Capacity-limited Thermal Tolerance Hypothesis Research Articles

Advances in understanding the impacts of global warming on marine fishes farmed offshore: Sparus aurata as a case study.

Monitoring variations in proteins involved in metabolic processes, oxidative stress responses, cell signalling and protein homeostasis is a powerful tool for developing hypotheses of how environmental variations affect marine organisms' physiology and biology. According to the oxygen- and capacity-limited thermal tolerance hypothesis, thermal acclimation mechanisms such as adjusting the activities of enzymes of intermediary metabolism and of antioxidant defence mechanisms, inducing heat shock proteins (Hsps) or activating mitogen-activated protein kinases may all shift tolerance windows. Few studies have, however, investigated the molecular, biochemical and organismal responses by fishes to seasonal temperature variations in the field to link these to laboratory findings. Investigation of the impacts of global warming on fishes farmed offsore, in the open sea, can provide a stepping stone towards understanding effects on wild populations because they experience similar environmental fluctuations. Over the last 30 years, farming of the gilthead sea bream Sparus aurata (Linnaeus 1758) has become widespread along the Mediterranean coastline, rendering this species a useful case study. Based on available information, the prevailing seasonal temperature variations expose the species to the upper and lower limits of its thermal range. Evidence for this includes oxygen restriction, reduced feeding, reduced responsiveness to environmental stimuli, plus a range of molecular and biochemical indicators that change across the thermal range. Additionally, close relationships between biochemical pathways and seasonal patterns of metabolism indicate a connection between energy demand and metabolic processes on the one hand, and cellular stress responses such as oxidative stress, inflammation and autophagy on the other. Understanding physiological responses to temperature fluctuations in fishes farmed offshore can provide crucial background information for the conservation and successful management of aquaculture resources in the face of global change.

Temperature-related heart rate in water and air and a comparison to other temperature-related measures of performance in the fiddler crab Leptuca pugilator (Bosc 1802).

Performance in poikilotherms is known to be sensitive to temperature, often with a low-sloping increase with temperature to a peak, and a steep decline with increasing temperature past the peak. We complemented past measures of performance by measuring heartbeat rates of the fiddler crab Leptuca pugilator in water and in air as a function of a range of temperatures previously shown to affect other measures of performance. In water over a range of 20-50°C, heartbeat increased steadily to a peak at 40°C and then steeply declined to near zero at 50°C. In air, heartbeat also increased, but to a peak at 35°C and then with a gentler decline than was found in water. Part of this different response may be due to evaporative water loss, which reduced body temperature in air, and therefore thermal stress, relative to body temperature when crabs were immersed in water. Increased availability of oxygen from air, according to the oxygen and capacity-limited thermal tolerance hypothesis, likely increased aerobic scope past the thermal peak, relative to within water, where oxygen delivery at higher temperatures may have been curtailed. We compared the heart rate performance relations to two previous measures of performance - endurance on a treadmill and sprint speed, both done in air. The peak performance temperature increased in the order: treadmill endurance time, sprint speed, heart rate in air, and heart rate in water, which demonstrates that different performance measures give different perspectives on the relation of thermal tolerance and fitness to temperature. Endurance may therefore be the limiting upper thermal stress factor in male fiddler crabs, when on hot sand flats. Temperature preference, found to be for temperatures <30°C in air, could be a bet-hedging evolutionary strategy to avoid aerobic scope affecting endurance.

Physiological and regulatory underpinnings of geographic variation in reptilian cold tolerance across a latitudinal cline.

Understanding the mechanisms that produce variation in thermal performance is a key component to investigating climatic effects on evolution and adaptation. However, disentangling the effects of local adaptation and phenotypic plasticity in shaping patterns of geographic variation in natural populations can prove challenging. Additionally, the physiological mechanisms that cause organismal dysfunction at extreme temperatures are still largely under debate. Using the green anole, Anolis carolinensis, we integrate measures of cold tolerance (CTmin ), standard metabolic rate, heart size, blood lactate concentration and RNAseq data from liver tissue to investigate geographic variation in cold tolerance and its underlying mechanisms along a latitudinal cline. We found significant effects of thermal acclimation and latitude of origin on variation in cold tolerance. Increased cold tolerance correlates with decreased rates of oxygen consumption and blood lactate concentration (a proxy for oxygen limitation), suggesting elevated performance is associated with improved oxygen economy during cold exposure. Consistent with these results, co-expression modules associated with blood lactate concentration are enriched for functions associated with blood circulation, coagulation and clotting. Expression of these modules correlates with thermal acclimation and latitude of origin. Our findings support the oxygen and capacity-limited thermal tolerance hypothesis as a potential contributor to variation in reptilian cold tolerance. Moreover, differences in gene expression suggest regulation of the blood coagulation cascade may play an important role in reptilian cold tolerance and may be the target of natural selection in populations inhabiting colder environments.

