species, with longest survival of A. aurita and R. pulmo at 14°C and of C. tuberculata at 21°C. More polyps were budded by all species at temperatures above 14°C. A. aurita produced the most buds polyp⁻¹ (43.5) and R. pulmo the fewest (8.8). Strobilation occurred only at 14°C for A. aurita and at 21°C for C. tuberculata. For R. pulmo, fewer polyps strobilated and strobilated later at 14°C. These patterns of survival and asexual reproduction were seasonally appropriate for each species in the NW Mediterranean, where A. aurita medusae occur earliest (~April–May) in cool waters, followed by R. pulmo during May–June, and then by C. tuberculata in mid-summer. Comparisons among scyphozoan species suggested that many may be restricted by low temperatures, and that global warming may benefit temperate species, but not tropical or boreal species.     

Life Cycle Reversal in Aurelia sp.1 (Cnidaria,Scyphozoa)

The genus Aurelia is one of the major contributors to jellyfish blooms in coastal waters, possibly due in part to hydroclimatic and anthropogenic causes, as well as their highly adaptive reproductive traits. Despite the wide plasticity of cnidarian life cycles, especially those recognized in certain Hydroza species, the known modifications of Aurelia life history were mostly restricted to its polyp stage. In this study, we document the formation of polyps directly from the ectoderm of degenerating juvenile medusae, cell masses from medusa tissue fragments, and subumbrella of living medusae. This is the first evidence for back-transformation of sexually mature medusae into polyps in Aurelia sp.1. The resulting reconstruction of the schematic life cycle of Aurelia reveals the underestimated potential of life cycle reversal in scyphozoan medusae, with possible implications for biological and ecological studies.     

Local versus Generalized Phenotypes in Two Sympatric Aurelia Species: Understanding Jellyfish Ecology Using Genetics and Morphometrics

For individuals living in environmentally heterogeneous environments, a key component for adaptation and persistence is the extent of phenotypic differentiation in response to local environmental conditions. In order to determine the extent of environmentally induced morphological variation in a natural population distributed along environmental gradients, it is necessary to account for potential genetic differences contributing to morphological differentiation. In this study, we set out to quantify geographic morphological variation in the moon jellyfish Aurelia exposed at the extremes of a latitudinal environmental gradient in the Gulf of Mexico (GoM). We used morphological data based on 28 characters, and genetic data taken from mitochondrial cytochrome oxidase I (COI) and nuclear internal transcribed spacer 1 (ITS-1). Molecular analyses revealed the presence of two genetically distinct species of Aurelia co-occurring in the GoM: Aurelia sp. 9 and Aurelia c.f. sp. 2, named for its divergence from (for COI) and similarity to (for ITS-1) Aurelia sp. 2 (Brazil). Neither species exhibited significant population genetic structure between the Northern and the Southeastern Gulf of Mexico; however, they differed greatly in the degree of geographic morphological variation. The morphology of Aurelia sp. 9 exhibited ecophenotypic plasticity and varied significantly between locations, while morphology of Aurelia c.f. sp. 2 was geographically invariant (i.e., canalized). The plastic, generalist medusae of Aurelia sp. 9 are likely able to produce environmentally-induced, “optimal” phenotypes that confer high relative fitness in different environments. In contrast, the non-plastic generalist individuals of Aurelia c.f. sp. 2 likely produce environmentally-independent phenotypes that provide the highest fitness across environments. These findings suggest the two Aurelia lineages co-occurring in the GoM were likely exposed to different past environmental conditions (i.e., different selective pressures) and evolved different strategies to cope with environmental variation. This study highlights the importance of using genetics and morphometric data to understand jellyfish ecology, evolution and systematics.     

