Misconceptions of the marine biological carbon pump in a changing climate: Thinking outside the "export" box.

The marine biological carbon pump (BCP) stores carbon in the ocean interior, isolating it from exchange with the atmosphere and thereby coregulating atmospheric carbon dioxide (CO2 ). As the BCP commonly is equated with the flux of organic material to the ocean interior, termed "export flux," a change in export flux is perceived to directly impact atmospheric CO2 , and thus climate. Here, we recap how this perception contrasts with current understanding of the BCP, emphasizing the lack of a direct relationship between global export flux and atmospheric CO2 . We argue for the use of the storage of carbon of biological origin in the ocean interior as a diagnostic that directly relates to atmospheric CO2 , as a way forward to quantify the changes in the BCP in a changing climate. The diagnostic is conveniently applicable to both climate model data and increasingly available observational data. It can explain a seemingly paradoxical response under anthropogenic climate change: Despite a decrease in export flux, the BCP intensifies due to a longer reemergence time of biogenically stored carbon back to the ocean surface and thereby provides a negative feedback to increasing atmospheric CO2 . This feedback is notably small compared with anthropogenic CO2 emissions and other carbon-climate feedbacks. In this Opinion paper, we advocate for a comprehensive view of the BCP's impact on atmospheric CO2 , providing a prerequisite for assessing the effectiveness of marine CO2 removal approaches that target marine biology.

Global variability in seawater Mg:Ca and Sr:Ca ratios in the modern ocean.

Seawater Mg:Ca and Sr:Ca ratios are biogeochemical parameters reflecting the Earth-ocean-atmosphere dynamic exchange of elements. The ratios' dependence on the environment and organisms' biology facilitates their application in marine sciences. Here, we present a measured single-laboratory dataset, combined with previous data, to test the assumption of limited seawater Mg:Ca and Sr:Ca variability across marine environments globally. High variability was found in open-ocean upwelling and polar regions, shelves/neritic and river-influenced areas, where seawater Mg:Ca and Sr:Ca ratios range from ∼4.40 to 6.40 mmol:mol and ∼6.95 to 9.80 mmol:mol, respectively. Open-ocean seawater Mg:Ca is semiconservative (∼4.90 to 5.30 mol:mol), while Sr:Ca is more variable and nonconservative (∼7.70 to 8.80 mmol:mol); both ratios are nonconservative in coastal seas. Further, the Ca, Mg, and Sr elemental fluxes are connected to large total alkalinity deviations from International Association for the Physical Sciences of the Oceans (IAPSO) standard values. Because there is significant modern seawater Mg:Ca and Sr:Ca ratios variability across marine environments we cannot absolutely assume that fossil archives using taxa-specific proxies reflect true global seawater chemistry but rather taxa- and process-specific ecosystem variations, reflecting regional conditions. This variability could reconcile secular seawater Mg:Ca and Sr:Ca ratio reconstructions using different taxa and techniques by assuming an error of 1 to 1.50 mol:mol, and 1 to 1.90 mmol:mol, respectively. The modern ratios' variability is similar to the reconstructed rise over 20 Ma (Neogene Period), nurturing the question of seminonconservative behavior of Ca, Mg, and Sr over modern Earth geological history with an overlooked environmental effect.

Taking action against ocean acidification: a review of management and policy options.

Ocean acidification has emerged over the last two decades as one of the largest threats to marine organisms and ecosystems. However, most research efforts on ocean acidification have so far neglected management and related policy issues to focus instead on understanding its ecological and biogeochemical implications. This shortfall is addressed here with a systematic, international and critical review of management and policy options. In particular, we investigate the assumption that fighting acidification is mainly, but not only, about reducing CO2 emissions, and explore the leeway that this emerging problem may open in old environmental issues. We review nine types of management responses, initially grouped under four categories: preventing ocean acidification; strengthening ecosystem resilience; adapting human activities; and repairing damages. Connecting and comparing options leads to classifying them, in a qualitative way, according to their potential and feasibility. While reducing CO2 emissions is confirmed as the key action that must be taken against acidification, some of the other options appear to have the potential to buy time, e.g. by relieving the pressure of other stressors, and help marine life face unavoidable acidification. Although the existing legal basis to take action shows few gaps, policy challenges are significant: tackling them will mean succeeding in various areas of environmental management where we failed to a large extent so far.

Effects of phytoplankton physiology on global ocean biogeochemistry and climate.

