Biological carbon pump estimate based on multidecadal hydrographic data.

The transfer of photosynthetically produced organic carbon from surface to mesopelagic waters draws carbon dioxide from the atmosphere1. However, current observation-based estimates disagree on the strength of this biological carbon pump (BCP)2. Earth system models (ESMs) also exhibit a large spread of BCP estimates, indicating limited representations of the known carbon export pathways3. Here we use several decades of hydrographic observations to produce a top-down estimate of the strength of the BCP with an inverse biogeochemical model that implicitly accounts for all known export pathways. Our estimate of total organic carbon (TOC) export at 73.4 m (model euphotic zone depth) is 15.00 ± 1.12 Pg C year-1, with only two-thirds reaching 100 m depth owing to rapid remineralization of organic matter in the upper water column. Partitioned by sequestration time below the euphotic zone, τ, the globally integrated organic carbon production rate with τ > 3 months is 11.09 ± 1.02 Pg C year-1, dropping to 8.25 ± 0.30 Pg C year-1 for τ > 1 year, with 81% contributed by the non-advective-diffusive vertical flux owing to sinking particles and vertically migrating zooplankton. Nevertheless, export of organic carbon by mixing and other fluid transport of dissolved matter and suspended particles remains regionally important for meeting the respiratory carbon demand. Furthermore, the temperature dependence of the sequestration efficiency inferred from our inversion suggests that future global warming may intensify the recycling of organic matter in the upper ocean, potentially weakening the BCP.

Convergent estimates of marine nitrogen fixation.

Uncertainty in the global patterns of marine nitrogen fixation limits our understanding of the response of the ocean's nitrogen and carbon cycles to environmental change. The geographical distribution of and ecological controls on nitrogen fixation are difficult to constrain with limited in situ measurements. Here we present convergent estimates of nitrogen fixation from an inverse biogeochemical and a prognostic ocean model. Our results demonstrate strong spatial variability in the nitrogen-to-phosphorus ratio of exported organic matter that greatly increases the global nitrogen-fixation rate (because phytoplankton manage with less phosphorus when it is in short supply). We find that the input of newly fixed nitrogen from microbial fixation and external inputs (atmospheric deposition and river fluxes) accounts for up to 50 per cent of carbon export in subtropical gyres. We also find that nitrogen fixation and denitrification are spatially decoupled but that nevertheless nitrogen sources and sinks appear to be balanced over the past few decades. Moreover, we propose a role for top-down zooplankton grazing control in shaping the global patterns of nitrogen fixation. Our findings suggest that biological carbon export in the ocean is higher than expected and that stabilizing nitrogen-cycle feedbacks are weaker than previously thought.

Sustained stoichiometric imbalance and its ecological consequences in a large oligotrophic lake.

Considerable attention is given to absolute nutrient levels in lakes, rivers, and oceans, but less is paid to their relative concentrations, their nitrogen:phosphorus (N:P) stoichiometry, and the consequences of imbalanced stoichiometry. Here, we report 38 y of nutrient dynamics in Flathead Lake, a large oligotrophic lake in Montana, and its inflows. While nutrient levels were low, the lake had sustained high total N: total P ratios (TN:TP: 60 to 90:1 molar) throughout the observation period. N and P loading to the lake as well as loading N:P ratios varied considerably among years but showed no systematic long-term trend. Surprisingly, TN:TP ratios in river inflows were consistently lower than in the lake, suggesting that forms of P in riverine loading are removed preferentially to N. In-lake processes, such as differential sedimentation of P relative to N or accumulation of fixed N in excess of denitrification, likely also operate to maintain the lake's high TN:TP ratios. Regardless of causes, the lake's stoichiometric imbalance is manifested in P limitation of phytoplankton growth during early and midsummer, resulting in high C:P and N:P ratios in suspended particulate matter that propagate P limitation to zooplankton. Finally, the lake's imbalanced N:P stoichiometry appears to raise the potential for aerobic methane production via metabolism of phosphonate compounds by P-limited microbes. These data highlight the importance of not only absolute N and P levels in aquatic ecosystems, but also their stoichiometric balance, and they call attention to potential management implications of high N:P ratios.

