Posts Tagged 'primary production'

Effects of shellfish and macro-algae IMTA in North China on the environment, inorganic carbon system, organic carbon system, and sea–air CO2 fluxes

Shellfish and macro-algae integrated multi-trophic aquaculture (IMTA) contribute greatly to the sustainability of aquaculture. However, the effects of large-scale shellfish and macro-algae aquaculture on the functions of the ocean carbon sink are not clear. To clarify these effects, we studied the spatial and temporal changes of inorganic and organic carbon systems in seawater under different aquaculture modes (monoculture or polyculture of shellfish and macro-algae) in Sanggou Bay, together with the variation of other environmental factors. The results show that the summertime dissolved oxygen (DO) concentration in the shellfish culture zone was significantly lower than other zones (p < 0.05), with a minimum value of 7.07 ± 0.25 mg/L. The variation of pH and total alkalinity (TA) were large across different culture modes, and the seawater in the shellfish culture zone had the lowest pH and TA than the other zones. Seasonal environment and aquaculture modes significantly affected the variation of dissolved inorganic carbon (DIC), CO2 partial pressure (pCO2), dissolved organic carbon (DOC), and particulate organic carbon (POC) concentrations. The highest values of DIC, pCO2, and POC appeared in summer, and the lowest appeared in winter. For DOC concentration, the lowest value appeared in autumn. Spatially, DIC and pCO2 were highest in the shellfish culture zone and lowest in the macro-algae culture zone, DOC was highest in the macro-algae culture zone and lowest in the shellfish culture zone, and POC was lower in the shellfish culture zone and macro-algae culture zone and higher in the remaining zones. The results of sea–air CO2 fluxes showed that except for the shellfish culture zone during summertime, which released CO2 to the atmosphere, all culture zones were the sinks of atmospheric CO2 during the culture period, with the whole bay being a strong CO2 sink during autumn and winter. In summary, large-scale shellfish–macro-algae IMTA plays an important role in the local carbon cycle and contributes to mitigating ocean acidification and hypoxia.

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The role of epiphytes in seagrass productivity under ocean acidification

Ocean Acidification (OA), due to rising atmospheric CO2, can affect the seagrass holobiont by changing the plant’s ecophysiology and the composition and functioning of its epiphytic community. However, our knowledge of the role of epiphytes in the productivity of the seagrass holobiont in response to environmental changes is still very limited. CO2 vents off Ischia Island (Italy) naturally reduce seawater pH, allowing to investigate the adaptation of the seagrass Posidonia oceanica L. (Delile) to OA. Here, we analyzed the percent cover of different epiphytic groups and the epiphytic biomass of P. oceanica leaves, collected inside (pH 6.9–7.9) and outside (pH 8.1–8.2) the CO2 vents. We estimated the contribution of epiphytes to net primary production (NPP) and respiration (R) of leaf sections collected from the vent and ambient pH sites in laboratory incubations. Additionally, we quantified net community production (NCP) and community respiration (CR) of seagrass communities in situ at vent and ambient pH sites using benthic chambers. Leaves at ambient pH sites had a 25% higher total epiphytic cover with encrusting red algae (32%) dominating the community, while leaves at vent pH sites were dominated by hydrozoans (21%). Leaf sections with and without epiphytes from the vent pH site produced and respired significantly more oxygen than leaf sections from the ambient pH site, showing an average increase of 47 ± 21% (mean ± SE) in NPP and 50 ± 4% in R, respectively. Epiphytes contributed little to the increase in R; however, their contribution to NPP was important (56 ± 6% of the total flux). The increase in productivity of seagrass leaves adapted to OA was only marginally reflected by the results from the in situ benthic chambers, underlining the complexity of the seagrass community response to naturally occurring OA conditions.

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Sensitivity of phytoplankton to climate change: direct and interactive effects of CO2 on primary production and community composition

Marine phytoplankton constitutes about half of the primary production on Earth. It forms the base of the marine food web and is a pivotal player in the marine biological carbon pump. The primary environmental drivers that control phytoplankton growth are temperature, nutrient availability, light, and the concentration of inorganic carbon species. Ongoing climate change modifies these drivers, leading to a warming, high-CO2 ocean with altered nutrient availabilities and light regimes. Changes in phytoplankton productivity and community composition resulting from these newly emerging environmental states in the ocean have important implications for the marine ecosystem and carbon cycling.

Biogeochemical ocean models are used to investigate how marine primary production may be affected by future climate change under different emission scenarios. Phytoplankton growth rates in models are typically determined by functions describing growth dependencies on temperature, light, and nutrients. However, a large body of laboratory studies on phytoplankton responses to environmental drivers reveals two points that are usually not considered in current biogeochemical models. Firstly, phytoplankton growth can be considerably modified by the state of the carbonate system. Changes in inorganic carbon species concentrations can be either growth-enhancing (CO2(aq) and bicarbonate are substrates for photosynthesis), or growth-dampening (increasing CO2(aq) levels lead to a shift in the carbonate equilibria and result in a pH decrease, a process which is called ocean acidification). Functions describing this growth dependence of phytoplankton on the carbonate system have not been implemented in large-scale ocean biogeochemical models so far. Secondly, growth responses towards one driver can be modified if the level of another driver is changing. Functions including these so-called interactive driver effects partly exist in models (e.g. the response to varying light levels may depend on the nutrient limitation term). However, the large number of laboratory studies on multiple driver effects has never been used to constrain driver interactions in large-scale ocean biogeochemical models. This holds especially true for the findings of growth responses to driver interactions that include ocean acidification, which make up the largest share of laboratory experiments.

