Seasonal Stability in the Microbiomes of Temperate Gorgonians and the Red Coral Corallium rubrum Across the Mediterranean Sea.

Populations of key benthic habitat-forming octocoral species have declined significantly in the Mediterranean Sea due to mass mortality events caused by microbial disease outbreaks linked to high summer seawater temperatures. Recently, we showed that the microbial communities of these octocorals are relatively structured; however, our knowledge on the seasonal dynamics of these microbiomes is still limited. To investigate their seasonal stability, we collected four soft gorgonian species (Eunicella singularis, Eunicella cavolini, Eunicella verrucosa and Leptogorgia sarmentosa) and the precious red coral (Corallium rubrum) from two coastal locations with different terrestrial impact levels in the Mediterranean Sea, and used next-generation amplicon sequencing of the 16S rRNA gene. The microbiomes of all soft gorgonian species were dominated by the same 'core microbiome' bacteria belonging to the Endozoicomonas and the Cellvibrionales clade BD1-7, whereas the red coral microbiome was primarily composed of 'core' Spirochaetes, Oceanospirillales ME2 and Parcubacteria. The associations with these bacterial taxa were relatively consistent over time at each location for each octocoral species. However, differences in microbiome composition and seasonal dynamics were observed between locations and could primarily be attributed to locally variant bacteria. Overall, our data provide further evidence of the intricate symbiotic relationships that exist between Mediterranean octocorals and their associated microbes, which are ancient and highly conserved over both space and time, and suggest regulation of the microbiome composition by the host, depending on local conditions.

Benthic diversity patterns and predictors: A study case with inferences for conservation.

Understanding which drivers cause diversity patterns is a key issue in conservation. Here we applied a spatially explicit model to predict marine benthic diversity patterns according to environmental factors in the NW Mediterranean Sea. While most conservation-oriented diversity studies consider species richness only and neglect equitability, we measured separately species richness, equitability, and 'overall' diversity (i.e., the Shannon-Wiener H' function) on a dataset of 890 benthic species × 209 samples. Diversity values were predicted by means of Random Forest regression, on the basis of 10 factors: depth, distance from the coast, distance from the shelf break, latitude, sea-floor slope, sediment grain size, sediment sorting, distance from harbours and marinas, distance from rivers, and sampling gear. Predictions by Random Forests were accurate, the main predictors being latitude, sediment grain size, depth and distance from the coast. Based on predicted values, diversity hotspots were identified as those localities where indices were in the 15% top segment of ranked values. Only a minority of the diversity hotspots was included within the boundaries of the protection institutes established in the region. Marine protected areas are often created in sites harbouring important coastal habitats, which risks neglecting the diversity hidden in the sedimentary seafloor. We suggest that marine protected areas should accommodate portions of sedimentary habitat within their boundaries to improve diversity conservation.

The Bryozoa collection of the Italian National Antarctic Museum, with an updated checklist from Terra Nova Bay, Ross Sea.

This study provides taxonomic and distributional data of bryozoan species from the Ross Sea area, mainly around Terra Nova Bay, based on specimens curated at the Italian National Antarctic Museum (MNA, Section of Genoa). Bryozoan specimens were collected at 75 different sampling stations in the Ross Sea and in the Magellan Strait, in a bathymetric range of 18-711 meters, during 13 expeditions of the Italian National Antarctic Research Program (PNRA) conducted between 1988 and 2014. A total of 282 MNA vouchers corresponding to 311 specimens and 127 morphospecies have been identified and included in the present dataset. 62% of the species were already reported for the Terra Nova Bay area, where most of the Italian samples come from, with a 35% of samples representing new records classified at the specific level, and 3% classified at the genus level. These new additions increase to 124 the total number of species known to occur in Terra Nova Bay. Four 3D-models of Antarctic bryozoans from the Ross Sea are also presented and will be released for research and educational purposes on the Museum website.

