Energetic Optimisation of Foraging Honeybees: Flexible Change of Strategies in Response to Environmental Challenges

Heterothermic insects like honeybees, foraging in a variable environment, face the challenge of keeping their body temperature high to enable immediate flight and to promote fast exploitation of resources. Because of their small size they have to cope with an enormous heat loss and, therefore, high costs of thermoregulation. This calls for energetic optimisation which may be achieved by different strategies. An ‘economizing’ strategy would be to reduce energetic investment whenever possible, for example by using external heat from the sun for thermoregulation. An ‘investment-guided’ strategy, by contrast, would be to invest additional heat production or external heat gain to optimize physiological parameters like body temperature which promise increased energetic returns. Here we show how honeybees balance these strategies in response to changes of their local microclimate. In a novel approach of simultaneous measurement of respiration and body temperature foragers displayed a flexible strategy of thermoregulatory and energetic management. While foraging in shade on an artificial flower they did not save energy with increasing ambient temperature as expected but acted according to an ‘investment-guided’ strategy, keeping the energy turnover at a high level (∼56–69 mW). This increased thorax temperature and speeded up foraging as ambient temperature increased. Solar heat was invested to increase thorax temperature at low ambient temperature (‘investment-guided’ strategy) but to save energy at high temperature (‘economizing’ strategy), leading to energy savings per stay of ∼18–76% in sunshine. This flexible economic strategy minimized costs of foraging, and optimized energetic efficiency in response to broad variation of environmental conditions.     

Raised thermoregulatory costs at exposed song posts increase the energetic cost of singing for willow warblers Phylloscopus trochilus

Sexually selected displays, such as bird song, are expected to be costly. We examined a novel potential cost to bird song: whether a less favourable microclimate at exposed song posts would be predicted to raise metabolic rate. We measured the microclimate and height at which willow warblers Phylloscopus trochilus sang and foraged. Song posts were higher than foraging sites. The wind speed was 0.6±0.3 ms⁻¹ greater at song posts (mean±SD, N=12 birds). Song rate and song post selection were not influenced consistently by temperature or wind speed, but the birds sang from lower positions on one particularly windy day. This may have resulted from difficulty in holding on to exposed branches in windy conditions rather than a thermoregulatory constraint. The results suggest that the extra thermoregulatory costs at song posts would increase metabolic rate by an average of 10±4% and a maximum of 25±8% (N=12 birds) relative to birds singing at foraging sites. We estimated that metabolic rate would be 3–8% greater during singing than during quiet respiration because of heat and evaporative water loss in exhaled gases. The combined energy requirements for sound production, thermoregulation at exposed song posts and additional heat loss in exhaled air could increase the metabolic rate of willow warblers by an average of 14–23%, and a maximum of 42–63%, during singing. The energetic cost of singing may thus be much greater for birds in a cold, windy environment than for birds singing in laboratory conditions.     

A hot lunch for herbivores: physiological effects of elevated temperatures on mammalian feeding ecology

Mammals maintain specific body temperatures (T_b) across a broad range of ambient temperatures. The energy required for thermoregulation ultimately comes from the diet, and so what animals eat is inextricably linked to thermoregulation. Endothermic herbivores must balance energy requirements and expenditure with complicated thermoregulatory challenges from changing thermal, nutritional and toxicological environments. In this review we provide evidence that plant‐based diets can influence thermoregulation beyond the control of herbivores, and that this can render them susceptible to heat stress. Notably, herbivorous diets often require specialised digestive systems, are imbalanced, and contain plant secondary metabolites (PSMs). PSMs in particular are able to interfere with the physiological processes responsible for thermoregulation, for example by uncoupling mitochondrial oxidative phosphorylation, binding to thermoreceptors, or because the pathways required to detoxify PSMs are thermogenic. It is likely, therefore, that increased ambient temperatures due to climate change may have greater and more‐specific impacts on herbivores than on other mammals, and that managing internal and external heat loads under these conditions could drive changes in feeding ecology.     

