Cross-shore transport and eddies promote large scale response to urban eutrophication.

A key control on the magnitude of coastal eutrophication is the degree to which currents quickly transport nitrogen derived from human sources away from the coast to the open ocean before eutrophication develops. In the Southern California Bight (SCB), an upwelling-dominated eastern boundary current ecosystem, anthropogenic nitrogen inputs increase algal productivity and cause subsurface acidification and oxygen (O 2 ) loss along the coast. However, the extent of anthropogenic influence on eutrophication beyond the coastal band, and the physical transport mechanisms and biogeochemical processes responsible for these effects are still poorly understood. Here, we use a submesoscale-resolving numerical model to document the detailed biogeochemical mass balance of nitrogen, carbon and oxygen, their physical transport, and effects on offshore habitats. Despite management of terrestrial nutrients that has occurred in the region over the last 20 years, coastal eutrophication continues to persist. The input of anthropogenic nutrients promote an increase in productivity, remineralization and respiration offshore, with recurrent O 2 loss and pH decline in a region located 30-90 km from the mainland. During 2013 to 2017, the spatially averaged 5-year loss rate across the Bight was 1.3 mmol m - 3 O 2 , with some locations losing on average up to 14.2 mmol m - 3 O 2 . The magnitude of loss is greater than model uncertainty assessed from data-model comparisons and from quantification of intrinsic variability. This phenomenon persists for 4 to 6 months of the year over an area of 278,40 km 2 ( ∼ 30% of SCB area). These recurrent features of acidification and oxygen loss are associated with cross-shore transport of nutrients by eddies and plankton biomass and their accumulation and retention within persistent eddies offshore within the SCB.

Oxygen rise in the tropical upper ocean during the Paleocene-Eocene Thermal Maximum.

The global ocean's oxygen inventory is declining in response to global warming, but the future of the low-oxygen tropics is uncertain. We report new evidence for tropical oxygenation during the Paleocene-Eocene Thermal Maximum (PETM), a warming event that serves as a geologic analog to anthropogenic warming. Foraminifera-bound nitrogen isotopes indicate that the tropical North Pacific oxygen-deficient zone contracted during the PETM. A concomitant increase in foraminifera size implies that oxygen availability rose in the shallow subsurface throughout the tropical North Pacific. These changes are consistent with ocean model simulations of warming, in which a decline in biological productivity allows tropical subsurface oxygen to rise even as global ocean oxygen declines. The tropical oxygen increase may have helped avoid a mass extinction during the PETM.

Projecting global biological N2 fixation under climate warming across land and ocean.

Biological N2 fixation sustains the global inventory of nitrogenous nutrients essential for the productivity of terrestrial and marine ecosystems. Like most metabolic processes, rates of biological N2 fixation vary strongly with temperature, making it sensitive to climate change, but a global projection across land and ocean is lacking. Here we use compilations of field and laboratory measurements to reveal a relationship between N2 fixation rates and temperature that is similar in both domains despite large taxonomic and environmental differences. Rates of N2 fixation increase gradually to a thermal optimum around ~25°C, and decline more rapidly toward a thermal maximum, which is lower in the ocean than on land. In both realms, the observed temperature sensitivities imply that climate warming this century could decrease N2 fixation rates by ~50% in the tropics while increasing rates by ~50% in higher latitudes. We propose a conceptual framework for understanding the physiological and ecological mechanisms that underpin and modulate the observed temperature dependence of global N2 fixation rates, facilitating cross-fertilization of marine and terrestrial research to assess its response to climate change.

Thermal optima in the hypoxia tolerance of marine ectotherms: Physiological causes and biogeographic consequences.

