Diego K. Kersting

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.

Persistent natural acidification drives major distribution shifts in marine benthic ecosystems

Ocean acidification is receiving increasing attention because of its potential to affect marine ecosystems. Rare CO2 vents offer a unique opportunity to investigate the response of benthic ecosystems to acidification. However, the benthic habitats investigated so far are mainly found at very shallow water (less than or equal to 5 m depth) and therefore are not representative of the broad range of continental shelf habitats. Here, we show that a decrease from pH 8.1 to 7.9 observed in a CO2 vent system at 40 m depth leads to a dramatic shift in highly diverse and structurally complex habitats. Forests of the kelp Laminaria rodriguezii usually found at larger depths (greater than 65 m) replace the otherwise dominant habitats (i.e. coralligenous outcrops and rhodolith beds), which are mainly characterized by calcifying organisms. Only the aragonite-calcifying algae are able to survive in acidified waters, while high-magnesium-calcite organisms are almost completely absent. Although a long-term survey of the venting area would be necessary to fully understand the effects of the variability of pH and other carbonate parameters over the structure and functioning of the investigated mesophotic habitats, our results suggest that in addition of significant changes at species level, moderate ocean acidification may entail major shifts in the distribution and dominance of key benthic ecosystems at regional scale, which could have broad ecological and socio-economic implications.

Development of Microsatellite Markers as a Molecular Tool for Conservation Studies of the Mediterranean Reef Builder Coral Cladocora caespitosa (Anthozoa, Scleractinia)

Cladocora caespitosa is a reef-building zooxanthellate scleractinian coral in the Mediterranean Sea. Mortality events have recurrently affected this species during the last decade. Thus, knowledge of its genetic structure, population diversity, and connectivity is needed to accomplish suitable conservation plans. In order to obtain a better understanding of the population genetics of this species, 13 highly variable microsatellites markers were developed from a naturally bleached colony. The developed primers failed to amplify zooxanthella DNA, isolated from C. caespitosa, verifying that these markers were of the coral and not algal symbiont origin. The degree of polymorphism of these loci was tested on tissue samples from 28 colonies. The allele number for each loci ranged from 2 to 13 (mean N(a) = 5.4), with an average observed heterozygosity of 0.42 (H(e) = 0.43) and all loci were in Hardy-Weinberg equilibrium. These new markers should be useful in future conservation genetic studies and will help to improve the resolution of the individual identification within this coral species. Primers were also tested in Oculina patagonica, with successful amplifications of several loci.

Experimental evidence of the synergistic effects of warming and invasive algae on a temperate reef-builder coral.

In the current global climate change scenario, stressors overlap in space and time, and knowledge on the effects of their interaction is highly needed to understand and predict the response and resilience of organisms. Corals, among many other benthic organisms, are affected by an increasing number of global change-related stressors including warming and invasive species. In this study, the cumulative effects between warming and invasive algae were experimentally assessed on the temperate reef-builder coral Cladocora caespitosa. We first investigated the potential local adaptation to thermal stress in two distant populations subjected to contrasting thermal and necrosis histories. No significant differences were found between populations. Colonies from both populations suffered no necrosis after long-term exposure to temperatures up to 29 °C. Second, we tested the effects of the interaction of both warming and the presence of invasive algae. The combined exposure triggered critical synergistic effects on photosynthetic efficiency and tissue necrosis. At the end of the experiment, over 90% of the colonies subjected to warming and invasive algae showed signs of necrosis. The results are of particular concern when considering the predicted increase of extreme climatic events and the spread of invasive species in the Mediterranean and other seas in the future.

S.O.S. Pinna nobilis: A Mass Mortality Event in Western Mediterranean Sea

A mass mortality event impacting the bivalve Pinna nobilis was detected across a wide geographical area of the Spanish Mediterranean Sea (Western Mediterranean Sea) in early autumn 2016. Underwater visual censuses were conducted across several localities separated by hundreds of kilometres along the Spanish Mediterranean coasts and revealed worrying high mortality rates reaching up to 100% in the center and southernmost coasts of the Iberian Peninsula including Balearic Islands. Populations on the northern coasts of the Spanish Mediterranean Sea seemed to be unaffected (Catalonian region). Histological examination of affected individuals revealed the presence of a haplosporidan-like parasite within the digestive gland being probably the pathogen that causes this mortality. The present mass mortality event has spread rapidly, causing high mortality rates in infected populations. Taking into account the degree of impact, the geographic extent, and the high probability that the infection is still in a spreading phase; this might be considered the largest mass mortality event ever registered for P. nobilis up to date, forcing this emblematic bivalve into a critical viability status over hundreds of kilometers of coast.