The similarity of the average ratios of nitrogen (N) and phosphorus (P) in marine dissolved inorganic and particulate organic matter, dN:P and pN:P, respectively, indicates tight links between those pools in the world ocean. Here, we analyze this linkage by varying phytoplankton N and P subsistence quotas in an optimality-based ecosystem model coupled to an Earth system model. The analysis of our ensemble of simulations discloses various feedbacks between changes in the N and P quotas, N2 fixation, and denitrification that weaken the often-hypothesized tight coupling between dN:P and pN:P. We demonstrate the importance of particulate N:C and P:C ratios for regulating dN:P on the global scale, with marine oxygen level being an important control. Our analysis provides further insight into the potential interdependence of phytoplankton physiology and global climate conditions.

Sensitivities of marine carbon fluxes to ocean change.

Throughout Earth's history, the oceans have played a dominant role in the climate system through the storage and transport of heat and the exchange of water and climate-relevant gases with the atmosphere. The ocean's heat capacity is approximately 1,000 times larger than that of the atmosphere, its content of reactive carbon more than 60 times larger. Through a variety of physical, chemical, and biological processes, the ocean acts as a driver of climate variability on time scales ranging from seasonal to interannual to decadal to glacial-interglacial. The same processes will also be involved in future responses of the ocean to global change. Here we assess the responses of the seawater carbonate system and of the ocean's physical and biological carbon pumps to (i) ocean warming and the associated changes in vertical mixing and overturning circulation, and (ii) ocean acidification and carbonation. Our analysis underscores that many of these responses have the potential for significant feedback to the climate system. Because several of the underlying processes are interlinked and nonlinear, the sign and magnitude of the ocean's carbon cycle feedback to climate change is yet unknown. Understanding these processes and their sensitivities to global change will be crucial to our ability to project future climate change.

Organic Phosphorus Scavenging Supports Efficient Growth of Diazotrophic Cyanobacteria Under Phosphate Depletion.

Considering the reported significant diazotrophic activities in open-ocean regions where primary production is strongly limited by phosphate, we explored the ability of diazotrophs to use other sources of phosphorus to alleviate the phosphate depletion. We tested the actual efficiency of the open-ocean, N2-fixer Crocosphaera watsonii to grow on organic phosphorus as the sole P source, and observed how the P source affects the cellular C, N, and P composition. We obtained equivalent growth efficiencies on AMP and DL-α-glycerophosphate as compared with identical cultures grown on phosphate, and survival of the population on phytic acid. Our results show that Crocosphaera cannot use all phosphomonoesters with the same efficiency, but it can grow without phosphate, provided that usable DOP and sufficient light energy are available. Also, results point out that organic phosphorus uptake is not proportional to alkaline phosphatase activity, demonstrating that the latter is not a suitable proxy to estimate DOP-based growth yields of organisms, whether in culture experiments or in the natural environment. The growth parameters obtained, as a function of the P source, will be critical to improve and calibrate mathematical models of diazotrophic growth and the distribution of nitrogen fixation in the global ocean.

A committed fourfold increase in ocean oxygen loss.

Less than a quarter of ocean deoxygenation that will ultimately be caused by historical CO2 emissions is already realized, according to millennial-scale model simulations that assume zero CO2 emissions from year 2021 onwards. About 80% of the committed oxygen loss occurs below 2000 m depth, where a more sluggish overturning circulation will increase water residence times and accumulation of respiratory oxygen demand. According to the model results, the deep ocean will thereby lose more than 10% of its pre-industrial oxygen content even if CO2 emissions and thus global warming were stopped today. In the surface layer, however, the ongoing deoxygenation will largely stop once CO2 emissions are stopped. Accounting for the joint effects of committed oxygen loss and ocean warming, metabolic viability representative for marine animals declines by up to 25% over large regions of the deep ocean, posing an unavoidable escalation of anthropogenic pressure on deep-ocean ecosystems.

Independence of a Marine Unicellular Diazotroph to the Presence of NO3.

Marine nitrogen (N2) fixation was historically considered to be absent or reduced in nitrate (NO3-) rich environments. This is commonly attributed to the lower energetic cost of NO3- uptake compared to diazotrophy in oxic environments. This paradigm often contributes to making inferences about diazotroph distribution and activity in the ocean, and is also often used in biogeochemical ocean models. To assess the general validity of this paradigm beyond the traditionally used model organism Trichodesmium spp., we grew cultures of the unicellular cyanobacterium Crocosphaera watsonii WH8501 long term in medium containing replete concentrations of NO3-. NO3- uptake was measured in comparison to N2 fixation to assess the cultures' nitrogen source preferences. We further measured culture growth rate, cell stoichiometry, and carbon fixation rate to determine if the presence of NO3- had any effect on cell metabolism. We found that uptake of NO3- by this strain of Crocosphaera was minimal in comparison to other N sources (~2-4% of total uptake). Furthermore, availability of NO3- did not statistically alter N2 fixation rate nor any aspect of cell physiology or metabolism measured (cellular growth rate, cell stoichiometry, cell size, nitrogen fixation rate, nitrogenase activity) in comparison to a NO3- free control culture. These results demonstrate the capability of a marine diazotroph to fix nitrogen and grow independently of NO3-. This lack of sensitivity of diazotrophy to NO3- suggests that assumptions often made about, and model formulations of, N2 fixation should be reconsidered.

