Implications of heat exchange for a free-living endangered marsupial determined by non-invasive thermal imaging.

We used thermal imagining and heat balance modelling to examine the thermal ecology of wild mammals, using the diurnal marsupial numbat (Myrmecobius fasciatus) as a model. Body surface temperature was measured using infra-red thermography at environmental wet and dry bulb temperatures of 11.7-29°C and 16.4-49.3°C, respectively; surface temperature varied for different body parts and with environmental temperature. Radiative and convective heat exchange varied markedly with environmental conditions and for various body surfaces reflecting their shapes, surface areas and projected areas. Both the anterior and posterior dorsolateral body areas functioned as thermal windows. Numbats in the shade had lower rates of solar radiative heat gain but non-solar avenues for radiative heat gain were substantial. Radiative gain was higher for black and lower for white stripes, but overall, the stripes had no thermal role. Total heat gain was generally positive (<4 to >20 W) and often greatly exceeded metabolic heat production (3-6 W). Our heat balance model indicates that high environmental heat loads limit foraging in open areas to as little as 10 min and that climate change may extend periods of inactivity, with implications for future conservation and management. We conclude that non-invasive thermal imaging is informative for modelling heat balance of free-living mammals.

Gas exchange patterns for a small, stored-grain insect pest, Tribolium castaneum.

Insects breathe using one or a combination of three gas exchange patterns; continuous, cyclic and discontinuous, which vary in their rates of exchange of oxygen, carbon dioxide and water. In general, there is a trade-off between lowering gas exchange using discontinuous exchange that limits water loss at the cost of lower metabolic rate. These patterns and hypotheses for the evolution of discontinuous exchange have been examined for relatively large insects (>20 mg) over relatively short periods (<4 h), but smaller insects and longer time periods have yet to be examined. We measured gas exchange patterns and metabolic rates for adults of a small insect pest of grain, the red flour beetle, Tribolium castaneum (Coleoptera: Tenebrionidae), using flow-through respirometry in dry air for 48 h. All adults survived the desiccating measurement period; initially they used continuous gas exchange, then after 24 h switched to cyclic gas exchange with a 27% decrease in metabolic rate, and then after 48 h switched to discontinuous gas exchange with increased interburst duration and further decrease in metabolic rate. The successful use of the Qubit, a lower cost and so more common gas analyser, to measure respiration in the very small T. castaneum, may prompt more flow-through respirometry studies of small insects. Running such studies over long durations may help to better understand the evolution of respiration physiology and thus suggest new methods of pest management.

Re-evaluating model assumptions suggests that Australian birds are more tolerant of heat and aridity than predicted: a response to Conradie et al. (2020).

Conradie et al. (2020) recently modelled the vulnerability of Australian arid birds to a changing climate. While the approach used by Conradie et al. (2020) is valuable, we argue that key assumptions in their study are poorly supported and the risks of a changing climate to arid zone avifauna are consequently overstated.

Water Costs of Gas Exchange by a Speckled Cockroach and a Darkling Beetle.

Respiratory water loss during metabolic gas exchange is an unavoidable cost of living for terrestrial insects. It has been suggested to depend on several factors, such as the mode of gas exchange (convective vs. diffusive), species habitat (aridity), body size and measurement conditions (temperature). We measured this cost in terms of respiratory water loss relative to metabolic rate (respiratory water cost of gas exchange; RWL/V˙CO2) for adults of two insect species, the speckled cockroach (Nauphoeta cinerea) and the darkling beetle (Zophobas morio), which are similar in their mode of gas exchange (dominantly convective), habitat (mesic), body size and measurement conditions, by measuring gas exchange patterns using flow-through respirometry. The speckled cockroaches showed both continuous and discontinuous gas exchange patterns, which had significantly a different metabolic rate and respiratory water loss but the same respiratory water cost of gas exchange. The darkling beetles showed continuous gas exchange pattern only, and their metabolic rate, respiratory water loss and respiratory cost of gas exchange were equivalent to those cockroaches using continuous gas exchange. This outcome from our study highlights that the respiratory water cost of gas exchange is similar between species, regardless of gas exchange pattern used, when the confounding factors affecting this cost are controlled. However, the total evaporative water cost of gas exchange is much higher than the respiratory cost because cuticular water loss contributes considerably more to the overall evaporative water loss than respiratory water. We suggest that the total water cost of gas exchange is likely to be a more useful index of environmental adaptation (e.g., aridity) than just the respiratory water cost.