AMPK affects thermal tolerance in decapod crustaceans

AMP‐activated protein kinase (AMPK) is a cellular master regulator of energy metabolism, that is activated during stress to ensure a stable ATP pool in the cell. Additional to substantial work on the role of AMPK in mammals, especially humans, it becomes increasingly clear that AMPK is also involved in multiple processes in marine invertebrates, like crustaceans. Following the Oxygen and Capacity‐Limited Thermal Tolerance Hypothesis (OCLTT) marine invertebrates' thermal tolerance is dependent on sufficient oxygen delivery to the tissues and subsequent cellular ATP supply. Recent work has shown AMPK activation during heat stress in the rock crab, Cancer irroratus and the lobster, Homarus americanus. However, heat stress did not activate AMPK in the green crab Carcinus maenas. In the current project we tested whether pharmaceutically activating AMPK prior to a heat stress affects subsequent thermal tolerance. We injected Metformin in C. irroratus and activated AMPK about 3 fold above control levels, without affecting HSP70 protein levels or glucose levels in the hemolymph, indicating that this treatment did not trigger a broader stress response. A subsequent progressive temperature challenge between 11 and 32°C led in the Metformin treated animals to a drop in the maximum heart rate from 150 to 100 BPM at 29 and 23°C (control vs. Metformin treated, respectively), and a drop of the critical temperature, indicated by a switch to anaerobic metabolism and lactate accumulation, from 30 to 26°C. Therefore, AMPK activation diminished thermal tolerance in C. irroratus. Injecting Metformin into C. maenas showed a 30% increase in AMPK activity in the gills, with no substantial increase in AMPK activity in the hepatopancreas or heart. First results on the effect on injecting another AMPK activator, AICAR, don't lead to a substantial increase in AMPK activity yet, and require further adjustments of the treatment protocol.Pharmaceutically activating AMPK and investigating the subsequent effect on stress tolerance will contribute to a mechanistic understanding of energy allocations during stress in the context of the dynamic energy budget framework.Support or Funding InformationSupported by a summer research fellowship from the American Physiological Society to P.L., and NSF grant DUE 1431955 to M.F.This abstract is from the Experimental Biology 2018 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.

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.

Reproductive acclimation to increased water temperature in a tropical reef fish.

Understanding the capacity of organisms to cope with projected global warming through acclimation and adaptation is critical to predicting their likely future persistence. While recent research has shown that developmental acclimation of metabolic attributes to ocean warming is possible, our understanding of the plasticity of key fitness-associated traits, such as reproductive performance, is lacking. We show that while the reproductive ability of a tropical reef fish is highly sensitive to increases in water temperature, reproductive capacity at +1.5°C above present-day was improved to match fish maintained at present-day temperatures when fish complete their development at the higher temperature. However, reproductive acclimation was not observed in fish reared at +3.0°C warmer than present-day, suggesting limitations to the acclimation possible within one generation. Surprisingly, the improvements seen in reproduction were not predicted by the oxygen- and capacity-limited thermal tolerance hypothesis. Specifically, pairs reared at +1.5°C, which showed the greatest capacity for reproductive acclimation, exhibited no acclimation of metabolic attributes. Conversely, pairs reared at +3.0°C, which exhibited acclimation in resting metabolic rate, demonstrated little capacity for reproductive acclimation. Our study suggests that understanding the acclimation capacity of reproductive performance will be critically important to predicting the impacts of climate change on biological systems.

Aerobic scope fails to explain the detrimental effects on growth resulting from warming and elevated CO2 in Atlantic halibut

As a consequence of increasing atmospheric CO2, the world's oceans are becoming warmer and more acidic. Whilst the ecological effects of these changes are poorly understood, it has been suggested that fish performance including growth will be reduced mainly as a result of limitations in oxygen transport capacity. Contrary to the predictions given by the oxygen- and capacity-limited thermal tolerance hypothesis, we show that aerobic scope and cardiac performance of Atlantic halibut (Hippoglossus hippoglossus) increase following 14-16 weeks exposure to elevated temperatures and even more so in combination with CO2-acidified seawater. However, the increase does not translate into improved growth, demonstrating that oxygen uptake is not the limiting factor for growth performance at high temperatures. Instead, long-term exposure to CO2-acidified seawater reduces growth at temperatures that are frequently encountered by this species in nature, indicating that elevated atmospheric CO2 levels may have serious implications on fish populations in the future.

Cardiorespiratory collapse at high temperature in swimming adult sockeye salmon.

Elevated summer river temperatures are associated with high in-river mortality in adult sockeye salmon (Oncorhynchus nerka) during their once-in-a-lifetime spawning migration up the Fraser River (British Columbia, Canada). However, the mechanisms underlying the decrease in whole-animal performance and cardiorespiratory collapse above optimal temperatures for aerobic scope (T opt) remain elusive for aquatic ectotherms. This is in part because all the relevant cardiorespiratory variables have rarely been measured directly and simultaneously during exercise at supra-optimal temperatures. Using the oxygen- and capacity-limited thermal tolerance hypothesis as a framework, this study simultaneously and directly measured oxygen consumption rate (MO2), cardiac output [Formula: see text], heart rate (f H), and cardiac stroke volume (V s), as well as arterial and venous blood oxygen status in adult sockeye salmon swimming at temperatures that bracketed T opt to elucidate possible limitations in oxygen uptake into the blood or internal delivery through the oxygen cascade. Above T opt, the decline in MO2max and aerobic scope was best explained by a cardiac limitation, triggered by reduced scope for f H. The highest test temperatures were characterized by a negative scope for f H, dramatic decreases in maximal [Formula: see text] and maximal V s, and cardiac dysrhythmias. In contrast, arterial blood oxygen content and partial pressure were almost insensitive to supra-optimal temperature, suggesting that oxygen delivery to and uptake by the gill were not a limiting factor. We propose that the high-temperature-induced en route mortality in migrating sockeye salmon may be at least partly attributed to physiological limitations in aerobic performance due to cardiac collapse via insufficient scope for f H. Furthermore, this improved mechanistic understanding of cardiorespiratory collapse at high temperature is likely to have broader application to other salmonids and perhaps other aquatic ectotherms.