Saving energy via short and shallow torpor bouts.

Maintaining a high and stable body temperature as observed in most endothermic mammals and birds is energetically costly and many heterothermic species reduce their metabolic demands during energetic bottlenecks through the use of torpor. With the increasing number of heterotherms revealed in a diversity of habitats, it becomes apparent that triggers and patterns of torpor use are more variable than previously thought. Here, we report the previously overlooked use of, shallow rest-time torpor (body temperature >30 °C) in African lesser bushbabies, Galago moholi. Body core temperature of three adult male bushbabies recorded over five months showed a clear bimodal distribution with an average active modal temperature of 39.2 °C and a resting modal body temperature of 36.7 °C. Shallow torpor was observed in two out of three males (n = 29 torpor bouts) between June and August (austral winter), with body temperatures dropping to an overall minimum of 30.7 °C and calculated energy savings of up to 10%. We suggest that shallow torpor may be an ecologically important, yet mostly overlooked energy-saving strategy employed by heterothermic mammals. Our data emphasise that torpor threshold temperatures need to be used with care if we aim to fully understand the level of physiological plasticity displayed by heterothermic species.

Disparate roost sites drive intraspecific physiological variation in a Malagasy bat.

Many species are widely distributed and individual populations can experience vastly different environmental conditions over seasonal and geographic scales. With such a broad ecological reality, datasets with limited spatial and temporal resolution may not accurately represent a species and could lead to poorly informed management decisions. Because physiological flexibility can help species tolerate environmental variation, we studied the physiological responses of two separate populations of Macronycteris commersoni, a bat widespread across Madagascar, in contrasting seasons. The populations roost under the following dissimilar conditions: either a hot, well-buffered cave or within open foliage, unprotected from the local weather. We found that flexible torpor patterns, used in response to prevailing ambient temperature and relative humidity, were central to keeping energy budgets balanced in both populations. While bats' metabolic rate during torpor and rest did not differ between roosts, adjusting torpor frequency, duration and timing helped bats maintain body condition. Interestingly, the exposed forest roost induced extensive use of torpor, which exceeded the torpor frequency of overwintering bats that stayed in the cave for months and consequently minimised daytime resting energy expenditure in the forest. Our current understanding of intraspecific physiological variation is limited and physiological traits are often considered to be fixed. The results of our study therefore highlight the need for examining species at broad environmental scales to avoid underestimating a species' full capacity for withstanding environmental variation, especially in the face of ongoing, disruptive human interference in natural habitats.

Tropical bats counter heat by combining torpor with adaptive hyperthermia.

Many tropical mammals are vulnerable to heat because their water budget limits the use of evaporative cooling for heat compensation. Further increasing temperatures and aridity might consequently exceed their thermoregulatory capacities. Here, we describe two novel modes of torpor, a response usually associated with cold or resource bottlenecks, as efficient mechanisms to counter heat. We conducted a field study on the Malagasy bat Macronycteris commersoni resting in foliage during the hot season, unprotected from environmental extremes. On warm days, the bats alternated between remarkably short micro-torpor bouts and normal resting metabolism within a few minutes. On hot days, the bats extended their torpor bouts over the hottest time of the day while tolerating body temperatures up to 42.9°C. Adaptive hyperthermia combined with lowered metabolic heat production from torpor allows higher heat storage from the environment, negates the need for evaporative cooling and thus increases heat tolerance. However, it is a high-risk response as the torpid bats cannot defend body temperature if ambient temperature increases above a critical/lethal threshold. Torpor coupled with hyperthermia and micro-torpor bouts broaden our understanding of the basic principles of thermal physiology and demonstrate how mammals can perform near their upper thermal limits in an increasingly warmer world.

Open-flow respirometry under field conditions: How does the airflow through the nest influence our results?

