Biogeographical patterns of algal communities in the Mediterranean Sea: Cystoseira crinita‐dominated assemblages as a case study

Aim The aim of this study was to describe the composition, community structure and biogeographical variation of subtidal algal assemblages dominated by the brown alga Cystoseira crinita across the Mediterranean Sea. Location The Mediterranean coast, from Spain (1°25′ E) to Turkey (30°26′ E). Methods Data on the species composition and structure of assemblages dominated by the species C. crinita were collected from 101 sites in nine regions across the Mediterranean Sea. Multivariate and univariate statistical tools were used to investigate patterns of variation in the composition of the assemblages among sites and regions, and to compare these with previously defined biogeographical regions. Linear regressions of species richness versus longitude and versus latitude were also carried out to test previously formulated hypotheses of biodiversity gradients in the Mediterranean Sea. Results The main features characterizing C. crinita‐dominated assemblages across the Mediterranean included a similar total cover of species, a similar cover of C. crinita, and consistency in the presence of the epiphyte Haliptilon virgatum. Biogeographical variation was detected as shifts in relative abundances of species among regions, partly coinciding with previously described biogeographical sectors. A significant positive correlation was found between species richness and latitude, while no significant correlation was detected between species richness and longitude. Main conclusions The patterns of variation in community structure detected among the studied regions reflected their geographical positions quite well. However, latitude seemed to contribute more to the explanation of biological patterns of diversity than did geographical distances or boundaries, which classically have been used to delimit biogeographical sectors. Moreover, the positive correlation between species richness and latitude reinforced the idea that latitude, and possibly temperature as a related environmental factor, plays a primary role in structuring biogeographical patterns in the Mediterranean Sea. The lack of correlation between species richness and longitude contradicts the notion that there is a decrease in species richness from west to east in the Mediterranean, following the direction of species colonization from the Atlantic.     

Monitoring biofouling communities could reduce impacts to mussel aquaculture by allowing synchronisation of husbandry techniques with peaks in settlement

Fouling organisms in bivalve aquaculture cause significant economic losses for the industry. Managing biofouling is typically reactive, and involves time- and labour-intensive removal techniques. Mussel spat settlement and biofouling were documented over 20 months at three mussel farms within Port Phillip Bay (PPB), Australia to determine if knowledge of settlement patterns could assist farmers in avoiding biofouling. Mussel spat settlement was largely confined to a 2-month period at one farm. Of the problematic foulers, Ectopleura crocea settlement varied in space and time at all three farms, whilst Ciona intestinalis and Pomatoceros taeniata were present predominantly at one farm and exhibited more distinct settlement periods. Within PPB, complete avoidance of biofouling is impossible. However, diligent monitoring may help farmers avoid peaks in detrimental biofouling species and allow them to implement removal strategies such as manual cleaning, and postpone grading and re-socking practices, until after these peaks.     

Biofouling community composition across a range of environmental conditions and geographical locations suitable for floating marine renewable energy generation

Knowledge of biofouling typical of marine structures is essential for engineers to define appropriate loading criteria in addition to informing other stakeholders about the ecological implications of creating novel artificial environments. There is a lack of information regarding biofouling community composition (including weight and density characteristics) on floating structures associated with future marine renewable energy generation technologies. A network of navigation buoys were identified across a range of geographical areas, environmental conditions (tidal flow speed, temperature and salinity), and deployment durations suitable for future developments. Despite the perceived importance of environmental and temporal factors, geographical location explained the greatest proportion of the observed variation in community composition, emphasising the importance of considering geography when assessing the impact of biofouling on device functioning and associated ecology. The principal taxa associated with variation in biofouling community composition were mussels (Mytilus edulis), which were also important when determining loading criteria.     

