Diatom-mediated food web functioning under ocean artificial upwelling.

Enhancing ocean productivity by artificial upwelling is evaluated as a nature-based solution for food security and climate change mitigation. Fish production is intended through diatom-based plankton food webs as these are assumed to be short and efficient. However, our findings from mesocosm experiments on artificial upwelling in the oligotrophic ocean disagree with this classical food web model. Here, diatoms did not reduce trophic length and instead impaired the transfer of primary production to crustacean grazers and small pelagic fish. The diatom-driven decrease in trophic efficiency was likely mediated by changes in nutritional value for the copepod grazers. Whilst diatoms benefitted the availability of essential fatty acids, they also caused unfavorable elemental compositions via high carbon-to-nitrogen ratios (i.e. low protein content) to which the grazers were unable to adapt. This nutritional imbalance for grazers was most pronounced in systems optimized for CO2 uptake through carbon-to-nitrogen ratios well beyond Redfield. A simultaneous enhancement of fisheries production and carbon sequestration via artificial upwelling may thus be difficult to achieve given their opposing stoichiometric constraints. Our study suggest that food quality can be more critical than quantity to maximize food web productivity during shorter-term fertilization of the oligotrophic ocean.

The appendicularian Oikopleura dioica can enhance carbon export in a high CO2 ocean.

Gelatinous zooplankton are increasingly recognized to play a key role in the ocean's biological carbon pump. Appendicularians, a class of pelagic tunicates, are among the most abundant gelatinous plankton in the ocean, but it is an open question how their contribution to carbon export might change in the future. Here, we conducted an experiment with large volume in situ mesocosms (~55-60 m3 and 21 m depth) to investigate how ocean acidification (OA) extreme events affect food web structure and carbon export in a natural plankton community, particularly focusing on the keystone species Oikopleura dioica, a globally abundant appendicularian. We found a profound influence of O. dioica on vertical carbon fluxes, particularly during a short but intense bloom period in the high CO2 treatment, during which carbon export was 42%-64% higher than under ambient conditions. This elevated flux was mostly driven by an almost twofold increase in O. dioica biomass under high CO2 . This rapid population increase was linked to enhanced fecundity (+20%) that likely resulted from physiological benefits of low pH conditions. The resulting competitive advantage of O. dioica resulted in enhanced grazing on phytoplankton and transfer of this consumed biomass into sinking particles. Using a simple carbon flux model for O. dioica, we estimate that high CO2 doubled the carbon flux of discarded mucous houses and fecal pellets, accounting for up to 39% of total carbon export from the ecosystem during the bloom. Considering the wide geographic distribution of O. dioica, our findings suggest that appendicularians may become an increasingly important vector of carbon export with ongoing OA.

Enhanced silica export in a future ocean triggers global diatom decline.

Diatoms account for up to 40% of marine primary production1,2 and require silicic acid to grow and build their opal shell3. On the physiological and ecological level, diatoms are thought to be resistant to, or even benefit from, ocean acidification4-6. Yet, global-scale responses and implications for biogeochemical cycles in the future ocean remain largely unknown. Here we conducted five in situ mesocosm experiments with natural plankton communities in different biomes and find that ocean acidification increases the elemental ratio of silicon (Si) to nitrogen (N) of sinking biogenic matter by 17 ± 6 per cent under [Formula: see text] conditions projected for the year 2100. This shift in Si:N seems to be caused by slower chemical dissolution of silica at decreasing seawater pH. We test this finding with global sediment trap data, which confirm a widespread influence of pH on Si:N in the oceanic water column. Earth system model simulations show that a future pH-driven decrease in silica dissolution of sinking material reduces the availability of silicic acid in the surface ocean, triggering a global decline of diatoms by 13-26 per cent due to ocean acidification by the year 2200. This outcome contrasts sharply with the conclusions of previous experimental studies, thereby illustrating how our current understanding of biological impacts of ocean change can be considerably altered at the global scale through unexpected feedback mechanisms in the Earth system.

Ocean acidification induces distinct metabolic responses in subtropical zooplankton under oligotrophic conditions and after simulated upwelling.

