Click
here to close Hello! We notice that
you are using Internet Explorer, which is not supported by Echinobase
and may cause the site to display incorrectly. We suggest using a
current version of Chrome,
FireFox,
or Safari.
Nat Commun
2023 Jun 27;141:3811. doi: 10.1038/s41467-023-39438-w.
Show Gene links
Show Anatomy links
Oxygen availability and body mass modulate ectotherm responses to ocean warming.
Duncan MI
,
Micheli F
,
Boag TH
,
Marquez JA
,
Deres H
,
Deutsch CA
,
Sperling EA
.
???displayArticle.abstract???
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.
Fig. 1. Shape of thermal relationships for different expressions of an organism’s oxygen balance in saturated water.A When the balance between oxygen supply (S) and basal demand (D) is expressed as a ratio (Solid black line), no clear temperature peak is identified if supply is a single monotonic function of temperature and only a single thermal limit can be identified (star). Note that the relationship between supply and temperature may not always be monotonic with temperature27, 29, 30. Thermal optima (lowest PO2crit) arise from the multi-step nature of O2 supply, which can be readily reproduced by the factorial form of the metabolic index30, but both the absolute and factorial forms shown here assume a single temperature-dependent supply function. B The same data expressed as the difference between S and D (solid black line) often yields a thermal peak and both warm and cold thermal limits can be estimated (stars). When additional energetic processes are performed the available oxygen balance decreases (red lines) in A and B. If these energetic processes are vital for performance a species’ thermal limits are defined as those temperatures where oxygen supply falls to match elevated oxygen demand (equal to a value of one in A and zero in B).The oxygen requirement of these additional processes can be quantified and removed from the total oxygen budget in B but must be measured in relation to demand in A, which is challenging if thermal sensitivities differ (i.e. additional energetic process does not equal 1.5 x basal demand across whole temperature range).
Fig. 2. The influence of oxygen availability (PO2, kPa) on oxygen supply (S) at a single temperature.A When oxygen availability is high, supply (S) is not constrained, and potential to consume excess oxygen is maximized (yellow area). As environmental oxygen decreases below PO2crit max, oxygen supply is limited at a rate equal to the oxygen supply capacity (αS) and potential for excess oxygen consumption is constrained (orange area). When oxygen supply (S) equals demand (D) the critical oxygen partial pressure (PO2crit) is reached, below which there is a deficit of oxygen required to fuel basal demand (red area). B Shape of oxygen limitation relationships when αS is constant (linear thick black line) or variable (non-linear blue line) yet PO2crit and PO2crit max are identical.
Fig. 3. Physiological measurements.Oxygen demand taken as standard metabolic rate (SMR; a, b) and critical oxygen partial pressure (PO2crit; c, d) data for the purple sea urchin, S. purpuratus (purple points) and red abalone, H. rufescens (red points) across experimental temperatures. Solid lines represent best fit Arrhenius models for SMR (a, b) and PO2crit fit with a quadratic (c) or exponential (d) model for S. purpuratus and H. rufescens, respectively. Models are illustrated for two different size classes corresponding to the smallest and largest wet weight (g) of experimental specimens. Source data are provided as a Source Data file.
Fig. 4. ΦA predictions across temperature-oxygen space.ΦA model predictions (viridis color scale) for S. purpuratus (a) and H. rufescens (b) across a temperature and oxygen state-space. ΦA values correspond to the median size (wet mass) of experimental organisms (S. purpuratus = 67.5 g, H. rufescens = 37.5 g), white lines are ΦA contours, and red points correspond to experimental PO2crit measurements where ΦA = zero. Source data are provided as a Source Data file.
Fig. 5. Variable optimum temperatures.Effect of oxygen availability (a, b) and mass (c, d) on the optimal temperature predictions from normalized absolute metabolic index (ΦA’) models for S. purpuratus (purple) and H. rufescens (red). Source data are provided as a Source Data file.
