Adapt,move or die – how will tropical coral reef fishes cope with ocean warming?

Previous studies hailed thermal tolerance and the capacity for organisms to acclimate and adapt as the primary pathways for species survival under climate change. Here we challenge this theory. Over the past decade, more than 365 tropical stenothermal fish species have been documented moving poleward, away from ocean warming hotspots where temperatures 2–3 °C above long‐term annual means can compromise critical physiological processes. We examined the capacity of a model species – a thermally sensitive coral reef fish, Chromis viridis (Pomacentridae) – to use preference behaviour to regulate its body temperature. Movement could potentially circumvent the physiological stress response associated with elevated temperatures and may be a strategy relied upon before genetic adaptation can be effectuated. Individuals were maintained at one of six temperatures (23, 25, 27, 29, 31 and 33 °C) for at least 6 weeks. We compared the relative importance of acclimation temperature to changes in upper critical thermal limits, aerobic metabolic scope and thermal preference. While acclimation temperature positively affected the upper critical thermal limit, neither aerobic metabolic scope nor thermal preference exhibited such plasticity. Importantly, when given the choice to stay in a habitat reflecting their acclimation temperatures or relocate, fish acclimated to end‐of‐century predicted temperatures (i.e. 31 or 33 °C) preferentially sought out cooler temperatures, those equivalent to long‐term summer averages in their natural habitats (~29 °C). This was also the temperature providing the greatest aerobic metabolic scope and body condition across all treatments. Consequently, acclimation can confer plasticity in some performance traits, but may be an unreliable indicator of the ultimate survival and distribution of mobile stenothermal species under global warming. Conversely, thermal preference can arise long before, and remain long after, the harmful effects of elevated ocean temperatures take hold and may be the primary driver of the escalating poleward migration of species.     

Effect of long-term thermal acclimation on the electrical avoidance conditioning of fish

The learning behaviour and memory formation of ectotherms, especially of fish, depend significantly on the acclimation temperature. Although temperature is known to affect different physiological factors in the nervous system, the exact manner in which memory and learning are affected by these alterations is not clear. Large variations in the acclimation time before learning takes place, are striking. With regard to long-lasting compensatory changes in the polarity of membrane-bound neuronal gangliosides (1) and in the bio-electrical activity of the CNS (post-synaptic potential amplitudes (2)) following thermal acclimation it was of interest to investigate the time course of acclimation on the learning ability of fish subjected to a new environmental temperature.     

泽陆蛙和饰纹姬蛙蝌蚪不同热驯化下选择体温和热耐受性

用泽陆蛙（Fejervarya limnocharis）蝌蚪和饰纹姬蛙（Microhyla ornata）蝌蚪做研究模型,检测热驯化（20 、25 和30 C）对选择体温（Tsel）、低温耐受性（CTMin）和高温耐受性（CTMax）的影响。结果显示,两种蝌蚪的Tsel既不受驯化温度的影响,也不存在种间差异;泽陆蛙蝌蚪的CTMin显著小于饰纹姬蛙蝌蚪,而CTMax和VTR则显著大于饰纹姬蛙蝌蚪;CTMin和CTMax随驯化温度的升高而升高,VTR则随驯化温度的升高而减小。研究结果表明,热驯化显著影响两种蝌蚪的CTMin、CTMax和VTR,而对两种蝌蚪的体温调定点无显著影响;这些热生物学特征对两种蝌蚪有效适应环境温度变化、利用资源、减少种间竞争具有重要的生态学意义。     

Response of juvenile diamond-backed terrapins (Malaclemys terrapin) to an aquatic thermal gradient

In many ectotherms, selection of environmental thermal niches may positively affect growth, nutrient assimilation rates, immune system function, and ultimately survival. Temperature preference in some turtle species may be influenced by environmental conditions, including acclimation temperature. We tested for effects of acclimation temperature (22 °C, 27 °C) on the selected temperature and movement patterns of 14 juvenile Malaclemys terrapin (Reptilia: Emydidae) in an aquatic thermal gradient of 14–34 °C and in single-temperature (22 °C, 27 °C) control tests. Among 8–10 month old terrapins, acclimation temperature influenced activity and movement patterns but did not affect temperature selection. In thermal gradient and single-temperature control tests, turtles acclimated to 27 °C used more tank chambers and relocated between chambers significantly more frequently than individuals acclimated to 22 °C. However, acclimation temperature did not affect temperature selection: both 22- and 27 °C-acclimated turtles selected the warmest temperature (34 °C), and avoided the other temperatures available, during thermal gradient tests. These results suggest that young M. terrapin are capable of detecting small temperature increments and prefer warm temperatures that may positively influence growth and metabolism.     

