Amoebic gill disease increases energy requirements and decreases hypoxia tolerance in Atlantic salmon (Salmo salar) smolts.

Globally, Atlantic salmon (Salmo salar Linnaeus) aquaculture is now routinely affected by amoebic gill disease (AGD; Neoparamoeba perurans). The disease proliferates throughout the summer and is implicated in decreasing tolerance of salmon to environmental perturbations, yet little empirical evidence exists to support these observations. Using salmon acclimated to 15 or 19 °C, our aim was to determine the effects of clinically light-moderate (industry-relevant) AGD on metabolism (MO2rest and MO2max), aerobic scope (MO2max - MO2rest), excess post-exercise oxygen consumption (EPOC), and hypoxia tolerance. An increase in MO2rest (~8% and ~ 13% increase within the 15 and 19 °C acclimation groups, respectively) with increasing disease signs demonstrated an increase in baseline energy requirements as the disease progressed. Conversely, MO2max remained stable at both temperatures (~364 mg O2 kg-1 h-1), resulting in a decline in aerobic scope by 13 and 19% in the 15 and 19 °C groups, respectively. There was evidence of a decrease in hypoxia tolerance as the dissolved oxygen concentrations at loss of equilibrium increased by ~8% with more severe lesion coverage of the gills. These results suggest an increase in basal energy requirements and reduction in hypoxia tolerance as AGD proliferates, lending support to the idea that AGD reduces environmental tolerance. However, the lack of an effect of acclimation temperature indicates that the temperature-disease interaction may be more complicated than currently thought.

Different strategies for convective O2 transport in high altitude birds: A graphical analysis.

For illustrative purposes, in this article we use "Johansen Plots" as a graphical way of simultaneously visualizing the inter-connected variables that compose the convective steps of the gas transport cascade. These plots are used to reflect on some of the physiological characteristics seen in five species of birds, four of which sojourn to, or are native to, high altitudes (the barnacle goose, bar-headed goose, Andean goose, speckled teal and ruddy duck). These species were chosen to emphasize the diversity of responses to hypoxia that can exist within a single family. This diversity likely arose for many possible reasons, including local adaptation to hypoxia, differences in flight or diving abilities, or as a result of other phylogenetically-based differences across waterfowl in physiology, behaviour, and/or life style.

The paradox of extreme high-altitude migration in bar-headed geese Anser indicus.

Bar-headed geese are renowned for migratory flights at extremely high altitudes over the world's tallest mountains, the Himalayas, where partial pressure of oxygen is dramatically reduced while flight costs, in terms of rate of oxygen consumption, are greatly increased. Such a mismatch is paradoxical, and it is not clear why geese might fly higher than is absolutely necessary. In addition, direct empirical measurements of high-altitude flight are lacking. We test whether migrating bar-headed geese actually minimize flight altitude and make use of favourable winds to reduce flight costs. By tracking 91 geese, we show that these birds typically travel through the valleys of the Himalayas and not over the summits. We report maximum flight altitudes of 7290 m and 6540 m for southbound and northbound geese, respectively, but with 95 per cent of locations received from less than 5489 m. Geese travelled along a route that was 112 km longer than the great circle (shortest distance) route, with transit ground speeds suggesting that they rarely profited from tailwinds. Bar-headed geese from these eastern populations generally travel only as high as the terrain beneath them dictates and rarely in profitable winds. Nevertheless, their migration represents an enormous challenge in conditions where humans and other mammals are only able to operate at levels well below their sea-level maxima.

An increase in minimum metabolic rate and not activity explains field metabolic rate changes in a breeding seabird.

The field metabolic rate (FMR) of a free-ranging animal can be considered as the sum of its maintenance costs (minimum metabolic rate, MMR) and additional costs associated with thermoregulation, digestion, production and activity. However, the relationships between FMR and BMR and how they relate to behaviour and extrinsic influences is not clear. In seabirds, FMR has been shown to increase during the breeding season. This is presumed to be the result of an increase in foraging activity, stimulated by increased food demands from growing chicks, but few studies have investigated in detail the factors that underlie these increases. We studied free-ranging Australasian gannets (Morus serrator) throughout their 5 month breeding season, and evaluated FMR, MMR and activity-related metabolic costs on a daily basis using the heart rate method. In addition, we simultaneously recorded behaviour (flying and diving) in the same individuals. FMR increased steadily throughout the breeding season, increasing by 11% from the incubation period to the long chick-brooding period. However, this was not accompanied by either an increase in flying or diving behaviour, or an increase in the energetic costs of activity. Instead, the changes in FMR could be explained exclusively by a progressive increase in MMR. Seasonal changes in MMR could be due to a change in body composition or a decrease in body condition associated with changing the allocation of resources between provisioning adults and growing chicks. Our study highlights the importance of measuring physiological parameters continuously in free-ranging animals in order to understand fully the mechanisms underpinning seasonal changes in physiology and behaviour.