Fig. 6. ΦA’ explains metabolic niche.OBIS geo-referenced occurrences (black points) for S. purpuratus (a) and H. rufescens (b) matched with corresponding temperature and oxygen conditions from the ROMS ocean model and layered over ΦA’ predictions across the temperature-oxygen state-space (viridis colors). Source data are provided as a Source Data file.
Fig. 7. Spatial modelling.Spatial predictions of contemporary (1995–2010, a, b) and future (2071–2100 under the RCP 8.5 emissions scenario, c, d) viable habitat for S. purpuratus (purple) and H. rufescens (red) derived by classifying the minimum normalized ΦA value for each cell as suitable above a 0.849 threshold for S. purpuratus and 0.928 threshold for H. rufescens (inserts). Dashed lines delimit core continuous distribution predictions. Note that the future distribution of H. rufescens is hard to visualize at this large spatial scale because it loses habitat at depth and hugs the coastline closely.
Audzijonyte,
Fish body sizes change with temperature but not all species shrink with warming.
2020, Pubmed
Audzijonyte,
Fish body sizes change with temperature but not all species shrink with warming.
2020,
Pubmed
Boag,
Oxygen, temperature and the deep-marine stenothermal cradle of Ediacaran evolution.
2018,
Pubmed
Braid,
Health and survival of red abalone, Haliotis rufescens, under varying temperature, food supply, and exposure to the agent of withering syndrome.
2005,
Pubmed
Breitburg,
Declining oxygen in the global ocean and coastal waters.
2018,
Pubmed
Brijs,
Experimental manipulations of tissue oxygen supply do not affect warming tolerance of European perch.
2015,
Pubmed
Christensen,
The combined effect of body size and temperature on oxygen consumption rates and the size-dependency of preferred temperature in European perch Perca fluviatilis.
2020,
Pubmed
Claireaux,
Responses by fishes to environmental hypoxia: integration through Fry's concept of aerobic metabolic scope.
2016,
Pubmed
Clark,
Aerobic scope measurements of fishes in an era of climate change: respirometry, relevance and recommendations.
2013,
Pubmed
Clarke,
Energy Flow in Growth and Production.
2019,
Pubmed
Deutsch,
Ecophysiology. Climate change tightens a metabolic constraint on marine habitats.
2015,
Pubmed
Deutsch,
Metabolic trait diversity shapes marine biogeography.
2020,
Pubmed
Duncan,
Oxygen availability and body mass modulate ectotherm responses to ocean warming.
2023,
Pubmed
,
Echinobase
Duncan,
Different drivers, common mechanism; the distribution of a reef fish is restricted by local-scale oxygen and temperature constraints on aerobic metabolism.
2020,
Pubmed
Enders,
Hypoxia but not shy-bold phenotype mediates thermal preferences in a threatened freshwater fish, Notropis percobromus.
2019,
Pubmed
Ern,
A mechanistic oxygen- and temperature-limited metabolic niche framework.
2019,
Pubmed
Esbaugh,
Is hypoxia vulnerability in fishes a by-product of maximum metabolic rate?
2021,
Pubmed
Gillooly,
Effects of size and temperature on metabolic rate.
2001,
Pubmed
Gräns,
Aerobic scope fails to explain the detrimental effects on growth resulting from warming and elevated CO2 in Atlantic halibut.
2014,
Pubmed
Hoegh-Guldberg,
The impact of climate change on the world's marine ecosystems.
2010,
Pubmed
Howard,
Climate-driven aerobic habitat loss in the California Current System.
2020,
Pubmed
Jutfelt,
Oxygen- and capacity-limited thermal tolerance: blurring ecology and physiology.
2018,
Pubmed
Killen,
Guidelines for reporting methods to estimate metabolic rates by aquatic intermittent-flow respirometry.
2021,
Pubmed
Lindmark,
Optimum growth temperature declines with body size within fish species.
2022,
Pubmed
McKenzie,
Conservation physiology of marine fishes: state of the art and prospects for policy.
2016,
Pubmed
Meyer-Gutbrod,
Moving on up: Vertical distribution shifts in rocky reef fish species during climate-driven decline in dissolved oxygen from 1995 to 2009.
