Spatial self-organization as a new perspective on cold-water coral mound development

Cold-water corals build extensive reefs on the seafloor that are oases of biodiversity, biomass, and organic matter processing rates. The reefs baffle sediments, and when coral growth and sedimentation outweigh ambient sedimentation, carbonate mounds of tens to hundreds of meters high and several kilometers wide can form. Because coral mounds form over ten-thousands of years, their development process remains elusive. While several environmental factors influence mound development, the mounds also have a major impact on their environment. This feedback between environment and mounds, and how this drives mound development is the focus of this paper. Based on the similarity of spatial coral mound patterns and patterns in self-organized ecosystems, we provide a new perspective on coral mound development. In accordance with the theory of self-organization through scale-dependent feedbacks, we first elicit the processes that are known to affect mound development, and might cause scale-dependent feedbacks. Then we demonstrate this concept with model output from a study on the Logachev area, SW Rockall Trough margin. Spatial patterns in mound provinces are the result of a complex set of interacting processes. Spatial self-organization provides a framework in which to place and compare these processes, so as to assess if and how they contribute to pattern formation in coral mounds

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

Resemblance of the global depth distribution of internal-tide generation and cold-water coral occurrences

Internal tides are known to be an important source of mixing in the oceans, especially in the bottom boundary layer. The depth of internal-tide generation therefore seems important for benthic life and the formation of cold-water coral mounds, but internal-tide conversion is generally investigated in a depth-integrated sense. Using both idealized and realistic simulations on continental slopes, we found that the depth of internal-tide generation increases with increasing slope steepness and decreases with intensified shallow stratification. The depth of internal-tide generation also shows a typical latitudinal dependency related to Coriolis effects. Using a global database of cold-water corals, we found that, especially in Northern Hemisphere autumn and winter, the global depth pattern of internal-tide generation correlates (rautumn D 0.70, rwinter D 0.65, p < 0.01) with that of coldwater corals: shallowest near the poles and deepest around the Equator, with a decrease in depth around 25° S and N, and shallower north of the Equator than south. We further found that cold-water corals are situated significantly more often on topography that is steeper than the internal-tide beam (i.e. where supercritical reflection of internal tides occurs) than would be expected from a random distribution: in our study, in 66.9 % of all cases, cold-water corals occurred on a topography that is supercritical to the M2 tide whereas globally only 9.4 % of all topography is supercritical. Our findings underline internal-tide generation and the occurrence of supercritical reflection of internal tides as globally important for cold-water coral growth. The energetic dynamics associated with internal-tide generation and the supercritical reflection of internal tides likely increase the food supply towards the reefs in food-limited winter months. With climate change, stratification is expected to increase. Based on our results, this would decrease the depth of internal-tide generation, possibly creating new suitable habitat for cold-water corals shallower on continental slopes

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

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

The global correlation between internal-tide generation and the depth-distribution of cold-water corals

Internal tides are known to be an important source of mixing in the oceans, especially in the bottom boundary layer. The depth of internal-tide generation therefore seems important for benthic life and the formation of cold-water coral mounds, but internal-tidal conversion is generally investigated in a depth-integrated sense. Using both idealized and realistic simulations on continental slopes, we found that the depth of internal-tide generation increases with increasing slope steepness and decreases with intensified shallow stratification. The depth of internal-tide generation also shows a typical latitudinal dependency. Using a global database of cold-water corals, we found that the depth-pattern of internal-tide generation is remarkably similar to the depth-pattern of cold-water corals globally: shallowest near the poles and deepest around the equator with a shoaling around 25 degrees South and North and shallower north of the equator than south of the equator. We further found that cold-water corals are, more than what would be expected by chance, associated to the (super)critical reflection of internal tides (i.e., situated on topography that is steeper than the internal tidal beam) and to trapped internal tides (i.e., above the critical latitude of 70 degrees for semidiurnal tides and 30 degrees for diurnal tides). The (super)critical reflection of internal tides and trapped internal tides therefore provide an interesting new angle of food supply mechanisms that has not yet been considered in cold-water coral studies. With climate change, stratification is expected to increase. Based on our results, this would cause a shoaling of internal-tide generation, possibly creating new shallower suitable habitat for cold-water corals on continental slopes

Tiger reefs: Self‐organized regular patterns in deep‐sea cold‐water coral reefs

Complexity theory predicts that self-organized, regularly patterned ecosystems store more biomass and are more resilient than spatially uniform systems. Self-organized ecosystems are well-known from the terrestrial realm, with “tiger bushes” being the archetypical example and mussel beds and tropical coral reefs the marine examples. We here identify regular spatial patterns in cold-water coral reefs (nicknamed “tiger reefs”) from video transects and argue that these are likely the result of self-organization. We used variograms and Lomb–Scargle analysis of seven annotated video transects to analyze spatial patterns in live coral and dead coral (i.e., skeletal remains) cover at the Logachev coral mound province (NE Atlantic Ocean) and found regular spatial patterns with length scales between 62 and 523 m in live and dead coral distribution along these transects that point to self-organization of cold-water coral reefs. Self-organization theory shows that self-organized ecosystems can withstand large environmental changes by adjusting their spatial configuration. We found indications that cold-water corals can similarly adjust their spatial configuration, possibly providing resilience in the face of climate change. Dead coral framework remains in the environment for extended periods of time, providing a template for spatial patterns that facilitates live coral recovery. The notion of regular spatial patterns in cold-water coral reefs is interesting for cold-water coral restoration, as transplantation will be more successful when it follows the patterns that are naturally present. This finding also underlines that anthropogenic effects such as ocean acidification and bottom trawling that destroy the dead coral template undermine cold-water coral resilience. Differences in the pattern periodicities of live and dead coral cover further present an interesting new angle to investigate past and present environmental conditions in cold-water coral reefs

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

Tiger reefs: Self-organized regular patterns in deep-sea cold-water coral reefs

Abstract Complexity theory predicts that self-organized, regularly patterned ecosystems store more biomass and are more resilient than spatially uniform systems. Self-organized ecosystems are well-known from the terrestrial realm, with “tiger bushes” being the archetypical example and mussel beds and tropical coral reefs the marine examples. We here identify regular spatial patterns in cold-water coral reefs (nicknamed “tiger reefs”) from video transects and argue that these are likely the result of self-organization. We used variograms and Lomb–Scargle analysis of seven annotated video transects to analyze spatial patterns in live coral and dead coral (i.e., skeletal remains) cover at the Logachev coral mound province (NE Atlantic Ocean) and found regular spatial patterns with length scales between 62 and 523 m in live and dead coral distribution along these transects that point to self-organization of cold-water coral reefs. Self-organization theory shows that self-organized ecosystems can withstand large environmental changes by adjusting their spatial configuration. We found indications that cold-water corals can similarly adjust their spatial configuration, possibly providing resilience in the face of climate change. Dead coral framework remains in the environment for extended periods of time, providing a template for spatial patterns that facilitates live coral recovery. The notion of regular spatial patterns in cold-water coral reefs is interesting for cold-water coral restoration, as transplantation will be more successful when it follows the patterns that are naturally present. This finding also underlines that anthropogenic effects such as ocean acidification and bottom trawling that destroy the dead coral template undermine cold-water coral resilience. Differences in the pattern periodicities of live and dead coral cover further present an interesting new angle to investigate past and present environmental conditions in 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