Oxygen Limitation Of Thermal Tolerance Research Articles

Body size dictates physiological and behavioural responses to hypoxia and elevated water temperatures in Murray cod (Maccullochella peelii).

Increasing drought frequency and duration pose a significant threat to fish species in dryland river systems. As ectotherms, fish thermal and hypoxia tolerances directly determine the capacity of species to persist in these environments during low flow periods when water temperatures are high and waterbodies become highly stratified. Chronic thermal stress can compound the impacts of acute hypoxic events on fish resulting in significant fish mortality; however, it is not known if all size classes are equally susceptible, or if the allometric scaling of physiological processes means some size classes are disproportionately affected. We investigated the physiological responses of Murray cod (Maccullochella peelii) over a four-fold body size range (0.2-3000g) to acute changes in water temperature and oxygen concentration following 4 weeks of acclimation to representative spring (20°C) and summer (28°C) water temperatures. We recorded maximum thermal tolerance (CT max), oxygen limited thermal tolerance (PCTmax ), lowest tolerable oxygen level (as the oxygen level at which lose equilibrium; O2,LOE), gill ventilation rates and aerial surface respiration threshold, blood oxygen transport capacity and lactate accumulation. Acclimation to elevated water temperatures improved thermal and hypoxia tolerance metrics across all size classes. However, body size significantly affected thermal and hypoxia responses. Small M. peelii were significantly less hypoxia tolerant than larger individuals, while larger fish were significantly less thermal tolerant than smaller fish. Hypoxia constrained thermal tolerance in M. peelii, with both small and large fish disproportionally compromised relative to mid-sized fish. Our findings indicate that both very small/young (larvae, fry, fingerlings) and very large/older M. peelii in dryland rivers are at significant risk from the combined impacts of a warming and drying climate and water extraction. These data will inform policy decisions that serve to balance competing demands on precious freshwater resources.

Oxygen supply limits the chronic heat tolerance of locusts during the first instar only

Although scientists know that overheating kills many organisms, they do not agree on the mechanism. According to one theory, referred to as oxygen- and capacity-limitation of thermal tolerance, overheating occurs when a warming organism’s demand for oxygen exceeds its supply, reducing the organism’s supply of ATP. This model predicts that an organism’s heat tolerance should decrease under hypoxia, yet most terrestrial organisms tolerate the same amount of warming across a wide range of oxygen concentrations. This point is especially true for adult insects, who deliver oxygen through highly efficient respiratory systems. However, oxygen limitation at high temperatures may be more common during immature life stages, which have less developed respiratory systems. To test this hypothesis, we measured the effects of heat and hypoxia on the survival of South American locusts (Schistocerca cancellata) throughout development and during specific instars. We demonstrate that the heat tolerance of locusts depends on oxygen supply during the first instar but not during later instars. This finding provides further support for the idea that oxygen limitation of thermal tolerance depends on respiratory performance, especially during immature life stages.

Nonspecific stress response to temperature increase in Gammarus lacustris Sars with respect to oxygen-limited thermal tolerance concept.

The previously undescribed dynamics of the heat shock protein HSP70 and subsequent lipid peroxidation products have been assessed alongside lactate dehydrogenase activity for Gammarus lacustris Sars, an amphipod species from the saltwater Lake Shira (Republic of Khakassia). Individuals were exposed to a gradual temperature increase of 1 °C/hour (total exposure duration of 26 hours) starting from the mean annual temperature of their habitat (7 °C) up to 33 °C. A complex of biochemical reactions occurred when saltwater G. lactustris was exposed to the gradual changes in temperature. This was characterized by a decrease in lactate dehydrogenase activity and the launching of lipid peroxidation. The HSP70 level did not change significantly during the entire experiment. In agreement with the concept of oxygen-limited thermal tolerance, an accumulation of the most toxic lipid peroxides (triene conjugates and Schiff bases) in phospholipids occurred at the same time and temperature as the accumulation of lactate. The main criterion overriding the temperature threshold was, therefore, the transition to anaerobiosis, confirmed by the elevated lactate levels as observed in our previous associated study, and by the development of cellular stress, which was expressed by an accumulation of lipid peroxidation products. An earlier hypothesis, based on freshwater individuals of the same species, has been confirmed whereby the increased thermotolerance of G. lacustris from the saltwater lake was caused by differences in energy metabolism and energy supply of nonspecific cellular stress-response mechanisms. With the development of global climate change, these reactions could be advantageous for saltwater G. lacustris. The studied biochemical reactions can be used as biomarkers for the stress status of aquatic organisms when their habitat temperature changes.