Ontogeny and phylogeny of endothermy and torpor in mammals and birds

Endothermic thermoregulation in small, altricial mammals and birds develops at about one third to half of adult size. The small size and consequently high heat loss in these young should result in more pronounced energetic challenges than in adults. Thus, employing torpor (a controlled reduction of metabolic rate and body temperature) during development would allow them to save energy. Although torpor during development in endotherms is likely to occur in many species, it has been documented in only a few. In small, altricial birds (4 orders) and marsupials (1 order), which are poikilothermic at hatching/birth, the development of competent endothermic thermoregulation during cold exposure appears to be concurrent with the capability to display torpor (i.e. poikilothermy is followed by heterothermy), supporting the view that torpor is phylogenetically old and likely plesiomorphic. In contrast, in small, altricial placental mammals (2 orders), poikilothermy at birth is followed first by a homeothermic phase after endothermic thermoregulation is established; the ability to employ torpor develops later (i.e. poikilothermy-homeothermy-heterothermy). This suggests that in placentals torpor is a derived trait that evolved secondarily after a homeothermic phase in certain taxa perhaps as a response to energetic challenges. As mammals and birds arose from different reptilian lineages, endothermy likely evolved separately in the two classes, and given that the developmental sequence of torpor differs between marsupials and placentals, torpor seems to have evolved at least thrice.     

Cost reduction in the cold: heat generated by terrestrial locomotion partly substitutes for thermoregulation costs in Knot Calidris canutus

To test whether heat generated during locomotion substitutes for the thermoregulation cost, oxygen consumption of four post-absorptive temperate-wintering Knot Calidris canutus was measured at air temperatures of 25̀C (thermoneutral) and 10̀C (c. 10̀ below the lower critical temperature) when the birds were at rest at night and during running on a treadmill. After allowing for body mass, the thermoregulation cost at 10̀C was significantly lower in active birds compared with birds at rest. At rest, the birds spent, on average, 0.50 watt (W; range, 0.47-0.57 W) on thermoregulation. During exercise, this cost factor averaged 0.33 W (range, 0.25-0.42 W). The average difference in thermoregulation cost was 35% (ranging from 26% to 49% between individuals) and provides an estimate of the amount of substituted heat. A review of nine studies, all restricted to small birds, showed that substitution is a widespread phenomenon. The consequences of such partial substitution for the annual energetics of Knot wintering in the temperate Wadden Sea v tropical west Africa are examined. Compared with a previous additive model, the model which includes substitution (i.e. the use of heat produced during activity) reduces the differences in maintenance metabolism between the two wintering strategies by 17%, from 1.19 W to 0.99 W.     

Thermoregulation in homeotherms: central temperature results from optimization of energy transfers

In contrast to the classical homeostatic concept of the constancy of the central temperature, this study proposes an original model of thermoregulation based on the optimization of energy transfers. Exchange of the energy consumed or produced by the cell between the cell and the external medium has an associated energy cost. The different variables of the internal medium — flows, pressures, concentrations and also temperatures, since heat is but a particular form of energy — are continuously set at optimal values such that this cost is always minimal for the prevailing constraints with which the organism is faced. The proposed thermoregulatory model accounts for the physiological spatial and temporal variability of the body's temperatures. The predictive curves suggest a new approach to experimental studies concerned with thermal regulation and throw new light on their results.     

A review of the energetics of pollination biology

Pollination biology is often associated with mutualistic interactions between plants and their animal pollen vectors, with energy rewards as the foundation for co-evolution. Energy is supplied as food (often nectar from flowers) or as heat (in sun-tracking or thermogenic plants). The requirements of pollinators for these resources depend on many factors, including the costs of living, locomotion, thermoregulation and behaviour, all of which are influenced by body size. These requirements are modified by the availability of energy offered by plants and environmental conditions. Endothermic insects, birds and bats are very effective, because they move faster and are more independent of environmental temperatures, than are ectothermic insects, but they are energetically costly for the plant. The body size of endothermic pollinators appears to be influenced by opposing requirements of the animals and plants. Large body size is advantageous for endotherms to retain heat. However, plants select for small body size of endotherms, as energy costs of larger size are not matched by increases in flight speed. If high energy costs of endothermy cannot be met, birds and mammals employ daily torpor, and large insects reduce the frequency of facultative endothermy. Energy uptake can be limited by the time required to absorb the energy or eliminate the excess water that comes with it. It can also be influenced by variations in climate that determine temperature and flowering season.     