Open-flow respirometry is a common method to measure oxygen-uptake as a proxy of energy expenditure of organisms in real-time. Although most often used in the laboratory it has seen increasing application under field conditions. Air is drawn or pushed through a metabolic chamber or the nest with the animal, and the O2 depletion and/or CO2 accumulation in the air is analysed to calculate metabolic rate and energy expenditure. Under field conditions, animals are often measured within the microclimate of their nest and in contrast to laboratory work, the temperature of the air entering the nest cannot be controlled. Thus, the aim of our study was to determine the explanatory power of respirometry in a set-up mimicking field conditions. We measured O2 consumption of 14 laboratory mice (Mus musculus) using three different flow rates [50 L*h-1 (834 mL*min-1), 60 L*h-1 (1000 mL*min-1) and 70 L*h-1 (1167 mL*min-1)] and two different temperatures of the inflowing air; either the same as the temperature inside the metabolic chamber (no temperature differential; 20 °C), or cooler (temperature differential of 10 °C). Our results show that the energy expenditure of the mice did not change significantly in relation to a cooler airflow, nor was it affected by different flow rates, despite a slight, but significant decrease of about 1.5 °C in chamber temperature with the cooler airflow. Our study emphasises the validity of the results obtained by open-flow respirometry when investigating energy budgets and physiological responses of animals to ambient conditions. Nevertheless, subtle changes in chamber temperature in response to changes in the temperature and flow rate of the air pulled or pushed through the system were detectable. Thus, constant airflow during open-flow respirometry and consequent changes in nest/chamber temperature should be measured.

Altered thyroid hormone levels affect the capacity for temperature-induced developmental plasticity in larvae of Rana temporaria and Xenopus laevis.

Anuran larvae show phenotypic plasticity in age and size at metamorphosis as a response to temperature variation. The capacity for temperature-induced developmental plasticity is determined by the thermal adaptation of a population. Multiple factors such as physiological responses to changing environmental conditions, however, might influence this capacity as well. In anuran larvae, thyroid hormone (TH) levels control growth and developmental rate and changes in TH status are a well-known stress response to sub-optimal environmental conditions. We investigated how chemically altered TH levels affect the capacity to exhibit temperature-induced developmental plasticity in larvae of the African clawed frog (Xenopus laevis) and the common frog (Rana temporaria). In both species, TH level influenced growth and developmental rate and modified the capacity for temperature-induced developmental plasticity. High TH levels reduced thermal sensitivity of metamorphic traits up to 57% (R. temporaria) and 36% (X. laevis). Rates of growth and development were more plastic in response to temperature in X. laevis (+30%) than in R. temporaria (+6%). Plasticity in rates of growth and development is beneficial to larvae in heterogeneous habitats as it allows a more rapid transition into the juvenile stage where rates of mortality are lower. Therefore, environmental stressors that increase endogenous TH levels and reduce temperature-dependent plasticity may increase risks and the vulnerability of anuran larvae. As TH status also influences metabolism, future studies should investigate whether reductions in physiological plasticity also increases the vulnerability of tadpoles to global change.

Tropical heterothermy is "cool": The expression of daily torpor and hibernation in primates.

Living nonhuman primates generally inhabit tropical forests, and torpor is regarded as a strategy employed by cold-adapted organisms. Yet, some primates employ daily torpor or hibernation (heterothermy) under obligatory, temporary, or emergency circumstances. Though heterothermy is present in most mammalian lineages, there are only three extant heterothermic primate lineages: bushbabies from Africa, lorises from Asia, and dwarf and mouse lemurs from Madagascar. Here, we analyze their phenotypes in the general context of tropical mammalian heterothermy. We focus on Malagasy lemurs as they have been the most intensively studied and also show an unmatched range of flexibility in their heterothermic responses. We discuss the evidence for whether heterothermy should be considered an ancestral or derived condition in primates. This consideration is particularly intriguing given that an understanding of the underlying mechanisms for hibernation in lemurs opens the possibility for insight into genotype-phenotype interactions, including those with biomedical relevance for humans.

Altered thyroid hormone levels affect body condition at metamorphosis in larvae of Xenopus laevis.