Chronic warm exposure impairs growth performance and reduces thermal safety margins in the common triplefin fish (Forsterygion lapillum)

Intertidal fish species face gradual chronic changes in temperature and greater extremes of acute thermal exposure through climate-induced warming. As sea temperatures rise, it has been proposed that whole-animal performance will be impaired through oxygen and capacity limited thermal tolerance [OCLTT; reduced aerobic metabolic scope (MS)] and, on acute exposure to high temperatures, thermal safety margins may be reduced because of constrained acclimation capacity of upper thermal limits. Using the New Zealand triplefin fish (Forsterygion lapillum), this study addressed how performance in terms of growth and metabolism (MS) and upper thermal tolerance limits would be affected by chronic exposure to elevated temperature. Growth was measured in fish acclimated (12 weeks) to present and predicted future temperatures and metabolic rates were then determined in fish at acclimation temperatures and with acute thermal ramping. In agreement with the OCLTT hypothesis, chronic exposure to elevated temperature significantly reduced growth performance and MS. However, despite the prospect of impaired growth performance under warmer future summertime conditions, an annual growth model revealed that elevated temperatures may only shift the timing of high growth potential and not the overall annual growth rate. While the upper thermal tolerance (i.e. critical thermal maxima) increased with exposure to warmer temperatures and was associated with depressed metabolic rates during acute thermal ramping, upper thermal tolerance did not differ between present and predicted future summertime temperatures. This suggests that warming may progressively decrease thermal safety margins for hardy generalist species and could limit the available habitat range of intertidal populations.

Development in a warm future ocean may enhance performance in some species

Understanding the capacity of organisms to cope with projected global warming through acclimation and adaptation is critical to predicting their likely future persistence. The vast majority of research on tropical species suggests they will be substantially negatively affected by future warming and have limited capacity to acclimate to changes. This study tested whether the spine cheek anemonefish, Premnas biaculeatus, has the capacity for developmental thermal acclimation of metabolic attributes and critical thermal maximum (CTmax) to increasing sea water temperature. Juveniles of P. biaculeatus exhibited high capacity for developmental thermal acclimation of aerobic physiology. Fish reared at +1.5°C and +3.0°C above present-day mean temperatures possessed enhanced performance across all testing temperatures (28.5°C to 31.5°C), i.e. overcompensation. Specifically, this occurred through increases in maximum oxygen consumption (MO2Maximum) that resulted in elevations in both net and factorial aerobic scope. In addition, fish reared at +1.5°C also exhibited a partial increase in critical thermal maximum (CTmax) by 0.5°C, however no increase was observed in fish reared at +3.0°C. Fish reared at +3.0°C were significantly longer, heavier and in better condition than +0.0°C present-day fish, suggesting that alterations to aerobic physiology correspond to enhancement of growth and condition as would be predicted with the oxygen and capacity limited thermal tolerance hypothesis. These results indicate that the acclimation to future warming may produce overall enhanced performance in some species. It also suggests that the developmental acclimation ability varies substantially between species within the same family and a greater understanding of promoted or reduced acclimation capacity will be critically important to predicting the impacts of climate change on coral reef systems.

Oxygen limited thermal tolerance is seen in a plastron breathing insect, and can be induced in a bimodal gas exchanger

ABSTRACTThermal tolerance has been hypothesized to result from a mismatch between oxygen supply and demand. However, the generality of this hypothesis has been challenged by studies on various animal groups, including air-breathing adult insects. Recently, comparisons across taxa have suggested that differences in gas exchange mechanisms could reconcile the discrepancies found in previous studies. Here, we test this suggestion by comparing the behaviour of related insect taxa with different gas exchange mechanisms, with and without access to air. We demonstrate oxygen-limited thermal tolerance in air-breathing adults of the plastron-exchanging water bug Aphelocheirus aestivalis. Ilyocoris cimicoides, a related, bimodal gas exchanger, did not exhibit such oxygen-limited thermal tolerance and relied increasingly on aerial gas exchange with warming. Intriguingly, however, when denied access to air, oxygen-limited thermal tolerance could also be induced in this species. Patterns in oxygen-limited thermal tolerance were found to be consistent across life-history stages in these insects, with nymphs employing the same gas exchange mechanisms as adults. These results advance our understanding of oxygen limitation at high temperatures; differences in the degree of respiratory control appear to modulate the importance of oxygen in setting tolerance limits.