Predation potential of the jellyfish Drymonema larsoni Bayha & Dawson (Scyphozoa: Drymonematidae) on the moon jellyfish Aurelia sp. in the northern Gulf of Mexico

The jellyfish Drymonema larsoni bloomed in the northern Gulf of Mexico in the Fall of 2000 and fed voraciously on the moon jellyfish Aurelia sp., especially where they were concentrated in frontal convergence. We evaluated the predation potential of D. larsoni on Aurelia sp. medusa using laboratory and field data. Our data set represents the most complete study to date on the new scyphozoan family Drymonematidae and indicates that D. larsoni may be one of the most effective predators on other jellyfish recorded to date. On average, each D. larsoni medusa contained 2.7 Aurelia sp. prey, but as many as 34. In addition, 94% of moon jellyfish unassociated with D. larsoni showed scarring from previous contact with D. larsoni tentacles. Digestion times for D. larsoni feeding on individual Aurelia sp. ranged from 2 to 3 h and averaged 2.7 h. Potential clearance rates for predation on Aurelia sp. were extremely high (320–1043.5 m³ d⁻¹) and indicate that D. larsoni is potentially an important predator on Aurelia sp. blooms where the species co-occur. When the two species co-occur in numbers, predation by D. larsoni medusae could reduce moon jellyfish blooms, possibly alleviating predation pressure on lower trophic levels utilized by Aurelia sp., such as copepods and the early life history stages of ecologically and economically important fish and invertebrate species.     

Spatial distribution of fifty ornamental fish species on coral reefs in the Red Sea and Gulf of Aden

The spatial distribution of 50 ornamental fish species from shallow water habitats on coral reefs were investigated using visual census techniques, between latitudes 11−29°N in the Red Sea, in Jordan, Egypt, Saudi Arabia, and Yemen, and in the adjacent Gulf of Aden in Djibouti. One hundred eighteen transects (each 100×5 m) were examined in 29 sites (3−8 sites per country). A total of 522,523 fish individuals were counted during this survey, with mean abundance of 4428.2 ± 87.26 individual per 500 m² transect. In terms of relative abundance (RA), the most abundant species were Blue green damselfish, Chromis viridis (RA=54.4%),followed bySea goldie, Pseudanthias squamipinnis (RA= 34.7), Whitetail dascyllus, Dascyllus aruanus (RA= 2.6%), Marginate dascyllus, Dascyllus marginatus (RA= 2.0),Red Sea eightline flasher Paracheilinus octotaenia (RA=1.0),andKlunzinger’s wrasse, Thalassoma rueppellii (0.7%). The highest number of species (S) per 500 m² transect was found on reefs at the latitude 20° in Saudi Arabia (S=21.8), and the lowest number of species was found at the latitude 15° in Djibouti (S=11.11). The highest mean abundance (8565.8) was found on reefs at latitude 20° in Saudi Arabia and the lowest mean abundance (230) was found on reefs at latitude 22°, also in Saudi Arabia. Whereas, the highest Shannon-Wiener Diversity Index was found in reefs at the latitude 22° (H`=2.4) and the lowest was found in reefs at the latitude 20° (H`=0.6). This study revealed marked differences in the structure of ornamental fish assemblages with latitudinal distribution. The data support the presence of two major biogeographic groups of fishes in the Red Sea and Gulf of Aden: the southern Red Sea and Gulf of Aden group and the group in the northern and central Red Sea. Strong correlations were found between live coral cover and the number of fish species, abundance and Shannon-Wiener Diversity indices, and the strength of these correlations varied among the reefs. A conclusion was done that environmental differences among the reefs and the habitats investigated were important components of abundance variations and species diversity of ornamental fish along latitudinal gradients in the Red Sea and the Gulf of Aden.     