A two-timescale model of plankton-oxygen dynamics predicts formation of oxygen minimum zones and global anoxia.

Decline of the dissolved oxygen in the ocean is a growing concern, as it may eventually lead to global anoxia, an elevated mortality of marine fauna and even a mass extinction. Deoxygenation of the ocean often results in the formation of oxygen minimum zones (OMZ): large domains where the abundance of oxygen is much lower than that in the surrounding ocean environment. Factors and processes resulting in the OMZ formation remain controversial. We consider a conceptual model of coupled plankton-oxygen dynamics that, apart from the plankton growth and the oxygen production by phytoplankton, also accounts for the difference in the timescales for phyto- and zooplankton (making it a "slow-fast system") and for the implicit effect of upper trophic levels resulting in density dependent (nonlinear) zooplankton mortality. The model is investigated using a combination of analytical techniques and numerical simulations. The slow-fast system is decomposed into its slow and fast subsystems. The critical manifold of the slow-fast system and its stability is then studied by analyzing the bifurcation structure of the fast subsystem. We obtain the canard cycles of the slow-fast system for a range of parameter values. However, the system does not allow for persistent relaxation oscillations; instead, the blowup of the canard cycle results in plankton extinction and oxygen depletion. For the spatially explicit model, the earlier works in this direction did not take into account the density dependent mortality rate of the zooplankton, and thus could exhibit Turing pattern. However, the inclusion of the density dependent mortality into the system can lead to stationary Turing patterns. The dynamics of the system is then studied near the Turing bifurcation threshold. We further consider the effect of the self-movement of the zooplankton along with the turbulent mixing. We show that an initial non-uniform perturbation can lead to the formation of an OMZ, which then grows in size and spreads over space. For a sufficiently large timescale separation, the spread of the OMZ can result in global anoxia.

In situ imaging reveals the biomass of giant protists in the global ocean.

Planktonic organisms play crucial roles in oceanic food webs and global biogeochemical cycles. Most of our knowledge about the ecological impact of large zooplankton stems from research on abundant and robust crustaceans, and in particular copepods. A number of the other organisms that comprise planktonic communities are fragile, and therefore hard to sample and quantify, meaning that their abundances and effects on oceanic ecosystems are poorly understood. Here, using data from a worldwide in situ imaging survey of plankton larger than 600 µm, we show that a substantial part of the biomass of this size fraction consists of giant protists belonging to the Rhizaria, a super-group of mostly fragile unicellular marine organisms that includes the taxa Phaeodaria and Radiolaria (for example, orders Collodaria and Acantharia). Globally, we estimate that rhizarians in the top 200 m of world oceans represent a standing stock of 0.089 Pg carbon, equivalent to 5.2% of the total oceanic biota carbon reservoir. In the vast oligotrophic intertropical open oceans, rhizarian biomass is estimated to be equivalent to that of all other mesozooplankton (plankton in the size range 0.2-20 mm). The photosymbiotic association of many rhizarians with microalgae may be an important factor in explaining their distribution. The previously overlooked importance of these giant protists across the widest ecosystem on the planet changes our understanding of marine planktonic ecosystems.

Adding Zooplankton to the OSMAC Toolkit: Effect of Grazing Stress on the Metabolic Profile and Bioactivity of a Diatom.

"One strain many compounds" (OSMAC) based approaches have been widely used in the search for bioactive compounds. Introducing stress factors like nutrient limitation, UV-light or cocultivation with competing organisms has successfully been used in prokaryote cultivation. It is known that diatom physiology is affected by changed cultivation conditions such as temperature, nutrient concentration and light conditions. Cocultivation, though, is less explored. Hence, we wanted to investigate whether grazing pressure can affect the metabolome of the marine diatom Porosira glacialis, and if the stress reaction could be detected as changes in bioactivity. P. glacialis cultures were mass cultivated in large volume bioreactor (6000 L), first as a monoculture and then as a coculture with live zooplankton. Extracts of the diatom biomass were screened in a selection of bioactivity assays: inhibition of biofilm formation, antibacterial and cell viability assay on human cells. Bioactivity was found in all bioassays performed. The viability assay towards normal lung fibroblasts revealed that P. glacialis had higher bioactivity when cocultivated with zooplankton than in monoculture. Cocultivation with diatoms had no noticeable effect on the activity against biofilm formation or bacterial growth. The metabolic profiles were analyzed showing the differences in diatom metabolomes between the two culture conditions. The experiment demonstrates that grazing stress affects the biochemistry of P. glacialis and thus represents a potential tool in the OSMAC toolkit.

