Some like it hot: Thermal tolerance and oxygen supply capacity in two eurythermal crustaceans

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.

Oxygen-dependence of upper thermal limits in fishes

“…These studies, performed on a range of species, found that AS is maintained in normoxia at environmentally relevant temperature extremes (Ern et al, 2015;Gräns et al, 2014;Norin et al, 2014), or showed that experimentally induced anemia (internal hypoxia) has very little effect on CT max (Brijs et al, 2015;Wang et al, 2014). The present study bridges these earlier studies, and confirms their findings, by showing an uncoupling of AS and CT max when fish are exposed to environmental (ambient) hypoxia.…”

“…It has also been suggested that oxygen-dependent upper thermal limits identified in the laboratory represent those in the field (Giomi et al, 2014;Pörtner and Knust, 2007). However, the link between oxygen supply capacity and upper thermal limits has recently been questioned, as other studies have reported that aerobic scope (AS, the difference between the maximum metabolic rate, MMR, and the standard metabolic rate, SMR) and cardiorespiratory performance are maintained in a number of fish and crustacean species experiencing ecologically relevant thermal extremes (Brijs et al, 2015;Clark et al, 2013;Ern et al, 2015Ern et al, , 2014Gräns et al, 2014;Healy and Schulte, 2012;Jost et al, 2012;Norin et al, 2014). It has, therefore, been suggested that some species possess a more thermally resistant cardiorespiratory system (Ern et al, 2014;Jost et al, 2012), and that insufficient tissue oxygen supply is not the primary determinant of upper thermal limits in all water-breathing ectotherms (Brijs et al, 2015;Wang et al, 2014).…”

Thermal acclimation and subspecies-specific effects on heart and brain mitochondrial performance in a eurythermal teleost (Fundulus heteroclitus)

“…Alternatively, temperature-induced declines in neural function are suggested to constrain thermal performance limits (Somero and DeVries, 1967;Ern et al, 2015;Cossins, 1977;Jastroch et al, 2007;Miller and Stillman, 2012). However, the relative importance of these organ systems in setting an organism's thermal performance limits is still subject to debate (Clark et al, 2013;Ern et al, 2015).…”

DIVING IN A WARMING WORLD: Thermal constraints on the diving capacity of estuarine crocodiles (Crocodylus porosus)

“…A narrowed aerobic scope is hypothesised to translate into a reduced capacity for activities including growth, movement, digestion and reproduction (Pörtner, 2002), and the thermal effects on individuals may scale up to affect population and community dynamics (Pörtner and Peck, 2010). Reduced aerobic capacity at high temperatures is apparent in many tropical ectotherms Nilsson et al, 2009;Johansen and Jones, 2011;Rummer et al, 2014); however the OCLTT hypothesis is not universally applicable Ern et al, 2014;Norin et al, 2014;Ern et al, 2015;Ern et al, 2016).…”

“…disrupted nervous function (Ern et al, 2015), oxidative damage (Lushchak and Bagnyukova, 2006), enzyme inactivation (Sharpe and DeMichele, 1977;Schoolfield et al, 1981) and protein denaturation (Hofmann and Somero, 1995;Tomanek, 2015).…”