On the paradox of thriving cold-water coral reefs in the food-limited deep sea

The deep sea is amongst the most food-limited habitats on Earth, as only a small fraction (<4%) of the surface primary production is exported below 200 m water depth. Here, cold-water coral (CWC) reefs form oases of life: their biodiversity compares with tropical coral reefs, their biomass and metabolic activity exceed other deep-sea ecosystems by far. We critically assess the paradox of thriving CWC reefs in the food-limited deep sea, by reviewing the literature and open-access data on CWC habitats. This review shows firstly that CWCs typically occur in areas where the food supply is not constantly low, but undergoes pronounced temporal variation. High currents, downwelling and/or vertically migrating zooplankton temporally boost the export of surface organic matter to the seabed, creating ‘feast’ conditions, interspersed with ‘famine’ periods during the non-productive season. Secondly, CWCs, particularly the most common reef-builder Desmophyllum pertusum (formerly known as Lophelia pertusa), are well adapted to these fluctuations in food availability. Laboratory and in situ measurements revealed their dietary flexibility, tissue reserves, and temporal variation in growth and energy allocation. Thirdly, the high structural and functional diversity of CWC reefs increases resource retention: acting as giant filters and sustaining complex food webs with diverse recycling pathways, the reefs optimise resource gains over losses. Anthropogenic pressures, including climate change and ocean acidification, threaten this fragile equilibrium through decreased resource supply, increased energy costs, and dissolution of the calcium-carbonate reef framework. Based on this review, we suggest additional criteria to judge the health of CWC reefs and their chance to persist in the future.publishedVersio

Reef communities associated with ‘dead’ cold-water coral framework drive resource retention and recycling in the deep sea

Cold-water coral (CWC) reefs create hotspots of metabolic activity in the deep sea, in spite of the limited supply of fresh organic matter from the ocean surface (i.e. phytodetritus). We propose that ‘dead’ coral framework, which harbours diverse faunal and microbial communities, boosts the metabolic activity of the reefs, through enhanced resource retention and recycling. Analysis of a video transect across a 700-540 m-deep CWC mound (Rockall Bank, North-East Atlantic) revealed a high benthic cover of dead framework (64%). Box-cored fragments of dead framework were incubated on-board and showed oxygen consumption rates of 0.078–0.182 μmol O2 (mmol organic carbon, i.e. OC)-1 h-1, indicating a substantial contribution to the total metabolic activity of the CWC reef. During the incubations, it was shown that the framework degradation stage influences nitrogen (re)cycling, corresponding to differences in community composition. New (less-degraded) framework released ammonium (0.005 ± 0.001 μmol NH4+ (mmol OC) 1 h 1), probably due to the activity of ammonotelic macrofauna. In contrast, old (more-degraded) framework released nitrate (0.015 ± 0.008 μmol NO3- (mmol OC)- 1 h- 1), indicating that nitrifying microorganisms recycled fauna-excreted ammonium to nitrate. Furthermore, the framework community removed natural dissolved organic matter (DOM) from the incubation water (0.005–0.122 μmol C (mmol OC)- 1 h- 1). Additional feeding experiments showed that all functional groups and macrofauna taxa of the framework community incorporated 13C-enriched (‘labelled’) DOM, indicating widespread DOM uptake and recycling. Finally, the framework effectively retained 13C-enriched phytodetritus, (a) by physical retention on the biofilm-covered surface and (b) by biological filtration through suspension-feeding fauna. We therefore suggest that the dead framework acts as a ‘filtration-recycling factory’ that enhances the metabolic activity of CWC reefs. The exposed framework, however, is particularly vulnerable to ocean acidification, jeopardizing this important aspect of CWC reef functioning

Biomass mapping for an improved understanding of the contribution of cold-water coral carbonate mounds to C and N cycling

