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.

Identification of tolerance levels on the cold-water coral Desmophyllum pertusum (Lophelia pertusa) from realistic exposure conditions to suspended bentonite, barite and drill cutting particles.

Cold-water coral (CWC) reefs are numerous and widespread along the Norwegian continental shelf where oil and gas industry operate. Uncertainties exist regarding their impacts from operational discharges to drilling. Effect thresholds obtained from near-realistic exposure of suspended particle concentrations for use in coral risk modeling are particularly needed. Here, nubbins of Desmophyllum pertusum (Lophelia pertusa) were exposed shortly (5 days, 4h repeated pulses) to suspended particles (bentonite BE; barite BA, and drill cuttings DC) in the range of ~ 4 to ~ 60 mg.l-1 (actual concentration). Physiological responses (respiration rate, growth rate, mucus-related particulate organic carbon OC and particulate organic nitrogen ON) and polyp mortality were then measured 2 and 6 weeks post-exposure to assess long-term effects. Respiration and growth rates were not significantly different in any of the treatments tested compared to control. OC production was not affected in any treatment, but a significant increase of OC:ON in mucus produced by BE-exposed (23 and 48 mg.l-1) corals was revealed 2 weeks after exposure. Polyp mortality increased significantly at the two highest DC doses (19 and 49 mg.l-1) 2 and 6 weeks post-exposure but no significant difference was observed in any of the other treatments compared to the control. These findings are adding new knowledge on coral resilience to short realistic exposure of suspended drill particles and indicate overall a risk for long-term effects at a threshold of ~20 mg.l-1.

Polymetallic nodules are essential for food-web integrity of a prospective deep-seabed mining area in Pacific abyssal plains.

Polymetallic nodule fields provide hard substrate for sessile organisms on the abyssal seafloor between 3000 and 6000 m water depth. Deep-seabed mining targets these mineral-rich nodules and will likely modify the consumer-resource (trophic) and substrate-providing (non-trophic) interactions within the abyssal food web. However, the importance of nodules and their associated sessile fauna in supporting food-web integrity remains unclear. Here, we use seafloor imagery and published literature to develop highly-resolved trophic and non-trophic interaction webs for the Clarion-Clipperton Fracture Zone (CCZ, central Pacific Ocean) and the Peru Basin (PB, South-East Pacific Ocean) and to assess how nodule removal may modify these networks. The CCZ interaction web included 1028 compartments connected with 59,793 links and the PB interaction web consisted of 342 compartments and 8044 links. We show that knock-down effects of nodule removal resulted in a 17.9% (CCZ) to 20.8% (PB) loss of all taxa and 22.8% (PB) to 30.6% (CCZ) loss of network links. Subsequent analysis identified stalked glass sponges living attached to the nodules as key structural species that supported a high diversity of associated fauna. We conclude that polymetallic nodules are critical for food-web integrity and that their absence will likely result in reduced local benthic biodiversity.

The BenBioDen database, a global database for meio-, macro- and megabenthic biomass and densities.

Benthic fauna refers to all fauna that live in or on the seafloor, which researchers typically divide into size classes meiobenthos (32/64 µm-0.5/1 mm), macrobenthos (250 µm-1 cm), and megabenthos (>1 cm). Benthic fauna play important roles in bioturbation activity, mineralization of organic matter, and in marine food webs. Evaluating their role in these ecosystem functions requires knowledge of their global distribution and biomass. We therefore established the BenBioDen database, the largest open-access database for marine benthic biomass and density data compiled so far. In total, it includes 11,792 georeferenced benthic biomass and 51,559 benthic density records from 384 and 600 studies, respectively. We selected all references following the procedure for systematic reviews and meta-analyses, and report biomass records as grams of wet mass, dry mass, or ash-free dry mass, or carbon per m2 and as abundance records as individuals per m2. This database provides a point of reference for future studies on the distribution and biomass of benthic fauna.