Calling behaviour under climate change: geographical and seasonal variation of calling temperatures in ectotherms

Calling behaviour is strongly temperature‐dependent and critical for sexual selection and reproduction in a variety of ectothermic taxa, including anuran amphibians, which are the most globally threatened vertebrates. However, few studies have explored how species respond to distinct thermal environments at time of displaying calling behaviour, and thus it is still unknown whether ongoing climate change might compromise the performance of calling activity in ectotherms. Here, we used new audio‐trapping techniques (automated sound recording and detection systems) between 2006 and 2009 to examine annual calling temperatures of five temperate anurans and their patterns of geographical and seasonal variation at the thermal extremes of species ranges, providing insights into the thermal breadths of calling activity of species, and the mechanisms that enable ectotherms to adjust to changing thermal environments. All species showed wide thermal breadths during calling behaviour (above 15 °C) and increases in calling temperatures in extremely warm populations and seasons. Thereby, calling temperatures differed both geographically and seasonally, both in terrestrial and aquatic species, and were 8–22 °C below the specific upper critical thermal limits (CT_max) and strongly associated with the potential temperatures of each thermal environment (operative temperatures during the potential period of breeding). This suggests that calling behaviour in ectotherms may take place at population‐specific thermal ranges, diverging when species are subjected to distinct thermal environments, and might imply plasticity of thermal adjustment mechanisms (seasonal and developmental acclimation) that supply species with means of coping with climate change. Furthermore, the thermal thresholds of calling at the onset of the breeding season were dissimilar between conspecific populations, suggesting that other factors besides temperature are needed to trigger the onset of reproduction. Our findings imply that global warming would not directly inhibit calling behaviour in the study species, although might affect other temperature‐dependent features of their acoustic communication system.     

Interactions of season and temperature acclimation in the control of metabolism in Amphibia

1. 1.|Studies concerning the seasonal variation and the temperature acclimation of metabolism and their control in Amphibia are reviewed.

2. 2.|Both season and temperature acclimation affect the activities of the central and autonomic nervous systems.

3. 3.|These changes are mediated especially by alterations in the activity of the thyroid and through the autonomic nerves.

4. 4.|The fact that common control mechanisms are involved may explain some of the often observed metabolic interactions of season and temperature acclimation.

Vulnerability to climate warming and acclimation capacity of tropical and temperate coastal organisms

Ecological forecasting on the likely impacts of climate warming is crucial at a time when several ecosystems seem to be responding to this environmental threat. Among the most important questions are: which are the most vulnerable organisms to climate warming and where are they? Recently, there has been debate on whether the tropics or temperate zones are more vulnerable to warming. Vulnerability toward higher temperatures will depend on the organisms’ thermal limits and also on their acclimation capacity, which remains largely unknown for most species. The aim of the present work was to estimate (1) the upper thermal limits (Critical Thermal Maximum (CTMax)), (2) the warming tolerance (CTMax – Maximum Habitat Temperature) and (3) the acclimation capacity of tropical and temperate rocky shore organisms. Differences in biological groups (decapod crustaceans vs fish) were investigated and the effect of region (tropical vs temperate) and habitat (intertidal vs subtidal) was tested. Overall, 35 species were tested. For the assessment of the acclimation capacity, tropical-temperate pairs of closely related species of shrimp, crab and fish were selected. Warming tolerance was higher for temperate species than for tropical species and higher for subtidal species than for intertidal species, confirming that species with the highest thermal limits have the lowest warming tolerance. All species tested presented some acclimation capacity (CTMax_Trial − CTMax_Control), with the exception of gobiid fish, which was not observed to acclimate. The tropical species tested showed a lower acclimation capacity than their temperate counterparts. Given that tropical rocky shore organisms are already living very close to their thermal limits and that their acclimation capacity is limited, it is likely that the impacts of global warming will be evident sooner in the tropics than in the temperate zone.     

