Potentially conflicting metabolic demands of diving and exercise in seals

Metabolic replacement rates (Ra) for glucose and free fatty acids (FFA) were determined during rest, exercise, and diving conditions in the gray seal using bolus injections of radiotracers. In the exercise experiments the seal swam at a metabolic rate elevated twofold over resting Ra for glucose and FFA while resting were similar to values found in terrestrial mammals and other marine mammal species. During exercise periods glucose turnover increased slightly while FFA turnover changes were variable. However, the energetic demands of exercise could not be met by the increase in the replacement rates of glucose or FFA even if both were completely oxidized. Under diving conditions the tracer pool displayed radically different specific activity curves indicative of the changes in perfusion and metabolic rate associated with a strong dive response. Since the radiotracer curves during exercise and diving differed qualitatively and quantitatively, it is possible that similar studies on freely diving animals can be used to assess the role of the diving response during underwater swimming in nature.     

Heart rate and plasma lactate responses during submerged swimming and trained diving in California sea lions, Zalophus californianus

California sea lions, Zalophus californianus, were trained to elicit maximum voluntary breath holds during stationary underwater targeting, submerged swimming, and trained diving. Lowest heart rate during rest periods was 57 bpm. The heart rate profiles in all three protocols were dominated by a bradycardia of 20–50 bpm, and demonstrated that otariid diving heart rates were at or below resting heart rate. Venous blood samples were collected after submerged swimming periods of 1–3 min. Plasma lactate began to increase only after 2.3-min submersions. This rise in lactate and our inability to train sea lions to dive or swim submerged for periods longer than 3 min lead us to conclude that an aerobic limit had been reached. Due to the similarity of heart rate responses and swimming velocities recorded during submerged swimming and trained diving, this 2.3-min limit should approximate the aerobic dive limit in these 40-kg sea lions. Total body O₂ stores, based on measurements of blood and muscle O₂ stores in these animals, and prior lung O₂ store analyses, were 37–43 ml O₂ kg⁻¹. The aerobic dive limit, calculated with these O₂ stores and prior measurements of at-sea metabolic rates of sea lions, is 1.8–2 min, similar to that measured by the change in post-submersion lactate concentration. Accepted: 7 July 1996     

Decreased exercise muscle lactate release after high altitude acclimatization

Blood lactate concentration during exercise decreases after acclimatization to high altitude, but it is not clear whether there is decreased lactate release from the exercising muscle or if other mechanisms are involved. We measured iliac venous and femoral arterial lactate concentrations and iliac venous blood flow during cycle exercise before and after acclimatization to 4,300 m. During hypoxia, at a given O2 consumption the venous and arterial lactate concentrations, the venous and arterial concentration differences, and the net lactate release were lower after acclimatization than during acute altitude exposure. While breathing O2-enriched air after acclimatization at a given O2 consumption the venous and arterial lactate concentrations and the venous and arterial concentration differences were significantly lower, and the net lactate release tended to be lower than while breathing ambient air at sea level before acclimatization. We conclude that the lower lactate concentration in venous and arterial blood during exercise after altitude acclimatization reflected less net release of lactate by the exercising muscles, and that this likely resulted from the acclimatization process itself rather than the hypoxia per se.     

Metabolic and work efficiencies during exercise in Andean natives

Maximum O2 and CO2 fluxes during exercise were less perturbed by hypoxia in Quechua natives from the Andes than in lowlanders. In exploring how this was achieved, we found that, for a given work rate, Quechua highlanders at 4,200 m accumulated substantially less lactate than lowlanders at sea level normoxia (approximately 5-7 vs. 10-14 mM) despite hypobaric hypoxia. This phenomenon, known as the lactate paradox, was entirely refractory to normoxia-hypoxia transitions. In lowlanders, the lactate paradox is an acclimation; however, in Quechuas, the lactate paradox is an expression of metabolic organization that did not deacclimate, at least over the 6-wk period of our study. Thus it was concluded that this metabolic organization is a developmentally or genetically fixed characteristic selected because of the efficiency advantage of aerobic metabolism (high ATP yield per mol of substrate metabolized) compared with anaerobic glycolysis. Measurements of respiratory quotient indicated preferential use of carbohydrate as fuel for muscle work, which is also advantageous in hypoxia because it maximizes the yield of ATP per mol of O2 consumed. Finally, minimizing the cost of muscle work was also reflected in energetic efficiency as classically defined (power output per metabolic power input); this was evident at all work rates but was most pronounced at submaximal work rates (efficiency approximately 1.5 times higher than in lowlander athletes). Because plots of power output vs. metabolic power input did not extrapolate to the origin, it was concluded 1) that exercise in both groups sustained a significant ATP expenditure not convertible to mechanical work but 2) that this expenditure was downregulated in Andean natives by thus far unexplained mechanisms.     

