Daily Energy Expenditure and the Cost of Activity in Mammals

Among 17 species of mammals, field metabolic rates exclusiveof thermoregulatory and productive costs (designated FMR*) averaged2.65 x standard metabolism (SMR). Daily activity costswere calculatedby subtraction from FMR* of the daily energy expenditure associatedwith SMR and assimilation of nutrients. Total expenditure foractivity was of a similar magnitude to that for daily standardmetabolism. Calculations indicate that expenditures by mammalsfor locomotion probably account for less than half of dailyactivity costs. Expenditures by mammals engaged in other kindsof activities are also reviewed. During their daily activityperiods, terrestrial mammals expend energy at a rate of about4.1 x SMR. The utility of energetic increments for activityin time-energy budgets, thermal energy budgets, and analysesof the economics of foraging are discussed.     

Validation of a Mechanistic Model for Non-Invasive Study of Ecological Energetics in an Endangered Wading Bird with Counter-Current Heat Exchange in its Legs

Mechanistic models provide a powerful, minimally invasive tool for gaining a deeper understanding of the ecology of animals across geographic space and time. In this paper, we modified and validated the accuracy of the mechanistic model Niche Mapper for simulating heat exchanges of animals with counter-current heat exchange mechanisms in their legs and animals that wade in water. We then used Niche Mapper to explore the effects of wading and counter-current heat exchange on the energy expenditures of Whooping Cranes, a long-legged wading bird. We validated model accuracy against the energy expenditure of two captive Whooping Cranes measured using the doubly-labeled water method and time energy budgets. Energy expenditure values modeled by Niche Mapper were similar to values measured by the doubly-labeled water method and values estimated from time-energy budgets. Future studies will be able to use Niche Mapper as a non-invasive tool to explore energy-based limits to the fundamental niche of Whooping Cranes and apply this knowledge to management decisions. Basic questions about the importance of counter-current exchange and wading to animal physiological tolerances can also now be explored with the model.     

The Energetic Costs of Fighting

SYNOPSIS. Current evolutionary theory predicts that energy expenditurewill be adjusted in contest situations to the value of the disputedresource and the relative probability of winningit. Estimatesof energy expended in contest situations support this prediction.I report on theenergetic costs of display relative to othercontest costs to individual fitness (e.g., risk ofpredation,losses in feeding time, injury and mortality) in territorialdisputes of the spider Agelenopsis aperta. Cost estimates obtainedin terms of decrements to milligrams wet-weight of future eggproduction resulting from single contests indicatethat actualenergy expenditure inthese territorial disputes represent insignificantcosts. Thesecosts are, in fact, 5–6 orders of magnitudesmaller than the costs associated with injury, potential predationand even loss infood as a result of time spent in the interactions.Review of the literature indicates that in most instances, energyexpenditure may be correlated with some other factor upon whichselection is acting (e.g., short contests wherepredation riskis high, variation in levels of escalation exhibited). Two exceptionsinclude the tremendous losses of workers to reproductives inant, termite, and bee colony territorial disputes and the productionof specializedagonistic organsexhibited by some corals, seaanemones and corallimopharians when encountering neighbors within"territorial"boundaries.     

Energetics of the annual cycle of Dippers Cinclus cinclus

Time-activity budgets and energy expenditure of Dippers Cinclus cinclus were studied in all months of the year and for every stage of the annual cycle. The commonest daytime activity was feeding (54%), then resting (43%) and flying (4%). On a 24-hr day basis the most marked changes in activity followed from changing daylengths. DEE (Daily Energy Expenditure), derived from time-activity budgets through the year and laboratory estimates of metabolism, averaged 201 kj d ^-1 in females and 228 kj d ^-1 in the larger males. Over a more restricted range of circumstances, direct estimates of DEE obtained from 77 Dippers using the doubly labelled water technique averaged 205 ± 43 kj d^-1 and 251 ± 55 kj d^-1 in females and males, respectively. Overall, the correspondence between these largely independent estimates of energy expenditure was reasonably close. DEE was highest during breeding (laying-females; rearing-males) and in late winter for both sexes. The lowest energy expenditures occurred during moult, amongst juveniles and in early winter. Incubating females and mate-guarding males also had low energy costs. Across all stages of the annual cycle body size, activity patterns, ambient temperature and river flow had significant effects on energy expenditure. The rate at which food was gathered to meet these changing energy demands varied widely. While some of this variation was imposed by a seasonal environment, it was also likely to reflect adaptive shifts in rates of food gathering, in some cases consequent upon the changing fitness benefits of various non-feeding activities.     

