The field energetics and water fluxes of free-living wombats (Marsupialia: Vombatidae)

Wombats are large, fossorial, herbivorous marsupials exhibiting physical and behavioural characteristics indicative of extreme energy conservation. Previous energetics studies have been limited to their basal metabolism under laboratory conditions; little is known of the energetics of free-living wombats. We measured seasonal field metabolic rates (FMR) and water fluxes in the three species of free-living wombat using the doubly labelled water technique, to further investigate the extent of energy conservation in the Vombatidae. Measurements were taken during the wet and dry annual extremes of their characteristically harsh environments, which corresponded to seasonal extremes of food and water availability. Seasonal FMRs for all wombat species were lower than that recorded for other marsupials and well below that predicted for herbivorous mammals. Dry-season FMR of Lasiorhinus kreftii was 40% of that predicted for a mammal. Wombats maintained energy balance during the poor season by reducing FMR to about half that of the good season. Water flux rates during the dry season for the arid-adapted Lasiorhinus are amongst the lowest recorded for mammals, being only 25% of that predicted for a similarly sized herbivorous mammal. These low water flux rates enable wombats in semi-arid areas to maintain water balance without drinking. Estimated food and nitrogen intake rates were also low. We conclude that the energetically frugal lifestyle of the Vombatidae is amongst the most extreme for mammals.     

Physiological ecology of frillneck lizards in a seasonal tropical environment

The frillneck lizard, Chlamydosaurus kingii, is a conspicuous component of the fauna of the wetdry tropics of northern Australia during the wet season, but it is rarely seen in the dry season. Previous studies have demonstrated that during the dry season the field metabolic rate (FMR) is only about one-quarter of the wet-season rate, and one factor involved in this seasonal drop is a change in the behavioural thermoregulation of the species such that lower body temperatures (T _bs) are selected during dry-season days. Here we examine other factors that could be responsible for the seasonal change in FMR: standard metabolic rates (SMR) and activity. Samples from stomach flushing revealed that the lizards in the dry season continued to feed, but the volume of food was half as much as in the wet season. SMR in the laboratory was 30% less in the dry season. During the dry season, the energy expended by the lizards is 60.4 kJ kg^-1 day^-1 less than during the wet season. Combining laboratory and field data, we determined the relative contribution of the factors involved in this energy savings: 10% can be attributed to lower nighttime T _b, 12% is attributable to lower daytime T _b, 12% is attributable to decreased metabolism, and the remaining 66% is attributable to other activities (including e.g. locomotion, reproductive costs, digestion). Calculations indicate that if FMR did not drop in the dry season the lizards would not survive on the observed food intake during this season. Seasonal analysis of blood plasma and urine indicated an accumulation of some electrolytes during the dry season suggesting modest levels of water stress.     

Energetic cost of foraging in free-diving emperor penguins.

Hypothesizing that emperor penguins (Aptenodytes forsteri) would have higher daily energy expenditures when foraging for their food than when being hand-fed and that the increased expenditure could represent their foraging cost, we measured field metabolic rates (FMR; using doubly labeled water) over 4-d periods when 10 penguins either foraged under sea ice or were not allowed to dive but were fed fish by hand. Surprisingly, penguins did not have higher rates of energy expenditure when they dove and captured their own food than when they did not forage but were given food. Analysis of time-activity and energy budgets indicated that FMR was about 1.7 x BMR (basal metabolic rate) during the 12 h d(-1) that penguins were lying on sea ice. During the remaining 12 h d(-1), which we termed their "foraging period" of the day, the birds were alert and active (standing, preening, walking, and either free diving or being hand-fed), and their FMR was about 4.1 x BMR. This is the lowest cost of foraging estimated to date among the eight penguin species studied. The calculated aerobic diving limit (ADL(C)), determined with the foraging period metabolic rate of 4.1 x BMR and known O(2) stores, was only 2.6 min, which is far less than the 6-min ADL previously measured with postdive lactate analyses in emperors diving under similar conditions. This indicates that calculating ADL(C) from an at-sea or foraging-period metabolic rate in penguins is not appropriate. The relatively low foraging cost for emperor penguins contributes to their relatively low total daily FMR (2.9 x BMR). The allometric relationship for FMR in eight penguin species, including the smallest and largest living representatives, is kJ d(-1)=1,185 kg(0.705).     