The diving paradox: new insights into the role of the dive response in air-breathing vertebrates

When aquatic reptiles, birds and mammals submerge, they typically exhibit a dive response in which breathing ceases, heart rate slows, and blood flow to peripheral tissues is reduced. The profound dive response that occurs during forced submergence sequesters blood oxygen for the brain and heart while allowing peripheral tissues to become anaerobic, thus protecting the animal from immediate asphyxiation. However, the decrease in peripheral blood flow is in direct conflict with the exercise response necessary for supporting muscle metabolism during submerged swimming. In free diving animals, a dive response still occurs, but it is less intense than during forced submergence, and whole-body metabolism remains aerobic. If blood oxygen is not sequestered for brain and heart metabolism during normal diving, then what is the purpose of the dive response? Here, we show that its primary role may be to regulate the degree of hypoxia in skeletal muscle so that blood and muscle oxygen stores can be efficiently used. Paradoxically, the muscles of diving vertebrates must become hypoxic to maximize aerobic dive duration. At the same time, morphological and enzymatic adaptations enhance intracellular oxygen diffusion at low partial pressures of oxygen. Optimizing the use of blood and muscle oxygen stores allows aquatic, air-breathing vertebrates to exercise for prolonged periods while holding their breath.     

Interconnection of carbohydrate and lipid metabolism in various modes of muscle activity

The activity of hexokinase and lipase has been determined in skeletal muscles of different metabolic types and adipose tissue of untrained albino rats during two variations of predominant aerobic physical exercise: long-term swimming and long-term swimming including short-term loads (20 s) of maximal intensity (acceleration). Muscle and liver glycogen depletion, serum lactate, glucose and free fatty acids concentrations are also investigated. It is shown that long-term swimming (first variation) has promoted a decrease of both enzymatic activities in muscle fibres and an increase in lipolytic activity of the adipose tissue. During the physical exercise with the acceleration an increase in hexokinase activity occurs in response to 20 min swimming, with its maximal decrease in response to 40 min of exercise. Activity of lipase in slow-twitch oxidative fibres of soleus and in the adipose tissue increases from 20 min to the end of the exercise. Depletion of glycogen in the muscles and liver is determined in fast-twitch oxidative-glycolytic fibres and in the liver in two types of exercises, being more significant in muscles after exercise with accelerations. Concentrations of serum lactate, glucose and free fatty acids remain unchanged after both variations of swimming. So, it may be concluded that acute adaptation to the predominant aerobic physical exercise with activity under short-term loads of maximal intensity has induced a rise of the capacity of oxidative muscles to utilise endogenous and exogenous carbohydrate and lipid reserves.     

The Uses of Anaerobiosis by Amphibians and Reptiles

Amphibians and reptiles rely upon anaerobic glycolysis to supporttheir energetic requirements under a variety of circumstances.Although adult frogs derive most of the energy for muscle contractionduring intense, short-term locomotion from glycolysis, anurantadpoles have a very low rate of lactate formation during 30sec of burst swimming; instead, they rely largely on the useof phosphocreatine stores. Among squamate reptiles, the rateof lactate formation during vigorous exercise is largely relatedto the duration of activity and to body temperature. Recentstudies have shown that fossorial, limbless reptiles do notdiffer from surface-dwelling, quadrupedal species in the rateof glycolysis during intense activity. The energetics of locomotiondiffers significantly between swimming and running turtles;thus the site of activity influences the role of anaerobiosisin movement. Lactate levels increase in some frogs during callingand nest building and in some reptiles during prey capture andingestion. However, voluntary locomotion and diving by reptilesare rarelyaccompanied by an increase in lactate levels. Freshwaterturtles rely heavily on glycolysis during aquatic hibernation.Thus, it can be concluded that amphibians and reptiles derivea significant proportion of their energetic requirements fromanaerobic metabolism only under selected circumstances whenthe benefits outweigh the costs associated with the accumulationof lactate.     