Beneficial acclimation and the Bogert effect

Few studies have examined the extent to which phenotypic plasticity in a given trait might be influenced by behavioural responses to an environmental cue. Regulatory behaviour might eliminate environmental variation such that little selection for physiological change would take place. Here, to test this Bogert effect on acclimation, we use two life-stages of a kelp fly that inhabit the same habitat, but differ profoundly in their behaviour. We predicted that when denied opportunities for behavioural regulation, mobile, though brachypterous adults would show a performance advantage in most thermal environments following acclimation to their preferred temperature(s). By contrast, in the less mobile larvae, that have a broader thermal preference, beneficial acclimation would be more evident. Ordered factor anova with orthogonal polynomial contrasts revealed that adults recovered faster from chill coma following any one of six short-term temperature treatments if they had been acclimated at low temperature, whilst larvae showed beneficial acclimation.     

Thermal preferences in upstream migrating glass-eels of Anguilla anguilla (L.)

The effect of temperature on the migratory behaviour of European glass-eels, Anguilla anguilla, during the first stages of their ascent into inland waters has been investigated. Very little research has documented the thermal preferences of glass-eels, most being directed instead to the study of their thermal resistance and survival. The experimental method adopted aimed at acquiring information on short- and long-term thermal choices and sought to provide evidence of the influence of preceding experiences on choices made during the tests. The results obtained in short-term choices (acute preferendum tests) show a clear preference for flows of water at temperature equal to acclimation temperature rather than for flows at temperatures lower or higher by 3° C. It is sufficient for the glass-eels to remain for about 1 h at a different temperature (acclimation temperature ± 3–4°C) for their subsequent choices to be influenced. When choosing between flows warmer or colder than acclimation water, glass-eels prefer the lower temperature. When the temperature presented is very low (about 3° C) the preference is inverted. There is evidence that the temperature gradient represents one of the main orienting cues. In long-term choices (final preference tests) the experimental apparatus allowed prolonged observation (from 24 to 52 h) of the choices between three shelters, the only difference between these being their internal temperatures. In this situation the glass-eels show a clear preference for temperatures higher than that of the environment. For both intervals of environmental temperature considered (11.0–12.6°C and 14.3–17.3° C) a linear correlation exists between temperature difference and number of choices made for the shelters at higher temperatures. The number of glass-eels choosing a higher temperature is greater in the case of lower environmental temperature. In acute preference tests the thermal stimulation is added to a rheotactic response. The glass-eels find themselves in an analogous situation to that during the ascent. On the other hand, in the second experimental situation the choices are an expression of a pure thermal preference.     

Juvenile Ribbontail Stingray, Taeniura lymma (Forssk?l, 1775) (Chondrichthyes, Dasyatidae), demonstrate a unique suite of physiological adaptations to survive hyperthermic nursery conditions

Juvenile ribbontail stingrays, Taeniura lymma (Forssk?l, 1775) of the tropical West Pacific inhabit mangal and seagrass nurseries that often experience rapid and extreme increases in water temperature. We hypothesized that juvenile rays possess a thermal strategy similar to other hyperthermic specialists, in which fish prefer high temperatures, are always prepared for thermal extremes regardless of previous thermal history, and exhibit low metabolic thermal sensitivity. Critical thermal methodology was used to determine the thermal niche, and a thermal gradient used to estimate stingray final preferendum. Temperature quotients (Q ₁₀) were calculated from metabolic rates determined at three temperatures using flow-through respirometry. As predicted, juvenile rays showed a relatively small thermal niche dominated by intrinsic tolerance with limited capacity for acclimation. Thermal preference values were higher than those reported for other elasmobranch species. Interestingly, the temperature quotient for juvenile rays was higher than expected, suggesting that these fish may have the ability to exploit the thermal heterogeneity in their environment. Temperature likely acts as a directing factor in this species, separating warm tolerant juveniles from adults living in deeper, cooler waters.     

