Search

Este artículo contiene 18 páginas, 4 figuras., Climate change is causing an increase in the frequency and intensity of marine heatwaves (MHWs) and mass mortality events (MMEs) of marine organisms are one of their main ecological impacts. Here, we show that during the 2015–2019 period, the Mediterranean Sea has experienced exceptional thermal conditions resulting in the onset of five consecutive years of widespread MMEs across the basin. These MMEs affected thousands of kilometers of coastline from the surface to 45 m, across a range of marine habitats and taxa (50 taxa across 8 phyla). Significant relationships were found between the incidence of MMEs and the heat exposure associated with MHWs observed both at the surface and across depths. Our findings reveal that the Mediterranean Sea is experiencing an acceleration of the ecological impacts of MHWs which poses an unprecedented threat to its ecosystems' health and functioning. Overall, we show that increasing the resolution of empirical observation is critical to enhancing our ability to more effectively understand and manage the consequences of climate change., This paper was supported by Euromarine. Joaquim Garrabou acknowledges the funding by the “Severo Ochoa Centre of Excellence” (CEX2019-000928-S), the MCIU/AEI/FEDER [HEATMED; RTI2018-095346-B-I00], Interreg-Med Programme MPA-Engage (1MED15_3.2_M2_337), the European Union Horizon 2020 research and innovation programme (Futuremares SEP-210597628). Nuria Teixido acknowledges the French National Research Agency (4Oceans-MOPGA grant, ANR-17-MPGA-0001) and internal funds from the Stazione Zoologica Anton Dohrn. Gil Rilov was supported by the Israel Ministry of Environmental Protection. Hocein Bazairi, Free Spinosa, and Vasilis Gerovasileiou acknowledge the funding by the MAVA Fondation (MedKeyHabitats I Project) and the European Commission (Ecap-MED II Project; projects implemented by UNEP/MAP-RAC/SPA). Alfonso Ramos was supported the CIESM “Tropical Signals,” Stelios Katsanevakis and Maria Sini were supported by the Project “Coastal Environment Observatory and Risk Management in Island Regions AEGIS+” (MIS 5047038), implemented within the Operational Programme “Competitiveness, Entrepreneurship and Innovation” (NSRF 2014–2020), co-financed by the Hellenic Government (Ministry of Development and Investments) and the European Union (European Regional Development Fund, Cohesion Fund), Stelios Katsanevakis, Maria Sini and Vasilis Gerovasileiou acknowledge the support of the MARISCA Project, co-funded by 85% by the EEA GRANTS, 2009–2014, and 15% by the Public Investments Programme (PIP) of the Hellenic Republic. Ivan Guala and Daniele Grech thanks thank the support of the project “Pinna nobilis—ricerca per la sopravvivenza: un'iniziativa di Citizen Science per tracciare la mortalità di massa di Pinna nobilis in Sardegna” project and the L/7 grant (CUP 87G17000070002) funded by the Regione Autonoma Sardegna. Jean-Baptiste Ledoux was funded by an assistant researcher contract framework of the RD Unit—UID/Multi/04423/2019—Interdisciplinary Centre of Marine and Environmental Research—financed by the European Regional Development Fund (ERDF) through COMPETE2020—Operational Program for Competitiveness and Internationalization (POCI) and national funds through FCT/MCTES (PIDDAC). This research was supported by the Strategic Funding UIDB/04423/2020 and UIDP/04423/2020 through national funds provided by the FCT—Foundation for Science and Technology and European Regional Development Fund (ERDF), in the framework of the program PT2020. Bernat Hereu and Cristina Linares acknowledge the support of the long-term monitoring programme of the catalan Natural Parks, funded by the Departament de Territori i Sostenibilitat of the Generalitat de Catalunya. Cristina Linares acknowledges the support of the ICREA Academia programme. David Díaz acknowledges the support the research grant CTM2016-77027-R of the Programa Estatal de Investigación, Desarrollo e Innovación Orientada a los Retos de la Sociedad and Program of Marines Strategies of Spain funded by MITERD. Jamila Ben Soussi was partially funded by the Fondation Albert 2 Monaco (MIMOSA Project) and the Tropical Signals Program of CIESM. Giovanni Chimienti was supported by the Italian Ministry of Education, University and Research (PON 2014–2020, AIM 1807508–1, Linea 1), by the Ente Parco Nazionale del Gargano (Research agreement with CoNISMa N. 21/2018), and by the National Geographic Society (Grant EC-176R-18). Nathaniel Bensoussan acknowledges financial support from the European Commission through the programme “Caroline Herschell” in the context of the action “Developing Downstream applications and services on BIO-PHYsical characterization of the seascape for COASTal management” (BIOPHYCOAST). Monica Montefalcone and Annalissa Azzola collected some of their data on MMEs in the frame of the project “Mare Caldo” funded by Greenpeace Italy. Núria Marbà acknowledges financial support from the Spanish Ministries of Economy and Competitiveness (CTM2012-32603, CGL2015-71809-P) and Ministerio de Ciencia, Innovación y Universidades (RTI2018-095441-B-C21). Diego K. Kersting acknowledges support by the postdoctoral fellowship programme Beatriu de Pinós funded by the Secretary of Universities and Research (Government of Catalonia) and the Horizon 2020 programme of research and innovation of the European Union under the Marie Sklodowska-Curie grant agreement No 801370.

