Rafael Coma

Global warming-enhanced stratification and mass mortality events in the Mediterranean

Summer conditions in the Mediterranean Sea are characterized by high temperatures and low food availability. This leads to “summer dormancy” in many benthic suspension feeders due to energetic constraints. Analysis of the most recent 33-year temperature time series demonstrated enhanced stratification due to global warming, which produced a ≈40% lengthening of summer conditions. Many biological processes are expected to be affected by this trend, culminating in such events as mass mortality of invertebrates. Climatic anomalies concomitant with the occurrence of these events represent prolonged exposure to warmer summer conditions coupled with reduced food resources. Simulation of the effects of these conditions on a model organism demonstrated a biomass loss of >35%. Losses of this magnitude result in mortality similar to that noted in field observations during mass mortality events. These results indicate that temperature anomalies are the underlying cause of the events, with energetic constraints serving as the main triggering mechanism.

From global to local genetic structuring in the red gorgonian Paramuricea clavata: the interplay between oceanographic conditions and limited larval dispersal.

Defining the scale of connectivity among marine populations and identifying the barriers to gene flow are tasks of fundamental importance for understanding the genetic structure of populations and for the design of marine reserves. Here, we investigated the population genetic structure at three spatial scales of the red gorgonian Paramuricea clavata (Cnidaria, Octocorallia), a key species dwelling in the coralligenous assemblages of the Mediterranean Sea. Colonies of P. clavata were collected from 39 locations across the Mediterranean Sea from Morocco to Turkey and analysed using microsatellite loci. Within three regions (Medes, Marseille and North Corsica), sampling was obtained from multiple locations and at different depths. Three different approaches (measures of genetic differentiation, Bayesian clustering and spatially explicit maximum‐difference algorithm) were used to determine the pattern of genetic structure. We identified genetic breaks in the spatial distribution of genetic diversity, which were concordant with oceanographic conditions in the Mediterranean Sea. We revealed a high level of genetic differentiation among populations and a pattern of isolation by distance across the studied area and within the three regions, underlining short effective larval dispersal in this species. We observed genetic differentiation among populations in the same locality dwelling at different depths, which may be explained by local oceanographic conditions and which may allow a process of local adaptation of the populations to their environment. We discuss the implications of our results for the conservation of the species, which is exposed to various threats.

Functional convergence of microbes associated with temperate marine sponges.

Most marine sponges establish a persistent association with a wide array of phylogenetically and physiologically diverse microbes. To date, the role of these symbiotic microbial communities in the metabolism and nutrient cycles of the sponge-microbe consortium remains largely unknown. We identified and quantified the microbial communities associated with three common Mediterranean sponge species, Dysidea avara, Agelas oroides and Chondrosia reniformis (Demospongiae) that cohabitate coralligenous community. For each sponge we quantified the uptake and release of dissolved organic carbon (DOC) and nitrogen (DON), inorganic nitrogen and phosphate. Low microbial abundance and no evidence for DOC uptake or nitrification were found for D. avara. In contrast A. oroides and C. reniformis showed high microbial abundance (30% and 70% of their tissue occupied by microbes respectively) and both species exhibited high nitrification and high DOC and NH(4) (+) uptake. Surprisingly, these unique metabolic pathways were mediated in each sponge species by a different, and host specific, microbial community. The functional convergence of microbial consortia found in these two sympatric sponge species, suggest that these metabolic processes may be of special relevance to the success of the holobiont.

Sea Urchins Predation Facilitates Coral Invasion in a Marine Reserve

Macroalgae is the dominant trophic group on Mediterranean infralittoral rocky bottoms, whereas zooxanthellate corals are extremely rare. However, in recent years, the invasive coral Oculina patagonica appears to be increasing its abundance through unknown means. Here we examine the pattern of variation of this species at a marine reserve between 2002 and 2010 and contribute to the understanding of the mechanisms that allow its current increase. Because indirect interactions between species can play a relevant role in the establishment of species, a parallel assessment of the sea urchin Paracentrotus lividus, the main herbivorous invertebrate in this habitat and thus a key species, was conducted. O. patagonica has shown a 3-fold increase in abundance over the last 8 years and has become the most abundant invertebrate in the shallow waters of the marine reserve, matching some dominant erect macroalgae in abundance. High recruitment played an important role in this increasing coral abundance. The results from this study provide compelling evidence that the increase in sea urchin abundance may be one of the main drivers of the observed increase in coral abundance. Sea urchins overgraze macroalgae and create barren patches in the space-limited macroalgal community that subsequently facilitate coral recruitment. This study indicates that trophic interactions contributed to the success of an invasive coral in the Mediterranean because sea urchins grazing activity indirectly facilitated expansion of the coral. Current coral abundance at the marine reserve has ended the monopolization of algae in rocky infralittoral assemblages, an event that could greatly modify both the underwater seascape and the sources of primary production in the ecosystem.