Time-activity budgets and energetics of Dipper Cinclus cinclus are dictated by temporal variability of river flow.

The white-throated Dipper (Cinclus cinclus) is unique among passerine birds by its reliance on diving to achieve energy gain in fast-flowing waters. Consequently, it should have evolved behavioural adaptations allowing responding directly to runoff patterns (one of the assumptions of the Natural Flow Regime Paradigm-NRFP). In this study (October 1998-August 2001), we investigated how behavioural and energy use strategies in Dippers might vary under the natural flow regime of snowmelt-dominated streams in The Pyrénées (France) where natural flow regime is highly seasonal and predictable. We recorded time spent in each of 5 behavioural activities of ringed birds to estimate time-activity budgets and derive time-energy budgets enabling the modelling of daily energy expenditure (DEE). Annual pattern in 'foraging' and 'resting' matched perfectly the annual pattern of the natural regime flow and there was a subtle relationship between water stage and time spent 'diving' the later increasing with rising discharge up to a point where it fell back. Thus, time-activity budgets meet the main prediction of the NRFP. For males and females Dippers, estimates of feeding rates (ratio E(obs)/E(req)=observed rate of energy gain/required foraging rate) and energy stress (M=DEE/Basal Metabolic Rate) also partly matched the NFRP. Maximum value for the ratio E(obs)/E(req) was registered in May whilst M peaked in spring. These ratios indicated that Pyrenean Dippers could face high energy stress during winter but paradoxically none during high snowmelt spates when food is expected to be difficult to obtain in the channel and when individual birds were observed spending ca 75% of the day 'resting'. Annual pattern in DEE did not match the NFRP; two phases were clearly identified, the first between January to June (with oscillating values 240-280 kJ d(-1) ind(-1)) and the second between July and December (200-220 kJ d(-1) ind(-1)). As total energy expenditure was higher during the most constraining season or life cycle, we suggest that energy management by Dippers in Pyrenean mountain streams may fit the 'peak total demand' hypothesis. At this step of the study, it is not possible to tell whether Dippers use an 'energy-minimisation' or an 'energy-maximisation' strategy.     

Optimal group size in territorial animals

Group territoriality is one possible origin of helping behavior in the vertebrates. The fitness of an individual in such a group is modeled as a function of territory quality, unit size, intruder pressure, risk of predation, cost of parental care and sensitivity of territories to resource depletion. All of these variables, as well as social status and sex, are viewed in the perspective of time-energy budgets. Each individual in a population of specified density and distribution of territory qualities is conceived as having a threshold of sociality. Optimal group size is expressed as a compromise between advantages gained by sharing costs and disadvantages arising from resource depletion. The use of time-energy budgets to study group territoriality provides new insights and approaches to the study of helping behavior. The role of resource depletion is singled out by the model for further field work.     

The time and energy expenditure of indigenous women horticulturalists in the Northwest Amazon

The energy cost of subsistence activities and the daily time and energy budgets of Tatuyo women were assessed as part of a village energy flow study. The Tatuyo are swidden horticulturalists relying on bitter manioc (Manihot esculenta) as a staple crop. Except for the actual felling of new gardens, women are responsible for most of the horticultural work and food preparation. Time budgets were assessed using 24-hour activity diaries. Rates of energy expenditure in typical activities were measured by indirect calorimetry using a Max-Planck respirometer. Daily energy expenditure was calculated using these rates in conjunction with the activity diaries. Rates of energy expenditure in standard activities were moderate and broadly comparable to published values for other populations living in tropical environments. The mean daily energy expenditure was 2,133 kcal (8.9 MJ). This value is similar to that reported for other subsistence horticulturalists and close to the FAO recommendation for energy intake for moderately active individuals.     

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.     

Individual differences in foraging site fidelity are not related to time-activity budgets in Herring Gulls

Many populations consist of individuals that differ consistently in their foraging behaviour through resource or foraging site selection. Foraging site fidelity has been reported in several seabird species as a common phenomenon. It is considered especially beneficial in spatially and/or temporally predictable environments in which fidelity is thought to increase energy intake, thereby affecting time-energy budgets. However, the consequences for activity and energy budget have not been adequately tested. In this paper, we studied the consequences of fine-scale foraging site fidelity in adult Herring Gulls Larus argentatus in a highly predictable foraging environment with distinct foraging patches. We measured their time-activity budgets using GPS tracking and tri-axial acceleration measurements, which also made it possible to estimate energy expenditure. Individual variation in foraging site fidelity was high, some individuals spending most of their time on a single foraging patch and others spending the same amount of time in up to 21 patches. While time and activity budgets differed between individuals, we found no clear relationship with foraging site fidelity. We did find a relationship between the size of the birds and the level of site fidelity; faithful birds tend to have a larger body size. Although differences in foraging time and habitat use between individuals could play a role in the results of the current study, short-term consequences of variation in foraging site fidelity within a population remain elusive, even when focusing on individuals with a similar foraging specialization (Blue Mussels Mytilus edulis). Studying individuals over multiple years and under varying environmental conditions may provide better insight into the consequences and plasticity of foraging site fidelity.     