Physiological ecology of the mangrove-dwelling varanid Varanus indicus

Some species of terrestrial lizards in wet-dry tropical climates reduce their body temperatures (T(b)'s) and activity and lower their metabolic rates during the dry season when food and water resources are scarce. However, semiaquatic lizards have access to water and presumably food throughout the year, so it is possible that they will not have the seasonal response seen in terrestrial species. We studied the thermal biology, energetics, and water flux of Varanus indicus, a semiaquatic, mangrove-dwelling varanid in tropical northern Australia. Although V. indicus remained active all year, they reduced their activity in the dry season, but not to the extent of terrestrial varanids. Varanus indicus field metabolic rates decreased by 38% in the dry season mostly as a result of the reduction in activity. Although food and water depletion are the driving forces behind decreases in dry season T(b) selection and energetics for many varanids, V. indicus appears not to be subject to these pressures to the same extent. Thermoregulatory indices indicate that V. indicus actively thermoregulate in the wet and dry seasons, but they do not fully exploit the available thermal resources. These lizards are unusual among varanid lizards in that their midday T(b)'s are relatively low (about 31 degrees C) despite the availability of thermal resources that would allow them to attain substantially higher T(b)'s.     

Living at the physiological limits: field and maximum metabolic rates of the common shrew (Sorex araneus)

Shrews (genus Sorex, small insectivorous mammals) are well known for their extremely high basal metabolic rates (BMRs) even when corrected for their small body size. We measured energy expenditure of the common shrew (Sorex araneus) under natural conditions (field metabolic rate [FMR]) by doubly labeled water method to test whether FMR is proportional to high BMR in this species. The study was performed in summer in northeastern Poland. In addition to the FMR, we also measured maximum metabolic rates induced by cold exposure and by intense activity (MMRCOLD and MMRRUN, respectively) to evaluate the aerobic reserve (MMR-FMR) in S. araneus. This aerobic reserve was used as an indicator of the potential for metabolic constraints. The FMR averaged 2.31+/-0.32 L CO2 d(-1) (+/-SD) or 58.1+/-8.0 kJ d(-1) in 8.2-g animals. This figure constituted 216%-258% of a value predicted for a "standard" mammal of the same body mass and was the highest mass-specific field metabolic rate in mammals. Because of the high BMR level in S. araneus, the FMR to BMR ratio (2.4) was not far off mammalian standards (median value of 3.1). The rate of water efflux determined in S. araneus (20.2 mL H2O d(-1) or 2.46 mL H2O g(-1) d(-1)) exceeded all figures reported to date in other mammals and was apparently linked to the high FMR level and relatively high water content of shrews' food. Maximal metabolic rates (MMRRUN of 18.1+/-1.6 mL O2 g(-1) h(-1) and MMRCOLD of 23.5+/-1.9 mL O2 g(-1) h(-1)) were not high in proportion to BMR or FMR that resulted in relatively narrow aerobic reserve in S. araneus: 20% when calculated against the MMRRUN and 39% when compared with the MMRCOLD. Our study reveals that S. araneus has high energy costs of living and operates close to its physiological limits.     

Body Size Overlap,Habitat Partitioning and Living Space Requirements of Terrestrial Vertebrate Predators: Implications for the Paleoecology of Large Theropod Dinosaurs

Ecological studies of extant tetrapod predators indicate that morphologically similar species which coexist in the same habitats routinely reduce interspecific competition for food by regular spacing of body size. The biggest predator species in the assemblage often differ more from one another in size than the smallest species. When coexisting carnivore species do not differ greatly in size, they commonly show morphological differences related to prey handling that may reduce dietary overlap. If carnivore species are very similar in both size and morphology, competition is avoided by habitat partitioning. Two tyrannosaurid species from the late Campanian Dinosaur Park Formation of western Canada are similar in both size and morphology, suggesting that they were segregated on the basis of habitat and/or biogeographic province. However; consideration of the living-space requirements of predator species of such large body size suggests that this kind of spatial separation would only have been possible had tyrannosaurids been more like ectotherms than endotherms in their metabolic rates. Distribution of different large theropod species across different, and surprisingly small (for the size of the animals) portions of Mesozoic landscapes may also account for the remarkably high diversity of morphologically similar large theropods in other dinosaur faunas.     