Does greater thermal plasticity facilitate range expansion of an invasive terrestrial anuran into higher latitudes?

Temperature has pervasive effects on physiological processes and is critical in setting species distribution limits. Since invading Australia, cane toads have spread rapidly across low latitudes, but slowly into higher latitudes. Low temperature is the likely factor limiting high-latitude advancement. Several previous attempts have been made to predict future cane toad distributions in Australia, but understanding the potential contribution of phenotypic plasticity and adaptation to future range expansion remains challenging. Previous research demonstrates the considerable thermal metabolic plasticity of the cane toad, but suggests limited thermal plasticity of locomotor performance. Additionally, the oxygen-limited thermal tolerance hypothesis predicts that reduced aerobic scope sets thermal limits for ectotherm performance. Metabolic plasticity, locomotor performance and aerobic scope are therefore predicted targets of natural selection as cane toads invade colder regions. We measured these traits at temperatures of 10, 15, 22.5 and 30°C in low- and high-latitude toads acclimated to 15 and 30°C, to test the hypothesis that cane toads have adapted to cooler temperatures. High-latitude toads show increased metabolic plasticity and higher resting metabolic rates at lower temperatures. Burst locomotor performance was worse for high-latitude toads. Other traits showed no regional differences. We conclude that increased metabolic plasticity may facilitate invasion into higher latitudes by maintaining critical physiological functions at lower temperatures.

Indirect genetic effects underlie oxygen-limited thermal tolerance within a coastal population of chinook salmon.

With global temperatures projected to surpass the limits of thermal tolerance for many species, evaluating the heritable variation underlying thermal tolerance is critical for understanding the potential for adaptation to climate change. We examined the evolutionary potential of thermal tolerance within a population of chinook salmon (Oncorhynchus tshawytscha) by conducting a full-factorial breeding design and measuring the thermal performance of cardiac function and the critical thermal maximum (CTmax) of offspring from each family. Additive genetic variation in offspring phenotype was mostly negligible, although these direct genetic effects explained 53% of the variation in resting heart rate (fH). Conversely, maternal effects had a significant influence on resting fH, scope for fH, cardiac arrhythmia temperature and CTmax. These maternal effects were associated with egg size, as indicated by strong relationships between the mean egg diameter of mothers and offspring thermal tolerance. Because egg size can be highly heritable in chinook salmon, our finding indicates that the maternal effects of egg size constitute an indirect genetic effect contributing to thermal tolerance. Such indirect genetic effects could accelerate evolutionary responses to the selection imposed by rising temperatures and could contribute to the population-specific thermal tolerance that has recently been uncovered among Pacific salmon populations.

Oxygen transport is not compromised at high temperature in pythons.

To evaluate whether the 'oxygen and capacity limited thermal tolerance' model (OCLTT) applies to an air-breathing ectothermic vertebrate, we measured oxygen uptake (V̇(O₂)), cardiac performance and arterial blood gases during a progressive rise of temperature from 30 to 40°C in the snake Python regius. V̇(O₂) of fasting snakes increased exponentially with temperature whereas V̇(O₂) of digesting snakes at high temperatures plateaued at a level 3- to 4-fold above fasting. The high and sustained aerobic metabolism over the entire temperature range was supported by pronounced tachycardia at all temperatures, and both fasting and digesting snakes maintained a normal acid-base balance without any indication of anaerobic metabolism. All snakes also maintained high arterial PO2, even at temperatures close to the upper lethal temperature. Thus, there is no evidence of a reduced capacity for oxygen transport at high temperatures in either fasting or digesting snakes, suggesting that the upper thermal tolerance of this species is limited by other factors.