This study used a novel approach combining biological, environmental, and ecosystem function data of the Logachev cold-water coral carbonate mound province to predictively map coral framework (bio)mass. A more accurate representation and quantification of cold-water coral reef ecosystem functions such as Carbon and Nitrogen stock and turnover were given by accounting for the spatial heterogeneity. Our results indicate that 45% is covered by dead and only 3% by live coral framework. The remaining 51%, is covered by fine sediments. It is estimated that 75,034–93,534 tons (T) of live coral framework is present in the area, of which ∼10% (7,747–9,316 T) consists of Cinorg and ∼1% (411–1,061 T) of Corg. A much larger amount of 3,485,828–4,357,435 T (60:1 dead:live ratio) dead coral framework contained ∼11% (418,299–522,892 T) Cinorg and &lt;1% (0–16 T) Corg. The nutrient turnover by dead coral framework is the largest, contributing 45–51% (2,596–3,626 T) C year–1 and 30–62% (290–1,989 T) N year–1 to the total turnover in the area. Live coral framework turns over 1,656–2,828 T C year–1 and 53–286 T N year–1. Sediments contribute between 1,216–1,512 T C year–1 and 629–919 T N year–1 to the area’s benthic organic matter mineralization. However, this amount is likely higher as sediments baffled by coral framework might play a much more critical role in reefs CN cycling than previously assumed. Our calculations showed that the area overturns 1–3.4 times the C compared to a soft-sediment area at a similar depth. With only 5–9% of the primary productivity reaching the corals via natural deposition, this study indicated that the supply of food largely depends on local hydrodynamical food supply mechanisms and the reefs ability to retain and recycle nutrients. Climate-induced changes in primary production, local hydrodynamical food supply and the dissolution of particle-baffling coral framework could have severe implications for the survival and functioning of cold-water coral reefs

On the paradox of thriving cold‐water coral reefs in the food‐limited deep sea

The deep sea is amongst the most food‐limited habitats on Earth, as only a small fraction of the surface primary production is exported below 200 m water depth. Here, cold‐water coral (CWC) reefs form oases of life: their biodiversity compares with tropical coral reefs, their biomass and metabolic activity exceed other deep‐sea ecosystems by far. We critically assess the paradox of thriving CWC reefs in the food‐limited deep sea, by reviewing the literature and open‐access data on CWC habitats. This review shows firstly that CWCs typically occur in areas where the food supply is not constantly low, but undergoes pronounced temporal variation. High currents, downwelling and/or vertically migrating zooplankton temporally boost the export of surface organic matter to the seabed, creating ‘feast’ conditions, interspersed with ‘famine’ periods during the non‐productive season. Secondly, CWCs, particularly the most common reef‐builder &lt;jats:italic&gt;Desmophyllum pertusum&lt;/jats:italic&gt; (formerly known as &lt;jats:italic&gt;Lophelia pertusa&lt;/jats:italic&gt;), are well adapted to these fluctuations in food availability. Laboratory and measurements revealed their dietary flexibility, tissue reserves, and temporal variation in growth and energy allocation. Thirdly, the high structural and functional diversity of CWC reefs increases resource retention: acting as giant filters and sustaining complex food webs with diverse recycling pathways, the reefs optimise resource gains over losses. Anthropogenic pressures, including climate change and ocean acidification, threaten this fragile equilibrium through decreased resource supply, increased energy costs, and dissolution of the calcium‐carbonate reef framework. Based on this review, we suggest additional criteria to judge the health of CWC reefs and their chance to persist in the future

Biomass mapping for an improved understanding of the contribution of cold-water coral carbonate mounds to C and N cycling

This study used a novel approach combining biological, environmental, and ecosystem function data of the Logachev cold-water coral carbonate mound province to predictively map coral framework (bio)mass. A more accurate representation and quantification of cold-water coral reef ecosystem functions such as Carbon and Nitrogen stock and turnover were given by accounting for the spatial heterogeneity. Our results indicate that 45% is covered by dead and only 3% by live coral framework. The remaining 51%, is covered by fine sediments. It is estimated that 75,034–93,534 tons (T) of live coral framework is present in the area, of which ∼10% (7,747–9,316 T) consists of Cinorg and ∼1% (411–1,061 T) of Corg. A much larger amount of 3,485,828–4,357,435 T (60:1 dead:live ratio) dead coral framework contained ∼11% (418,299–522,892 T) Cinorg and &lt;1% (0–16 T) Corg. The nutrient turnover by dead coral framework is the largest, contributing 45–51% (2,596–3,626 T) C year–1 and 30–62% (290–1,989 T) N year–1 to the total turnover in the area. Live coral framework turns over 1,656–2,828 T C year–1 and 53–286 T N year–1. Sediments contribute between 1,216–1,512 T C year–1 and 629–919 T N year–1 to the area’s benthic organic matter mineralization. However, this amount is likely higher as sediments baffled by coral framework might play a much more critical role in reefs CN cycling than previously assumed. Our calculations showed that the area overturns 1–3.4 times the C compared to a soft-sediment area at a similar depth. With only 5–9% of the primary productivity reaching the corals via natural deposition, this study indicated that the supply of food largely depends on local hydrodynamical food supply mechanisms and the reefs ability to retain and recycle nutrients. Climate-induced changes in primary production, local hydrodynamical food supply and the dissolution of particle-baffling coral framework could have severe implications for the survival and functioning of cold-water coral reefs