Ontogeny of thermoregulation in precocial birds

The aim of this paper is to summarise the results of earlier experiments on thermoregulation and heat balance in birds, to present new results concerning thermoregulation during the perinatal period in precocial embryos and to develop a model of the ontogeny of thermoregulation over the whole lifespan of birds. The ontogeny of thermoregulation in precocial birds is characterised by three phases with different efficiency of the system. In the prenatal phase, all control elements of the thermoregulatory system can function, but the efficiency of the system is low. It is postulated that endothermic reactions during the prenatal period do not have a proximate (immediate), but rather an ultimate influence on the efficiency of thermoregulation. They may support adaptivity to expected environmental conditions and may be involved in epigenetic adaptation processes. During the early postnatal phase, the thermoregulatory system develops and matures. Summit metabolism and resting metabolic rate and their thermoregulatory set points increase. Preferred temperature is significantly different during different behavioural activities. The phase of full-blown homeothermy starts at approximately the 10th day of life. It is characterised by an activation order of thermoregulatory control elements and by secondary chemical thermoregulation. The influence of thermal and non-thermal climatic factors on heat production and heat loss may be described by mathematical models.     

Radiant heat affects thermoregulation and energy expenditure during rewarming from torpor

The high expenditure of energy required for endogenous rewarming is one of the widely perceived disadvantages of torpor. However, recent evidence demonstrates that passive rewarming either by the increase of ambient temperature or by basking in the sun appears to be common in heterothermic birds and mammals. As it is presently unknown how radiant heat affects energy expenditure during rewarming from torpor and little is known about how it affects normothermic thermoregulation, we quantified the effects of radiant heat on body temperature and metabolic rate of the small (body mass 25 g) marsupial Sminthopsis macroura in the laboratory. Normothermic resting individuals exposed to radiant heat were able to maintain metabolic rates near basal levels (at 0.91 ml O(2) g(-1) h(-1)) and a constant body temperature down to an ambient temperature of 12 degrees C. In contrast, metabolic rates of individuals without access to radiant heat were 4.5-times higher at an ambient temperature of 12 degrees C and body temperature fell with ambient temperature. During radiant heat-assisted passive rewarming from torpor, animals did not employ shivering but appeared to maximise uptake of radiant heat. Their metabolic rate increased only 3.2-times with a 15- degrees C rise of body temperature (Q(10)=2.2), as predicted by Q(10) effects. In contrast, during active rewarming shivering was intensive and metabolic rates showed an 11.6-times increase. Although body temperature showed a similar absolute change between the beginning and the end of the rewarming process, the overall energetic cost during active rewarming was 6.3-times greater than that during passive, radiant heat-assisted rewarming. Our study demonstrates that energetic models assuming active rewarming from torpor at low ambient temperatures can substantially over-estimate energetic costs. The low energy expenditure during passive arousal provides an alternative explanation as to why daily torpor is common in sunny regions and suggests that the prevalence of torpor in low latitudes may have been under-estimated in the past.     

Seasonal variations in the behavioural thermoregulation of roosting Humboldt penguins ( Spheniscus humboldti) in north-central Chile

We examined the thermoregulatory behaviour (TRB) of roosting Humboldt penguins (Spheniscus humboldti) in north central Chile during summer and winter, when ambient temperatures (T_a) are most extreme. Each body posture was considered to represent a particular TRB, which was ranked in a sequence that reflected different degrees of thermal load and was assigned an arbitrary thermoregulatory score. During summer, birds exhibited eight different TRBs, mainly oriented to heat dissipation, and experienced a wide range of T_a (from 14 to 31°C), occasionally above their thermoneutral zone (TNZ, from 2 to 30°C), this being evident by observations of extreme thermoregulatory responses such as panting. In winter, birds exhibited only three TRBs, mainly oriented to heat retention, and experienced a smaller range of T_a (from 11 to 18°C), always within the TNZ, even at night. The components of behavioural responses increased directly with the heat load which explains the broader behavioural repertoire observed in summer. Since penguins are primarily adapted in morphology and physiology to cope with low water temperatures, our results suggest that behavioural thermoregulation may be important in the maintenance of the thermal balance in Humboldt penguins while on land.     

Heterothermy,body size,and locomotion as ecological predictors of migration in mammals