This thesis aims to investigate sensitivities of marine phytoplankton to changing CO2(aq) levels as well as to interactive effects between CO2 and other environmental drivers. A comprehensive and reproducible literature search in combination with a statistical analysis (Publication I) reveals that increasing CO2(aq) levels robustly dampen the growth-increasing effects of warming and improving light conditions. In addition, the results show that the calcifying phytoplankton group of coccolithophores experiences the strongest negative effects by ocean acidification compared to other phytoplankton groups. A second study (Publication II) examines the effects of mechanistically described carbonate system dependencies on primary production and community composition in a model. To this end, carbonate system dependencies of phytoplankton growth and and coccolithophore calcification are implemented into the global biogeochemical ocean model REcoM. The study shows that responses to ocean acidification cascade on growth responses to other drivers, which partly balance or counteract the direct impact of the carbonate system on growth rates. In addition, warming is identified as the main driver of the observed recent increase of coccolithophore biomass in the North Atlantic. A final study (Publication III) investigates the interactive effects between CO2 and temperature as well as between CO2 and light on phytoplankton biomass and community composition in a high emission scenario. For the parametrization in REcoM, growth responses to interacting drivers as synthesized in Publication I are used. The decrease of global future phytoplankton biomass and net community production by the end of the century is similar in simulations with and without driver interactions (-6% and -8%, respectively). However, phytoplankton responses to future climate conditions are considerably modified on a regional scale and the share of individual phytoplankton groups in the community changes both globally and regionally when accounting for multiple driver effects. Globally, diatoms and coccolithophores are impacted more and small phytoplankton less severely by future oceanic conditions when accounting for driver interactions. Future projections of the Southern Ocean phytoplankton community are modified most dramatically with the new interactive growth formulation, as diatoms and coccolithophores become less and small phytoplankton more abundant, while it is the other way round in simulations without driver interactions.

The thesis highlights 1) that the carbonate system is a critical growth-modifying driver for phytoplankton in a high-CO2 ocean, which can furthermore modify growth responses to other drivers substantially, and 2) that driver interactions have considerable effects on climate-change induced alterations in the phytoplankton community as well as on regional biomass changes in a future ocean.

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Response of Cymodocea nodosa to ocean acidification and warming in the Canary Islands: direct and indirect effects


  • Ocean acidification increase growth and gross primary production of Cymodocea nodosa.
  • The rise of temperature limited the net and gross primary production of Cymodocea nodosa.
  • A positive effect of decrased pH on greater vulnerability to consumption by Paracentrotus lividus.
  • A future scenario of climate change will affect metabolic rates of C.nodosa.
  • Different responses to climate change have been observed by C. nodosa from Canary Islands.


As detected in warming and ocean acidification, global change can have profound impact on marine life. Its effects on seagrasses are becoming increasingly well-known, since several studies have focused on the responses of these species to global change conditions. However a few studies have assessed the combined effect of temperature and acidification on seagrasses. Overall in this study, the combined effects of increased ocean temperature and pH levels expected at the end of this century (+5 °C and pH 7.5) on Cymodocea nodosa from Canary Islands, were evaluated for one month through manipulative laboratory experiments. Growth, net production, respiration, gross primary production, chlorophyll-a concentration and its vulnerability to herbivory were quantified. Results showed a positive effect of decreased pH on growth and gross primary production, as well as greater vulnerability to consumption by the sea urchin Paracentrotus lividus. In contrast, increased temperature limited net and gross primary production. This study shows than in future scenarios, C. nodosa from the Canary Islands may be a losing species in the global change stakes.

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Physiological control on carbon isotope fractionation in marine phytoplankton

One of the great challenges in biogeochemical research over the past half a century has been to quantify and understand the mechanisms underlying stable carbon isotope fractionation (εp) in phytoplankton in response to changing pCO2. Partly, this interest is grounded in the use of fossil photosynthetic organism remains as a proxy for past atmospheric CO2 concentrations. Phytoplankton organic carbon is depleted in 13C compared to its source because of kinetic fractionation by the enzyme RubisCO during photosynthetic carbon fixation, as well as through physiological pathways upstream of RubisCO. Moreover, other factors such as nutrient limitation, variations in light regime as well as phytoplankton culturing systems and inorganic carbon manipulation approaches may confound the influence of CO2 on εp. Here, based on experimental data compiled from the literature, we assess which underlying physiological processes cause the observed differences in εp for various phytoplankton groups in response to C-demand/C-supply and test potential confounding factors. Culturing approaches and methods of carbonate chemistry manipulation were found to best explain the differences in εp between studies, although daylength was an important predictor for εp in haptophytes. Extrapolating results from culturing experiments to natural environments and for proxy applications therefore requires caution, and it should be carefully considered whether culture methods and experimental conditions are representative of natural environments.