Identification of Bacterial Strains Isolated from the Mediterranean Sea Exhibiting Different Abilities of Biofilm Formation

The Mediterranean Sea has rarely been investigated for the characterization of marine bacteria as compared to other marine environments such as the Atlantic or Pacific Ocean. Bacteria recovered from inert surfaces are poorly studied in these environments, when it has been shown that the community structure of attached bacteria can be dissimilar from that of planktonic bacteria present in the water column. The objectives of this study were to identify and characterize marine bacteria isolated from biofilms developed on inert surfaces immersed in the Mediterranean Sea and to evaluate their capacity to form a biofilm in vitro. Here, 13 marine bacterial strains have been isolated from different supports immersed in seawater in the Bay of Toulon (France). Phylogenetic analysis and different biological and physico-chemical properties have been investigated. Among the 13 strains recovered, 8 different genera and 12 different species were identified including 2 isolates of a novel bacterial species that we named Persicivirga mediterranea and whose genus had never been isolated from the Mediterranean Sea. Shewanella sp. and Pseudoalteromonas sp. were the most preponderant genera recovered in our conditions. The phenotypical characterization revealed that one isolate belonging to the Polaribacter genus differed from all the other ones by its hydrophobic properties and poor ability to form biofilms in vitro. Identifying and characterizing species isolated from seawater including from Mediterranean ecosystems could be helpful for example, to understand some aspects of bacterial biodiversity and to further study the mechanisms of biofilm (and biofouling) development in conditions approaching those of the marine environment.     

The microcopepod fauna in the Eastern Mediterranean and Arabian Seas: a comparison with the Red Sea fauna

Multiple opening-closing nets of 0.05 mm mesh size were employed to study the community structure and vertical distribution of microcopepods at selected stations in the Red Sea, Arabian Sea and Eastern Mediterranean Sea down to a maximum depth of 1850 m. Calanoids, cyclopoids (Oithona and Paroithona) and poecilostomatoids (mainly Oncaea) were the 3 most abundant orders. In the epipelagic zone (0–100 m), these orders occurred at similar abundance levels, whereas in the meso- and bathypelagic zones the poecilostomatoid genus Oncaea dominated numerically by about 60–80% of all copepodids.The species diversity of Oncaea in the Red Sea is compared with preliminary results from the two adjacent regions. In the deep Eastern Mediterranean Sea, the number of species appears to be similar to that in the deep Red Sea and low as compared to the deep Arabian Sea. In this latter area an extremely speciose Oncaea fauna was found at depth below the oxygen-minimum-zone (900–1850 m). The results are related to the differences in the hydrographic conditions of these 3 areas.     

A comparison of droplet digital polymerase chain reaction (PCR), quantitative PCR and metabarcoding for species‐specific detection in environmental DNA

Targeted species‐specific and community‐wide molecular diagnostics tools are being used with increasing frequency to detect invasive or rare species. Few studies have compared the sensitivity and specificity of these approaches. In the present study environmental DNA from 90 filtered seawater and 120 biofouling samples was analyzed with quantitative PCR (qPCR), droplet digital PCR (ddPCR) and metabarcoding targeting the cytochrome c oxidase I (COI) and 18S rRNA genes for the Mediterranean fanworm Sabella spallanzanii. The qPCR analyses detected S. spallanzanii in 53% of water and 85% of biofouling samples. Using ddPCR S. spallanzanii was detected in 61% of water of water and 95% of biofouling samples. There were strong relationships between COI copy numbers determined via qPCR and ddPCR (water R² = 0.81, p < .001, biofouling R² = 0.68, p < .001); however, qPCR copy numbers were on average 125‐fold lower than those measured using ddPCR. Using metabarcoding there was higher detection in water samples when targeting the COI (40%) compared to 18S rRNA (5.4%). The difference was less pronounced in biofouling samples (25% COI, 29% 18S rRNA). Occupancy modelling showed that although the occupancy estimate was higher for biofouling samples (ψ = 1.0), higher probabilities of detection were derived for water samples. Detection probabilities of ddPCR (1.0) and qPCR (0.93) were nearly double metabarcoding (0.57 to 0.27 marker dependent). Studies that aim to detect specific invasive or rare species in environmental samples should consider using targeted approaches until a detailed understanding of how community and matrix complexity, and primer biases affect metabarcoding data.     