Bats on a Budget: Torpor-Assisted Migration Saves Time and Energy

Bats and birds must balance time and energy budgets during migration. Migrating bats face similar physiological challenges to birds, but nocturnality creates special challenges for bats, such as a conflict between travelling and refueling, which many birds avoid by feeding in daylight and flying at night. As endothermic animals, bats and birds alike must expend substantial amounts of energy to maintain high body temperatures. For migratory birds refueling at stopovers, remaining euthermic during inactive periods reduces the net refuelling rate, thereby prolonging stopover duration and delaying subsequent movement. We hypothesized that bats could mitigate similar ambient-temperature dependent costs by using a torpor-assisted migration strategy. We studied silver-haired bats Lasionycteris noctivagans during autumn migration using a combination of respirometry and temperature-sensitive radiotelemetry to estimate energy costs incurred under ambient temperature conditions, and the energy that bats saved by using torpor during daytime roosting periods. All bats, regardless of sex, age, or body condition used torpor at stopover and saved up to 91% of the energy they would have expended to remain euthermic. Furthermore, bats modulated use of torpor depending on ambient temperature. By adjusting the time spent torpid, bats achieved a rate of energy expenditure independent of the ambient temperature encountered at stopover. By lowering body temperature during inactive periods, fuel stores are spared, reducing the need for refuelling. Optimal migration models consider trade-offs between time and energy. Heterothermy provides a physiological strategy that allows bats to conserve energy without paying a time penalty as they migrate. Although uncommon, some avian lineages are known to use heterothermy, and current theoretical models of migration may not be appropriate for these groups. We propose that thermoregulatory strategies should be an important consideration of future migration studies of both bats and birds.     

Seasonal sex–specific energy expenditure in breeding and non-breeding Palestine sunbirds Nectarinia osea

The timing of the chick‐rearing phase is known to have a profound effect on the reproductive success of birds. However, little is known about the energetic costs faced by the parents during different periods of the breeding season. These costs may have vital consequences for both their survival and future reproduction. In most studies, daily energy expenditure (DEE) of breeding and non‐breeding birds has been compared, without controlling for the effect of season. In the present study, we examined the energy demands of breeding compared to non‐breeding Palestine sunbirds Nectarinia osea and whether there were sex‐specific differences in DEE within and between different seasons. We predicted that DEE would be elevated when birds rear chicks, especially at cooler ambient temperatures. Time‐energy budgets were constructed for pairs of sunbirds, rearing chicks, or not breeding, in spring and summer. There were significant seasonal differences in estimates of DEE in non‐breeders that were 21% higher in spring than in summer. We attributed these to increases in non‐flight metabolic rate rather than changes in time spent on different activities. Our estimates of DEE for the birds that were rearing chicks were higher than non‐breeding adults. In females the increase in DEE when breeding, compared to when not breeding, was similar in both spring and summer, while males increased their DEE much less when breeding in spring. The differences in estimated DEE, however, were not significant between male and female birds in any season. Between seasons, female breeders had 17.1% higher DEE in spring than in summer, while male breeders showed no difference in DEE when rearing chicks in different seasons. Accordingly, our initial prediction was supported, as DEE in chick‐rearing adults was higher than in non‐breeding adults. In addition, although temperatures are lower in spring, breeding in the spring is only more costly than breeding in summer for females. Apparently, males are more flexible in reallocating their time and energy spent on different activities.     

Influence of growth rate retardation on time budgets and energetics of Arctic Tern Sterna paradisaea and Common Tern S. hirundo chicks

Time budgets of free-living chicks of Arctic Terns Sterna paradisaea and Common Terns S. hirundo throughout development are presented with special reference to changes in time allocation when growth rate varies. Chicks of both species were inactive most of the time observed (87%). Time allocated to the different behaviours changed during development and was generally better correlated with body mass than age. Slower growing nestlings were brooded more and allocated more time to quiescence and less time to locomotion, preening, begging and attacking (the latter two significant only for the Arctic Tern). The energetic implications of variation in time budgets with age and growth rate were considered. Parental brooding resulted in an average energy saving of nearly 40% of an individual nestling's thermoregulatory costs. Whereas thermoregulatory costs remained nearly unchanged in Arctic Tern chicks, these were negatively correlated with growth rate in Common Terns. Tentatively, we estimated a 30% reduction in a nestling's total energy requirement for a 50% reduction in average growth rate for both species.     