An account of the taxonomy and distribution of Syllidae (Annelida, Polychaetes) in the eastern Mediterranean, with notes on the genus Prosphaerosyllis San Martín, 1984 in the Mediterranean

The syllid fauna of three locations in Crete and Israel (eastern Mediterranean Sea) was studied, yielding 82 syllid species, many of which were found for the first time in the respective areas: Seventeen species were recorded for the first time on the Israeli coasts and 20 in Greek waters. Perkinsyllis augeneri (Hartmann-Schröder, 1979) and Prosphaerosyllis chauseyensis Olivier et al., 2011 are new records for the Mediterranean Sea. Detailed information is given on the morphology, ecology and distribution of the species recorded for the first time in the studied areas. In addition, an update on the distribution of the genus Prosphaerosyllis San Martín, 1984 in the Mediterranean is given and an identification key to the Mediterranean species is provided.     

Spread of Microcosmus squamiger (Ascidiacea: Pyuridae) in the Mediterranean Sea and adjacent waters

The Mediterranean Sea is subject to an ever-increasing arrival of non-indigenous marine organisms. Microcosmus squamiger is a solitary ascidian that inhabits shallow rocky littoral habitats. It probably originated in Australia and it has shown great invasive potential in other parts of the world. In the Mediterranean, M. squamiger has only been reported at a few sites in Spain and Italy. However, the closely related species Microcosmus exasperatus has been reported in several areas of the western Mediterranean. As these species can be easily confused, we re-examined most of the material from previous studies and our personal collections. In addition, sampling was done at several sites along the western Mediterranean and Atlantic coasts. The results showed that the majority of the M. exasperatus reports correspond to M. squamiger, and that M. squamiger is common on the Atlantic shores. This suggests that M. squamiger has entered the Mediterranean through the Gibraltar Strait, while the restricted distribution in the eastern Mediterranean of M. exasperatus suggests that this species is probably a Lessepsian migrant. In the Mediterranean Sea, M. squamiger has the ability to occupy extensive areas of hard substrata and to outcompete native species. Further studies are necessary to assess what impacts this invasive species have on native communities.     

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.     

Lessepsian invasion without bottleneck: example of two rabbitfish species (Siganus rivulatus and Siganus luridus)

Since the opening of the Suez Canal in the 19th century, a growing number of teleosts species have become permanently established in the eastern Mediterranean. As environmental parameters in the Mediterranean are very different from those in the Red Sea, there is an opportunity to evaluate the gene flow associated with the acclimatisation of these species to their new environment. Initial colonisation may have been restricted to individuals with marginal genotypes compared to populations of the Red Sea, eventually better adapted to the Mediterranean environment. Alternatively, colonisation may have occurred without major genetic differentiation, due to a large flux of immigrants and a continuous gene flow from the populations of origin. Using different molecular genetic techniques (mitochondrial DNA, Exon-Primed Intron-Crossing PCR amplification (EPIC) and Inter-Simple Sequence Repeats (ISSRs), patterns of genetic differentiation on both sides of the Suez isthmus were tested on two Lessepsian rabbitfish species (Siganus rivulatus and Siganus luridus). The absence of genetic differentiation between Mediterranean and Red Sea populations in both species showed that a great number of migrants participated to the colonisation of the Mediterranean, excluding any bottleneck event. This colonisation success suggests large eco-physiological plasticity in S. rivulatus and S. luridus that allowed them to thrive in the new environment.     

Jellyfish as Prey: Frequency of Predation and Selective Foraging of Boops boops (Vertebrata,Actinopterygii) on the Mauve Stinger Pelagia noctiluca (Cnidaria,Scyphozoa)