Genetic diversity increases with depth in red gorgonian populations of the Mediterranean Sea and the Atlantic Ocean.

BACKGROUND: In the ocean, the variability of environmental conditions found along depth gradients exposes populations to contrasting levels of perturbation, which can be reflected in the overall patterns of species genetic diversity. At shallow sites, resource availability may structure large, persistent and well-connected populations with higher levels of diversity. In contrast, the more extreme conditions, such as thermal stress during heat waves, can lead to population bottlenecks and genetic erosion, inverting the natural expectation. Here we examine how genetic diversity varies along depth for a long-lived, important ecosystem-structuring species, the red gorgonian, Paramuricea clavata. METHODS: We used five polymorphic microsatellite markers to infer differences in genetic diversity and differentiation, and to detect bottleneck signs between shallow and deeper populations across the Atlantic Ocean and the Mediterranean Sea. We further explored the potential relationship between depth and environmental gradients (temperature, ocean currents, productivity and slope) on the observed patterns of diversity by means of generalized linear mixed models. RESULTS: An overall pattern of higher genetic diversity was found in the deeper sites of the Atlantic Ocean and the Mediterranean Sea. This pattern was largely explained by bottom temperatures, with a linear pattern of decreasing genetic diversity with increasing thermal stress. Genetic differentiation patterns showed higher gene flow within sites (i.e., shallow vs. deeper populations) than between sites. Recent genetic bottlenecks were found in two populations of shallow depths. DISCUSSION: Our results highlight the role of deep refugial populations safeguarding higher and unique genetic diversity for marine structuring species. Theoretical regression modelling demonstrated how thermal stress alone may reduce population sizes and diversity levels of shallow water populations. In fact, the examination of time series on a daily basis showed the upper water masses repeatedly reaching lethal temperatures for P. clavata. Differentiation patterns showed that the deep richer populations are isolated. Gene flow was also inferred across different depths; however, not in sufficient levels to offset the detrimental effects of surface environmental conditions on genetic diversity. The identification of deep isolated areas with high conservation value for the red gorgonian represents an important step in the face of ongoing and future climate changes.

Low pH conditions impair module capacity to regenerate in a calcified colonial invertebrate, the bryozoan Cryptosula pallasiana.

Many aquatic animals grow into colonies of repeated, genetically identical, modules (zooids). Zooid interconnections enable colonies to behave as integrated functional units, while plastic responses to environmental changes may affect individual zooids. Plasticity includes the variable partitioning of resources to sexual reproduction, colony growth and maintenance. Maintenance often involves regeneration, which is also a routine part of the life history in some organisms, such as bryozoans. Here we investigate changes in regenerative capacity in the encrusting bryozoan Cryptosula pallasiana when cultured at different seawater pCO2 levels. The proportion of active zooids showing polypide regeneration was highest at current oceanic pH (8.1), but decreased progressively as pH declined below that value, reaching a six-fold reduction at pH 7.0. The zone of budding of new zooids at the colony periphery declined in size below pH 7.7. Under elevated pCO2 conditions, already experienced sporadically in coastal areas, skeletal corrosion was accompanied by the proportional reallocation of resources from polypide regeneration in old zooids to the budding of new zooids at the edge of the colony. Thus, future ocean acidification can affect colonial organisms by changing how they allocate resources, with potentially profound impacts on life-history patterns and ecological interactions.

Genetic Diversity and Local Connectivity in the Mediterranean Red Gorgonian Coral after Mass Mortality Events.