Rolling corals in the Mediterranean Sea

Nodular morphology is typical of free-living coralline algae (Rhodophyta), which form extensive rhodolith beds worldwide over broad latitudinal and depth ranges (Foster 2001). Strikingly, under certain environmental conditions, coral coloniesmay also be able to live unattached to the substratum, as has been reported in the Atlantic, Indian and Pacific oceans (Glynn 1974; Roff 2008; Capel et al. 2012). Here, we report the occurrence of nodules of the Mediterraneanendemic reef-building coralCladocora caespitosa in Formentera (Balearic Islands, Mediterranean Sea). Cladocora caespitosa builds globose to hemispherical colonies that formbanks and beds (Peirano et al. 1998). On the islet of Espardelló (Formentera), C. caespitosa colonies make unique beds composed mainly of small colonies (under 10 cm in diameter) that occur in high densities on a rocky bottom dominated by erect macroalgae (mainlyCystoseira spinosa) between6and14 mdepth.Manyof the coral colonies are unattached and display a nodular morphology characterized by spherical growth (i.e., polyps growing in all directions) (Fig. 1a). These coral nodules or coralliths occur among algae on mixed rock and coarse sand bottoms and accumulate in highnumbers indepressions, togetherwith coralline algal rhodoliths (Lithophyllum racemus, L. coralloides and other species) (Fig. 1b). We hypothesize that this unusual coral morphology may be the result of periodical wave-induced turnover of small coral colony fragments inside the algal forest.Coralliths are foundalive inside the algal forest, while living and totally or partially dead coralliths are found together in the rocky depressionswhere frondosemacroalgae are absent (Fig. 1b). This is the first report of high abundances of free-living nodular corals in the Mediterranean Sea.

Regional genetic differentiation among populations of Cladocora caespitosa in the Western Mediterranean

Cladocora caespitosa is the only reef-forming zooxanthellate scleractinian in the Mediterranean Sea. This endemic coral has suffered severe mortality events at different Mediterranean sites owing to anomalous summer heat waves related to global climate change. In this study, we assessed genetic structure and gene flow among four populations of this species in the Western Mediterranean Sea: Cape Palos (SE Spain), Cala Galdana (Balearic Islands), Columbretes Islands, and L’Ametlla (NE Spain). The results obtained from Bayesian approaches, FST statistics, and Bayesian analysis of migration rates suggest certain levels of genetic differentiation driven by high levels of self-recruitment, a fact that is supported by egg-retention mechanisms. Conversely, genetic connectivity among distant populations, even if generally low, seems to be related to sporadic dispersal events through regional surface currents linked to the spawning period that occurs at the end of summer-beginning of autumn. These features, together with a certain isolation of the Columbretes Islands, could explain the regional genetic differentiation found among populations. These results help to better understand population structure and connectivity of the species and will serve as an approach for further studies on different aspects of the biology and ecology of C. caespitosa.

Biogeographic Differences in the Microbiome and Pathobiome of the Coral Cladocora caespitosa in the Western Mediterranean Sea

The endemic Mediterranean zooxanthellate scleractinian reef-builder Cladocora caespitosa is among the organisms most affected by warming-related mass mortality events in the Mediterranean Sea. Corals are known to contain a diverse microbiota that plays a key role in their physiology and health. Here we report the first study that examines the microbiome and pathobiome associated with C. caespitosa in three different Mediterranean locations (i.e., Genova, Columbretes Islands, and Tabarca Island). The microbial communities associated with this species showed biogeographical differences, but shared a common core microbiome that probably plays a key role in the coral holobiont. The putatively pathogenic microbial assemblage (i.e., pathobiome) of C. caespitosa also seemed to depend on geographic location and the human footprint. In locations near the coast and with higher human influence, the pathobiome was entirely constituted by Vibrio species, including the well-known coral pathogens Vibrio coralliilyticus and V. mediterranei. However, in the Columbretes Islands, located off the coast and the most pristine of the analyzed locations, no changes among microbial communities associated to healthy and necrosed samples were detected. Hence, our results provide new insights into the microbiome of the temperate corals and its role in coral health status, highlighting its dependence on the local environmental conditions and the human footprint.

