A role for haemolymph oxygen capacity in heat tolerance of eurythermal crabs

Abstract

Heat tolerance in aquatic ectotherms is constrained by a mismatch, occurring at high temperatures, between oxygen delivery and demand which compromises the maintenance of aerobic scope. The present study analyses how the wide thermal tolerance range of an eurythermal model species, the green crab Carcinus maenas is supported and limited by its ability to sustain efficient oxygen transport to tissues. Similar to other eurytherms, C. maenas sustains naturally occurring acute warming events through the integrated response of circulatory and respiratory systems. The response of C. maenas to warming can be characterized by two phases. During initial warming, oxygen consumption and heart rate increase, while stroke volume and haemolymph oxygen partial pressure decrease. During further warming, dissolved oxygen levels in the venous compartment decrease below the threshold of full haemocyanin oxygen saturation. The progressive release of haemocyanin bound oxygen with further warming follows an exponential pattern, thereby saving energy in oxygen transport and causing an associated leveling off of metabolic rate. According to the concept of oxygen and capacity limited thermal tolerance (OCLTT), this indicates that the thermal tolerance window is widened by the increasing contribution of haemocyanin oxygen transport and associated energy savings in cardiocirculation. Haemocyanin bound oxygen sustains cardiac performance to cover the temperature range experienced by C. maenas in the field. To our knowledge this is the first study providing evidence of a relationship between thermal tolerance and blood (haemolymph) oxygen transport in a eurythermal invertebrate.

Aerobic scope does not predict the performance of a tropical eurythermal fish at elevated temperatures

“…Consistent with our findings, a study on Murray cod (Maccullochella peelii peelii) from southeastern Australia revealed that a continual increase in AS with temperature (from 14 to 29°C) was accompanied by a consistent rise in heart rate scope (Clark et al, 2005). Recent research on a eurythermal crustacean, the green crab (Carcinus maenas), showed that cardiac output remained unaffected by acute heat stress as temperature was increased from 10 to 25°C at a rate of 1°C h −1 (Giomi and Pörtner, 2013). Taken together, these results from waterbreathers resemble those recently reported for the air-breathing and semi-terrestrial cane toad (Rhinella marina) (Seebacher and Franklin, 2011;Overgaard et al, 2012).…”

“…Frederich and Pörtner, 2000;Sartoris et al, 2003;Lannig et al, 2004;Steinhausen et al, 2008;Farrell, 2009;Pörtner, 2010;Clark et al, 2011;Giomi and Pörtner, 2013). However, more chronic thermal exposures are arguably more relevant from a climate change perspective, especially if examining species that do not naturally experience broad thermal ranges over small temporal scales.…”

Can respiratory physiology predict thermal niches?

“…The well‐known progressive lowering of the affinity of oxygen‐binding proteins with increasing temperatures could explain how eurytherm crustaceans maintain efficient oxygen delivery at high temperatures. This mechanism has been demonstrated for the green crab ( Carcinus maenas ), showing that during acute heating the progressive hypoxemia and the resultant hemolymph acidosis greatly facilitated the unloading of oxygen into tissues. Thus, organisms with a good oxyregulatory ability may better tolerate high temperatures.…”

Thermal specialization across large geographical scales predicts the resilience of mangrove crab populations to global warming

“…Arterial haemolymph was withdrawn with the pipette from a hole (0.2 mm width) previously drilled through the carapace, over the pericardial sinus following Frederich and Pörtner (). Similarly, venous blood was withdrawn from the sinus below the arthrodial membrane, at the base of the fourth or fifth pereiopod (Giomi and Pörtner ). At each measurement the pipette was changed and the sensor properly washed with sterile water.…”