The black coral Leiopathes glaberrima (Esper, 1788) is widely distributed in the Western Mediterranean Sea and in the Northern Atlantic Ocean at depths ranging from 100 to 2048 meters (Roark et al., 2006; Etnoyer et al., 2018; Massi et al., 2018). Some specimens were also reported from Hawaiian waters (Grigg and Opresko, 1977), but it turned out to be a misidentification of the endemic congeneric Leiopathes annosa (Wagner and Opresko, 2015). L. glaberrima settles on rocky bottoms where it tends to aggregate in patches with three-dimensional colonies which may exceed two-meters height. These aggregations of tree-like organisms represent a key component of deep-sea animal forests (sensu Rossi et al., 2017), communities comparable in complexity, biodiversity, and structuring role to the terrestrial forests, but composed of suspension-feeding organisms, e.g. sponges, anthozoans, bryozoans and bivalves (Bo et al., 2009, 2015; Buhl-Mortensen et al., 2010; Cerrano et al., 2010; Rossi et al., 2017). Despite challenges posed by taxonomic heterogeneity and spatial organization, the term marine animal forest provides an evocative representation of the concept as it was intended to be used. In fact, such a term groups diverse benthic ecosystems including coral gardens, oyster reefs, and sponge grounds, each with characteristic dominant species, yet collectively sharing a common ecological role. Suspension-feeding communities play an important role in benthic-pelagic coupling – thus the transfer of energy, biomass and nutrients between the pelagic and the benthic ecosystems - by recycling particulate organic matter sinking from upper photosynthetic layers (Gili and Coma, 1998; Bo et al., 2014a). The three-dimensionality of marine animal forests provides secondary substrates and niches, forming a spawning, nursery and shelter ground for a rich associated fauna (Cerrano et al., 2010; Bo et al., 2014a; Cau et al., 2017; D’Onghia et al., 2017; Rueda et al., 2019). For these reasons, ecosystems dominated by Cold-Water Corals (CWCs) – a group of habitat-forming azooxanthellate anthozoans (Phylum Cnidaria) with an affinity for cold waters - are considered as biodiversity hotspots (Mastrototaro et al., 2010; Tsounis et al., 2010). Another aspect that these marine ecosystems share with the terrestrial ones is the longevity of the structuring species. The dating of several species of stony corals, black corals and gorgonian octocorals, has shown that those anthozoans can live for hundreds of years (Roark et al., 2006; Prouty et al., 2011; Tracey et al., 2018; Hitt et al., 2020) and the black corals belonging to the Leiopathes genus are among the most longevous marine species known so far. Roark et al. (2009) carried out radiocarbon dating on a specimen of Leiopathes sp. from Hawaiian waters, estimating an age of 4265 ± 44 years old. In the Mediterranean Sea, Bo et al. (2015) carried out the same analysis on a specimen of Leiopathes glaberrima collected off the southwestern Sardinian coasts, estimating an age of 1973 ± 55 years old.

Longevity, as well as other biological characteristics, namely maturation at relatively old ages, slow growth, low natural mortality rates, intermittent recruitment of successful year classes and spawning that may not occur every year, are indicators of highly sensitive species (FAO, 2008).

For these reasons, Leiopathes glaberrima belongs to the “Endangered” category in the IUCN Red List of Mediterranean Anthozoans and is listed in Annex II of the SPA/BD protocol of the Barcelona Convention. In addition, this species is a key component of hard-bottom coral gardens, which are considered VMEs (Vulnerable Marine Ecosystems) in relation to several human activities (FAO, 2008; Aguilar and Marín, 2013; D’Onghia et al., 2017). Its bathymetric distribution greatly enhances the risk of being subjected to locally high fishing pressure (Bo et al., 2009, 2014a, 2014b; Deidun et al., 2010). Among the main threats, bottom trawling can entirely remove colonies while re-suspension of soft sediments increases turbidity, even beyond the trawling footprint, which can lead to smothering of benthic communities (Bo et al., 2014b; D’Onghia et al., 2017; Paradis et al., 2017; Otero and Marin, 2019; Bilan et al., 2023). Numerous other fishing gears such as gillnets, trammel nets, long lines, and traps can cause physical damage and removal of benthic species (Chiappone et al., 2005; Macfadyen et al., 2009; Bo et al., 2014b; Otero and Marin, 2019). Moreover, derelict fishing gears (also referred to as Abandoned, Lost or otherwise Discarded Fishing Gears - ALDFGs) may abrade tissues by either getting entangled or drifting on the seafloor (Laist, 1997; Brown and Macfadyen, 2007; Bo et al., 2014b). In anthozoans, the abrasion of coenenchyme favors the growth of epibionts. which can weaken their skeletons and enhance the detachment of branches (Bavestrello et al., 1997).

Other threats are related to the exploitation of the geological resources of the seabed, as well as the laying of submarine pipelines and cables or the dumping of waste into the sea (Turley et al., 2007; Roberts and Cairns, 2014; Roberts et al., 2016). Moreover, there are the potential effects of climate change on deep-sea communities, including rising temperatures, acidification, deoxygenation, and changes in trophic inputs, which could lead to a reduction in suitable habitats (Thresher et al., 2015; Morato et al., 2020).

