Oxygen delivery does not limit thermal tolerance in a tropical eurythermal crustacean

Abstract

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.

Oxygen safety margins set thermal limits in an insect model system

“…Nijhout, 2011, 2012;Kaiser et al, 2007;Klok et al, 2009;Harrison et al, 2010; and see review by Harrison and Haddad, 2011), but few other physiological parameters pertinent to OCLTT have been reported. However, recent examinations of OCLTT have found that oxygen delivery (availability) does not limit upper thermal tolerance in several insect species (including flies, cockroaches, crickets and beetles) or in the tropical eurythermal crustacean Macrobrachium rosenbergii (Mölich et al, 2012;McCue and De Los Santos, 2013;Ern et al, 2014).…”

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

“…Decrements in cardiac output, growth, swimming performance and reproductive output have been observed in ectotherms despite maintained or increased aerobic scope across the same thermal range Johansen and Jones, 2011;Healy and Schulte, 2012;Ern et al, 2014;. These findings suggest mechanisms other than oxygen demands exceeding supply/delivery capacities limit performance (Clarke et al, 2013).…”

“…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).…”

“…Ectotherms exposed to stressfully high temperatures are hypothesised to experience compromised metabolic functioning, where maximal rates of oxygen consumption decrease but resting metabolic rates increase exponentially with increasing temperature, creating an imbalance between oxygen supply and demand (oxygen-and capacity-limited thermal tolerance hypothesis, OCLTT; Pörtner, 2002). This mismatch in oxygen supply and demand is thought to constrain aerobic metabolism, depriving tissues of oxygen and subsequently causing a collapse in wholeorganism functioning and/or mortality (Pörtner, 2001(Pörtner, , 2002(Pörtner, , 2010, however support for this hypothesis is mixed (Ern et al, 2014;Norin et al, 2014).Tropical ectotherms living close to their upper thermal limits are therefore predicted to be vulnerable to even very slight rises in temperature (Sunday et al, 2014).…”

“…For example, AAS can narrow at thermal extremes Nilsson et al, 2009;Johansen and Jones., 2011;Rummer et al, 2014), continually increase with rising temperature up to lethal limits (Norin et al, 2014), or be thermally independent (Ern et al, 2014;Verhille et al, 2016;Poletto et al, 2017). Likewise, the thermal plasticity of metabolism can differ within a species depending on level of assessment (i.e.…”