Low acclimation capacity of narrow‐ranging thermal specialists exposes susceptibility to global climate change

Thermal acclimation is hypothesized to offer a selective advantage in seasonal habitats and may underlie disparities in geographic range size among closely‐related species with similar ecologies. Understanding this relationship is also critical for identifying species that are more sensitive to warming climates. Here, we study North American plethodontid salamanders to investigate whether acclimation ability is associated with species’ latitudinal extents and the thermal range of the environments they inhabit. We quantified variation in thermal physiology by measuring standard metabolic rate (SMR) at different test and acclimation temperatures for 16 species of salamanders with varying latitudinal extents. A phylogenetically‐controlled Markov chain Monte Carlo generalized linear mixed model (MCMCglmm) was then employed to determine whether there are differences in SMR between wide‐ and narrow‐ranging species at different acclimation temperatures. In addition, we tested for a relationship between the acclimation ability of species and the environmental temperature ranges they inhabit. Further, we investigated if there is a trade‐off between critical thermal maximum (CTMax) and thermal acclimation ability. MCMCglmm results show a significant difference in acclimation ability between wide and narrow‐ranging temperate salamanders. Salamanders with wide latitudinal distributions maintain or slightly increase SMR when subjected to higher test and acclimation temperatures, whereas several narrow‐ranging species show significant metabolic depression. We also found significant, positive relationships between acclimation ability and environmental thermal range, and between acclimation ability and CTMax. Wide‐ranging salamander species exhibit a greater capacity for thermal acclimation than narrow‐ranging species, suggesting that selection for acclimation ability may have been a key factor enabling geographic expansion into areas with greater thermal variability. Further, given that narrow‐ranging salamanders are found to have both poor acclimation ability and lower tolerance to warm temperatures, they are likely to be more susceptible to environmental warming associated with anthropogenic climate change.     

Thermoregulatory behaviour explains countergradient variation in the upper thermal limit of a rainforest skink

The vulnerability of a terrestrial ectotherm to high environmental temperatures depends on the animal's thermal physiology and thermoregulatory behaviour. These variables – environment, physiology, and behaviour – interact with each other, complicating assessment of species vulnerability to global warming. We previously uncovered a counterintuitive pattern in rainforest sunskinks Lampropholis coggeri: a negative relationship between their critical thermal maximum (CT_max) and the temperature of their environment. Could this result be explained by a three‐way interaction between environment, physiology, and behaviour? Here we find that sunskink thermal preference is correlated positively with CT_max, but, importantly, skinks from hotter environments prefer lower temperatures than conspecifics from cooler environments. In an acclimation experiment, we find that CT_max is plastic and shifts in alignment with acclimation temperature. We also found heritable variation in this trait in a common garden study, but this variation was small relative to the plastic shifts observed in CT_max. Thus, our previous observation of a negative correlation between field CT_max and temperature is explained, at least in part, by the lizard's thermoregulatory behaviour: lizards from hot environments preferentially choose cool microenvironments, and their physiology acclimates to these cooler experienced temperatures. Our results suggest that behavioural adjustments to the environment can produce countergradient variation in physiological traits. More broadly, our work underscores the importance of interactions between environment, behaviour, and physiology in ectotherms. Understanding these interactions will be crucial in assessing vulnerability to climate change.     

Thermal acclimation of photosynthesis: on the importance of adjusting our definitions and accounting for thermal acclimation of respiration

While interest in photosynthetic thermal acclimation has been stimulated by climate warming, comparing results across studies requires consistent terminology. We identify five types of photosynthetic adjustments in warming experiments: photosynthesis as measured at the high growth temperature, the growth temperature, and the thermal optimum; the photosynthetic thermal optimum; and leaf-level photosynthetic capacity. Adjustments of any one of these variables need not mean a concurrent adjustment in others, which may resolve apparently contradictory results in papers using different indicators of photosynthetic acclimation. We argue that photosynthetic thermal acclimation (i.e., that benefits a plant in its new growth environment) should include adjustments of both the photosynthetic thermal optimum (T _opt) and photosynthetic rates at the growth temperature (A _growth), a combination termed constructive adjustment. However, many species show reduced photosynthesis when grown at elevated temperatures, despite adjustment of some photosynthetic variables, a phenomenon we term detractive adjustment. An analysis of 70 studies on 103 species shows that adjustment of T _opt and A _growth are more common than adjustment of other photosynthetic variables, but only half of the data demonstrate constructive adjustment. No systematic differences in these patterns were found between different plant functional groups. We also discuss the importance of thermal acclimation of respiration for net photosynthesis measurements, as respiratory temperature acclimation can generate apparent acclimation of photosynthetic processes, even if photosynthesis is unaltered. We show that while dark respiration is often used to estimate light respiration, the ratio of light to dark respiration shifts in a non-predictable manner with a change in leaf temperature.     

