Daily Torpor in Birds and Mammals: Past, Present, and Future of the Field.

Torpor is an incredibly efficient energy-saving strategy that many endothermic birds and mammals use to save energy, by lowering their metabolic rates, heart rates, and typically body temperatures. Over the last few decades, the study of daily torpor-in which torpor is used for less than 24 hours per bout-has advanced rapidly. The papers in this issue cover the ecological and evolutionary drivers of torpor, as well as some of the mechanisms governing torpor use. We identified broad focus areas that need special attention: clearly defining the various parameters that indicate torpor use and identifying the genetic and neurological mechanisms regulating torpor. Recent studies on daily torpor and heterothermy, including the ones in this issue, have furthered the field immensely. We look forward to a period of immense growth in this field.

Rare and Opportunistic Use of Torpor in Mammals-An Echo from the Past?

Torpor was traditionally seen as a winter survival mechanism employed by animals living in cold and highly seasonal habitats. Although we now know that torpor is also used by tropical and subtropical species, and in response to a variety of triggers, torpor is still largely viewed as a highly controlled, seasonal mechanism shown by Northern hemisphere species. To scrutinize this view, we report data from a macroanalysis in which we characterized the type and seasonality of torpor use from mammal species currently known to use torpor. Our findings suggest that predictable, seasonal torpor patterns reported for Northern temperate and polar species are highly derived forms of torpor expression, whereas the more opportunistic and variable forms of torpor that we see in tropical and subtropical species are likely closer to the patterns expressed by ancestral mammals. Our data emphasize that the torpor patterns observed in the tropics and subtropics should be considered the norm and not the exception.

Long-term survival, temperature, and torpor patterns.

Mammalian and avian torpor is highly effective in reducing energy expenditure. However, the extent of energy savings achieved and thus long-term survival appear to differ between species capable of multiday hibernation and species restricted to daily heterothermy, which could, however, be due to thermal effects. We tested how long-term survival on stored body fat (i.e. time to lean body mass), crucial for overcoming adverse periods, is related to the pattern of torpor expressed under different ambient temperatures (Ta: 7 °C typical of hibernation, 15 and 22 °C typical of daily torpor) in the small marsupial hibernator the pygmy-possum (Cercartetus nanus). Possums expressed torpor at all Tas and survived without food for 310 days on average at Ta 7 °C, 195 days at Ta 15 °C, and 127 days at Ta 22 °C. At Ta 7 and 15 °C, torpor bout duration (TBD) increased from < 1-3 to ~ 5-16 days over 2 months, whereas at Ta 22 °C, TBD remained at < 1 to ~ 2 days. At all Tas daily energy use was substantially lower and TBD and survival times of possums much longer (3-12 months) than in daily heterotherms (~ 10 days). Such pronounced differences in torpor patterns and survival times even under similar thermal conditions provide strong support for the concept that torpor in hibernators and daily heterotherms are physiologically distinct and have evolved for different ecological purposes.

Flexible Employment of Torpor in Squirrel Gliders (Petaurus norfolcensis): An Adaptation to Unpredictable Climate?

AbstractTorpor is a highly effective response to counter various ecological and physiological bottlenecks in endotherms. In this study, we examined interrelations between thermoregulatory responses and key environmental variables in free-living squirrel gliders (Petaurus norfolcensis) in a habitat with drastic climatic and ecological changes across seasons. To this end, we measured body temperature (Tb) and heart rate (fH) simultaneously throughout the year using implanted data loggers. Squirrel gliders in our study experienced fluctuations in ambient temperature (Ta) between -4.0°C and 44.1°C and expressed torpor at different times during the year. In contrast to our expectations, torpor seemed to be employed flexibly, on demand, and most frequently in spring rather than during the coldest and/or hottest periods. Torpor bouts lasted, on average, about 5 h, and Tb during torpor dropped as low as 17.9°C. The fH during torpor decreased below 50 bpm, which is about one-third of the basal level. The ability to record fH alongside Tb enabled us to also report periods of low fH during thermoconforming hyperthermia at Ta's above 35°C that likely occurred to conserve energy and water. Our findings double the body size of Australian gliders for which data on torpor are available and advance our ecological understanding of the dynamics of torpor expression in wild mammals and of how animals cope with varying conditions. Moreover, they highlight that the flexibility of physiology and thermoregulatory responses are clearly more complex than previously thought.