Ocean acidification (OA) is one of the most critical anthropogenic threats to marine ecosystems. While significant ecological responses of plankton communities to OA have been revealed mainly by small-scale laboratory approaches, the interactive effect of OA-related changes on zooplankton metabolism and their biogeochemical implications in the natural environment still remains less well understood. Here, we explore the responses of zooplankton respiration and ammonium excretion, two key processes in the nutrient cycling, to high pCO2 levels in a 9-week in situ mesocosm experiment conducted during the autumn oligotrophic season in the subtropical northeast Atlantic. By simulating an upwelling event halfway through the study, we further evaluated the combined effects of OA and nutrient availability on the physiology of micro-and mesozooplankton. OA conditions generally resulted in a reduction in the biomass-specific metabolic and enzymatic rates, particularly in the mesozooplankton community. The situation reversed after the nutrient-rich deep-water addition, which initially promoted a diatom bloom and increased heterotrophic activities in all mesocosms. Under high pCO2 conditions (>800 µatm), however, the nutrient fertilization triggered the proliferation of the harmful alga Vicicitus globosus, with important consequences for the metabolic performance of the two zooplankton size classes. Here, the zooplankton contribution to the remineralization of organic matter and nitrogen regeneration dropped by 30% and 24%, respectively, during the oligotrophic period, and by 40% and 70% during simulated upwelling. Overall, our results indicate a potential reduction in the biogeochemical role of zooplankton under future ocean conditions, with more evident effects on the large mesozooplankton and during high productivity events.

Enhanced transfer of organic matter to higher trophic levels caused by ocean acidification and its implications for export production: A mass balance approach.

Ongoing acidification of the ocean through uptake of anthropogenic CO2 is known to affect marine biota and ecosystems with largely unknown consequences for marine food webs. Changes in food web structure have the potential to alter trophic transfer, partitioning, and biogeochemical cycling of elements in the ocean. Here we investigated the impact of realistic end-of-the-century CO2 concentrations on the development and partitioning of the carbon, nitrogen, phosphorus, and silica pools in a coastal pelagic ecosystem (Gullmar Fjord, Sweden). We covered the entire winter-to-summer plankton succession (100 days) in two sets of five pelagic mesocosms, with one set being CO2 enriched (~760 µatm pCO2) and the other one left at ambient CO2 concentrations. Elemental mass balances were calculated and we highlight important challenges and uncertainties we have faced in the closed mesocosm system. Our key observations under high CO2 were: (1) A significantly amplified transfer of carbon, nitrogen, and phosphorus from primary producers to higher trophic levels, during times of regenerated primary production. (2) A prolonged retention of all three elements in the pelagic food web that significantly reduced nitrogen and phosphorus sedimentation by about 11 and 9%, respectively. (3) A positive trend in carbon fixation (relative to nitrogen) that appeared in the particulate matter pool as well as the downward particle flux. This excess carbon counteracted a potential reduction in carbon sedimentation that could have been expected from patterns of nitrogen and phosphorus fluxes. Our findings highlight the potential for ocean acidification to alter partitioning and cycling of carbon and nutrients in the surface ocean but also show that impacts are temporarily variable and likely depending upon the structure of the plankton food web.

Food web changes under ocean acidification promote herring larvae survival.

Ocean acidification-the decrease in seawater pH due to rising CO2 concentrations-has been shown to lower survival in early life stages of fish and, as a consequence, the recruitment of populations including commercially important species. To date, ocean-acidification studies with fish larvae have focused on the direct physiological impacts of elevated CO2, but largely ignored the potential effects of ocean acidification on food web interactions. In an in situ mesocosm study on Atlantic herring (Clupea harengus) larvae as top predators in a pelagic food web, we account for indirect CO2 effects on larval survival mediated by changes in food availability. The community was exposed to projected end-of-the-century CO2 conditions (~760 µatm pCO2) over a period of 113 days. In contrast with laboratory studies that reported a decrease in fish survival, the survival of the herring larvae in situ was significantly enhanced by 19 ± 2%. Analysis of the plankton community dynamics suggested that the herring larvae benefitted from a CO2-stimulated increase in primary production. Such indirect effects may counteract the possible direct negative effects of ocean acidification on the survival of fish early life stages. These findings emphasize the need to assess the food web effects of ocean acidification on fish larvae before we can predict even the sign of change in fish recruitment in a high-CO2 ocean.

Ocean acidification effects on mesozooplankton community development: Results from a long-term mesocosm experiment.

Ocean acidification may affect zooplankton directly by decreasing in pH, as well as indirectly via trophic pathways, where changes in carbon availability or pH effects on primary producers may cascade up the food web thereby altering ecosystem functioning and community composition. Here, we present results from a mesocosm experiment carried out during 113 days in the Gullmar Fjord, Skagerrak coast of Sweden, studying plankton responses to predicted end-of-century pCO2 levels. We did not observe any pCO2 effect on the diversity of the mesozooplankton community, but a positive pCO2 effect on the total mesozooplankton abundance. Furthermore, we observed species-specific sensitivities to pCO2 in the two major groups in this experiment, copepods and hydromedusae. Also stage-specific pCO2 sensitivities were detected in copepods, with copepodites being the most responsive stage. Focusing on the most abundant species, Pseudocalanus acuspes, we observed that copepodites were significantly more abundant in the high-pCO2 treatment during most of the experiment, probably fuelled by phytoplankton community responses to high-pCO2 conditions. Physiological and reproductive output was analysed on P. acuspes females through two additional laboratory experiments, showing no pCO2 effect on females' condition nor on egg hatching. Overall, our results suggest that the Gullmar Fjord mesozooplankton community structure is not expected to change much under realistic end-of-century OA scenarios as used here. However, the positive pCO2 effect detected on mesozooplankton abundance could potentially affect biomass transfer to higher trophic levels in the future.

