Oxygen- And Capacity-limited Thermal Tolerance Research Articles

Relatedness of hypoxia and hyperthermia tolerances in the Nile tilapia (Oreochromis niloticus) and their relationships with cardiac and gill traits

In fish, thermal and hypoxia tolerances may be functionally related, as suggested by the oxygen- and capacity-limited thermal tolerance (OCLTT) concept, which explains performance failure at high temperatures due to limitations in oxygen delivery. In this study the interrelatedness of hyperthermia and hypoxia tolerances in the Nile tilapia (Oreochromis niloticus), and their links to cardiorespiratory traits were examined. Different groups of O. niloticus (n = 51) were subjected to hypoxia and hyperthermia challenges and the O2 tension for aquatic surface respiration (ASR pO2) and critical thermal maximum (CTmax) were assessed as measurement endpoints. Gill filament length, total filament number, ventricle mass, length and width were also measured. Tolerance to hypoxia, as evidenced by ASR pO2 thresholds of the individual fish, was highly variable and varied between 0.26 and 3.39 kPa. ASR events increased more profoundly as O2 tensions decreased below 2 kPa. The CTmax values recorded for the O. niloticus individuals ranged from 43.1 to 44.8 °C (Mean: 44.2 ± 0.4 °C). Remarkably, there was a highly significant correlation between ASR pO2 and CTmax in O. niloticus (r = −0.76, p < 0.0001) with ASR pO2 increasing linearly with decreasing CTmax. There were, however, no discernible relationships between the measured cardiorespiratory properties and hypoxia or hyperthermia tolerances. The strong relationship between hypoxia and hyperthermia tolerances in this study may be related to the ability of the cardiorespiratory system to provide oxygen to respiring tissues under thermal stress, and thus provides some support for the OCLTT concept in this species, at least at the level of the entire organism.

Thermal preference does not align with optimal temperature for aerobic scope in zebrafish (Danio rerio).

Warming is predicted to have negative consequences for fishes by causing a mismatch between oxygen demand and supply, and a consequent reduction in aerobic scope (AS) and performance. This oxygen and capacity limited thermal tolerance (OCLTT) hypothesis features prominently in the literature but remains controversial. Within the OCLTT framework, we hypothesised that fish would select temperatures that maximise their AS, and thus their performance. We tested this hypothesis using intermittent flow respirometry to measure AS at, above (+2.5°C) and below (-2.5°C) the self-selected, preferred temperature (Tpref) of individual zebrafish (Danio rerio). AS was greatest 2.5°C above Tpref, which was driven by an increase in maximal metabolic rate. This mismatch between Tpref and the optimal temperature for AS suggests that factor(s) aside from AS maximisation influence the thermal preference of zebrafish.

Warmer temperature decreases the maximum length of six species of marine fishes, crustacean, and squid in New Zealand

As global oceans continue to warm and deoxygenate, it is expected that marine ectotherms will reduce in body size resulting from the interactive effects of temperature and dissolved oxygen availability. A temperature-size response describes how wild populations of ectothermic species grow faster and reach a smaller size within warmer temperatures. While temperature-size responses are well observed in marine ectotherms, the mechanisms underpinning such a reduction in body size remain debated. Here, we analyse the relative influence of temperature, dissolved oxygen concentration, and geographic location (which encompasses multiple latent variables), on the maximum body length of four fish, one crustacean, and one squid species, which inhabit shallow to deep sea (1000 m) New Zealand waters across a temperature gradient of 1.5 to 18 °C. We found that all study species displayed a temperature-size response, with the strongest response exhibited by the largest species, hoki (Macruronus novaezelandiae). We also found that temperature was more important than dissolved oxygen concentration in determining maximum body length, as dissolved oxygen levels were at or near saturation in the study area. Our results suggest that larger-bodied species may experience the strongest temperature-size responses, and support expectations from the gill-oxygen limitation theory (GOLT) and the oxygen and capacity limited thermal tolerance (OCLTT) concept that increases in oxygen demand may be size- and temperature-dependent, thus driving a reduction in maximum body length of marine ectotherms with warming.

The role of mechanistic physiology in investigating impacts of global warming on fishes.