Responses of foraminifera communities to aquaculture‐derived organic enrichment as revealed by environmental DNA metabarcoding

Current monitoring methods to assess benthic impacts of marine finfish aquaculture are based on complex biological indices and/or geochemistry data. The former requires benthic macrofauna morpho‐taxonomic characterization that is time‐ and cost‐intensive, while the latter provides rapid assessment of the organic enrichment status of sediments but does not directly measure biotic impacts. In this study, sediment samples were collected from seven stations at six salmon farms in British Columbia, Canada, and analyzed for geochemical parameters and by eDNA metabarcoding to investigate linkages between geochemistry and foraminifera. Sediment texture across farm sites ranged from sand to silty loam, while the maximum sediment pore‐water sulphide concentration at each site ranged from 1,000 to 13,000 μM. Foraminifera alpha diversity generally increased with distance from cage edge. Adonis analyses revealed that farm site explained the most variation in foraminifera community, followed by sediment type, enrichment status, and distance from cage edge. Farm‐specific responses were observed in diversity analyses, taxonomic difference analyses, and correlation analyses. Results demonstrated that species diversity and composition of foraminifera characterized by eDNA metabarcoding generated signals consistent with benthic biodiversity being impacted by finfish farming activities. This substantiates the validity of eDNA metabarcoding for augmenting current approaches to benthic impact assessments by providing more cost‐effective and practicable biotic measures than traditional morpho‐taxonomy. To capitalize on this potential, further work is needed to design a new nomogram that combines eDNA metabarcoding data and geochemistry data to enable accurate monitoring of benthic impacts of fish farming in a time‐ and cost‐efficient way.     

Sponge-specific Bacterial Associations of the Mediterranean Sponge <Emphasis Type="Italic">Chondrilla nucula</Emphasis> (Demospongiae,Tetractinomorpha)

A stable and specific bacterial community was shown to be associated with the Mediterranean sponge Chondrilla nucula. The associated bacterial communities were demonstrated to be highly similar for all studied specimens regardless of sampling time and geographical region. In addition, analysis of 16S rDNA clone libraries revealed three constantly C. nucula-associated bacterial phylotypes belonging to the Acidobacteria, the Gamma- and Deltaproteobacteria present in sponge specimens from two Mediterranean regions with distinct water masses (Ligurian Sea and Adriatic Sea). For the first time, candidate division TM7 bacteria were found in marine sponges. A major part (79%) of the C. nucula-derived 16S rDNA sequences were closely related to other sponge-associated bacteria. Phylogenetic analysis identified 14 16S rRNA gene sequence clusters, seven of which consisted of exclusively sponge-derived sequences, whereas the other seven clusters contained additional environmental sequences. This study adds to a growing database on the stability and variability of microbial consortia associated with marine sponges.     

The effect of substratum type,orientation and depth on the development of bacterial deep-sea biofilm communities grown on artificial substrata deployed in the Eastern Mediterranean

An increasing number of deep-sea studies have highlighted the importance of deep-sea biofouling, especially in relation to the protection of deep-sea instruments. In this study, the microbial communities developed on different substrata (titanium, aluminum, limestone, shale and neutrino telescope glass) exposed for 155 days at different depths (1500 m, 2500 m, 3500 m and 4500 m) and positions (vertical and horizontal) in the Eastern Mediterranean Deep Sea were compared. Replicated biofilm samples were analyzed using a Terminal Restriction Fragment Length Polymorphisms (T-RFLP) method. The restriction enzymes CfoI and RsaI produced similar total numbers (94, 93) of different T-RFLP peaks (T-RFs) along the vertical transect. In contrast, the mean total T-RF number between each sample according to substratum type and depth was higher in more samples when CfoI was used. The total species richness (S) of the bacterial communities differed significantly between the substrata, and depended on the orientation of each substratum within one depth and throughout the water column (ANOVA). T-RFLP analyses using the Jaccard similarity index showed that within one depth layer, the composition of microbial communities on different substrata was different and highly altered among communities developed on the same substratum but exposed to fouling at different depths. Based on Multidimensional Scaling Analyses (MDS), the study suggests that depth plays an important role in the composition of deep-sea biofouling communities, while substratum type and orientation of substrata throughout the water column are less important. To the authors’ knowledge, this is the first study of biofilm development in deep waters, in relation to the effects of substratum type, orientation and depth.     