The Rate of Cooling during Torpor Entry Drives Torpor Patterns in a Small Marsupial.

AbstractTo maximize energy savings, entry into torpor should involve a fast reduction of metabolic rate and body temperature (Tb); that is, animals should thermoconform. However, animals often defend against the decrease in Tb via a temporary increase in thermoregulatory heat production, slowing the cooling process. We investigated how thermoregulating or thermoconforming during torpor entry affects temporal and thermoenergetic aspects in relation to body mass and age in juvenile and adult fat-tailed dunnarts (Sminthopsis crassicaudata; Marsupialia: Dasyuridae). During torpor entry, juvenile thermoconformers cooled twice as fast as and used less energy during cooling than juvenile thermoregulators. While both juvenile and adult thermoconformers had a lower minimum Tb, a lower torpor metabolic rate, and longer torpor bouts than thermoregulators, these differences were more pronounced in the juveniles. Rewarming from torpor took approximately twice as long for juvenile thermoconformers, and the costs of rewarming were greater. To determine the difference in average daily metabolic rate between thermoconformers and thermoregulators independent of body mass, we compared juveniles of a similar size (∼13 g) and similarly sized adults (∼17 g). The average daily metabolic rate was 7% (juveniles) and 17% (adults) less in thermoconformers than in thermoregulators, even though thermoconformers were active for longer. Our data suggest that thermoconforming during torpor entry provides an energetic advantage for both juvenile and adult dunnarts and may aid growth for juveniles. While thermoregulation during torpor entry is more costly, it still saves energy, and the higher Tb permits greater alertness and mobility and reduces the energetic cost of endogenous rewarming.

Pronounced differences in heart rate and metabolism distinguish daily torpor and short-term hibernation in two bat species.

Torpor, and its differential expression, is essential to the survival of many mammals and birds. Physiological characteristics of torpor appear to vary between those species that express strict daily heterothermy and those capable of multiday hibernation, but comparisons are complicated by the temperature-dependence of variables. Previous reviews have compared these different torpor strategies by measuring the depth and duration of torpor in multiple species. However, direct comparison of multiple physiological parameters under similar thermal conditions are lacking. Here, we quantified three physiological variables; body temperature, metabolic rate (MR) and heart rate (HR) of two small heterothermic bats (daily heterotherm Syconycteris australis, and hibernator Nyctophilus gouldi) under comparable thermal conditions and torpor bout durations. When normothermic and resting both MR and HR were similar for the two species. However, during torpor the minimum HR was more than fivefold higher, and minimum MR was 6.5-fold higher for the daily heterotherm than for the hibernator at the same subcutaneous Tb (16 ± 0.5 °C). The data show that the degree of heterothermy defined using Tb is not necessarily a precise proxy for physiological capacity during torpor in these bats and is unlikely to reveal accurate energy budgets. Our study provides evidence supporting a distinction between daily torpor in a daily heterotherm and short term torpor in a hibernator, at least within the Chiroptera with regard to these physiological variables. This exists even when individuals display the same degree of Tb reduction, which has clear implications for the modelling of their energy expenditure.

Thermal biology and roost selection of free-ranging male little forest bats, Vespadelus vulturnus, during winter.

Insectivorous bats are particularly susceptible to heat loss due to their relatively large surface area to volume ratio. Therefore, to maintain a high normothermic body temperature, bats require large amounts of energy for thermoregulation. This can be energetically challenging for small bats during cold periods as heat loss is augmented and insect prey is reduced. To conserve energy many bats enter a state of torpor characterized by a controlled reduction of metabolism and body temperature in combination with selecting roosts based upon thermal properties. Our study aimed to quantify torpor patterns and roost preferences of free-ranging little forest bats (Vespadelus vulturnus) during winter to identify physiological and behavioral mechanisms used by this species for survival of the cold season. All bats captured were male (body mass 4.9 ± 0.7 g, n = 6) and used torpor on every day monitored, with bouts lasting up to 187.58 h (mean = 35.5 ± 36.7 h, n = 6, total number of samples [N] = 61). Torpor bout duration was significantly correlated with daily minimum and maximum ambient temperature, mean skin temperature, insect mass, and body mass of individuals and the multiday torpor bouts recorded in the cold qualify as hibernation. The lowest skin temperature recorded was 5.2°C, which corresponded to the lowest ambient temperature measurement of -5.8°C. Most bats chose tall, large, live Eucalyptus trees for roosting and to leave their roost for foraging on warmer days. Many individuals often switched roosts (every 3-5 days) and movements increased as spring approached (every 1-2 days). Our data suggest that V. vulturnus are capable of using the environmental temperature to gauge potential foraging opportunities and as a cue to reenter torpor when conditions are unsuitable. Importantly, frequent use of torpor and appropriate roost selection form key roles in the winter survival of these tiny bats.

