Abstract
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.
Highlights
Reported to reach a ceiling in heart and gill ventilation performance that limits their ability to increase maximum oxygen uptake rate (ṀO2max) above standard metabolic rate (SMR), resulting in falling blood oxygen levels and a transition to anaerobic metabolism[13,14,15,16,17,18,19]
We investigated the association between Tcrit and loss of oxygen delivery by quantifying absolute aerobic scope, heart rate and ventilation rate during temperature elevation
Since early literature on the physiological mechanisms underlying Tcrit in aquatic ectotherms suggested that compromised neural activity may be a critical factor for thermal tolerance 27–30, we measured the impact of elevating temperature on the ability of nerve preparations from A. astacus to conduct action potentials
Summary
Reported to reach a ceiling in heart and gill ventilation performance that limits their ability to increase maximum oxygen uptake rate (ṀO2max) above standard metabolic rate (SMR), resulting in falling blood oxygen levels and a transition to anaerobic metabolism[13,14,15,16,17,18,19]. Recent studies in a number of eurythermal temperate and tropical species have demonstrated that the cardiorespiratory system (e.g., heart and gill ventilation rates) is able to increase oxygen supply proportionally with tissue oxygen demand as temperature increases to Tcrit In these species the excess capacity for oxygen uptake beyond the SMR requirement (absolute aerobic scope), is not significantly reduced approaching the Tcrit. That eurythermal species have been evolutionarily selected for a thermally resistant cardiorespiratory system[20,24] It is argued, the OCLTT model fails to explain thermal effects on species living in environments where they frequently encounter unpredictably high temperatures, such as the tropical M. rosenbergii[24] and the intertidal Green crab (Carcinus maenas)[20]. Since early literature on the physiological mechanisms underlying Tcrit in aquatic ectotherms suggested that compromised neural activity may be a critical factor for thermal tolerance 27–30, we measured the impact of elevating temperature on the ability of nerve preparations from A. astacus to conduct action potentials
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