Marine heatwaves (MHWs) are periods of extremely high seawater temperature that affect marine ecosystems in several ways. Anthozoans (corals and gorgonians) and Porifera (sponges) are usually among the taxa most affected by MHWs. Both are holobiont entities that form complex interactions with a wide range of microbes, which are an essential part of these organisms and play key roles in their health status. Here, we determine microbial community changes suffered in two corals (Cladocora caespitosa and Oculina patagonica), one gorgonian (Leptogorgia sarmentosa), and one sponge (Sarcotragus fasciculatus) during the 2015 MHW. The microbial communities were different among hosts and displayed shifts related to host health status, with a higher abundance in necrosed tissues of Ruegeria species or of potential pathogens like Vibrio. We also carry out a meta-analysis using 93 publicly accessible 16S rRNA gene libraries from O. patagonica, C. caespitosa and L. sarmentosa to establish a Mediterranean core microbiome in these species. We have identified one Ruegeria OTU that maintained a stable and consistent association with these species, which was also related with tissue necrosis in their hosts. Therefore, Ruegeria sp. could play an important and still underexplored role in the health status of its hosts.

The microbialization of coral reefs predicts that microbial oxygen consumption will cause reef deoxygenation. Here we tested this hypothesis by analyzing reef microbial and primary producer oxygen metabolisms. Metagenomic data and in vitro incubations of bacteria with primary producer exudates showed that fleshy algae stimulate incomplete carbon oxidation metabolisms in heterotrophic bacteria. These metabolisms lead to increased cell sizes and abundances, resulting in bacteria consuming 10 times more oxygen than in coral incubations. Experiments probing the dissolved and gaseous oxygen with primary producers and bacteria together indicated the loss of oxygen through ebullition caused by heterogenous nucleation on algae surfaces. A model incorporating experimental production and loss rates predicted that microbes and ebullition can cause the loss of up to 67% of gross benthic oxygen production. This study indicates that microbial respiration and ebullition are increasingly relevant to reef deoxygenation as reefs become dominated by fleshy algae., eLife digest Rising water temperatures, pollution and other factors are increasingly threatening corals and the entire reef ecosystems they build. The potential for corals to resist and recover from the stress these factors cause ultimately depends on their ability to compete against fast-growing fleshy algae that can rapidly take over the reefs. Living on the fleshy algae, the coral and in the surrounding water are communities of bacteria and other microbes that help maintain the health of the coral reef. Both corals and algae modify the chemical and physical environment of the reef to alter the composition of the microbial communities for their own benefit. Algae, for instance, release large amounts of sugars and other molecules of organic carbon into the water. These carbon molecules are then taken up by the bacteria, along with oxygen, to produce chemical energy via a process called respiration. This could cause the levels of oxygen in the water to decrease, potentially damaging the corals and creating more open space for the algae. Previous studies have revealed how communities of microbes on coral reefs use organic carbon, but it remains unclear how they affect the levels of oxygen in the reefs. To address this question, Silveira et al. used an approach called metagenomics to analyze the bacteria in samples of water from 87 reefs across the Pacific and the Caribbean, and also performed experiments with reef bacteria grown in the laboratory. The experiments showed that bacteria growing in the presence of fleshy algae became larger and more abundant than bacteria growing near corals, resulting in the water containing lower levels of oxygen. Furthermore, the fleshy algae produced bubbles of oxygen that were released from the water. Silveira et al. developed a mathematical model that predicted that these bubbles, combined with the respiration of bacteria that live near algae, caused the loss of 67% of the oxygen in the water surrounding the reef. These findings represent a fundamental step towards understanding how changes in the levels of oxygen in water affect the ability of coral reefs to resist and recover from stress.

