Climate-induced changes in the suitable habitat of cold-water corals and commercially important deep-sea fishes in the North Atlantic.

The deep sea plays a critical role in global climate regulation through uptake and storage of heat and carbon dioxide. However, this regulating service causes warming, acidification and deoxygenation of deep waters, leading to decreased food availability at the seafloor. These changes and their projections are likely to affect productivity, biodiversity and distributions of deep-sea fauna, thereby compromising key ecosystem services. Understanding how climate change can lead to shifts in deep-sea species distributions is critically important in developing management measures. We used environmental niche modelling along with the best available species occurrence data and environmental parameters to model habitat suitability for key cold-water coral and commercially important deep-sea fish species under present-day (1951-2000) environmental conditions and to project changes under severe, high emissions future (2081-2100) climate projections (RCP8.5 scenario) for the North Atlantic Ocean. Our models projected a decrease of 28%-100% in suitable habitat for cold-water corals and a shift in suitable habitat for deep-sea fishes of 2.0°-9.9° towards higher latitudes. The largest reductions in suitable habitat were projected for the scleractinian coral Lophelia pertusa and the octocoral Paragorgia arborea, with declines of at least 79% and 99% respectively. We projected the expansion of suitable habitat by 2100 only for the fishes Helicolenus dactylopterus and Sebastes mentella (20%-30%), mostly through northern latitudinal range expansion. Our results projected limited climate refugia locations in the North Atlantic by 2100 for scleractinian corals (30%-42% of present-day suitable habitat), even smaller refugia locations for the octocorals Acanella arbuscula and Acanthogorgia armata (6%-14%), and almost no refugia for P. arborea. Our results emphasize the need to understand how anticipated climate change will affect the distribution of deep-sea species including commercially important fishes and foundation species, and highlight the importance of identifying and preserving climate refugia for a range of area-based planning and management tools.

Parasite communities of the white seabream Diplodus sargus sargus in the marine protected area of Medes Islands, north-west Mediterranean Sea.

Marine protected areas are considered a useful tool to preserve and recover the biodiversity of ecosystems. It is suggested that fisheries not only affect populations of target and bycatch species but also their parasite communities. Parasites can indicate fishery effects on host species and also on the whole local community, but the effects of fisheries and protection measures on parasite communities are relatively unknown. This study analyses parasite communities of the white seabream Diplodus sargus sargus in order to assess potential effects exerted by protection measures within and by fisheries outside a reserve in the western Mediterranean Sea. This small scale analysis offered the opportunity to study different degrees of fishery effects on parasite infracommunities, without considering climatic effects as an additional factor. Parasite infracommunities of fishes from the no-take zone (NTZ) differed in their composition and structure compared with areas completely or partially open to fisheries. The detected spatial differences in the infracommunities derived from generalist parasites and varied slightly between transmission strategies. Monoxenous parasites were richer and more diverse in both fished areas, but more abundant in the no-take, whereas richness and abundance of heteroxenous parasites were higher for the NTZ. In addition to host body size as one factor explaining these spatial variations, differences within parasite infracommunities between the areas may also be linked to increased host densities and habitat quality since the implementation of the NTZ and its protection measures.

Mapping the habitat refugia of Isidella elongata under climate change and trawling impacts to preserve Vulnerable Marine Ecosystems in the Mediterranean.

The bamboo-coral Isidella elongata is a key habitat-forming species in the deep Mediterranean Sea. This alcyonacean is listed as an indicator of Vulnerable Marine Ecosystems (VMEs) and as Critically Endangered due to bottom trawling impacts. In this work, a modeling approach was used to predict and map the habitat suitability of I. elongata in the Mediterranean Sea under current environmental conditions. Occurrence data were modeled as a function of environmental parameters. Using climate change scenarios and fishing effort data, the risk of climate change and fisheries impacts on habitat suitability were estimated, and climate refugia were identified. A drastic loss of habitat is predicted, and climate change scenarios suggest a loss of 60% of suitable habitats by 2100. In the central Mediterranean, climate refugia overlapped with active fishing grounds. This study represents the first attempt to identify hot spots for the protection of soft bottom Vulnerable Marine Ecosystems for the entire Mediterranean Sea, and highlights areas most at risk from trawling. This work is relevant to the objectives of the EU Marine Strategy Framework and Maritime Spatial Planning Directives, the Biodiversity Strategy for 2030 regarding priority areas for conservation.