The minimum O2 needed to fuel the demand of aquatic animals is commonly observed to increase with temperature, driven by accelerating metabolism. However, recent measurements of critical O2 thresholds ("Pcrit") reveal more complex patterns, including those with a minimum at an intermediate thermal "optimum". To discern the prevalence, physiological drivers, and biogeographic manifestations of such curves, we analyze new experimental and biogeographic data using a general dynamic model of aquatic water breathers. The model simulates the transfer of oxygen from ambient water through a boundary layer and into animal tissues driven by temperature-dependent rates of metabolism, diffusive gas exchange, and ventilatory and circulatory systems with O2-protein binding. We find that a thermal optimum in Pcrit can arise even when all physiological rates increase steadily with temperature. This occurs when O2 supply at low temperatures is limited by a process that is more temperature sensitive than metabolism, but becomes limited by a less sensitive process at warmer temperatures. Analysis of published species respiratory traits suggests that this scenario is not uncommon in marine biota, with ventilation and circulation limiting supply under cold conditions and diffusion limiting supply at high temperatures. Using occurrence data, we show that species with these physiological traits inhabit lowest O2 waters near the optimal temperature for hypoxia tolerance and are restricted to higher O2 at temperatures above and below this optimum. Our results imply that hypoxia tolerance can decline under both cold and warm conditions and thus may influence both poleward and equatorward species range limits.

Geographical and taxonomic patterns in aerobic traits of marine ectotherms.

The metabolism and hypoxia tolerance of marine ectotherms play key roles in limiting species geographical ranges, but underlying traits have only been directly measured for a small fraction of biodiversity. Here we diagnose and analyse spatial and phylogenetic patterns in hypoxia tolerance and its temperature sensitivity at ecologically active metabolic rates, by combining a model of organismal oxygen (O2) balance with global climate and biogeographic data for approximately 25 000 animal species from 13 phyla. Large-scale spatial trait patterns reveal that active hypoxia tolerance is greater and less temperature sensitive among tropical species compared to polar ones, consistent with sparse experimental data. Species energetic demands for activity vary less with temperature than resting costs, an inference confirmed by available rate measurements. Across the tree of life, closely related species share similar hypoxia traits, indicating that evolutionary history shapes physiological tolerances to O2 and temperature. Trait frequencies are highly conserved across phyla, suggesting the breadth of global aerobic conditions selects for convergent trait diversity. Our results support aerobic limitation as a constraint on marine habitat distributions and their responses to climate change and highlight the under-sampling of aerobic traits among species living in the ocean's tropical and polar oxythermal extremes. This article is part of the theme issue 'The evolutionary significance of variation in metabolic rates'.

Skillful multiyear prediction of marine habitat shifts jointly constrained by ocean temperature and dissolved oxygen.

The ability to anticipate marine habitat shifts responding to climate variability has high scientific and socioeconomic value. Here we quantify interannual-to-decadal predictability of habitat shifts by combining trait-based aerobic habitat constraints with a suite of initialized retrospective Earth System Model forecasts, for diverse marine ecotypes in the North American Large Marine Ecosystems. We find that aerobic habitat viability, defined by joint constraints of temperature and oxygen on organismal energy balance, is potentially predictable in the upper-600 m ocean, showing a substantial improvement over a simple persistence forecast. The skillful multiyear predictability is dominated by the oxygen component in most ecosystems, yielding higher predictability than previously estimated based on temperature alone. Notable predictability differences exist among ecotypes differing in temperature sensitivity of hypoxia vulnerability, especially along the northeast coast with predictability timescale ranging from 2 to 10 years. This tool will be critical in predicting marine habitat shifts in face of a changing climate.

Climate, Oxygen, and the Future of Marine Biodiversity.

The ocean enabled the diversification of life on Earth by adding O2 to the atmosphere, yet marine species remain most subject to O2 limitation. Human industrialization is intensifying the aerobic challenges to marine ecosystems by depleting the ocean's O2 inventory through the global addition of heat and local addition of nutrients. Historical observations reveal an ∼2% decline in upper-ocean O2 and accelerating reports of coastal mass mortality events. The dynamic balance of O2 supply and demand provides a unifying framework for understanding these phenomena across scales from the global ocean to individual organisms. Using this framework, we synthesize recent advances in forecasting O2 loss and its impacts on marine biogeography, biodiversity, and biogeochemistry. We also highlight three outstanding uncertainties: how long-term global climate change intensifies ocean weather events in which simultaneous heat and hypoxia create metabolic storms, how differential species O2 sensitivities alter the structure of ecological communities, and how global O2 loss intersects with coastal eutrophication. Projecting these interacting impacts on future marine ecosystems requires integration of climate dynamics, biogeochemistry, physiology, and ecology, evaluated with an eye on Earth history. Reducing global and local impacts of warming and O2 loss will be essential if humankind is to preserve the health and biodiversity of the future ocean.