Warming of aquatic environments as a result of climate change is already having measurable impacts on fishes, manifested as changes in phenology, range shifts and reductions in body size. Understanding the physiological mechanisms underlying these seemingly universal patterns is crucial if we are to reliably predict the fate of fish populations with future warming. This includes an understanding of mechanisms for acute thermal tolerance, as extreme heatwaves may be a major driver of observed effects. The hypothesis of gill oxygen limitation (GOL) is claimed to explain asymptotic fish growth, and why some fish species are decreasing in size with warming; but its underlying assumptions conflict with established knowledge and direct mechanistic evidence is lacking. The hypothesis of oxygen- and capacity-limited thermal tolerance (OCLTT) has stimulated a wave of research into the role of oxygen supply capacity and thermal performance curves for aerobic scope, but results vary greatly between species, indicating that it is unlikely to be a universal mechanism. As thermal performance curves remain important for incorporating physiological tolerance into models, we discuss potentially fruitful alternatives to aerobic scope, notably specific dynamic action and growth rate. We consider the limitations of estimating acute thermal tolerance by a single rapid measure whose mechanism of action is not known. We emphasise the continued importance of experimental physiology, particularly in advancing our understanding of underlying mechanisms, but also the challenge of making this knowledge relevant to the more complex reality.

Heat tolerance and thermal preference of the copepod Tigriopus californicus are insensitive to ecologically relevant dissolved oxygen levels

Shifting climate patterns may impose novel combinations of abiotic conditions on animals, yet understanding of the present-day interactive effects of multiple stressors remains under-developed. We tested the oxygen and capacity limited thermal tolerance (OCLTT) hypothesis and quantified environmental preference of the copepod Tigriopus californicus, which inhabits rocky-shore splashpools where diel fluctuations of temperature and dissolved oxygen (DO) are substantial. Egg-mass bearing females were exposed to a 5 h heat ramp to peak temperatures of 34.1–38.0 °C crossed with each of four oxygen levels: 22, 30, 100 and 250% saturation (4.7–5.3, 5.3–6.4, 21.2–21.3, and 50.7–53.3 kPa). Survival decreased at higher temperatures but was independent of DO. The behavioral preference of females was quantified in seven combinations of gradients of both temperature (11–37 °C) and oxygen saturation (17–206% or 3.6–43.6 kPa). Females avoided high temperatures regardless of DO levels. This pattern was more pronounced when low DO coincided with high temperature. In uniform temperature treatments, the distribution shifted toward high DO levels, especially in uniform high temperature, confirming that Tigriopus can sense environmental pO2. These results question the ecological relevance of OCLTT for Tigriopus and raise the possibility of microhabitat selection being used within splashpool environments to avoid physiologically stressful combinations of conditions.

Seasonal cellular stress responses of commercially important invertebrates at different habitats of the North Aegean Sea

In many aquatic species, the negative effect of temperature variations has a significant impact on physiological performance since beyond Tp (upper pejus) and Tc (critical temperatures), according to the oxygen- and capacity-limited thermal tolerance (OCLTT), transition to hypoxemia and mitochondrial metabolism triggers the increase in reactive oxygen species (ROS) production. However, climate change may have different spatial impact, and as a result, areas with more favorable climatic conditions (refugia) can be identified. The aim of the present study, based on cellular stress responses, is the demarcation of these areas and the preservation of commercially important marine species. Under this prism, individuals of the species Callinectes sapidus (blue crab), Sepia officinalis (common cuttlefish), Holothuria tubulosa (sea cucumber) and Venus verrucosa (clam) from Thermaikos, Pagasitikos and Vistonikos gulf were collected seasonally. The results showed an increase in the levels of several stress indicators exhibiting the triggering of Heat Shock Response, MAPK activation, apoptotic phenomena and increased ubiquitilination during the summer sampling in relation to the spring and autumn samplings concerning blue crab and clam, while no changes were observed for common cuttlefish and sea cucumber. It seems that these cellular responses consist a cytoprotective mechanism against environmental thermal stress. Regarding collection sites, for all examined species, higher cellular stress levels were observed in Pagasitikos, and lower in Vistonikos gulf. This analysis of biochemical and molecular markers is expected to provide a clearer picture for the definition of “refugia” for the above species.