Daily energy expenditure and the cost of activity in a free-living mammal

Summary Antelope ground squirrels (Ammospermophilus leucurus, 80–100 g) began surface activity 1.0–1.5 h after sunrise and ended it 0.5–1.25 h before sunset throughout the year near Barstow, California. Daily energy expenditure (DEE) of free-living animals measured with doubly labeled water (H³H¹⁸O) decreased from 1,340 kJ kg^-1 d^-1 in April to 970 in October. Resting metabolic rates (RMR) of freshly-captured, fed, ground squirrels varied through the year (22.1 J g^-1 h^-1 in August, 19.1 in January) but most of the change in DEE could be explained by differences in thermoregulatory costs between seasons. The ground squirrels had lower rates of resting metabolism at night (15.3J g^-1 H^-1) than during the day.The cost of activity (calculated by subtracting 24 h resting costs from total DEE during August and October, periods when thermoregulatory costs were negligible) was 550 kJ kg^-1 d^-1 in August and October. Thus, activity accounted for about 50% of the total DEE. The mean rate of energy expenditure during the activity period, calculated as activity cost (kJ d^-1) divided by activity time (h d^-1), then plus RMR, was about 3xRMR. This multiplication factor may be useful as an estimator of foraging costs or in estimating DEE from time budgets.     

Estimating the energy expenditure of free‐ranging polar bears using tri‐axial accelerometers: A validation with doubly labeled water

Measures of energy expenditure can be used to inform animal conservation and management, but methods for measuring the energy expenditure of free‐ranging animals have a variety of limitations. Advancements in biologging technologies have enabled the use of dynamic body acceleration derived from accelerometers as a proxy for energy expenditure. Although dynamic body acceleration has been shown to strongly correlate with oxygen consumption in captive animals, it has been validated in only a few studies on free‐ranging animals. Here, we use relationships between oxygen consumption and overall dynamic body acceleration in resting and walking polar bears Ursus maritimus and published values for the costs of swimming in polar bears to estimate the total energy expenditure of 6 free‐ranging polar bears that were primarily using the sea ice of the Beaufort Sea. Energetic models based on accelerometry were compared to models of energy expenditure on the same individuals derived from doubly labeled water methods. Accelerometer‐based estimates of energy expenditure on average predicted total energy expenditure to be 30% less than estimates derived from doubly labeled water. Nevertheless, accelerometer‐based measures of energy expenditure strongly correlated (r² = 0.70) with measures derived from doubly labeled water. Our findings highlight the strengths and limitations in dynamic body acceleration as a measure of total energy expenditure while also further supporting its use as a proxy for instantaneous, detailed energy expenditure in free‐ranging animals.     

The cost of disturbance: a waste of time and energy?

Quantifying the effect of disturbance is a central issue in conservation. Using time and energy budgets, we obtain a range of ways to assess the importance of disturbance. One measure is the time that must be spent foraging in order to balance the energy budget. From this we derive critical levels of wastage (rate of disturbance multiplied by duration of disturbance) at which the animal runs out of time or reaches a limit on energy expenditure. In the case of the time constraint, the critical wastage is the net rate of energetic gain while foraging divided by the rate of energetic expenditure during a disturbance. The associated critical rate of disturbance is the net rate of energetic gain while foraging divided by the energy spent during a disturbance. The model is illustrated using data from the African wild dog, which suffers disturbance from lions and kleptoparasitism from hyenas. Findings suggest that disturbance imposes significant costs on wild dog time and energy budgets. We show how alternative environments can be evaluated in terms of their effective rate of gain, which is the net rate of gain from foraging minus the rate of energy expenditure as a result of disturbance.     