Facial dysmorphology in children exposed in pregnancy to anticonvulsant medications correlates with deficits in IQ.

Some children exposed at conception to the antiepileptic drugs (AEDs) phenytoin (PHT), phenobarbital (PB), and carbamazepine (CBZ) have changes in their midface and fingers. It has been suggested that the anticonvulsant-exposed child with these subtle changes in facial features (the "anticonvulsant face") has a greater likelihood of having deficits in IQ in comparison with children exposed to the same anticonvulsants who do not have these features. 115 AED-exposed children (40, PHT; 34, PB; and 41, CBZ) between 6.5 and 16 years of age and 111 unexposed children matched by sex, race, and year in school were evaluated. The evaluations were (WISC-III), physical examination with measurements of facial features and digits and photographs. The AED-exposed children had cephalometric radiographs, but not the unexposed. Each parent had a similar examination of face and hands plus tests of intelligence. These AED-exposed children showed an increased frequency of a short nose and anteverted nares, features of the "anticonvulsant face." Lateral skull radiographs showed a decrease in the angle between the anterior cranial base and nasal bone, which produces anteverted nares. Mean IQs were significantly lower on one or more IQ measures for the children with these facial features. Shortening of the distal phalanges and small fingernails correlated with the presence of a short nose in that child. The findings in 115 children exposed at conception to either phenytoin, phenobarbital, or carbamazepine, as monotherapy, confirmed the hypothesis that those with a short nose and anteverted nares had a lower IQ than exposed children without those features.

Coexistence of Dominant Marine Phytoplankton Sustained by Nutrient Specialization.

Prochlorococcus and Synechococcus are the two dominant picocyanobacteria in the low-nutrient surface waters of the subtropical ocean, but the basis for their coexistence has not been quantitatively demonstrated. Here, we combine in situ microcosm experiments and an ecological model to show that this coexistence can be sustained by specialization in the uptake of distinct nitrogen (N) substrates at low-level concentrations that prevail in subtropical environments. In field incubations, the response of both Prochlorococcus and Synechococcus to nanomolar N amendments demonstrates N limitation of growth in both populations. However, Prochlorococcus showed a higher affinity to ammonium, whereas Synechococcus was more adapted to nitrate uptake. A simple ecological model demonstrates that the differential nutrient preference inferred from field experiments with these genera may sustain their coexistence. It also predicts that as the supply of NO3- decreases, as expected under climate warming, the dominant genera should undergo a nonlinear shift from Synechococcus to Prochlorococcus, a pattern that is supported by subtropical field observations. Our study suggests that the evolution of differential nutrient affinities is an important mechanism for sustaining the coexistence of genera and that climate change is likely to shift the relative abundance of the dominant plankton genera in the largest biomes in the ocean. IMPORTANCE Our manuscript addresses the following fundamental question in microbial ecology: how do different plankton using the same essential nutrients coexist? Prochlorococcus and Synechococcus are the two dominant picocyanobacteria in the low-nutrient surface waters of the subtropical ocean, which support a significant amount of marine primary production. The geographical distributions of these two organisms are largely overlapping, but the basis for their coexistence in these biomes remains unclear. In this study, we combined in situ microcosm experiments and an ecosystem model to show that the coexistence of these two organisms can arise from specialization in the uptake of distinct nitrogen substrates; Prochlorococcus prefers ammonium, whereas Synechococcus prefers nitrate when these nutrients exist at low concentrations. Our framework can be used for simulating and predicting the coexistence in the future ocean and may provide hints toward understanding other similar types of coexistence.

Oxygen availability and body mass modulate ectotherm responses to ocean warming.

In an ocean that is rapidly warming and losing oxygen, accurate forecasting of species' responses must consider how this environmental change affects fundamental aspects of their physiology. Here, we develop an absolute metabolic index (ΦA) that quantifies how ocean temperature, dissolved oxygen and organismal mass interact to constrain the total oxygen budget an organism can use to fuel sustainable levels of aerobic metabolism. We calibrate species-specific parameters of ΦA with physiological measurements for red abalone (Haliotis rufescens) and purple urchin (Strongylocentrotus purpuratus). ΦA models highlight that the temperature where oxygen supply is greatest shifts cooler when water loses oxygen or organisms grow larger, providing a mechanistic explanation for observed thermal preference patterns. Viable habitat forecasts are disproportionally deleterious for red abalone, revealing how species-specific physiologies modulate the intensity of a common climate signal, captured in the newly developed ΦA framework.