On the paradox of thriving cold‐water coral reefs in the food‐limited deep sea

The deep sea is amongst the most food‐limited habitats on Earth, as only a small fraction of the surface primary production is exported below 200 m water depth. Here, cold‐water coral (CWC) reefs form oases of life: their biodiversity compares with tropical coral reefs, their biomass and metabolic activity exceed other deep‐sea ecosystems by far. We critically assess the paradox of thriving CWC reefs in the food‐limited deep sea, by reviewing the literature and open‐access data on CWC habitats. This review shows firstly that CWCs typically occur in areas where the food supply is not constantly low, but undergoes pronounced temporal variation. High currents, downwelling and/or vertically migrating zooplankton temporally boost the export of surface organic matter to the seabed, creating ‘feast’ conditions, interspersed with ‘famine’ periods during the non‐productive season. Secondly, CWCs, particularly the most common reef‐builder &lt;jats:italic&gt;Desmophyllum pertusum&lt;/jats:italic&gt; (formerly known as &lt;jats:italic&gt;Lophelia pertusa&lt;/jats:italic&gt;), are well adapted to these fluctuations in food availability. Laboratory and measurements revealed their dietary flexibility, tissue reserves, and temporal variation in growth and energy allocation. Thirdly, the high structural and functional diversity of CWC reefs increases resource retention: acting as giant filters and sustaining complex food webs with diverse recycling pathways, the reefs optimise resource gains over losses. Anthropogenic pressures, including climate change and ocean acidification, threaten this fragile equilibrium through decreased resource supply, increased energy costs, and dissolution of the calcium‐carbonate reef framework. Based on this review, we suggest additional criteria to judge the health of CWC reefs and their chance to persist in the future

Building your own mountain: the effects, limits, and drawbacks of cold-water coral ecosystem engineering

Framework-forming cold-water corals (CWCs) are ecosystem engineers that build mounds in the deep sea that can be up to several hundred metres high. The effect of the presence of cold-water coral mounds on their surroundings is typically difficult to separate from environmental factors that are not affected by the mounds. We investigated the environmental control on and the importance of ecosystem engineering for cold-water coral reefs using annotated video transect data, spatial variables (MEMs), and hydrodynamic model outputs in a redundancy analysis and with variance partitioning. Using available hydrodynamic simulations with cold-water coral mounds and simulations where the mounds were artificially removed, we investigated the effect of coral mound ecosystem engineering on the spatial configuration of reef habitat and discriminated which environmental factors are and which are not affected by the mounds. We find that downward velocities in winter, related to non-engineered environmental factors, e.g. deep winter mixing and dense-water cascading, cause substantial differences in reef cover at the broadest spatial scale (20-30km). Such hydrodynamic processes that stimulate the food supply towards the corals in winter seem more important for the reefs than cold-water coral mound engineering or similar hydrodynamic processes in summer. While the ecosystem-engineering effect of cold-water corals is frequently discussed, our results also highlight the importance of non-engineered environmental processes. We further find that, due to the interaction between the coral mound and the water flow, different hydrodynamic zones are found on coral mounds that likely determine the typical benthic zonations of coral rubble at the mound foot, the dead coral framework on the mound flanks, and the living corals near the summit. Moreover, we suggest that a so-called Massenerhebung effect (well known for terrestrial mountains) exists, meaning that benthic zonation depends on the location of the mound rather than on the height above the seafloor or water depth. Our finding that ecosystem engineering determines the configuration of benthic habitats on cold-water coral mounds implies that cold-water corals cannot grow at deeper depths on the mounds to avoid the adverse effects of climate change

Drivers of Coral and Sponge Community Composition and Size Structure Revealed With Cumulative Abundance Profiles

Deep-sea corals and sponges form ecologically significant habitats that support biodiversity hotspots and contribute to important ecosystem functions such as carbon and nutrient cycling as well as benthic-pelagic coupling. However, quantifying their contributions to ecosystem functioning requires examination not only of the fine spatial distribution of community composition but also community size structure, because larger individuals are expected to contribute more to ecosystem functions than smaller ones. Here we create novel cumulative abundance profiles (CAPs) by combining body size structure with species abundance data to identify ecological drivers of sponge and coral community composition and size structure. Data were collected from 226 drop camera images captured near Saglek Bank, on the northern Labrador shelf and upper slope in the northwest Atlantic. The density of four coral and 17 sponge morphospecies were recorded from each image. The surface area covered by coral and sponge specimens was measured (1458 measurements in total) and converted to size estimates using data from live specimens collected with a rock dredge. Cumulative abundance profiles were then constructed and combined with cluster analysis to identify distinct community assemblages. In addition, distance-based redundancy analysis was used to identify environmental drivers influencing cluster community composition and/or size structure. Finally, organic carbon turnover was calculated for each cluster using published respiration data. Three assemblages were identified with differing composition and size structures. One of these was characterized by large coral and sponge morphospecies and individuals. The spatial distribution of this cluster was controlled by interactions between substrate type, terrain position index (TPI) and orientation of the slope (eastness). When analysing composition or size structure separately, dissolved oxygen and current speed respectively were also identified as key parameters. This finding indicates that substrate type and TPI influence the presence of coral and sponges in the study area, while dissolved oxygen may constrain which morphospecies are present and bottom currents restrict the size of individuals. As predicted, high levels of carbon turnover were driven by large sponge and coral individuals, likely maintained in part by the sponge loop in which sponges recycle dissolved organic matter into particulate organic matter. This study gives the first demonstration of how CAPs can be used to analyse spatial variation in deep-sea benthic community composition and size structure and appropriately quantify contribution to ecosystem functions such as carbon turnover