Phylogenetic differences of mammalian basal metabolic rate are not explained by mitochondrial basal proton leak.

Metabolic rates of mammals presumably increased during the evolution of endothermy, but molecular and cellular mechanisms underlying basal metabolic rate (BMR) are still not understood. It has been established that mitochondrial basal proton leak contributes significantly to BMR. Comparative studies among a diversity of eutherian mammals showed that BMR correlates with body mass and proton leak. Here, we studied BMR and mitochondrial basal proton leak in liver of various marsupial species. Surprisingly, we found that the mitochondrial proton leak was greater in marsupials than in eutherians, although marsupials have lower BMRs. To verify our finding, we kept similar-sized individuals of a marsupial opossum (Monodelphis domestica) and a eutherian rodent (Mesocricetus auratus) species under identical conditions, and directly compared BMR and basal proton leak. We confirmed an approximately 40 per cent lower mass specific BMR in the opossum although its proton leak was significantly higher (approx. 60%). We demonstrate that the increase in BMR during eutherian evolution is not based on a general increase in the mitochondrial proton leak, although there is a similar allometric relationship of proton leak and BMR within mammalian groups. The difference in proton leak between endothermic groups may assist in elucidating distinct metabolic and habitat requirements that have evolved during mammalian divergence.

Respiratory characteristics of the tammar wallaby pouch young and functional limitations in a newborn with skin gas exchange.

A short gestation, low birth weight and presence of cutaneous exchange of O2 and CO2 comprise altricial features of newborn marsupials and that collectively implies a highly immature respiratory system. In the present study, we investigated various respiratory characteristics of the neonatal/postnatal tammar wallaby, a species of marsupial in which > 30% of the newborn's total O2 demands are supported by cutaneous rather than pulmonary gas exchange. The ventilatory response (HVR) to acute hypoxia (10% inspired O2) was absent in the newborn (1 day old) pouch young; a hypoxic hypometabolism contributed entirely to the hyperventilation (increased pulmonary convection requirement). A high (compared to older animals) resting metabolic cost to breathe and an inefficient respiratory system suggest the lack of a HVR might be due to an energetic constraint that impinges on their ability to sustain an increase in ventilation. The latter was supported by the inability of the newborn to tolerate metabolic-ventilatory stimulation following administration of the metabolic uncoupler, 2,4-dinitrophenol (2,4-DNP). At 1 week of age, the cost of breathing was reduced, which coincided with the expression of a significant ventilatory response to hypoxia, a more energetically efficient respiratory system, and tolerance to 2,4-DNP. These data suggest this species of marsupial is born with major respiratory insufficiency, and that their pronounced dependence on the skin for metabolic gas exchange is of critical importance for survival.

Aerobic and anaerobic movement energetics of hybrid and pure parental abalone.

The underlying mechanisms controlling growth heterosis in marine invertebrates remain poorly understood. We used pure blacklip (Haliotis rubra) and greenlip (Haliotis laevigata) abalone, as well as their hybrid, to test whether differences in movement and/or aerobic versus anaerobic energy use are linked to a purported increased growth rate in hybrids. Abalone were acclimated to control (16 °C) and typical summer temperatures (23 °C), each with oxygen treatments of 100% air saturation (O2sat) or 70% O2sat. The experiment then consisted of two phases. During the first phase (chronic exposure), movement and oxygen consumption rates (MO2) of abalone were measured during a 2 day observation period at stable acclimation conditions. Additionaly, lactate dehydrogenase (LDH) and tauropine dehydrogenase (TDH) activities were measured. During phase two (acute exposure), O2sat was raised to 100% for abalone acclimated to 70% O2sat followed by an acute decrease in oxygen to anoxia for all acclimation groups during which movement and MO2 were determined again. During the chronic exposure, hybrids and H. laevigata moved shorter distances than H. rubra. Resting MO2, LDH and TDH activities, however, were similar between abalone types but were increased at 23 °C compared to 16 °C. During the acute exposure, the initial increase to 100% O2sat for individuals acclimated to 70% O2sat resulted in increased movement compared to individuals acclimated to 100% O2sat for hybrids and H. rubra when compared within type of abalone. Similarly, MO2 during spontaneous activity of all three types of abalone previously subjected to 70% O2sat increased above those at 100% O2sat. When oxygen levels had dropped below the critical oxygen level (Pcrit), movement in hybrids and H. laevigata increased up to 6.5-fold compared to movement above Pcrit. Differences in movement and energy use between hybrids and pure species were not marked enough to support the hypothesis that the purportedly higher growth in hybrids is due to an energetic advantage over pure species.

