Hans-Otto Pörtner

Climate variations and the physiological basis of temperature dependent biogeography: systemic to molecular hierarchy of thermal tolerance in animals☆

The physiological mechanisms limiting and adjusting cold and heat tolerance have regained interest in the light of global warming and associated shifts in the geographical distribution of ectothermic animals. Recent comparative studies, largely carried out on marine ectotherms, indicate that the processes and limits of thermal tolerance are linked with the adjustment of aerobic scope and capacity of the whole animal as a crucial step in thermal adaptation on top of parallel adjustments at the molecular or membrane level. In accordance with Shelfords law of tolerance decreasing whole animal aerobic scope characterises the onset of thermal limitation at low and high pejus thresholds (pejus=getting worse). The drop in aerobic scope of an animal indicated by falling oxygen levels in the body fluids and or the progressively limited capacity of circulatory and ventilatory mechanisms. At high temperatures, excessive oxygen demand causes insufficient oxygen levels in the body fluids, whereas at low temperatures the aerobic capacity of mitochondria may become limiting for ventilation and circulation. Further cooling or warming beyond these limits leads to low or high critical threshold temperatures (T(c)) where aerobic scope disappears and transition to an anaerobic mode of mitochondrial metabolism and progressive insufficiency of cellular energy levels occurs. The adjustments of mitochondrial densities and their functional properties appear as a critical process in defining and shifting thermal tolerance windows. The finding of an oxygen limited thermal tolerance owing to loss of aerobic scope is in line with Taylors and Weibels concept of symmorphosis, which implies that excess capacity of any component of the oxygen delivery system is avoided. The present study suggests that the capacity of oxygen delivery is set to a level just sufficient to meet maximum oxygen demand between the average highs and lows of environmental temperatures. At more extreme temperatures only time limited passive survival is supported by anaerobic metabolism or the protection of molecular functions by heat shock proteins and antioxidative defence. As a corollary, the first line of thermal sensitivity is due to capacity limitations at a high level of organisational complexity, i.e. the integrated function of the oxygen delivery system, before individual, molecular or membrane functions become disturbed. These interpretations are in line with the more general consideration that, as a result of the high level of complexity of metazoan organisms compared with simple eukaryotes and then prokaryotes, thermal tolerance is reduced in metazoans. A similar sequence of sensitivities prevails within the metazoan organism, with the highest sensitivity at the organismic level and wider tolerance windows at lower levels of complexity. However, the situation is different in that loss in aerobic scope and progressive hypoxia at the organismic level define the onset of thermal limitation which then transfers to lower hierarchical levels and causes cellular and molecular disturbances. Oxygen limitation contributes to oxidative stress and, finally, denaturation or malfunction of molecular repair, e.g. during suspension of protein synthesis. The sequence of thermal tolerance limits turns into a hierarchy, ranging from systemic to cellular to molecular levels.

Climate change and temperature-dependent biogeography: oxygen limitation of thermal tolerance in animals

Abstract. Recent years have shown a rise in mean global temperatures and a shift in the geographical distribution of ectothermic animals. For a cause and effect analysis the present paper discusses those physiological processes limiting thermal tolerance. The lower heat tolerance in metazoa compared with unicellular eukaryotes and bacteria suggests that a complex systemic rather than molecular process is limiting in metazoa. Whole-animal aerobic scope appears as the first process limited at low and high temperatures, linked to the progressively insufficient capacity of circulation and ventilation. Oxygen levels in body fluids may decrease, reflecting excessive oxygen demand at high temperatures or insufficient aerobic capacity of mitochondria at low temperatures. Aerobic scope falls at temperatures beyond the thermal optimum and vanishes at low or high critical temperatures when transition to an anaerobic mitochondrial metabolism occurs. The adjustment of mitochondrial densities on top of parallel molecular or membrane adjustments appears crucial for maintaining aerobic scope and for shifting thermal tolerance. In conclusion, the capacity of oxygen delivery matches full aerobic scope only within the thermal optimum. At temperatures outside this range, only time-limited survival is supported by residual aerobic scope, then anaerobic metabolism and finally molecular protection by heat shock proteins and antioxidative defence. In a cause and effect hierarchy, the progressive increase in oxygen limitation at extreme temperatures may even enhance oxidative and denaturation stress. As a corollary, capacity limitations at a complex level of organisation, the oxygen delivery system, define thermal tolerance limits before molecular functions become disturbed.

Oxygen- and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems.

