Over the last decade, numerous studies have investigated the role of oxygen in setting thermal tolerance in aquatic animals, and there has been particular focus on arthropods. Arthropods comprise one of the most species-rich taxonomic groups on Earth, and display great diversity in the modes of ventilation, circulation, blood oxygen transport, with representatives living both in water (mainly crustaceans) and on land (mainly insects). The oxygen and capacity limitation of thermal tolerance (OCLTT) hypothesis proposes that the temperature dependent performance curve of animals is shaped by the capacity for oxygen delivery in relation to oxygen demand. If correct, oxygen limitation could provide a mechanistic framework to understand and predict both current and future impacts of rapidly changing climate.In arthropods, most studies testing the OCLTT hypothesis have considered tolerance to thermal extremes. These studies likely operate from the philosophical viewpoint that if the model can predict these critical thermal limits, then it is more likely to also explain loss of performance at less extreme, non-lethal temperatures, for which much less data is available. Nevertheless, the extent to which lethal temperatures are influenced by limitations in oxygen supply remains unresolved. Here we critically evaluate the support and universal applicability for oxygen limitation being involved in lethal temperatures in crustaceans and insects.The relatively few studies investigating the OCLTT hypothesis at low temperature do not support a universal role for oxygen in setting the lower thermal limits in arthropods. With respect to upper thermal limits, the evidence supporting OCLTT is stronger for species relying on underwater gas exchange, while the support for OCLTT in air-breathers is weak. Overall, strongest support was found for increased anaerobic metabolism close to thermal maxima. In contrast, there was only mixed support for the prediction that aerobic scope decreases near critical temperatures, a key feature of the OCLTT hypothesis. In air-breathers, only severe hypoxia (< 2 kPa) affected heat tolerance. The discrepancies for heat tolerance between aquatic and terrestrial organisms can to some extent be reconciled by differences in the capacity to increase oxygen transport. As air-breathing arthropods are unlikely to become oxygen limited under normoxia (especially at rest), the oxygen limitation component in OCLTT does not seem to provide sufficient information to explain lethal temperatures. Nevertheless, many animals may simultaneously face hypoxia and thermal extremes and the combination of these potential stressors is particularly relevant for aquatic organisms where hypoxia (and hyperoxia) is more prevalent. In conclusion, whether taxa show oxygen limitation at thermal extremes may be contingent on their capacity to regulate oxygen uptake, which in turn is linked to their respiratory medium (air vs. water).Fruitful directions for future research include testing multiple predictions of OCLTT in the same specie...
Temperature-induced limitations on the capacity of the cardiorespiratory system to transport oxygen from the environment to the tissues, manifested as a reduced aerobic scope (maximum minus standard metabolic rate), have been proposed as the principal determinant of the upper thermal limits of fishes and other waterbreathing ectotherms. Consequently, the upper thermal niche boundaries of these animals are expected to be highly sensitive to aquatic hypoxia and other environmental stressors that constrain their cardiorespiratory performance. However, the generality of this dogma has recently been questioned, as some species have been shown to maintain aerobic scope at thermal extremes. Here, we experimentally tested whether reduced oxygen availability due to aquatic hypoxia would decrease the upper thermal limits (i.e. the critical thermal maximum, CT max ) of the estuarine red drum (Sciaenops ocellatus) and the marine lumpfish (Cyclopterus lumpus). In both species, CT max was independent of oxygen availability over a wide range of oxygen levels despite substantial (>72%) reductions in aerobic scope. These data show that the upper thermal limits of waterbreathing ectotherms are not always linked to the capacity for oxygen transport. Consequently, we propose a novel metric for classifying the oxygen dependence of thermal tolerance; the oxygen limit for thermal tolerance (P CTmax ), which is the water oxygen tension (Pw O2 ) where an organism's CT max starts to decline. We suggest that this metric can be used for assessing the oxygen sensitivity of upper thermal limits in water-breathing ectotherms, and the susceptibility of their upper thermal niche boundaries to environmental hypoxia.
The effect of salinity on resting oxygen uptake was measured in the perch Perca fluviatilis and available information on oxygen uptake in teleost species at a variety of salinities was reviewed. Trans-epithelial ion transport against a concentration gradient requires energy and exposure to salinities osmotically different from the body fluids therefore imposes an energetic demand that is expected to be lowest in brackish water compared to fresh and sea water. Across species, there is no clear trend between oxygen uptake and salinity, and estimates of cost of osmotic and ionic regulation vary from a few per cent to >30% of standard metabolism.