Change in plasma amino acid concentrations during breath-hold diving at high altitude

We studied the plasma concentration of various amino acids in 6 Italian sport divers in Italy and at approximately 4,500 m altitude in Peru; 6 Peruvian inhabitants were examined for comparison. We attempted to create a situation of pronounced hypoxia in muscles by breath-hold diving at altitude. The diving reflex diverts blood away from muscles while diving increases central oxygen tension and prevents loss of consciousness. Differences in certain amino acids, probably related to diet, were noted between Italy and Peru. Increases in concentration of plasma alanine and some branched-chain amino acids occurred after breath-hold diving. These changes were similar to those seen after prolonged hard exercise, even though physical work was low. Hypoxia in muscles, common during hard work and during breath-hold diving at altitude, might thus be the stimulus for amino acid release from working muscles.     

Time course of muscular blood metabolites during forearm rhythmic exercise in hypoxia

O2 concentration, PO2, PCO2, pH, osmolarity, lactate (LA), and hemoglobin (Hb) concentrations in deep forearm venous blood were repeatedly measured during submaximal exercise of forearm muscles. Concentrations of arterial blood gases were determined at rest and during exercise. Experiments were conducted under normoxia and hypobaric hypoxia (PB = 465 Torr). In arterial blood, data obtained during exercise were the same as those obtained during rest under either normoxia or hypoxia. In venous muscular blood, PO2 and O2 concentration were lower at rest and during exercise in hypoxia. The muscular arteriovenous O2 difference during exercise in hypoxia was increased by no more than 10% compared with normoxia, which implied that muscular blood flow during exercise also increased by the same percentage, if we assume that exercise O2 consumption was not affected by hypoxia. Despite increased [LA], the magnitude of changes in PCO2 and pH in hypoxia were smaller than in normoxia during exercise and recovery; this finding is probably due to the increased blood buffer value induced by the greater amount of reduced Hb in hypoxia. Hence all the changes occurring in hypoxia showed that local metabolism was less affected than we expected from the decrease in arterial PO2. The rise in [Hb] that occurred during exercise was lower in hypoxia. Possible underlying mechanisms of the [Hb] rise during exercise are discussed.     

Changes in HIF-1α protein, pyruvate dehydrogenase phosphorylation, and activity with exercise in acute and chronic hypoxia

Exercise under acute hypoxia elicits a large increase in blood lactate concentration ([La](b)) compared with normoxic exercise. However, several studies in humans show that with the transition to chronic hypoxia, exercise [La](b) returns to normoxic levels. Although extensively examined over the last decades, the muscle-specific mechanisms responsible for this phenomenon remain unknown. To assess the changes in skeletal muscle associated with a transition from acute to chronic hypoxia, CD-1 mice were exposed for 24 h (24H), 1 wk (1WH), or 4 wk (4WH) to hypobaric hypoxia (equivalent to 4,300 m), exercised under 12% O(2), and compared with normoxic mice (N) at 21% O(2). Since the enzyme pyruvate dehydrogenase (PDH) plays a major role in the metabolic fate of pyruvate (oxidation vs. lactate production), we assessed the changes in its activity and regulation. Here we report that when run under hypoxia, 24H mice exhibited the highest blood and intramuscular lactate of all groups, while the 1WH group approached N group values. Concomitantly, the 24H group exhibited the lowest PDH activity, associated with a higher phosphorylation (inactive) state of the Ser(232) residue of PDH, a site specific to PDH kinase-1 (PDK1). Furthermore, protein levels of PDK1 and its regulator, the hypoxia inducible factor-1α (HIF-1α), were both elevated in the 24H group compared with N and 1WH groups. Overall, our results point to a novel mechanism in muscle where the HIF-1α pathway is desensitized in the transition from acute to chronic hypoxia, leading to a reestablishment of PDH activity and a reduction in lactate production by the exercising muscles.     