Marsupial uncoupling protein 1 sheds light on the evolution of mammalian nonshivering thermogenesis.

Brown adipose tissue expressing uncoupling protein 1 (UCP1) is responsible for adaptive nonshivering thermogenesis giving eutherian mammals crucial advantage to survive the cold. The emergence of this thermogenic organ during mammalian evolution remained unknown as the identification of UCP1 in marsupials failed so far. Here, we unequivocally identify the marsupial UCP1 ortholog in a genomic library of Monodelphis domestica. In South American and Australian marsupials, UCP1 is exclusively expressed in distinct adipose tissue sites and appears to be recruited by cold exposure in the smallest species under investigation (Sminthopsis crassicaudata). Our data suggest that an archetypal brown adipose tissue was present at least 150 million yr ago allowing early mammals to produce endogenous heat in the cold, without dependence on shivering and locomotor activity.

Moving with the beat: heart rate and visceral temperature of free-swimming and feeding bluefin tuna.

Owing to the inherent difficulties of studying bluefin tuna, nothing is known of the cardiovascular function of free-swimming fish. Here, we surgically implanted newly designed data loggers into the visceral cavity of juvenile southern bluefin tuna (Thunnus maccoyii) to measure changes in the heart rate (fH) and visceral temperature (TV) during a two-week feeding regime in sea pens at Port Lincoln, Australia. Fish ranged in body mass from 10 to 21 kg, and water temperature remained at 18-19 degrees C. Pre-feeding fH typically ranged from 20 to 50 beats min(-1). Each feeding bout (meal sizes 2-7% of tuna body mass) was characterized by increased levels of activity and fH (up to 130 beats min(-1)), and a decrease in TV from approximately 20 to 18 degrees C as cold sardines were consumed. The feeding bout was promptly followed by a rapid increase in TV, which signified the beginning of the heat increment of feeding (HIF). The time interval between meal consumption and the completion of HIF ranged from 10 to 24 hours and was strongly correlated with ration size. Although fH generally decreased after its peak during the feeding bout, it remained elevated during the digestive period and returned to routine levels on a similar, but slightly earlier, temporal scale to TV. These data imply a large contribution of fH to the increase in circulatory oxygen transport that is required for digestion. Furthermore, these data oppose the contention that maximum fH is exceptional in bluefin tuna compared with other fishes, and so it is likely that enhanced cardiac stroke volume and blood oxygen carrying capacity are the principal factors allowing superior rates of circulatory oxygen transport in tuna.

Predicting rate of oxygen consumption from heart rate while little penguins work, rest and play.

The relationship between heart rate (f(H)) and rate of oxygen consumption (V(.)O2) was investigated under changing conditions of ambient temperature, digestive state and exercise state in the little penguin (Eudyptula minor). Both f(H) and V(.)O2 were recorded simultaneously from 12 little penguins while they each (a) rested and exercised within their reported thermo-neutral zone (TNZ), (b) rested and exercised below their reported TNZ and (c) digested a meal of sardines within their reported TNZ. Contrary to our expectations, we found that minimum V(.)O2 did not vary between the two temperatures used. Comparison with values from the literature suggests that both minimum V(.)O2 and the extent of the TNZ in this species may vary along a latitudinal gradient. Furthermore, while minimum V(.)O2 was unchanged at the lower temperature, minimum f(H) was significantly higher, suggesting a hitherto undescribed cardiac response to lowered ambient temperature in an avian species. This response was maintained when the penguins exercised within and below their apparent TNZ as f(H) was significantly greater in cold conditions for a given level of V(.)O2. Furthermore, both f(H) and V(.)O2 were slightly but significantly elevated for a given walking speed during exercise at the lower temperature. This suggests that the penguins may have been close to their TNZ and that the measures employed to counteract heat loss while at rest may have been compromised during exercise. There was no significant difference in the relationship between f(H) and V(.)O2 while the penguins were inactive ina post-digestive state or inactive and digesting a meal within their TNZ, though both of these relationships were significantly different from that during exercise. This suggests that while digestion has no effect on the f(H)/V(.)O2 relationship, for little penguins at least, it is of little value in deriving a predictive relationship for application to active free-ranging animals.

Thermal effects on the blood respiratory properties of southern bluefin tuna, Thunnus maccoyii.

