Implications of elevated CO2 on pelagic carbon fluxes in an Arctic mesocosm study – an elemental mass balance approach (update)

Recent studies on the impacts of ocean acidification on pelagic communities have identified changes in carbon to nutrient dynamics with related shifts in elemental stoichiometry. In principle, mesocosm experiments provide the opportunity of determining temporal dynamics of all relevant carbon and nutrient pools and, thus, calculating elemental budgets. In practice, attempts to budget mesocosm enclosures are often hampered by uncertainties in some of the measured pools and fluxes, in particular due to uncertainties in constraining air–sea gas exchange, particle sinking, and wall growth. In an Arctic mesocosm study on ocean acidification applying KOSMOS (Kiel Off-Shore Mesocosms for future Ocean Simulation), all relevant element pools and fluxes of carbon, nitrogen and phosphorus were measured, using an improved experimental design intended to narrow down the mentioned uncertainties. Water-column concentrations of particulate and dissolved organic and inorganic matter were determined daily. New approaches for quantitative estimates of material sinking to the bottom of the mesocosms and gas exchange in 48 h temporal resolution as well as estimates of wall growth were developed to close the gaps in element budgets. However, losses elements from the budgets into a sum of insufficiently determined pools were detected, and are principally unavoidable in mesocosm investigation. The comparison of variability patterns of all single measured datasets revealed analytic precision to be the main issue in determination of budgets. Uncertainties in dissolved organic carbon (DOC), nitrogen (DON) and particulate organic phosphorus (POP) were much higher than the summed error in determination of the same elements in all other pools. With estimates provided for all other major elemental pools, mass balance calculations could be used to infer the temporal development of DOC, DON and POP pools.

Future elevated pCO₂ was found to enhance net autotrophic community carbon uptake in two of the three experimental phases but did not significantly affect particle elemental composition. Enhanced carbon consumption appears to result in accumulation of dissolved organic carbon under nutrient-recycling summer conditions. This carbon over-consumption effect becomes evident from mass balance calculations, but was too small to be resolved by direct measurements of dissolved organic matter. Faster nutrient uptake by comparatively small algae at high CO₂ after nutrient addition resulted in reduced production rates under future ocean CO₂ conditions at the end of the experiment. This CO₂ mediated shift towards smaller phytoplankton and enhanced cycling of dissolved matter restricted the development of larger phytoplankton, thus pushing the system towards a retention type food chain with overall negative effects on export potential.

Contrasting responses of DMS and DMSP to ocean acidification in Arctic waters

Increasing atmospheric CO₂ is decreasing ocean pH most rapidly in colder regions such as the Arctic. As a component of the EPOCA pelagic mesocosm experiment off Spitzbergen in 2010, we examined the consequences of decreased pH and increased pCO₂ on the concentrations of dimethylsulphide (DMS). DMS is an important reactant and contributor to aerosol formation and growth in the Arctic troposphere. In the nine mesocosms with initial pH 8.3 to 7.5, equivalent to pCO₂ of 180 to 1420 μatm, highly significant but inverse responses to acidity (hydrogen ion concentration [H⁺]) occurred following nutrient addition. Compared to ambient [H⁺], average concentrations of DMS during the most representative phase of the 30 d experiment were reduced by approximately 60% at the highest [H⁺] and by 35% at [H⁺] equivalent to 750 μatm pCO₂, as predicted for 2100. In contrast, concentrations of dimethylsulphoniopropionate (DMSP), the precursor of DMS, were elevated by approximately 50% at the highest [H⁺] and by 30% at [H⁺] corresponding to 750 μatm pCO₂. Measurements of the specific rate of synthesis of DMSP by phytoplankton indicate increased production at high [H⁺], in parallel to rates of inorganic carbon fixation. The elevated DMSP production at high [H⁺] was largely a consequence of increased dinoflagellate biomass and in particular, the increased abundance of the species Heterocapsa rotundata. We discuss both phytoplankton and bacterial processes that may explain the reduced ratios of DMS:DMSPt at higher [H⁺]. The experimental design of eight treatment levels provides comparatively robust empirical relationships of DMS and DMSP concentration, DMSP production and dinoflagellate biomass versus [H⁺] in Arctic waters.