Chemical, physical and biological environmental stressors may affect the endocrine system, such as the thyroid hormone (TH) axis in larval amphibians with consequences for energy partitioning among development, growth and metabolism. We studied the effects of two TH level affecting compounds, exogenous l-thyroxine (T4 ) and sodium perchlorate (SP), on various measures of development and body condition in larvae of the African clawed frog (Xenopus laevis). We calculated the scaled mass index, hepatosomatic index and relative tail muscle mass as body condition indices to estimate fitness. Altered TH levels significantly altered the growth, development, survival and body condition in metamorphic larvae in different directions. While exogeno us T4 reduced growth and accelerated development, SP treatment increased growth but slowed down development. Altered TH levels improved body conditions in both treatments and particularly in larvae of the SP treatment but to the detriment of lower survival rates in both TH level altering treatments. The hepatosomatic index was negatively affected by exogenous T4 , but not by SP treatment indicating a lower lipid reserve in the liver in larvae of T4 treatment. These altered TH levels as caused by several environmental stressors may have an influence on individual fitness across life, as body condition at the onset of metamorphosis determines metamorphic and juvenile survival. Further research is needed to determine synergetic effects of environmental stressors on TH levels and its effects on physiological traits such as metabolic rate.

Patterns of temperature induced developmental plasticity in anuran larvae.

Anurans exhibit plasticity in the timing of metamorphosis and tadpoles show phenotypic plasticity in age and size at metamorphosis as a response to temperature variation. This developmental plasticity to changing thermal conditions is expected to be a primary factor that dictates the vulnerability of amphibians to increasing ambient temperatures such as are predicted in climate change scenarios. We analyzed the patterns of thermal effects on size and age at metamorphosis to investigate whether the intraspecific "temperature-size rule" is applicable over a broad range of anuran species by carrying out a combined analysis based on the data from 25 studies performed on 18 anuran species. Furthermore, we tested whether the thermal background of respective populations impacts the capacity for a plastic response in metamorphic traits. We could confirm this pattern for across-population comparisons. All included populations developed faster and 75% were smaller at the onset of metamorphosis when developmental temperatures were warmer, but the sensitivity of growth and developmental rate to a given temperature change was different. We found that the thermal background of a population influences the sensitivity of metamorphic traits and thus, the capacity for a plastic response in growth and developmental rate. Warm adapted populations were less sensitive to temperature variation indicating a reduced capacity for developmental plasticity and therefore, those species may be more vulnerable to the impacts of climate change. Future studies should include a broader range of rearing temperatures and temperature fluctuations to determine full knowledge of the capacity for developmental plasticity within a species-specific thermal window.

Primate Torpor Expression: Ghost of the Climatic Past.

Torpor, the controlled depression of virtually all bodily function during scarce periods, was verified in primates under free-ranging conditions less than two decades ago. The large variety of different torpor patterns found both within and among closely related species is particularly remarkable. To help unravel the cause of these variable patterns, our review investigates primate torpor use within an evolutionary framework. First, we provide an overview of heterothermic primate species, focusing on the Malagasy lemurs, and discuss their use of daily torpor or hibernation in relation to habitat type and climatic conditions. Second, we investigate environmental characteristics that may have been involved in shaping the high variability of torpor expression found in lemurs today. Third, we examine potential triggers for torpor use in lemurs. We propose the "torpor refugia hypothesis" to illustrate how disparate primate torpor patterns possibly evolved in response to environmental cues during glacial periods, when animals were restricted to different refuge habitats along riverine corridors. For example, individuals enduring harsher conditions at higher altitudes likely developed seasonal hibernation, whereas those inhabiting lower elevation river catchments might have coped with unfavorable conditions by employing daily torpor. The ultimate stimuli triggering torpor use today likely differ between the different habitats of Madagascar. The broad diversity of torpor patterns in lemurs among closely related species, both within the same and in distinctly different habitat types, provides an ideal base for research into the stimuli for torpor use in endotherms in general. Our hypothesis highlights the importance of considering the environmental conditions under which ecosystems and species evolved when trying to explain physiological adaptations seen today.

Acclimatization patterns in tropical reptiles: uncoupling temperature and energetics.