Selective advantages conferred by the high performance physiology of tunas,billfishes, and dolphin fish

Tunas are extensively distributed throughout world's oceans and grow and reproduce fast enough to support one of the world's largest commercial fisheries. Yet they are apex predators living in the energy depauperate pelagic environment. It is often presumed that tunas evolved their specialized anatomy, physiology, and biochemistry to be capable of (a) high maximum swimming speeds, (b) high sustained swimming speeds, and/or (c) very efficient swimming, all of which help account for their wide distribution and reproductive success. However, a growing body of data on the energetics and physiological abilities of tunas do not support these assumptions. The three things demonstratively “high performance” about tunas, and probably other pelagic species such as marlin (Makaira spp. and Tetrapturus spp.) and dolphin fish (Coryphaena spp.), are (a) rates of somatic and gonadal growth, (b) rates of digestion, (c) rates of recovery from exhaustive exercise (i.e., clearance of muscle lactate and the concomitant acid load). All of these are energy consuming processes requiring rates of oxygen and substrate delivery above those needed by the swimming muscles for sustained propulsion and for other routine metabolic activities. I hypothesize that the ability of high performance pelagic species (tunas, billfishes, and dolphin fish) to deliver oxygen and metabolic substrates to the tissues at high rates evolved to permit rapid somatic and gonadal growth, rapid digestion, and rapid recovery from exhaustive exercise (abilities central to success in the pelagic environment), not exceptionally high sustained swimming speeds.     

Effects of PDH activation by dichloroacetate in human skeletal muscle during exercise in hypoxia

During the onset of exercise in hypoxia, the increased lactate accumulation is associated with a delayed activation of pyruvate dehydrogenase (PDH; Parolin ML, Spreit LL, Hultman E, Hollidge-Horvat MG, Jones NL, and Heigenhauser GJF. Am J Physiol Endocrinol Metab 278: E522-E534, 2000). The present study investigated whether activation of PDH with dichloroacetate (DCA) before exercise would reduce lactate accumulation during exercise in acute hypoxia by increasing oxidative phosphorylation. Six subjects cycled on two occasions for 15 min at 55% of their normoxic maximal oxygen uptake after a saline (control) or DCA infusion while breathing 11% O(2). Muscle biopsies of the vastus lateralis were taken at rest and after 1 and 15 min of exercise. DCA increased PDH activity at rest and at 1 min of exercise, resulting in increased acetyl-CoA concentration and acetylcarnitine concentration at rest and at 1 min. In the first minute of exercise, there was a trend toward a lower phosphocreatine (PCr) breakdown with DCA compared with control. Glycogenolysis was lower with DCA, resulting in reduced lactate concentration ([lactate]), despite similar phosphorylase a mole fractions and posttransformational regulators. During the subsequent 14 min of exercise, PDH activity was similar, whereas PCr breakdown and muscle [lactate] were reduced with DCA. Glycogenolysis was lower with DCA, despite similar mole fractions of phosphorylase a, and was due to reduced posttransformational regulators. The results from the present study support the hypothesis that lactate production is due in part to metabolic inertia and cannot solely be explained by an oxygen limitation, even under conditions of acute hypoxia.     

Effects of exercise in normoxia and acute hypoxia on respiratory muscle metabolites