Primary production and respiration of hypersaline microbial mats as a response for high and low CO2 availability

Here we report a time series of experiments performed in a microcosm to test the response of hypersaline microbial mats to diverse atmospheric CO₂ conditions. Different from most part of the literature, our study used a sample chamber were carbon dioxide concentration was controlled. Our aim was to test the effect of different atmospheric CO₂ conditions in benthic gross and net primary production, and respiration. This study showed for the first time to our knowledge absolute carbon limitation in a microbial mat. Oxygen concentration profile varied from a flattened shape to almost linear when atmospheric CO₂ at the chamber reached 0 ppm, with NPP reaching 0 nmol cm⁻³ s⁻¹ throughout most part of the profile. In this conditions sediment community respiration represented 100% of GPP. Extreme close coupling between primary production and respiration in microbial mats can be even self-sustainable in environments with temporally no atmospheric CO₂ available. When submitted to even high CO₂ concentrations (550 ppm), our sample showed a characteristic shape that indicate limitation composed by a more rectilinear oxygen profile, and NPP peaks mainly restricted to deeper layers. Therefore, we suggest that phototrophic communities in aquatic shallow ecosystems can be carbon limited. This limitation could be common especially in ecosystems submitted to variable water depth conditions, like coastal lagoons and intertidal sediments.

Temporal biomass dynamics of an Arctic plankton bloom in response to increasing levels of atmospheric carbon dioxide

Ocean acidification and carbonation, driven by anthropogenic emissions of carbon dioxide (CO₂), have been shown to affect a variety of marine organisms and are likely to change ecosystem functioning. High latitudes, especially the Arctic, will be the first to encounter profound changes in carbonate chemistry speciation at a large scale, namely the under-saturation of surface waters with respect to aragonite, a calcium carbonate polymorph produced by several organisms in this region. During a CO₂ perturbation study in 2010, in the framework of the EU-funded project EPOCA, the temporal dynamics of a plankton bloom was followed in nine mesocosms, manipulated for CO₂ levels ranging initially from about 185 to 1420 μatm. Dissolved inorganic nutrients were added halfway through the experiment. Autotrophic biomass, as identified by chlorophyll a standing stocks (Chl a), peaked three times in all mesocosms. However, while absolute Chl a concentrations were similar in all mesocosms during the first phase of the experiment, higher autotrophic biomass was measured at high in comparison to low CO₂ during the second phase, right after dissolved inorganic nutrient addition. This trend then reversed in the third phase. There were several statistically significant CO₂ effects on a variety of parameters measured in certain phases, such as nutrient utilization, standing stocks of particulate organic matter, and phytoplankton species composition. Interestingly, CO₂ effects developed slowly but steadily, becoming more and more statistically significant with time. The observed CO₂ related shifts in nutrient flow into different phytoplankton groups (mainly diatoms, dinoflagellates, prasinophytes and haptophytes) could have consequences for future organic matter flow to higher trophic levels and export production, with consequences for ecosystem productivity and atmospheric CO₂.

Arctic microbial community dynamics influenced by elevated CO2 levels

The Arctic Ocean ecosystem is particular vulnerable for ocean acidification (OA) related alterations due to the relatively high CO₂ solubility and low carbonate saturation states of its cold surface waters. Thus far, however, there is only little known about the consequences of OA on the base of the food web. In a mesocosm CO₂-enrichment experiment (overall CO₂ levels ranged from ∼180 to 1100 μatm) in the Kongsfjord off Svalbard, we studied the consequences of OA on a natural pelagic microbial community. The most prominent finding of our study is the profound effect of OA on the composition and growth of the Arctic phytoplankton community, i.e. the picoeukaryotic photoautotrophs and to a lesser extent the nanophytoplankton prospered. A shift towards the smallest phytoplankton as a result of OA will have direct consequences for the structure and functioning of the pelagic food web and thus for the biogeochemical cycles. Furthermore, the dominant pico- and nanophytoplankton groups were found prone to viral lysis, thereby shunting the carbon accumulation in living organisms into the dissolved pools of organic carbon and subsequently affecting the efficiency of the biological pump in these Arctic waters.