In recent years, jellyfish blooms have attracted considerable scientific interest for their potential impacts on human activities and ecosystem functioning, with much attention paid to jellyfish as predators and to gelatinous biomass as a carbon sink. Other than qualitative data and observations, few studies have quantified direct predation of fish on jellyfish to clarify whether they may represent a seasonally abundant food source. Here we estimate predation frequency by the commercially valuable Mediterranean bogue, Boops boops on the mauve stinger jellyfish, Pelagia noctiluca, in the Strait of Messina (NE Sicily). A total of 1054 jellyfish were sampled throughout one year to quantify predation by B. boops from bite marks on partially eaten jellyfish and energy density of the jellyfish. Predation by B. boops in summer was almost twice that in winter, and they selectively fed according to medusa gender and body part. Calorimetric analysis and biochemical composition showed that female jellyfish gonads had significantly higher energy content than male gonads due to more lipids and that gonads had six-fold higher energy content than the somatic tissues due to higher lipid and protein concentrations. Energetically, jellyfish gonads represent a highly rewarding food source, largely available to B. boops throughout spring and summer. During the remainder of the year, when gonads were not very evident, fish predation switched towards less-selective foraging on the somatic gelatinous biomass. P. noctiluca, the most abundant jellyfish species in the Mediterranean Sea and a key planktonic predator, may represent not only a nuisance for human leisure activities and a source of mortality for fish eggs and larvae, but also an important resource for fish species of commercial value, such as B. boops.     

New insights into global biogeography,population structure and natural selection from the genome of the epipelagic copepod Oithona

In the epipelagic ocean, the genus Oithona is considered as one of the most abundant and widespread copepods and plays an important role in the trophic food web. Despite its ecological importance, little is known about Oithona and cyclopoid copepods genomics. Therefore, we sequenced, assembled and annotated the genome of Oithona nana. The comparative genomic analysis integrating available copepod genomes highlighted the expansions of genes related to stress response, cell differentiation and development, including genes coding Lin12‐Notch‐repeat (LNR) domain proteins. The Oithona biogeography based on 28S sequences and metagenomic reads from the Tara Oceans expedition showed the presence of O. nana mostly in the Mediterranean Sea (MS) and confirmed the amphitropical distribution of Oithona similis. The population genomics analyses of O. nana in the Northern MS, integrating the Tara Oceans metagenomic data and the O. nana genome, led to the identification of genetic structure between populations from the MS basins. Furthermore, 20 loci were found to be under positive selection including four missense and eight synonymous variants, harbouring soft or hard selective sweep patterns. One of the missense variants was localized in the LNR domain of the coding region of a male‐specific gene. The variation in the B‐allele frequency with respect to the MS circulation pattern showed the presence of genomic clines between O. nana and another undefined Oithona species possibly imported through Atlantic waters. This study provides new approaches and results in zooplankton population genomics through the integration of metagenomic and oceanographic data.     

Habitat niche breadth predicts invasiveness in solitary ascidians

A major focus of invasion biology is understanding the traits associated with introduction success. Most studies assess these traits in the invaded region, while only few compare nonindigenous species to the pool of potential invaders in their native region. We focused on the niche breadth hypothesis, commonly evoked but seldom tested, which states that generalist species are more likely to become introduced as they are capable of thriving under a wide set of conditions. Based on the massive introduction of tropical species into the Mediterranean via the Suez Canal (Lessepsian migration), we defined ascidians in the Red Sea as the pool of potential invaders. We constructed unique settlement plates, each representing six different niches, to assess ascidian niche breadth, and deployed them in similar habitats in the native and invaded regions. For each species found on plates, we evaluated its abundance, relative abundance across successional stages, and niche breadth, and then compared (1) species in the Red Sea known to have been introduced into the Mediterranean (Lessepsian species) and those not known from the Mediterranean (non‐Lessepsian); and (2) nonindigenous and indigenous species in the Mediterranean. Lessepsian species identified on plates in the Red Sea demonstrated wider niche breadth than non‐Lessepsian species, supporting the niche breadth hypothesis within the native region. No differences were found between Lessepsian and non‐Lessepsian species in species abundance and successional stages. In the Mediterranean, nonindigenous species numerically dominated the settlement plates. This precluded robust comparisons of niche breadth between nonindigenous and indigenous species in the invaded region. In conclusion, using Red Sea ascidians as the pool of potential invaders, we found clear evidence supporting the niche breadth hypothesis in the native region. We suggest that such patterns may often be obscured when conducting trait‐based studies in the invaded regions alone. Our findings indicate that quantifying the niche breadth of species in their native regions will improve estimates of invasiveness potential.     

