Tribute to P. L. Lutz: cardiac performance and cardiovascular regulation during anoxia/hypoxia in freshwater turtles

Abstract

SUMMARY Freshwater turtles overwintering in ice-covered ponds in North America may be exposed to prolonged anoxia, and survive this hostile environment by metabolic depression. Here, we review their cardiovascular function and regulation, with particular emphasis on the factors limiting cardiac performance. The pronounced anoxia tolerance of the turtle heart is based on the ability to match energy consumption with the low anaerobic ATP production during anoxia. Together with a well-developed temporal and spatial energy buffering by creatine kinase, this allows for cellular energy charge to remain high during anoxia. Furthermore, the turtle heart is well adapted to handle the adverse effects of free phosphate arising when phosphocreatine stores are used. Anoxia causes tenfold reductions in heart rate and blood flows that match the metabolic depression, and blood pressure is largely maintained through increased systemic vascular resistance. Depression of the heart rate is not driven by the autonomic nervous system and seems to arise from direct effects of oxygen lack and the associated hyperkalaemia and acidosis on the cardiac pacemaker. These intra- and extracellular changes also affect cardiac contractility, and both acidosis and hyperkalaemia severely depress cardiac contractility. However, increased levels of adrenaline and calcium may, at least partially, salvage cardiac function under prolonged periods of anoxia.

Circulating nitric oxide metabolites and cardiovascular changes in the turtleTrachemys scriptaduring normoxia, anoxia and reoxygenation

“…Also, the lower heart rate in the present study is probably due to long breath-holds and high vagal tone, which indicates that the turtles were undisturbed and unstressed. Consistent with previous studies on turtles, anoxia caused significant reductions in heart rate and systemic arterial pressure (Hicks and Wang, 1998;Stecyk et al, 2004;Overgaard et al, 2007). Although blood flow was not measured in the present study, earlier studies at a similar temperature have demonstrated a peripheral vasoconstriction mediated by increased sympathetic tone on the systemic vessels (Stecyk et al, 2004), and that H 2 S generation may play some role, particularly at low temperatures (Stecyk et al, 2010).…”

“…Hicks and Wang, 1998; Stecyk et al, 2004;Overgaard et al, 2007). Large variation in heart rates amongst studies can be expected due to the pronounced tachycardia during pulmonary ventilation and the bradycardia associated with apnoea (e.g.…”

“…In contrast to mammals, where particularly the heart and brain are extremely sensitive to even brief periods of anoxia, freshwater turtles, including Trachemys scripta, survive weeks of anoxia during winter when submerged under icecovered ponds or several hours at room temperature (Ultsch and Jackson, 1982;Herbert and Jackson, 1985). This is achieved by a core of adaptations: (1) strong metabolic depression (whereby a reduced anaerobic energy supply is at balance with a reduced energy demand), (2) reorganization of blood flow to the most vital organs, (3) utilization of the shell calcium carbonate to buffer metabolic acidosis and high lactate levels, and (4) constitutively high levels of antioxidants, including thiols, that act as a redox buffer against reactive oxygen species generated at reoxygenation (Jackson, 2000;Hermes-Lima and Zenteno-Savín, 2002;Nilsson and Lutz, 2004;Bickler and Buck, 2007;Overgaard et al, 2007;Jackson and Ultsch, 2010). However, the molecular mechanisms underlying these extreme adaptive responses to low O 2 remain to be fully understood.…”

Diving strategy of Amyda cartilaginea (Boddaert, 1770) and Cuora amboinensis (Daudin, 1802) in the perspective of respiratory structure and function

“…There are many studies about respiratory system related to the diving strategy of some turtle species. They are dominated by studies on sea turtle [8][9][10][11][12][13], while the studies on softshells turtle and terrapene only on turtles' species from America and other regions except South East Asia [14][15][16].…”

Light-dark dependence of electrocardiographic changes during asphyxia and reoxygenation in a rat model

“…Acute systemic asphyxia causes profound electrophysiologic dysfunction in the conductive system of the myocardium, which affects sinus node function, the atrioventricular (AV) node refractory period [14][15][16], PQ interval [17][18][19], distribution of refractory periods [19], and changes in heart rate [20,21], as well as the threshold for ventricular arrhythmias [22].…”