Ocean acidification causes ecosystem shifts via altered competitive interactions

Ocean acidification represents a pervasive environmental change that is predicted to affect a wide range of species^{1, 2}, yet our understanding of the emergent ecosystem impacts is very limited. Many studies report detrimental effects of acidification on single species in lab studies, especially those with calcareous shells or skeletons^{3, 4, 5}. Observational studies using naturally acidified ecosystems have shown profound shifts away from such calcareous species^{6, 7, 8}, and there has been an assumption that direct impacts of acidification on sensitive species drive most ecosystem responses. We tested an alternative hypothesis that species interactions attenuate or amplify the direct effects of acidification on individual species^{9, 10, 11, 12}. Here, we show that altered competitive dynamics between calcareous species and fleshy seaweeds drive significant ecosystem shifts in acidified conditions. Although calcareous species recruited and grew at similar rates in ambient and low pH conditions during early successional stages, they were rapidly overgrown by fleshy seaweeds later in succession in low pH conditions. The altered competitive dynamics between calcareous species and fleshy seaweeds is probably the combined result of decreased growth rates of calcareous species, increased growth rates of fleshy seaweeds, and/or altered grazing rates¹³. Phase shifts towards ecosystems dominated by fleshy seaweed are common in many marine ecosystems^{14, 15, 16}, and our results suggest that changes in the competitive balance between these groups represent a key leverage point through which the physiological responses of individual species to acidification could indirectly lead to profound ecosystem changes in an acidified ocean.

Element budgets in an Arctic mesocosm CO2 perturbation study

Recent studies on the impacts of ocean acidification on pelagic communities have identified changes in carbon to nutrient dynamics with related shifts in elemental stoichiometry. In principle, mesocosm experiments provide the opportunity of determining the temporal dynamics of all relevant carbon and nutrient pools and, thus, calculating elemental budgets. In practice, attempts to budget mesocosm enclosures are often hampered by uncertainties in some of the measured pools and fluxes, in particular due to uncertainties in constraining air/sea gas exchange, particle sinking, and wall growth. In an Arctic mesocosm study on ocean acidification using KOSMOS (Kiel Off-Shore Mesocosms for future Ocean Simulation) all relevant element pools and fluxes of carbon, nitrogen and phosphorus were measured, using an improved experimental design intended to narrow down some of the mentioned uncertainties. Water column concentrations of particulate and dissolved organic and inorganic constituents were determined daily. New approaches for quantitative estimates of material sinking to the bottom of the mesocosms and gas exchange in 48 h temporal resolution, as well as estimates of wall growth were developed to close the gaps in element budgets. Future elevated pCO₂ was found to enhance net autotrophic community carbon uptake in 2 of the 3 experimental phases but did not significantly affect particle elemental composition. Enhanced carbon consumption appears to result in accumulation of dissolved organic compounds under nutrient recycling summer conditions. This carbon over-consumption effect becomes evident from budget calculations, but was too small to be resolved by direct measurements of dissolved organics. The out-competing of large diatoms by comparatively small algae in nutrient uptake caused reduced production rates under future ocean CO₂ conditions in the end of the experiment. This CO₂induced shift away from diatoms towards smaller phytoplankton and enhanced cycling of dissolved organics was pushing the system towards a retention type food chain with overall negative effects on export potential.