High Growth Rate of Diatoms Explained by Reduced Carbon Requirement and Low Energy Cost of Silica Deposition.

The rapid growth of diatoms makes them one of the most pervasive and productive types of plankton in the world's ocean, but the physiological basis for their high growth rates remains poorly understood. Here, we evaluate the factors that elevate diatom growth rates, relative to other plankton, using a steady-state metabolic flux model that computes the photosynthetic C source from intracellular light attenuation and the carbon cost of growth from empirical cell C quotas, across a wide range of cell sizes. For both diatoms and other phytoplankton, growth rates decline with increased cell volume, consistent with observations, because the C cost of division increases with size faster than photosynthesis. However, the model predicts overall higher growth rates for diatoms due to reduced C requirements and the low energetic cost of Si deposition. The C savings from the silica frustule are supported by metatranscriptomic data from Tara Oceans, which show that the abundance of transcripts for cytoskeleton components in diatoms is lower than in other phytoplankton. Our results highlight the importance of understanding the origins of phylogenetic differences in cellular C quotas, and suggest that the evolution of silica frustules may play a critical role in the global dominance of marine diatoms. IMPORTANCE This study addresses a longstanding issue regarding diatoms, namely, their fast growth. Diatoms, which broadly are phytoplankton with silica frustules, are the world's most productive microorganisms and dominate in polar and upwelling regions. Their dominance is largely supported by their high growth rate, but the physiological reasoning behind that characteristic has been obscure. In this study, we combine a quantitative model and metatranscriptomic approaches and show that diatoms' low carbon requirements and low energy costs for silica frustule production are the key factors supporting their fast growth. Our study suggests that the effective use of energy-efficient silica as a cellular structure, instead of carbon, enables diatoms to be the most productive organisms in the global ocean.

Global patterns in marine organic matter stoichiometry driven by phytoplankton ecophysiology.

The proportion of major elements in marine organic matter links cellular processes to global nutrient, oxygen and carbon cycles. Differences in the C:N:P ratios of organic matter have been observed between ocean biomes, but these patterns have yet to be quantified from the underlying small-scale physiological and ecological processes. Here we use an ecosystem model that includes adaptive resource allocation within and between ecologically distinct plankton size classes to attribute the causes of global patterns in the C:N:P ratios. We find that patterns of N:C variation are largely driven by common physiological adjustment strategies across all phytoplankton, while patterns of N:P are driven by ecological selection for taxonomic groups with different phosphorus storage capacities. Although N:C varies widely due to cellular adjustment to light and nutrients, its latitudinal gradient is modest because of depth-dependent trade-offs between nutrient and light availability. Strong latitudinal variation in N:P reflects an ecological balance favouring small plankton with lower P storage capacity in the subtropics, and larger eukaryotes with a higher cellular P storage capacity in nutrient-rich high latitudes. A weaker N:P difference between southern and northern hemispheres, and between the Atlantic and Pacific oceans, reflects differences in phosphate available for cellular storage. Despite simulating only two phytoplankton size classes, the emergent global variability of elemental ratios resembles that of all measured species, suggesting that the range of growth conditions and ecological selection sustain the observed diversity of stoichiometry among phytoplankton.

The origin of carbonate mud and implications for global climate.

Carbonate mud represents one of the most important geochemical archives for reconstructing ancient climatic, environmental, and evolutionary change from the rock record. Mud also represents a major sink in the global carbon cycle. Yet, there remains no consensus about how and where carbonate mud is formed. Here, we present stable isotope and trace-element data from carbonate constituents in the Bahamas, including ooids, corals, foraminifera, and algae. We use geochemical fingerprinting to demonstrate that carbonate mud cannot be sourced from the abrasion and mixture of any combination of these macroscopic grains. Instead, an inverse Bayesian mixing model requires the presence of an additional aragonite source. We posit that this source represents a direct seawater precipitate. We use geological and geochemical data to show that "whitings" are unlikely to be the dominant source of this precipitate and, instead, present a model for mud precipitation on the bank margins that can explain the geographical distribution, clumped-isotope thermometry, and stable isotope signature of carbonate mud. Next, we address the enigma of why mud and ooids are so abundant in the Bahamas, yet so rare in the rest of the world: Mediterranean outflow feeds the Bahamas with the most alkaline waters in the modern ocean (>99.7th-percentile). Such high alkalinity appears to be a prerequisite for the nonskeletal carbonate factory because, when Mediterranean outflow was reduced in the Miocene, Bahamian carbonate export ceased for 3-million-years. Finally, we show how shutting off and turning on the shallow carbonate factory can send ripples through the global climate system.