Reproductive characteristics and gametogenic cycle of the scleractinian coral Dendrophyllia ramea.

The present study marks a pioneering investigation into the reproductive cycle of the scleractinian coral Dendrophyllia ramea. This is one of the first reproduction studies conducted in the Mediterranean Sea for a colonial azooxanthellate coral. Coral samples were collected in 2017 (May and October) and 2018 (February and July) in the Alborán Sea (SW Mediterranean). This location was selected due to its rarity as one of the few sites where this species thrives at depths shallower than 40 m. These samples were used to study the sexual patterns, fertilization mechanisms and gametogenic cycles by means of histological techniques. To broaden the scope, Sea Surface Temperature (SST) and Chlorophyll-a (Chl-a) data from open access databases have been considered to explore the potential influence of these environmental factors as triggers for gamete development and spawning time. The findings cast D. ramea as a gonochoric species, since no hermaphroditic specimens were observed among the analysed samples. Additionally, the lack of larvae and embryos in any of the analysed polyps, suggest that this species is fertilised externally. Two oocyte cohorts have been detected simultaneously, hinting at a yearly reproductive cycle, characterised by a prolonged oocyte maturation and seasonal spawning period taking place between August and October. Nevertheless, D. ramea display a low fecundity compared to other scleractinians inhabiting deep waters. Lastly, the early stages of gametogenesis seem to be coupled with the highest Chl-a values (i.e., March and December), whereas spawning takes place throughout the warmest period of the year (August to October).

Ecophysiological and behavioural response of juveniles of the Chilean cold-water coral Caryophyllia (Caryophyllia) huinayensis to increasing sediment loads.

Chilean Patagonia is a hotspot of biodiversity, harbouring cold-water corals (CWCs) that populate steep walls and overhangs of fjords and channels. Through anthropogenic activities such as deforestation, roadworks, aquafarming and increased landslide frequency, sediment input increases in the fjord region. While the absence of CWCs on moderately steep slopes has been suggested to reflect high vulnerability to sedimentation, experimental evidence has been lacking. Here, we investigated the sensitivity of CWCs to sediment stress, using juvenile Caryophyllia (Caryophyllia) huinayensis as a model. A 12-week aquarium experiment was conducted with three sediment loads: the average natural sediment concentration in Comau Fjord, 100- and 1000-fold higher sediment levels, expected from gravel road use and coastal erosion. Changes in coral mass and calyx dimensions, polyp expansion, tissue retraction and respiration were measured. For CWCs exposed to two and three order of magnitude higher sediment concentrations, 32% and 80% of the animals experienced a decrease in tissue cover, respectively, along with a decrease in respiration rate of 34% and 66%. Under the highest concentration corals showed reduced polyp expansion and a significantly reduced growth of ~ 95% compared to corals at natural concentration. The results show that C. huinayensis is affected by high sediment loads. As human activities that increase sedimentation steadily intensify, coastal planners need to consider detrimental effects on CWCs.

Trophic ecology of Angolan cold-water coral reefs (SE Atlantic) based on stable isotope analyses.