Reconciliation of the carbon budget in the ocean's twilight zone.

Photosynthesis in the surface ocean produces approximately 100 gigatonnes of organic carbon per year, of which 5 to 15 per cent is exported to the deep ocean. The rate at which the sinking carbon is converted into carbon dioxide by heterotrophic organisms at depth is important in controlling oceanic carbon storage. It remains uncertain, however, to what extent surface ocean carbon supply meets the demand of water-column biota; the discrepancy between known carbon sources and sinks is as much as two orders of magnitude. Here we present field measurements, respiration rate estimates and a steady-state model that allow us to balance carbon sources and sinks to within observational uncertainties at the Porcupine Abyssal Plain site in the eastern North Atlantic Ocean. We find that prokaryotes are responsible for 70 to 92 per cent of the estimated remineralization in the twilight zone (depths of 50 to 1,000 metres) despite the fact that much of the organic carbon is exported in the form of large, fast-sinking particles accessible to larger zooplankton. We suggest that this occurs because zooplankton fragment and ingest half of the fast-sinking particles, of which more than 30 per cent may be released as suspended and slowly sinking matter, stimulating the deep-ocean microbial loop. The synergy between microbes and zooplankton in the twilight zone is important to our understanding of the processes controlling the oceanic carbon sink.

Mycosporine-Like Amino Acids (MAAs) in Zooplankton.

Organisms have different adaptations to avoid damage from ultraviolet radiation and one such adaptation is the accumulation of mycosporine-like amino acids (MAAs). These compounds are common in aquatic taxa but a comprehensive review is lacking on their distribution and function in zooplankton. This paper shows that zooplankton MAA concentrations range from non-detectable to ~13 µg mgDW-1. Copepods, rotifers, and krill display a large range of concentrations, whereas cladocerans generally do not contain MAAs. The proposed mechanisms to gain MAAs are via ingestion of MAA-rich food or via symbiotic bacteria providing zooplankton with MAAs. Exposure to UV-radiation increases the concentrations in zooplankton both via increasing MAA concentrations in the phytoplankton food and due to active accumulation. Concentrations are generally low during winter and higher in summer and females seem to deposit MAAs in their eggs. The concentrations of MAAs in zooplankton tend to increase with altitude but only up to a certain altitude suggesting some limitation for the uptake. Shallow and UV-transparent systems tend to have copepods with higher concentrations of MAAs but this has only been shown in a few species. A high MAA concentration has also been shown to lead to lower UV-induced mortality and an overall increased fitness. While there is a lot of information on MAAs in zooplankton we still lack understanding of the potential costs and constraints for accumulation. There is also scarce information in some taxa such as rotifers as well as from systems in tropical, sub(polar) areas as well as in marine systems in general.

Effects of zooplankton carcasses degradation on freshwater bacterial community composition and implications for carbon cycling.

Non-predatory mortality of zooplankton provides an abundant, yet, little studied source of high quality labile organic matter (LOM) in aquatic ecosystems. Using laboratory microcosms, we followed the decomposition of organic carbon of fresh 13 C-labelled Daphnia carcasses by natural bacterioplankton. The experimental setup comprised blank microcosms, that is, artificial lake water without any organic matter additions (B), and microcosms either amended with natural humic matter (H), fresh Daphnia carcasses (D) or both, that is, humic matter and Daphnia carcasses (HD). Most of the carcass carbon was consumed and respired by the bacterial community within 15 days of incubation. A shift in the bacterial community composition shaped by labile carcass carbon and by humic matter was observed. Nevertheless, we did not observe a quantitative change in humic matter degradation by heterotrophic bacteria in the presence of LOM derived from carcasses. However, carcasses were the main factor driving the bacterial community composition suggesting that the presence of large quantities of dead zooplankton might affect the carbon cycling in aquatic ecosystems. Our results imply that organic matter derived from zooplankton carcasses is efficiently remineralized by a highly specific bacterial community, but does not interfere with the bacterial turnover of more refractory humic matter.