Geographical variation in the standard physiology of brushtail possums (Trichosurus): implications for conservation translocations.

Identifying spatial patterns in the variation of physiological traits that occur within and between species is a fundamental goal of comparative physiology. There has been a focus on identifying and explaining this variation at broad taxonomic scales, but more recently attention has shifted to examining patterns of intra-specific physiological variation. Here we examine geographic variation in the physiology of brushtail possums (Trichosurus), widely distributed Australian marsupials, and discuss how pertinent intra-specific variation may be to conservation physiology. We found significant geographical patterns in metabolism, body temperature, evaporative water loss and relative water economy. These patterns suggest that possums from warmer, drier habitats have more frugal energy and water use and increased capacity for heat loss at high ambient temperatures. Our results are consistent with environmental correlates for broad-scale macro-physiological studies, and most intra-generic and intra-specific studies of marsupials and other mammals. Most translocations of brushtail possums occur into Australia's arid zone, where the distribution and abundance of possums and other native mammals have declined since European settlement, leading to reintroduction programmes aiming to re-establish functional mammal communities. We suggest that the sub-species T. vulpecula hypoleucus from Western Australia would be the most physiologically appropriate for translocation to these arid habitats, having physiological traits most favourable for the extreme Ta, low and variable water availability and low productivity that characterize arid environments. Our findings demonstrate that geographically widespread populations can differ physiologically, and as a consequence some populations are more suitable for translocation to particular habitats than others. Consideration of these differences will likely improve the success and welfare outcomes of translocation, reintroduction and management programmes.

Measuring metabolic rates of small terrestrial organisms by fluorescence-based closed-system respirometry.

We explore a recent, innovative variation of closed-system respirometry for terrestrial organisms, whereby oxygen partial pressure (PO2 ) is repeatedly measured fluorometrically in a constant-volume chamber over multiple time points. We outline a protocol that aligns this technology with the broader literature on aerial respirometry, including the calculations required to accurately convert O2 depletion to metabolic rate (MR). We identify a series of assumptions, and sources of error associated with this technique, including thresholds where O2 depletion becomes limiting, that impart errors to the calculation and interpretation of MR. Using these adjusted calculations, we found that the resting MR of five species of angiosperm seeds ranged from 0.011 to 0.640 ml g-1 h-1, consistent with published seed MR values. This innovative methodology greatly expands the lower size limit of terrestrial organisms that can be measured, and offers the potential for measuring MR changes over time as a result of physiological processes of the organism.

Adsorption and movement of water by skin of the Australian thorny devil (Agamidae: Moloch horridus).

Moisture-harvesting lizards, such as the Australian thorny devil Moloch horridus, have remarkable adaptations for inhabiting arid regions. Their microstructured skin surface, with channels in between overlapping scales, enables them to collect water by capillarity and passively transport it to the mouth for ingestion. We characterized this capillary water transport for live thorny devils using high-speed video analyses. Comparison with preserved specimens showed that live lizards are required for detailed studies of skin water transport. For thorny devils, there was no directionality in cutaneous water transport (unlike Phrynosoma) as 7 µl water droplets applied to the skin were transported radially over more than 9.2 mm. We calculated the total capillary volume as 5.76 µl cm-2 (dorsal) and 4.45 µl cm-2 (ventral), which is reduced to 50% filling by the time transportation ceases. Using micro-computed tomography and scanning electron microscopy of shed skin to investigate capillary morphology, we found that the channels are hierarchically structured as a large channel between the scales that is sub-divided by protrusions into smaller sub-capillaries. The large channel quickly absorbs water whereas the sub-capillary structure extends the transport distance by about 39% and potentially reduces the water volume required for drinking. An adapted dynamics function, which closely reflects the channel morphology, includes that ecological role.

