Digestive state influences the heart rate hysteresis and rates of heat exchange in the varanid lizard Varanus rosenbergi

© The Company of Biologists LtdTo maximize the period where body temperature (Tb) exceeds ambient temperature (Ta), many reptiles have been reported to regulate heart rate (fH) and peripheral blood flow so that the rate of heat gain in a warming environment occurs more rapidly than the rate of heat loss in a cooling environment. It may be hypothesized that the rate of cooling, particularly at relatively cool Tbs, would be further reduced during postprandial periods when specific dynamic action (SDA) increases endogenous heat production (i.e. the heat increment of feeding). Furthermore, it may also be hypothesized that the increased perfusion of the gastrointestinal organs that occurs during digestion may limit peripheral blood flow and thus compromise the rate of heating. Finally, if the changes in fH are solely for the purpose of thermoregulation, there should be no associated changes in energy demand and, consequently, no hysteresis in the rate of oxygen consumption (O2). To test these hypotheses, seven individual Varanus rosenbergi were heated and cooled between 19°C and 35°C following at least 8 days fasting and then approximately 25 h after consumption of a meal (mean 10% of fasted body mass). For a given Tb between the range of 19-35°C, fH of fasting lizards was higher during heating than during cooling. Postprandial lizards also displayed a hysteresis in fH, although the magnitude was reduced in comparison with that of fasting lizards as a result of a higher fH during cooling in postprandial animals. Both for fasting and postprandial lizards, there was no hysteresis in O2 at any Tb throughout the range although, as a result of SDA, postprandial animals displayed a significantly higher O2 than fasting animals both during heating and during cooling at Tbs above 24°C. The values of fH during heating at a given Tb were the same for fasting and postprandial animals, which, in combination with a slower rate of heating in postprandial animals, suggests that a prioritization of blood flow to the gastrointestinal organs during digestion is occurring at the expense of higher rates of heating. Additionally, postprandial lizards took longer to cool at Tbs below 23°C, suggesting that the endogenous heat produced during digestion temporarily enhances thermoregulatory ability at lower temperatures, which would presumably assist V. rosenbergi during cooler periods in the natural environment by augmenting temperature-dependent physiological processes

Oxygen transfer during aerobic exercise in a varanid lizard Varanus mertensi is limited by the circulation

Oxygen transfer during sustained maximal exercise while locomoting on a treadmill at 0.33 m s(-1) was examined in a varanid lizard Varanus mertensi at 35degreesC. The rate of oxygen consumption ((V)over dot (O 2)) increased with locomotion from 3.49+/-0.75 (mean+/-S.D.) to 14.0+/-4.0 ml O-2 kg(-1) min(-1). Ventilation (V-E) increased, aided by increases in both tidal volume and frequency, in direct proportion to (V)over dot(O 2). The air convection requirement ((V)over dot(E)/(V)over dot(O 2)=27) was therefore maintained, together with arterial Pa-CO 2 and Pa-O 2. The alveolar-arterial P-O 2 difference (PA(O 2)-Pa-O 2) also remained unchanged during exercise from its value at rest, which was approximately 20 mmHg. Pulmonary diffusion for carbon monoxide (0.116+/-0.027 ml kg(-1) min(-1) mmHg(-1)) was double the value previously reported in V. exanthematicus and remained unchanged with exercise. Furthermore, exercise was associated with an increase in the arterial-venous O-2 content difference (Ca-O2-Cv(O 2)), which was assisted by a marked Bohr shift in the hemoglobin saturation curve and further unloading of venous O-2. During exercise the increase in cardiac output ((Q)over dot(tot)) did not match the increase in (V)over dot(O2) such that the blood convection requirement ((Q)over dot(tot)/(V)over dot (O 2)) decreased from the pre-exercise value of approximately 35 to 16 during exercise. Together, the results suggest that ventilation and O-2 transfer across the lung are adequate to meet the aerobic needs of V. mertensi during exercise, but the decrease in the blood convection requirement in the presence of a large arterial-venous O-2 content difference suggests that a limit in the transport of O-2 is imposed by the circulation

The influence of locomotion on air-sac pressures in little penguins

© The Company of BiologistsAir-sac pressures have been reported to oscillate with wing beat in flying magpies and with foot paddling in diving ducks. We sought to determine the impact on air-sac pressure of wing beats during swimming and of the step cycle during walking in little penguins (Eudyptula minor). Fluctuations averaged 0.16±0.06 kPa in the interclavicular air sacs, but only 0.06±0.04 kPa in the posterior thoracic sac, generating a small differential pressure between sacs of 0.06±0.02 kPa (means ± S.E.M., N=4). These fluctuations occurred at approximately 3 Hz and corresponded to wing beats during swimming, indicated by electromyograms from the pectoralis and supracoracoideus muscles. There was no abdominal muscle activity associated with swimming or exhalation, but the abdominal muscles were active with the step cycle in walking penguins, and oscillations in posterior air-sac pressure (0.08±0.038 kPa) occurred with steps. We conclude that high-frequency oscillations in differential air-sac pressure enhance access to and utilization of the O2 stores in the air sacs during a dive.D.F. Boggs, R.V. Baudinette, P.B. Frappell and P.J. Butle