Lack of a genetic bottleneck in a recent Lessepsian bioinvader, the blue-barred parrotfish, Scarus ghobban

The present study investigates the genetic diversity of Scarus ghobban, a recently introduced parrotfish in the Mediterranean Sea via the Suez Canal. Two mitochondrial and one nuclear DNA regions were sequenced and phylogenetic relationships investigated, from samples collected from Lebanon and across its natural range. Scarus ghobban clustered in two major clades, Pacific Ocean and Indian Ocean, indicating strong population structure, or cryptic speciation. Expectedly, Mediterranean samples clustered with Indian Ocean-Red Sea individuals. However, unlike other recent Lessepsian invaders, S. ghobban displayed high genetic diversity. These results underscore that genetic diversity is a poor predictor of success of an invasive species.     

Bacterial community diversity in paper mills processing recycled paper

Paper mills processing recycled paper suffer from biofouling causing problems both in the mill and final product. The total bacterial community composition and identification of specific taxa in the process water and biofilms at the stock preparation and paper machine areas in a mill with recycled paper pulp was described by using a DNA-based approach. Process water in a similar mill was also analyzed to investigate if general trends can be found between mills and over time. Bacterial community profiles, analyzed by terminal-restriction fragment length polymorphism (T-RFLP), in process water showed that the dominant peaks in the profiles were similar between the two mills, although the overall composition was unique for each mill. When comparing process water and biofilm at different locations within one of the mills, we observed a separation according to location and sample type, with the biofilm from the paper machine being most different. 16S rRNA gene clone libraries were generated and 404 clones were screened by RFLP analysis. Grouping of RFLP patterns confirmed that the biofilm from the paper machine was most different. A total of 99 clones representing all RFLP patterns were analyzed, resulting in sequences recovered from nine bacterial phyla, including two candidate phyla. Bacteroidetes represented 45% and Actinobacteria 23% of all the clones. Sequences with similarity to organisms implicated in biofouling, like Chryseobacterium spp. and Brevundimonas spp., were recovered from all samples even though the mill had no process problems during sampling, suggesting that they are part of the natural paper mill community. Moreover, many sequences showed little homology to as yet uncultivated bacteria implying that paper mills are interesting for isolation of new organisms, as well as for bioprospecting.     

Population genetics,gene flow,and biogeographical boundaries of Carcinus aestuarii (Crustacea: Brachyura: Carcinidae) along the European Mediterranean coast

Carcinus aestuarii Nardo, 1847 is a widespread coastal crab species throughout the Mediterranean Sea with a pelagic larval phase. This species tolerates a wide range of environmental conditions and typically inhabits fragmented habitats, such as embayments, lagoons and estuaries. It is therefore a good candidate species for studying and testing different phylogeographical hypotheses in the Mediterranean Sea. By contrast to its Atlantic sister species, Carcinus maenas, studies on the population genetic structure of C. aestuarii in its native range are still scarce. In the present study, specimens from along the European Mediterranean Sea were collected and DNA‐sequenced and analyses were applied to discriminate between present day and historical factors influencing the population genetic structure of this species. The results obtained demonstrate the existence of two genetically distinct geographical groups, corresponding to the eastern and western Mediterranean, with further subdivision within the East Mediterranean Basin. A strong asymmetric gene flow was recorded toward the Eastern Basin, which may play a crucial role in shaping the present day biogeographical patterns of this species and potentially other sympatric ones with pelagic larvae. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 771–790.     

