Two “pillars” of cold-water coral reefs along Atlantic European margins: Prevalent association of Madrepora oculata with Lophelia pertusa, from reef to colony scale

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Abstract

The scleractinian coral Lophelia pertusa has been the focus of deep-sea research since the recognition of the vast extent of coral reefs in North Atlantic waters two decades ago, long after their existence was mentioned by fishermen. These reefs where shown to provide habitat, concentrate biomass and act as feeding or nursery grounds for many species, including those targeted by commercial fisheries. Thus, the attention given to this cold-water coral (CWC) species from researchers and the wider public has increased. Consequently, new research programs triggered research to determine the full extent of the corals geographic distribution and ecological dynamics of “Lophelia reefs”. The present study is based on a systematic standardised sampling design to analyze the distribution and coverage of CWC reefs along European margins from the Bay of Biscay to Iceland. Based on Remotely Operated Vehicle (ROV) image analysis, we report an almost systematic occurrence of Madrepora oculata in association with L. pertusa with similar abundances of both species within explored reefs, despite a tendency of increased abundance of L. pertusa compared to M. oculata toward higher latitudes. This systematic association occasionally reached the colony scale, with “twin” colonies of both species often observed growing next to each other when isolated structures were occurring off-reefs. Finally, several “false chimaera” were observed within reefs, confirming that colonial structures can be “coral bushes” formed by an accumulation of multiple colonies even at the inter-specific scale, with no need for self-recognition mechanisms. Thus, we underline the importance of the hitherto underexplored M. oculata in the Eastern Atlantic, re-establishing a more balanced view that both species and their yet unknown interactions are required to better elucidate the ecology, dynamics and fate of European CWC reefs in a changing environment.

Introduction

According to Jones׳ definition (Jones et al., 1994), corals are considered as autogenic engineers as they “change the environment via their own physical structures, i.e. their living and dead tissues”. The population dynamics of these engineering species is determinant for the dynamics of the communities they support and the persistence of ecosystems they belong to.

Two main species of stony corals form reefs in the East Atlantic (Fig. 1), the scleractinians Lophelia pertusa (Linnaeus 1758) and Madrepora oculata (Linnaeus 1758). Historical reports of locations of cold-water coral (CWC) reefs date back to the 18th century in Norway (Gunnerus 1768) and early 20th century in Ireland and the Bay of Biscay (Joubin, 1922a, Joubin, 1922b, Le Danois, 1948) where massive formations were reported. In these reports, however, no distinction was made between L. pertusa and M. oculata, both refered to as “white corals”. These reef-building “white corals” were opposed to the “yellow” corals that included species from the genus Dendrophyllia, such as Dendrophyllia cornigera (Lamarck 1816). Fisheries moving to deeper areas and seabed surveys motivated by prospecting for fossil energies (oil and gas) in the past two to three decades, have indeed led to the discovery of vast CWC reefs along continental margins (Rogers, 1999). The long-standing view that cold-water scleractinians would most often occur as isolated colonies at high latitudes, with occasional occurrence of dense formations, was then challenged by the discovery of the large Sula reef dominated by L. pertusa on the mid-Norwegian shelf (Freiwald et al., 1999). Several reefs have been discovered and studied along European Atlantic margins in Norway and the Faroe Islands in the 90׳s (Frederiksen et al., 1992, Hovland et al., 1998, Hovland and Thomsen, 1997, Mortensen et al., 1995, Mortensen et al., 2001), followed by Ireland and the UK (Costello et al., 2005, De Mol et al., 2002, Roberts et al., 2003) and Sweden (Jonsson et al., 2004). Fosså et al. (2002) identified seven species of scleractinians occurring in Norwegian waters, of which only L. pertusa and M. oculata form reefs; these same authors also mentioned the lower abundance of M. oculata compared to L. pertusa, and that the former has never been reported to build reefs (Dons, 1944, Frederiksen et al., 1992). On a more recent quantitative study, Purser et al. (2013) also report a much lower abundance of M. oculata in the same waters. Possibly owing to the dominance of L. pertusa in the first explored reefs (Freiwald et al., 1999), this species remained the dominant focus of most subsequent cruises and ecological studies (Fig. 2) which target was often stated as “Lophelia reefs”, whereas M. oculata remained comparatively rather neglected up to the mid 2000׳s (Fig. 2).