Adding new pieces to the Azadinium (Dinophyceae) diversity and biogeography puzzle: Non-toxigenic Azadinium zhuanum sp. nov. from China,toxigenic A. poporum from the Mediterranean,and a non-toxigenic A. dalianense from the French Atlantic

The marine planktonic dinophyceaen genus Azadinium is a primary source of azaspiracids, but due to their small size its diversity may be underestimated and information on its biogeography is still limited. A new Azadinium species, A. zhuanum was obtained from the East China Sea and Yellow Sea of China by incubating surface sediments. Five strains were established by isolating single germinated cells and their morphology was examined with light microscopy and scanning electron microscopy. Azadinium zhuanum was characterized by a plate pattern of Po, cp, X, 4′, 2a, 6′′, 6C, 5S, 6′′′, 2′′′′, by a distinct ventral pore at the junction of Po, the first and fourth apical plates, and a conspicuous antapical spine. Moreover, Azadinium poporum was obtained for the first time from the Mediterranean by incubating surface sediment collected from Diana Lagoon (Corsica) and a new strain of Azadinium dalianense was isolated from the French Atlantic. The morphology of both strains was examined. Small subunit ribosomal DNA (SSU rDNA), large subunit ribosomal DNA (LSU rDNA) and internal transcribed spacer (ITS) sequences were obtained from cultured strains. In addition, LSU sequences were obtained by single cell sequencing of two presumable A. poporum cells collected from the French Atlantic. Molecular phylogeny based on concatenated SSU, LSU and ITS sequences revealed that A. zhuanum was closest to A. polongum. French A. poporum from Corsica (Mediterranean) and from the Atlantic showed some genetic differences but were nested within one of the A. poporum ribotypes together with other European strains. Azadinium dalianense from France together with the type strain of the species from China comprised a well resolved clade now consisting of two ribotypes. Azaspiracid profiles were analyzed for the cultured Azadinium strains using LC–MS/MS and demonstrate that the Mediterranean A. poporum strain produced AZA-2 and AZA-2 phosphate with an amount of 0.44 fg cell⁻¹. Azadinium zhuanum and A. dalianense did not produce detectable AZA. Results of the present study support the view of a high diversity and wide distribution of species belonging to Azadinium. The first record of AZA-2 producing A. poporum from the Mediterranean suggests that this species may be responsible for azaspiracid contaminations in shellfish from the Mediterranean Sea.     

Molecular Evidence for Lessepsian Invasion of Soritids (Larger Symbiont Bearing Benthic Foraminifera)

The Mediterranean Sea is considered as one of the hotspots of marine bioinvasions, largely due to the influx of tropical species migrating through the Suez Canal, so-called Lessepsian migrants. Several cases of Lessepsian migration have been documented recently, however, little is known about the ecological characteristics of the migrating species and their aptitude to colonize the new areas. This study focused on Red Sea soritids, larger symbiont-bearing benthic foraminifera (LBF) that are indicative of tropical and subtropical environments and were recently found in the Israeli coast of the Eastern Mediterranean. We combined molecular phylogenetic analyses of soritids and their algal symbionts as well as network analysis of Sorites orbiculus Forskål to compare populations from the Gulf of Elat (northern Red Sea) and from a known hotspot in Shikmona (northern Israel) that consists of a single population of S. orbiculus. Our phylogenetic analyses show that all specimens found in Shikmona are genetically identical to a population of S. orbiculus living on a similar shallow water pebbles habitat in the Gulf of Elat. Our analyses also show that the symbionts found in Shikmona and Elat soritids belong to the Symbiodinium clade F5, which is common in the Red Sea and also present in the Indian Ocean and Caribbean Sea. Our study therefore provides the first genetic and ecological evidences that indicate that modern population of soritids found on the Mediterranean coast of Israel is probably Lessepsian, and is less likely the descendant of a native ancient Mediterranean species.