1. Migration is ubiquitous among animals and has evolved repeatedly and independently. Comparative studies of the evolutionary origins of migration in birds are widespread, but are lacking in mammals. Mammalian species have greater variation in functional traits that may be relevant for migration. Interspecific variation in migration behaviour is often attributed to mode of locomotion (i.e. running, swimming, and flying) and body size, but traits associated with the evolutionary precursor hypothesis, including geographic distribution, habitat, and diet, could also be important predictors of migration in mammals. Furthermore, mammals vary in thermoregulatory strategies and include many heterothermic species, providing an alternative strategy to avoid seasonal resource depletion.
2. We tested the evolutionary precursor hypothesis for the evolution of migration in mammals and tested predictions linking migration to locomotion, body size, geographic distribution, habitat, diet, and thermoregulation. We compiled a dataset of 722 species from 27 mammalian orders and conducted a series of analyses using phylogenetically informed models.
3. Swimming and flying mammals were more likely to migrate than running mammals, and larger species were more likely to migrate than smaller ones. However, heterothermy was common among small running mammals that were unlikely to migrate. High-latitude swimming and flying mammals were more likely to migrate than high-latitude running mammals (where heterothermy was common), and most migratory running mammals were herbivorous. Running mammals and frugivorous bats with high thermoregulatory scope (greater capacity for heterothermy) were less likely to migrate, while insectivorous bats with high thermoregulatory scope were more likely to migrate.
4. Our results indicate a broad range of factors that influence migration, depending on locomotion, body size, and thermoregulation. Our analysis of migration in mammals provided insight into some of the general rules of migration, and we highlight opportunities for future investigations of exceptions to these rules, ultimately leading to a comprehensive understanding of the evolution of migration.

     

Thermal strategies and energetics in two sympatric colubrid snakes with contrasted exposure

The thermoregulatory strategy of reptiles should be optimal if ecological costs (predation risk and time devoted to thermoregulation) are minimized while physiological benefits (performance efficiency and energy gain) are maximized. However, depending on the exact shape of the cost and benefit curves, different thermoregulatory optima may exist, even between sympatric species. We studied thermoregulation in two coexisting colubrid snakes, the European whipsnake (Hierophis viridiflavus, Lacépède 1789) and the Aesculapian snake (Zamenis longissimus, Laurenti 1768) that diverge markedly in their exposure, but otherwise share major ecological and morphological traits. The exposed species (H. viridiflavus) selected higher body temperatures (~30°C) than the secretive species (Z. longissimus, ~25°C) both in a laboratory thermal gradient and in the field. Moreover, this difference in body temperature was maintained under thermophilic physiological states such as digestion and molting. Physiological and locomotory performances were optimized at higher temperatures in H. viridiflavus compared to Z. longissimus, as predicted by the thermal coadaptation hypothesis. Metabolic and energetic measurements indicated that energy requirements are at least twice higher in H. viridiflavus than in Z. longissimus. The contrasted sets of coadapted traits between H. viridiflavus and Z. longissimus appear to be adaptive correlates of their exposure strategies.     

Thermal and digestive constraints to foraging behaviour in marine mammals

While foraging models of terrestrial mammals are concerned primarily with optimizing time/energy budgets, models of foraging behaviour in marine mammals have been primarily concerned with physiological constraints. This has historically centred on calculations of aerobic dive limits. However, other physiological limits are key to forming foraging behaviour, including digestive limitations to food intake and thermoregulation. The ability of an animal to consume sufficient prey to meet its energy requirements is partly determined by its ability to acquire prey (limited by available foraging time, diving capabilities and thermoregulatory costs) and process that prey (limited by maximum digestion capacity and the time devoted to digestion). Failure to consume sufficient prey will have feedback effects on foraging, thermoregulation and digestive capacity through several interacting avenues. Energy deficits will be met through catabolism of tissues, principally the hypodermal lipid layer. Depletion of this blubber layer can affect both buoyancy and gait, increasing the costs and decreasing the efficiency of subsequent foraging attempts. Depletion of the insulative blubber layer may also increase thermoregulatory costs, which will decrease the foraging abilities through higher metabolic overheads. Thus, an energy deficit may lead to a downward spiral of increased tissue catabolism to pay for increased energy costs. Conversely, the heat generated through digestion and foraging activity may help to offset thermoregulatory costs. Finally, the circulatory demands of diving, thermoregulation and digestion may be mutually incompatible. This may force animals to alter time budgets to balance these exclusive demands. Analysis of these interacting processes will lead to a greater understanding of the physiological constraints within which the foraging behaviour must operate.     