Avian torpor or alternative thermoregulatory strategies for overwintering?

It is unclear whether torpor really is uncommon amongst passerine birds. We therefore examined body temperature and thermoregulatory strategies of an Austral passerine, the white-browed babbler (Pomatostomus superciliosus), which has characteristics related to a high probability of torpor use; it is a sedentary, insectivorous, cooperative breeding species, which we studied during winter in a temperate habitat. Wild, free-living babblers maintained normothermy overnight, even at sub-zero ambient temperatures, with a mean minimum body temperature of 38.5±0.04°C that was independent of minimum black bulb temperature. Physiological variables measured in the laboratory revealed that babblers had a low basal metabolic rate and evaporative water loss, but their body temperature and thermal conductance were typical of those of other birds and they had a typical endothermic response to low ambient temperature. Huddling yielded significant energy savings at low temperatures and a roost nest created a microclimate that buffered against low temperatures. Low basal energy requirements, communal roosting and the insulation of a roost nest confer sufficient energetic benefits, allowing babblers to meet energy requirements without resorting to heterothermia, even in their depauperate, low-productivity landscape, suggesting that passerine birds use alternatives to torpor to balance their energy budgets when possible.

The private life of echidnas: using accelerometry and GPS to examine field biomechanics and assess the ecological impact of a widespread, semi-fossorial monotreme.

The short-beaked echidna (Tachyglossus aculeatus) is a monotreme and therefore provides a unique combination of phylogenetic history, morphological differentiation and ecological specialisation for a mammal. The echidna has a unique appendicular skeleton, a highly specialised myrmecophagous lifestyle and a mode of locomotion that is neither typically mammalian nor reptilian, but has aspects of both lineages. We therefore were interested in the interactions of locomotor biomechanics, ecology and movements for wild, free-living short-beaked echidnas. To assess locomotion in its complex natural environment, we attached both GPS and accelerometer loggers to the back of echidnas in both spring and summer. We found that the locomotor biomechanics of echidnas is unique, with lower stride length and stride frequency than reported for similar-sized mammals. Speed modulation is primarily accomplished through changes in stride frequency, with a mean of 1.39 Hz and a maximum of 2.31 Hz. Daily activity period was linked to ambient air temperature, which restricted daytime activity during the hotter summer months. Echidnas had longer activity periods and longer digging bouts in spring compared with summer. In summer, echidnas had higher walking speeds than in spring, perhaps because of the shorter time suitable for activity. Echidnas spent, on average, 12% of their time digging, which indicates their potential to excavate up to 204 m3 of soil a year. This information highlights the important contribution towards ecosystem health, via bioturbation, of this widespread Australian monotreme.

Cutaneous water collection by a moisture-harvesting lizard, the thorny devil (Moloch horridus).

Moisture-harvesting lizards, such as the Australian thorny devil, Moloch horridus, have the remarkable ability to inhabit arid regions. Special skin structures, comprising a micro-structured surface with capillary channels in between imbricate overlapping scales, enable the lizard to collect water by capillarity and transport it to the mouth for ingestion. The ecological role of this mechanism is the acquisition of water from various possible sources such as rainfall, puddles, dew, condensation on the skin, or absorption from moist sand, and we evaluate here the potential of these various sources for water uptake by M. horridus The water volume required to fill the skin capillary system is 3.19% of body mass. Thorny devils standing in water can fill their capillary system and then drink from this water, at approximately 0.7 µl per jaw movement. Thorny devils standing on nearly saturated moist sand could only fill the capillary channels to 59% of their capacity, and did not drink. However, placing moist sand on skin replicas showed that the capillary channels could be filled from moist sand when assisted by gravity, suggesting that their field behaviour of shovelling moist sand onto the dorsal skin might fill the capillary channels and enable drinking. Condensation facilitated by thermal disequilibrium between a cool thorny devil and warm moist air provided skin capillary filling to approximately 0.22% of body weight, which was insufficient for drinking. Our results suggest that rain and moist sand seem to be ecologically likely water sources for M. horridus on a regular basis.

Phenophysiological variation of a bee that regulates hive humidity, but not hive temperature.

