Nathaniel Bensoussan

Temperature Anomalies and Mortality Events in Marine Communities: Insights on Factors behind Differential Mortality Impacts in the NW Mediterranean

Two large-scale mass mortality events (MMEs) of unprecedented extent and severity affecting rocky benthic communities occurred during the summers of 1999 and 2003 along the coasts of the NW Mediterranean Sea. These mortality outbreaks were associated with positive thermal anomalies. In this study, we performed an analysis of inter-regional and inter-annual differences in temperature (T) conditions associated with MMEs of the red gorgonian Paramuricea clavata by analyzing high resolution T time series (hourly records for 3 to 8 years) from four regions of the NW Mediterranean with differing hydrological conditions and biological impacts. High resolution records allowed a detailed analysis using classical and new descriptors to characterize T anomalies. We were able to determine that the MMEs were triggered by two main types of positive thermal anomalies, with the first type being characterized by short periods (2 to 5 days) with high Mean T reaching more than 27°C in some regions and being associated with high intra-day and intra-period variability, while the second type of anomaly presented long duration (near one month) at warm T (24°C) with low intra-period variability. Inter-regional patterns arose; some regions displayed both types of anomalies, while others exhibited only one type. The results showed that T conditions should be considered as the main factor that explains the observed inter-regional and inter-annual differences in mortality impacts. In explaining these differences, the late timing of T anomalies, in addition to their magnitude was found to be determinant. Finally, by combining thermotolerance experimental data with the maximal T stress conditions observed in the four regions, we were able to determine the differential risk of mass mortality across regions. We conclude that expanding high resolution T series is important for the development of sound management and conservation plans to protect Mediterranean marine biodiversity in the face of climate change.

Long-term responses of the endemic reef-builder Cladocora caespitosa to Mediterranean warming

Recurrent climate-induced mass-mortalities have been recorded in the Mediterranean Sea over the past 15 years. Cladocora caespitosa, the sole zooxanthellate scleractinian reef-builder in the Mediterranean, is among the organisms affected by these episodes. Extensive bioconstructions of this endemic coral are very rare at the present time and are threatened by several stressors. In this study, we assessed the long-term response of this temperate coral to warming sea-water in the Columbretes Islands (NW Mediterranean) and described, for the first time, the relationship between recurrent mortality events and local sea surface temperature (SST) regimes in the Mediterranean Sea. A water temperature series spanning more than 20 years showed a summer warming trend of 0.06°C per year and an increased frequency of positive thermal anomalies. Mortality resulted from tissue necrosis without massive zooxanthellae loss and during the 11-year study, necrosis was recorded during nine summers separated into two mortality periods (2003–2006 and 2008–2012). The highest necrosis rates were registered during the first mortality period, after the exceptionally hot summer of 2003. Although necrosis and temperature were significantly associated, the variability in necrosis rates during summers with similar thermal anomalies pointed to other acting factors. In this sense, our results showed that these differences were more closely related to the interannual temperature context and delayed thermal stress after extreme summers, rather than to acclimatisation and adaption processes.

Physiological response of the symbiotic gorgonian Eunicella singularis to a long-term temperature increase.

SUMMARY Increase in seawater temperature is one of the major effects of global climate change that affects marine organisms, including Cnidaria. Among them, gorgonians from the NW Mediterranean Sea, such as the species Eunicella singularis, have suffered spectacular and extensive damage. We thus investigated in a controlled laboratory experiment the response of E. singularis to a long-term increase in temperature and we took a special interest in its photosynthetic and calcification response to the stress. Two populations collected at 15 and 35 m depths were studied in order to determine whether there was a difference in sensitivity to thermal stress between living depths. Our results show: (a) that calcification and photosynthesis were impacted only when gorgonians were maintained for more than two weeks at 26°C, and (b) that colonies of E. singularis living in shallow waters were less tolerant than those living in deep waters. Because E. singularis is a symbiotic species, we have also discussed the potential role of symbiosis in the thermotolerance response.