Biological sensitivities to high-resolution climate change projections in the California current marine ecosystem.

The California Current Marine Ecosystem is a highly productive system that exhibits strong natural variability and vulnerability to anthropogenic climate trends. Relating projections of ocean change to biological sensitivities requires detailed synthesis of experimental results. Here, we combine measured biological sensitivities with high-resolution climate projections of key variables (temperature, oxygen, and pCO2 ) to identify the direction, magnitude, and spatial distribution of organism-scale vulnerabilities to multiple axes of projected ocean change. Among 12 selected species of cultural and economic importance, we find that all are sensitive to projected changes in ocean conditions through responses that affect individual performance or population processes. Response indices were largest in the northern region and inner shelf. While performance traits generally increased with projected changes, fitness traits generally decreased, indicating that concurrent stresses can lead to fitness loss. For two species, combining sensitivities to temperature and oxygen changes through the Metabolic Index shows how aerobic habitat availability could be compressed under future conditions. Our results suggest substantial and specific ecological susceptibility in the next 80 years, including potential regional loss of canopy-forming kelp, changes in nearshore food webs caused by declining rates of survival among red urchins, Dungeness crab, and razor clams, and loss of aerobic habitat for anchovy and pink shrimp. We also highlight fillable gaps in knowledge, including specific physiological responses to stressors, variation in responses across life stages, and responses to multistressor combinations. These findings strengthen the case for filling information gaps with experiments focused on fitness-related responses and those that can be used to parameterize integrative physiological models, and suggest that the CCME is susceptible to substantial changes to ecosystem structure and function within this century.

Impact of warming on aquatic body sizes explained by metabolic scaling from microbes to macrofauna.

Rising temperatures are associated with reduced body size in many marine species, but the biological cause and generality of the phenomenon is debated. We derive a predictive model for body size responses to temperature and oxygen (O2) changes based on thermal and geometric constraints on organismal O2 supply and demand across the size spectrum. The model reproduces three key aspects of the observed patterns of intergenerational size reductions measured in laboratory warming experiments of diverse aquatic ectotherms (i.e., the "temperature-size rule" [TSR]). First, the interspecific mean and variability of the TSR is predicted from species' temperature sensitivities of hypoxia tolerance, whose nonlinearity with temperature also explains the second TSR pattern-its amplification as temperatures rise. Third, as body size increases across the tree of life, the impact of growth on O2 demand declines while its benefit to O2 supply rises, decreasing the size dependence of hypoxia tolerance and requiring larger animals to contract by a larger fraction to compensate for a thermally driven rise in metabolism. Together our results support O2 limitation as the mechanism underlying the TSR, and they provide a physiological basis for projecting ectotherm body size responses to climate change from microbes to macrofauna. For small species unable to rapidly migrate or evolve greater hypoxia tolerance, ocean warming and O2 loss in this century are projected to induce >20% reductions in body mass. Size reductions at higher trophic levels could be even stronger and more variable, compounding the direct impact of human harvesting on size-structured ocean food webs.

Avoiding ocean mass extinction from climate warming.

Global warming threatens marine biota with losses of unknown severity. Here, we quantify global and local extinction risks in the ocean across a range of climate futures on the basis of the ecophysiological limits of diverse animal species and calibration against the fossil record. With accelerating greenhouse gas emissions, species losses from warming and oxygen depletion alone become comparable to current direct human impacts within a century and culminate in a mass extinction rivaling those in Earth's past. Polar species are at highest risk of extinction, but local biological richness declines more in the tropics. Reversing greenhouse gas emissions trends would diminish extinction risks by more than 70%, preserving marine biodiversity accumulated over the past ~50 million years of evolutionary history.

Paleobiology provides glimpses of future ocean.

Fossil records from tropical oceans predict biodiversity loss in a warmer world.