Can Top-Down Controls Expand the Ecological Niche of Marine N2 Fixers?

The ability of marine diazotrophs to fix dinitrogen gas (N2) is one of the most influential yet enigmatic processes in the ocean. With their activity diazotrophs support biological production by fixing about 100-200 Tg N/year and turning otherwise unavailable dinitrogen into bioavailable nitrogen (N), an essential limiting nutrient. Despite their important role, the factors that control the distribution of diazotrophs and their ability to fix N2 are not fully elucidated. We discuss insights that can be gained from the emerging picture of a wide geographical distribution of marine diazotrophs and provide a critical assessment of environmental (bottom-up) versus trophic (top-down) controls. We expand a simplified theoretical framework to understand how top-down control affects competition for resources that determine ecological niches. Selective mortality, mediated by grazing or viral-lysis, on non-fixing phytoplankton is identified as a critical process that can broaden the ability of diazotrophs to compete for resources in top-down controlled systems and explain an expanded ecological niche for diazotrophs. Our simplified analysis predicts a larger importance of top-down control on competition patterns as resource levels increase. As grazing controls the faster growing phytoplankton, coexistence of the slower growing diazotrophs can be established. However, these predictions require corroboration by experimental and field data, together with the identification of specific traits of organisms and associated trade-offs related to selective top-down control. Elucidation of these factors could greatly improve our predictive capability for patterns and rates of marine N2 fixation. The susceptibility of this key biogeochemical process to future changes may not only be determined by changes in environmental conditions but also via changes in the ecological interactions.

Loss of fixed nitrogen causes net oxygen gain in a warmer future ocean.

Oceanic anoxic events have been associated with warm climates in Earth history, and there are concerns that current ocean deoxygenation may eventually lead to anoxia. Here we show results of a multi-millennial global-warming simulation that reveal, after a transitory deoxygenation, a marine oxygen inventory 6% higher than preindustrial despite an average 3 °C ocean warming. An interior-ocean oxygen source unaccounted for in previous studies explains two thirds of the oxygen excess reached after a few thousand years. It results from enhanced denitrification replacing part of today's ocean's aerobic respiration in expanding oxygen-deficient regions: The resulting loss of fixed nitrogen is equivalent to an oceanic oxygen gain and depends on an incomplete compensation of denitrification by nitrogen fixation. Elevated total oxygen in a warmer ocean with larger oxygen-deficient regions poses a new challenge for explaining global oceanic anoxic events and calls for an improved understanding of environmental controls on nitrogen fixation.

Global Marine N2 Fixation Estimates: From Observations to Models.

Fixed nitrogen (N) limits productivity across much of the low-latitude ocean. The magnitude of its inventory results from the balance of N input and N loss, the latter largely occurring in regionally well-defined low-oxygen waters and sediments (denitrification and anammox). The rate and distribution of N input by biotic N2 fixation, the dominant N source, is not well known. Here we compile N2 fixation estimates from experimental measurements, tracer-based geochemical and modeling approaches, and discuss their limitations and uncertainties. The lack of adequate experimental data coverage and the insufficient understanding of the controls of marine N2 fixation result in high uncertainties, which make the assessment of the current N-balance a challenge. We suggest that a more comprehensive understanding of the environmental and ecological interaction of marine N2 fixers is required to advance the field toward robust N2 fixation rates estimates and predictions.

Immediate action is the best strategy when facing uncertain climate change.

Mitigating the detrimental effects of climate change is a collective problem that requires global cooperation. However, achieving cooperation is difficult since benefits are obtained in the future. The so-called collective-risk game, devised to capture dangerous climate change, showed that catastrophic economic losses promote cooperation when individuals know the timing of a single climatic event. In reality, the impact and timing of climate change is not certain; moreover, recurrent events are possible. Thus, we devise a game where the risk of a collective loss can recur across multiple rounds. We find that wait and see behavior is successful only if players know when they need to contribute to avoid danger and if contributions can eliminate the risks. In all other cases, act quickly is more successful, especially under uncertainty and the possibility of repeated losses. Furthermore, we incorporate influential factors such as wealth inequality and heterogeneity in risks. Even under inequality individuals should contribute early, as long as contributions have the potential to decrease risk. Most importantly, we find that catastrophic scenarios are not necessary to induce such immediate collective action.

The Effects of Carbon Dioxide Removal on the Carbon Cycle.