Using aerobic exercise to evaluate sub-lethal tolerance of acute warming in fishes

ABSTRACTWe investigated whether fatigue from sustained aerobic swimming provides a sub-lethal endpoint to define tolerance of acute warming in fishes, as an alternative to loss of equilibrium (LOE) during a critical thermal maximum (CTmax) protocol. Two species were studied, Nile tilapia (Oreochromis niloticus) and pacu (Piaractus mesopotamicus). Each fish underwent an incremental swim test to determine gait transition speed (UGT), where it first engaged the unsteady anaerobic swimming mode that preceded fatigue. After suitable recovery, each fish was exercised at 85% of their own UGT and warmed 1°C every 30 min, to identify the temperature at which they fatigued, denoted as CTswim. Fish were also submitted to a standard CTmax, warming at the same rate as CTswim, under static conditions until LOE. All individuals fatigued in CTswim, at a mean temperature approximately 2°C lower than their CTmax. Therefore, if exposed to acute warming in the wild, the ability to perform aerobic metabolic work would be constrained at temperatures significantly below those that directly threatened survival. The collapse in performance at CTswim was preceded by a gait transition qualitatively indistinguishable from that during the incremental swim test. This suggests that fatigue in CTswim was linked to an inability to meet the tissue oxygen demands of exercise plus warming. This is consistent with the oxygen and capacity limited thermal tolerance (OCLTT) hypothesis, regarding the mechanism underlying tolerance of warming in fishes. Overall, fatigue at CTswim provides an ecologically relevant sub-lethal threshold that is more sensitive to extreme events than LOE at CTmax.

Thermal performance of the European flat oyster, Ostrea edulis (Linnaeus, 1758)—explaining ecological findings under climate change

Climate change challenges marine organisms by constraining their temperature-dependent scope for performance, fitness, and survival. According to the concept of Oxygen and Capacity Limited Thermal Tolerance (OCLTT), the overall thermal performance curve relates to an organism’s aerobic power budget, its overall aerobic scope for growth, exercise, reproduction, and other performances. We hypothesize that physiological principles shaping tolerance in extant ecosystems have also been operative during climatic changes in the distant past. To compare response patterns in extant fauna and their palaeo-relatives, we started here by studying the metabolic background of performance in the European flat oyster Ostrea edulis at organismic and cellular levels, focusing on the acute thermal window and the metabolic changes towards upper lethal temperatures. We investigated the response of the oysters (pre-acclimated at 12 °C) to a short-term warming protocol (by 2 °C every 48 h) from 14 to 36 °C which we identified as the lethal temperature. At the organismic level, heart and filtration rates were recorded. Gill metabolites were studied by 1H NMR spectroscopy to address thermal responses at the cellular level. Feeding activity by O. edulis (assessed by the filtration rates) was highest between 18 and 24 °C when overall energy expenditure (indicated by heart rate as a proxy for routine metabolic rate) was moderate. We conclude that this range reflects the thermal optimum of this species. Beyond 26 °C, the gill tissue of O. edulis became partly anaerobic, and cardiac dysfunction (arrhythmia) developed at 28 °C followed by an Arrhenius break point (30 °C). This mirrors performance constraints and indicates a wide temperature range of passive tolerance which may be a long-standing characteristic of ostreids supporting survival in extreme environments as well as during past and present climate oscillations.

The effect of ambient oxygen on the thermal performance of a cockroach, Nauphoeta cinerea.

The oxygen and capacity-limited thermal tolerance (OCLTT) hypothesis proposes that the thermal tolerance of an animal is shaped by its capacity to deliver oxygen in relation to oxygen demand. Studies testing this hypothesis have largely focused on measuring short-term performance responses in animals under acute exposure to critical thermal maximums. The OCLTT hypothesis, however, emphasises the importance of sustained animal performance over acute tolerance. The present study tested the effect of chronic hypoxia and hyperoxia during development on moderate to long-term performance indicators at temperatures spanning the optimal temperature for growth in the speckled cockroach, Nauphoeta cinerea In contrast to the predictions of the OCLTT hypothesis, development under hypoxia did not significantly reduce growth rate or running performance, and development under hyperoxia did not significantly increase growth rate or running performance. The effects of developmental temperature and oxygen on tracheal morphology and metabolic rate were also not consistent with OCLTT predictions, suggesting that oxygen delivery capacity is not the primary driver shaping thermal tolerance in this species. Collectively, these findings suggest that the OCLTT hypothesis does not explain moderate to long-term thermal performance in N.cinerea, which raises further questions about the generality of the hypothesis.

Hypoxia but not shy-bold phenotype mediates thermal preferences in a threatened freshwater fish, Notropis percobromus.