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In contrast to diatoms, cryptophytes are susceptible to iron limitation, but not to ocean acidification

Previous field studies in the Southern Ocean (SO) indicated an increased occurrence and dominance of cryptophytes over diatoms due to climate change. To gain a better mechanistic understanding of how the two ecologically important SO phytoplankton groups cope with ocean acidification (OA) and iron (Fe) availability, we chose two common representatives of Antarctic waters, the cryptophyte Geminigera cryophila and the diatom Pseudo-nitzschia subcurvata. Both species were grown at 2°C under different pCO2 (400 vs. 900 μatm) and Fe (0.6 vs. 1.2 nM) conditions. For P. subcurvata, an additional high pCO2 level was applied (1400 μatm). At ambient pCO2 under low Fe supply, growth of G. cryophila almost stopped while it remained unaffected in P. subcurvata. Under high Fe conditions, OA was not beneficial for P. subcurvata, but stimulated growth and carbon production of G. cryophila. Under low Fe supply, P. subcurvata coped much better with OA than the cryptophyte, but invested more energy into photoacclimation. Our study reveals that Fe limitation was detrimental for the growth of G. cryophila and suppressed the positive OA effect. The diatom was efficient in coping with low Fe, but was stressed by OA while both factors together strongly impacted its growth. The distinct physiological response of both species to OA and Fe limitation explains their occurrence in the field. Based on our results, Fe availability is an important modulator of OA effects on SO phytoplankton, with different implications on the occurrence of cryptophytes and diatoms in the future.

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Calcification moderates the biochemical responses of Gephyrocapsa oceanica to ocean acidification

We compared the physiological performance of two sub-strains of coccolithophore Gephyrocapsa oceanica NIES-1318, the originally well-calcified strain, and its low-calcified counterpart that significantly decreased the capacity to calcify under present (400 µatm, LC) and elevated pCO2 (1000 µatm, HC) conditions. There were no significant differences in the growth rates between the two sub-strains under LC condition. The growth rates of both sub-strains reduced under HC conditions and the decrease was significantly higher in the high-calcified cells than the low-calcified ones. The low-calcified cultures exhibited reduced production rates of particulate organic carbon (POC) and particulate organic nitrogen (PON), irrespective of CO2 conditions. The decrease in the PON production rates was considerably higher than that in the POC production rates. Compared with the high-calcified cells, a slight decrease was observed in cellular POC contents in the low-calcified cells, whereas cellular PON contents decreased more prominently. The POC/PON ratio showed no significant difference between the two pCO2 treatments in the high-calcified cultures, whereas elevated CO2 increased the rates in the low-calcified cells. We believe that the nitrogen acquisition by low-calcified cells was more susceptible to ocean acidification, probably due to a lack of stabilized microenvironment provided by coccoliths. Our results demonstrate that the calcification level can affect the biochemical responses of G. oceanica to ocean acidification, with likely consequences for marine biogeochemical cycling.

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Attributing controlling factors of acidification and hypoxia in a deep, nutrient-enriched estuarine embayment

Measuring and attributing controlling factors of acidification and hypoxia are essential for management of coastal ecosystems affected by those stressors. We address this using surveys in the Firth of Thames, a deep, seasonally stratified estuarine embayment adjoing the Hauraki Gulf in northern Aotearoa/New Zealand. The Firth’s catchment has undergone historic land-use intensification transforming it from native forest cover to dominance by pastoral use, increasing its riverine total nitrogen loading by ∼82% over natural levels and switching it’s predominate loading source from offshore to the catchment. We hypothesised that seasonal variation in net ecosystem metabolism [NEM: dissolved inorganic carbon (DIC) uptake/release] will be a primary factor determining carbonate and oxic responses in the Firth, and that organic matter involved in the metabolism will originate primarily by fixation within the Firth system and be driven by catchment dissolved inorganic nitrogen (DIN) loading. Seasonal ship-based and biophysical mooring surveys across the Hauraki Gulf and Firth showed depressed pH and O2 reaching pH ∼7.8 and O2 ∼4.8 mg L–1 in autumn in the inner Firth, matched by shoreward increasing nutrient loading, phytoplankton, organic matter, gross primary production (GPP) and apparent O2 utilization. A carbonate system deconvolution of the ship survey data, combined with other ship survey and mooring results, showed how CO2 partial pressure responded to seasonal shifts in temperature, NEM, phytoplankton sinking and mineralisation and water column stratification, that underlay the late-season expression of acidification and hypoxia. This aligned with seasonal shifts in net DIC fluxes determined in a coincident nutrient mass-balance analysis, showing near-neutral fluxes from spring to summer, but respiratory NEM from summer to autumn. Particulate C:N and ratios of organic C fixed by Firth GPP to that from river inputs (∼29- to 100-fold in summer and autumn) showed that the dominant source of organic matter fuelling heterotrophy in autumn was autochthonous GPP, driven by riverine DIN loading. The results signified the sensitivity of deep, long-residence time, seasonally stratifying estuaries to acidification and hypoxia, and are important for coastal resource management, including aquaculture developments and catchment runoff limit-setting for maintenance of ecosystem health.

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Derivation of seawater pCO2 from net community production identifies the South Atlantic Ocean as a CO2 source

A key step in assessing the global carbon budget is the determination of the partial pressure of CO2 in seawater (pCO2 (sw)). Spatially complete observational fields of pCO2 (sw) are routinely produced for regional and global ocean carbon budget assessments by extrapolating sparse in situ measurements of pCO2 (sw) using satellite observations. As part of this process, satellite chlorophyll a (Chl a) is often used as a proxy for the biological drawdown or release of CO2. Chl a does not, however, quantify carbon fixed through photosynthesis and then respired, which is determined by net community production (NCP).