Hypothesis and Theory: A Two-Process Model of Torpor-Arousal Regulation in Hibernators.

Hibernating mammals drastically lower their metabolic rate (MR) and body temperature (Tb) for up to several weeks, but regularly rewarm and stay euthermic for brief periods. It has been hypothesized that the necessity for rewarming is due to the accumulation or depletion of metabolites, or the accrual of cellular damage that can be eliminated only in the euthermic state. Recent evidence for significant inverse relationships between the duration of torpor bouts (TBD) and MR in torpor strongly supports this hypothesis. We developed a new mathematical model that simulates hibernation patterns. The model involves an hourglass process H (Hibernation) representing the depletion/accumulation of a crucial enzyme/metabolite, and a threshold process Hthr. Arousal, modelled as a logistic process, is initiated once the exponentially declining process H reaches Hthr. We show that this model can predict several phenomena observed in hibernating mammals, namely the linear relationship between TMR and TBD, effects of ambient temperature on TBD, the modulation of torpor depth and duration within the hibernation season, (if process Hthr undergoes seasonal changes). The model does not need but allows for circadian cycles in the threshold T, which lead to arousals occurring predominantly at certain circadian phases, another phenomenon that has been observed in certain hibernators. It does not however, require circadian rhythms in Tb or MR during torpor. We argue that a two-process regulation of torpor-arousal cycles has several adaptive advantages, such as an easy adjustment of TBD to environmental conditions as well as to energy reserves and, for species that continue to forage, entrainment to the light-dark cycle.

Small Alpine Marsupials Regulate Evaporative Water Loss, Suggesting a Thermoregulatory Role Rather than a Water Conservation Role.

AbstractWe show here that evaporative water loss (EWL) is constant over a wide range of ambient relative humidity for two species of small, mesic habitat dasyurid marsupials (Antechinus agilis and Antechinus swainsonii) below thermoneutrality (20°C) and within thermoneutrality (30°C). This independence of EWL from the water vapor pressure deficit between the animal and its environment indicates that EWL is physiologically controlled by both species. The magnitude of this control of EWL was similar to that of two other small marsupials from more arid habitats, which combined with the observation that there were no effects of relative humidity on body temperature or metabolic rate, suggests that control of EWL is a consequence of precise thermoregulation to maintain heat balance rather than a water-conserving strategy at low relative humidities. The antechinus appear to manipulate cutaneous EWL rather than respiratory EWL to control their total EWL by modifying their cutaneous resistance and/or skin temperature. We propose that there is a continuum between enhanced thermoregulatory EWL at high ambient temperature and so-called insensible EWL at and below thermoneutrality.

Do small precocial birds enter torpor to conserve energy during development?

Precocial birds hatch feathered and mobile, but when they become fully endothermic soon after hatching, their heat loss is high and they may become energy depleted. These chicks could benefit from using energy-conserving torpor, which is characterised by controlled reductions of metabolism and body temperature (Tb). We investigated at what age the precocial king quail Coturnix chinensis can defend a high Tb under a mild thermal challenge and whether they can express torpor soon after achieving endothermy to overcome energetic and thermal challenges. Measurements of surface temperature (Ts) using an infrared thermometer showed that king quail chicks are partially endothermic at 2-10 days, but can defend high Tb at a body mass of ∼13 g. Two chicks expressed shallow nocturnal torpor at 14 and 17 days for 4-5 h with a reduction of metabolism by >40% and another approached the torpor threshold. Although chicks were able to rewarm endogenously from the first torpor bout, metabolism and Ts decreased again by the end of the night, but they rewarmed passively when removed from the chamber. The total metabolic rate increased with body mass. All chicks measured showed a greater reduction of nocturnal metabolism than previously reported in quails. Our data show that shallow torpor can be expressed during the early postnatal phase of quails, when thermoregulatory efficiency is still developing, but heat loss is high. We suggest that torpor may be a common strategy for overcoming challenging conditions during development in small precocial and not only altricial birds.