More recent expeditions and historical record compilations (Reveillaud et al., 2008) have shed more light on the southern European margins, highlighting the frequent occurrence and engineering role of M. oculata, at least in the Bay of Biscay and in the Western and Central Mediterranean (Gori et al., 2013, Orejas et al., 2009, Vertino et al., 2010) that were less studied than Northern reefs. However, due to the relatively recent consideration of this species and to the logistic difficulties inherent to deep-sea sampling and observation, no quantitative estimates exist, thus far, to appraise the compared geographical distribution of M. oculata and L. pertusa in the Northeastern Atlantic. Species structuring habitat, referred to as “structural” (Huston, 1994), “ecosystem engineers” (Jones et al., 1994), or “founder” species (Bruno and Bertness, 2001, Dayton, 1975), have a major role as driver of the prospects of ecosystems and associated communities under environmental fluctuations (Peterson et al., 1984). Identifying these habitat-forming species and defining their potential and realised ecological niche (Bruno et al., 2003) to better understand their role as a driver of community composition and dynamics is a prerequisite to most ecological studies including habitat modeling, the study of ecological interactions, the reconstruction of past history or the projection of future range shifts under environmental changes.

Here, we report on the observations made during two cruises taken place in 2011 and 2012, respectively, to locate reefs and appraise their extent in the Bay of Biscay, off Ireland and off south Iceland. We assessed the relative densities and seafloor area covered by both species in five sites sampled according to a standardised scheme (Becheler et al., 2017) using random sampling of transects and video analysis. Results provide the first estimates of the relative abundances of the two scleractinian species found in reefs identified along Atlantic European margins, supporting an equivalent importance of M. oculata and L. pertusa in terms of abundance and spatial extent.

Section snippets

Study sites

During the BobEco cruise (September/October 2011), reefs from the Bay of Biscay and Celtic Sea were explored using the Remotely Operated Vehicle (ROV) Victor 6000 (Ifremer). The continental slope of the Bay of Biscay is regularly cut by a succession of submarine canyons connecting the continental shelf and the continental rise (Bourillet et al., 2003). In this area, CWC reefs formed by scleractinians were found to be typically located between 600 and 900 m depth, standing mostly above soft

Results

During exploration dives (to find reefs), isolated colonies of the two reef-building scleractinians were observed outside of reefs during prospective dives in all three regions. These colonies were extremely frequent (pers. obs.) and were often made of a compound of both species growing next to each other or interspersed, resulting in “twin colonies”.

Additionally, when samples were sorted on deck, four “chimaera-like” colonies formed of fully merged branches of L. pertusa and M. oculata were

Discussion

Here we propose a re-appraisal of the relative importance of both reef-forming scleractinians M. oculata and L. pertusa along Northeastern Atlantic European margins, based on most recent exploration cruises and on standardised strategy allowing a formal comparison of data among sites. Within Northeast Atlantic CWC reefs spanning from the Bay of Biscay to Iceland, our results revealed a quasi-systematic co-occurrence of L. pertusa and M. oculata at nested scales: the region, reef, and also often

Conclusion

In conclusion, CWC reefs along European margins are reliant on two pillars of scleractinian species, namely L. pertusa and M. oculata, as opposed to the current held misconceived view that only the former species provides vast structural habitats for a diverse community of associated species. The prevalence of M. oculata being more important than considered to date, particularly at lower latitudes, indicates that the designation of “Lophelia reefs” may thus not be adapted to most reefs along

Acknowledgments

This work was performed in the framework of the EC FP7 project ‘CoralFISH’ under Grant agreement no. 213144.We would like to thank the captains and crew of the R/V Pourquoi Pas? (BobEco cruise 2011) and the R/V Le Thalassa (Ice-CTD cruise 2012) as well as all participants who directly or indirectly contributed to the data acquisition. We wish to thank Stefán Ragnarsson for his invaluable help for planning dive plans in Iceland during IceCTD, Jaime Davies for her comments on the manuscript, as

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