In this study, pCO2 (sw) over the South Atlantic Ocean is estimated using a feed forward neural network (FNN) scheme and either satellite-derived NCP, net primary production (NPP) or Chl a to compare which biological proxy produces the most accurate fields of pCO2 (sw). Estimates of pCO2 (sw) using NCP, NPP or Chl a were similar, but NCP was more accurate for the Amazon Plume and upwelling regions, which were not fully reproduced when using Chl a or NPP. A perturbation analysis assessed the potential maximum reduction in pCO2 (sw) uncertainties that could be achieved by reducing the uncertainties in the satellite biological parameters. This illustrated further improvement using NCP compared to NPP or Chl a. Using NCP to estimate pCO2 (sw) showed that the South Atlantic Ocean is a CO2 source, whereas if no biological parameters are used in the FNN (following existing annual carbon assessments), this region appears to be a sink for CO2. These results highlight that using NCP improved the accuracy of estimating pCO2 (sw) and changes the South Atlantic Ocean from a CO2 sink to a source. Reducing the uncertainties in NCP derived from satellite parameters will ultimately improve our understanding and confidence in quantification of the global ocean as a CO2 sink.

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The carbon and nitrogen budget of Desmophyllum dianthus—a voracious cold-water coral thriving in an acidified Patagonian fjord

In the North Patagonian fjord region, the cold-water coral (CWC) Desmophyllum dianthus occurs in high densities, in spite of low pH and aragonite saturation. If and how these conditions affect the energy demand of the corals is so far unknown. In a laboratory experiment, we investigated the carbon and nitrogen (C, N) budget of D. dianthus from Comau Fjord under three feeding scenarios: (1) live fjord zooplankton (100–2,300 µm), (2) live fjord zooplankton plus krill (>7 mm), and (3) four-day food deprivation. In closed incubations, C and N budgets were derived from the difference between C and N uptake during feeding and subsequent C and N loss through respiration, ammonium excretion, release of particulate organic carbon and nitrogen (POC, PON). Additional feeding with krill significantly increased coral respiration (35%), excretion (131%), and POC release (67%) compared to feeding on zooplankton only. Nevertheless, the higher C and N losses were overcompensated by the threefold higher C and N uptake, indicating a high assimilation and growth efficiency for the krill plus zooplankton diet. In contrast, short food deprivation caused a substantial reduction in respiration (59%), excretion (54%), release of POC (73%) and PON (87%) compared to feeding on zooplankton, suggesting a high potential to acclimatize to food scarcity (e.g., in winter). Notwithstanding, unfed corals ‘lost’ 2% of their tissue-C and 1.2% of their tissue-N per day in terms of metabolism and released particulate organic matter (likely mucus). To balance the C (N) losses, each D. dianthus polyp has to consume around 700 (400) zooplankters per day. The capture of a single, large krill individual, however, provides enough C and N to compensate daily C and N losses and grow tissue reserves, suggesting that krill plays an important nutritional role for the fjord corals. Efficient krill and zooplankton capture, as well as dietary and metabolic flexibility, may enable D. dianthus to thrive under adverse environmental conditions in its fjord habitat; however, it is not known how combined anthropogenic warming, acidification and eutrophication jeopardize the energy balance of this important habitat-building species.

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Configuration and validation of an oceanic physical and biogeochemical model to investigate coastal eutrophication in the Southern California Bight


The Southern California Bight (SCB), an eastern boundary upwelling system, is impacted by global warming, acidification and oxygen loss, and receives anthropogenic nutrients from a coastal population of 20 million people. We describe the configuration, forcing, and validation of a realistic, submesoscale resolving ocean model as a tool to investigate coastal eutrophication. This modeling system represents an important achievement because it strikes a balance of capturing the forcing by U.S. Pacific Coast-wide phenomena, while representing the bathymetric features and submesoscale circulation that affect the transport of nutrients from natural and human sources. Moreover, the model allows simulations at timescales that approach the interannual frequencies of ocean variability. The model simulation is evaluated against a broad suite of observational data throughout the SCB, showing realistic depiction of the mean state and its variability with satellite and in situ measurements of state variables and biogeochemical rates. The simulation reproduces the main structure of the seasonal upwelling front, the mean current patterns, the dispersion of wastewater plumes, as well as their seasonal variability. Furthermore, it reproduces the mean distributions of key biogeochemical and ecosystem properties and their variability. Biogeochemical rates reproduced by the model, such as primary production and nitrification, are also consistent with measured rates. This validation exercise demonstrates the utility of using fine-scale resolution modeling and local observations to identify, investigate, and communicate uncertainty to stakeholders to support management decisions on local anthropogenic nutrient discharges to coastal zones.

Plain Language Summary

We applied and validated an ocean numerical model to investigate the effects of land-based and atmospheric nutrient loading on coastal eutrophication and its effects on carbon, nitrogen and oxygen cycles of the Southern California Bight, an upwelling-dominated marine embayment on the U.S. West Coast. The model is capable of high resolution, multi-year hindcast simulations, which enable investigations to disentangle natural variability, climate change, and local human pressures that accelerate land-based and atmospheric nutrient loads. The model performance assessment illustrates that it faithfully reproduces monitored ocean properties related to algal blooms, oxygen and water acidity, among others, that can be traced to land-based and atmospheric inputs of nutrients and carbon from human activities. The model performance assessment helps to constrain uncertainties in predictions to support ongoing conversations on approaches to reduce the effects of climate change, including considerations of management of local nutrient and carbon inputs.