Thermal effects on the blood respiratory properties of southern bluefin tuna (Thunnus maccoyii) at 10, 23 and 36 degrees C, and at 0.5 and 1.5% CO(2) were investigated. A reversed temperature effect occurred as the oxygen partial pressure required for 50% haemoglobin saturation (P(50)) at 0.5% CO(2) decreased from 2.9 kPa at 10 degrees C to 1.7 kPa at 23 degrees C (apparent heat of oxygenation, DeltaH degrees , =+27 kJ mol(-1)). However, oxygen binding was essentially independent of temperature at warmer temperatures (P(50)=1.7-2.0 kPa from 23-36 degrees C at 0.5% CO(2); DeltaH degrees =-6.5 kJ mol(-1)). Hill's coefficient (n(H)) ranged from 1.3 to 1.6, and there was a large effect of temperature on the Bohr factor (DeltalogP(50)/DeltapH=-1.6 at 10 degrees C and -0.9 at 36 degrees C). This is the first study of whole blood to demonstrate the thermal dependence of DeltaH degrees itself, whereby the oxygen equilibrium curve is more sensitive to temperature in the lowest thermal range examined. We suggest that the functional basis for these observations lies in the necessity to ensure a sufficient oxygen supply to all tissues, including the heart and liver, without suffering from premature or excessive oxygen unloading around the heat exchanger prior to delivery of oxygen to organs and tissues that lie efferent to the exchanger.

Improving the precision and accuracy for estimating energy expenditure using the heart rate method.

The "heart rate technique" is commonly used to estimate the rate of oxygen consumption (a proxy for energy expenditure) of free-ranging animals. However, a major limitation of this technique is that interindividual variability in the relationship between heart rate (f(H)) and rate of oxygen consumption (Vo2) generates large errors of estimation when the technique is applied to individual free-ranging animals. In this study, we present a new analysis technique that takes advantage of the observation that the f(H) or Vo2 relationships between individuals are frequently parallel and differ only in elevation. This technique offers superior accuracy and precision of Vo2 estimates, reducing the coefficient of variability from 18% to 9% for individual animals in an example application in macaroni penguins. This approach enables application of the heart rate technique to deduce the energetic strategies of individual animals.

Development of the respiratory system in marsupials.

Marsupials at birth are small and relatively undeveloped. At birth, the lung in some species is at the canalicular stage of development and though lung diffusion and metabolic rate are strongly correlated, the allometric exponent suggests that smaller newborns have relatively smaller diffusing capacity with respect to their demand for oxygen. Without improvement in functional or structural parameters newborn marsupials are reliant to varying degrees on skin gas exchange to compensate for the immaturity of the lung. Indeed, in some species there is complete reliance on the skin for gas exchange at birth. Nevertheless, with an early dependence on ventilation, the CNS would appear already to contain neurons with properties and connections that permit rhythmic motor output at birth and pulmonary reflexes mature soon after. Despite appropriate neural control and the presence of surfactant, the highly compliant nature of the newborn chest wall results in substantial chest wall distortion during inspiratory effort which reduce the efficacy of the lung for ventilation. This review explores the morpho-functional development of the respiratory system, including oxygen transport and cardiac shunts, and the establishment of convective requirement in marsupials, a group that places emphasis on extended postnatal development.

Physiological response to feeding in little penguins.

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 (VO2) 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 VO2, implying that there were no substantial circulatory adjustments during digestion and that the relationship between fH and VO2 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 (Vb) during exercise is mainly the result of an increase in cardiac stroke volume (V(S)) 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 (Mo2; normalised to a mass of 1 kg, given as Mo2kg) of six Murray cod (Maccullochella peelii peelii; mean mass+/-SE = 1.81+/-0.14 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 degrees C to 29 degrees C resulted in linear increases in Mo2kg (26.67-41.78 micromol 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 micromol beat(-1) kg(-1)). During maximum exercise, the factorial increase in Mo2kg 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.

The roller coaster flight strategy of bar-headed geese conserves energy during Himalayan migrations.

The physiological and biomechanical requirements of flight at high altitude have been the subject of much interest. Here, we uncover a steep relation between heart rate and wingbeat frequency (raised to the exponent 3.5) and estimated metabolic power and wingbeat frequency (exponent 7) of migratory bar-headed geese. Flight costs increase more rapidly than anticipated as air density declines, which overturns prevailing expectations that this species should maintain high-altitude flight when traversing the Himalayas. Instead, a "roller coaster" strategy, of tracking the underlying terrain and discarding large altitude gains only to recoup them later in the flight with occasional benefits from orographic lift, is shown to be energetically advantageous for flights over the Himalayas.