Microbial diversity and putative diazotrophy in high and low microbial abundance Mediterranean sponges

ABSTRACT Microbial communities associated with marine sponges carry out nutrient transformations essential for benthic-pelagic coupling; however, knowledge about their composition and function is still sparse. We evaluated the richness and diversity of prokaryotic assemblages associated with three high-microbial-abundance (HMA) and three low-microbial-abundance (LMA) sympatric Mediterranean sponges to address their stability and uniqueness. Moreover, to examine functionality and because an imbalance between nitrogen ingestion and excretion has been observed for some of these species, we sequenced nitrogenase genes (nifH) and measured N2 fixation. The prokaryotic communities in the two sponge types did not differ in terms of richness, but the highest diversity was found in HMA sponges. Moreover, the discrete composition of the communities in the two sponge types relative to that in the surrounding seawater indicated that horizontal transmission and vertical transmission affect the microbiomes associated with the two sponge categories. nifH genes were found in all LMA species and sporadically in one HMA species, and about half of the nifH gene sequences were common between the different sponge species and were also found in the surrounding water, suggesting horizontal transmission. 15N2-enriched incubations showed that N2 fixation was measurable in the water but was not associated with the sponges. Also, the analysis of the isotopic ratio of 15N to 14N in sponge tissue indicated that N2 fixation is not an important source of nitrogen in these Mediterranean sponges. Overall, our results suggest that compositional and functional features differ between the prokaryotic communities associated with HMA and LMA sponges, which may affect sponge ecology.

Specificity and temporal dynamics of complex bacteria-sponge symbiotic interactions

Microbes are known to form intricate and intimate relationships with most animal and plant taxa. Microbe--host symbiotic associations are poorly explored in comparison with other species interaction networks. The current paradigm on symbiosis research stems from species-poor systems where pairwise and reciprocally specialized interactions between a single microbe and a single host that coevolve are the norm. These symbioses involving just a few species are fascinating in their own right, but more diverse and complex host-associated microbial communities are increasingly found, with new emerging questions that require new paradigms and approaches. Here we adopt an intermediate complexity approach to study the specificity, phylogenetic community structure, and temporal variability of the subset of the most abundant bacteria associated with different sponge host species with diverse eco-evolutionary characteristics. We do so by using a monthly resolved annual temporal series of host-associated and free-living bacteria. Bacteria are very abundant and diverse within marine sponges, and these symbiotic interactions are hypothesized to have a very ancient origin. We show that host-bacteria reciprocal specialization depends on the temporal scale and level of taxonomic aggregation considered. Sponge hosts with similar eco-evolutionary characteristics (e.g., volume of tissue corresponding to microbes, water filtering rates, and microbial transmission type) have similar bacterial phylogenetic community structure when looking at interactions aggregated over time. In general, sponge hosts hypothesized to form more intricate relationships with bacteria show a remarkably persistent bacterial community over time. Other hosts, however, show a large turnover similar to that observed for free-living bacterioplankton. Our study highlights the importance of exploring temporal variability in host--microbe interaction networks if we aim to determine how specific and persistent these poorly explored but extremely common interactions are.

Evidence for coral range expansion accompanied by reduced diversity of Symbiodinium genotypes

Zooxanthellate corals are threatened by climate change but may be able to escape increasing temperatures by colonizing higher latitudes. To determine the effect of host range expansion on symbiont genetic diversity, we examined genetic variation among populations of Symbiodinium psygmophilum associated with Oculina patagonica, a range-expanding coral that acquires its symbionts through horizontal transmission. We optimized five microsatellite primer pairs for S. psygmophilum and tested them on Oculina spp. samples from the western North Atlantic and the Mediterranean. We then used them to compare symbiont genotype diversity between an Iberian core and an expansion front population of O. patagonica. Only one multilocus S. psygmophilum genotype was identified at the expansion front, and it was shared with the core population, which harbored seven multilocus genotypes. This pattern suggests that O. patagonica range expansion is accompanied by reduced symbiont genetic diversity, possibly due to limited dispersal of symbionts or local selection.