Corals are known to contain a diverse microbiota that plays a paramount role in the physiology and health of holobiont. However, few studies have addressed the variability of bacterial communities within the coral host. In this study, bacterial community composition from the mucus, tissue and skeleton of the scleractinian coral Oculina patagonica were investigated seasonally at two locations in the Western Mediterranean Sea, to further understand how environmental conditions and the coral microbiome structure are related. We used denaturing gradient gel electrophoresis in combination with next-generation sequencing and electron microscopy to characterize the bacterial community. The bacterial communities were significantly different among coral compartments, and coral tissue displayed the greatest changes related to environmental conditions and coral health status. Species belonging to the Rhodobacteraceae and Vibrionaceae families form part of O. patagonica tissues core microbiome and may play significant roles in the nitrogen cycle. Furthermore, sequences related to the coral pathogens, Vibrio mediterranei and Vibrio coralliilyticus, were detected not only in bleached corals but also in healthy ones, even during cold months. This fact opens a new view onto unveiling the role of pathogens in the development of coral diseases in the future.

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. This work was funded by the European Union’s framework program Horizon 2020 (LEIT - BIO - 2015 - 685474, Metafluidics, to JA) and the Ministerio de Economía y Competitividad Smart project (CGL2012-32194, to CL).

Bleaching of Oculina patagonica has been extensively studied in the Eastern Mediterranean Sea, although no studies have been carried out in the Western basin. In 1996 Vibrio mediterranei was reported as the causative agent of bleaching in O. patagonica but it has not been related to bleached or healthy corals since 2003, suggesting that it was no longer involved in bleaching of O. patagonica. In an attempt to clarify the relationship between Vibrio spp., seawater temperature and coral diseases, as well as to investigate the putative differences between Eastern and Western Mediterranean basins, we have analysed the seasonal patterns of the culturable Vibrio spp. assemblages associated with healthy and diseased O. patagonica colonies. Two sampling points located in the Spanish Mediterranean coast were chosen for this study: Alicante Harbour and the Marine Reserve of Tabarca. A complex and dynamic assemblage of Vibrio spp. was present in O. patagonica along the whole year and under different environmental conditions and coral health status. While some Vibrio spp. were detected all year around in corals, the known pathogens V. mediteranei and V. coralliilyticus were only present in diseased specimens. The pathogenic potential of these bacteria was studied by experimental infection under laboratory conditions. Both vibrios caused diseased signs from 24 °C, being higher and faster at 28 °C. Unexpectedly, the co-inoculation of these two Vibrio species seemed to have a synergistic pathogenic effect over O. patagonica, as disease signs were readily observed at temperatures at which bleaching is not normally observed. This work was supported by the projects CGL2009-12651-C02-01 and CGL2012-39627-C03-01 (to JA) of the Spanish Ministry of Economy and Competitiveness, which were also co-financed with FEDER support from the European Union (EU), and the EU project SYMBIOMICS (www.symbiomics.de) grant no.264774 (to AAR).

Background: We analyzed the sipunculan fauna inhabiting the scleractinian coral Oculina patagonica in the Marine Reserve of Tabarca Island (western Mediterranean). Results: Five sipunculan species were collected from 2011 to 2014: Phascolosoma stephensoni, P. granulatum, P. cf. agassizii, Aspidosiphon misakiensis, and Golfingia vulgaris. All five species were reported for the first time inhabiting O. patagonica; with P. cf. agassizii being a new record for the Iberian Peninsula. The average abundance of sipunculans inhabiting the coral was 468.75 ± 158.04 ind m−2, representing the second most abundant taxonomic group, in biomass, after Mollusca. Conclusions: Sipunculan diversity was low comparing with tropical reefs, but species abundances were higher than in soft-bottom nearby areas and community structure appears to be more homogeneous. There may be a considerable contribution to the erosion of the coral skeleton by sipunculans.