For ectothermic animals, ambient temperature strongly influences developmental growth rate and individual fitness. While many ectotherms live in environments that are spatially hetero-thermal, the coupling between behavioural phenotypes (e.g., shy or bold behaviour) and thermal preferences remains uncertain. Relative to shy counterparts, bolder phenotypes may exert higher preference for ambient temperatures that are closer to their thermal optimum, thereby accelerating development. In addition, ectotherms should select colder temperatures in low oxygen conditions (hypoxia) according to the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis. Using wild caught carmine shiner (Notropis percobromus), this study examined thermoregulatory behaviour in individuals exhibiting consistent behavioural phenotypes along the shy-bold continuum and between ecologically relevant normal oxygen concentration (normoxic) and hypoxic treatments. Furthermore, the behaviour observed in the laboratory was compared to environmental data from the natal stream. Results demonstrated that individual shy-bold behavioural phenotype was consistent before and after a simulated aerial predator attack, indicating consistency of behaviour across situations. Individual preferred and avoidance temperatures varied substantially, but were unrelated to shy-bold behavioural phenotypes. In contrast, individual preferred and maximum avoidance temperatures were significantly reduced in hypoxia, consistent with the OCLTT hypothesis. These findings might indicate suppressed development rates in hypoxia, not only by the limited oxygen for aerobic metabolism, but also by the preference for colder water in hypoxia. Furthermore, the tolerated thermal ranges were reduced in hypoxia. Using test conditions confirmed by field data, our study demonstrates the strong influence of oxygen availability on thermoregulatory behaviours and preferences in aquatic environments.

Oxygen limitation is not the cause of death during lethal heat exposure in an insect.

Oxygen- and capacity-limited thermal tolerance (OCLTT) is a controversial hypothesis claiming to explain variation in, and mechanistically determine, animal thermal limits. The lack of support from Insecta is typically argued to be a consequence of their high-performance respiratory systems. However, no studies have reported internal body oxygen levels during thermal ramping so it is unclear if changes in ambient gas are partially or fully offset by a compensatory respiratory system. Here we provide such an assessment by simultaneously recording haemolymph oxygen (pO2) levels-as an approximation of tissue oxygenation-while experimentally manipulating ambient oxygen and subjecting organisms to thermal extremes in a series of thermolimit respirometry experiments using pupae of the butterfly Pieris napi. The main results are that while P. napi undergo large changes in haemolymph pO2 that are positively correlated with experimental oxygen levels, haemolymph pO2 is similar pre- and post-death during thermal assays. OCLTT predicts that reduction in body oxygen level should lead to a reduction in CTmax. Despite finding the former, there was no change in CTmax across a wide range of body oxygen levels. Thus, we argue that oxygen availability is not a functional determinant of the upper thermal limits in pupae of P. napi.

Oxygen- and capacity-limited thermal tolerance: bridging ecology and physiology.

Observations of climate impacts on ecosystems highlight the need for an understanding of organismal thermal ranges and their implications at the ecosystem level. Where changes in aquatic animal populations have been observed, the integrative concept of oxygen- and capacity-limited thermal tolerance (OCLTT) has successfully characterised the onset of thermal limits to performance and field abundance. The OCLTT concept addresses the molecular to whole-animal mechanisms that define thermal constraints on the capacity for oxygen supply to the organism in relation to oxygen demand. The resulting 'total excess aerobic power budget' supports an animal's performance (e.g. comprising motor activity, reproduction and growth) within an individual's thermal range. The aerobic power budget is often approximated through measurements of aerobic scope for activity (i.e. the maximum difference between resting and the highest exercise-induced rate of oxygen consumption), whereas most animals in the field rely on lower (i.e. routine) modes of activity. At thermal limits, OCLTT also integrates protective mechanisms that extend time-limited tolerance to temperature extremes - mechanisms such as chaperones, anaerobic metabolism and antioxidative defence. Here, we briefly summarise the OCLTT concept and update it by addressing the role of routine metabolism. We highlight potential pitfalls in applying the concept and discuss the variables measured that led to the development of OCLTT. We propose that OCLTT explains why thermal vulnerability is highest at the whole-animal level and lowest at the molecular level. We also discuss how OCLTT captures the thermal constraints on the evolution of aquatic animal life and supports an understanding of the benefits of transitioning from water to land.

