Mediterranean marine keystone species on the brink of extinction

Abstract

Several consecutive heatwaves affected Europe in summer 2022 (Heating up, 2022). In France, it has been the third most intense event on record, the benchmark heatwave remaining that of August 2003, with extremely high temperatures that lasted for several days throughout the country (https://meteofrance.fr/actualite/publications/2022-les-bilans-climatiques). As of 2003, this new extreme event has particularly impacted Mediterranean countries and spread to the marine realm. The North Western part of the Mediterranean Sea has experienced the strongest anomaly, with sea surface temperatures reaching 5°C higher than average (https://www.esa.int/Applications/Observing_the_Earth/Mediterranean_Sea_hit_by_marine_heatwave). Marine heatwaves (MHWs) are generally not restricted to the ocean surface, and although there is a clear trend in their increasing frequency (Oliver et al., 2018), they can have highly variable patterns, making it difficult to predict their occurrence and impact. In summer 2022, a warm water mass plunged to over 20 m depth in some locations of the NW Mediterranean Sea. The Marseille area experienced a record peak of 27.4°C in mid-August and a whole week displaying records over 26°C (Figure 1a). The mean temperature during the two hottest months of the summer was up to 2°C higher than in previous years and even higher than in the summer of 2003 (Figure 1a). Past Mediterranean MHWs have been related to disease outbreaks and mass mortality of benthic animals, occasionally leading to species shifts (Garrabou et al., 2022; Lejeusne et al., 2010). Several species of sponges, gorgonians, bryozoans, tunicates, and mollusks, most of them keystones that shape Mediterranean seascapes, were among the main victims. The recurrence of MHWs, therefore, appears to drive the current major biodiversity crisis in the Mediterranean Sea. Although very alarming, these past events reached the general public as related to disease outbreaks and mortality, not to the disappearance of species. Here, we show that the 2022 NW Mediterranean MHW is more directly in line with the sixth mass extinction expectations (Cowie et al., 2022; Thomas et al., 2004). Off the Marseille coast, the above mentioned record temperatures coincided with the first observations of mass mortality. From then on, the phenomenon rapidly spread down to 30 m depth, and new mortality cases were reported every day. This year, the main victims were again gorgonians and first and foremost, the purple sea-fan Paramuricea clavata. In the Marseille region, one of the coldest parts of the NW Mediterranean, this sea-fan was the major contributor to shallow seascapes. Today, thousands of naked axes of this forest-forming erect soft coral testify of its destruction between the surface and 25 m depth, reminiscent of an “underwater wildfire.” Fortunately, this charismatic species has a wide bathymetric distribution in the Mediterranean, and therefore, beyond a depth of 30 m and down to more than 100 m, it is still possible to find dense populations. The case of bath sponges (Porifera, family Spongiidae) is much more critical. These marine animals have been harvested since antiquity for the fineness, softness, and absorbent quality of their skeleton. This fishery remains nowadays a particularly lively cultural heritage in several Mediterranean countries. It has been recently hypothesized that past MHWs, between the 1980s and today, played a key role in the disappearance of several sponge beds across the Mediterranean Sea, particularly in the Eastern basin (Fourt et al., 2020). The NW basin was one of the last parts of the Mediterranean Sea harboring dense populations, barely exploited, although in rather shallow waters. Evaluating the mortality of these marine animals can only be achieved by sponge experts because many species of similar size and color can be confused underwater. The outcome of the 2022 MHW is unfortunately clear. All Spongiidae species known along the French coast (e.g., Spongia officinalis, Spongia lamella, Hippospongia communis) appear to have been wiped out between the surface and 25 m depth. Densest populations of S. officinalis (Figure 1b–d) used to occur at 10 m depth in the vicinity of Marseille, some of these populations having been monitored for over 25 years. Mortality rates are a bleak 100% mortality; there are no survivors down to 25 m depth. After a total of 30 dives in 20 different locations along the French Mediterranean coast, only very few live individuals (1–4 per location) could be found between 25 and 30 m, but no true population survived. Sponges provide many important ecosystem services, such as shelter for various juvenile and adult animals. As filter-feeders, they recycle particulate and dissolved organic matter in the water column, thus affecting entire food webs (De Goeij et al., 2013). They are also well-known producers of bioactive compounds with potent pharmacological activities (Calado et al., 2022). In this context, bath sponge taxonomy and a part of the systematics are currently under revision, with species complexes to be deciphered and new species to be described (Grenier et al., 2022): a sponge biodiversity under risk of extinction before formal description. Appendix S1. 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