Article

# Metabolic, hygric and ventilatory physiology of the red-tailed phascogale (Phascogale calura; Marsupialia, Dasyuridae): Adaptations to aridity or arboreality?

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## Abstract

The red-tailed phascogale is a small arboreal dasyurid marsupial that inhabits semi-arid to arid regions of Western Australia's wheat belt. Its body mass (34.7 g) is only ∼15% of that predicted based on its phylogenetic position among other dasyuromorphs; we interpret this as an adaptation to its scansorial and semi-arid/arid lifestyle. The standard physiology of this species at a thermoneutral ambient temperature of 30 °C conforms to that of other dasyurid marsupials; body temperature (34.7 ± 0.37 °C), basal metabolic rate (0.83 ± 0.076 mL O2 g−1 h−1), evaporative water loss (1.68 ± 0.218 mg H2O g−1 h−1) and wet thermal conductance (3.8 ± 0.26 J g−1 h−1 °C−1) all fall within the 95% predication limits for the respective allometric relationships for other dasyurid species. Thermolability confers an energy savings at low Ta and water savings at high Ta. Torpor, observed at low Ta, was found to be more beneficial for energy savings than for water economy. The red-tailed phascogale therefore has a physiology suitable for the challenges of arid environments without any obvious requirement for adaptations to its scansorial lifestyle, other than its considerably lower-than-expected body mass.