SUMMARY The concept of oxygen- and capacity-dependent thermal tolerance in aquatic ectotherms has successfully explained climate-induced effects of rising temperatures on species abundance in the field. Oxygen supply to tissues and the resulting aerobic performance characters thus form a primary link between organismal fitness and its role and functioning at the ecosystem level. The thermal window of performance in water breathers matches their window of aerobic scope. Loss of performance reflects the earliest level of thermal stress, caused by hypoxaemia and the progressive mismatch of oxygen supply and demand at the borders of the thermal envelope. Oxygen deficiency elicits the transition to passive tolerance and associated systemic and cellular stress signals like hormonal responses or oxidative stress as well as the use of protection mechanisms like heat shock proteins at thermal extremes. Thermal acclimatization between seasons or adaptation to a climate regime involves shifting thermal windows and adjusting window widths. The need to specialize on a limited temperature range results from temperature-dependent trade-offs at several hierarchical levels, from molecular structure to whole-organism functioning, and may also support maximized energy efficiency. Various environmental factors like CO2 (ocean acidification) and hypoxia interact with these principal relationships. Existing knowledge suggests that these factors elicit metabolic depression supporting passive tolerance to thermal extremes. However, they also exacerbate hypoxaemia, causing a narrowing of thermal performance windows and prematurely leading the organism to the limits of its thermal acclimation capacity. The conceptual analysis suggests that the relationships between energy turnover, the capacities of activity and other functions and the width of thermal windows may lead to an integrative understanding of specialization on climate and, as a thermal matrix, of sensitivity to climate change and the factors involved. Such functional relationships might also relate to climate-induced changes in species interactions and, thus, community responses at the ecosystem level.

Climate change effects on fishes and fisheries: towards a cause-and-effect understanding.

Ongoing climate change is predicted to affect individual organisms during all life stages, thereby affecting populations of a species, communities and the functioning of ecosystems. These effects of climate change can be direct, through changing water temperatures and associated phenologies, the lengths and frequency of hypoxia events, through ongoing ocean acidification trends or through shifts in hydrodynamics and in sea level. In some cases, climate interactions with a species will also, or mostly, be indirect and mediated through direct effects on key prey species which change the composition and dynamic coupling of food webs. Thus, the implications of climate change for marine fish populations can be seen to result from phenomena at four interlinked levels of biological organization: (1) organismal-level physiological changes will occur in response to changing environmental variables such as temperature, dissolved oxygen and ocean carbon dioxide levels. An integrated view of relevant effects, adaptation processes and tolerance limits is provided by the concept of oxygen and capacity-limited thermal tolerance (OCLT). (2) Individual-level behavioural changes may occur such as the avoidance of unfavourable conditions and, if possible, movement into suitable areas. (3) Population-level changes may be observed via changes in the balance between rates of mortality, growth and reproduction. This includes changes in the retention or dispersion of early life stages by ocean currents, which lead to the establishment of new populations in new areas or abandonment of traditional habitats. (4) Ecosystem-level changes in productivity and food web interactions will result from differing physiological responses by organisms at different levels of the food web. The shifts in biogeography and warming-induced biodiversity will affect species productivity and may, thus, explain changes in fisheries economies. This paper tries to establish links between various levels of biological organization by means of addressing the effective physiological principles at the cellular, tissue and whole organism levels.

Contrasting futures for ocean and society from different anthropogenic CO2 emissions scenarios