Energetics of bluetongue lizards (<Emphasis Type="Italic">Tiliqua scincoides</Emphasis>) in a seasonal tropical environment

We studied the physiological ecology of bluetongue lizards (Tiliqua scincoides) on the Adelaide River floodplain in tropical Australia to determine the seasonal patterns of energy expenditure and to determine the mechanisms by which seasonal differences were achieved. Field metabolic rates (FMR) were significantly lower in the dry season (37.6 kJ kg(-1) day(-1); n=9) than in the wet (127.3 kJ kg(-1) day(-1); n=7). Water flux was also lower in the dry season (6.8 ml kg(-1) day(-1); n=9) than in the wet (39.4 ml kg(-1) day(-1); n=7). Measurements of body temperatures (T(b)) and movements of free-ranging animals, and standard metabolic rate (SMR) of recently caught animals, allowed a detailed analysis of energy budgets for wet and dry seasons. In the dry, bluetongue lizards expended 90 kJ kg(-1) day(-1) less energy than in the wet season. Unlike some other lizards of the wet-dry tropics, SMR did not differ between seasons. About 5% of the seasonal difference in FMR was due to lower night time T(b) during the dry season, and about 7% was due to lower diurnal T(b). The remaining 88% of the decrease in energy expended in the dry season was due to a substantial decrease in other costs that may include reproduction, growth, digestion and activity. If we assume the animals fed daily and the costs of digestion are taken into account, the estimates are: 14% of the savings result from lower T(b) at night, 20% from lower T(b) in the day, and 66% result from decreased activity. It is therefore apparent that, unlike some agamid and varanid lizards that use a combination of behavioural and physiological mechanisms to conserve energy when food and water are limited, bluetongue lizards primarily use behavioural mechanisms to achieve a dramatic reduction in energy expenditure in the dry season.     

Wide home ranges for widely foraging lizards

Space usage by animals may be influenced by a range of factors. In this study we investigate whether foraging behaviour affects the home range size of lizards. Two distinct tactics of foraging have been recognized in predators: sit-and-wait foraging (SW) and active foraging (AF). Foraging activity level of a data set of lizard species, mainly compiled from literature, is compared with their home range sizes. Two opposite predictions can be made about foraging in connection with home range area: on the one hand, SW species may exhibit larger home ranges due to their mating system; on the other hand, AF species have higher metabolic energy and thus food requirements and can be expected to have larger home ranges that have to yield this food. This study shows that percentage of the time moving (as an index of foraging mode) correlates positively with home range, even after correcting for body mass, and these patterns remain when phylogenetic relationships are taken into account. We thus conclude that home range areas parallel activity levels in lizards.     

Xantusiid "night" lizards: a puzzling phylogenetic problem revisited using likelihood-based Bayesian methods on mtDNA sequences

Contentious issues in Night Lizard (Xantusiidae) evolution are revisited using Maximum Likelihood-based Bayesian methods and compared with results from Neighbor-Joining and Maximum Parsimony analyses. Fragments of three mitochondrial genes, the 12S and 16S ribosomal genes, and the cytochrome b gene, are sampled across an ingroup composed of seven xantusiid species and a 12-species outgroup chosen to bracket ancestral states for six additional clades of scleroglossan lizards. Our phylogenetic analyses afford robust support for the following conclusions: Xantusiidae is part of Scincomorpha, rather than being allied with Gekkota; Lepidophyma is sister to Xantusia, rather than to Cricosaura; Xantusia riversiana is imbedded within, rather than being sister to, other Xantusia species; and rock-morph Xantusia are not closely related to one another. Convergence related to retarded rates of growth and development, or to physical constraints imposed by living in rock crevices, may be responsible for much of the character discordance underlying conflicts in xantusiid phylogeny. Fossil-calibrated Maximum Likelihood-based divergence time estimates suggest that although the xantusiid stem may have originated in the Mesozoic, the crown clade is exclusively Tertiary in age. Thus, the clade including extant Cricosaura does not appear to have been extant during the K-T boundary bolide impact, as has been suggested. Moreover, our divergence-time estimates indicate that the xantusiid island endemics, Cricosaura typica on Cuba and Xantusia riversiana on the California Channel Islands, arrived via dispersal rather than vicariance, as previously proposed.     