We determined changes in rat plantaris, diaphragm, and intercostal muscle metabolites following exercise of various intensities and durations, in normoxia and hypoxia (FIO2 = 0.12). Marked alveolar hyperventilation occurred during all exercise conditions, suggesting that respiratory muscle motor activity was high. [ATP] was maintained at rest levels in all muscles during all normoxic and hypoxic exercise bouts, but at the expense of creatine phosphate (CP) in plantaris muscle and diaphragm muscle following brief exercise at maximum O2 uptake (VO2max) in normoxia. In normoxic exercise plantaris [glycogen] fell as exercise exceeded 60% VO2max, and was reduced to less than 50% control during exhaustive endurance exercise (68% VO2max for 54 min and 84% for 38 min). Respiratory muscle [glycogen] was unchanged at VO2max as well as during either type of endurance exercise. Glucose 6-phosphate (G6P) rose consistently during heavy exercise in diaphragm but not in plantaris. With all types of exercise greater than 84% VO2max, lactate concentration ([LA]) in all three muscles rose to the same extent as arterial [LA], except at VO2max, where respiratory muscle [LA] rose to less than half that in arterial blood or plantaris. Exhaustive exercise in hypoxia caused marked hyperventilation and reduced arterial O2 content; glycogen fell in plantaris (20% of control) and in diaphragm (58%) and intercostals (44%). We conclude that respiratory muscle glycogen stores are spared during exhaustive exercise in the face of substantial glycogen utilization in plantaris, even under conditions of extreme hyperventilation and reduced O2 transport. This sparing effect is due primarily to G6P inhibition of glycogen phosphorylase in diaphragm muscle. The presence of elevated [LA] in the absence of glycogen utilization suggests that increased lactate uptake, rather than lactate production, occurred in the respiratory muscles during exhaustive exercise.     

Gastrointestinal blood flow and postprandial metabolism in swimming sea bass Dicentrarchus labrax

In trout and salmon, the metabolic costs of exercise and feeding are additive, which would suggest that gastrointestinal blood flow during exercise is maintained to preserve digestive and absorptive processes related to the specific dynamic action (SDA) of food. However, in most published studies, gastrointestinal blood flow drops during swimming, hypoxia, and general stress. To test whether gastrointestinal blood flow is spared during exercise after feeding, sea bass were instrumented with flow probes to measure cardiac output and celiacomesenteric blood flow while swimming in a respirometer before and after feeding. Swimming at 2 body lengths per second (bl s(-1)) increased metabolic rate considerably more than did feeding (208% vs. 32% increase, respectively, relative to resting), and a similar pattern was observed for cardiac output. In unfed fish, resting gastrointestinal blood flow was 13.8+/-0.5 mL min(-1) kg(-1). After feeding, resting gastrointestinal blood flow increased by 82% but then decreased progressively with increasing swimming speeds. At 2 bl s(-1), gastrointestinal blood flow in fed fish was not significantly different compared with that in unfed swimming fish, and, therefore, the data do not support the gastrointestinal sparing hypothesis. The magnitude of the SDA was maintained despite the decrease in gastrointestinal blood flow and the consequent reduction in oxygen supply to the gut. An estimate of maximal oxygen flow to the gastrointestinal tract after feeding yielded 2.6 mmol O(2) h(-1) kg(-1), but this amount is not able to cover the oxygen demand of 3.16 mmol O(2) h(-1) kg(-1). Therefore, the SDA must reflect metabolic processes in tissues other than those directly perfused by the celiacomesenteric artery.     

Diving physiology of birds: a history of studies on polar species

Our knowledge of avian diving physiology has been based primarily on research with polar species. Since Scholander's 1940 monograph, research has expanded from examination of the 'diving reflex' to studies of free-diving birds, and has included laboratory investigations of oxygen stores, muscle adaptations, pressure effects, and cardiovascular/metabolic responses to swimming exercise. Behavioral and energetic studies at sea have shown that common diving durations of many avian species exceed the calculated aerobic diving limits (ADL). Current physiological research is focused on factors, such as heart rate and temperature, which potentially affect the diving metabolic rate and duration of aerobic diving.     

The effects of low-speed swimming following exhaustive exercise on metabolic recovery and swimming performance in brook trout (Salvelinus fontinalis)

Experiments were conducted to determine whether low-speed swimming during recovery from exhaustive exercise improved both metabolic recovery and performance during a swimming challenge. For these experiments, brook trout were allowed to recover from exhaustive exercise for 2 h while swimming at 0, 0.5, 1.0, or 1.5 body length (BL) s(-1) or allowed to recover from exhaustive exercise for 1, 2, or 3 h while swimming at 1.0 BL s(-1). At the appropriate interval, either (i) muscle and blood samples were removed from the fish or (ii) fish were assessed for performance (i.e., fatigue time) during a fixed-interval swimming test. Low-speed swimming during recovery from exhaustive exercise resulted in significantly longer fatigue times compared with fish recovering in still water (i.e., 0 BL s(-1)). However, swimming during recovery did not expedite recovery of muscle lactate or blood variables (e.g., lactate, osmolarity, glucose). These observations suggest that metabolic recovery and subsequent swimming performance may not be directly linked and that other factors play a role in swimming recovery in brook trout.     