The largescaled terapon Terapon theraps: a new Indo‐Pacific fish in the Mediterranean Sea

A specimen of the largescaled terapon Terapon theraps was recorded for the first time from the Mediterranean Sea. The finding of T. theraps in the northernmost part of the Mediterranean Sea raises the number of Lessepsian migrant species to at least 68 and in the Adriatic Sea to at least 11.     

Endemic and Indo-Pacific plankton in the Mediterranean Sea: a study based on dinoflagellate records

Aim To investigate biogeographical patterns based on published dinoflagellate records from the Mediterranean and Black Seas, and to provide a tentative list of endemic and Indo‐Pacific dinoflagellates in the Mediterranean Sea. Location Mediterranean Sea, Black Sea. Methods Checklists of dinoflagellates of the Mediterranean and Black Seas were compared with worldwide literature records. Only species reported in the Indo‐Pacific Ocean or exclusively known in the Mediterranean Sea were selected for biogeographical analysis. Results Dinoflagellates in the Mediterranean Sea comprised c. 43% of the world marine species and c. 88% of the dinoflagellate genera. Species richness among the Mediterranean sub‐basins showed marked differences due to the less reliable records of unarmoured (athecate) and rare dinoflagellates. These differences disappeared when only the more easily identifiable taxa were considered. Of the 673 dinoflagellates cited in the Mediterranean, 87% were also reported in the Atlantic Ocean. Only 40 taxa (6% of the total) were considered to be potential Indo‐Pacific species. Most were reported from the Ligurian Sea (21), and only two species from the Levantine basin. The other 48 taxa (7% of total) were known exclusively from the Mediterranean Sea, mainly from the Ligurian Sea. Half of these taxa were reported by a single author. Main conclusions Substantial dinoflagellates species richness can be attributed, in part, to the historical tradition of taxonomic studies in the Mediterranean Sea. The list of species of both Indo‐Pacific and exclusively Mediterranean species included taxa of dubious taxonomic validity or that were insufficiently known. The exclusion of these questionable taxa revealed the near absence of endemic dinoflagellates in the Mediterranean Sea compared with macroscopic organisms. This could be related to: (1) continuous replenishment of the plankton populations by the inflow of Atlantic water through the Strait of Gibraltar, (2) the possibility that species introduced during the Pliocenic flooding after the Messinian salinity crisis have not had enough time to diverge from their Atlantic ancestors, and/or (3) the reliance on traditional taxonomy based on morphological characters, which precludes the detection of cryptic speciation.     

Using passive acoustics to assess habitat selection by the brown meagre Sciaena umbra in a northern Adriatic Sea mussel farm

Passive acoustic monitoring (PAM) of the brown meagre Sciaena umbra was conducted in a northern Adriatic Sea mussel farm. The level of acoustic activity was found to be constantly high from June to August before declining sharply in September and there was significantly higher acoustic activity in the structured habitats within the mussel farm than in the bare sandy bottom outside the farm. Results are discussed in the context of the use of this species as an indicator species of artificial rocky habitats along the Mediterranean coastal environments.     

Jellyfish Stings Trigger Gill Disorders and Increased Mortality in Farmed Sparus aurata (Linnaeus, 1758) in the Mediterranean Sea