Studies on the distribution of antipatharians in the Mediterranean Sea only started in the 2000s, primarily through the work of Bo et al. (2008, 2009, 2011a, 2011b, 2012, 2014a, 2014b, 2015), garnering a growing interest over the years. Published data over black coral distribution in the Mediterranean Sea is reviewed in the work of Chimienti et al. (2019), while a literature review focused on Leiopathes glaberrima populations along Italian waters was undertaken by Ingrassia and Di Bella (2021) and Lauria et al. (2021). The low number of detailed studies describing these populations and the lack of parameters that allow for an unequivocal definition of marine animal forests, make their quantification in L. glaberrima challenging. As a result, the reviews previously mentioned report several findings throughout the Mediterranean Sea but aggregations of L. glaberrima have been described only in few locations.

The conservation status of such forests varies from pristine, as the case of those reported by Bo et al. (2015) in Carloforte Shoal (SW Sardinia) which reached a peak of 8 colonies/m^-2, to highly impacted, as the ones described at Marco Bank (NW Sicily) by Bo et al. (2014b). The health status was assessed as a result of the quantification of damaged colonies and ALDFGs, in relation to fishing effort. Fishing activities turned out to be the main contributor to the mortality of this species.

This study is based on a dataset of 1020 colonies of L. glaberrima, used to characterize its environmental preferences, associated fauna and the population structure in terms of distribution, abundance, size and health status. Additionally, a site where almost all the specimens were dead has been observed, reporting a rare case of mass mortality in the deep-sea environment and the first ever described for black corals.

Mass mortality events (MMEs) among benthic species have been documented across coastal and upper coralligenous environments. In the last thirty years the frequency of these events increased exponentially, marking a concerning trend. Garrabou et al. (2019) tracked these events within the Mediterranean, unveiling a predominant impact on Cnidaria (47.4%) and Porifera (37.6%). The causes of MMEs in anthozoans have frequently been linked to strong and recurrent marine heat waves and, only in a few cases, to heightened sedimentation. Temperature anomalies induce physiological stress which can directly result in the death of the organism or in the weakening of its immune response, thereby heightening the susceptibility to pathogenic infections (Garrabou et al., 2001; Vezzulli et al., 2010; Carella et al., 2014). MMEs have been predominantly recorded within the first 50 meters depth, a zone that has historically commanded the focus of scientific exploration conducted by scuba divers. The expansion of research efforts into deeper environments is progressively extending the boundaries of our understanding of mass mortalities. The deepest MMEs have been recorded from 120 to 180 meters depth and confined to the red coral Corallium rubrum off the Provence coastline, the Gulf of Napoli and Salerno and the southeastern shores of Sardinia. In these cases, the possible causes were hypothesized to be current-driven pollutants, unusual drops of summer thermocline and warmwater emissions in areas characterized by volcanic activities (Rivoire, 1991; Bavestrello et al., 2014; Toma et al., 2022).

Despite these recent studies, most of the instances of mass mortalities in the deep Mediterranean Sea are referred to fossil reefs from late Neogene and Quaternary of Madrepora oculata and Desmophyllum pertusum due to changes of the paleo-environmental conditions and tectonic evolutions (Fink et al., 2015; Taviani et al., 2019).

The extensive exploration of such a vast area provided us with new information, on a medium to large scale, over the distribution patterns and the types of aggregations of Leiopathes glaberrima ( Figure 3 ). The bathymetric range of this species in this area is comparable with the data reported for the Mediterranean Sea in the review made by Chimienti et al. (2019). The species occurrence on diverse hard bottoms with varying slopes emphasizes its adaptability to such environmental drivers.

The scarcity of Abandoned, Lost, or Otherwise Discarded Fishing Gears (ALDFGs) in the vicinity of the colonies might be interpreted as a low anthropogenic impact. However, the contrasting data revealing breakage at the trunks of specimens, accounting for 6.4% of the total observations, appeared to be an objective indicator of impact. The removal of colonies may be caused by both demersal longlines and bottom trawling, the most common techniques used in many deep-sea fisheries (Clark et al., 2016).

Concerning the spatial distribution, the species can occur as aggregated in dense patches as well as single isolated colonies. While the results of the spatial analysis in the area confirmed the tendency of the species for aggregation, least expected was the presence of several isolated specimens. Despite the individual colonies being fewer, this pattern raises questions about the factors influencing distribution, larval dispersion, and connectivity of this species. The high number of isolated colonies in locations with low or absent fishing impact may be attributed to a challenging accessibility of larvae to such sites or the presence of borderline environmental conditions.