Disentangling the mechanisms behind climate effects on zooplankton.

Understanding how climate influences ecosystems is complicated by the many correlated and interrelated impacting factors. Here we quantify climate effects on Calanus finmarchicus in the northeastern Norwegian Sea and southwestern Barents Sea. By combining oceanographic drift models and statistical analyses of field data from 1959 to 1993 and investigating effects across trophic levels, we are able to elucidate pathways by which climate influences zooplankton. The results show that both chlorophyll biomass in spring and C. finmarchicus biomass in summer relate positively to a combination of shallow mixed layer depth and increased wind in spring, suggesting that C. finmarchicus biomass in summer is influenced by bottom-up effects of food availability. Furthermore, spatially resolved C. finmarchicus biomass in summer is linked to favorable transport from warmer, core areas to the south. However, increased mean temperature in spring does not lead to increased C. finmarchicus biomass in summer. Rather, spring biomass is generally higher, but population growth from spring to summer is lower, after a warm compared with a cold spring. Our study illustrates how improved understanding of climate effects can be obtained when different datasets and different methods are combined in a unified approach.

Eco-Evolutionary Dynamics of Ecological Stoichiometry in Plankton Communities.

Nitrogen (N) and phosphorus (P) limit primary production in many aquatic ecosystems, with major implications for ecological interactions in plankton communities. Yet it remains unclear how evolution may affect the N∶P stoichiometry of phytoplankton-zooplankton interactions. Here, we address this issue by analyzing an eco-evolutionary model of phytoplankton-zooplankton interactions with explicit nitrogen and phosphorus dynamics. In our model, investment of phytoplankton in nitrogen versus phosphorus uptake is an evolving trait, and zooplankton display selectivity for phytoplankton with N∶P ratios matching their nutritional requirements. We use this model to explore implications of the contrasting N∶P requirements of copepods versus cladocerans. The model predicts that selective zooplankton strongly affect the N∶P ratio of phytoplankton, resulting in deviations from their optimum N∶P ratio. Specifically, selective grazing by nitrogen-demanding copepods favors dominance of phytoplankton with low N∶P ratios, whereas phosphorus-demanding cladocerans favor dominance of phytoplankton with high N∶P ratios. Interestingly, selective grazing by nutritionally balanced zooplankton leads to the occurrence of alternative stable states, where phytoplankton may evolve either low, optimum, or high N∶P ratios, depending on the initial conditions. These results offer a new perspective on commonly observed differences in N∶P stoichiometry between plankton of freshwater and those of marine ecosystems and indicate that selective grazing by zooplankton can have a major impact on the stoichiometric composition of phytoplankton.

Dependency of Antarctic zooplankton species on ice algae-produced carbon suggests a sea ice-driven pelagic ecosystem during winter.

How the abundant pelagic life of the Southern Ocean survives winter darkness, when the sea is covered by pack ice and phytoplankton production is nearly zero, is poorly understood. Ice-associated ("sympagic") microalgae could serve as a high-quality carbon source during winter, but their significance in the food web is so far unquantified. To better understand the importance of ice algae-produced carbon for the overwintering of Antarctic organisms, we investigated fatty acid (FA) and stable isotope compositions of 10 zooplankton species, and their potential sympagic and pelagic carbon sources. FA-specific carbon stable isotope compositions were used in stable isotope mixing models to quantify the contribution of ice algae-produced carbon (αIce ) to the body carbon of each species. Mean αIce estimates ranged from 4% to 67%, with large variations between species and depending on the FA used for the modelling. Integrating the αIce estimates from all models, the sympagic amphipod Eusirus laticarpus was the most dependent on ice algal carbon (αIce : 54%-67%), and the salp Salpa thompsoni showed the least dependency on ice algal carbon (αIce : 8%-40%). Differences in αIce estimates between FAs associated with short-term vs. long-term lipid pools suggested an increasing importance of ice algal carbon for many species as the winter season progressed. In the abundant winter-active copepod Calanus propinquus, mean αIce reached more than 50% in late winter. The trophic carbon flux from ice algae into this copepod was between 3 and 5 mg C m-2  day-1 . This indicates that copepods and other ice-dependent zooplankton species transfer significant amounts of carbon from ice algae into the pelagic system, where it fuels the food web, the biological carbon pump and elemental cycling. Understanding the role of ice algae-produced carbon in these processes will be the key to predictions of the impact of future sea ice decline on Antarctic ecosystem functioning.