Lower haematocrit,haemoglobin and red blood cell number in zebra finches acclimated to cold compared to thermoneutral temperature

Thermoregulation constitutes an important share of the energy budget of endotherms. Elevated thermoregulatory requirements must be met by oxygen supply through the blood, as heat is produced mainly via aerobic processes. In contrast to mammal studies, it remains unclear whether elevated thermoregulatory needs are followed by changes in haematological variables in birds. We investigated haematocrit (HCT), haemoglobin content per volume of blood (HGB), number of red blood cells (RBC_count), and size of the erythrocytes (RBC_area) in zebra finches Taeniopygia guttata acclimated to either cold or thermoneutral ambient temperatures under laboratory conditions. Seventy‐nine females were maintained for six weeks either in cold (T = +12°C) or thermoneutral (T = +32°C) ambient temperature prior to blood collection. On average, HGB, HCT and RBC_count were significantly lower by about 10% in cold acclimated compared to thermoneutral acclimated birds. Only RBC_area was not different between the two acclimation temperatures. Mean HCT, one of the most commonly measured haematological variable for example was 53 ± 0.9% (LSM ± SEM) in thermoneutral and 49 ± 0.8 % (LSM ± SEM) in cold acclimated zebra finches. On first sight, the observed lower values for three out of the four determined haematological variables in response to acclimation to cold question oxygen supply to be indeed a limiting factor for heat production. However, higher demands of oxygen supply due to increased thermoregulation in birds may instead require specific optimisation of blood viscosity and modulation by other cardiovascular properties. Nucleated red blood cells in birds may pose different strain on blood viscosity compared to non‐nucleated mammalian erythrocytes and explain the contrasting response in haematological variables to temperature acclimation between birds and mammals.     

Food, Fat, and Feathers

The annual cycle of the White-throated Sparrow, Zonotrichiaalbicollis, is reviewed with brief references to facets of nutritionaland energetic importance (1) illustrating the life of a smallbird in a varying environment, and (2) showing that certainannual events in field populations can be compared with similarmanifestations in caged individuals. Data from captives areemployed in discussions of energetic variations related to (1)food, the source of nutritive input, (2) fat, the major formof caloric storage in birds, and (3) caloric expenditure. Metabolizableenergy is partitioned by phase of the annual cycle into existenceenergy, including the costs of thermoregulation, and productiveenergy, including expenditures for nocturnal activity (Zugunruhe)and molt. Costs of vernal migration in field birds are comparedwith costs of nocturnal activity in captives to show that energeticestimates in each situation are compatible. This conclusionis supported by a metabolic estimate made for field birds thatis within 6% of the estimated metabolism of captives under similarconditions. Data and statistics from seven additional speciesof buntings are used to examine several bioenergetic principlesfor homoiotherms. (1) Minimal metabolism measured by energybalance methods is proportional to the 0.7 power of body weightbut is higher than standard or resting metabolism measured bygaseous methods. (2) Metabolized energy is inversely relatedto ambient temperature below 25°C, the estimated ad libitumcritical temperature. (3) Heat production and loss are proportionatelyhigher in summer-acclimatized birds below the ad libitum criticaltemperature due to reduced insulation. Two summary plots, relatingtemperature, metabolizable energy, and body weight are given.Directions for future research in the study of avian nutritionare suggested.     

THERMOREGULATORY ADAPTATIONS IN MARINE MAMMALS: INTERACTING EFFECTS OF EXERCISE AND BODY MASS. A REVIEW1

A review of thermoregulation in marine mammals led to the following conclusions: very little is known about thermoregulation in large cetaceans. The only measured value for the metabolic rate of a whale, albeit a young one, was substantially higher than the predicted value for a terrestrial mammal of similar size. Very small and newborn marine mammals rely on a high metabolic heat production to sustain their body temperature during exposure to cold or in the water. The considerable insulation of some adult marine mammals may absolve them from the need for a high level of heat production. One marine mammal in tropical or subtropical waters is hypometabolic. There is evidence for a powerful control of thermoregulatory mechanisms by the anterior hypothalamic/preoptic region of the brain in two species. Thermoregulation in marine mammals during exercise remains paradoxical.     

Meeting the energy demands of reproduction in female koalas,<Emphasis Type="Italic"> Phascolarctos cinereus</Emphasis>: evidence for energetic compensation