In the late summer of 2015, extensive mortality of scleratinian corals, gorgonians, and sponges was observed in the Marine Protected Area of Tabarca (southeast Spain). Quantitative data indicated that at 25 m depth the sea fan Eunicella singularis was the most affected species (50% of colonies affected by partial mortality); while in shallow waters more than 40% of the endemic scleractinian coral Cladocora caespitosa population showed tissue lesions that affected more than 10% of their surfaces. Other affected species were the scleractinian corals Oculina patagonica and Phyllangia mouchezii, the sea fan Leptogorgia sarmentosa and the sponge Sarcotragus fasciculatus. This mortality event coincided with an abnormal rise in seawater temperature in this region. Microbiological analysis showed a higher abundance of culturable Vibrio species in invertebrates exhibiting tissue lesions, which indicated that these opportunistic pathogens could be a key factor in the process.

The success that the putative alien species Oculina patagonica is able to survive under different environmental conditions may be benefiting its establishment and spreading along the Mediterranean Basin. Our objectives were to determine the response of this species, in terms of growth and bleaching, under different environmental conditions. Field data on colony growth and bleaching were obtained for a period of 18 months (from June 2010 to December 2011), in the Alicante Harbour (38°20′11″N, 00°29′11″W) and the Marine Protected Area of Tabarca (38°09′59″N, 00°28′56″W). Additionally, data on sedimentation rates, chlorophyll a concentration and organic matter were also collected. Moreover, the role of light over growth and bleaching of the coral was also studied with a field experiment. Our results showed that growth rates were similar among localities (eutrophic and oligotrophic environments), decreasing with increasing perimeter of the colony. Growth rates were at a minimum during cold months (13 °C) and enhanced during warm months until a threshold temperature; thereafter, bleaching was observed (>28 °C), being adverse for coral growth. In addition, light attenuation could act such as local stress, increasing the coral bleaching with the increase in seawater temperature. Our findings confirmed that O. patagonica has a broad tolerance to seawater temperature, irradiance and trophic water conditions, in addition to its ability to thrive through bleaching events, mainly in eutrophic environments, probably related to food availability.

Oculina patagonica is a putative alien scleractinian coral from the Southwest Atlantic that inhabits across the Mediterranean Sea. Here, we have addressed the diversity of Eukarya associated with this coral and its changes related to the environmental conditions and coral status. A total of 46 colonies of O. patagonica were taken from Alicante coast (Spain) and Pietra Ligure coast (Italy) and analyzed using denaturing gradient gel electrophoresis (DGGE) of the small-subunit 18S rRNA and 16S plastid rRNA genes, internal transcribed spacer region 2 (ITS 2) analyses, and electron microscopy. Our results show that Eukarya and plastid community associated to O. patagonica change with environmental conditions and coral status. Cryptic species, which can be difficult to identify by optical methods, were distinguished by 18S rRNA gene DGGE: the barnacle Megatrema anglicum, which was detected at two locations, and two boring sponges related to Cliona sp. and Siphonodictyon coralliphagum detected in samples from Tabarca and Alicante Harbour, respectively. Eukaryotic phototrophic community from the skeletal matrix of healthy corals was dominated by Ochrosphaera sp. while bleached corals from the Harbour and Tabarca were associated to different uncultured phototrophic organism. Differences in ultrastructural morphologies of the zooxanthellae between healthy and bleached corals were observed. Nevertheless, no differences were found in Symbiodinium community among time, environments, coral status and location, showing that O. patagonica hosted only one genotype of Symbiodinium belonging to clade B2. The fact that this clade has not been previously detected in other Mediterranean corals and is more frequent in the tropical Western Atlantic, is a new evidence that O. patagonica is an alien species in the Mediterranean Sea. We are grateful to the University of Alicante for awarding a predoctorate grant to ERP. This work was funded by projects CTM2012-38222-C02-02 (to AdlRM) and CGL2012-39627-C03-01 (to JA) of the Spanish Ministry of Economy and Competitiveness, which were also co-financed with FEDER support from the European Union (EU).