Cold-water coral (CWC) reefs of the Angolan margin (SE Atlantic) are dominated by Desmophyllum pertusum and support a diverse community of associated fauna, despite hypoxic conditions. In this study, we use carbon and nitrogen stable isotope analyses (δ13C and δ15N) to decipher the trophic network of this relatively unknown CWC province. Although fresh phytodetritus is available to the reef, δ15N signatures indicate that CWCs (12.90 ± 1.00 ‰) sit two trophic levels above Suspended Particulate Organic Matter (SPOM) (4.23 ± 1.64 ‰) suggesting that CWCs are highly reliant on an intermediate food source, which may be zooplankton. Echinoderms and the polychaete Eunice norvegica occupy the same trophic guild, with high δ13C signatures (-14.00 ± 1.08 ‰) pointing to a predatory feeding behavior on CWCs and sponges, although detrital feeding on 13C enriched particles might also be important for this group. Sponges presented the highest δ15N values (20.20 ± 1.87 ‰), which could be due to the role of the sponge holobiont and bacterial food in driving intense nitrogen cycling processes in sponges' tissue, helping to cope with the hypoxic conditions of the reef. Our study provides first insights to understand trophic interactions of CWC reefs under low-oxygen conditions.

Local-scale feedbacks influencing cold-water coral growth and subsequent reef formation.

Despite cold-water coral (CWC) reefs being considered biodiversity hotspots, very little is known about the main processes driving their morphological development. Indeed, there is a considerable knowledge gap in quantitative experimental studies that help understand the interaction between reef morphology, near-bed hydrodynamics, coral growth, and (food) particle transport processes. In the present study, we performed a 2-month long flume experiment in which living coral nubbins were placed on a reef patch to determine the effect of a unidirectional flow on the growth and physiological condition of Lophelia pertusa. Measurements revealed how the presence of coral framework increased current speed and turbulence above the frontal part of the reef patch, while conditions immediately behind it were characterised by an almost stagnant flow and reduced turbulence. Owing to the higher current speeds that likely promoted a higher food encounter rate and intake of ions involved in the calcification process, the coral nubbins located on the upstream part of the reef presented a significantly enhanced average growth and a lower expression of stress-related enzymes than the downstream ones. Yet, further experiments would be needed to fully quantify how the variations in water hydrodynamics modify particle encounter and ion intake rates by coral nubbins located in different parts of a reef, and how such discrepancies may ultimately affect coral growth. Nonetheless, the results acquired here denote that a reef influenced by a unidirectional water flow would grow into the current: a pattern of reef development that coincides with that of actual coral reefs located in similar water flow settings. Ultimately, the results of this study suggest that at the local scale coral reef morphology has a direct effect on coral growth thus, indicating that the spatial patterns of living CWC colonies in reef patches are the result of spatial self-organisation.

Patterns of eukaryotic diversity from the surface to the deep-ocean sediment.

Remote deep-ocean sediment (DOS) ecosystems are among the least explored biomes on Earth. Genomic assessments of their biodiversity have failed to separate indigenous benthic organisms from sinking plankton. Here, we compare global-scale eukaryotic DNA metabarcoding datasets (18S-V9) from abyssal and lower bathyal surficial sediments and euphotic and aphotic ocean pelagic layers to distinguish plankton from benthic diversity in sediment material. Based on 1685 samples collected throughout the world ocean, we show that DOS diversity is at least threefold that in pelagic realms, with nearly two-thirds represented by abundant yet unknown eukaryotes. These benthic communities are spatially structured by ocean basins and particulate organic carbon (POC) flux from the upper ocean. Plankton DNA reaching the DOS originates from abundant species, with maximal deposition at high latitudes. Its seafloor DNA signature predicts variations in POC export from the surface and reveals previously overlooked taxa that may drive the biological carbon pump.

First evidence for zooplankton feeding sustaining key physiological processes in a scleractinian cold-water coral.

Scleractinian cold-water corals (CWC) represent key taxa controlling deep-sea reef ecosystem functioning by providing structurally complex habitats to a high associated biodiversity, and by fuelling biogeochemical cycles via the release of organic matter. Nevertheless, our current knowledge on basic CWC properties, such as feeding ecology and key physiological processes (i.e. respiration, calcification and organic matter release), is still very limited. Here, we show evidence for the trophic significance of zooplankton, essentially sustaining levels of the investigated key physiological processes in the cosmopolitan CWC Desmophyllum dianthus (Esper 1794). Our results from laboratory studies reveal that withdrawal (for up to 3 weeks) of zooplankton food (i.e. Artemia salina) caused a significant decline in respiration (51%) and calcification (69%) rates compared with zooplankton-fed specimens. Likewise, organic matter release, in terms of total organic carbon (TOC), decreased significantly and eventually indicated TOC net uptake after prolonged zooplankton exclusion. In fed corals, zooplankton provided 1.6 times the daily metabolic C demand, while TOC release represented 7% of zooplankton-derived organic C. These findings highlight zooplankton as a nutritional source for D. dianthus, importantly sustaining respiratory metabolism, growth and organic matter release, with further implications for the role of CWC as deep-sea reef ecosystem engineers.