2021,
Pubmed
Monaco,
Dietary generalism accelerates arrival and persistence of coral-reef fishes in their novel ranges under climate change.
2020,
Pubmed
Moore,
Health and survival of red abalone Haliotis rufescens from San Miguel Island, California, USA, in a laboratory simulation of La Niña and El Niño conditions.
2011,
Pubmed
Nelson,
Oxygen consumption rate v. rate of energy utilization of fishes: a comparison and brief history of the two measurements.
2016,
Pubmed
Nilsson,
Does size matter for hypoxia tolerance in fish?
2008,
Pubmed
Norin,
Aerobic scope does not predict the performance of a tropical eurythermal fish at elevated temperatures.
2014,
Pubmed
Oliver,
Longer and more frequent marine heatwaves over the past century.
2018,
Pubmed
Pan,
Acclimation to prolonged hypoxia alters hemoglobin isoform expression and increases hemoglobin oxygen affinity and aerobic performance in a marine fish.
2017,
Pubmed
Pante,
marmap: A package for importing, plotting and analyzing bathymetric and topographic data in R.
2013,
Pubmed
Pecl,
Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being.
2017,
Pubmed
Penn,
Avoiding ocean mass extinction from climate warming.
2022,
Pubmed
Penn,
Temperature-dependent hypoxia explains biogeography and severity of end-Permian marine mass extinction.
2018,
Pubmed
Pinsky,
Climate-Driven Shifts in Marine Species Ranges: Scaling from Organisms to Communities.
2020,
Pubmed
Pörtner,
Climate change affects marine fishes through the oxygen limitation of thermal tolerance.
2007,
Pubmed
Rogers-Bennett,
Marine heat wave and multiple stressors tip bull kelp forest to sea urchin barrens.
2019,
Pubmed
,
Echinobase
Rubalcaba,
Oxygen limitation may affect the temperature and size dependence of metabolism in aquatic ectotherms.
2020,
Pubmed
Schulte,
Thermal performance curves, phenotypic plasticity, and the time scales of temperature exposure.
2011,
Pubmed
Schulte,
The effects of temperature on aerobic metabolism: towards a mechanistic understanding of the responses of ectotherms to a changing environment.
2015,
Pubmed
Seebacher,
Determining environmental causes of biological effects: the need for a mechanistic physiological dimension in conservation biology.
2012,
Pubmed
Seibel,
Oxygen supply capacity breathes new life into critical oxygen partial pressure (Pcrit).
2021,
Pubmed
Seibel,
Oxygen supply capacity in animals evolves to meet maximum demand at the current oxygen partial pressure regardless of size or temperature.
2020,
Pubmed
Svendsen,
Design and setup of intermittent-flow respirometry system for aquatic organisms.
2016,
Pubmed
Tigchelaar,
Compound climate risks threaten aquatic food system benefits.
2021,
Pubmed
Ultsch,
The utility and determination of Pcrit in fishes.
2019,
Pubmed
Verberk,
Oxygen supply in aquatic ectotherms: partial pressure and solubility together explain biodiversity and size patterns.
2011,
Pubmed
Verberk,
Can respiratory physiology predict thermal niches?
2016,
Pubmed
Verberk,
Shrinking body sizes in response to warming: explanations for the temperature-size rule with special emphasis on the role of oxygen.
2021,
Pubmed
Verberk,
Does oxygen limit thermal tolerance in arthropods? A critical review of current evidence.
2016,
Pubmed
Wishner,
Ocean deoxygenation and zooplankton: Very small oxygen differences matter.
2018,
Pubmed
Wisz,
The role of biotic interactions in shaping distributions and realised assemblages of species: implications for species distribution modelling.
2013,
Pubmed
Wood,
The fallacy of the Pcrit - are there more useful alternatives?
2018,
Pubmed
Zhang,
Hypoxia Performance Curve: Assess a Whole-Organism Metabolic Shift from a Maximum Aerobic Capacity towards a Glycolytic Capacity in Fish.
2021,
Pubmed