Does control of insensible evaporative water loss by two species of mesic parrot have a thermoregulatory role?

Insensible evaporative water loss (EWL) at or below thermoneutrality is generally assumed to be a passive physical process. However, some arid zone mammals and a single arid zone bird can control their insensible water loss, so we tested the hypothesis that the same is the case for two parrot species from a mesic habitat. We investigated red-rumped parrots (Psephotus haematonotus) and eastern rosellas (Platycercus eximius), measuring their EWL, and other physiological variables, at a range of relative humidities at ambient temperatures of 20 and 30°C (below and at thermoneutrality). We found that, despite a decrease in EWL with increasing relative humidity, rates of EWL were not fully accounted for by the water vapour deficit between the animal and its environment, indicating that the insensible EWL of both parrots was controlled. It is unlikely that this deviation from physical expectations was regulation with a primary role for water conservation because our mesic-habitat parrots had equivalent regulatory ability as the arid habitat budgerigar (Melopsittacus undulatus). This, together with our observations of body temperature and metabolic rate, instead support the hypothesis that acute physiological control of insensible water loss serves a thermoregulatory purpose for endotherms. Modification of both cutaneous and respiratory avenues of evaporation may be involved, possibly via modification of expired air temperature and humidity, and surface resistance.

Seasonal Expression of Avian and Mammalian Daily Torpor and Hibernation: Not a Simple Summer-Winter Affair†.

Daily torpor and hibernation (multiday torpor) are the most efficient means for energy conservation in endothermic birds and mammals and are used by many small species to deal with a number of challenges. These include seasonal adverse environmental conditions and low food/water availability, periods of high energetic demands, but also reduced foraging options because of high predation pressure. Because such challenges differ among regions, habitats and food consumed by animals, the seasonal expression of torpor also varies, but the seasonality of torpor is often not as clear-cut as is commonly assumed and differs between hibernators and daily heterotherms expressing daily torpor exclusively. Hibernation is found in mammals from all three subclasses from the arctic to the tropics, but is known for only one bird. Several hibernators can hibernate for an entire year or express torpor throughout the year (8% of species) and more hibernate from late summer to spring (14%). The most typical hibernation season is the cold season from fall to spring (48%), whereas hibernation is rarely restricted to winter (6%). In hibernators, torpor expression changes significantly with season, with strong seasonality mainly found in the sciurid and cricetid rodents, but seasonality is less pronounced in the marsupials, bats and dormice. Daily torpor is diverse in both mammals and birds, typically is not as seasonal as hibernation and torpor expression does not change significantly with season. Torpor in spring/summer has several selective advantages including: energy and water conservation, facilitation of reproduction or growth during development with limited resources, or minimisation of foraging and thus exposure to predators. When torpor is expressed in spring/summer it is usually not as deep and long as in winter, because of higher ambient temperatures, but also due to seasonal functional plasticity. Unlike many other species, subtropical nectarivorous blossom-bats and desert spiny mice use more frequent and pronounced torpor in summer than in winter, which is related to seasonal availability of nectar or water. Thus, seasonal use of torpor is complex and differs among species and habitats.

Responding to the weather: energy budgeting by a small mammal in the wild.

Energy conservation is paramount for small mammals because of their small size, large surface area to volume ratio, and the resultant high heat loss to the environment. To survive on limited food resources and to fuel their expensive metabolism during activity, many small mammals employ daily torpor to reduce energy expenditure during the rest phase. We hypothesized that a small terrestrial semelparous marsupial, the brown antechinus Antechinus stuartii, would maximize activity when foraging conditions were favorable to gain fat reserves before their intense breeding period, but would increase torpor use when conditions were poor to conserve these fat reserves. Female antechinus were trapped and implanted with small temperature-sensitive radio transmitters to record body temperature and to quantify torpor expression and activity patterns in the wild. Most antechinus used torpor at least once per day over the entire study period. Total daily torpor use increased and mean daily body temperature decreased significantly with a reduction in minimum ambient temperature. Interestingly, antechinus employed less torpor on days with more rain and decreasing barometric pressure. In contrast to torpor expression, activity was directly related to ambient temperature and inversely related to barometric pressure. Our results reveal that antechinus use a flexible combination of physiology and behavior that can be adjusted to manage their energy budget according to weather variables.

