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First published online May 8, 2007
Journal of Experimental Biology 210, 1687-1699 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.001925

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

Johannes Overgaard¹, Hans Gesser² and Tobias Wang^2,*

¹ National Environmental Research Institute, Aarhus University, Silkeborg, Denmark
² Department of Zoophysiology, Aarhus University, 8000 Aarhus C, Denmark

View larger version (32K): [in this window] [in a new window]   Fig. 1. Anoxic twitch force relative to twitch force under oxygenation (%) in isolated and electrically paced cardiac strips from: red-eared slider (Trachemys scripta); painted turtle (Chrysemys picta); softshelled turtle (Apalone Spinifera); European viper (Vipera berus); ball python (Python regius); American alligator (Alligator mississippiensis); edible frog (Rana esculenta); marine toad (Bufo marinus); common Carp (Cyprinus carpio); European eel (Anguilla Anguilla); Atlantic cod (Gadus morhua); rainbow trout (Oncorhynchus mykiss); guinea pig (Cavia porcellus); rat (Rattus rattus). Data are obtained from: 1(Hartmund and Gesser, 1996), 2(Bing et al., 1972), 3(Bobb and Jackson, 2005), 4(Overgaard et al., 2005), 5(Gesser and Poupa, 1978), 6(Zaar et al., 2007), 7(W.G. and T.W., unpublished), 8(Joseph et al., 2000), 9(Andersen et al., 2004), 10(Gesser, 1977), 11(McDonald and Macleod, 1971). For Python regius, CA is a preparation from Cavum arteriosum, and CP is a preparation from Cavum pulmonale. For Alligator mississippiensis, LV is left ventricle and RV is right ventricle.

View larger version (32K): [in this window] [in a new window]   Fig. 2. Major effects of anoxia on cellular energetic turnover and on intra- and extracellular environments of a turtle cardiac cell. Top: normoxic conditions; Bottom: anoxic conditions; Left: ATP production; Right: ATP consumption. Top left: 36 mol ATP are produced mol–1 glucose and waste products in the form of CO2 and water are lost to the blood; Top right: in the normoxic cell, energy is predominantly used for protein synthesis, contractile work and ion-motive pumps such as the Na+/K+ ATPase and the Ca2+ATPase that are both important for contractile performance and Ca2+ transport. Thus, the Na+ gradient established by the Na+/K+ ATPase pump is used for the extrusion of Ca2+ through the Na+/Ca2+ exchanger during relaxation. The energetic state is high with a high ATP/ADP ratio and low levels of free phosphate. Bottom left: Anaerobic respiration only produces 3 mol ATP mol–1 glucose, and the waste product lactic acid accumulates intra- and extracellularly causing intra- and extracellular acidification. The turtle shell buffers a considerable part of the lactic acidosis whereby calcium- and magnesium ions are released. During anoxia, energy state, i.e. the ATP/ADP ratio, decreases and the level of free phosphate increases. Anoxia is associated with a general metabolic depression due to translational arrest, spike and channel arrest. Moreover, mechanical work is reduced. Despite channel and spike arrest, long-term anoxia in turtles is associated with a progressive leak of K+, which accumulates in the extracellular space and cause a depolarisation.

View larger version (17K): [in this window] [in a new window]   Fig. 3. Haemodynamic changes during submersion in anoxic water at 3 or 5°C in Trachemys scripta and Chrysemys picta. [Redrawn from Herbert and Jackson (Herbert and Jackson, 1985a); Hicks and Farrell (Hicks and Farrell, 2000a) and Stecyk et al. (Stecyk et al., 2004).]

View larger version (13K): [in this window] [in a new window]   Fig. 4. Heart rates of red-eared slider Trachemys scripta in normoxic or anoxic water at 5 and 22°C. The anoxic turtles had been forcefully submerged for 22 days at 5°C and 6 h at 22°C. At this time, the vagal innervation of the heart was blocked by infusion of the cholinergic antagonist atropine, followed by infusion of the ß-adrenergic antagonist nadolol, resulting in a complete autonomic blockade of the heart. [Redrawn from Hicks and Farrell (Hicks and Farrell, 2000b).]

View larger version (14K): [in this window] [in a new window]   Fig. 5. Progressive changes in the extracellular environment of the cold anoxic turtle (C. picta) based on studies using different durations of cold anoxic exposure data. (A) [K+]o (Jackson and Ultsch, 1982), free [Ca2+]o (Jackson and Heisler, 1982) and catecholamine levels (Keiver et al., 1992) and (B) Plasma lactate and pH (Ultsch and Jackson, 1982).

View larger version (16K): [in this window] [in a new window]   Fig. 6. Effects of anoxia, hyperkalemia, acidosis, adrenaline and hypercalcemia on cardiac performance in cold-acclimated C. picta. The experiments were performed at 5°C and show isometric twitch force of ventricular strips as a percentage of untreated control force. The changes in the buffer solution were applied either (A) one by one to show the isolated effects, or (B) in sequence to investigate the combined effects. The experimental changes used were as follows: anoxia; hyperkalemia (K+ from 2.5 to 10 mmol l–1); acidosis (pH from 7.9 to 6.9); adrenaline (10 µmol l–1) and hypercalcemia (Ca2+ from 2 to 6 mmol l–1). Data are from Overgaard et al. (Overgaard et al., 2005).

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