Net community production and stoichiometry of nutrient consumption in a pelagic ecosystem of a northern high latitude fjord: mesocosm CO2 perturbation study

Net community production (NCP) and ratios of carbon to nutrient consumption were studied during a large-scale mesocosm experiment on ocean acidification in Kongsfjorden, West Spitsbergen, during June–July 2010. Nutrient-deplete fjord water with natural phyto- and bacteriaplankton assemblages, enclosed in nine mesocosms of ~ 50 m³ volume, was exposed to pCO₂levels ranging from 185 to 1420 μatm on initial state. Mean values of pCO₂ levels during experiment ranged from 175 to 1085 μatm in different mesocosms. Phytoplankton growth was stimulated by nutrient addition. In this study NCP is estimated as a cumulative change in dissolved inorganic carbon concentrations. Stoichiometric couping between inorganic carbon and nutrient is shown as a ratio of a cumulative NCP to a cumulative change in inorganic nutrients. Three peaks of chlorophyll a concentration occurred during the experiment. Accordingly the experiment was divided in three phases. Overall cumulative NCP was similar in all mesocosms by the final day of experiment. However, NCP varied among phases, showing variable response to CO₂ perturbation. Carbon to nitrogen (C : N) and carbon to phosphorus (C : P) uptake ratios were estimated only for the period after nutrient addition (post-nutrient period). For the total post-nutrient period ratios were close to Redfield proportions, however varied from it in different phases. The response of C : N and C : P uptake ratios to CO₂ perturbation was different for three phases of the experiment, reflecting variable NCP and dependence on changing microbial community. Through the variable NCP, C : N and C : P uptake ratios for 31 days of the experiment we show a flexibility of biogeochemical response establishing a strong microbial loop in Kongsfjorden under different CO₂ scenarios.

Diel variability in seawater pH relates to calcification and benthic community structure on coral reefs

Community structure and assembly are determined in part by environmental heterogeneity. While reef-building corals respond negatively to warming (i.e. bleaching events) and ocean acidification (OA), the extent of present-day natural variability in pH on shallow reefs and ecological consequences for benthic assemblages is unknown. We documented high resolution temporal patterns in temperature and pH from three reefs in the central Pacific and examined how these data relate to community development and net accretion rates of early successional benthic organisms. These reefs experienced substantial diel fluctuations in temperature (0.78°C) and pH (>0.2) similar to the magnitude of ‘warming’ and ‘acidification’ expected over the next century. Where daily pH within the benthic boundary layer failed to exceed pelagic climatological seasonal lows, net accretion was slower and fleshy, non-calcifying benthic organisms dominated space. Thus, key aspects of coral reef ecosystem structure and function are presently related to natural diurnal variability in pH.

Mesozooplankton community development at elevated CO2 concentrations: results from a mesocosm experiment in an Arctic fjord

The increasing CO₂ concentration in the atmosphere caused by burning fossil fuels leads to increasing pCO₂ and decreasing pH in the world oceans. These changes may have severe consequences for marine biota, especially in cold-water ecosystems due to higher solubility of CO₂. However, studies on the response of mesozooplankton communities to elevated pCO₂ are yet lacking. In order to test whether abundance and taxonomic composition change with pCO₂, we have sampled nine mesocosms, which were deployed in Kongsfjorden, an Arctic fjord at Svalbard, and were adjusted to eight CO₂ concentrations, initially ranging from 185 μatm to 1420 μatm. Samples were taken weekly over a six-week period with an Apstein net (55 μm mesh size) in all mesocosms and the surrounding fjord. In addition, sediment trap samples, taken every second day in the mesocosms, were analyzed to account for losses due to vertical migration and mortality. The taxonomic analysis revealed that meroplanktonic larvae (cirripeds, polychaetes, bivalves, gastropod, and decapods) dominated in the mesocosms while copepods (Calanus spp., Oithona similis, Acartia longiremis and Microsetella norvegica) were found in lower abundances. In the fjord copepods prevailed for most of our study. With time, abundance and taxonomic composition developed similarly in all mesocosms; the pCO₂ had no significant effect on the overall community structure. However, single taxa responded to elevated CO₂concentrations. The ratio of cirripedia nauplii to cypris larvae, the next developmental stage, in the sediment traps averaged over the entire experiment increased with pCO₂ and this suggests that increased pCO₂ may have delayed their development. Also, the number of bivalves, averaged over the experimental period, decreased significantly with increasing pCO₂. The nature of the CO₂ effect, either direct or indirect, remains open and needs to be addressed in future.