Hamsters vs. rats: metabolic and ventilatory response to development in chronic hypoxia.

The postnatal developments of the rat and hamster were compared after the animals were raised from birth for 21 days either in normoxia (control animals) or chronic hypoxia (PO2 of 80-90 Torr). Compared with control rats, hypoxic rats had a reduction in body mass. Hypoxic rats had lowered O2 consumption (VO2) and increased (67%) ventilation (VE), whereas hypoxic hamsters maintained the same metabolic rate as control hamsters but increased VE by 100%. As a result, when raised in hypoxia both species increased VE/VO2 to the same extent. When acutely exposed to hypoxia, control animals of both species increased VE (54-58%) and lowered VO2 (26%). Thus, whether the exposure to hypoxia is acute or chronic, both species hyperventilated (i.e., increased VE/VO2) to approximately the same degree. However, in the rat VO2 decreased similarly in both acute and chronic hypoxia, whereas in the hamster VO2 decreased with acute hypoxia but was maintained under chronic hypoxia. Within 1 day of the animals being returned to normoxia, metabolic and ventilatory parameters of hypoxic animals returned to control values. In conclusion, the semifossorial hamster seems better suited to development in chronic hypoxia than the surface-dwelling rat because by avoiding prolonged hypometabolism it can better maintain body growth.

Minimal metabolic rate, what it is, its usefulness, and its relationship to the evolution of endothermy: a brief synopsis.

Minimal metabolic rate represents the minimal cost of living and appears to have the same relative composition of adenosine triphosphate processes in all organisms. Minimal metabolic rate is influenced by temperature and defines the standard metabolic rate (SMR) of animals. Animals that achieve SMR only for a given temperature are strictly ectothermic. Endotherms, on the other hand, are characterized by leakier membranes and an associated increase in cellular metabolism for a given temperature. The increase in cellular metabolism is coupled with an increase in heat production (i.e., obligatory thermogenesis) that, together with SMR, defines the basal metabolic rate of an endotherm. Consideration of minimal metabolic rate must take into account ecological and physiological processes, environmental influences, evolutionary arguments, and body size.

The influence of haemoglobin on behavioural thermoregulation and oxygen consumption in Daphnia carinata.

When placed in a temperature gradient, most ectotherms have a strict thermal preference that is lowered on exposure to hypoxia. Branchiopods, small aquatic crustaceans, are known to synthesise haemoglobin (Hb) when exposed to hypoxia; hypoxia can occur diurnally and seasonally in ponds. The effect of Hb on behavioural thermoregulation in the branchiopod Daphnia carinata following exposure to both normoxia and hypoxia was examined. Control animals raised in normoxia (Po2=150 mmHg, [Hb]=0.026+/-0.007 mg g dry wt-1) and Hb-rich animals raised in hypoxia (Po2=70 mmHg, [Hb]=0.080+/-0.017 mg g dry wt-1) were placed (N=30) in a tube (length=500 mm, diameter=8 mm) filled with pond water. In the absence of a thermal gradient, control and Hb-rich animals in normoxic water were uniformly distributed along the tube. The presence of a thermal gradient (13 degrees -28 degrees C) elicited clustering at a preferred temperature, T approximately 23 degrees C for both groups. Exposure to hypoxic water in a thermal gradient resulted in a behavioural shift: T approximately 16 degrees C for controls and T approximately 19 degrees C for Hb-rich animals. Measurements of oxygen consumption (V&d2;o2) at fixed temperatures revealed that Hb is associated with a metabolic acclimation to hypoxia.

Scaling of respiratory variables and the breathing pattern in birds: an allometric and phylogenetic approach.

Allometric equations can be useful in comparative physiology in a number of ways, not the least of which include assessing whether a particular species deviates from the norm for its size and phylogenetic group with respect to some specific physiological process or determining how differences in design among groups may be reflected in differences in function. The allometric equations for respiratory variables in birds were developed 30 yr ago by Lasiewski and Calder and presented as "preliminary" because they were based on a small number of species. With the expanded data base now available to reconstruct these allometries and the call for taking account of the nonindependence of species in this process through a phylogenetically independent contrasts (PIC) approach, we have developed new allometric equations for respiratory variables in birds using both the traditional and PIC approaches. On the whole, the new equations agree with the old ones with only minor changes in the coefficients, and the primary difference between the traditional and PIC approaches is in the broader confidence intervals given by the latter. We confirm the lower VE/VO2 ratio for birds compared to mammals and observe a common scaling of inspiratory flow and oxygen consumption for birds as has been reported for mammals. Use of allometrics and comparisons among avian groups are also discussed.