Seasonal acclimatisation of thermal tolerance, evaporative water loss and metabolic rate, along with regulation of the hive environment, are key ways whereby hive-based social insects mediate climatic challenges throughout the year, but the relative importance of these traits remains poorly understood. Here, we examined seasonal variation in metabolic rate and evaporative water loss of worker bees, and seasonal variation of hive temperature and relative humidity (RH), for the stingless bee Austroplebeia essingtoni (Apidae: Meliponini) in arid tropical Australia. Both water loss and metabolic rate were lower in the cooler, dry winter than in the hot, wet summer at most ambient temperatures between 20°C and 45°C. Contrary to expectation, thermal tolerance thresholds were higher in the winter than in the summer. Hives were cooler in the cooler, dry winter than in the hot, wet summer, linked to an apparent lack of hive thermoregulation. The RH of hives was regulated at approximately 65% in both seasons, which is higher than unoccupied control hives in the dry season, but less than unoccupied control hives in the wet season. Although adaptations to promote water balance appear more important for survival of A. essingtoni than traits related to temperature regulation, their capacity for water conservation is coincident with increased thermal tolerance. For these small, eusocial stingless bees in the arid tropics, where air temperatures are relatively high and stable compared with temperate areas, regulation of hive humidity appears to be of more importance than temperature for maintaining hive health.

Marsupials don't adjust their thermal energetics for life in an alpine environment.

Marsupials have relatively low body temperatures and metabolic rates, and are therefore considered to be maladapted for life in cold habitats such as alpine environments. We compared body temperature, energetics and water loss as a function of ambient temperature for 4 Antechinus species, 2 from alpine habitats and 2 from low altitude habitats. Our results show that body temperature, metabolic rate, evaporative water loss, thermal conductance and relative water economy are markedly influenced by ambient temperature for each species, as expected for endothermic mammals. However, despite some species and individual differences, habitat (alpine vs non-alpine) does not affect any of these physiological variables, which are consistent with those for other marsupials. Our study suggests that at least under the environmental conditions experienced on the Australian continent, life in an alpine habitat does not require major physiological adjustments by small marsupials and that they are physiologically equipped to deal with sub-zero temperatures and winter snow cover.

Pulmonary compliance and lung volume are related to terrestriality in anuran amphibians.

Dehydration tolerance of anuran amphibians is directly related to their ability to mobilize lymphatic reserves, with more terrestrial species having more effective lymph mobilization dependent on specialized skeletal muscles acting directly on the lymph sacs and via pulmonary ventilation. Consequently, we tested the hypothesis that pulmonary compliance, lung volume, and femoral lymphatic sac volume were related to terrestriality-and, hence, lymph mobilization-for 18 species of aquatic, semiaquatic, or terrestrial anuran amphibians. Lung compliance and volume were significantly related to body mass, but there was no significant phylogenetic pattern. There were significant habitat-related patterns for mass-corrected and phylogenetically corrected residuals for these pulmonary variables. Femoral lymph volume was significantly related to body mass, with no significant phylogenetic pattern, and there was only a weak correlation for habitat with mass-corrected and phylogenetically corrected residuals. These results suggest that pulmonary volume and compliance are strongly related to terrestriality in anuran amphibians and are under significant selection pressure to enhance lymph mobilization, but lymph sac volume does not appear to have a major role in adaptation to terrestriality.

Physiological regulation of evaporative water loss in endotherms: is the little red kaluta (Dasykaluta rosamondae) an exception or the rule?

It is a central paradigm of comparative physiology that the effect of humidity on evaporative water loss (EWL) is determined for most mammals and birds, in and below thermoneutrality, essentially by physics and is not under physiological regulation. Fick's law predicts that EWL should be inversely proportional to ambient relative humidity (RH) and linearly proportional to the water vapour pressure deficit (Δwvp) between animal and air. However, we show here for a small dasyurid marsupial, the little kaluta (Dasykaluta rosamondae), that EWL is essentially independent of RH (and Δwvp) at low RH (as are metabolic rate and thermal conductance). These results suggest regulation of a constant EWL independent of RH, a hitherto unappreciated capacity of endothermic vertebrates. Independence of EWL from RH conserves water and heat at low RH, and avoids physiological adjustments to changes in evaporative heat loss such as thermoregulation. Re-evaluation of previously published data for mammals and birds suggests that a lesser dependence of EWL on RH is observed more commonly than previously thought, suggesting that physiological independence of EWL of RH is not just an unusual capacity of a few species, such as the little kaluta, but a more general capability of many mammals and birds.