Influence of ocean acidification on plankton community structure during a winter-to-summer succession: An imaging approach indicates that copepods can benefit from elevated CO2 via indirect food web effects.

Plankton communities play a key role in the marine food web and are expected to be highly sensitive to ongoing environmental change. Oceanic uptake of anthropogenic carbon dioxide (CO2) causes pronounced shifts in marine carbonate chemistry and a decrease in seawater pH. These changes-summarized by the term ocean acidification (OA)-can significantly affect the physiology of planktonic organisms. However, studies on the response of entire plankton communities to OA, which also include indirect effects via food-web interactions, are still relatively rare. Thus, it is presently unclear how OA could affect the functioning of entire ecosystems and biogeochemical element cycles. In this study, we report from a long-term in situ mesocosm experiment, where we investigated the response of natural plankton communities in temperate waters (Gullmarfjord, Sweden) to elevated CO2 concentrations and OA as expected for the end of the century (~760 µatm pCO2). Based on a plankton-imaging approach, we examined size structure, community composition and food web characteristics of the whole plankton assemblage, ranging from picoplankton to mesozooplankton, during an entire winter-to-summer succession. The plankton imaging system revealed pronounced temporal changes in the size structure of the copepod community over the course of the plankton bloom. The observed shift towards smaller individuals resulted in an overall decrease of copepod biomass by 25%, despite increasing numerical abundances. Furthermore, we observed distinct effects of elevated CO2 on biomass and size structure of the entire plankton community. Notably, the biomass of copepods, dominated by Pseudocalanus acuspes, displayed a tendency towards elevated biomass by up to 30-40% under simulated ocean acidification. This effect was significant for certain copepod size classes and was most likely driven by CO2-stimulated responses of primary producers and a complex interplay of trophic interactions that allowed this CO2 effect to propagate up the food web. Such OA-induced shifts in plankton community structure could have far-reaching consequences for food-web interactions, biomass transfer to higher trophic levels and biogeochemical cycling of marine ecosystems.

Influence of Ocean Acidification on a Natural Winter-to-Summer Plankton Succession: First Insights from a Long-Term Mesocosm Study Draw Attention to Periods of Low Nutrient Concentrations.

Every year, the oceans absorb about 30% of anthropogenic carbon dioxide (CO2) leading to a re-equilibration of the marine carbonate system and decreasing seawater pH. Today, there is increasing awareness that these changes-summarized by the term ocean acidification (OA)-could differentially affect the competitive ability of marine organisms, thereby provoking a restructuring of marine ecosystems and biogeochemical element cycles. In winter 2013, we deployed ten pelagic mesocosms in the Gullmar Fjord at the Swedish west coast in order to study the effect of OA on plankton ecology and biogeochemistry under close to natural conditions. Five of the ten mesocosms were left unperturbed and served as controls (~380 µatm pCO2), whereas the others were enriched with CO2-saturated water to simulate realistic end-of-the-century carbonate chemistry conditions (~760 µatm pCO2). We ran the experiment for 113 days which allowed us to study the influence of high CO2 on an entire winter-to-summer plankton succession and to investigate the potential of some plankton organisms for evolutionary adaptation to OA in their natural environment. This paper is the first in a PLOS collection and provides a detailed overview on the experimental design, important events, and the key complexities of such a "long-term mesocosm" approach. Furthermore, we analyzed whether simulated end-of-the-century carbonate chemistry conditions could lead to a significant restructuring of the plankton community in the course of the succession. At the level of detail analyzed in this overview paper we found that CO2-induced differences in plankton community composition were non-detectable during most of the succession except for a period where a phytoplankton bloom was fueled by remineralized nutrients. These results indicate: (1) Long-term studies with pelagic ecosystems are necessary to uncover OA-sensitive stages of succession. (2) Plankton communities fueled by regenerated nutrients may be more responsive to changing carbonate chemistry than those having access to high inorganic nutrient concentrations and may deserve particular attention in future studies.