TEMPERATURE ACCLIMATION AND THE NERVOUS SYSTEM

1. The conduction velocity of the compound action potential of peripheral nerves shows compensatory acclimation to temperature in a fish, a snail, a crab, and probably also in the frog. The heat and cold tolerances of peripheral conduction are probably both increased by cold acclimation in the frog. 2. The properties of compound action potentials are not suitable for temperature acclimation studies, since different neuronal populations in the same nerve have been found to exhibit different temperature characteristics. 3. Single but septate giant nerve fibres of earthworms show compensatory temperature acclimation of the conduction properties, the form of the action potential and of the axonal cable properties, especially below 13–19 °C. 4. The fatty acids and the plasmalogen aldehydes of the phospholipids of the goldfish brain are more unsaturated at lower acclimation temperatures. 5. The Na⁺-K⁺ ATPase activity of the earthworm nerve cord shows compensatory acclimation at low temperatures. 6. The spontaneous activity of the central nervous system of insects is altered in a compensatory manner by temperature acclimation. In fish, the cold tolerance of simple and complex reflexes and of conditioning is adaptively altered by temperature acclimation. The role of the central nervous system, especially of the thermoregulatory centre, in the temperature acclimation of homeotherms is established. 7. There are adaptive isoenzymes of acetylcholinesterase in the brain of the rainbow trout. These isoenzymes differ from each other in respect of the temperature dependence of their enzyme-substrate affinity. The synthesis of acetylcholine receptor molecules may also be affected by temperature acclimation. 8. The metabolism of putative synaptic neurotransmitters (5-hydroxytryptamine, adrenaline, noradrenaline) is altered in the frog and mouse brains during the early phases of temperature acclimation. These changes may initiate the physiological processes connected with temperature acclimation. 9. The neuromuscular transmission in the frog shows after acclimation to cold, increased resistance to it and some indications of temperature compensation. 10. Changes in neurosecretion seem to be involved in temperature acclimation both in poikilotherms and homeotherms. The fast axonal transport of proteins shows compensatory acclimation to cold in the frog.     

The role of antennae in the thermopreference and biting response of haematophagous bugs

Insects sense thermal cues mainly through thermoreceptors located in the antenna. To analyse the impact of antennectomy on the thermal behaviour of the haematophagous bug Triatomainfestans, we studied the distribution of intact and antennectomised bugs in an experimental arena where a temperature gradient was established, as well as the biting response of insects with and without antennae to objects at the temperature of a potential host. Antennectomy did not abolish thermopreference, but modified the temperature at which the insects preferred to stay. In the arena, antennectomised insects chose to remain at a higher temperature (ca. 3 °C higher in unfed bugs), and exhibited a larger dispersion around that preferred temperature, than intact bugs. In addition, ablated insects temporarily lost their ability to bite an object at the temperature of a potential host, but that ability was gradually recovered after the fifth day post-antennectomy. Results presented here show that thermoreceptors other than those located on the antennae can also guide thermal behaviours. We conclude that the function of antennal thermoreceptors can be taken over by other receptors located in different regions of the body. Those receptors have a different sensitivity and confer the insects with a different responsiveness.     

Effects of evolutionary thermal environment on temperature-preference relationships in fishes

Fishes exhibit a perplexing variety of temperature-preference relationships, ranging from positive to negative functions of acclimation temperature. However, these relationships tend to be consistent within species even across broad geographic ranges. We developed and tested an hypothesis that temperature-preference relationships are related to the amplitude of the annual thermal-cycle experienced by species during their recent evolutionary histories. Species experiencing annual cycles of relatively high amplitude (temperate species) were predicted to exhibit temperature-preference relationships that are positive functions of acclimation temperature. Those with low thermal amplitudes, such as cold stenotherms, or relatively high short-term amplitudes, such as tropical mesotherms, were predicted to exhibit relationships that are either independent or negative functions of acclimation temperature. This hypothesis was tested and strongly supported by a synthesis of studies from the literature. Of 42 species, for which data were available, 40 exhibited the class of temperature-preference relationships that we predicted on the basis of their thermal cycle. The concept of thermal guilds can be expanded by taking into consideration the capacity of fishes to adjust preferred temperatures through acclimation. This work shows the adaptive nature of temperature-preference behavior and may be useful for predicting general characteristics of temperature-preference relationships for the many species not yet examined in this regard.     