Quantification of sulphur amino acids by ultra-high performance liquid chromatography in aquatic invertebrates.

We examined the performance of an ultra-high performance liquid chromatography method to quantify protein-bound sulphur amino acids in zooplankton. Both cysteic acid and methionine sulfone were linear from 5 to 250 pmol (r2 = 0.99), with a method detection limit of 13 pmol and 9 pmol, respectively. Although there was no matrix effect on linearity, adjacent peaks and co-eluting noise from the invertebrate proteins increased the detection limits when compared to common standards. Overall, performance characteristics were reproducible and accurate, and provide a means for quantifying sulphur amino acids in aquatic invertebrates, an understudied group.

Nano-sized polystyrene affects feeding, behavior and physiology of brine shrimp Artemia franciscana larvae.

Nano-sized polymers as polystyrene (PS) constitute one of the main challenges for marine ecosystems, since they can distribute along the whole water column affecting planktonic species and consequently disrupting the energy flow of marine ecosystems. Nowadays very little knowledge is available on the impact of nano-sized plastics on marine organisms. Therefore, the present study aims to evaluate the effects of 40nm anionic carboxylated (PS-COOH) and 50nm cationic amino (PS-NH2) polystyrene nanoparticles (PS NPs) on brine shrimp Artemia franciscana larvae. No signs of mortality were observed at 48h of exposure for both PS NPs at naplius stage but several sub-lethal effects were evident. PS-COOH (5-100µg/ml) resulted massively sequestered inside the gut lumen of larvae (48h) probably limiting food intake. Some of them were lately excreted as fecal pellets but not a full release was observed. Likewise, PS-NH2 (5-100µg/ml) accumulated in larvae (48h) but also adsorbed at the surface of sensorial antennules and appendages probably hampering larvae motility. In addition, larvae exposed to PS-NH2 undergo multiple molting events during 48h of exposure compared to controls. The activation of a defense mechanism based on a physiological process able to release toxic cationic NPs (PS-NH2) from the body can be hypothesized. The general observed accumulation of PS NPs within the gut during the 48h of exposure indicates a continuous bioavailability of nano-sized PS for planktonic species as well as a potential transfer along the trophic web. Therefore, nano-sized PS might be able to impair food uptake (feeding), behavior (motility) and physiology (multiple molting) of brine shrimp larvae with consequences not only at organism and population level but on the overall ecosystem based on the key role of zooplankton on marine food webs.

Carbon sequestration capacity of sediments, algae, and zooplankton from fresh water aquaculture ponds.

The contribution of aquaculture and allied activities to the emission of green house gases and consequently to global warming is an emerging concern among environmentalists in the recent past. However, there exists ample scope for aquaculture activities to sequester carbon and thus compensate for the carbon emissions linked to aquaculture. This article attempts to elucidate the carbon sequestration capacity of sediments, algae, and zooplankton from fresh water aquaculture ponds. The percent organic carbon in the pond sediments ranged from 0.39 to 1.31 with an average value of 0.912 ± 0.321 whereas the carbon sequestration capacity ranged from 0.442 to 1.882 MgC/ha (1 Mg = 10(6) g) with an average value of 1.018 ± 0.447 MgC/ha. In the case of zooplankton and algae from pond, the percent organic carbon was 7.688 ± 0.196 and 2.354 ± 0.047, respectively, whereas the total estimated carbon burial rate was 0.009 ± 0.005 and 0.150 ± 0.003 MgC/ha, respectively. These findings are discussed with the previous reports available at present and are found to be in comparable ranges.

Spatio-temporal study of carbon sequestration through piscicultural practice at East Kolkata Wetland.