Carbon emissions and their ocean impacts Anthropogenic CO2 emissions directly affect atmospheric chemistry but also have a strong influence on the oceans. Gattuso et al. review how the physics, chemistry, and ecology of the oceans might be affected based on two CO2 emission trajectories: one business as usual and one with aggressive reductions. Ocean warming, acidification, sea-level rise, and the expansion of oxygen minimum zones will continue to have distinct impacts on marine communities and ecosystems. The path that humanity takes regarding CO2 emissions will largely determine the severity of these phenomena. Science, this issue 10.1126/science.aac4722 The amount and pace of our carbon dioxide emissions will determine how the oceans respond. BACKGROUND Although the ocean moderates anthropogenic climate change, this has great impacts on its fundamental physics and chemistry, with important consequences for ecosystems and people. Yet, despite the ocean’s critical role in regulating climate—and providing food security and livelihoods for millions of people—international climate negotiations have only minimally considered impacts on the ocean. Here, we evaluate changes to the ocean and its ecosystems, as well as to the goods and services they provide, under two contrasting CO2 scenarios: the current high-emissions trajectory (Representative Concentration Pathway 8.5, RCP8.5) and a stringent emissions scenario (RCP2.6) consistent with the Copenhagen Accord of keeping mean global temperature increase below 2°C in the 21st century. To do this, we draw on the consensus science in the latest assessment report of the Intergovernmental Panel on Climate Change and papers published since the assessment. ADVANCES Warming and acidification of surface ocean waters will increase proportionately with cumulative CO2 emissions (see figure). Warm-water corals have already been affected, as have mid-latitude seagrass, high-latitude pteropods and krill, mid-latitude bivalves, and fin fishes. Even under the stringent emissions scenario (RCP2.6), warm-water corals and mid-latitude bivalves will be at high risk by 2100. Under our current rate of emissions, most marine organisms evaluated will have very high risk of impacts by 2100 and many by 2050. These results—derived from experiments, field observations, and modeling—are consistent with evidence from high-CO2 periods in the paleorecord. Impacts to the ocean’s ecosystem services follow a parallel trajectory. Services such as coastal protection and capture fisheries are already affected by ocean warming and acidification. The risks of impacts to these services increase with continued emissions: They are predicted to remain moderate for the next 85 years for most services under stringent emission reductions, but the business-as-usual scenario (RCP8.5) would put all ecosystem services we considered at high or very high risk over the same time frame. These impacts will be cumulative or synergistic with other human impacts, such as overexploitation of living resources, habitat destruction, and pollution. Fin fisheries at low latitudes, which are a key source of protein and income for millions of people, will be at high risk. OUTLOOK Four key messages emerge. First, the ocean strongly influences the climate system and provides important services to humans. Second, impacts on key marine and coastal organisms, ecosystems, and services are already detectable, and several will face high risk of impacts well before 2100, even under the low-emissions scenario (RCP2.6). These impacts will occur across all latitudes, making this a global concern beyond the north/south divide. Third, immediate and substantial reduction of CO2 emissions is required to prevent the massive and mostly irreversible impacts on ocean ecosystems and their services that are projected with emissions greater than those in RCP2.6. Limiting emissions to this level is necessary to meet stated objectives of the United Nations Framework Convention on Climate Change; a substantially different ocean would result from any less-stringent emissions scenario. Fourth, as atmospheric CO2 increases, protection, adaptation, and repair options for the ocean become fewer and less effective. The ocean provides compelling arguments for rapid reductions in CO2 emissions and eventually atmospheric CO2 drawdown. Hence, any new global climate agreement that does not minimize the impacts on the ocean will be inadequate. Changes in ocean physics and chemistry and impacts on organisms and ecosystem services according to stringent (RCP2.6) and high business-as-usual (RCP8.5) CO2 emissions scenarios. Changes in temperature (∆T) and pH (∆pH) in 2090 to 2099 are relative to preindustrial (1870 to 1899). Sea level rise (SLR) in 2100 is relative to 1901. RCP2.6 is much more favorable to the ocean, although important ecosystems, goods, and services remain vulnerable, and allows more-efficient management options. l, m, h: low, mid-, and high latitudes, respectively. The ocean moderates anthropogenic climate change at the cost of profound alterations of its physics, chemistry, ecology, and services. Here, we evaluate and compare the risks of impacts on marine and coastal ecosystems—and the goods and services they provide—for growing cumulative carbon emissions under two contrasting emissions scenarios. The current emissions trajectory would rapidly and significantly alter many ecosystems and the associated services on which humans heavily depend. A reduced emissions scenario—consistent with the Copenhagen Accord’s goal of a global temperature increase of less than 2°C—is much more favorable to the ocean but still substantially alters important marine ecosystems and associated goods and services. The management options to address ocean impacts narrow as the ocean warms and acidifies. Consequently, any new climate regime that fails to minimize ocean impacts would be incomplete and inadequate.

Climate induced temperature effects on growth performance, fecundity and recruitment in marine fish: developing a hypothesis for cause and effect relationships in Atlantic cod (Gadus morhua) and common eelpout (Zoarces viviparus)