Diseases of coralline algae in the Mediterranean Sea

Diseases of coralline algae, first reported in the 1990s in the Pacific (Littler and Littler 1995), have recently been reported associatedwith high seawater temperature in several localities in the Caribbean (Quéré et al. 2015). Here, we report the first record of coralline algal diseases similar to the previously described corallinewhite band syndrome (CWBS) and corallinewhite patch disease (CWPD) in a temperate sea. In October 2015, after a summer characterized by positive thermal anomalies, we observed mortality affecting coralline algae at depths ranging from 0 tomore than 30 m at three northwestern Mediterranean sites separated by hundreds of kilometers: Medes Islands (42 03¢N, 3 13¢E), Cap de Creus (42 19¢N, 3 19¢E), and Columbretes Islands (39 53¢N, 0 41¢E). CWBS, characterized by a welldefined white band, affected crustose coralline algae, mainly Lithophyllum incrustans (Fig. 1a),Mesophyllum alternans (Fig. 1b), and Neogoniolithon mamillosum (Fig. 1c). The dead tissue associated with the disease appeared greenish, probably colonized by endophytic algae (Ballantine et al. 2005). The extent of injuries varied in diameter from several centimeters to about 1 m.CWPDaffected the same species, togetherwith thegeniculate coralline algae Corallina elongata (Fig. 1d), Jania rubens, and Amphiroa rigida at shallowdepths.These species showedadiffusewhite discoloration affecting the living algal tissue. In some cases, coralline algae had completely disappeared leaving bare rock areas. This process may have been enhanced by grazing by sea urchins. The emergence of thermo-dependent diseases may pose a new threat toMediterranean coralligenous ecosystems in the context of global warming.

Cetáceos en la Reserva Marina de las Islas Columbretes (Mediterráneo noroccidental): 20 años de avistamientos oportunistas

espanolEn el presente trabajo se recopilan veinte anos de observaciones realizadas por los servicios de vigilancia de la Reserva Marina y Reserva Natural de las Islas Columbretes, asi como aquellas notificadas por embarcaciones de recreo y pesca, desde la creacion de la reserva en 1990. Las observaciones fueron realizadas durante todo el ano en el interior de la Reserva Marina e inmediaciones. Por avistamiento se ha anotado la especie, el tamano de grupo, hora y situacion aproximada. Para cada especie se ha analizado la presencia a lo largo de los meses del ano, la distancia a las islas y el tamano de los grupos. Se han obtenido datos de un total de 366 observaciones y 4928 individuos. La especie mas frecuente ha sido el delfin mular Tursiops truncatus con el 71 % de las observaciones totales, seguida por el rorcual comun Balaenoptera physalus (20 %), delfin listado Stenella coeruleoalba (5 %), delfin comun Delphinus delphis (1.4 %), y con porcentajes inferiores al 1%: calderon comun Globicephala melas, calderon gris Grampus griseus, cachalote Physeter catodon y orca Orcinus orca. La presencia constante de delfin mular en la Reserva Marina durante estos 20 anos es una evidencia de que la proteccion de estas aguas ha contribuido a la conservacion de esta especie en la zona. Por otra parte, las observaciones de rorcual comun al este de la Reserva Marina indican la existencia de una zona de paso de los individuos en su migracion latitudinal. EnglishAll the observations of cetaceans registered by the wardens of the Columbretes Islands Marine Reserve and Natural Reserve since 1990, as well as those made by fishing and touristic boats, have been compiled in this work. The opportunistic sightings were made inside the Marine Reserve and the surrounding area. For each sighting the following data was registered: species, group size, time of the day and geographical location. For each cetacean species temporal presence, distance to the islands and group size was analyzed. An overall of 366 observations were made during these 20 years and 4928 individuals were registered. The most common species was the bottlenose dolphin Tursiops truncatus with 71 % of the observations. The other observed species and their sightings percentage are as follows: fin whale Balaenoptera physalus (20 %), striped dolphin Stenella coeruleoalba (5 %), common delphin Delphinus delphis (1.4 %), and under 1 %: long finned pilot whale Globicephala melas, Rissos dolphin Grampus griseus, sperm whale Physeter catodon and killer whale Orcinus orca. The continuous presence of the bottlenose dolphin in the Marine Reserve during these 20 years evidences that the protection of these waters has played an important role in the conservation of these species. The repeated sightings of the fin whale to the east of the Marine Reserve show the existence of a migratory passage near the Columbretes Islands.