Variation in temperature tolerance among families of Atlantic salmon (Salmo salar) is associated with hypoxia tolerance, ventricle size and myoglobin level

In fishes, performance failure at high temperature is thought to be due to a limitation on oxygen delivery (the theory of oxygen and capacity limited thermal tolerance, OCLTT), which suggests that thermal tolerance and hypoxia tolerance might be functionally associated. Here we examined variation in temperature and hypoxia tolerance among 41 families of Atlantic salmon (Salmo salar), which allowed us to evaluate the association between these two traits. Both temperature and hypoxia tolerance varied significantly among families and there was a significant positive correlation between critical maximum temperature (CTmax) and hypoxia tolerance, supporting the OCLTT concept. At the organ and cellular levels, we also discovered support for the OCLTT concept as relative ventricle mass (RVM) and cardiac myoglobin (Mb) levels both correlated positively with CTmax (R(2)=0.21, P<0.001 and R(2)=0.17, P=0.003, respectively). A large RVM has previously been shown to be associated with high cardiac output, which might facilitate tissue oxygen supply during elevated oxygen demand at high temperatures, while Mb facilitates the oxygen transfer from the blood to tissues, especially during hypoxia. The data presented here demonstrate for the first time that RVM and Mb are correlated with increased upper temperature tolerance in fish. High phenotypic variation between families and greater similarity among full- and half-siblings suggests that there is substantial standing genetic variation in thermal and hypoxia tolerance, which could respond to selection either in aquaculture or in response to anthropogenic stressors such as global climate change.

The synergistic effects of increasing temperature and CO2 levels on activity capacity and acid–base balance in the spider crab, Hyas araneus

With global climate change, ocean warming and acidification occur concomitantly. In this study, we tested the hypothesis that increasing CO2 levels affect the acid–base balance and reduce the activity capacity of the Arctic spider crab Hyas araneus, especially at the limits of thermal tolerance. Crabs were acclimated to projected oceanic CO2 levels for 12 days (today: 380, towards the year 2100: 750 and 1,120 and beyond: 3,000 μatm) and at two temperatures (1 and 4 °C). Effects of these treatments on the righting response (RR) were determined (1) at acclimation temperatures followed by (2) righting when exposed to an additional acute (15 min) heat stress at 12 °C. Prior to (resting) and after the consecutive stresses of combined righting activity and heat exposure, acid–base status and lactate contents were measured in the haemolymph. Under resting conditions, CO2 caused a decrease in haemolymph pH and an increase in oxygen partial pressure. Despite some buffering via an accumulation of bicarbonate, the extracellular acidosis remained uncompensated at 1 °C, a trend exacerbated when animals were acclimated to 4 °C. The additional combined exposure to activity and heat had only a slight effect on blood gas and acid–base status. Righting activity in all crabs incubated at 1 and 4 °C was unaffected by elevated CO2 levels or acute heat stress but was significantly reduced when both stressors acted synergistically. This impact was much stronger in the group acclimated at 1 °C where some individuals acclimated to high CO2 levels stopped responding. Lactate only accumulated in the haemolymph after combined righting and heat stress. In the group acclimated to 1 °C, lactate content was highest under normocapnia and lowest at the highest CO2 level in line with the finding that RR was largely reduced. In crabs acclimated to 4 °C, the RR was less affected by CO2 such that activity caused lactate to increase with rising CO2 levels. In line with the concept of oxygen and capacity limited thermal tolerance, all animals exposed to temperature extremes displayed a reduction in scope for performance, a trend exacerbated by increasing CO2 levels. Additionally, the differences seen between cold- and warm-acclimated H. araneus after heat stress indicate that a small shift to higher acclimation temperatures also alleviates the response to temperature extremes, indicating a shift in the thermal tolerance window which reduces susceptibility to additional CO2 exposure.

Oxygen and capacity limited thermal tolerance of the lugworm Arenicola marina: A seasonal comparison

Lugworms Arenicola marina were collected from Arcachon Bay in two summers and winters of consecutive years. The worms were acclimated to different temperatures (5 and 10 °C for winter animals and 15 °C for summer animals). Each group was investigated over an experimental temperature range concerning its optimum in exercise performance, acute growth rate as well as respiration and ventilation activities to reveal seasonal acclimatisation effects, potential inter-annual differences and the influence of laboratory acclimation temperatures on the parameters of interest. The groups investigated at the two consecutive summers yielded nearly identical results for ventilation and respiration activities. A clear seasonal difference developed in exercise performance, with an optimum at lower temperatures in winter than in summer, irrespective of acclimation temperature. Respiration and ventilation activities showed no significant differences between winter specimens acclimated to 10 °C and summer specimens acclimated to 15 °C. However, an acclimation temperature of 5 °C for winter animals caused noticeable differences to those acclimated at 10 °C. Acute growth rates differed seasonally as well as between acclimation temperatures with the highest rates found around 10 °C in summer and around 15 °C in winter. The lowest rates were recorded in winter worms acclimated to 5 °C. These acute patterns may reflect high thermal limits in warm acclimated winter worms and temperature dependent shifts in energy demand in summer animals.