Patches 1, 2, 16 and 17 exhibit similar features except for the substrate composition, indeed the first two predominantly thrive on rocky bottom while the others grow on a CWCs framework. High density of colonies, predominance of medium/small-sized specimens in excellent health condition are representative of relatively young forests. The proximity of such prosperous aggregations implies that the sub-area experiences suitable environmental conditions for the settlement and growth of L. glaberrima, suggesting that additional forests may occur on the surrounding hard bottoms. The mean density values of these aggregations are in line with data available for other pristine populations in literature, while the peak of density of 14.5 colonies/m² observed in Patch 2 constitutes the highest value recorded so far, compared with the maximum densities ranging from 4 to 11 colonies/m² registered in several locations of the Central Mediterranean Sea (Bo et al., 2014b, 2015; Deidun et al., 2015; Ingrassia et al., 2016; Angiolillo et al., 2023). It is worth pointing that the patches abundance could have been partially underestimated as the contiguity of the canopies in high density aggregations makes the discrimination between small-sized individuals challenging.

The mass mortality documented in Patch 4 represents a rare case in the deep-sea environment and the first ever described for black corals. The total absence of fishing gears and broken colonies along the transect suggests that the direct impact of fishing, despite being a heavily performed activity in the area and a key factor often associated with mortality in deep-sea environments, can be ruled out as a contributing cause. Other possible causes of mass mortality proposed for the red coral C. rubrum are linked to the transport of urban pollutants by dominant currents and to the unusual dropping of the summer thermocline due to a gravity flow of coastal debris. Both hypotheses are to be excluded given the depth and the offshore location of the site. Putative causes could be related to poisoning from toxic wastes, e.g. barrels of toxic chemicals and batteries, as well as pathogens-related diseases (Garrabou et al., 2001; Vezzulli et al., 2010; Carella et al., 2014; Silva et al., 2016; Merrifield et al., 2023). Another possible explanation could be reconducted to changes in physical and chemical conditions caused by past hydrothermal emissions, as assumed for the red coral bank around Li Galli Island (Gulf of Salerno) by Bavestrello et al. (2014).

Patches from 7 to 13 have been clustered according to geographical proximity and geomorphological features. Moreover, the whole sub-area displays a precarious health state, which is not excluded to be attributable to the events that caused the mass mortality of Patch 4, geographically not far away. The high number of broken specimens and the longline observed throughout the sub-area. let us suppose that fishing activities could potentially act as a cumulative stressor for the populations.

Geographical proximity is also a common factor also for Patches 3, 5 and 6. Nevertheless, they differ in terms of colony height and health status. In Patch 3, the presence of very small individuals suggests that they are new recruits. In contrast, Patch 6 is constituted by large specimens with high percentages of tissue loss, characteristic aspects of a population that has stopped recruiting.

The discovery of L. glaberrima in a different water mass in Patch 14 may hide a potential level of plasticity to environmental parameters, considering that CWCs have usually been reported to settle along the path of the well-ventilated and nutrient-rich LIW (Chimienti et al., 2019; Lauria et al., 2021). However, all the explored sites along the bank share nearly identical environmental conditions, L. glaberrima was observed in a single location situated on the western margin. The absence of this species in other areas of the bank is indicative of how local factors may play a key role for its distribution.

Patch 15 is unique as it was attached to the iron surface of a shipwreck. Those kinds of anthropogenic structures act as artificial reefs and biodiversity hotspot by providing hard substrata, food supply, protection and higher exposure to currents (Frizzel, 2020). Knowing the sinking date of shipwrecks, or at least the approximate period, allows us to estimate the growth rates of sessile fauna without the need for traditional dating techniques like radioisotope analysis.

This work describes the distribution pattern, health status, associated fauna and types of aggregations of Leiopathes glaberrima populations in the northern part of the Strait of Sicily, laying out fresh insights about the ecology of the species and its conservation.

Extensive and pristine forests have been documented, achieving density values never reported before for the species. Such pristine populations are rare, representing a true biodiversity gem of the Mediterranean Sea.

In contrast, the study also provides the description of a rare case of mass mortality in a deep-sea environment, which leaves room for another consideration: large-scale mortality events due to anthropogenic climate change are now common in shallower environments, as sadly observed for tropical corals and temperate mesophotic ecosystems (Cerrano et al., 2019), while the stability of deep-sea environments coupled with the long water sinking times have led to the idea that such phenomena were virtually non-existent at great depths and their impact was negligible. In such a context, this study opens new scenarios regarding the possibility that mass mortality events can occur in deep environments too, even if they were considered safe from danger. The triggering causes of these events in inaccessible environments are actually only hypothesized, but it is not to be excluded that, sooner or later, a similar effect could potentially result from anthropogenic climate changes.

The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation.

The manuscript presents research on animals that do not require ethical approval for their study.

AG: Conceptualization, Data curation, Formal analysis, Writing – original draft, Writing – review & editing. SC: Conceptualization, Investigation, Supervision, Writing – original draft, Writing – review & editing, Project administration. BD: Data curation, Investigation, Writing – review & editing. TR: Project administration, Resources, Supervision, Writing – review & editing. SG: Funding acquisition, Project administration, Resources, Writing – review & editing.