Heterotrophy in the earliest gut: a single-cell view of heterotrophic carbon and nitrogen assimilation in sponge-microbe symbioses.

Sponges are the oldest known extant animal-microbe symbiosis. These ubiquitous benthic animals play an important role in marine ecosystems in the cycling of dissolved organic matter (DOM), the largest source of organic matter on Earth. The conventional view on DOM cycling through microbial processing has been challenged by the interaction between this efficient filter-feeding host and its diverse and abundant microbiome. Here we quantify, for the first time, the role of host cells and microbial symbionts in sponge heterotrophy. We combined stable isotope probing and nanoscale secondary ion mass spectrometry to compare the processing of different sources of DOM (glucose, amino acids, algal-produced) and particulate organic matter (POM) by a high-microbial abundance (HMA) and low-microbial abundance (LMA) sponge with single-cell resolution. Contrary to common notion, we found that both microbial symbionts and host choanocyte (i.e. filter) cells and were active in DOM uptake. Although all DOM sources were assimilated by both sponges, higher microbial biomass in the HMA sponge corresponded to an increased capacity to process a greater variety of dissolved compounds. Nevertheless, in situ feeding data demonstrated that DOM was the primary carbon source for both the LMA and HMA sponge, accounting for ~90% of their heterotrophic diets. Microbes accounted for the majority (65-87%) of DOM assimilated by the HMA sponge (and ~60% of its total heterotrophic diet) but <5% in the LMA sponge. We propose that the evolutionary success of sponges is due to their different strategies to exploit the vast reservoir of DOM in the ocean.

Recycling pathways in cold-water coral reefs: Use of dissolved organic matter and bacteria by key suspension feeding taxa.

Cold-water coral (CWC) reefs are one of the most diverse and productive ecosystems in the deep sea. Especially in periods of seasonally-reduced phytodetritus food supply, their high productivity may depend on the recycling of resources produced on the reef, such as dissolved organic matter (DOM) and bacteria. Here, we demonstrate that abundant suspension feeders Geodia barretti (high-microbial-abundance sponge), Mycale lingua (low-microbial-abundance sponge) and Acesta excavata (bivalve) are able to utilize 13C-enriched (diatom-derived) DOM and bacteria for tissue growth and respiration. While DOM was an important potential resource for all taxa, utilization of bacteria was higher for the sponges as compared to the bivalve, indicating a particle-size differentiation among the investigated suspension feeders. Interestingly, all taxa released 13C-enriched particulate organic carbon, which in turn may feed the detritus pathway on the reef. Especially A. excavata produced abundant (pseudo-)fecal droppings. A second stable-isotope tracer experiment revealed that detritivorous ophiuroids utilized these droppings. The high resource flexibility of dominant reef suspension feeders, and the efficient recycling of their waste products by the detritivore community, may provide important pathways to maintain the high productivity on cold-water coral reefs, especially in periods of low external food supply.

A Worm's World: Ecological Flexibility Pays Off for Free-Living Nematodes in Sediments and Soils.

Free-living nematodes, an ancient animal phylum of unsegmented microscopic roundworms, have successfully adapted to nearly every ecosystem on Earth: from marine and freshwater to land, from the polar regions to the tropics, and from the mountains to the ocean depths. They are globally the most abundant animals in sediments and soils. In the present article, we identify the factors that collectively explain the successful ecological proliferation of free-living nematodes and demonstrate the impact they have on vital sediment and soil processes. The ecological success of nematodes is strongly linked to their ability to feed on various food sources that are present in both sediments and soils, and to proliferate rapidly and survive in contrasting environmental conditions. The adaptations, roles, and behaviors of free-living nematodes have important implications for the resilience of sediments and soils, and for emergent animal communities responding to human alterations to ecosystems worldwide.

Corrigendum: A Worm's World: Ecological Flexibility Pays Off for Free-Living Nematodes in Sediments and Soils.

