Adaptations to diving hypoxia in the heart, kidneys and splanchnic organs of harbor seals (Phoca vitulina)

Abstract

Based on forced submergence studies conducted from the 1940s to the early 1970s, it was believed that marine mammals relied primarily on anaerobic metabolism during diving (Elsner and Gooden, 1983;Butler and Jones, 1997). After a forced submergence, there was a net accumulation of lactic acid in the plasma, indicating that anaerobic glycolysis had provided ATP as the organs and tissues became hypoxic. Therefore, it was assumed that marine mammals might have enhanced enzyme activities for anaerobic glycolysis. However, showed that, on average, marine mammals do not posses significantly elevated anaerobic enzyme activities when compared with terrestrial mammals. These results were difficult to reconcile with the apparent reliance of marine mammals on anaerobic metabolism during forced submergence. In the early 1980s, Kooyman et al. (1981) established the concept of the aerobic dive limit (ADL) by measuring the post-dive blood lactate concentration in Weddell seals (Leptonycotes weddellii) following voluntary dives from an isolated ice hole in Antarctica. The ADL is defined as the longest dive that a marine mammal can make while relying principally on oxygen stored in the lungs, blood and muscles to maintain aerobic metabolism. They found that dives shorter in duration than the ADL showed no post-dive increase in blood lactic acid, indicating that metabolism had remained aerobic. By attaching time-depth recorders to free-ranging Weddell seals, they showed that most voluntary dives were within the ADL. Similar results have been dehydrogenase (HOAD) activities in their swimming muscles to maintain an aerobic, fat-based metabolism during diving. The goal of this study was to determine whether the heart, kidneys and splanchnic organs have an elevated VV(mt) and CS and HOAD activities as parallel adaptations for sustaining aerobic metabolism and normal function during hypoxia in harbor seals (Phoca vitulina).Samples of heart, liver, kidney, stomach and small intestine were taken from 10 freshly killed harbor seals and fixed in glutaraldehyde for transmission electron microscopy or frozen in liquid nitrogen for enzymatic analysis. Samples from dogs and rats were used for comparison. Within the harbor seal, the liver and stomach had the highest VV(mt). The liver also had the highest CS activity. The kidneys and heart had the highest HOAD activities, and the liver and heart had the highest lactate dehydrogenase (LDH) activities. Mitochondrial volume densities scaled to tissue-specific resting metabolic rate [VV(mt)/RMR] in the heart, liver, kidneys, stomach and small intestine of harbor seals were elevated (range 1.2-6.6×) when compared with those in the dog and/or rat. In addition, HOAD activity scaled to tissue-specific RMR in the heart and liver of harbor seals was elevated compared with that in the dog and rat (3.2× and 6.2× in the heart and 8.5× and 5.5× in the liver, respectively). These data suggest that organs such as the liver, kidneys and stomach possess a heightened ability for aerobic, fatbased metabolism dur...

Development of aerobic and anaerobic metabolism in cardiac and skeletal muscles from harp and hooded seals

“…However, seal cardiac Mb levels are more similar to terrestrial values than are skeletal muscle Mb values (Table4), suggesting that the heart does not require large endogenous O 2 stores to continue functioning during dives. That seal cardiac muscle relies primarily on aerobic pathways for ATP production is also indicated by cardiac CS and HOAD activities that were slightly higher than those reported in other large terrestrial and marine mammals (Fuson et al, 2003;Murphy et al, 1980;Ohtsuka and Gilbert, 1995). While the high CS levels are likely to be due to cardiac tissue's high metabolic rates and MT content (Driedzic et al, 1987;Sordahl et al, 1983;Winder et al, 1974), muscle metabolic rate was not measured in this study.…”

Glyceraldehyde-3-Phosphate Dehydrogenase Mediates Anoxia Response and Survival in Caenorhabditis elegans

“…However, the reduction or absence of oxygen is not always fatal to organisms; some survive days or even years of hypoxia or anoxia. For example, the harbor seal (Phoca vitulina), turtle (Chrysemys picta belli), brine shrimp (Artemia franciscana), zebrafish (Danio rerio), fruit fly (Drosophila melanogaster), and nematode (Caenorhabditis elegans) have adapted to survive oxygen deprivation (Foe and Alberts 1985;Hochachka et al 1993;Hand 1998;Padilla et al 2002;Fuson et al 2003). Thus, it is likely that various oxygen-deprivation protective mechanisms exist in metazoans.…”

High-Altitude Adaptation of Yak Based on Genetic Variants and Activity of Lactate Dehydrogenase-1

“…For example, training of athletes at high altitude leads to marked increases in muscle mitochondria density, activity of cytochrome c oxidase (involved in oxidative phosphorylation), and fructose phosphate kinase (a key enzyme in glycolysis) . Enzyme activity of heart tissue from trained dove seals also exhibits similar adaptive changes (Fuson et al 2003). However, there is variation in results reported for different animals and from different researchers.…”