The present study focus the variation of carbon concentrations within three trophic level i.e., primary producer (phytoplankton), primary consumers (zooplankton) and secondary consumers (fish) in three selected ponds at East Kolkata Wetland area. Depending on the amount and frequency of wastewater input, physico-chemical characteristics of pond, species richness, predator-prey interactions and pond wise different piscicultural practices, the amount of carbon sequestration varied spatially. Significant temporal variations were also observed in each trophic level of these three selected East Kolkata Wetland pond ecosystems. On average primary producers were sequestered 2038.6 ± 244.8mg C m-3 d-1 whereas 307 ± 19.3 mg C m-3 and 11531.4 ± 318.2mg C m-3 was sequestered by primary and secondary consumers, respectively. In Kolkata and its nearby districts over 90% of the production was marked from the East Kolkata Wetland area. Consequently, a significant amount of sequestered carbon was exported from the East Kolkata Wetland ecosystem in the form of fish and this continuous system might increase the carbon sequestration efficiency of the aquatic ecosystem.

Zooplankton community changes confound the biodilution theory of methylmercury accumulation in a recovering mercury-contaminated lake.

In this study, the biodilution hypothesis of methylmercury (MeHg) accumulation was examined in a Hg-contaminated ecosystem that has undergone concurrent changes in nutrient loading and zooplankton community composition. Using a long-term record of 17 years (between 1980 and 2009), we demonstrate that zooplankton MeHg concentrations in Onondaga Lake, NY, are strongly driven by changes in the zooplankton community and body size. MeHg concentrations in zooplankton increased with an increase in body size and biomass. The highest concentrations of MeHg were observed under eutrophic and hypereutrophic conditions when large-bodied Daphnia species, Daphnia pulicaria and Daphnia galeata mendotae, were present. Bioconcentration rather than biodilution was governing the accumulation of MeHg in zooplankton without apparent growth dilution or zooplankton biomass dilution. Algal-bloom dilution controlled the variability in the MeHg concentration only under hypereutrophic conditions when Ceriodaphnia predominated the cladoceran population. Our study demonstrates that changes in zooplankton community composition confound the biodilution theory in Onondaga Lake and that the presence of large-bodied zooplankton species drives elevated MeHg concentrations.

Simulation of Observed PCBs and Pesticides in the Water Column during the North Atlantic Bloom Experiment.

The dynamics of persistent organic pollutants in the oceans are not well constrained, in particular during a bloom formation and collapse. Polychlorinated biphenyls (PCBs) and some pesticides were measured in air, water, and zooplankton tracking the North Atlantic Bloom in May 2008. Lower weight PCBs were entering the water column from the atmosphere during the main bloom period but reached equilibrium after the bloom collapsed. The PCBs in the lipids of zooplankton Calanus were in equilibrium with those in the dissolved phase. A Lagrangian box model was developed to simulate the dissolved phase PCBs and pesticides by including the following processes: air-water exchange, reversible sorption to POC, changes in mixed layer depth, removal by sinking particles, and degradation. Results suggest that sorption to (sinking) POC was the dominant removal process for hydrophobic pollutants from seawater. Statistical test suggested simulated results were not significantly different from observed values for hydrophobic pollutants (p,p'-DDE).

Combined Effects from γ Radiation and Fluoranthene Exposure on Carbon Transfer from Phytoplankton to Zooplankton.

Risk assessment does not usually take into account mixtures of contaminants, thus potentially under- or overestimating environmental effects. We investigated how the transfer of carbon between a primary producer, Pseudokirchneriella subcapitata, and a consumer, Daphnia magna, is affected by acute exposure of γ radiation (GR) in combination with the polycyclic aromatic hydrocarbon fluoranthene (FA). We exposed D. magna to five concentrations of FA and five acute doses of GR as single contaminants and in nine binary combinations. We compared the observed data for three end points (incorporation of carbon by D. magna, D. magna ingestion rates, and growth) to the predicted joint effects of the mixed stressors based on the independent action (IA) concept. There were deviations from the IA predictions, especially for ingestion rates and carbon incorporation by D. magna, where antagonistic effects were observed at the lower doses, while synergism was seen at the highest doses. Our results highlight the importance of investigating the effects of exposure to GR in a multistressor context. In mixtures of GR and FA, the IA-predicted effects seem to be conservative as antagonism between the two stressors was the dominant pattern, possibly due to stimulation of cellular antioxidative stress mechanisms.