Desiccation resistance and water balance in southern African keratin beetles (Coleoptera, Trogidae): the influence of body size and habitat

Desiccation resistance and water balance were examined in the adults of seven trogid species, which differed both in body size and in the habitats from which they were collected. Body water contents (51–58% fresh mass) and desiccation rates at 27 °C (0.00026–0.00093 g h⁻¹) in these species were very similar to those of unrelated, similar-sized beetles from arid habitats. The keratin beetles differed markedly from many other adult Coleoptera by virtue of their very high haemolymph osmolality and inability to regulate haemolymph osmolality, and to catabolise lipids for water production, during desiccation. Like most other insects, the xeric trogid species had lower rates of water loss and longer survival times than trogids from mesic areas. This was due both to lower rates of water loss and to the larger body size of species from the more arid areas. Because absolute body water content was higher in large beetles than in small ones, larger body size conferred higher desiccation resistance on the very large Kalahari desert species. This suggests that there may be strong selection for large body size in such insects from arid areas. Most ecological and ecophysiological investigations of geographical variation in body size, and the species-body size distribution, have focused on temperature and metabolic rate as explanatory variables. This study suggests that attention should also be given to desiccation resistance. Accepted: 29 September 1997     

Relative longevity and field metabolic rate in birds

Metabolism is a defining feature of all living organisms, with the metabolic process resulting in the production of free radicals that can cause permanent damage to DNA and other molecules. Surprisingly, birds, bats and other organisms with high metabolic rates have some of the slowest rates of senescence begging the question whether species with high metabolic rates also have evolved mechanisms to cope with damage induced by metabolism. To test whether species with the highest metabolic rates also lived the longest I determined the relationship between relative longevity (maximum lifespan), after adjusting for annual adult survival rate, body mass and sampling effort, and mass-specific field metabolic rate (FMR) in 35 species of birds. There was a strongly positive relationship between relative longevity and FMR, consistent with the hypothesis. This conclusion was robust to statistical control for effects of potentially confounding variables such as age at first reproduction, latitude and migration distance, and similarity in phenotype among species because of common phylogenetic descent. Therefore, species of birds with high metabolic rates senesce more slowly than species with low metabolic rates.     

Extreme water efficiency of Cape gannet Morus capensis chicks as an adaptation to water scarcity and heat stress in the breeding colony

Cape gannet Morus capensis chicks depend entirely on fish prey and metabolic water for water requirements during development. Water loss through evaporative cooling due to heat stress is substantial. We measured water flux and field metabolic rates (FMR) of Cape gannet chicks and adults to determine if gannets developed water saving strategies. The water economy index (WEI, g kJ^?1) decreased with chick age according to the model WEI = 0.676 – 0.272 × log₁₀(t), indicating that water efficiency increased with age. At fledging, the WEI of chicks was at the level expected of adult desert birds. Desert birds maintain a low WEI by also having a low FMR, whereas Cape gannet chicks have FMR comparable to other seabird species’ nestling requirements. We propose that maintaining low WEI is adaptive for Cape gannets because (1) chicks need to balance water loss through evaporative cooling, (2) fledglings need to overcome a period of up to a week when they cannot ingest any water and (3) adults spend extended periods in the breeding colony during which water can become a limiting factor. Understanding the physiological mechanism of maintaining low WEI will become increasingly important with future rising temperatures.     

Measuring the energy expenditure and water flux in free-ranging alpacas (Lama pacos) in the peruvian andes using the doubly labelled water technique

