Dick van Oevelen

Quantifying Food Web Flows Using Linear Inverse Models

The quantitative mapping of food web flows based on empirical data is a crucial yet difficult task in ecology. The difficulty arises from the under-sampling of food webs, because most data sets are incomplete and uncertain. In this article, we review methods to quantify food web flows based on empirical data using linear inverse models (LIM). The food web in a LIM is described as a linear function of its flows, which are estimated from empirical data by inversemodeling. The under-sampling of food webs implies that infinitely many different solutions exist that are consistent with a given data set. The existing approaches to food web LIM select a single solution from this infinite set by invoking additional assumptions: either a specific selection criterion that has no solid ecological basis is used or the data set is artificially upgraded by assigning fixed values to, for example, physiological parameters. Here, we advance a likelihood approach (LA) that follows a different solution philosophy. Rather than singling out one particular solution, the LA generates a large set of possible solutions from which the marginal probability density function (mPDF) of each flow and correlations between flows can be derived. The LA is exemplified with an example model of a soil food web and is made available in the open-source R-software. Moreover, we show how stoichiometric data, stable isotope signatures, and fatty acid compositions can be included in the LIM to alleviate the under-sampling problem. Overall, LIM prove to be a powerful tool in food web research, which can bridge the gap between empirical data and the analysis of food web structures.

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.

Tolerance to long-term exposure of suspended benthic sediments and drill cuttings in the cold-water coral Lophelia pertusa

The cold-water coral Lophelia pertusa was exposed to suspended particles (<63 μm) for 12 weeks. Skeletal growth was significantly lower under exposure concentrations of ∼25 mg l⁻¹ than ∼5 mg l⁻¹ and there was a trend of lower growth rates when exposed to water-based drill cuttings than to natural benthic sediment. Polyp extension was less in corals exposed to higher material concentrations, which provides a possible explanation for observed skeletal growth differences between particle concentrations. Particle exposure had no significant impact on respiration or proportions of tissue and fatty acids in corals. The volume of additional cleaning mucus released by exposed corals was low and release did not significantly affect coral energy expenditure. Our results indicate that L. pertusa polyps can deal comparatively well with enhanced particle deposition rates and suspended matter concentrations. However, a small pilot experiment indicated that coral larvae might be particularly vulnerable to high particle concentrations.

Cold-water coral reefs and adjacent sponge grounds: hotspots of benthic respiration and organic carbon cycling in the deep sea

Cold-water coral reefs and adjacent sponge grounds are distributed widely in the deep ocean, where only a small fraction of the surface productivity reaches the seafloor as detritus. It remains elusive how these hotspots of biodiversity can thrive in such a food-limited environment, as data on energy flow and organic carbon utilization are critically lacking. Here we report in situ community respiration rates for cold-water coral and sponge ecosystems obtained by the non-invasive aquatic Eddy Correlation technique. Oxygen uptake rates over coral reefs and adjacent sponge grounds in the Traena Coral Field (Norway) were 9-20 times higher than those of the surrounding soft sediments. These high respiration rates indicate strong organic matter consumption, and hence suggest a local focusing onto these ecosystems of the downward flux of organic matter that is exported from the surface ocean. Overall, our results show that coral reefs and adjacent sponge grounds are hotspots of carbon processing in the food-limited deep ocean, and that these deep-sea ecosystems play a more prominent role in marine biogeochemical cycles than previously recognized.

Deep-sea nematodes actively colonise sediments, irrespective of the presence of a pulse of organic matter: Results from an in-situ experiment

A colonisation experiment was performed in situ at 2500 m water depth at the Arctic deep-sea long-term observatory HAUSGARTEN to determine the response of deep-sea nematodes to disturbed, newly available patches, enriched with organic matter. Cylindrical tubes,laterally covered with a 500 µm mesh, were filled with azoic deep-sea sediment and 13C-labelled food sources (diatoms and bacteria). After 10 days of incubation the tubes were analysed for nematode response in terms of colonisation and uptake. Nematodes actively colonised the tubes,however with densities that only accounted for a maximum of 2.13% (51 ind.10 cm−2) of the ambient nematode assemblages. Densities did not differ according to the presence or absence of organic matter, nor according to the type of organic matter added. The fact that the organic matter did not function as an attractant to nematodes was confirmed by the absence of notable 13C assimilation by the colonising nematodes. Overall, colonisationappears to be a process that yields reproducible abundance and diversity patterns, with certain taxa showing more efficiency. Together with the high variability between the colonising nematode assemblages, this lends experimental support to the existence of a spatio-temporal mosaic that emerges from highly localised, partially stochastic community dynamics.

Meiofauna metabolism in suboxic sediments: currently overestimated.