The physiological compensation of animals in changing environments through acclimatization has long been considered to be of minor importance in tropical ectotherms due to more stable climatic conditions compared to temperate regions. Contrasting this assumption are reports about a range of metabolic adjustments in tropical species, especially during the last two decades from field acclimatized animals. Metabolic rates are strongly linked to temperature in ectotherms but they also reflect energetic requirements and restrictions. We therefore postulate that the observed variety of acclimatization patterns in tropical reptiles results from an interaction of multiple influences, including food and water availability, rather than from thermal constraints alone. We present new data from two sympatric Malagasy lizards with contrasting acclimatization patterns and, complemented with an extensive literature search, discuss the variety of acclimatization patterns in tropical reptiles with regard to thermal and energetic influences. This broad consideration of constraints allows a rearrangement of apparently controversial patterns into a scheme of decreasing metabolic costs, including two new categories for selective and selective inverse acclimatization, where metabolic shifts are restricted to body temperatures below those preferred during activity.

Nonshivering thermogenesis in the African lesser bushbaby, Galago moholi.

The capacity for nonshivering thermogenesis (NST) plays an important role during arousal from torpid states. Recent data on heterotherms inhabiting warmer regions, however, suggest that passive rewarming reduces the need of metabolic heat production during arousal significantly, leading to the question: to what extent do subtropical or tropical heterotherms depend on NST? The African lesser bushbaby, Galago moholi, enters torpid states as an emergency response only, but otherwise stays normothermic throughout the cold and dry winter season. In addition, this species shows unusual rewarming difficulties during arousal from torpor on cold days. We therefore examined the seasonal adjustments of the capacity for NST of naturally acclimatized G. moholi by stimulation with noradrenaline (NA) injection. Dissection of two adult female bushbabies revealed that G. moholi possesses brown adipose tissue, and NA treatment (0.5 mg kg(-1), s.c.) induced a significant elevation in oxygen consumption compared with control (saline) injection. However, the increase in oxygen consumption following injection of NA was not significantly different between winter and summer. Our results show that the ability to produce heat via NST seems to be available throughout the year and that G. moholi is able to change NST capacity within a very short time frame in response to cold spells. Together with results from studies on other (Afro-)tropical heterotherms, which also indicate low or even absent seasonal difference in NST capacity, this raises the question of whether the definition of NST needs to be refined for (Afro-)tropical mammals.

City comfort: weaker metabolic response to changes in ambient temperature in urban red squirrels.

The ecophysiological responses of species to urbanisation reveal important information regarding the processes of successful urban colonization and biodiversity patterns in urban landscapes. Investigating these responses will also help uncover whether synurban species are indeed urban 'winners'. Yet we still lack basic knowledge about the physiological costs and overall energy budgets of most species living in urban habitats, especially for mammals. Within this context, we compared the energetic demands of Eurasian red squirrels (Sciurus vulgaris) from the core of an urban environment with those from a nearby forest. We measured oxygen consumption as a proxy for resting metabolic rate (RMR) of 20 wild individuals (13 urban, 7 forest), at naturally varying ambient temperature (Ta) in an outdoor-enclosure experiment. We found that the variation in RMR was best explained by the interaction between Ta and habitat, with a significant difference between populations. Urban squirrels showed a shallower response of metabolic rate to decreasing Ta than woodland squirrels. We suggest that this is likely a consequence of urban heat island effects, as well as widespread supplemental food abundance. Our results indicate energy savings for urban squirrels at cooler temperatures, yet with possible increased costs at higher temperatures compared to their woodland conspecifics. Thus, the changed patterns of metabolic regulation in urban individuals might not necessarily represent an overall advantage for urban squirrels, especially in view of increasing temperatures globally.

In Search of Suitable Breeding Sites: Habitat Heterogeneity and Environmental Filters Determine Anuran Diversity of Western Madagascar.