Seasonal and interannual variations (1996–2000) of the coastal waters east of the Rhone river mouth as indicated by the SORCOM series

Between 1996 and 2000, 79 cruises have been achieved following always the same transect between Marseilles and the Rhone river’s mouth. While cruising, salinity, temperature and fluorescence of surface waters (1.5 m) were recorded every minute, in association with precise GPS position. The whole set of data (i.e. 128 measured points per cruise) constitutes the Sorcom series whose synthetic results are presented here. Despite the high spatial and temporal variability encountered between two successive cruises, the regularity and duration of the sampling strategy permitted to define coherent spatial zonation and temporal evolutions. In the Cape Couronne vicinity the dynamic of the eastern extension of the dilution plume clearly changes. Westward, waters are frequently under its influence, but more sporadically to the east, with a less pronounced gradient. In few cases, salinity lowering has been measured up to the gulf of Marseilles. In these two areas, which can be divided in two sub zones, seasonal evolutions are different. In the eastern area (Cape Couronne–Marseilles), the classical rhythm prevailing over marine waters is observed but with earlier phytoplanktonic bloom than usually reported. In the western part, and as getting closer to the Rhone river mouth, a weaker seasonal variability is observed for the phytoplanktonic biomass then salinity and temperature differences remain high. The better knowledge of the eastern dilution plume is of important socio-economical concern due to the numerous population living on this coast and the presence of pollutants in the river waters.

Potential for adaptive evolution at species range margins: contrasting interactions between red coral populations and their environment in a changing ocean

Studying population-by-environment interactions (PEIs) at species range margins offers the opportunity to characterize the responses of populations facing an extreme regime of selection, as expected due to global change. Nevertheless, the importance of these marginal populations as putative reservoirs of adaptive genetic variation has scarcely been considered in conservation biology. This is particularly true in marine ecosystems for which the deep refugia hypothesis proposes that disturbed shallow and marginal populations of a given species can be replenished by mesophotic ones. This hypothesis therefore assumes that identical PEIs exist between populations, neglecting the potential for adaptation at species range margins. Here, we combine reciprocal transplant and common garden experiments with population genetics analyses to decipher the PEIs in the red coral, Corallium rubrum. Our analyses reveal partially contrasting PEIs between shallow and mesophotic populations separated by approximately one hundred meters, suggesting that red coral populations may potentially be locally adapted to their environment. Based on the effective population size and connectivity analyses, we posit that genetic drift may be more important than gene flow in the adaptation of the red coral. We further investigate how adaptive divergence could impact population viability in the context of warming and demonstrate differential phenotypic buffering capacities against thermal stress. Our study questions the relevance of the deep refugia hypothesis and highlights the conservation value of marginal populations as a putative reservoir of adaptive genetic polymorphism.

Separate the wheat from the chaff: genomic analysis of local adaptation in the red coral Corallium rubrum

Genomic data allow an in-depth and renewed study of local adaptation. The red coral (Corallium rubrum, Cnidaria) is a highly genetically structured species and a promising model for the study of adaptive processes along an environmental gradient. Here, we used RAD-Sequencing in order to study the vertical genetic structure of this species and to search for signals of local adaptation to depth and thermal regime in the red coral. Previous studies have shown different thermotolerance levels according to depth in this species which could correspond to genetic or environmental differences. We designed a sampling scheme with six pairs of ‘shallow vs deep’ populations distributed in three geographical regions as replicates. Our results showed significant differentiation among locations and among sites separated by around 20 m depth. The tests of association between genetics and environment allowed the identification of candidate loci under selection but with a potentially high rate of false positive. We discuss the methodological obstacles and biases encountered for the detection of selected loci in such a strongly genetically structured species. On this basis, we discuss the significance of the candidate loci for local adaptation detected in each geographical region and the evolution of red coral populations along environmental gradients.

Biologists ignore ocean weather at their peril

Ecologists must understand how marine life responds to changing local conditions, rather than to overall global temperature rise, say Amanda E. Bates and 16 colleagues.Ecologists must understand how marine life responds to changing local conditions, rather than to overall global temperature rise.

Regional and local environmental conditions do not shape the response to warming of a marine habitat-forming species

The differential response of marine populations to climate change remains poorly understood. Here, we combine common garden thermotolerance experiments in aquaria and population genetics to disentangle the factors driving the population response to thermal stress in a temperate habitat-forming species: the octocoral Paramuricea clavata. Using eight populations separated from tens of meters to hundreds of kilometers, which were differentially impacted by recent mortality events, we identify 25 °C as a critical thermal threshold. After one week of exposure at this temperature, seven of the eight populations were affected by tissue necrosis and after 30 days of exposure at this temperature, the mean % of affected colonies increased gradually from 3 to 97%. We then demonstrate the weak relation between the observed differential phenotypic responses and the local temperature regimes experienced by each population. A significant correlation was observed between these responses and the extent of genetic drift impacting each population. Local adaptation may thus be hindered by genetic drift, which seems to be the main driver of the differential response. Accordingly, conservation measures should promote connectivity and control density erosion in order to limit the impact of genetic drift on marine populations facing climate change.