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Impact of dust addition on the metabolism of Mediterranean plankton communities and carbon export under present and future conditions of pH and temperature (update)

Although atmospheric dust fluxes from arid as well as human-impacted areas represent a significant source of nutrients to surface waters of the Mediterranean Sea, studies focusing on the evolution of the metabolic balance of the plankton community following a dust deposition event are scarce, and none were conducted in the context of projected future levels of temperature and pH. Moreover, most of the experiments took place in coastal areas. In the framework of the PEACETIME project, three dust-addition perturbation experiments were conducted in 300 L tanks filled with surface seawater collected in the Tyrrhenian Sea (TYR), Ionian Sea (ION) and Algerian basin (FAST) on board the R/V Pourquoi Pas? in late spring 2017. For each experiment, six tanks were used to follow the evolution of chemical and biological stocks, biological activity and particle export. The impacts of a dust deposition event simulated at their surface were followed under present environmental conditions and under a realistic climate change scenario for 2100 (ca. +3 C and −0.3 pH units). The tested waters were all typical of stratified oligotrophic conditions encountered in the open Mediterranean Sea at this period of the year, with low rates of primary production and a metabolic balance towards net heterotrophy. The release of nutrients after dust seeding had very contrasting impacts on the metabolism of the communities, depending on the station investigated. At TYR, the release of new nutrients was followed by a negative impact on both particulate and dissolved 14C-based production rates, while heterotrophic bacterial production strongly increased, driving the community to an even more heterotrophic state. At ION and FAST, the efficiency of organic matter export due to mineral/organic aggregation processes was lower than at TYR and likely related to a lower quantity/age of dissolved organic matter present at the time of the seeding and a smaller production of DOM following dust addition. This was also reflected by lower initial concentrations in transparent exopolymer particles (TEPs) and a lower increase in TEP concentrations following the dust addition, as compared to TYR. At ION and FAST, both the autotrophic and heterotrophic community benefited from dust addition, with a stronger relative increase in autotrophic processes observed at FAST. Our study showed that the potential positive impact of dust deposition on primary production depends on the initial composition and metabolic state of the investigated community. This impact is constrained by the quantity of nutrients added in order to sustain both the fast response of heterotrophic prokaryotes and the delayed one of primary producers. Finally, under future environmental conditions, heterotrophic metabolism was overall more impacted than primary production, with the consequence that all integrated net community production rates decreased with no detectable impact on carbon export, therefore reducing the capacity of surface waters to sequester anthropogenic CO2.

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Influence of seawater acidification on biochemical composition and oxidative status of green algae Ulva compressa


  • Seawater acidification improved primary productivity, pigments and carbon storage.
  • No significant change in the cellular redox status of U. compressa under acidification.
  • Elevated level of essential amino acids and polyunsaturated fatty acids.
  • Possible benefits to U. compressa in future predicted acidified waters.


The sequestration of elevated atmospheric CO2 levels in seawater results in increasing acidification of oceans and it is unclear what the consequences of this will be on seaweed ecophysiology and ecological services they provide in the coastal ecosystem. In the present study, we examined the physiological and biochemical response of intertidal green seaweed Ulva compressa to elevated pCO2 induced acidification. The green seaweed was exposed to control (pH 8.1) and acidified (pH 7.7) conditions for 2 weeks following which net primary productivity, pigment content, oxidative status and antioxidant enzymes, primary and secondary metabolites, and mineral content were assessed. We observed an increase in primary productivity of the acidified samples, which was associated with increased levels of photosynthetic pigments. Consequently, primary metabolites levels were increased in the thalli grown under lowered pH conditions. There was also richness in various minerals and polyunsaturated fatty acids, indicating that the low pH elevated the nutritional quality of U. compressa. We found that low pH reduced malondialdehyde (MDA) content, suggesting reduced oxidative stress. Consistently we found reduced total antioxidant capacity and a general reduction in the majority of enzymatic and non-enzymatic antioxidants in the thalli grown under acidified conditions. Our results indicate that U. compressa will benefit from seawater acidification by improving productivity. Biochemical changes will affect its nutritional qualities, which may impact the food chain/food web under future acidified ocean conditions.

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Climate change negates positive CO2 effects on marine species biomass and productivity by altering the strength and direction of trophic interactions


  • We need more insight into how future food webs might be altered under climate change
  • We used empirical data of species interactions from multi-species mesocosms to model trophic interaction strengths within the food web
  • We separate direct from indirect species interactions, something which is seldom considered in climate studies
  • We show that warming is an overwhelming climate stressor that alters trophic interactions in both negative and positive ways
  • Ocean acidification boosted primary productivity which enabled energy to flow upward to higher trophic levels
  • We further show that the direct effects of warming are more severe than its indirect effects