Extensive Acclimation in Ectotherms Conceals Interspecific Variation in Thermal Tolerance Limits

Species’ tolerance limits determine their capacity to tolerate climatic extremes and limit their potential distributions. Interspecific variation in thermal tolerances is often proposed to indicate climatic vulnerability and is, therefore, the subject of many recent meta-studies on differential capacities of species from climatically different habitats to deal with climate change. Most studies on thermal tolerances do not acclimate animals or use inconsistent, and insufficient, acclimation times, limiting our knowledge of the shape, duration and extent of acclimation responses. Consequently patterns in thermal tolerances observed in meta-analyses, based on data from the literature are based on inconsistent, partial acclimation and true trends may be obscured. In this study we describe time-course of complete acclimation of critical thermal minima in the tropical ectotherm Carlia longipes and compare it to the average acclimation response of other reptiles, estimated from published data, to assess how much acclimation time may contribute to observed differences in thermal limits. Carlia longipes decreased their lower critical thermal limits by 2.4°C and completed 95% of acclimation in 17 weeks. Wild populations did not mirror this acclimation process over the winter. Other reptiles appear to decrease cold tolerance more quickly (95% in 7 weeks) and to a greater extent, with an estimated average acclimation response of 6.1°C. However, without data on tolerances after longer acclimation times available, our capacity to estimate final acclimation state is very limited. Based on the subset of data available for meta-analysis, much of the variation in cold tolerance observed in the literature can be attributed to acclimation time. Our results indicate that (i) acclimation responses can be slow and substantial, even in tropical species, and (ii) interspecific differences in acclimation speed and extent may obscure trends assessed in some meta-studies. Cold tolerances of wild animals are representative of cumulative responses to recent environments, while lengthy acclimation is necessary for controlled comparisons of physiological tolerances. Measures of inconsistent, intermediate acclimation states, as reported by many studies, represent neither the realised nor the potential tolerance in that population, are very likely underestimates of species’ physiological capacities and may consequently be of limited value.     

The complex drivers of thermal acclimation and breadth in ectotherms

Thermal acclimation capacity, the degree to which organisms can alter their optimal performance temperature and critical thermal limits with changing temperatures, reflects their ability to respond to temperature variability and thus might be important for coping with global climate change. Here, we combine simulation modelling with analysis of published data on thermal acclimation and breadth (range of temperatures over which organisms perform well) to develop a framework for predicting thermal plasticity across taxa, latitudes, body sizes, traits, habitats and methodological factors. Our synthesis includes > 2000 measures of acclimation capacities from > 500 species of ectotherms spanning fungi, invertebrates, and vertebrates from freshwater, marine and terrestrial habitats. We find that body size, latitude, and methodological factors often interact to shape acclimation responses and that acclimation rate scales negatively with body size, contributing to a general negative association between body size and thermal breadth across species. Additionally, we reveal that acclimation capacity increases with body size, increases with latitude (to mid‐latitudinal zones) and seasonality for smaller but not larger organisms, decreases with thermal safety margin (upper lethal temperature minus maximum environmental temperatures), and is regularly underestimated because of experimental artefacts. We then demonstrate that our framework can predict the contribution of acclimation plasticity to the IUCN threat status of amphibians globally, suggesting that phenotypic plasticity is already buffering some species from climate change.     

Thermal acclimation in the microcrustacean Daphnia: a survey of behavioural, physiological and biochemical mechanisms

Thermal acclimation in Daphnia magna was studied on various levels to test the recent “oxygen-limited thermal tolerance” hypothesis. Preference behaviour in a thermal gradient was determined by both, ambient temperature and corresponding oxygen concentration. Swimming activity depended on aerobic energy provision and reflected the match or mismatch of oxygen supply and energy demand at different ambient temperatures. Thermal acclimation modified both types of behaviour and more slightly heat tolerance. Perfusion and haemoglobin properties turned out to be central control variables to adapt oxygen transport to varying energy demands at different ambient temperatures. Exceptional advantages of Daphnia as an experimental model organism allowed to confirm on a behavioural, physiological and biochemical level that thermal acclimation is strongly based on the adaptation of oxygen transport allowing unidirectional shifts of the thermal tolerance range to warmer or colder temperatures.