Embryo and larval biology of the deep-sea octocoral Dentomuricea aff. meteor under different temperature regimes.

Deep-sea octocorals are common habitat-formers in deep-sea ecosystems, however, our knowledge on their early life history stages is extremely limited. The present study focuses on the early life history of the species Dentomuricea aff. meteor, a common deep-sea octocoral in the Azores. The objective was to describe the embryo and larval biology of the target species under two temperature regimes, corresponding to the minimum and maximum temperatures in its natural environment during the spawning season. At temperature of 13 ±0.5 °C, embryos of the species reached the planula stage after 96h and displayed a median survival of 11 days. Planulae displayed swimming only after stimulation, swimming speed was 0.24 ±0.16 mm s-1 and increased slightly but significantly with time. Under a higher temperature (15 °C ±0.5 °C) embryos reached the planula stage 24 h earlier (after 72 h), displayed a median survival of 16 days and had significantly higher swimming speed (0.3 ±0.27 mm s-1). Although the differences in survival were not statistically significant, our results highlight how small changes in temperature can affect embryo and larval characteristics with potential cascading effects in larval dispersal and success. In both temperatures, settlement rates were low and metamorphosis occurred even without settlement. Such information is rarely available for deep-sea corals, although essential to achieve a better understanding of dispersal, connectivity and biogeographical patterns of benthic species.

Madrepora oculata forms large frameworks in hypoxic waters off Angola (SE Atlantic).

This study aims to map the occurrence and distribution of Madrepora oculata and to quantify density and colony sizes across recently discovered coral mounds off Angola. Despite the fact that the Angolan populations of M. oculata thrive under extreme hypoxic conditions within the local oxygen minimum zone, they reveal colonies with remarkable heights of up to 1250 mm-which are the tallest colonies ever recorded for this species-and average densities of 0.53 ± 0.37 (SD) colonies m-2. This is particularly noteworthy as these values are comparable to those documented in areas without any oxygen constraints. The results of this study show that the distribution pattern documented for M. oculata appear to be linked to the specific regional environmental conditions off Angola, which have been recorded in the direct vicinity of the thriving coral community. Additionally, an estimated average colony age of 95 ± 76 (SD) years (total estimated age range: 16-369 years) indicates relatively old M. oculata populations colonizing the Angolan coral mounds. Finally, the characteristics of the Angolan populations are benchmarked and discussed in the light of the existing knowledge on M. oculata gained from the North Atlantic and Mediterranean Sea.

Diversity and Biogeography of Bathyal and Abyssal Seafloor Bacteria and Archaea Along a Mediterranean-Atlantic Gradient.

Seafloor sediments cover the majority of planet Earth and microorganisms inhabiting these environments play a central role in marine biogeochemical cycles. Yet, description of the biogeography and distribution of sedimentary microbial life is still too sparse to evaluate the relative contribution of processes driving this distribution, such as the levels of drift, connectivity, and specialization. To address this question, we analyzed 210 archaeal and bacterial metabarcoding libraries from a standardized and horizon-resolved collection of sediment samples from 18 stations along a longitudinal gradient from the eastern Mediterranean to the western Atlantic. Overall, we found that biogeographic patterns depended on the scale considered: while at local scale the selective influence of contemporary environmental conditions appeared strongest, the heritage of historic processes through dispersal limitation and drift became more apparent at regional scale, and ended up superseding contemporary influences at inter-regional scale. When looking at environmental factors, the structure of microbial communities was correlated primarily with water depth, with a clear transition between 800 and 1,200 meters below sea level. Oceanic basin, water temperature, and sediment depth were other important explanatory parameters of community structure. Finally, we propose increasing dispersal limitation and ecological drift with sediment depth as a probable factor for the enhanced divergence of deeper horizons communities.