One of the biggest challenges in more accurately forecasting the effects of climate change on future food web dynamics relates to how climate change affects multi-trophic species interactions, particularly when multiple interacting stressors are considered. Using a dynamic food web model, we investigate the individual and combined effect of ocean warming and acidification on changes in trophic interaction strengths (both direct and indirect) and the consequent effects on biomass structure of food web functional groups. To do this, we mimicked a species-rich multi-trophic-level temperate shallow-water rocky reef food web and integrated empirical data from mesocosm experiments on altered species interactions under warming and acidification, into food-web models. We show that a low number of strong temperature-driven changes in direct trophic interactions (feeding and competition) will largely determine the magnitude of biomass change (either increase or decrease) of high-order consumers, with increasing consumer biomass suppressing that of prey species. Ocean acidification, in contrast, alters a large number of weak indirect interactions (e.g. cascading effects of increased or decreased abundances of other groups), enabling a large increase in consumer and prey biomass. The positive effects of ocean acidification are driven by boosted primary productivity, with energy flowing up to higher trophic levels. We show that warming is a much stronger driver of positive as well as negative modifications of species biomass compared to ocean acidification. Warming affects a much smaller number of existing trophic interactions, though, with direct consumer-resource effects being more important than indirect effects. We conclude that the functional role of consumers in future food webs will be largely regulated by alterations in the strength of direct trophic interactions under ocean warming, with ensuing effects on the biomass structure of marine food webs.

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Editorial: Microbial response to a rapidly changing marine environment: global warming and ocean acidification

The World Ocean is undergoing rapid and substantial changes, particularly, in terms of warming and acidification. Global sea surface temperatures have risen by 0.7°C in recent years (2005–2014) relative to pre-industrial times (1870–1899) (Gattuso et al., 2015). The ocean pH is decreasing in response to the increasing anthropogenic CO2 emissions (Ocean Acidification; OA). This clear trend of ocean warming and acidification was documented in the fifth Assessment Report (AR5) by Intergovernmental Panel on Climate Change (IPCC). The warming of the surface ocean could increase stratification, suppress transport of nutrients into the upper photic zone and alter hydrographic properties or patterns of ocean circulation. The effects of OA include the changes of seawater carbonate chemistry such as an increase in partial pressure of seawater CO2 (pCO2) concentration and a decrease in calcium carbonate (CaCO3) saturation state (Royal Society, 2005IPCC, 2014). Consequently, the warming and acidification will have substantial impacts on the growth and survival of marine organisms (e.g., Brander, 2010Doney et al., 2012Hollowed et al., 2013). In particular, microbes, as a vital component of the marine ecosystem that includes microalga (phytoplankton), protists, fungi, viruses, and the two main groups of prokaryotes (Bacteria and Archaea), are vulnerable to these environmental changes. Since these microscopic organisms drive major biogeochemical cycles and support higher food webs globally, physiological, and ecological alterations in microbial communities caused by marine environmental changes can herald changes not only in pathways of energy transfer through the food web but also in global biogeochemical cycles. Considering the microbial communities’ pivotal roles in the marine ecosystem and biogeochemical cycles, it is important to understand recent changes in microbial communities and how future changes might arise under the ongoing environmental forcing of the warming and acidifying oceans.

The goal of this Research Topic was to collect studies on present and future possible changes in microbial communities with respect to environmental change and their consequences within various oceans. The topic contains 10 diverse scientific contributions on many fundamental questions related to microbial communities in oceanic environments, and report on physiological and ecological responses of microbial communities to environmental changes. The studies from a range of geographic regions were collected, from more coastal systems to open oceans, and include Tera Nova Bay in Antarctica, Mediterranean waters, the East/Japan Sea, the South China Sea, the Western Pacific Ocean, the South Pacific Ocean, and the Ross Sea of the Southern Ocean. In the context of taxonomic diversity, heterotrophic bacteria, viruses, microalga, and other prokaryotes were included in this Research Topic.

Out of the 10 works published, seven of them are focused on the phytoplankton communities, or single species of microalgae, or environmental drivers. Kim et al. describe the seasonal variability in the macromolecular composition of the sea surface in front of the Korean station in Terra Nova Bay, Ross Sea, Antarctica. They show changes in organic matter composition mainly derived by changes in phytoplankton metabolism between the productive and the non-productive season. Their study helps us to understand the effect of future climate change on the composition of organic matter derived from phytoplankton in the polar oceans. Biochemical compositions such as macromolecular and amino acids of phytoplankton in the Ross Sea, Antarctica was investigated by Jo et al.. They found distinct differences in the biochemical composition between two major bloom-forming phytoplankton groups (diatoms and Phaeocystis antarctica). They discuss how these different compositions may highlight the different strategies of these two phytoplankton communities to cope with ongoing environmental changes in the Antarctic Ocean. Kang et al. demonstrate the differences in carbon uptake rates and intracellular biochemical compositions between two different size fractions of phytoplankton to understand the ecological roles of the small phytoplankton in terms of food quantity and quality in the East/Japan Sea where the water temperature has rapidly increased. Their findings show that the increase of small phytoplankton under the warming ocean conditions could negatively affect the primary productivity and caloric content, with further consequences on the marine food webs. The photosynthetic responses to oceanic physio-chemical conditions and phytoplankton communities in the oligotrophic Western Pacific Ocean were presented by Wei et al.. Their study found that the important biotic variables influencing Fv/Fm are diatoms, Prochlorococcus, and picoeukaryotes, whilst the maximum of primary production is closely related to cyanobacteria, dinoflagellates, and Synechococcus. The detailed investigation of a chromophytic phytoplankton community using high-throughput sequencing of rbcL genes in the Western Pacific Ocean was presented by Pujari et al.. The authors found that the diversity of RuBisCO encoding rbcL gene varies with depth and across latitudes in the Western Pacific Ocean. The variation observed in chromophytic phytoplankton suggests the strong influence of environmental variables on biological production induced by oceanographic features. Thangaraj et al. investigated comprehensive proteomic profiling of diatom Skeletonema dohrnii with a change of temperature and silicate deprivation based on the iTRAQ proteomic approach, to understand the effect of the temperature and nutrient on the physiology of marine diatoms growth and photosynthesis. Their study shows that the proteome analysis for environmental stress-response of diatoms could extend our understanding for the potential impacts of climate change on the physiological adjustment to the metabolic process of phytoplankton. Sow et al. present a clear and concise description of the biogeography of Phaeocystis along a transect from the ice edge to the equator in the South Pacific Ocean, by way of high-throughput 18S rRNA gene sequencing. Their study shows that Phaeocystis could be occasionally highly abundant and diverse in the South Pacific Ocean, whereas the oceanic fronts could be the driving force for the distribution and structure of Phaeocystis assemblages in the ocean. Their work greatly expands our knowledge about the biodiversity patterns and abundances of Phaeocystis as a globally important nano-eukaryote.