Environmental filtering shapes animal communities by preventing the colonization and persistence of certain species in a given habitat. More heterogenous environments are presumed to support a greater number of species and, consequently, increased species diversity, as environmental filters are also likely more heterogenous. Amphibians are especially sensitive to environmental influences due to distinct characteristics like permeable skin and low mobility. By analyzing the species richness and assemblage composition of tadpoles in 132 breeding ponds, we examined how the interplay of environmental variables shapes anuran species assemblages in breeding habitats of the dry forest of Western Madagascar. We found that environmental filtering is prevalent and habitat heterogeneity not only increases larval species richness but also alters species composition between these assemblages. Our study highlights the need for conserving heterogenous habitats to maintain local diversity. Furthermore, we recommend including multivariate modelling approaches to conservation efforts to acknowledge differences between specific habitats and beta diversity.

Seasonal changes in the parasite prevalence of a small Malagasy lemur species (Lepilemur edwardsi).

Parasitic infections can impact the fitness of individuals and can have influence on animals' population dynamics. An individuals' parasite prevalence often changes depending on external or seasonal changes, for example, rainfall and ambient temperatures, but also on internal changes, for example, changes in body condition. In this study we aimed to identify the environmental factors that may influence the intestinal parasite and ectoparasite prevalence of the folivorous Malagasy primate species, Lepilemur edwardsi, living in a seasonal dry deciduous forest. Species living in this habitat have to adapt to seasonal changes of ambient temperature, with almost no precipitation during the dry season and hence strong fluctuations of resource availability throughout the year. We sampled the feces and ectoparasites of L. edwardsi throughout the year. Intestinal parasite prevalence increased from the wet to the dry season and was highest in the late dry season, which might be due to the accompanying decrease in diet quality. Conversely, ectoparasite prevalence decreased in the dry season, presumably due to the prevailing unfavorable environmental conditions for the development of ectoparasites (i.e., mites and ticks). Paired with the higher resting metabolism and stress level of L. edwardsi during the late dry season, it seems that this species may struggle when dry seasons intensify in its habitat.

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.

Thermal tolerance and acclimation capacity in the European common frog (Rana temporaria) change throughout ontogeny.

Phenotypic plasticity may allow ectotherms with complex life histories such as amphibians to cope with climate-driven changes in their environment. Plasticity in thermal tolerance (i.e., shifts of thermal limits via acclimation to higher temperatures) has been proposed as a mechanism to cope with warming and extreme thermal events. However, thermal tolerance and, hence, acclimation capacity, is known to vary with life stage. Using the common frog (Rana temporaria) as a model species, we measured the capacity to adjust lower (CTmin ) and upper (CTmax ) critical thermal limits at different acclimation temperatures. We calculated the acclimation response ratio as a metric to assess the stage-specific acclimation capacity at each of seven consecutive ontogenetic stages and tested whether acclimation capacity was influenced by body mass and/or age. We further examined how acclimation temperature, body mass, age, and ontogenetic stage influenced CTmin and CTmax . In the temperate population of R. temporaria that we studied, thermal tolerance and acclimation capacity were affected by the ontogenetic stage. However, acclimation capacity at both thermal limits was well below 100% at all life stages tested. The lowest and highest acclimation capacity in thermal limits was observed in young and late larvae, respectively. The relatively low acclimation capacity of young larvae highlights a clear risk of amphibian populations to ongoing climate change. Ignoring stage-specific differences in thermal physiology may drastically underestimate the climate vulnerability of species, which will hamper successful conservation actions.

Season and reproductive activity influence cortisol levels in the Malagasy primate Lepilemur edwardsi.