Growing Up in a Changing Climate: How Temperature Affects the Development of Morphological, Behavioral and Physiological Traits of a Marsupial Mammal.

Climate change is likely to affect many mammalian phenotypes, yet little is known whether and how phenotypic plasticity is involved in responding to thermal challenges during mammalian development. We investigated the effect of continuous cold or warm exposure during development on morphological, behavioral, and functional variables of yellow-footed antechinus (Antechinus flavipes), a semelparous Australian marsupial mammal. Captive-bred young were exposed to two ambient temperatures (T a ), cold (17°C) or warm (25°C), once weaned. Treatments were reversed and metabolic rate (MR) measurements repeated after 2 months. We measured body mass weekly, activity continuously, and MRs over a range of T a once they were adults. Growth rate was similar in both groups, but was faster in males. Antechinus in the warm group were initially more active than the cold group and decreased activity when exposed to cold, whereas the cold group increased activity when exposed to warm. Interestingly, females changed their night-time activity when T a was changed, whereas males changed their daytime activity. MRs were originally lower in the warm group in comparison to the cold group for both sexes and increased slightly for females, but not for males, after being exposed to cold. After exposure to warm T a , the MRs of the cold group decreased significantly over the entire T a -range for both sexes. Our results reveal that temperatures experienced during development can influence behavioral and physiological traits in antechinus. Such phenotypic plasticity is vital for a species that within 1 year is dependent on a single breeding event and experiences a complete population turnover.

White mouse pups can use torpor for energy conservation.

White mice are ubiquitous laboratory animals and have been extensively studied. To reveal potential undiscovered traits, we tested the hypothesis that during development, when heat loss in mouse pups is high, they can use daily torpor for energy conservation. We determined at what age individual mouse pups are able to defend their body temperature at room temperature (ambient temperature, Ta = 20 °C) and whether they could use torpor from that time. Initially at 5/6 days (body mass, BM ~ 3 g), still naked mice cooled rapidly. In contrast, at ~ 14 days (BM ~ 6 g), they could maintain a high, constant body temperature and, therefore, had reached competent endothermy. These mouse pups at ~ 20% of adult BM were able to enter into and arouse from torpor as determined via the rate of oxygen consumption; this was the case for both individuals that were exposed to a cooling regime as well as those that were not. During torpor, metabolism fell by up to > 90% and torpor lasted for up to 12 h. As mice grew, torpor was still used but was less pronounced. Our study shows that although the physiology of laboratory mice has been widely examined, their functional capabilities have still not been fully revealed, which has implications for biomedicine. Our and other developmental data suggest that because torpor is so efficient in conserving energy, it is likely to be used during the growth phase by diverse mammals and birds to survive energetic and thermal challenges.

Thermal physiology and activity in relation to reproductive status and sex in a free-ranging semelparous marsupial.

In a changing climate, southern hemisphere mammals are predicted to face rising temperatures and aridity, resulting in food and water shortages, which may further challenge already constrained energetic demands. Especially semelparous mammals may be threatened because survival of the entire population depends on the success of a single breeding event. One of these species, the yellow-footed antechinus, Antechinus flavipes, a small, heterothermic marsupial mammal, commences reproduction during winter, when insect prey is limited and energetic constraints are high. We examined the inter-relations between thermal and foraging biology of free-ranging A. flavipes and examined whether they use torpor for energy conservation, despite the fact that reproduction and torpor are considered to be incompatible for many mammals. Females used torpor during the reproductive season, but patterns changed with reproductive status. Prior to breeding, females used frequent (86% of days), deep and long torpor that was more pronounced than any other reproductive group, including pre-mating males (64% of days). Pregnant females continued to use torpor, albeit torpor was less frequent (28% of days) and significantly shorter and shallower than before breeding. Parturient and lactating females did not express torpor. During the mating period, males reduced torpor use (24% of days). Pre-reproductive females and pre-mating males were the least active and may use torpor to minimize predator exposure and enhance fat deposition in anticipation of the energetic demands associated with impending mating, gestation and lactation. Reproductive females were most active and likely foraged and fed to promote growth and development of young. Our data show that A. flavipes are balancing energetic demands during the reproductive season by modifying torpor and activity patterns. As the timing of reproduction is fixed for this genus, it is probable that climate change will render these behavioural and physiological adaptations as inadequate and threaten this and other semelparous species.