Temperature effects on aerobic scope and cardiac performance of European perch (Perca fluviatilis)

Several recent studies have highlighted how impaired cardiac performance at high temperatures and in hypoxia may compromise the capacity for oxygen transport. Thus, at high temperatures impaired cardiac capacity is proposed to reduce oxygen transport to a degree that lowers aerobic scope and compromises thermal tolerance (the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis). To investigate this hypothesis, we measured aerobic and cardiac performance of a eurythermal freshwater teleost, the European perch (Perca fluviatilis). Rates of oxygen consumption were measured during rest and activity at temperatures between 5°C and 27°C, and we evaluated cardiac function by in vivo measurements of heart rate and in vitro studies to determine contractility of myocardial strips. Aerobic scope increased progressively from 5°C to 21°C, after which it levelled off. Heart rate showed a similar response. We found little difference between resting and active heart rate at high temperature suggesting that increased cardiac scope during activity is primarily related to changes in stroke volume. To examine the effects of temperature on cardiac capacity, we measured isometric force development in electrically paced myocardial preparations during different combinations of temperature, pacing frequency, oxygenation and adrenergic stimulation. The force-frequency product increased markedly upon adrenergic stimulation at 21 and 27°C (with higher effects at 21°C) and the cardiac preparations were highly sensitive to hypoxia. These findings suggest that at (critically) high temperatures, cardiac output may diminish due to a decreased effect of adrenergic stimulation and that this effect may be further exacerbated if the heart becomes hypoxic. Hence cardiac limitations may contribute to the inability to increase aerobic scope at high temperatures in the European perch (Perca fluviatilis).

Impacts of Climate Variability and Change on (Marine) Animals: Physiological Underpinnings and Evolutionary Consequences.

Understanding thermal ranges and limits of organisms becomes important in light of climate change and observed effects on ecosystems as reported by the IPCC (2014). Evolutionary adaptation to temperature is presently unable to keep animals and other organisms in place; if they can these rather follow the moving isotherms. These effects of climate change on aquatic and terrestrial ecosystems have brought into focus the mechanisms by which temperature and its oscillations shape the biogeography and survival of species. For animals, the integrative concept of oxygen and capacity limited thermal tolerance (OCLTT) has successfully characterized the sublethal limits to performance and the consequences of such limits for ecosystems. Recent models illustrate how routine energy demand defines the realized niche. Steady state temperature-dependent performance profiles thus trace the thermal window and indicate a key role for aerobic metabolism, and the resulting budget of available energy (power), in defining performance under routine conditions, from growth to exercise and reproduction. Differences in the performance and productivity of marine species across latitudes relate to changes in mitochondrial density, capacity, and other features of cellular design. Comparative studies indicate how and why such mechanisms underpinning OCLTT may have developed on evolutionary timescales in different climatic zones and contributed to shaping the functional characteristics and species richness of the respective fauna. A cause-and-effect understanding emerges from considering the relationships between fluctuations in body temperature, cellular design, and performance. Such principles may also have been involved in shaping the functional characteristics of survivors in mass extinction events during earth's history; furthermore, they may provide access to understanding the evolution of endothermy in mammals and birds. Accordingly, an understanding is emerging how climate changes and variability throughout earth's history have influenced animal evolution and co-defined their success or failure from a bio-energetic point of view. Deepening such understanding may further reduce uncertainty about projected impacts of anthropogenic climate variability and change on the distribution, productivity and last not least, survival of aquatic and terrestrial species.

Integrated studies of organismal plasticity through physiological and transcriptomic approaches: examples from marine polar regions

Transcriptomic methods are now widely used in functional genomic research. The vast amount of information received from these studies comes along with the challenge of developing a precise picture of the functional consequences and the characteristic regulatory mechanisms. Here we assess recent studies in marine species and their adaptation to polar (and seasonal) cold and explore how they have been able to draw reliable conclusions from transcriptomic patterns on functional consequences in the organisms. Our analysis indicates that the interpretation of transcriptomic data suffers from insufficient understanding of the consequences for whole organism performance and fitness and comes with the risk of supporting only preliminary and superficial statements.We propose that the functional understanding of transcriptomic data may be improved by their tighter integration into overarching physiological concepts that support the more specific interpretation of the 'omics' data and, at the same time, can be developed further through embedding the transcriptomic phenomena observed. Such possibilities have not been fully exploited.In the context of thermal adaptation and limitation, we explore preliminary evidence that the concept of oxygen and capacity limited thermal tolerance (OCLTT) may provide sufficient complexity to guide the integration of such data and the development of associated functional hypotheses. At the same time, we identify a lack of methodological approaches linking genes and function to higher levels of integration, in terms of organism and ecosystem functioning, at temporal and geographical scales, to support more reliable conclusions and be predictive with respect to the effects of global changes.