Energy expenditure and water flux were measured in free-ranging alpacas Lama pacos, a South American camelid, on natural pastures of the Peruvian Andes (altitude: 4,400 m above sea level). Water influx rate (WIR) was estimated in 16 males (age 2 years, weight 48.5+/-8.6 kg) labelled with 2H. In addition, the field metabolic rate (FMR) was measured in four of these animals labelled with both an oxygen (18O) and a hydrogen (2H) isotope. The WIR averaged 3.62 L H2O/day and the mean total body water 33.1 kg, equal to 68.2% of body weight (BW). The FMR of the four doubly labelled animals was 14.05 MJ/day. New allometric equations were calculated describing the relationships between WIR or FMR and BW, respectively, including published data on ruminants and the present alpaca results. The regression equation indicates that daily WIR scales to a similar metabolic size (kilograms of BW(0.94)) in alpacas than in wild or domesticated ruminants and camelids originating from arid and semiarid habitats. The resulting regression equation for FMR explained over 99% of the variation and corresponded to the function FMR (kilojoules per day)=1079 (kilograms of BW0.668) (n=5, r2=0.995, P<0.001). The FMR measured in this study, the first reported for a South American camelid species, suggests that free-ranging alpacas have similar energy expenditures on a metabolic weight basis as other wild ruminants living under harsh climatic conditions.     

The energy economy of the arctic-breeding Kittiwake (Rissa tridactyla): a review

The present paper reviews recent studies on changes in body mass, body composition and rates of energy expenditure during the breeding season in the black-legged Kittiwake (Rissa tridactyla) on Svalbard (79 degrees N). The main characteristic of the energy budget is a pronounced decrease in body mass as well as basal metabolic rate (BMR) after the eggs have hatched. While most internal organs lose mass in direct proportion to the general decrease in body mass, the liver and kidney masses decrease to a disproportionately greater extent. Since both the liver and the kidney have high intrinsic metabolic rates, these results support an earlier notion that the reduction in body mass is an adaptation to reduce maintenance costs. Alternatively, the reduced BMR is due to a decrease in energy uptake from the gastrointestinal tract, thereby ensuring that undigested food is ready to be regurgitated to the chicks. At the end of the chick-rearing period, the field metabolic rate (FMR) reaches its highest level, probably due to an increased workload associated with chick feeding. This occurs at a time of low body mass and BMR. A pronounced increase in the metabolic scope (FMR/BMR) during the latter part of the chick-rearing period demonstrates that BMR and FMR may change independently of each other and that the ratio FMR/BMR may not be a good measure of energy stress.     

Physiological ecology of a tropical dragon,Lophognathus temporalis

Lophognathus temporalis is an arboreal lizard from the wet–dry tropics of Australia. During the wet season the field metabolic rate (FMR) of the lizards was 209 kJ kg^?1 d^?1, but during the dry season FMR was only 62 kJ kg^?1 d^?1. Similarly, water flux decreased from 73.6 mL kg^?1 d^?1 in the wet season to 18.5 mL kg^?1 d^?1 in the dry season. Body temperatures (T_b) were significantly lower in the dry season, and operative temperatures, calculated by incorporating microclimatic data with characteristics of the lizards, indicated that the seasonal shift was due to changes in thermoregulatory behaviour rather than limitations of the thermal environment. By combining field measurements of T_b and FMR with laboratory measurements of standard metabolic rate over a range of T_b, we were able to subdivide the FMR into its components and to determine which factors contributed to the seasonal reduction in energy expenditure. During the dry season, lizards used 147 kJ kg^?1 d^?1 less energy than during the wet season, and 24% of this decrease was estimated to be due to the passive effects of lower nighttime T_b, 14% was due to the active selection of lower daytime T_b, 27% was due to the physiological shift to lower standard metabolic rates, and 35% was due to reduced activity in the dry season. Although the population size remained relatively constant (107 lizards ha^?1 during the wet season and 125 lizards ha^?1 during the dry season), the population structure changed, reflecting the seasonal patterns of recruitment and mortality. The number of lizards active at any one time was much lower in the dry season, reflecting the lower levels of activity in this season. The energy expenditure of the population of L. temporalis was 612 kJ ha^?1 d^?1 during the wet season and 113 kJ ha^?1 d^?1 during the dry season.     

Energy metabolism and evaporative water loss of Pristidactylus lizards

The effects of thermal conditions on the components of the physiological traits, energy metabolism and evaporative water loss, were studied in two species of Pristidactylus lizards, from different thermal habitats, forest and scrubland areas. The compared species had similar average daily metabolic rates, pulmo-cutaneous and pulmonary evaporative water loss. They differ in the daily distribution of energy expenditure, and in the voluntary aerobic scope. Similarities in most of the studied variables, may reflect either functional or historical constraints on these variables.     