Huddling behaviour and energetics of Sminthopsis spp. (Marsupialia, Dasyruidae) in response to environmental challenge.

We describe how behavioural responses are an important adjunct to physiological responses for two dunnart marsupials that live in arid environments. Behavioural responses of the stripe-faced dunnart Sminthopsis macroura and the Ooldea dunnart Sminthopsis ooldea differed with acclimation to four ambient temperature (T(a)) regimes, 12 h:12 h of 5-15 °C, 12-22 °C, 18-28 °C and 25-35 °C. Aggression levels were low at regimes 5-15 °C and 12-22 °C, and high at regimes 18-28 °C and 25-35 °C. The proportion of S. macroura huddled in groups increased significantly with decreasing T(a) regime, but there was no aggregation by S. ooldea at low T(a) regimes. The energetic benefit of huddling by S. macroura was highest for pairs of dunnarts (27% saving compared with singles) and only 3% for triplets at T(a)=10 °C. Thermal conductance decreased for pairs but not triplets compared to singles. There were no energetic savings for S. ooldea with increased numbers, and thermal conductance was the same per individual for single, pairs and triplets, reflecting their lack of huddling behaviour. The flexible behavioural (huddling) responses of S. macroura may facilitate their capacity to occupy a broad geographical distribution, unlike S. ooldea, which had inflexible behavioural responses (no huddling) and has a more restricted geographical range. The phylogenetic relationships of the dunnarts suggest that social behaviours may have arisen only once in the most adaptable subgroup of the Sminthopsini.

Evolutionary implications of the distribution and variation of the skeletal muscles of the anuran lymphatic system.

Lymphatic return to the circulation in anurans is dependent upon the interaction of a number of skeletal muscles and lung deflation. We define character states and describe variation of these putative lymphatic skeletal muscles: the M. cutaneus pectoris (CP), M. cutaneus dorsi (CD), M. piriformis (P), M. sphincter ani cloacalis (SAC), and the complex of the M. gracilis minor/M. abdominal crenator (GM/AC). We include examination of over 400 specimens of 377 species belonging to 40 of the 42 currently recognized anuran families. Some muscles show limited variation (P) or are clearly linked to phylogeny (CP; CD) and thus have limited value in the determination of form and function. However, the GM/AC and SAC show a high degree of structural variation that appears in taxa across the phylogenetic spectrum. This allows us to make phylogenetically independent determinations of form and function. We define an ancestral state of the GM and conclude that evolution of the GM/AC and SAC has progressed in two directions from this ancestral state: toward either elaboration or reduction. Where present, the character states of both of these muscle groups were observed in all species examined and the number of states correlated within each family as well. The degree of development of the GM/AC and SAC compliance pump system is strongly correlated with previously determined lymph flux rates in a three species test. Our data suggest there may be a relationship between greater elaboration of the GM/AC and SAC system and terrestriality among the Anura.

Lizard tricks: overcoming conflicting requirements of speed versus climbing ability by altering biomechanics of the lizard stride.

Adaptations promoting greater performance in one habitat are thought to reduce performance in others. However, there are many examples of animals in which, despite habitat differences, such predicted differences in performance do not occur. One such example is the relationship between locomotory performance to habitat for varanid lizards. To explain the lack of difference in locomotor performance we examined detailed observations of the kinematics of each lizard's stride. Differences in kinematics were greatest between climbing and non-climbing species. For terrestrial lizards, the kinematics indicated that increased femur adduction, femur rotation and ankle angle all contributed positively to changes in stride length, but they were constrained for climbing species, probably because of biomechanical restrictions on the centre of mass height (to increase stability on vertical surfaces). Despite climbing species having restricted stride length, no differences have been previously reported in sprint speed between climbing and non-climbing varanids. This is best explained by climbing varanids using an alternative speed modulation strategy of varying stride frequency to avoid the potential trade-off of speed versus stability on vertical surfaces. Thus, by measuring the relevant biomechanics for lizard strides, we have shown how kinematic differences among species can mask performance differences typically associated with habitat variation.