Koalas are generally considered to be limited by their ability to acquire energy from their diet of Eucalyptus foliage and have the lowest mass-specific peak lactational energy output measured in any mammal to date. This study considered the energetics and sources of energy utilised for reproduction in free-ranging female koalas. Energy requirements and foliage intake were greater in both lactating and non-lactating females in winter than summer, presumably due to demands of thermoregulation. Koalas met the peak energy requirements of lactation primarily by a 36% increase in their intake of foliage. Metabolic energy expenditure (field metabolic rate, 1778 kJ.day^–1 for a 6.25-kg female at the time of peak lactation) was not elevated during lactation. This was due to compensation for part of their lactational demands by reduction of another, non-reproductive, component of their energy budget. The observed energetic compensation was probably due primarily to substitution of the waste heat from the metabolic costs of milk production and increased heat increment of feeding for thermoregulatory energy expenditure. There may also have been energetic compensation by reduction of some aspect of maintenance metabolism. Such energetic compensation, together with the strategy of spreading lactation over a long period, minimises the magnitude of lactational energy demands on koalas, and thus the increase in daily food intake required during lactation. As the nutritional requirements of females at peak lactation are the highest of any members of the population, low reproductive requirements effectively increase the types and amount of habitat able to support koala populations.Abbreviations FMR field metabolic rate - HIF heat increment of feeding - RMR resting metabolic rate - _O2 rate of oxygen consumptionCommunicated by I.D. Hume     

A phenology of the evolution of endothermy in birds and mammals

Recent palaeontological data and novel physiological hypotheses now allow a timescaled reconstruction of the evolution of endothermy in birds and mammals. A three‐phase iterative model describing how endothermy evolved from Permian ectothermic ancestors is presented. In Phase One I propose that the elevation of endothermy – increased metabolism and body temperature (T_b) – complemented large‐body‐size homeothermy during the Permian and Triassic in response to the fitness benefits of enhanced embryo development (parental care) and the activity demands of conquering dry land. I propose that Phase Two commenced in the Late Triassic and Jurassic and was marked by extreme body‐size miniaturization, the evolution of enhanced body insulation (fur and feathers), increased brain size, thermoregulatory control, and increased ecomorphological diversity. I suggest that Phase Three occurred during the Cretaceous and Cenozoic and involved endothermic pulses associated with the evolution of muscle‐powered flapping flight in birds, terrestrial cursoriality in mammals, and climate adaptation in response to Late Cenozoic cooling in both birds and mammals. Although the triphasic model argues for an iterative evolution of endothermy in pulses throughout the Mesozoic and Cenozoic, it is also argued that endothermy was potentially abandoned at any time that a bird or mammal did not rely upon its thermal benefits for parental care or breeding success. The abandonment would have taken the form of either hibernation or daily torpor as observed in extant endotherms. Thus torpor and hibernation are argued to be as ancient as the origins of endothermy itself, a plesiomorphic characteristic observed today in many small birds and mammals.     

Metabolism during flight in two species of bats, Phyllostomus hastatus and Pteropus gouldii.

The energetic cost of flight in a wind-tunnel was measured at various combinations of speed and flight angle from two species of bats whose body masses differ by almost an order of magnitude. The highest mean metabolic rate per unit body mass measured from P. hastatus (mean body mass, 0.093 kg) was 130.4 Wkg-1, and that for P. gouldii (mean body mass, 0.78 kg) was 69.6 Wkg-1. These highest metabolic rates, recorded from flying bats, are essentially the same as those predicted for flying birds of the same body masses, but are from 2.5 to 3.0 times greater than the highest metabolic rates of which similar-size exercising terrestrial mammals appear capable. The lowest mean rate of energy utilization per unit body mass P. hastatus required to sustain level flight was 94.2 Wkg-1 and that for P. gouldii was 53.4 Wkg-1. These data from flying bats together with comparable data for flying birds all fall along a straight line when plotted on double logarithmic coordinates as a function of body mass. Such data show that even the lowest metabolic requirements of bats and birds during level flight are about twice the highest metabolic capabilities of similar-size terrestrial mammals. Flying bats share with flying birds the ability to move substantially greater distance per unit energy consumed than walking or running mammals. Calculations show that P. hastatus requires only one-sixth the energy to cover a given distance as does the same-size terrestrial mammal, while P. gouldii requires one-fourth the energy of the same-size terrestrial mammal. An empirically derived equation is presented which enables one to make estimates of the metabolic rates of bats and birds during level flight in nature from body mass data alone. Metabolic data obtained in this study are compared with predictions calculated from an avian flight theory.     

Energy budget of the chicken foot

1. 1.|A mathematical model predicts the energy loss from a chicken foot provided the following variables are known: body temperature, air temperature, wind velocity, blood flow to the foot, and the relative partitioning of blood flow via two distinct venous returns.

2. 2.|Chickens are capable of keeping their feet from freezing at temperatures as low as −30°C ambient, but at a high energy cost.

3. 3.|Chickens can modulate blood flow to their feet at thermoneutral temperatures enough to vary heat loss to environment by about one-fourth metabolic heat production.