Oxygen is recognized as a structuring factor of metazoan communities in marine sediments. The importance of oxygen as a controlling factor on meiofauna (32 µm-1 mm in size) respiration rates is however less clear. Typically, respiration rates are measured under oxic conditions, after which these rates are used in food web studies to quantify the role of meiofauna in sediment carbon turnover. Sediment oxygen concentration ([O2]) is generally far from saturated, implying that (1) current estimates of the role of meiofauna in carbon cycling may be biased and (2) meiofaunal organisms need strategies to survive in oxygen-stressed environments. Two main survival strategies are often hypothesized: 1) frequent migration to oxic layers and 2) morphological adaptation. To evaluate these hypotheses, we (1) used a model of oxygen turnover in the meiofauna body as a function of ambient [O2], and (2) performed respiration measurements at a range of [O2] conditions. The oxygen turnover model predicts a tight coupling between ambient [O2] and meiofauna body [O2] with oxygen within the body being consumed in seconds. This fast turnover favors long and slender organisms in sediments with low ambient [O2] but even then frequent migration between suboxic and oxic layers is for most organisms not a viable strategy to alleviate oxygen limitation. Respiration rates of all measured meiofauna organisms slowed down in response to decreasing ambient [O2], with Nematoda displaying the highest metabolic sensitivity for declining [O2] followed by Foraminifera and juvenile Gastropoda. Ostracoda showed a behavioral stress response when ambient [O2] reached a critical level. Reduced respiration at low ambient [O2] implies that meiofauna in natural, i.e. suboxic, sediments must have a lower metabolism than inferred from earlier respiration rates conducted under oxic conditions. The implications of these findings are discussed for the contribution of meiofauna to carbon cycling in marine sediments.

The Symbiosis between Lophelia pertusa and Eunice norvegica Stimulates Coral Calcification and Worm Assimilation

We investigated the interactions between the cold-water coral Lophelia pertusa and its associated polychaete Eunice norvegica by quantifying carbon (C) and nitrogen (N) budgets of tissue assimilation, food partitioning, calcification and respiration using 13C and 15N enriched algae and zooplankton as food sources. During incubations both species were kept either together or in separate chambers to study the net outcome of their interaction on the above mentioned processes. The stable isotope approach also allowed us to follow metabolically derived tracer C further into the coral skeleton and therefore estimate the effect of the interaction on coral calcification. Results showed that food assimilation by the coral was not significantly elevated in presence of E. norvegica but food assimilation by the polychaete was up to 2 to 4 times higher in the presence of the coral. The corals kept assimilation constant by increasing the consumption of smaller algae particles less favored by the polychaete while the assimilation of Artemia was unaffected by the interaction. Total respiration of tracer C did not differ among incubations, although E. norvegica enhanced coral calcification up to 4 times. These results together with the reported high abundance of E. norvegica in cold-water coral reefs, indicate that the interactions between L. pertusa and E. norvegica can be of high importance for ecosystem functioning.

Differential recycling of coral and algal dissolved organic matter via the sponge loop

Corals and macroalgae release large quantities of dissolved organic matter (DOM), one of the largest sources of organic matter produced on coral reefs. By rapidly taking up DOM and transforming it into particulate detritus, coral reef sponges are proposed to play a key role in transferring the energy and nutrients in DOM to higher trophic levels via the recently discovered sponge loop. DOM released by corals and algae differs in quality and composition, but the influence of these different DOM sources on recycling by the sponge loop has not been investigated. Here, we used stable isotope pulse-chase experiments to compare the processing of naturally sourced coral- and algal-derived DOM by three Red Sea coral reef sponge species: Chondrilla sacciformis, Hemimycale arabica and Mycale fistulifera. Incubation experiments were conducted to trace 13C- and 15N-enriched coral- and algal-derived DOM into the sponge tissue and detritus. Incorporation of 13C into specific phospholipid-derived fatty acids (PLFAs) was used to differentiate DOM assimilation within the sponge holobiont (i.e. the sponge host vs. its associated bacteria). All sponges assimilated both coral- and algal-derived DOM, but incorporation rates were significantly higher for algal-derived DOM. The two DOM sources were also processed differently by the sponge holobiont. Algal-derived DOM was incorporated into bacteria-specific PLFAs at a higher rate while coral-derived DOM was more readily incorporated into sponge-specific PLFAs. A substantial fraction of the dissolved organic carbon (C) and nitrogen (N) assimilated by the sponges was subsequently converted into and released as particulate detritus (15–24% C and 27–49% N). However, algal-derived DOM was released as detritus at a higher rate. The higher uptake and transformation rates of algal- compared with coral-derived DOM suggest that reef community phase shifts from coral to algal dominance may stimulate DOM cycling through the sponge loop with potential consequences for coral reef biogeochemical cycles and food webs.

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.

Soil and Freshwater and Marine Sediment Food Webs: Their Structure and Function

The food webs of terrestrial soils and of freshwater and marine sediments depend on adjacent aboveground or pelagic ecosystems for organic matter input that provides nutrients and energy. There are important similarities in the flow of organic matter through these food webs and how this flow feeds back to primary production. In both soils and sediments, trophic interactions occur in a cycle in which consumers stimulate nutrient cycling such that mineralized resources are made available to the primary producers. However, aquatic sediments and terrestrial soils differ greatly in the connectivity between the production and the consumption of organic matter. Terrestrial soils and shallow aquatic sediments can receive organic matter within hours of photosynthesis when roots leak carbon, whereas deep oceanic sediments receive organic matter possibly months after carbon assimilation by phytoplankton. This comparison has implications for the capacity of soils and sediments to affect the global carbon balance.