Effects of acute hypobaric hypoxia and exhaustive exercise on AMP-activated protein kinase phosphorylation in rat skeletal muscle

The present study was aimed to explore the changes of phosphorylated AMP-activated protein kinase (pAMPK) level in skeletal muscle after exposure to acute hypobaric hypoxia and exhaustive exercise. Thirty-two male Sprague-Dawley (SD) rats were randomly divided into sea level and high altitude groups. The rats in high altitude group were submitted to simulated 5 000 m of high altitude in a hypobaric chamber for 24 h, and sea level group was maintained at normal conditions. All the rats were subjected to exhaustive swimming exercise. The exhaustion time was recorded. Before and after the exercise, blood lactate and glycogen content in skeletal muscle were determined; AMPK and pAMPK levels in skeletal muscle were detected by Western blot. The results showed that the exhaustion time was significantly decreased after exposure to high altitude. At the moment of exhaustion, high altitude group had lower blood lactate concentration and higher surplus glycogen content in gastrocnemius compared with sea level group. Exhaustive exercise significantly increased the pAMPK/AMPK ratio in rat skeletal muscles from both sea level and high altitude groups. However, high altitude group showed lower pAMPK/AMPK ratio after exhaustion compared to sea level group. These results suggest that, after exposure to acute hypobaric hypoxia, the decrement in exercise capacity may not be due to running out of glycogen, accumulation of lactate or disturbance in energy status in skeletal muscle.     

Aerobic metabolic scope and swimming performance in juvenile cod, Gadus morhua L.

Juvenile cod (Gadus morhua) were made to swim in a tunnel respirometer to determine the oxygen consumption during swimming at different speeds. Results were compared with measurements of standard and active metabolic rates in static respirometers before and after intense exercise. The oxygen consumption at maximum sustainable swimming speed was considerably lower than the peak oxygen consumption following exhausting exercise. It is suggested that these fish have a poorly developed system of aerobic (red) locomotor muscles which do not normally make a major demand upon oxygen consumption. Apparent specific dynamic action following feeding and repayment of oxygen debt following anaerobic exercise can each give rise to greater rates of oxygen consumption. Following exhausting exercise there is a delay of about 1 h before oxygen consumption reaches a peak level some 40% higher than the peak level observed during sustained swimming.     

Substitution of heat from exercise and digestion by ducks diving for mussels at varying depths and temperatures

Diving birds can lose significant body heat to cold water, but costs can be reduced if heat from exercising muscles or the heat increment of feeding (HIF) can substitute for thermogenesis. Potential for substitution depends jointly on the rate of heat loss, the rate of heat produced by exercise, and the level of HIF. To explore these interactions, we measured oxygen consumption by lesser scaup ducks (Aythya affinis) diving to depths of 1.2 and 2 m at thermoneutral (23°C) and sub-thermoneutral (18 and 8°C) temperatures. Birds dove while fasted and when feeding on blue mussels (Mytilus edulis). Substitution occurred if HIF or costs of diving above resting metabolic rate (RMR) were lower at 18 or 8°C than at 23°C, indicating reduction in the thermoregulatory part of RMR. For fasted scaup diving to 1.2 m, substitution from exercise heat was not apparent at either 18 or 8°C. At 2 m depth, dive costs above RMR were reduced by 5% at 18°C and by 40% at 8°C, indicating substitution. At 1.2 m depth (with voluntary intake of only 14–17% of maintenance requirements), HIF did not differ between temperatures, indicating no substitution. However, at 2 m (intake 13–25% of maintenance), substitution from HIF was 23% of metabolizable energy intake at 18°C and 22% at 8°C. These results show that even with low HIF due to low intake rates, substitution from HIF can add to substitution from the heat of exercise.