Elevated metabolic costs while resting on water in a surface feeder: the Black-legged Kittiwake Rissa tridactyla

Measurements of the energy costs of individual behaviours provide insights into how animals trade-off resource allocation and energy acquisition decisions. The energetic costs while resting on water are poorly known for seabirds but could comprise a substantial proportion of their daily energy expenditure. We measured the cost of resting on water in Black-legged Kittiwakes Rissa tridactyla , a species which does not fly during the night and for which estimating energy expenditure while resting on the water is therefore important. Their resting metabolic rate on water at 12.5 °C was at least 40% higher compared with resting at the same temperature in air. This indicates that, at comparable temperatures, metabolic costs are elevated for birds resting at sea compared with on land. We argue that Kittiwakes meet much of this extra thermoregulatory demand by dedicated metabolic activity. During the winter months, their costs are likely to be even higher owing to lower sea temperatures. Accordingly, we suggest that migration to milder latitudes, following breeding, will provide enhanced benefits, particularly to seabirds such as Kittiwakes which rest on the sea surface during darkness.     

The costs of carnivory

Mammalian carnivores fall into two broad dietary groups: smaller carnivores (<20 kg) that feed on very small prey (invertebrates and small vertebrates) and larger carnivores (>20 kg) that specialize in feeding on large vertebrates. We develop a model that predicts the mass-related energy budgets and limits of carnivore size within these groups. We show that the transition from small to large prey can be predicted by the maximization of net energy gain; larger carnivores achieve a higher net gain rate by concentrating on large prey. However, because it requires more energy to pursue and subdue large prey, this leads to a 2-fold step increase in energy expenditure, as well as increased intake. Across all species, energy expenditure and intake both follow a three-fourths scaling with body mass. However, when each dietary group is considered individually they both display a shallower scaling. This suggests that carnivores at the upper limits of each group are constrained by intake and adopt energy conserving strategies to counter this. Given predictions of expenditure and estimates of intake, we predict a maximum carnivore mass of approximately a ton, consistent with the largest extinct species. Our approach provides a framework for understanding carnivore energetics, size, and extinction dynamics.     

Seasonal variations in the energetics of an Australian nectarivorous bird, Lichmera indistincta

1. Seasonal variations in unit perching costs, flying costs and energy budgets for Lichmera indistincta were investigated. 2. Unit perching and flying costs were greatest in winter and least in summer. Variations in perching costs occurred principally because of changes in conductance. Flying cost variations may have been due to changes in wing disc loading and/or the integrity of wing feathers. 3. Rates of net energy intake were greatest in winter and least in summer. Variations in these rates were such that they offset changes in the rates of total energy expenditure to provide diurnal energy balance. 4. Regardless of the season, net daytime energy storage proceeded at a uniform rate and resulted in the storage of sufficient energy to offset overnight expenditure.     

Energetic costs of parasitism in the Cape ground squirrel Xerus inauris

Parasites have been suggested to influence many aspects of host behaviour. Some of these effects may be mediated via their impact on host energy budgets. This impact may include effects on both energy intake and absorption as well as components of expenditure, including resting metabolic rate (RMR) and activity (e.g. grooming). Despite their potential importance, the energy costs of parasitism have seldom been directly quantified in a field setting. Here we pharmacologically treated female Cape ground squirrels (Xerus inauris) with anti-parasite drugs and measured the change in body composition, the daily energy expenditure (DEE) using doubly labelled water, the RMR by respirometry and the proportions of time spent looking for food, feeding, moving and grooming. Post-treatment animals gained an average 19g of fat or approximately 25kJd-1. DEE averaged 382kJd-1 prior to and 375kJd-1 post treatment (p>0.05). RMR averaged 174kJd-1 prior to and 217kJd-1 post treatment (p<0.009). Post-treatment animals spent less time looking for food and grooming, but more time on feeding. A primary impact of infection by parasites could be suppression of feeding behaviour and, hence, total available energy resources. The significant elevation of RMR after treatment was unexpected. One explanation might be that parasites produce metabolic by-products that suppress RMR. Overall, these findings suggest that impacts of parasites on host energy budgets are complex and are not easily explained by simple effects such as stimulation of a costly immune response. There is currently no broadly generalizable framework available for predicting the energetic consequences of parasitic infection.     

The effect of thermoregulatory substitution on optimal energy reserves of small birds in winter

Previous models have predicted the body mass of small birds in winter on the basis of a trade-off between starvation and predation. Many of these models have assumed that energy expenditure while active increases with body mass. The implications of the fact that the metabolic cost of activity can substitute for internal heat production and help keep the bird warm have not been investigated. In this paper we show that if thermoregulatory substitution occurs then there is a critical level of energy reserves above which an active bird is thermoneutral. This critical level increases as temperature decreases. Below this level, substitution of energy results in higher optimal levels of reserves than would be predicted in the absence of substitution. Our model thus predicts that at low temperatures body mass will be higher when thermoregulatory substitution occurs.