The Burramys Project: a conservationist's reach should exceed history's grasp, or what is the fossil record for?

The fossil record provides important information about changes in species diversity, distribution, habitat and abundance through time. As we understand more about these changes, it becomes possible to envisage a wider range of options for translocations in a world where sustainability of habitats is under increasing threat. The Critically Endangered alpine/subalpine mountain pygmy-possum, Burramys parvus (Marsupialia, Burramyidae), is threatened by global heating. Using conventional strategies, there would be no viable pathway for stopping this iconic marsupial from becoming extinct. The fossil record, however, has inspired an innovative strategy for saving this species. This lineage has been represented over 25 Myr by a series of species always inhabiting lowland, wet forest palaeocommunities. These fossil deposits have been found in what is now the Tirari Desert, South Australia (24 Ma), savannah woodlands of the Riversleigh World Heritage Area, Queensland (approx. 24-15 Ma) and savannah grasslands of Hamilton, Victoria (approx. 4 Ma). This palaeoecological record has led to the proposal overviewed here to construct a lowland breeding facility with the goal of monitoring the outcome of introducing this possum back into the pre-Quaternary core habitat for the lineage. If this project succeeds, similar approaches could be considered for other climate-change-threatened Australian species such as the southern corroboree frog (Pseudophryne corroboree) and the western swamp tortoise (Pseudemydura umbrina). This article is part of a discussion meeting issue 'The past is a foreign country: how much can the fossil record actually inform conservation?'

Does aridity affect spatial ecology? Scaling of home range size in small carnivorous marsupials.

The aim of our study was to determine how body mass affects home range size in carnivorous marsupials (dasyurids) and whether those species living in desert environments require relatively larger areas than their mesic counterparts. The movement patterns of two sympatric species of desert dasyurids (body mass 16 and 105 g) were investigated via radio-telemetry in southwestern Queensland and compared with published records for other Australian dasyurids. Both species monitored occupied stable home ranges. For all dasyurids, home range size scaled with body mass with a coefficient of > 1.2, almost twice that for metabolic rate. Generally, males occupied larger home ranges than females, even after accounting for the size dimorphism common in dasyurids. Of the three environmental variables tested, primary productivity and habitat, a categorical variable based on the 500 mm rainfall isopleth, further improved model performance demonstrating that arid species generally occupy larger home ranges. Similar patterns were still present in the dataset after correcting for phylogeny. Consequently, the trend towards relatively larger home ranges with decreasing habitat productivity can be attributed to environmental factors and was not a result of taxonomic affiliation. We therefore conclude that alternative avenues to reduce energy requirements on an individual and population level (i.e. torpor, basking and population density) do not fully compensate for the low resource availability of deserts demanding an increase in home range size.

Frequent nocturnal torpor in a free-ranging Australian honeyeater, the noisy miner.

Torpor in birds is considered to be far less common than in mammals. This is particularly true for passerine birds for which knowledge of torpor expression is scarce, although almost all are small, have high energy expenditure and could profit energetically from using torpor. To assess whether the extent and diversity of avian and especially passerine torpor expression and heterothermy may be currently underestimated because of limited long-term data on free-ranging birds, core body temperature fluctuations were quantified over ~ 4.3 months in a medium-sized honeyeater, the noisy miner (Manorina melanocephala, ~ 75 g), in an open woodland during the cold season in eastern Australia. Miners used shallow nocturnal torpor frequently (63% of days), torpor bouts lasted on average for 6.5 h (maximum 13.5 h) and, unlike during hypothermia, torpor was terminated by endogenous heat production for rewarming. Body temperatures (Tb) ranged from a maximum of 43.5 °C to a minimum of 33.0 °C, often fell by 7 °C at night, and the overall mean Tb was 38.7 ± 0.7 °C. The data show that yet another passerine bird, widely viewed to be homeothermic, expresses torpor in the wild for energy conservation. Considering the size of miners, it seems probable that many other, especially smaller birds, use a similar approach at least in winter to enhance the chance of survival in the face of high energy expenditure and low food availability.