Polyp bail-out by the coral Astroides calycularis (Scleractinia, Dendrophylliidae)

Knowledge of reproductive biology is essential for ecological studies on coral population dynamics. The azooxanthellate colonial coral Astroides calycularis is endemic to the western Mediterranean Sea and adjacent Atlantic coasts. Specimens of this species in artificial conditions, an aquarium with enclosed seawater and low food availability, appeared to show an asexual dispersal mechanism. This mechanism consisted of the detachment and release of single, skeletonless polyps from the underlying colony skeleton (i.e., polyp bail-out). While the released free-living polyps regularly showed extended tentacles and most of them survived, they did not show re-attachment to the substrate or any skeleton formation until the end of the experiment, ∼2–3 months after bail-out. Formation of new reproductive colonies, thereby the eventual completion of asexual reproduction through polyp bail-out in A. calycularis, still needs to be confirmed. In addition to sexual reproduction, polyp bail-out may constitute an alternative propagation mechanism during periods of environmental stress, thereby potentially increasing the survival rate of the parental genotype and the dispersal by drifting soft polyps.

Demographics of the zooxanthellate coral Oculina patagonica along the Mediterranean Iberian coast in relation to environmental parameters

Marine ecosystems are threatened by cumulative human-related impacts that cause structural and functional alterations. In the Mediterranean Sea, the zooxanthellate coral Oculina patagonica (Scleractinia, Oculinidae) can turn algal forests into coral-dominated ecosystems and provides a case study for examining how zooxanthellate corals can affect the structure of algal-dominated shallow-water rocky ecosystems in temperate areas. Our goal was to provide a quantitative baseline assessment of O. patagonica demographics along ~1300km of the Mediterranean Iberian coast and relate them to environmental parameters. The highest coral success was in the South Balearic Sea zone, where the populations exhibited >6-fold higher mean living coral cover, lower partial colony mortality and colony size distributions indicating that the populations in this zone were growing faster than those in the peripheral south-west (North Alborán Sea) and north-east (Mid and North Balearic Sea, and West Gulf of Lyons) zones. The coral demographics (i.e., density, cover, and skewness and kurtosis coefficients of colony size distributions) were positively correlated with each other and the annual mean seawater temperature (ST), 10th-ST percentile (P10th-ST), 90th-ST percentile (P90th-ST) and photosynthetically active radiation at 3-m depth (PAR-3m), but they were negatively correlated with chlorophyll-a. Based on these results, we identified the following thresholds that may constrain the growth of O. patagonica colonies and populations: annual mean ST <19-20°C, P10th-ST <14°C, P90th-ST <25°C and >27°C, and PAR-3m <30molphotonsm-2day-1. The species abundance along the Iberian coast conforms to the abundant-center pattern of distribution. However, the coral demographics indicated that this pattern was not only related to the time of establishment but also to differences in coral population growth, which were correlated with key environmental parameters. Our results contribute understanding of the forces driving population growth of O. patagonica and support the hypothesis of an ongoing coral-mediated tropicalization of macroalgae-dominated temperate ecosystems.

Host-targeted RAD-Seq reveals genetic changes in the coral Oculina patagonica associated with range expansion along the Spanish Mediterranean coast

Many organisms are expanding their ranges in response to changing environmental conditions. Understanding the patterns of genetic diversity and adaptation along an expansion front is crucial to assessing a species’ long‐term success. While next‐generation sequencing techniques can reveal these changes in fine detail, ascribing them to a particular species can be difficult for organisms that live in close association with symbionts. Using a novel modified restriction site‐associated DNA sequencing (RAD‐Seq) protocol to target coral DNA, we collected 595 coral‐specific single nucleotide polymorphisms from 189 colonies of the invasive coral Oculina patagonica from the Spanish Mediterranean coast, including established core populations and two expansion fronts. Surprisingly, populations from the recent northern expansion are genetically distinct from the westward expansion and core populations and also harbour greater genetic diversity. We found that temperature may have driven adaptation along the northern expansion, as genome scans for selection found three candidate loci associated with temperature in the north but none in the west. We found no genomic signature of selection associated with artificial substrate, which has been proposed for explaining the rapid spread of O. patagonica. This suggests that this coral is simply an opportunistic colonizer of free space made available by coastal habitat modifications. Our results suggest that unique genetic variation, possibly due to limited dispersal across the Ibiza Channel, an influx of individuals from different depths and/or adaptation to cooler temperatures along the northern expansion front may have facilitated the northward range expansion of O. patagonica in the western Mediterranean.