[This corrects the article DOI: 10.1093/biosci/biz086.].

The SCOC database, a large, open, and global database with sediment community oxygen consumption rates.

Sediment community oxygen consumption (SCOC) rates provide important information about biogeochemical processes in marine sediments and the activity of benthic microorganisms and fauna. Therefore, several databases of SCOC data have been compiled since the mid-1990s. However, these earlier databases contained much less data records and were not freely available. Additionally, the databases were not transparent in their selection procedure, so that other researchers could not assess the quality of the data. Here, we present the largest, best documented, and freely available database of SCOC data compiled to date. The database is comprised of 3,540 georeferenced SCOC records from 230 studies that were selected following the procedure for systematic reviews and meta-analyses. Each data record states whether the oxygen consumption was measured ex situ or in situ, as total oxygen uptake, diffusive or advective oxygen uptake, and which measurement device was used. The database will be curated and updated annually to secure and maintain an up-to-date global database of SCOC data.

Spiculous skeleton formation in the freshwater sponge Ephydatia fluviatilis under hypergravity conditions.

Successful dispersal of freshwater sponges depends on the formation of dormant sponge bodies (gemmules) under adverse conditions. Gemmule formation allows the sponge to overcome critical environmental conditions, for example, desiccation or freezing, and to re-establish as a fully developed sponge when conditions are more favorable. A key process in sponge development from hatched gemmules is the construction of the silica skeleton. Silica spicules form the structural support for the three-dimensional filtration system the sponge uses to filter food particles from ambient water. We studied the effect of different hypergravity forces (1, 2.5, 5, 10, and 20 × g for 48 h)-as measure for environmental stress-on the ability of developing sponges to set-up their spiculous skeleton. Additionally, we assessed whether the addition of nutrients (i.e., dissolved 13C- and 15N-labeled amino acids) compensates for this stress. Our results show that freshwater sponges can withstand prolonged periods of hypergravity exposure and successfully set-up their skeleton, even after 48 h under 20 × g. Developing sponges were found to take up and assimilate dissolved food before forming a functional filtering system. However, fed and non-fed sponges showed no differences in skeleton formation and relative surface area growth, suggesting that the gemmules' intrinsic energy fulfills the processes of skeleton construction. Additionally, non-fed sponges formed oscula significantly more often than fed sponges, especially under higher g-forces. This suggests that the eventual formation of a filtration system might be stimulated by food deprivation and environmentally stressful conditions. These findings indicate that the process of spiculous skeleton formation is energy-efficient and highly resilient. The uptake of dissolved food substances by freshwater sponges may contribute to the cycling of dissolved organic matter in freshwater ecosystems where sponges are abundant.

Metabolic rates are significantly lower in abyssal Holothuroidea than in shallow-water Holothuroidea.

Recent analyses of metabolic rates in fishes, echinoderms, crustaceans and cephalopods have concluded that bathymetric declines in temperature- and mass-normalized metabolic rate do not result from resource-limitation (e.g. oxygen or food/chemical energy), decreasing temperature or increasing hydrostatic pressure. Instead, based on contrasting bathymetric patterns reported in the metabolic rates of visual and non-visual taxa, declining metabolic rate with depth is proposed to result from relaxation of selection for high locomotory capacity in visual predators as light diminishes. Here, we present metabolic rates of Holothuroidea, a non-visual benthic and benthopelagic echinoderm class, determined in situ at abyssal depths (greater than 4000 m depth). Mean temperature- and mass-normalized metabolic rate did not differ significantly between shallow-water (less than 200 m depth) and bathyal (200-4000 m depth) holothurians, but was significantly lower in abyssal (greater than 4000 m depth) holothurians than in shallow-water holothurians. These results support the dominance of the visual interactions hypothesis at bathyal depths, but indicate that ecological or evolutionary pressures other than biotic visual interactions contribute to bathymetric variation in holothurian metabolic rates. Multiple nonlinear regression assuming power or exponential models indicates that in situ hydrostatic pressure and/or food/chemical energy availability are responsible for variation in holothurian metabolic rates. Consequently, these results have implications for modelling deep-sea energetics and processes.