Estimating the patterns of connectivity in marine taxa with planktonic dispersive stages is a challenging but crucial task because of its conservation implications. The red gorgonian Paramuricea clavata is a habitat forming species, characterized by short larval dispersal and high reproductive output, but low recruitment. In the recent past, the species was impacted by mass mortality events caused by increased water temperatures in summer. In the present study, we used 9 microsatellites to investigate the genetic structure and connectivity in the highly threatened populations from the Ligurian Sea (NW Mediterranean). No evidence for a recent bottleneck neither decreased genetic diversity in sites impacted by mass mortality events were found. Significant IBD pattern and high global FST confirmed low larval dispersal capability in the red gorgonian. The maximum dispersal distance was estimated at 20-60 km. Larval exchange between sites separated by hundreds of meters and between different depths was detected at each site, supporting the hypothesis that deeper subpopulations unaffected by surface warming peaks may provide larvae for shallower ones, enabling recovery after climatically induced mortality events.

Biomineralization in bryozoans: present, past and future.

Many animal phyla have the physiological ability to produce biomineralized skeletons with functional roles that have been shaped by natural selection for more than 500 million years. Among these are bryozoans, a moderately diverse phylum of aquatic invertebrates with a rich fossil record and importance today as bioconstructors in some shallow-water marine habitats. Biomineralizational patterns and, especially, processes are poorly understood in bryozoans but are conventionally believed to be similar to those of the related lophotrochozoan phyla Brachiopoda and Mollusca. However, bryozoan skeletons are more intricate than those of these two phyla. Calcareous skeletons have been acquired independently in two bryozoan clades - Stenolaemata in the Ordovician and Cheilostomata in the Jurassic - providing an evolutionary replicate. This review aims to highlight the importance of biomineralization in bryozoans and focuses on their skeletal ultrastructures, mineralogy and chemistry, the roles of organic components, the evolutionary history of bimineralization in bryozoans with respect to changes in seawater chemistry, and the impact of contemporary global changes, especially ocean acidification, on bryozoan skeletons. Bryozoan skeletons are constructed from three different wall types (exterior, interior and compound) differing in the presence/absence and location of organic cuticular layers. Skeletal ultrastructures can be classified into wall-parallel (i.e. laminated) and wall-perpendicular (i.e. prismatic) fabrics, the latter apparently found in only one of the two biomineralizing clades (Cheilostomata), which is also the only clade to biomineralize aragonite. A plethora of ultrastructural fabrics can be recognized and most occur in combination with other fabrics to constitute a fabric suite. The proportion of aragonitic and bimineralic bryozoans, as well as the Mg content of bryozoan skeletons, show a latitudinal increase into the warmer waters of the tropics. Responses of bryozoan mineralogy and skeletal thickness to oscillations between calcite and aragonite seas through geological time are equivocal. Field and laboratory studies of living bryozoans have shown that predicted future changes in pH (ocean acidification) combined with global warming are likely to have detrimental effects on calcification, growth rate and production of polymorphic zooids for defence and reproduction, although some species exhibit reasonable levels of resilience. Some key questions about bryozoan biomineralization that need to be addressed are identified.

Morphological plasticity in a calcifying modular organism: evidence from an in situ transplant experiment in a natural CO2 vent system.

Understanding is currently limited of the biological processes underlying the responses of modular organisms to climate change and the potential to adapt through morphological plasticity related to their modularity. Here, we investigate the effects of ocean acidification and seawater warming on the growth, life history and morphological plasticity in the modular bryozoan Calpensia nobilis using transplantation experiments in a shallow Mediterranean volcanic CO2 vents system that simulates pH values expected for the year 2100. Colonies exposed at vent sites grew at approximately half the rate of those from the control site. Between days 34 and 48 of the experiment, they reached a possible 'threshold', due to the combined effects of exposure time and pH. Temperature did not affect zooid length, but longer zooids with wider primary orifices occurred in low pH conditions close to the vents. Growth models describing colony development under different environmental scenarios suggest that stressed colonies of C. nobilis reallocate metabolic energy to the consolidation and strengthening of existing zooids. This is interpreted as a change in life-history strategy to support persistence under unfavourable environmental conditions. Changes in the skeletal morphology of zooids evident in C. nobilis during short-time (87 days) exposure experiments reveal morphological plasticity that may indicate a potential to adapt to the more acidic Mediterranean predicted for the future.