Can Oxygen Set Thermal Limits in an Insect and Drive Gigantism?

BackgroundThermal limits may arise through a mismatch between oxygen supply and demand in a range of animal taxa. Whilst this oxygen limitation hypothesis is supported by data from a range of marine fish and invertebrates, its generality remains contentious. In particular, it is unclear whether oxygen limitation determines thermal extremes in tracheated arthropods, where oxygen limitation may be unlikely due to the efficiency and plasticity of tracheal systems in supplying oxygen directly to metabolically active tissues. Although terrestrial taxa with open tracheal systems may not be prone to oxygen limitation, species may be affected during other life-history stages, particularly if these rely on diffusion into closed tracheal systems. Furthermore, a central role for oxygen limitation in insects is envisaged within a parallel line of research focussing on insect gigantism in the late Palaeozoic.Methodology/Principal FindingsHere we examine thermal maxima in the aquatic life stages of an insect at normoxia, hypoxia (14 kPa) and hyperoxia (36 kPa). We demonstrate that upper thermal limits do indeed respond to external oxygen supply in the aquatic life stages of the stonefly Dinocras cephalotes, suggesting that the critical thermal limits of such aquatic larvae are set by oxygen limitation. This could result from impeded oxygen delivery, or limited oxygen regulatory capacity, both of which have implications for our understanding of the limits to insect body size and how these are influenced by atmospheric oxygen levels.Conclusions/SignificanceThese findings extend the generality of the hypothesis of oxygen limitation of thermal tolerance, suggest that oxygen constraints on body size may be stronger in aquatic environments, and that oxygen toxicity may have actively selected for gigantism in the aquatic stages of Carboniferous arthropods.

Metabolic and molecular stress responses of gilthead seam bream Sparus aurata during exposure to low ambient temperature: an analysis of mechanisms underlying the winter syndrome

The winter syndrome in the gilthead sea bream Sparus aurata indicates that the species is exposed to critically low temperatures in Mediterranean aquaculture in winter. The present study of metabolic patterns and molecular stress responses during cold exposure was carried out to investigate this "disease", in light of the recent concept of oxygen and capacity limited thermal tolerance. The metabolic profile of fuel oxidation was examined by determining the activities of the enzymes hexokinase (HK), aldolase (Ald), pyruvate kinase (PK), L-lactate dehydrogenase (L-LDH), citrate synthase (CS), malate dehydrogenase (MDH) and 3-hydroxyacyl CoA dehydrogenase (HOAD) in heart, red and white muscle after exposure to temperatures of 10, 14 and 18°C. Especially, the increase in LDH activity combined with the accumulation of L-lactate in tissues indicates that temperatures below 14°C are critical for Sparus aurata and stimulate the anaerobic component of metabolism. Increase in the activity of HOAD suggests that oxidation of free fatty acids might contribute to ATP turnover at low temperatures. The expression of Hsp70 and Hsp90 in all tissues examined revealed a cellular stress response during cooling below 18°C. In the light of winter temperatures in S. aurata cultures around 10°C, our data suggest that the fish are exposed to stressful conditions at the low end of their thermal tolerance window. These conditions likely impair the aerobic capacity of the fish, compromise the rates of growth and reproduction and may contribute to elicit pathological conditions.

Indicators of oxygen- and capacity-limited thermal tolerance in the lugworm Arenicola marina

Thermal tolerance windows were investigated in lugworms Arenicola marina (L.) from the North Sea, the English Channel and the Atlantic during winter and summer seasons. We adopted the concept of oxygen- and capacity-limited thermal tolerance and tested a variety of methods for their suitability to identify characteristics of the respective thermal window, such as critical, pejus (lat.: getting worse) and optimum temperatures (Tc, Tp and Topt), as well as temperature-dependent perfor- mance. First, the effect of acute temperature changes on oxygen consumption and pumping activity was examined in artificial burrows ventilated by lugworms collected in winter and summer from North Sea mudflats (acclimation temperatures 5 and 10°C). Second, the window of acutely temperature- dependent growth was evaluated by following the integration of uniformly labelled 13 C-L-phenylala- nine into proteins of the cuticulo-muscular tube, using nuclear magnetic resonance spectroscopy, possibly providing access to Tp values. Third, seasonal changes in haemoglobin half-saturation oxy- gen tension (P50) and haemoglobin oxygen status in vivo were studied in lugworms from the North Sea population. Tc values were defined by use of oxygen consumption measurements, whereas pumping activity, growth performance and tissue oxygenation allowed determination of Topt. Our results show that the thermal window of actively ventilating lugworms is narrower in winter than in summer. The acute optimum temperature of growth performance was tilted towards the lower Tc and likely shifts with acclimation. Methods were found suitable to identify the acute thermal window of oxygen-limited thermal tolerance in the lugworm. Consecutive comparison of populations during various seasons in a latitudinal cline should thus lead to a better understanding of the impacts of climate change on marine ecosystems.