Niche overlap between a cold-water coral and an associated sponge for isotopically-enriched particulate food sources.

The cold-water coral Lophelia pertusa is an ecosystem engineer that builds reef structures on the seafloor. The interaction of the reef topography with hydrodynamics is known to enhance the supply of suspended food sources to the reef communities. However, the reef framework is also a substrate for other organisms that may compete for the very same suspended food sources. Here, we used the passive suspension feeder Lophelia pertusa and the active suspension feeding sponge Hymedesmia coriacea as model organisms to study niche overlap using isotopically-enriched algae and bacteria as suspended food sources. The coral and the sponge were fed with a combination of 13C-enriched bacteria/15N-enriched algae or 15N-enriched bacteria/13C-enriched algae, which was subsequently traced into bulk tissue, coral skeleton and dissolved inorganic carbon (i.e. respiration). Both the coral and the sponge assimilated and respired the suspended bacteria and algae, indicating niche overlap between these species. The assimilation rates of C and N into bulk tissue of specimens incubated separately were not significantly different from assimilation rates during incubations with co-occurring corals and sponges. Hence, no evidence for exploitative resource competition was found, but this is likely due to the saturating experimental food concentration that was used. We do not rule out that exploitative competition occurs in nature during periods of low food concentrations. Food assimilation and respiration rates of the sponge were almost an order of magnitude higher than those of the cold-water coral. We hypothesize that the active suspension feeding mode of the sponge explains the observed differences in resource uptake as opposed to the passive suspension feeding mode of the cold-water coral. These feeding mode differences may set constraints on suitable habitats for cold-water corals and sponges in their natural habitats.

Resilience of benthic deep-sea fauna to mining activities.

With increasing demand for mineral resources, extraction of polymetallic sulphides at hydrothermal vents, cobalt-rich ferromanganese crusts at seamounts, and polymetallic nodules on abyssal plains may be imminent. Here, we shortly introduce ecosystem characteristics of mining areas, report on recent mining developments, and identify potential stress and disturbances created by mining. We analyze species' potential resistance to future mining and perform meta-analyses on population density and diversity recovery after disturbances most similar to mining: volcanic eruptions at vents, fisheries on seamounts, and experiments that mimic nodule mining on abyssal plains. We report wide variation in recovery rates among taxa, size, and mobility of fauna. While densities and diversities of some taxa can recover to or even exceed pre-disturbance levels, community composition remains affected after decades. The loss of hard substrata or alteration of substrata composition may cause substantial community shifts that persist over geological timescales at mined sites.

Ecosystem engineering creates a direct nutritional link between 600-m deep cold-water coral mounds and surface productivity.

Cold-water corals (CWCs) form large mounds on the seafloor that are hotspots of biodiversity in the deep sea, but it remains enigmatic how CWCs can thrive in this food-limited environment. Here, we infer from model simulations that the interaction between tidal currents and CWC-formed mounds induces downwelling events of surface water that brings organic matter to 600-m deep CWCs. This positive feedback between CWC growth on carbonate mounds and enhanced food supply is essential for their sustenance in the deep sea and represents an example of ecosystem engineering of unparalleled magnitude. This 'topographically-enhanced carbon pump' leaks organic matter that settles at greater depths. The ubiquitous presence of biogenic and geological topographies along ocean margins suggests that carbon sequestration through this pump is of global importance. These results indicate that enhanced stratification and lower surface productivity, both expected consequences of climate change, may negatively impact the energy balance of CWCs.

Direct Visualization of Mucus Production by the Cold-Water Coral Lophelia pertusa with Digital Holographic Microscopy.