Effects of global warming on animal distribution and performance become visible in many marine ecosystems. The present study was designed to develop a concept for a cause and effect understanding with respect to temperature changes and to explain ecological findings based on physiological processes. The concept is based on a wide comparison of invertebrate and fish species with a special focus on recent data obtained in two model species of fish. These fish species are both characterized by northern and southern distribution limits in the North Atlantic: eelpout (Zoarces viviparus), as a typical non-migrating inhabitant of the coastal zone and the cod (Gadus morhua), as a typical inhabitant of the continental shelf with a high importance for fisheries. Mathematical modelling demonstrates a clear significant correlation between climate induced temperature fluctuations and the recruitment of cod stocks. Growth performance in cod is optimal at temperatures close to 10°C, regardless of the population investigated in a latitudinal cline. However, temperature specific growth rates decrease at higher latitudes. Also, fecundity is less in White Sea than in North and Baltic Sea cod or eelpout populations. These findings suggest that a cold-induced shift in energy budget occurs which is unfavorable for growth performance and fecundity. Thermal tolerance limits shift depending on latitude and are characterized by oxygen limitation at both low or high temperatures. Oxygen supply to tissues is optimized at low temperature by a shift in hemoglobin isoforms and oxygen binding properties to lower affinities and higher unloading potential. Protective stimulation of heat shock protein synthesis was not observed. According to a recent model of thermal tolerance the downward shift of tolerance limits during cold adaptation is associated with rising mitochondrial densities and, thus, aerobic capacity and performance in the cold, especially in eurythermal species. At the same time the costs of mitochondrial maintenance reflected by mitochondrial proton leakage should rise leaving a lower energy fraction for growth and reproduction. The preliminary conclusion can be drawn that warming will cause a northern shift of distribution limits for both species with a rise in growth performance and fecundity larger than expected from the Q10 effect in the north and lower growth or even extinction of the species in the south. Such a shift may heavily affect fishing activities in the North Sea.

Impact of Ocean Acidification on Energy Metabolism of Oyster, Crassostrea gigas—Changes in Metabolic Pathways and Thermal Response

Climate change with increasing temperature and ocean acidification (OA) poses risks for marine ecosystems. According to Pörtner and Farrell [1], synergistic effects of elevated temperature and CO2-induced OA on energy metabolism will narrow the thermal tolerance window of marine ectothermal animals. To test this hypothesis, we investigated the effect of an acute temperature rise on energy metabolism of the oyster, Crassostrea gigas chronically exposed to elevated CO2 levels (partial pressure of CO2 in the seawater ~0.15 kPa, seawater pH ~ 7.7). Within one month of incubation at elevated Pco2 and 15 °C hemolymph pH fell (pHe = 7.1 ± 0.2 (CO2-group) vs. 7.6 ± 0.1 (control)) and Peco2 values in hemolymph increased (0.5 ± 0.2 kPa (CO2-group) vs. 0.2 ± 0.04 kPa (control)). Slightly but significantly elevated bicarbonate concentrations in the hemolymph of CO2-incubated oysters ([HCO− 3]e = 1.8 ± 0.3 mM (CO2-group) vs. 1.3 ± 0.1 mM (control)) indicate only minimal regulation of extracellular acid-base status. At the acclimation temperature of 15 °C the OA-induced decrease in pHe did not lead to metabolic depression in oysters as standard metabolism rates (SMR) of CO2-exposed oysters were similar to controls. Upon acute warming SMR rose in both groups, but displayed a stronger increase in the CO2-incubated group. Investigation in isolated gill cells revealed a similar temperaturedependence of respiration between groups. Furthermore, the fraction of cellular energy demand for ion regulation via Na+/K+-ATPase was not affected by chronic hypercapnia or temperature. Metabolic profiling using 1H-NMR spectroscopy revealed substantial changes in some tissues following OA exposure at 15 °C. In mantle tissue alanine and ATP levels decreased significantly whereas an increase in succinate levels was observed in gill tissue. These findings suggest shifts in metabolic pathways following OA-exposure. Our study confirms that OA affects energy metabolism in oysters and suggests that climate change may affect populations of sessile coastal invertebrates such as mollusks.

Production of reactive oxygen species by isolated mitochondria of the Antarctic bivalve Laternula elliptica (King and Broderip) under heat stress.

Formation of reactive oxygen species (ROS) in mitochondrial isolates from gill tissues of the Antarctic polar bivalve Laternula elliptica was measured fluorimetrically under in vitro conditions. When compared to the rates measured at habitat temperature (1 degrees C), significantly elevated ROS formation was found under temperature stress of 7 degrees C and higher. ROS formation correlated significantly with oxygen consumption in individual mitochondrial preparations over the entire range of experimental temperatures (1-12 degrees C). ROS generation per mg of mitochondrial protein was significantly higher in state 3 at maximal respiration and coupling to energy conservation, than in state 4+, where ATPase-activity is inhibited by oligomycin and only proton leakage is driving the residual oxygen consumption. The percent conversion of oxygen to the membrane permeant hydrogen peroxide amounted to 3.7% (state 3) and 6.5% (state 4+) at habitat temperature (1 degrees C), and to 7% (state 3) and 7.6% (state 4+) under experimental warming to 7 degrees C. This is high compared to 1-3% oxygen to ROS conversion in mammalian mitochondrial isolates and speaks for a comparatively low control of toxic oxygen formation in mitochondria of the polar bivalve. However, low metabolic rates at cold Antarctic temperatures keep absolute rates of mitochondrial ROS production low and control oxidative stress at habitat temperatures. Mitochondrial coupling started to fall beyond 3 degrees C, closely to pejus temperature (4 degrees C) of the bivalve. Accordingly, the proportion of state 4 respiration increased from below 30% at 1 degrees C to over 50% of total oxygen consumption at 7 degrees C, entailing reduced ADP/O ratios under experimental warming. Progressive mitochondrial uncoupling and formation of hazardous ROS contribute to bias mitochondrial functioning under temperature stress in vitro. Deduced from a pejus temperature, heat stress commences already at 5 degrees C, and is linked to progressive loss of phosphorylation efficiency, increased mitochondrial oxygen demand and elevated oxidative stress above pejus temperatures.