Energetics of terrestrial locomotion of the platypus Ornithorhynchus anatinus

© Company of BiologistsThe platypus Ornithorhynchus anatinus Shaw displays specializations in its limb structure for swimming that could negatively affect its terrestrial locomotion. Platypuses walked on a treadmill at speeds of 0.19-1.08 m x s(-1). Video recordings were used for gait analysis, and the metabolic rate of terrestrial locomotion was studied by measuring oxygen consumption. Platypuses used walking gaits (duty factor >0.50) with a sprawled stance. To limit any potential interference from the extensive webbing on the forefeet, platypuses walk on their knuckles. Metabolic rate increased linearly over a 2.4-fold range with increasing walking speed in a manner similar to that of terrestrial mammals, but was low as a result of the relatively low standard metabolic rate of this monotreme. The dimensionless cost of transport decreased with increasing speed to a minimum of 0.79. Compared with the cost of transport for swimming, the metabolic cost for terrestrial locomotion was 2.1 times greater. This difference suggests that the platypus may pay a price in terrestrial locomotion by being more aquatically adapted than other semi-aquatic or terrestrial mammals.F.E. Fish, P.B. Frappell, R.V. Baudinette and P.M. MacFarlan

Physiological Response to Feeding in Little Penguins

© 2006 by The University of Chicago.Specific dynamic action (SDA), the increase in metabolic rate above resting levels that accompanies the processes of digestion and assimilation of food, can form a substantial part of the daily energy budget of free-ranging animals. We measured heart rate (fH) and rate of oxygen consumption ( ) in 12 little penguins while they digested a meal of sardines in order to determine whether they show specific dynamic action. In contrast to some studies of other penguin species, little penguins showed a substantial SDA, the magnitude of which was proportional to the size of the meal. The energy utilized in SDA was equivalent to 13.4% of the available energy content of the fish. Furthermore, animals such as penguins that forage in a cold environment will probably expend further energy in heating their food to body temperature to facilitate efficient digestion. It is estimated that this additional energy expenditure was equivalent to 1.6%-2.3% of the available energy content of the fish, depending on the time of year and therefore the temperature of the water. Changes in fH during digestion were qualitatively similar to those in , implying that there were no substantial circulatory adjustments during digestion and that the relationship between fH and in penguins is unaffected by digestive state

Factorial aerobic scope is independent of temperature and primarily modulated by heart rate in exercising Murray Cod (Maccullochella peelii peelii)

Several previous reports, often from studies utilising heavily instrumented animals, have indicated that for teleosts, the increase in cardiac output ( ) during exercise is mainly the result of an increase in cardiac stroke volume (VS) rather than in heart rate (fH). More recently, this contention has been questioned following studies on animals carrying less instrumentation, though the debate continues. In an attempt to shed more light on the situation, we examined the heart rates and oxygen consumption rates ( ; normalised to a mass of 1 kg, given as ) of six Murray cod (Maccullochella peelii peelii; kg) equipped with implanted fH and body temperature data loggers. Data were determined during exposure to varying temperatures and swimming speeds to encompass the majority of the biological scope of this species. An increase in body temperature (Tb) from 14°C to 29°C resulted in linear increases in (26.67-41.78 μmol min−1 kg−1) and fH (22.3-60.8 beats min−1) during routine exercise but a decrease in the oxygen pulse (the amount of oxygen extracted per heartbeat; 1.28-0.74 μmol beat−1 kg−1). During maximum exercise, the factorial increase in was calculated to be 3.7 at all temperatures and was the result of temperature-independent 2.2- and 1.7-fold increases in fH and oxygen pulse, respectively. The constant factorial increases in fH and oxygen pulse suggest that the cardiovascular variables of the Murray cod have temperature-independent maximum gains that contribute to maximal oxygen transport during exercise. At the expense of a larger factorial aerobic scope at an optimal temperature, as has been reported for species of salmon and trout, it is possible that the Murray cod has evolved a lower, but temperature-independent, factorial aerobic scope as an adaptation to the largely fluctuating and unpredictable thermal climate of southeastern Australia

Control of breathing and respiratory gas exchange in high-altitude ducks native to the Andes

We examined the control of breathing and respiratory gas exchange in six species of high-altitude duck that independently colonized the high Andes. We compared ducks from high-altitude populations in Peru (Lake Titicaca at ∼3800 m above sea level; Chancay River at ∼3000–4100 m) with closely related populations or species from low altitude. Hypoxic ventilatory responses were measured shortly after capture at the native altitude. In general, ducks responded to acute hypoxia with robust increases in total ventilation and pulmonary O2 extraction. O2 consumption rates were maintained or increased slightly in acute hypoxia, despite ∼1–2°C reductions in body temperature in most species. Two high-altitude taxa – yellow-billed pintail and torrent duck – exhibited higher total ventilation than their low-altitude counterparts, and yellow-billed pintail exhibited greater increases in pulmonary O2 extraction in severe hypoxia. In contrast, three other high-altitude taxa – Andean ruddy duck, Andean cinnamon teal and speckled teal – had similar or slightly reduced total ventilation and pulmonary O2 extraction compared with low-altitude relatives. Arterial O2 saturation (SaO2) was elevated in yellow-billed pintails at moderate levels of hypoxia, but there were no differences in SaO2 in other high-altitude taxa compared with their close relatives. This finding suggests that improvements in SaO2 in hypoxia can require increases in both breathing and haemoglobin–O2 affinity, because the yellow-billed pintail was the only high-altitude duck with concurrent increases in both traits compared with its low-altitude relative. Overall, our results suggest that distinct physiological strategies for coping with hypoxia can exist across different high-altitude lineages, even among those inhabiting very similar high-altitude habitats