Lophelia pertusa is the dominant reef-building organism of cold-water coral reefs, and is known to produce significant amounts of mucus, which could involve an important metabolic cost. Mucus is involved in particle removal and feeding processes, yet the triggers and dynamics of mucus production are currently still poorly described because the existing tools to study these processes are not appropriate. Using a novel microscopic technique-digital holographic microscopy (DHM)-we studied the mucus release of L. pertusa under various experimental conditions. DHM technology permits µm-scale observations and allows the visualization of transparent mucoid substances in real time without staining. Fragments of L. pertusa were first maintained in flow-through chambers without stressors and imaged with DHM, then exposed to various stressors (suspended particles, particulate food and air exposure) and re-imaged. Under non-stressed conditions no release of mucus was observed, whilst mucus strings and sheaths were produced in response to suspended particles (activated charcoal and drill cuttings sediment) i.e. in a stressed condition. Mucus strings and so-called 'string balls' were also observed in response to exposure to particulate food (brine shrimp Artemia salina). Upon air-exposure, mucus production was clearly visible once the fragments were returned to the flow chamber. Distinct optical properties such as optical path length difference (OPD) were measured with DHM in response to the various stimuli suggesting that different mucus types are produced by L. pertusa. Mucus produced to reject particles is similar in refractive index to the surrounding seawater, suggesting that the energy content of this mucus is low. In contrast, mucus produced in response to either food particle addition or air exposure had a higher refractive index, suggesting a higher metabolic investment in the production of these mucoid substances. This paper shows for the first time the potential of DHM technology for the detection, characterization and quantification of mucus production through OPD measurements in L. pertusa.

Coral mucus fuels the sponge loop in warm- and cold-water coral reef ecosystems.

Shallow warm-water and deep-sea cold-water corals engineer the coral reef framework and fertilize reef communities by releasing coral mucus, a source of reef dissolved organic matter (DOM). By transforming DOM into particulate detritus, sponges play a key role in transferring the energy and nutrients in DOM to higher trophic levels on Caribbean reefs via the so-called sponge loop. Coral mucus may be a major DOM source for the sponge loop, but mucus uptake by sponges has not been demonstrated. Here we used laboratory stable isotope tracer experiments to show the transfer of coral mucus into the bulk tissue and phospholipid fatty acids of the warm-water sponge Mycale fistulifera and cold-water sponge Hymedesmia coriacea, demonstrating a direct trophic link between corals and reef sponges. Furthermore, 21-40% of the mucus carbon and 32-39% of the nitrogen assimilated by the sponges was subsequently released as detritus, confirming a sponge loop on Red Sea warm-water and north Atlantic cold-water coral reefs. The presence of a sponge loop in two vastly different reef environments suggests it is a ubiquitous feature of reef ecosystems contributing to the high biogeochemical cycling that may enable coral reefs to thrive in nutrient-limited (warm-water) and energy-limited (cold-water) environments.

Discovery of symbiotic nitrogen fixation and chemoautotrophy in cold-water corals.

Cold-water corals (CWC) are widely distributed around the world forming extensive reefs at par with tropical coral reefs. They are hotspots of biodiversity and organic matter processing in the world's deep oceans. Living in the dark they lack photosynthetic symbionts and are therefore considered to depend entirely on the limited flux of organic resources from the surface ocean. While symbiotic relations in tropical corals are known to be key to their survival in oligotrophic conditions, the full metabolic capacity of CWC has yet to be revealed. Here we report isotope tracer evidence for efficient nitrogen recycling, including nitrogen assimilation, regeneration, nitrification and denitrification. Moreover, we also discovered chemoautotrophy and nitrogen fixation in CWC and transfer of fixed nitrogen and inorganic carbon into bulk coral tissue and tissue compounds (fatty acids and amino acids). This unrecognized yet versatile metabolic machinery of CWC conserves precious limiting resources and provides access to new nitrogen and organic carbon resources that may be essential for CWC to survive in the resource-depleted dark ocean.