Jellyfish are of particular concern for marine finfish aquaculture. In recent years repeated mass mortality episodes of farmed fish were caused by blooms of gelatinous cnidarian stingers, as a consequence of a wide range of hemolytic, cytotoxic, and neurotoxic properties of associated cnidocytes venoms. The mauve stinger jellyfish Pelagia noctiluca (Scyphozoa) has been identified as direct causative agent for several documented fish mortality events both in Northern Europe and the Mediterranean Sea aquaculture farms. We investigated the effects of P. noctiluca envenomations on the gilthead sea bream Sparus aurata by in vivo laboratory assays. Fish were incubated for 8 hours with jellyfish at 3 different densities in 300 l experimental tanks. Gill disorders were assessed by histological analyses and histopathological scoring of samples collected at time intervals from 3 hours to 4 weeks after initial exposure. Fish gills showed different extent and severity of gill lesions according to jellyfish density and incubation time, and long after the removal of jellyfish from tanks. Jellyfish envenomation elicits local and systemic inflammation reactions, histopathology and gill cell toxicity, with severe impacts on fish health. Altogether, these results shows P. noctiluca swarms may represent a high risk for Mediterranean finfish aquaculture farms, generating significant gill damage after only a few hours of contact with farmed S. aurata. Due to the growth of the aquaculture sector and the increased frequency of jellyfish blooms in the coastal waters, negative interactions between stinging jellyfish and farmed fish are likely to increase with the potential for significant economic losses.     

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.     

Seasonal variability of copepod abundance in the Balearic region (Western Mediterranean) as an indicator of basin scale hydrological changes

Spatial and temporal changes of the copepod community have been investigated and related to the environmental variability of the Balearic Sea (Western Mediterranean). The period studied spans from 1994 to 1999 during which we analyzed the abundance and structure copepod variability over a cross-shore transect. Results showed a close link between hydrological changes and the variations of copepod abundance. The synchronous variability of copepods and hydrography indicated the rapid response of this zooplankton group to the inflow of cold and warm water masses coming through the study area. Cluster analysis revealed four main copepod assemblages that distinguished the coastal from the oceanic species and those species with different water masses preference. The copepod assemblage composed of Calanus helgolandicus, Clausocalanus arcuicornis, C. pergens, C. paululus, Calocalanus tenuis and Pleuromamma gracilis was associated with cool salty waters, whereas the assemblage formed by Temora stylifera, C. pavo, C. styliremis, Centropages bradyi and Acartia danae was related to warmer less saline Mediterranean waters. Moreover, it is suggested that changes in sea water temperature and salinity are linked to large-scale changes likely occurring at a basin scale, which is reflected in the Western Mediterranean mesoscale hydrographic changes. Therefore, it is stressed that changes in the Balearic copepod community can be used as potential tracers of the western Mediterranean water masses. Guest editors: S. Souissi & G. A. Boxshall Copepoda in the Mediterranean: Papers from the 9th International Conference on Copepoda, Hammamet, Tunisia     

Diet composition of bluefin tuna (Thunnus thynnus L. 1758) in the Eastern Mediterranean Sea,Turkey

This study gives relevant information on the diet composition of the bluefin tuna (Thunnus thynnus) during the spawning period in the eastern Mediterranean Sea. The stomach contents of 218 bluefin tuna were sampled from 2003 to 2006 during the fishing season (May–June) aboard purse seiners operating in the northern Levantine Sea off the coast of Turkey. Stomachs were removed from the fish soon after landing and kept frozen at ?18°C until analysis. Prey items were classified into large taxonomic categories and preserved in 70% ethanol. A total of 745 different prey specimens belonging to 47 taxa were identified, including 34 species of fish, 11 of squid, and two of crustaceans. The most important fish and cephalopod prey belonged to the families Myctophidae, Carangidae, Chauliodontidae, Paralepididae, and Octopoda. This study marks the observation of myctophid fish in the stomach contents of bluefin tuna from the Mediterranean Sea. The paper offers some new information of regional importance and compares the feeding habits of the species to other regions, bringing confirmation on the opportunistic feeding ecology of the species in the enclosed Mediterranean Sea, where bluefin tuna seasonally occur as a strong cohort. New information on the diet composition of T. thynnus in the eastern Mediterranean Sea is revealed; the findings indicate that, depending on the abundance of the different prey species in the habitat, the dominant prey species can be distinctive.