Throughout the year, wild animals are exposed to a variety of challenges such as changing environmental conditions and reproductive activity. These challenges may affect their stress hormone levels for varying durations and in varying intensities and impacts. Measurements of the glucocorticoid hormone cortisol in the hair of mammals are considered a good biomarker for measuring physiological stress and are increasingly used to evaluate stress hormone levels of wild animals. Here, we examined the influence of season, reproductive activity, sex, as well as body condition on hair cortisol concentrations (HCC) in Lepilemur edwardsi, a small Malagasy primate species. L. edwardsi lives in the seasonal dry forests of western Madagascar, which are characterized by a strongly changing resource availability throughout the year. We hypothesized that these seasonal changes of resource availability and additionally the reproductive cycle of this species would influence HCC of L. edwardsi. Results revealed that hair cortisol concentration of females did not change seasonally or with the reproductive cycle. However, we found a significant increase of hair cortisol levels in males from the early wet season during the early dry season (mating season). This increase is presumably due to changed behavior during the mating season, as sportive lemurs travel more and show aggressive behavior during this time of the year. This behavior is energy-costly and stressful, and presumably leads to elevated HCC. As elevated cortisol levels may impair immune function, L. edwardsi males might also be more susceptible to parasites and diseases, which is unfavorable in particular during a period of low resource availability (dry season).

Sportive lemurs elevate their metabolic rate during challenging seasons and do not enter regular heterothermy.

Animals experience seasonal changes of environmental and ecological conditions in most habitats. Fluctuations in ambient temperature have a strong influence on thermoregulation, particularly on small endothermic mammals. However, different mammalian species cope differently with these changes. Understanding the physiological responses of organisms to different seasons and analysing the mechanisms that account for intra- and inter-specific differences and the ecological consequences of these variations is important to predict species responses to climatic changes. Consequences of climatic changes will be most pronounced in climatically already challenging habitats, such as the dry regions of western Madagascar. We aimed to identify the seasonal responses and adaptive possibilities in energy budgeting of Lepilemur edwardsi, a small primate of this habitat, by measuring metabolic rate (MR; open-flow respiratory) and skin temperature in the field during different seasons. Resting metabolism was generally low, but our study did not detect any signs of regular heterothermic episodes, despite the fact that these are known in other sympatrically living lemurs with a similar lifestyle. Surprisingly, L. edwardsi responded by elevating its resting MR in the poor-resourced dry season, compared to the better-resourced wet season, presumably to master detoxification of their increasingly toxic diet. As body mass decreased over this time, this strategy is obviously not energetically balanced on the long term. This is cause for concern, as it suggests that L. edwardsi has a very small leeway to adjust to changing conditions as experienced due to climate change, as dry season are expected to become longer and hotter, straining water budgets and food quality even more. Moreover, our findings highlight the importance of studying physiological parameters directly in the field and under differing climatic conditions.

Communally breeding bats use physiological and behavioural adjustments to optimise daily energy expenditure.

Small endotherms must change roosting and thermoregulatory behaviour in response to changes in ambient conditions if they are to achieve positive energy balance. In social species, for example many bats, energy expenditure is influenced by environmental conditions, such as ambient temperature, and also by social thermoregulation. Direct measurements of daily fluctuations in metabolic rates in response to ambient and behavioural variables in the field have not been technologically feasible until recently. During different reproductive periods, we investigated the relationships between ambient temperature, group size and energy expenditure in wild maternity colonies of Bechstein's bats (Myotis bechsteinii). Bats used behavioural and physiological adjustments to regulate energy expenditure. Whether bats maintained normothermia or used torpor, the number of bats in the roosts as well changed with reproductive status and ambient temperature. During pregnancy and lactation, bats remained mostly normothermic and daily group sizes were relatively large, presumably to participate in the energetic benefits of social thermoregulation. In contrast, smaller groups were formed on days when bats used torpor, which occurred mostly during the post-lactation period. Thus, we were able to demonstrate on wild animals under natural conditions the significance of behavioural and physiological flexibility for optimal thermoregulatory behaviour in small endotherms.

Physiology: hibernation in a tropical primate.

The Madagascan fat-tailed dwarf lemur, Cheirogaleus medius, hibernates in tree holes for seven months of the year, even though winter temperatures rise to over 30 degrees C. Here we show that this tropical primate relies on a flexible thermal response that depends on the properties of its tree hole: if the hole is poorly insulated, body temperature fluctuates widely, passively following the ambient temperature; if well insulated, body temperature stays fairly constant and the animal undergoes regular spells of arousal. Our findings indicate that arousals are determined by maximum body temperatures and that hypometabolism in hibernating animals is not necessarily coupled to a low body temperature.