Lymphatic regulation in nonmammalian vertebrates.

All vertebrate animals share in common the production of lymph through net capillary filtration from their closed circulatory system into their tissues. The balance of forces responsible for net capillary filtration and lymph formation is described by the Starling equation, but additional factors such as vascular and interstitial compliance, which vary markedly among vertebrates, also have a significant impact on rates of lymph formation. Why vertebrates show extreme variability in rates of lymph formation and how nonmammalian vertebrates maintain plasma volume homeostasis is unclear. This gap hampers our understanding of the evolution of the lymphatic system and its interaction with the cardiovascular system. The evolutionary origin of the vertebrate lymphatic system is not clear, but recent advances suggest common developmental factors for lymphangiogenesis in teleost fishes, amphibians, and mammals with some significant changes in the water-land transition. The lymphatic system of anuran amphibians is characterized by large lymphatic sacs and two pairs of lymph hearts that return lymph into the venous circulation but no lymph vessels per se. The lymphatic systems of reptiles and some birds have lymph hearts, and both groups have extensive lymph vessels, but their functional role in both lymph movement and plasma volume homeostasis is almost completely unknown. The purpose of this review is to present an evolutionary perspective in how different vertebrates have solved the common problem of the inevitable formation of lymph from their closed circulatory systems and to point out the many gaps in our knowledge of this evolutionary progression.

Thermal and hygric physiology of Australian burrowing mygalomorph spiders (Aganippe spp.).

This study investigated the standard metabolic rate (SMR) and evaporative water loss (EWL) responses of three Australian trapdoor-constructing mygalomorph spider species, two undescribed arid-zone species (Aganippe 'Tropicana A' and A. 'Tropicana B') and a mesic-dwelling species (A. rhaphiduca) to acute environmental regimes of temperature and relative humidity. There were significant effects of species, temperature, and relative humidity on SMR. SMR was lower for A. raphiduca than both A. 'Tropicana' spp. with no difference between the two A. 'Tropicana' spp. Metabolic rate increased at higher temperature and relative humidity for all three species. There were significant effects of species, temperature, and relative humidity on EWL. The mesic Aganippe species had a significantly higher EWL than either arid Tropicana species. EWL was significantly higher at lower relative humidity. Our results suggest an environmental effect on EWL but not SMR, and that mygalomorphs are so vulnerable to desiccation that the burrow provides a crucial refuge to ameliorate the effects of low environmental humidity. We conclude that mygalomorphs are highly susceptible to disturbance, and are of high conservation value as many are short-range endemics.

Thermoregulation by an Australian murine rodent, the ash-grey mouse (Pseudomys albocinereus).

We examine here the thermal physiology of the ash-grey mouse, as there is a paucity of data to explain how Australian rodents meet thermoregulatory demands. Most ash-grey mice remained normothermic over a range of ambient temperatures (10 °C to 30 °C), although they became hyperthermic at high ambient temperatures. One individual entered torpor at ambient temperatures of 20 °C and 25 °C, with minimal body temperatures of 24.5 °C and 28.4 °C respectively, before spontaneously arousing. This is the first evidence of torpor use by an Australian murine rodent. Our data suggest that although ash-grey mice have the physiological ability to use torpor, it is used rarely, presumably due to other behavioural and physiological adaptations. Their higher-than-expected basal metabolic rate (1.56±0.25 mL O(2)g(-1) h(-1)) indicates that ash-grey mice do not have a frugal approach to energy expenditure. Other standard physiological variables were typical of a generalised rodent. A readily-available omnivorous diet, nocturnal activity, semi-fossorial habit and social behaviour presumably allow a high energy lifestyle. A reluctance to use torpor, despite an apparent physiological ability to do so, supports the idea that the use of torpor reflects a net balance between the costs and benefits of a heterothermic thermoregulatory strategy.