Building your own mountain: The effects, limits, and drawbacks of cold-water coral ecosystem engineering

Framework-forming cold-water corals are ecosystem engineers that build mounds in the deep-sea that can be several hundred meters high. The effect of the presence of cold-water coral mounds on their surrounding is typically difficult to separate from environmental factors that are not affected by the mounds. We investigated the environmental control on cold-water coral reefs at multiple spatial scales, using annotated video transects data, spatial variables (MEMs) and hydrodynamic model output in a redundancy analysis and with variance partitioning. Using available hydrodynamic simulations with cold-water coral mounds and simulations where the mounds were artificially removed, we investigated the effect of coral mound ecosystem engineering on the spatial configuration of reef habitat and discriminated which environmental factors are and which are not affected by the mounds. We find that, due to the interaction between the coral mound and the water flow, different hydrodynamic zones are created on a coral mound that likely determine the typical benthic zonation of coral rubble at the mound foot, dead coral framework on the mound flank, and living corals near the summit. Moreover, we observed a so-called massenerhebung effect (well-known for terrestrial mountains) meaning that benthic zonation depends on the location on the mound rather than on the height above the seafloor or water depth. Our finding that ecosystem engineering determines the configuration of benthic habitats on cold-water coral mounds has many implications, such as that cold-water corals cannot simply move towards deeper water depths to avoid the adverse effects of climate change. We further find that downward velocities in winter, related to non-engineered environmental factors, e.g., deep winter mixing and dense water cascading, correlated to substantial differences in reef cover at the broadest spatial scale (20–30 km). Such hydrodynamic processes that stimulate the food supply towards the corals in winter are more important for the reefs than similar hydrodynamic processes in summer. There is much research on the ecosystem engineering effects of cold-water corals, but our results highlight that the influence of non-engineered environmental processes that accelerate the food supply towards the cold-water corals should not be underestimated

Characterizing regional oceanography and bottom environmental conditions at two contrasting sponge grounds on the northern Labrador Shelf

Abstract. Deep-sea sponge grounds are distributed globally and are considered hotspots of biological diversity and biogeochemical cycling. To date, little is known about the environmental conditions that allow high sponge biomass to develop in the deep sea. Here, we characterize oceanographic conditions at two contrasting sites off the northern Labrador Shelf with respective high and low sponge biomass. Data were collected by year-long benthic lander deployments equipped with current meters, a turbidity and chlorophyll-a measuring device, and a sediment trap. Additionally, regional oceanography was described by analysing vertical conductivity–temperature–depth (CTD) casts, Argo float profiles, and surface buoy drifter data for the northern Labrador Shelf from 2005 to 2022. The stable isotopic composition of benthic fauna was determined to investigate food web structure at the sponge grounds. Our results revealed strong (0.26±0.14 m s−1; mean ± SD) semidiurnal tidal currents at the high-sponge-biomass site but 2-fold weaker currents (0.14±0.08 m s−1; mean ± SD) at the low-sponge-biomass site. Tidal analysis suggests that kinetic energy is dissipated from barotropic tide to baroclinic tide/turbulence at the high-sponge-biomass site, which could enhance food availability for benthic organisms. Bottom nutrient concentrations were elevated at the high-sponge-biomass site, which would benefit growth in deep-sea sponges. Organic matter flux to the seafloor was increased at the high-sponge-biomass site and consisted of fresher material. Finally, both sponge grounds demonstrated tight benthic–pelagic coupling prior to the onset of stratification. Stable isotope signatures indicated that soft corals (Primnoa resedaeformis) fed on suspended particulate organic matter, while massive sponges (Geodia spp.) likely utilized additional food sources. Our results imply that benthic fauna at the high-sponge-biomass site benefit from strong tidal currents, which increase the food supply, and favourable regional ocean currents, which increase the nutrient concentration in bottom waters. </jats:p