Three of the 10 published works have focused on the response of viruses, prokaryotes or microbial communities to environmental stress. The response of viruses to two anthropogenic stressors (OA and eutrophication) was presented by Malits et al.. Their study demonstrates that the effect of OA on viral dynamics and viral-mediated mortality varies depending on the nutrient regime of the studied systems. It helps us to understand how viral-mediated mortality of microbes (VMMM) can be modified with environmental forcing. Another work looks into the contribution of grazers and viruses in controlling ecologically distinct prokaryotic sub-groups (i.e., high nucleic acid (HNA) and low nucleic acid (LNA) cells) along a cross-shore nutrient gradient in the northern South China Sea (Hu et al.). Their study shows how the nutrient regime influences the fate of ecologically relevant prokaryotic groups in the actual context of global warming and the anticipated oligotrophication of the future ocean. Sörenson et al. address the resilience of a marine microbial community, cultivated in an outdoor photobioreactor, when exposed to a naturally occurring seasonal stress. Differential gene expression analyses suggest that community function at warm temperatures is based on concomitant utilization of inorganic and organic carbon assigned to autotrophs and heterotrophs, while at colder temperatures, the uptake of organic carbon was performed primarily by autotrophs. Overall, the microbial community maintains a similar level of diversity and function within and across autotrophic and heterotrophic levels, confirming the cross-scale resilience theory.

The topics of the papers published in this Research Topic range from viruses, prokaryotes to phytoplankton and cover microbial communities from the various oceans. The studies confirm that the changes already occurring in ocean environments affect the metabolism and physiology of microbial communities, and further suggest that future changes will impact the physiological and ecological function or strategy of the microbial community in the marine ecosystem. Since most of these studies focus on the response of a single taxonomic population of microbes to environmental changes, our special issue highlights the need for studies to understand how ecological interactions occurring within and among the microbial community in the changing ocean will affect ecosystem structure and function. Finally, we hope that the group of papers that we have drawn together here will be a valuable addition to the accumulating observational evidence of how microbial communities are responding to the climate-related changes and consequently useful for evaluating and predicting the ongoing and future responses of marine ecosystems associated with the global climate change.

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Short-term effects of winter warming and acidification on phytoplankton growth and mortality: more losers than winners in a temperate coastal lagoon

Changes in temperature and CO2 are typically associated with climate change, but they also act on shorter time scales, leading to alterations in phytoplankton physiology and community structure. Interactions among stressors may cause synergistic or antagonistic effects on phytoplankton dynamics. Therefore, the main goal of this work is to understand the short-term isolated and interactive effects of warming and high CO2 on phytoplankton nutrient consumption, growth, production, and community structure in the Ria Formosa coastal lagoon (southern Portugal). We performed microcosm experiments with temperature and CO2 manipulation, and dilution experiments under temperature increase, using winter phytoplankton assemblages. Phytoplankton responses were evaluated using inverted and epifluorescence microscopy. Overall, phytoplankton growth and microzooplankton grazing on phytoplankton decreased with warming. Negative antagonist interactions with CO2 alleviated the negative effect of temperature on phytoplankton and cryptophytes. In contrast, higher temperature benefited smaller-sized phytoplankton, namely cyanobacteria and eukaryotic picophytoplankton. Diatom growth was not affected by temperature, probably due to nutrient limitation, but high CO2 had a positive effect on diatoms, alleviating the effect of nutrient limitation. Results suggest that this winter phytoplankton assemblage is well acclimated to ambient conditions, and short-term increases in temperature are detrimental, but can be alleviated by high CO2.