Long-term hypoxia exposure alters the cardiorespiratory physiology of steelhead trout (Oncorhynchus mykiss), but does not affect their upper thermal tolerance

It has been suggested that exposure to high temperature or hypoxia may confer tolerance to the other oxygen-limited stressor (i.e., ‘cross-tolerance’). Thus, we investigated if chronic hypoxia-acclimation (>3 months at 40% air saturation) improved the steelhead trout's critical thermal maximum (CTMax), or affected key physiological variables that could impact upper thermal tolerance. Neither CTMax (24.7 vs. 25.3°C) itself, nor oxygen consumption (ṀO2), haematocrit, blood haemoglobin concentration, or heart rate differed between hypoxia- and normoxia-acclimated trout when acutely warmed. However, the cardiac output (Q̇) of hypoxia-acclimated fish plateaued earlier compared to normoxia-acclimated fish due to an inability to maintain stroke volume (SV), and this resulted in a ~50% lower maximum Q̇. Despite this reduced maximum cardiac function, hypoxia-acclimated trout were able to consume more O2 per volume of blood pumped as evidenced by the equivalent ṀO2. These results provide additional evidence that long-term hypoxia improves tissue oxygen utilization, and that this compensates for diminished cardiac pumping capacity. The limited SV in hypoxia-acclimated trout in vivo was not associated with changes in cardiac morphology or in vitro maximum SV, but the affinity and density of myocardial ß-adrenoreceptors were lower and higher, respectively, than in normoxia-acclimated fish. These data suggest that alterations in ventricular filling dynamics or myocardial contractility constrain cardiac function in hypoxia-acclimated fish at high temperatures. Our results do not support (1) ‘cross-tolerance’ between high temperature and hypoxia when hypoxia is chronic, or (2) that cardiac function is always the determinant of temperature-induced changes in fish ṀO2, and thus thermal tolerance, as suggested by the oxygen- and capacity-limited thermal tolerance (OCLTT) theory.

Lake Baikal amphipods under climate change: thermal constraints and ecological consequences

AbstractLake Baikal, the world's most voluminous freshwater lake, has experienced unprecedented warming during the last decades. A uniquely diverse amphipod fauna inhabits the littoral zone and can serve as a model system to identify the role of thermal tolerance under climate change. This study aimed to identify sublethal thermal constraints in two of the most abundant endemic Baikal amphipods, Eulimnogammarus verrucosus and Eulimnogammarus cyaneus, and Gammarus lacustris, a ubiquitous gammarid of the Holarctic. As the latter is only found in some shallow isolated bays of the lake, we further addressed the question whether rising temperatures could promote the widespread invasion of this non‐endemic species into the littoral zone. Animals were exposed to gradual temperature increases (4 week, 0.8 °C/d; 24 h, 1 °C/h) starting from the reported annual mean temperature of the Baikal littoral (6 °C). Within the framework of oxygen‐ and capacity‐limited thermal tolerance (OCLTT), we used a nonlinear regression approach to determine the points at which the changing temperature‐dependence of relevant physiological processes indicates the onset of limitation. Limitations in ventilation representing the first limits of thermal tolerance (pejus (= “getting worse”) temperatures (Tp)) were recorded at 10.6 (95% confidence interval; 9.5, 11.7), 19.1 (17.9, 20.2), and 21.1 (19.8, 22.4) °C in E. verrucosus, E. cyaneus, and G. lacustris, respectively. Field observations revealed that E. verrucosus retreated from the upper littoral to deeper and cooler waters once its Tp was surpassed, identifying Tp as the ecological thermal boundary. Constraints in oxygen consumption at higher than critical temperatures (Tc) led to an exponential increase in mortality in all species. Exposure to short‐term warming resulted in higher threshold values, consistent with a time dependence of thermal tolerance. In conclusion, species‐specific limits to oxygen supply capacity are likely key in the onset of constraining (beyond pejus) and then life‐threatening (beyond critical) conditions. Ecological consequences of these limits are mediated through behavioral plasticity in E. verrucosus. However, similar upper thermal limits in E. cyaneus (endemic, Baikal) and G. lacustris (ubiquitous, Holarctic) indicate that the potential invader G. lacustris would not necessarily benefit from rising temperatures. Secondary effects of increasing temperatures remain to be investigated.