Exposure to elevated temperatures and hydrogen peroxide elicits oxidative stress and antioxidant response in the Antarctic intertidal limpet Nacella concinna

This study deals with the occurrence of oxidative stress and antioxidant response in the Antarctic intertidal limpet Nacella concinna, as an effect of temperature increments and H2O2 exposure under controlled laboratory conditions. Experiments were designed to simulate transient conditions of increased T and:or H2O2 accumulation met by the limpets in intertidal rockpool habitats [5]. Specimens were collected at Jubany Station, South Shetland Islands, transferred to the Alfred-Wegener Institute, Bremerhaven and maintained in seawater aquaria at 0°C. Different groups of animals were acclimated at 4 and 9°C for 24‐48 h (controls at 0°C). The effect of starvation was studied at 0°C and of H2O2 exposure at 4°C. Temperature acclimation above 0°C resulted in a progressive alteration of the lysosomal compartment in digestive gland cells, as shown by cytochemical analyses (lipofuscin and neutral lipid accumulation and lysosomal membrane destabilization). Concurrently, real activities of the antioxidant enzymes superoxide dismutase (SOD) and catalase (i.e. measured at the respective experimental temperature or calculated by means of previously determined Q10 values) increased in gills and digestive gland tissues. Measurements of intracellular pH at the different temperatures showed a rise from pH 7.21 at 0°C to 7.36 at 9°C. These changes in pH are indicated to increase SOD activity by approximately 10% in both kinds of tissue at 9° as compared to 0°C. H2O2 exposure at 4°C produced physiological alterations at the systemic (lowered O2 consumption) and at the cellular levels (enhanced lysosome damage). Starvation induced lysosomal alterations in animals kept at 0°C and inhibited CAT activation under H2O2 exposure at 4°C. The complex of data suggests that when Nacella migrates to intertidal levels during the Austral Spring it experiences oxidative stress which induces an antioxidant response, which is facilitated by higher temperatures and increasing intracellular pH and the exploitation of intertidal food resources. Yet, the occurrence of cellular damage and systemic alterations shows that the limpets approach their boundaries of physiological tolerance during prolonged exposure to higher temperatures and H2O2 in intertidal habitats.

Climate change tightens a metabolic constraint on marine habitats

Double trouble It is well known that climate change will warm ocean waters, but dissolved oxygen levels also decrease as water warms. Deutsch et al. combined data on metabolism, temperature, and demographics to determine the impact of marine deoxygenation on a variety of fish and crustacean species (see the Perspective by Kleypas). Predicted climate and oxygen conditions can be expected to contract the distribution of marine fish poleward, as equatorward waters become too low in oxygen to support their energy needs. Furthermore, even the more-poleward waters will have reduced oxygen levels. Science, this issue p. 1132; see also p. 1086 Warming waters and reduced O2 will contract fish distributions poleward. [Also see Perspective by Kleypas] Warming of the oceans and consequent loss of dissolved oxygen (O2) will alter marine ecosystems, but a mechanistic framework to predict the impact of multiple stressors on viable habitat is lacking. Here, we integrate physiological, climatic, and biogeographic data to calibrate and then map a key metabolic index—the ratio of O2 supply to resting metabolic O2 demand—across geographic ranges of several marine ectotherms. These species differ in thermal and hypoxic tolerances, but their contemporary distributions are all bounded at the equatorward edge by a minimum metabolic index of ~2 to 5, indicative of a critical energetic requirement for organismal activity. The combined effects of warming and O2 loss this century are projected to reduce the upper ocean’s metabolic index by ~20% globally and by ~50% in northern high-latitude regions, forcing poleward and vertical contraction of metabolically viable habitats and species ranges.