Metabolic and molecular stress responses of sublittoral bearded horse musselModiolus barbatusto warming sea water: implications for vertical zonation

The present study set out to investigate the thermal limits of the Mediterranean bivalve Modiolus barbatus, acclimated to various temperatures, and includes a comparison of laboratory determined limits with its temperature-dependent restriction to deeper water layers in its natural habitat. Thermal responses and limits were determined by integrating information from various levels of biological organization, including the expression of Hsp70 and Hsp90, the phosphorylation of stress-activated protein kinases, p38 mitogen-activated protein kinase (p38 MAPK) and cJun-N-terminal kinases (JNKs) as well as metabolic adjustments. The latter were assessed by examining temperature effects on the activity of the key glycolytic enzyme pyruvate kinase (PK). The expression of Hsp70 and Hsp90 was activated when mussels were acclimated to temperatures above 20 degrees C. Increased phosphorylation of p38 MAPK and JNKs at about the same temperatures indicate activation of MAPK signaling cascades and their potential involvement in the induction of Hsp genes. As indicated by the activity of PK, Modiolus barbatus maintains some aerobic capacity when acclimated to temperatures up to 24 degrees C, while further warming probably caused metabolic depression and a shift from aerobic to anaerobic metabolism. An increase in mortality occurred in parallel, during acclimation to temperatures above 24 degrees C. Our results indicate that both the biochemical stress indicators and metabolic status respond in parallel once hypoxemia becomes extreme. Comparison with our previous study of thermal limits and vertical distribution in M. galloprovincialis dwelling in shallow waters emphasizes the relevance of maintained aerobic scope over that of passive tolerance for permanent vertical zonation at higher temperatures in the field. These findings and conclusions are in line with the concept of oxygen and capacity limited thermal tolerance and the associated systemic to molecular hierarchy of thermal limitation.

Critical thermal limits and their responses to acclimation in two sub-Antarctic spiders: Myro kerguelenensis and Prinerigone vagans

Despite the relative richness of spider species across the Southern Ocean islands remarkably little information is available on their biology. Here, the critical thermal limits of an indigenous (Myro kerguelenensis, Desidae) and an introduced (Prinerigone vagans, Linyphiidae) spider species from Marion Island were studied after 7–8 days acclimation to 0, 5, 10 and 15°C. Critical thermal minima (CTMin) were low in these species by comparison with other spiders and insects measured to date, and ranged from −6 to −7°C in M. kerguelenensis and from −7 to −8°C in P. vagans. In contrast, critical thermal maxima (CTMax) were similar to other insects on Marion Island (M. kerguelenensis: 35.0–35.6°C; P. vagans: 35.1–36.0°C), although significantly lower than those reported for other spider species in the literature. The magnitude of acclimation responses in CTMax was lower than those in CTMin for both species and this suggests decoupled responses to acclimation. Whilst not conclusive, the results raise several important considerations: that oxygen limitation of thermal tolerance needs to be more widely investigated in terrestrial species, that indigenous and alien species might differ in the nature and extent of their plasticity, and that upper and lower thermal tolerance limits might be decoupled in spiders as is the case in insects.