Tiny is mighty: seagrass beds have a large role in the export of organic material in the tropical coastal zone.

Ecosystems in the tropical coastal zone exchange particulate organic matter (POM) with adjacent systems, but differences in this function among ecosystems remain poorly quantified. Seagrass beds are often a relatively small section of this coastal zone, but have a potentially much larger ecological influence than suggested by their surface area. Using stable isotopes as tracers of oceanic, terrestrial, mangrove and seagrass sources, we investigated the origin of particulate organic matter in nine mangrove bays around the island of Phuket (Thailand). We used a linear mixing model based on bulk organic carbon, total nitrogen and δ13C and δ15N and found that oceanic sources dominated suspended particulate organic matter samples along the mangrove-seagrass-ocean gradient. Sediment trap samples showed contributions from four sources oceanic, mangrove forest/terrestrial and seagrass beds where oceanic had the strongest contribution and seagrass beds the smallest. Based on ecosystem area, however, the contribution of suspended particulate organic matter derived from seagrass beds was disproportionally high, relative to the entire area occupied by mangrove forests, the catchment area (terrestrial) and seagrass beds. The contribution from mangrove forests was approximately equal to their surface area, whereas terrestrial contributions to suspended organic matter under contributed compared to their relative catchment area. Interestingly, mangrove forest contribution at 0 m on the transects showed a positive relationship with the exposed frontal width of the mangrove, indicating that mangrove forest exposure to hydrodynamic energy may be a controlling factor in mangrove outwelling. However we found no relationship between seagrass bed contribution and any physical factors, which we measured. Our results indicate that although seagrass beds occupy a relatively small area of the coastal zone, their role in the export of organic matter is disproportional and should be considered in coastal management especially with respect to their importance as a nutrient source for other ecosystems and organisms.

Phospholipid-derived fatty acids and quinones as markers for bacterial biomass and community structure in marine sediments.

Phospholipid-derived fatty acids (PLFA) and respiratory quinones (RQ) are microbial compounds that have been utilized as biomarkers to quantify bacterial biomass and to characterize microbial community structure in sediments, waters, and soils. While PLFAs have been widely used as quantitative bacterial biomarkers in marine sediments, applications of quinone analysis in marine sediments are very limited. In this study, we investigated the relation between both groups of bacterial biomarkers in a broad range of marine sediments from the intertidal zone to the deep sea. We found a good log-log correlation between concentrations of bacterial PLFA and RQ over several orders of magnitude. This relationship is probably due to metabolic variation in quinone concentrations in bacterial cells in different environments, whereas PLFA concentrations are relatively stable under different conditions. We also found a good agreement in the community structure classifications based on the bacterial PLFAs and RQs. These results strengthen the application of both compounds as quantitative bacterial biomarkers. Moreover, the bacterial PLFA- and RQ profiles revealed a comparable dissimilarity pattern of the sampled sediments, but with a higher level of dissimilarity for the RQs. This means that the quinone method has a higher resolution for resolving differences in bacterial community composition. Combining PLFA and quinone analysis as a complementary method is a good strategy to yield higher resolving power in bacterial community structure.

Surviving in a marine desert: the sponge loop retains resources within coral reefs.

Ever since Darwin's early descriptions of coral reefs, scientists have debated how one of the world's most productive and diverse ecosystems can thrive in the marine equivalent of a desert. It is an enigma how the flux of dissolved organic matter (DOM), the largest resource produced on reefs, is transferred to higher trophic levels. Here we show that sponges make DOM available to fauna by rapidly expelling filter cells as detritus that is subsequently consumed by reef fauna. This "sponge loop" was confirmed in aquarium and in situ food web experiments, using (13)C- and (15)N-enriched DOM. The DOM-sponge-fauna pathway explains why biological hot spots such as coral reefs persist in oligotrophic seas--the reef's paradox--and has implications for reef ecosystem functioning and conservation strategies.