Temperature responses of standard, aerobic metabolism by the California legless lizard, Anniella pulchra

Standard metabolic rates, measured for the lizard Anniella pulchra at 6 and 13 degrees C were statistically identical, showing notable thermal-independence at low temperature. Metabolic rates, measured at 25 and 30 degrees C, were significantly less than the rates predicted by standard equations. Thermal-independence and reduced aerobic metabolism at temperatures above the preferred range may result in water and energy savings in the fossorial habitat. Body-mass adjusted comparisons with other lizards suggest that reduced metabolism may be a correlative adaptation in small, fossorial lizards.     

Seasonal energetics of northern phocid seals

The metabolic rate of harp (Pagophilus groenlandicus), harbor (Phoca vitulina), and ringed seals (Pusa hispida) was measured at various temperatures in air and water to estimate basal metabolic rates (BMRs) in these species. The basal rate and body composition of three harp seals were also measured throughout the year to examine the extent to which they vary seasonally. Marine mammalian carnivores generally have BMRs that are over three times the rates expected from body mass in mammals generally, both as a response to a cold-water distribution and to carnivorous food habits with the basal rates of terrestrial carnivores averaging about 1.8 times the mean of mammals. Phocid seals, however, have basal rates of metabolism that are 30% lower than other marine carnivores. Captive seals undergo profound changes in body mass and food consumption throughout the year, and after accounting for changes in body mass, the lowest rate of food intake occurs in summer. Contrary to earlier observations, harp seals also have lower basal rates during summer than during winter, but the variation in BMR, relative to mass expectations, was not associated with changes in the size of fat deposits. The summer reduction in energy expenditure and food consumption correlated with a reduction in BMR. That is, changes in BMR account for a significant portion of the seasonal variation in energy expenditure in the harp seal. Changes in body mass of harp seals throughout the year were due not only to changes in the size of body fat deposits, but also to changes in lean body mass. These results suggest that bioenergetics models used to predict prey consumption by seals should include time-variant energy requirements.     

Egg size,postembryonic yolk,and survival ability

Summary Neonates of many species are dependent upon a post-embryonic yolk (PEY), a residual of the energy reserve of the developing embryo. Offspring hatching from large eggs have relatively more PEY than offspring from small eggs. Among daphniid Cladocera, large species produce larger eggs than smaller species. We have found that the proportional amount of energy reserve in eggs of five species of Cladocera is similar, but neonates of the larger Cladocera are born with a greater relative amount of postembryonic yolk, as triacylglycerol, than small species. Apparently, more of the reserve is metabolized by embryos of small species. This is correlated with the higher unitweight metabolic rates of smaller animals. It has been argued that animals should produce relatively larger eggs when exposed to low or unpredictable food conditions to increase the survivorship of their offspring. The physiological constraint of greater relative energy requirements of small embryos may limit PEY and explain why offspring of larger eggs survive better in low or unpredictable food resource environments.     

Field metabolic rates and water uptake in the blossom-bat Syconycteris australis (Megachiroptera)

Blossom-bats, Syconycteris australis (18 g) are known to be highly active throughout the night. Since this species frequently enters torpor, we postulated that their use of heterothermy may be related to a high energy expenditure in the field. To test this hypothesis we measured field metabolic rates (FMR) of S. australis at a subtropical site using the doubly labelled water (DLW) method. We also measured DLW turnover in captive animals held at constant ambient temperature (T _a) with ad libitum food to estimate whether T _a and food availability affect energy expenditure under natural conditions. The FMR of S. australis was 8.55 ml CO₂ g⁻¹h⁻¹ or 76.87 kJ day⁻¹ which is 7.04 times the basal metabolic rate (BMR) and one of the highest values reported for endotherms to date. Mass-specific energy expenditure by bats in the laboratory was about two-thirds of that of bats in the field, but some of this difference was explained by the greater body mass in captive bats. This suggests that foraging times in the field and laboratory were similar, and daily energy expenditure was not strongly affected by T _a or ad libitum food. Water uptake in the field was significantly higher than in the laboratory, most likely because nectar contained more water than the laboratory diet. Our study shows that S. australis has a FMR that is about double that predicted for its size although its BMR is lower than predicted. This supports the view that caution must be used in making assumptions from measurements of BMR in the laboratory about energy and other biological requirements in free-ranging animals. Accepted: 4 January 1999