Increasing atmospheric CO2 is having detrimental effects on the Earth system. Societies have recognized that anthropogenic CO2 release must be rapidly reduced to avoid potentially catastrophic impacts. Achieving this via emissions reductions alone will be very difficult. Carbon dioxide removal (CDR) has been suggested to complement and compensate for insufficient emissions reductions, through increasing natural carbon sinks, engineering new carbon sinks, or combining natural uptake with engineered storage. Here, we review the carbon cycle responses to different CDR approaches and highlight the often-overlooked interaction and feedbacks between carbon reservoirs that ultimately determines CDR efficacy. We also identify future research that will be needed if CDR is to play a role in climate change mitigation, these include coordinated studies to better understand (i) the underlying mechanisms of each method, (ii) how they could be explicitly simulated, (iii) how reversible changes in the climate and carbon cycle are, and (iv) how to evaluate and monitor CDR.

Evaluating climate geoengineering proposals in the context of the Paris Agreement temperature goals.

Current mitigation efforts and existing future commitments are inadequate to accomplish the Paris Agreement temperature goals. In light of this, research and debate are intensifying on the possibilities of additionally employing proposed climate geoengineering technologies, either through atmospheric carbon dioxide removal or farther-reaching interventions altering the Earth's radiative energy budget. Although research indicates that several techniques may eventually have the physical potential to contribute to limiting climate change, all are in early stages of development, involve substantial uncertainties and risks, and raise ethical and governance dilemmas. Based on present knowledge, climate geoengineering techniques cannot be relied on to significantly contribute to meeting the Paris Agreement temperature goals.

Declining oxygen in the global ocean and coastal waters.

Oxygen is fundamental to life. Not only is it essential for the survival of individual animals, but it regulates global cycles of major nutrients and carbon. The oxygen content of the open ocean and coastal waters has been declining for at least the past half-century, largely because of human activities that have increased global temperatures and nutrients discharged to coastal waters. These changes have accelerated consumption of oxygen by microbial respiration, reduced solubility of oxygen in water, and reduced the rate of oxygen resupply from the atmosphere to the ocean interior, with a wide range of biological and ecological consequences. Further research is needed to understand and predict long-term, global- and regional-scale oxygen changes and their effects on marine and estuarine fisheries and ecosystems.

Ocean ventilation and deoxygenation in a warming world: introduction and overview.

Changes of ocean ventilation rates and deoxygenation are two of the less obvious but important indirect impacts expected as a result of climate change on the oceans. They are expected to occur because of (i) the effects of increased stratification on ocean circulation and hence its ventilation, due to reduced upwelling, deep-water formation and turbulent mixing, (ii) reduced oxygenation through decreased oxygen solubility at higher surface temperature, and (iii) the effects of warming on biological production, respiration and remineralization. The potential socio-economic consequences of reduced oxygen levels on fisheries and ecosystems may be far-reaching and significant. At a Royal Society Discussion Meeting convened to discuss these matters, 12 oral presentations and 23 posters were presented, covering a wide range of the physical, chemical and biological aspects of the issue. Overall, it appears that there are still considerable discrepancies between the observations and model simulations of the relevant processes. Our current understanding of both the causes and consequences of reduced oxygen in the ocean, and our ability to represent them in models are therefore inadequate, and the reasons for this remain unclear. It is too early to say whether or not the socio-economic consequences are likely to be serious. However, the consequences are ecologically, biogeochemically and climatically potentially very significant, and further research on these indirect impacts of climate change via reduced ventilation and oxygenation of the oceans should be accorded a high priority.This article is part of the themed issue 'Ocean ventilation and deoxygenation in a warming world'.

Patterns of deoxygenation: sensitivity to natural and anthropogenic drivers.

Observational estimates and numerical models both indicate a significant overall decline in marine oxygen levels over the past few decades. Spatial patterns of oxygen change, however, differ considerably between observed and modelled estimates. Particularly in the tropical thermocline that hosts open-ocean oxygen minimum zones, observations indicate a general oxygen decline, whereas most of the state-of-the-art models simulate increasing oxygen levels. Possible reasons for the apparent model-data discrepancies are examined. In order to attribute observed historical variations in oxygen levels, we here study mechanisms of changes in oxygen supply and consumption with sensitivity model simulations. Specifically, the role of equatorial jets, of lateral and diapycnal mixing processes, of changes in the wind-driven circulation and atmospheric nutrient supply, and of some poorly constrained biogeochemical processes are investigated. Predominantly wind-driven changes in the low-latitude oceanic ventilation are identified as a possible factor contributing to observed oxygen changes in the low-latitude thermocline during the past decades, while the potential role of biogeochemical processes remains difficult to constrain. We discuss implications for the attribution of observed oxygen changes to anthropogenic impacts and research priorities that may help to improve our mechanistic understanding of oxygen changes and the quality of projections into a changing future.This article is part of the themed issue 'Ocean ventilation and deoxygenation in a warming world'.