Partitioning the metabolic scope: the importance of anaerobic metabolism and implications for the oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis.

Ongoing climate change is predicted to affect the distribution and abundance of aquatic ectotherms owing to increasing constraints on organismal physiology, in particular involving the metabolic scope (MS) available for performance and fitness. The oxygen- and capacity-limited thermal tolerance (OCLTT) hypothesis prescribes MS as an overarching benchmark for fitness-related performance and assumes that any anaerobic contribution within the MS is insignificant. The MS is typically derived from respirometry by subtracting standard metabolic rate from the maximal metabolic rate; however, the methodology rarely accounts for anaerobic metabolism within the MS. Using gilthead sea bream (Sparus aurata) and Trinidadian guppy (Poecilia reticulata), this study tested for trade-offs (i) between aerobic and anaerobic components of locomotor performance; and (ii) between the corresponding components of the MS. Data collection involved measuring oxygen consumption rate at increasing swimming speeds, using the gait transition from steady to unsteady (burst-assisted) swimming to detect the onset of anaerobic metabolism. Results provided evidence of the locomotor performance trade-off, but only in S. aurata. In contrast, both species revealed significant negative correlations between aerobic and anaerobic components of the MS, indicating a trade-off where both components of the MS cannot be optimized simultaneously. Importantly, the fraction of the MS influenced by anaerobic metabolism was on average 24.3 and 26.1% in S. aurata and P. reticulata, respectively. These data highlight the importance of taking anaerobic metabolism into account when assessing effects of environmental variation on the MS, because the fraction where anaerobic metabolism occurs is a poor indicator of sustainable aerobic performance. Our results suggest that without accounting for anaerobic metabolism within the MS, studies involving the OCLTT hypothesis could overestimate the metabolic scope available for sustainable activities and the ability of individuals and species to cope with climate change.

Pragmatic perspective on aerobic scope: peaking, plummeting, pejus and apportioning.

A major challenge for fish biologists in the 21st century is to predict the biotic effects of global climate change. With marked changes in biogeographic distribution already in evidence for a variety of aquatic animals, mechanistic explanations for these shifts are being sought, ones that then can be used as a foundation for predictive models of future climatic scenarios. One mechanistic explanation for the thermal performance of fishes that has gained some traction is the oxygen and capacity-limited thermal tolerance (OCLTT) hypothesis, which suggests that an aquatic organism's capacity to supply oxygen to tissues becomes limited when body temperature reaches extremes. Central to this hypothesis is an optimum temperature for absolute aerobic scope (AAS, loosely defined as the capacity to deliver oxygen to tissues beyond a basic need). On either side of this peak for AAS are pejus temperatures that define when AAS falls off and thereby reduces an animal's absolute capacity for activity. This article provides a brief perspective on the potential uses and limitations of some of the key physiological indicators related to aerobic scope in fishes. The intent is that practitioners who attempt predictive ecological applications can better recognize limitations and make better use of the OCLTT hypothesis and its underlying physiology.

Physiological ecology meets climate change.

In this article, we pointed out that understanding the physiology of differential climate change effects on organisms is one of the many urgent challenges faced in ecology and evolutionary biology. We explore how physiological ecology can contribute to a holistic view of climate change impacts on organisms and ecosystems and their evolutionary responses. We suggest that theoretical and experimental efforts not only need to improve our understanding of thermal limits to organisms, but also to consider multiple stressors both on land and in the oceans. As an example, we discuss recent efforts to understand the effects of various global change drivers on aquatic ectotherms in the field that led to the development of the concept of oxygen and capacity limited thermal tolerance (OCLTT) as a framework integrating various drivers and linking organisational levels from ecosystem to organism, tissue, cell, and molecules. We suggest seven core objectives of a comprehensive research program comprising the interplay among physiological, ecological, and evolutionary approaches for both aquatic and terrestrial organisms. While studies of individual aspects are already underway in many laboratories worldwide, integration of these findings into conceptual frameworks is needed not only within one organism group such as animals but also across organism domains such as Archaea, Bacteria, and Eukarya. Indeed, development of unifying concepts is relevant for interpreting existing and future findings in a coherent way and for projecting the future ecological and evolutionary effects of climate change on functional biodiversity. We also suggest that OCLTT may in the end and from an evolutionary point of view, be able to explain the limited thermal tolerance of metazoans when compared to other organisms.