Oxygen limited thermal tolerance: The scale of individual variation, and the effects of size

Oxygen limited thermal tolerance: The scale of individual variation, and the effects of size

Climate-dependent evolution of Antarctic ectotherms: An integrative analysis

Abstract The paper explores the climate-dependent evolution of marine Antarctic fauna and tries to identify key mechanisms involved as well as the driving forces that have caused the physiological and life history characteristics observed today. In an integrative approach it uses the recent concept of oxygen and capacity limited thermal tolerance to identify potential links between molecular, cellular, whole-organism, and ecological characteristics of marine animal life in the Antarctic. As a generalized pattern, minimization of baseline energy costs, for the sake of maximized growth in the cold, appears as one over-arching principle shaping the evolution and functioning of Antarctic marine ectotherms. This conclusion is supported by recent comparisons with (sub-) Arctic ectotherms, where elevated levels of energy turnover result at unstable, including cold temperatures, and are related to wide windows of thermal tolerance and associated metabolic features. At biochemical levels, metabolic regulation at low temperatures in general, is supported by the cold compensation of enzyme kinetic parameters like substrate affinities and turnover numbers, through minute structural modifications of the enzyme molecule. These involve a shift in protein folding, sometimes supported by the replacement of individual amino acids. The hypothesis is developed that efficient metabolic regulation at low rates in Antarctic marine stenotherms occurs through high mitochondrial densities at low capacities and possibly enhanced levels of Arrhenius activation energies or activation enthalpies. This contrasts the more costly patterns of metabolic regulation at elevated rates in cold-adapted eurytherms. Energy savings in Antarctic ectotherms, largely exemplified in fish, typically involve low-cost, diffusive oxygen distribution due to high density of lipid membranes, loss of haemoglobin, myoglobin and the heat shock response, reduced anaerobic capacity, large myocytes with low ion exchange activities, and the use of lipid body stores for neutral buoyancy. Important trade-offs result from obligatory energy savings in the permanent cold: low metabolic rates support cold-compensated growth but imply narrow windows of thermal tolerance and reduced scopes for activity. The degree of thermal specialization is not uniformly defined by cold temperature but varies with life style characteristics and activity levels and associated aerobic scope. Trade-offs for the sake of cold compensated growth parallel reduced capacities for exercise performance, exacerbated by the effect of high haemolymph magnesium levels in crustaceans and, possibly, other invertebrates. High magnesium levels likely exclude the group of reptant decapod crustaceans from Antarctic waters below 0 °C. The hypothesis is developed that energy savings imposed by the permanent cold bear specific life history consequences. Due to effects of allometry, energy savings are exacerbated at small body size, favouring passive lecithotrophic larvae. At all stages of life history, reduced energy turnover for the sake of growth causes delays and low rates in other higher functions, with the result of late maturity, fecundity and offspring release, as well as extended development. As a consequence, extended life spans evolved due to life history requirements. At the same time, polar gigantism is enabled by a combination of elevated oxygen levels in cold waters, of reduced metabolism and of extended periods of growth at slow developmental rates.

Critical temperatures in the cephalopodSepia officinalisinvestigated usingin vivo31P NMR spectroscopy

The present study was designed to test the hypothesis of an oxygen limitation defining thermal tolerance in the European cuttlefish (Sepia officinalis). Mantle muscle organ metabolic status and pHi were monitored using in vivo 31P NMR spectroscopy, while mantle muscle performance was determined by recording mantle cavity pressure oscillations during ventilation and spontaneous exercise. Under control conditions (15 degrees C), changes in muscle phospho-L-arginine (PLA) and inorganic phosphate (Pi) levels could be linearly related to frequently occurring, high-pressure mantle contractions with pressure amplitudes (MMPA) of >0.2 kPa. Accordingly, mainly MMPA of >2 kPa affected muscle PLA reserves, indicating that contractions with MMPA of <2 kPa only involve the thin layers of aerobic circular mantle musculature. On average, no more than 20% of muscle PLA was depleted during spontaneous exercise under control conditions. Subjecting animals to acute thermal change at an average rate of 1 deg. h-1 led to significant Pi accumulation (equivalent to PLA breakdown) and decrements in the free energy of ATP hydrolysis (dG/dzeta) at both ends of the temperature window, starting at mean critical temperatures (Tc) of 7.0 and 26.8 degrees C, respectively. Frequent groups of high-pressure mantle contractions could not (in the warm) or only partially (in the cold) be related to net PLA breakdown in mantle muscle, indicating an oxygen limitation of routine metabolism rather than exercise-related phosphagen use. We hypothesize that it is mainly the constantly working radial mantle muscles that become progressively devoid of oxygen. Estimates of very low dG/dzeta values (-44 kJ mol-1) in this compartment, along with correlated stagnating ventilation pressures in the warm, support this hypothesis. In conclusion, we found evidence for an oxygen limitation of thermal tolerance in the cuttlefish Sepia officinalis, as indicated by a progressive transition of routine mantle metabolism to an anaerobic mode of energy production.