In aquatic environments, rising water temperatures reduce water oxygen content while increasing oxygen demand, leading several authors to propose cardiorespiratory oxygen transport capacity as the main determinant of aquatic animal fitness. It has also been argued that tropical species, compared with temperate species, live very close to their upper thermal limit and hence are vulnerable to even small elevations in temperature. Little, however, is known about physiological responses to high temperatures in tropical species. Here we report that the tropical giant freshwater shrimp (Macrobrachium rosenbergii) maintains normal growth when challenged by a temperature rise of 6°C above the present day average (from 27°C to 33°C). Further, by measuring heart rate, gill ventilation rate, resting and maximum oxygen uptake, and hemolymph lactate, we show that oxygen transport capacity is maintained up to the critical maximum temperature around 41°C. In M. rosenbergii heart rate and gill ventilation rate increases exponentially until immediately below critical temperatures and at 38°C animals still retained more than 76% of aerobic scope measured at 30°C, and there was no indication of anaerobic metabolism at the high temperatures. Our study shows that the oxygen transport capacity is maintained at high temperatures, and that other mechanisms, such as protein dysfunction, are responsible for the loss of ecological performance at elevated temperatures.
Thermal sensitivity of the cardiorespiratory oxygen supply capacity has been proposed as the cardinal link underlying the upper boundary of the temperature niche in aquatic ectotherms. Here we examined the evidence for this link in two eurythermal decapods, the Giant tiger shrimp (Penaeus monodon) and the European crayfish (Astacus astacus). We found that both species have a temperature resistant cardiorespiratory system, capable of maintaining oxygen delivery up to their upper critical temperature (Tcrit). In neither species was Tcrit reduced in hypoxia (60% air saturation) and both species showed an exponential increase in heart and gill ventilation rates up to their Tcrit. Further, failure of action potential conduction in preparations of A. astacus motor neurons coincided with Tcrit, indicating that compromised nervous function may provide the underlying determinant for Tcrit rather than oxygen delivery. At high temperatures, absolute aerobic scope was maintained in P. monodon, but reduced in A. astacus. However, A. astacus also displayed reduced exercise intensity indicating that impaired muscle performance with resulting reduced tissue oxygen demand may explain the reduced scope rather than insufficient oxygen supply capacity. This interpretation agrees with early literature on aquatic ectotherms, correlating loss of nervous function with impaired locomotion as temperatures approach Tcrit.
The changes in ocean chemistry stemming from anthropogenic CO2 release--termed ocean acidification (OA)--are predicted to have wide-ranging effects on fish and ultimately threaten global populations. The ability of fish to adapt to environmental change is currently unknown, but phenotypic plasticity has been highlighted as a crucial factor in determining species resilience. Here we show that red drum, a long-lived estuarine-dependent fish species native to the Gulf of Mexico, exhibit respiratory plasticity that increases CO2 excretion capacity when acclimated to OA conditions. Specifically, fish exposed to 14 days of 1000 µatm CO2 had a 32% reduction in branchial diffusion distance and increased expression of two putative CO2 channel proteins--rhag and rhcg1. No changes were observed in the erythrocyte CO2 transport pathways. Surprisingly, no significant changes in blood chemistry were observed between acclimated and acutely challenged animals; however, a non-significant 30 % drop in the magnitude of plasma C(CO2) elevation was observed. Reduced diffusion distance also comes with the cost of increased diffusive water loss, which would require greater osmoregulatory investment by the animal. OA exposure induced increased gill Na(+), K(+) ATPase activity and intestinal nkcc2 expression, supporting both the presumed osmotic stress and increased osmoregulatory investment. However, no differences in standard metabolic rate, maximum metabolic rate or aerobic scope were detected between control and OA acclimated individuals. Similarly, no differences in critical swim speed were detected between groups, suggesting the energetic cost related to respiratory plasticity is negligible against background metabolism. The current study demonstrated that red drum exhibit respiratory plasticity with only mild physiological trade-offs; however, this plasticity is insufficient to fully offset the OA-induced acid-base disturbance and as such is unlikely to impact species resilience.
Rising ocean temperatures are predicted to cause a poleward shift in the distribution of marine fishes occupying the extent of latitudes tolerable within their thermal range boundaries. A prevailing theory suggests that the upper thermal limits of fishes are constrained by hypoxia and ocean acidification. However, some eurythermal fish species do not conform to this theory, and maintain their upper thermal limits in hypoxia. Here we determine if the same is true for stenothermal species. In three coral reef fish species we tested the effect of hypoxia on upper thermal limits, measured as critical thermal maximum (CT). In one of these species we also quantified the effect of hypoxia on oxygen supply capacity, measured as aerobic scope (AS). In this species we also tested the effect of elevated CO (simulated ocean acidification) on the hypoxia sensitivity of CT We found that CT was unaffected by progressive hypoxia down to approximately 35 mmHg, despite a substantial hypoxia-induced reduction in AS. Below approximately 35 mmHg, CT declined sharply with water oxygen tension (O). Furthermore, the hypoxia sensitivity of CT was unaffected by elevated CO Our findings show that moderate hypoxia and ocean acidification do not constrain the upper thermal limits of these tropical, stenothermal fishes.
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