Seafloor litter sorting in different domains of Cap de Creus continental shelf and submarine canyon (NW Mediterranean Sea).

We analyzed litter occurrence in 68 underwater video transects performed on the middle/outer continental shelf and submarine canyon off Cap de Creus (NW Mediterranean), an area recently declared Site of Community Importance (SCI). Low densities of urban litter were registered on the shelf (7.2 items ha-1), increasing in abundance towards the deepest part of the submarine canyon, with 188 items ha-1 below 1000 m depth. We hypothesize that the strong bottom currents that recurrently affect this area efficiently move litter objects from the shelf towards the deep. Of all litter items, approximately 50% had a fishing-related origin, mostly longlines entangled on rocks in the canyon head and discarded trawl nets in deeper areas. Over 10% of cold-water colonies observed had longlines entangled, indicating the harmful effects of such practices over benthic habitats. These results should be considered when designing mitigation measures to reduce litter pollution in Cap de Creus SCI.

Role of suspension feeders in antarctic pelagic-benthic coupling: Trophic ecology and potential carbon sinks under climate change.

Sea-ice and coastal glacier loss in the Western Antarctic Peninsula open new ice-free areas. They allowing primary production and providing new seabed for colonisation, both acting as a negative feedback of climate change. However, the injection of sediment-laden runoff from the melting of land-terminating glaciers may reduce this feedback. Changes in particulate matter will affect nutrition and excretion (faeces stoichiometry and properties) of suspension feeders, reshaping coastal carbon dynamics and pelagic-benthic coupling. Absorption efficiency and biodeposition of Euphausia superba and Cnemidocarpa verrucosa were quantified for different food treatments and varying sediment concentrations. Both species showed high overall absorption efficiency for free-sediment diets, but were negatively affected by sediment addition. High sediment conditions increased krill biodeposition, while it decreased in ascidians. Energy balance estimation indicated high carbon sink potential in ascidians, but it is modulated by food characteristics and negatively affected by sediment inputs in the water column.

Assessing the living and dead proportions of cold-water coral colonies: implications for deep-water Marine Protected Area monitoring in a changing ocean.

Coral growth patterns result from an interplay of coral biology and environmental conditions. In this study colony size and proportion of live and dead skeletons in the cold-water coral (CWC) Lophelia pertusa (Linnaeus, 1758) were measured using video footage from Remotely Operated Vehicle (ROV) transects conducted at the inshore Mingulay Reef Complex (MRC) and at the offshore PISCES site (Rockall Bank) in the NE Atlantic. The main goal of this paper was to explore the development of a simple method to quantify coral growth and its potential application as an assessment tool of the health of these remote habitats. Eighteen colonies were selected and whole colony and dead/living layer size were measured. Live to dead layer ratios for each colony were then determined and analysed. The age of each colony was estimated using previously published data. Our paper shows that: (1) two distinct morphotypes can be described: at the MRC, colonies displayed a 'cauliflower-shaped' morphotype whereas at the PISCES site, colonies presented a more flattened 'bush-shaped' morphotype; (2) living layer size was positively correlated with whole colony size; (3) live to dead layer ratio was negatively correlated to whole colony size; (4) live to dead layer ratio never exceeded 0.27. These results suggest that as a colony develops and its growth rate slows down, the proportion of living polyps in the colony decreases. Furthermore, at least 73% of L. pertusa colonies are composed of exposed dead coral skeleton, vulnerable to ocean acidification and the associated shallowing of the aragonite saturation horizon, with significant implications for future deep-sea reef framework integrity. The clear visual contrast between white/pale living and grey/dark dead portions of the colonies also gives a new way by which they can be visually monitored over time. The increased use of marine autonomous survey vehicles offers an important new platform from which such a surveying technique could be applied to monitor deep-water marine protected areas in the future.