Does hyperthermia constrain flight duration in a short-distance migrant?

While some migratory birds perform non-stop flights of over 11 000 km, many species only spend around 15% of the day in flight during migration, posing a question as to why flight times for many species are so short. Here, we test the idea that hyperthermia might constrain flight duration (FD) in a short-distance migrant using remote biologging technology to measure heart rate, hydrostatic pressure and body temperature in 19 migrating eider ducks (Somateria mollissima), a short-distance migrant. Our results reveal a stop-and-go migration strategy where migratory flights were frequent (14 flights day(−1)) and short (15.7 min), together with the fact that body temperature increases by 1°C, on average, during such flights, which equates to a rate of heat storage index (HSI) of 4°C h(−1). Furthermore, we could not find any evidence that short flights were limited by heart rate, together with the fact that the numerous stops could not be explained by the need to feed, as the frequency of dives and the time spent feeding were comparatively small during the migratory period. We thus conclude that hyperthermia appears to be the predominant determinant of the observed migration strategy, and suggest that such a physiological limitation to FD may also occur in other species. This article is part of the themed issue ‘Moving in a moving medium: new perspectives on flight’

Cardiovascular responses to progressive hypoxia in ducks native to high altitude in the Andes

The cardiovascular system is critical for delivering O2 to tissues. Here, we examined the cardiovascular responses to progressive hypoxia in four high-altitude Andean duck species compared with four related low-altitude populations in North America, tested at their native altitude. Ducks were exposed to stepwise decreases in inspired partial pressure of O2 while we monitored heart rate, O2 consumption rate, blood O2 saturation, haematocrit (Hct) and blood haemoglobin (Hb) concentration. We calculated O2 pulse (the product of stroke volume and the arterial–venous O2 content difference), blood O2 concentration and heart rate variability. Regardless of altitude, all eight populations maintained O2 consumption rate with minimal change in heart rate or O2 pulse, indicating that O2 consumption was maintained by either a constant arterial–venous O2 content difference (an increase in the relative O2 extracted from arterial blood) or by a combination of changes in stroke volume and the arterial–venous O2 content difference. Three high-altitude taxa (yellow-billed pintails, cinnamon teal and speckled teal) had higher Hct and Hb concentration, increasing the O2 content of arterial blood, and potentially providing a greater reserve for enhancing O2 delivery during hypoxia. Hct and Hb concentration between low- and high-altitude populations of ruddy duck were similar, representing a potential adaptation to diving life. Heart rate variability was generally lower in high-altitude ducks, concurrent with similar or lower heart rates than low-altitude ducks, suggesting a reduction in vagal and sympathetic tone. These unique features of the Andean ducks differ from previous observations in both Andean geese and bar-headed geese, neither of which exhibit significant elevations in Hct or Hb concentration compared with their low-altitude relatives, revealing yet another avian strategy for coping with high altitude

Exhaustive exercise training enhances aerobic capacity in American alligator (Alligator mississippiensis)

The oxygen transport system in mammals is extensively remodelled in response to repeated bouts of activity, but many reptiles appear to be ‘metabolically inflexible’ in response to exercise training. A recent report showed that estuarine crocodiles (Crocodylus porosus) increase their maximum metabolic rate in response to exhaustive treadmill training, and in the present study, we confirm this response in another crocodilian, American alligator (Alligator mississippiensis). We further specify the nature of the crocodilian training response by analysing effects of training on aerobic [citrate synthase (CS)] and anaerobic [lactate dehydrogenase (LDH)] enzyme activities in selected skeletal muscles, ventricular and skeletal muscle masses and haematocrit. Compared to sedentary control animals, alligators regularly trained for 15 months on a treadmill (run group) or in a flume (swim group) exhibited peak oxygen consumption rates higher by 27 and 16%, respectively. Run and swim exercise training significantly increased ventricular mass (~11%) and haematocrit (~11%), but not the mass of skeletal muscles. However, exercise training did not alter CS or LDH activities of skeletal muscles. Similar to mammals, alligators respond to exercise training by increasing convective oxygen transport mechanisms, specifically heart size (potentially greater stroke volume) and haematocrit (increased oxygen carrying-capacity of the blood). Unlike mammals, but similar to squamate reptiles, alligators do not also increase citrate synthase activity of the skeletal muscles in response to exercise