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.

Metabolic trait diversity shapes marine biogeography.

Climate and physiology shape biogeography, yet the range limits of species can rarely be ascribed to the quantitative traits of organisms1-3. Here we evaluate whether the geographical range boundaries of species coincide with ecophysiological limits to acquisition of aerobic energy4 for a global cross-section of the biodiversity of marine animals. We observe a tight correlation between the metabolic rate and the efficacy of oxygen supply, and between the temperature sensitivities of these traits, which suggests that marine animals are under strong selection for the tolerance of low O2 (hypoxia)5. The breadth of the resulting physiological tolerances of marine animals predicts a variety of geographical niches-from the tropics to high latitudes and from shallow to deep water-which better align with species distributions than do models based on either temperature or oxygen alone. For all studied species, thermal and hypoxic limits are substantially reduced by the energetic demands of ecological activity, a trait that varies similarly among marine and terrestrial taxa. Active temperature-dependent hypoxia thus links the biogeography of diverse marine species to fundamental energetic requirements that are shared across the animal kingdom.

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.

Microbial ecosystem dynamics drive fluctuating nitrogen loss in marine anoxic zones.

The dynamics of nitrogen (N) loss in the ocean's oxygen-deficient zones (ODZs) are thought to be driven by climate impacts on ocean circulation and biological productivity. Here we analyze a data-constrained model of the microbial ecosystem in an ODZ and find that species interactions drive fluctuations in local- and regional-scale rates of N loss, even in the absence of climate variability. By consuming O2 to nanomolar levels, aerobic nitrifying microbes cede their competitive advantage for scarce forms of N to anaerobic denitrifying bacteria. Because anaerobes cannot sustain their own low-O2 niche, the physical O2 supply restores competitive advantage to aerobic populations, resetting the cycle. The resulting ecosystem oscillations induce a unique geochemical signature within the ODZ-short-lived spikes of ammonium that are found in measured profiles. The microbial ecosystem dynamics also give rise to variable ratios of anammox to heterotrophic denitrification, providing a mechanism for the unexplained variability of these pathways observed in the ocean.

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'.

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.

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.

Climate-driven aerobic habitat loss in the California Current System.

Climate warming is expected to intensify hypoxia in the California Current System (CCS), threatening its diverse and productive marine ecosystem. We analyzed past regional variability and future changes in the Metabolic Index (Φ), a species-specific measure of the environment's capacity to meet temperature-dependent organismal oxygen demand. Across the traits of diverse animals, Φ exhibits strong seasonal to interdecadal variations throughout the CCS, implying that resident species already experience large fluctuations in available aerobic habitat. For a key CCS species, northern anchovy, the long-term biogeographic distribution and decadal fluctuations in abundance are both highly coherent with aerobic habitat volume. Ocean warming and oxygen loss by 2100 are projected to decrease Φ below critical levels in 30 to 50% of anchovies' present range, including complete loss of aerobic habitat-and thus likely extirpation-from the southern CCS. Aerobic habitat loss will vary widely across the traits of CCS taxa, disrupting ecological interactions throughout the region.

Temperature-dependent hypoxia explains biogeography and severity of end-Permian marine mass extinction.

Rapid climate change at the end of the Permian Period (~252 million years ago) is the hypothesized trigger for the largest mass extinction in Earth's history. We present model simulations of the Permian/Triassic climate transition that reproduce the ocean warming and oxygen (O2) loss indicated by the geologic record. The effect of these changes on animal survival is evaluated using the Metabolic Index (Φ), a measure of scope for aerobic activity governed by organismal traits sampled in diverse modern species. Modeled loss of aerobic habitat predicts lower extinction intensity in the tropics, a pattern confirmed with a spatially explicit analysis of the marine fossil record. The combined physiological stresses of ocean warming and O2 loss can account for more than half the magnitude of the "Great Dying."