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Impact of anthropogenic pH perturbation on dimethyl sulfide cycling: a peek into the microbial black box

The objective of this study was to assess experimentally the potential impact of anthropogenic pH perturbation (ApHP) on concentrations of dimethyl sulfide (DMS) and dimethylsulfoniopropionate (DMSP), as well as processes governing the microbial cycling of sulfur compounds. A summer planktonic community from surface waters of the Lower St. Lawrence Estuary was monitored in microcosms over 12 days under three pCO2 targets: 1 × pCO2 (775 µatm), 2 × pCO2 (1,850 µatm), and 3 × pCO2 (2,700 µatm). A mixed phytoplankton bloom comprised of diatoms and unidentified flagellates developed over the course of the experiment. The magnitude and timing of biomass buildup, measured by chlorophyll a concentration, changed in the 3 × pCO2 treatment, reaching about half the peak chlorophyll a concentration measured in the 1 × pCO2 treatment, with a 2-day lag. Doubling and tripling the pCO2 resulted in a 15% and 40% decline in average concentrations of DMS compared to the control. Results from 35S-DMSPd uptake assays indicated that neither concentrations nor microbial scavenging efficiency of dissolved DMSP was affected by increased pCO2. However, our results show a reduction of the mean microbial yield of DMS by 34% and 61% in the 2 × pCO2 and 3 × pCO2 treatments, respectively. DMS concentrations correlated positively with microbial yields of DMS (Spearman’s ρ = 0.65; P < 0.001), suggesting that the impact of ApHP on concentrations of DMS in diatom-dominated systems may be strongly linked with alterations of the microbial breakdown of dissolved DMSP. Findings from this study provide further empirical evidence of the sensitivity of the microbial DMSP switch under ApHP. Because even small modifications in microbial regulatory mechanisms of DMSP can elicit changes in atmospheric chemistry via dampened efflux of DMS, results from this study may contribute to a better comprehension of Earth’s future climate.

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Positive species interactions strengthen in a high-CO2 ocean

Negative interactions among species are a major force shaping natural communities and are predicted to strengthen as climate change intensifies. Similarly, positive interactions are anticipated to intensify and could buffer the consequences of climate-driven disturbances. We used in situ experiments at volcanic CO2 vents within a temperate rocky reef to show that ocean acidification can drive community reorganization through indirect and direct positive pathways. A keystone species, the algal-farming damselfish Parma alboscapularis, enhanced primary productivity through its weeding of algae whose productivity was also boosted by elevated CO2. The accelerated primary productivity was associated with increased densities of primary consumers (herbivorous invertebrates), which indirectly supported increased secondary consumers densities (predatory fish) (i.e. strengthening of bottom-up fuelling). However, this keystone species also reduced predatory fish densities through behavioural interference, releasing invertebrate prey from predation pressure and enabling a further boost in prey densities (i.e. weakening of top-down control). We uncover a novel mechanism where a keystone herbivore mediates bottom-up and top-down processes simultaneously to boost populations of a coexisting herbivore, resulting in altered food web interactions and predator populations under future ocean acidification.

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Ocean acidification may mitigate negative effects of warming on carbon burial potential in subtidal unvegetated estuarine sediments

Estuarine sediments make an important contribution to the global carbon cycle, but we do not know how this will change under a future climate, which is expected to have lower pH oceans and frequent high-temperature days. Six combinations of warming and partial pressures of CO2 (pCO2) were chosen to investigate the combined and individual effects of short-term pressures on the diel metabolic response of shallow unvegetated sediments ex-situ. Whereas warming significantly increased respiration, making sediments more heterotrophic, high-pCO2 increased net primary productivity, resulting in less heterotrophic sediments. As a result, warming decreased the carbon burial potential of estuarine sediments and high-pCO2 had the opposite effect. High-pCO2 mitigates the negative effects of warming on benthic metabolism under the combined scenario, with carbon burial similar to that expected under high-pCO2 conditions alone. Climate scenarios also changed the diurnal pCO2 variation, with ranges increasing by 33% with warming, and almost doubling under high-pCO2 conditions. An additive response in pCO2 variability was observed under the combined scenario, increasing to 2.3× the current diel-pCO2 range, highlighting the reduced buffering capacity of the water associated with a high CO2 climate. Future carbon burial and export under increased frequencies of unseasonably warm days projected for mid and end of century (30% and 50% of days-per-year, respectively) were estimated with and without ocean acidification. By 2100, warming alone could decrease annual estuarine sediment burial potential by 25%. However, ocean acidification could mitigate the negative effects of more frequent high-temperature days and increase carbon burial potential over current conditions by ~18%.

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Global coral reef ecosystems exhibit declining calcification and increasing primary productivity

Long-term coral reef resilience to multiple stressors depends on their ability to maintain positive calcification rates. Estimates of coral ecosystem calcification and organic productivity provide insight into the environmental drivers and temporal changes in reef condition. Here, we analyse global spatiotemporal trends and drivers of coral reef calcification using a meta-analysis of ecosystem-scale case studies. A linear mixed effects regression model was used to test whether ecosystem-scale calcification is related to seasonality, methodology, calcifier cover, year, depth, wave action, latitude, duration of data collection, coral reef state, Ωar, temperature and organic productivity. Global ecosystem calcification estimated from changes in seawater carbonate chemistry was driven primarily by depth and benthic calcifier cover. Current and future declines in coral cover will significantly affect the global reef carbonate budget, even before considering the effects of sub-lethal stressors on calcification rates. Repeatedly studied reefs exhibited declining calcification of 4.3 ± 1.9% per year (x̄  = 1.8 ± 0.7 mmol m−2 d−1 yr−1), and increasing organic productivity at 3.0 ± 0.8 mmol m−2 d−1 per year since 1970. Therefore, coral reef ecosystems are experiencing a shift in their essential metabolic processes of calcification and photosynthesis, and could become net dissolving worldwide around 2054.

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