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... We used lmer (Bates et al. 2014) and lmerTest (Kuznetsova et al. 2014) for EWL, and Bradley and Deavers (1980) for C wet . Ventilatory variables were compared to the combined datasets of Casey et al. (1979) and , with additional data from Darden (1972), Arieli and Ar (1979), Chappell (1985Chappell ( , 1992, Schlenker (1985), Chappell and Roverud (1990) Pusey et al. (2013) and Withers and Cooper (2011). StatistiXL (version 1.6), SPSS (v17 for windows; SPSS Inc.) and custom-written Excel macros and Visual Basic (VB 6) programmes (P Withers) were used for statistical analyses. ...
... The overall T b /T a slope of 0.35 for our short-beaked echidnas, although closer to that of effective thermoregulators (0) than thermoconformers (1), nevertheless suggests that echidnas are less effective thermoregulators than other mammals, at least when inactive and non-reproductive. Indeed, the thermolability below thermoneutrality of a 3.5 kg echidna of 0.282 o C o C -1 is much greater than for various small heterothermic dasyurid marsupials (0.064 o C o C -1 ; Pusey et al. 2013). Nevertheless, they are clearly able to maintain a considerable T b -T a differential. ...
... Generally, PRWE is dependent on body mass, with smaller mammals having higher values (Cooper et al. 2005), so echidnas would be expected to have a reasonably poor PRWE (about 0°C) due to their size (Pusey et al. 2013), although arid-adapted mammals have a higher PRWE than those from more mesic environments (MacMillen and Hinds 1983;MacMillen 1990). The very low PRWE of echidnas is also a consequence of their low energy physiology and myrmecophagous diet. ...
Article
The early divergence of monotremes and therian mammals has resulted in considerable interest in the comparative physiology of the short-beaked echidna (Tachyglossus aculeatus), the most common and widespread living monotreme. However, there are many and varied interpretations of its physiology, reflecting the many and varied studies, limitations and uncertainties of aspects of some previous studies, and potential differences between the various subspecies. Consequently, we thoroughly examine here the standardized physiology of the most widely distributed subspecies of short-beaked echidna (T. aculeatus acanthion) over a wide range of ambient temperatures to definitively assess its physiology in a comparative context. We conclude that the low and variable body temperature of the short-beaked echidna is physiologically "primitive," but it also reflects adaptation to its myrmecophagous niche. Other aspects of its physiology are more typically mammalian. A low metabolic rate reflects its low body temperature, and ventilatory variables are matched to accommodate a modest gas exchange requirement. Thermal conductance is typical for a mammal of equivalent mass. In contrast to previous studies, we demonstrate that short-beaked echidnas can enhance evaporative water loss above thermoneutrality, like other mammals, with a similar capacity for evaporative heat loss. Cooling of their nasal blood sinus with nasal mucous may contribute to this enhanced evaporative cooling. Their capacity to evaporatively cool explains how their distribution can include habitats where ambient temperature, even in shelters, exceeds their supposed critical thermal limit.
... Ten red-tailed phascogales were captured at Dryandra (31846 0 S, 11781 0 E), Western Australia. Metabolic rate (MR; oxygen consumption, VO 2 and carbon dioxide production, VCO 2 ) and EWL were measured by flow-through respirometry at T a values of 20, 25 and 308C (at and below thermoneutrality [8]) and RHs of approximately 17, 36, 48, 63 and 81%, following [6], exploring as close to the entire range of dry to saturated conditions at each T a as logistically possible. Six to 10 post-absorptive phascogales were measured at each RH and T a combination during their rest phase. ...
... Inhibition of EHL at lower DWVP would have the effect of shifting their thermal balance closer to thermoneutrality. However, we calculate this shift to be small, equivalent to an increase in T a of only 0.48C for the lowest DWVP, based on the relationship between VO 2 and T a [8]. ...
... 208C), increased ventilatory minute volume (to accommodate increased MR) should increase insensible EWL above that at T a ¼ 308C in the absence of EWL regulatory control. If respiratory EWL was 50% of total EWL and ventilation increased fourfold [8] (and cutaneous EWL remained constant), then EWL/DWVPT b and EHL would increase 2.5-fold. However, EWL is constant at a range of DWVP at low T a , and this regulation maintains EHL constant despite increased ventilation. ...
Article
'Insensible' evaporative water loss of mammals has been traditionally viewed as a passive process, but recent studies suggest that insensible water loss is under regulatory control, although the physiological role of this control is unclear. We test the hypothesis that regulation of insensible water loss has a thermoregulatory function by quantifying for the first time evaporative water loss control, along with metabolic rate and body temperature, of a heterothermic mammal during normothermia and torpor. Evaporative water loss was independent of ambient relative humidity at ambient temperatures of 20 and 30°C, but not at 25°C or during torpor at 20°C. Evaporative water loss per water vapour pressure deficit had a positive linear relationship with relative humidity at ambient temperatures of 20 and 30°C, but not at 25°C or during torpor at 20 or 25°C. These findings suggest that insensible water loss deviates from a physical model only during thermoregulation, providing support for the hypothesis that regulation of insensible evaporative water loss has a thermoregulatory role.
... Arid zones of Australia are characterized by high temperatures, variable rainfall and low nutrient availability (Morton et al., 2011). Physiological adaptations (e.g., energy conservation and torpor) of red-tailed phascogales is typical of arid zone marsupials and it has been suggested they do not require drinking water (Green et al., 1989;Pusey et al., 2013). Generally species that inhabit arid zones show flexibility in their diet choice to enable their survival (Morton et al., 2011). ...
... Many dasyurids use torpor, the controlled reduction of body temperature and metabolism (Ruf & Geiser, 2014). In captivity phascogales have been observed to enter torpor at ambient temperatures of T a = 13°C, 18°C, and 25°C, and mean normothermic body temperature (T b ) ranges between 30.2°C and 34.7°C (Pusey et al., 2013). ...
Article
There are many limitations when using traditional laboratory species. Limits on variation, may result in limited outcomes, at both the species and individual level, due to different individuals/species having diverse physiological processes, or differing molecular and genetic mechanisms. By using a variety of model species, we will be able to develop creative solutions to biological problems and identify differences of which we were not previously aware. The laboratory mouse has been a suitable model species for various mammalian studies, however most are bred specifically for laboratory research with limited variability due to selective breeding. Marsupial models offer unique research opportunities compared to eutherian models. We believe that there should be an expansion in marsupial model species, and the introduction of the red‐tailed phascogale (Phascogale calura), a dasyurid marsupial, should be one of them. Phascogales are easily managed in captivity, and there are now multiple studies involving their development, reproduction, nutrition, behavior and immune system, which can serve as a baseline for future studies. The addition of the phascogale as a model species will improve future mammalian studies by introducing variability and offer alternate solutions to biological problems, particularly in the areas of genetics, nutrition, immunology, the neuro‐endocrine system, and ageing, due to their semelparous reproductive strategy and hence, subsequent predictive physiology. In this review, we provide information based on existing research on red‐tailed phascogales to support their inclusion as a model species. Highlights • Traditional laboratory species are limited in variation, hence can limit scientific outcomes. • Red‐tailed phascogales are semelparous and easily managed in captivity. • They offer an alternative animal model to investigate biological problems.
... Captive breeding programs have therefore been implemented since 2001 with the end-goal of re-establishing wild populations [14]. Captive breeding colonies have provided excellent opportunities to study the unique biology of the red-tailed phascogale in regards to its nutrition [15][16][17], metabolism [18,19], reproduction [20][21][22], pouch young growth and development [14], nervous tissues [23], and immune tissues and molecules [24][25][26][27][28][29][30]. While most findings are likely to reflect the natural physiology of the red-tailed phascogale, wild and captive populations strikingly differ when it comes to male longevity; in the absence of external stressors, adult phascogale males can survive for more than 2 years in captivity but become infertile after their first breeding season [1,22]. ...
... Water obtained through drinking has been reported to account for more than 1/3 of the total water intake in captive Tasmanian devils and dusky antechinus (Antechinus swainsonii) [41,42], thus suggesting the importance of this source of water for these dasyurids in captivity. However, the energy and water requirements of wild red-tailed phascogales have been suggested to be lower than those of other dasyurid marsupials [18,43]. ...
Article
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Background The red-tailed phascogale is a ‘Near Threatened’ dasyurid marsupial. Males are semelparous and die off shortly after the breeding season in the wild due to a stress-related syndrome, which has many physiological and immunological repercussions. In captivity, males survive for more than 2 years but become infertile after their first breeding season. Meanwhile, females can breed for many years. This suggests that captive males develop similar endocrine changes as their wild counterparts and undergo accelerated aging. However, this remains to be confirmed. The health status and immune function of this species in captivity have also yet to be characterized. Results Through an integrative approach combining post-mortem examinations, blood biochemical and hematological analyses, we investigated the physiological and health status of captive phascogales before, during, and after the breeding season. Adult males showed only mild lesions compatible with an endocrine disorder. Both sexes globally maintained a good body condition throughout their lives, most likely due to a high quality diet. However, biochemistry changes potentially compatible with an early onset of renal or hepatic insufficiency were detected in older individuals. Masses and possible hypocalcemia were observed anecdotally in old females. With this increased knowledge of the physiological status of captive phascogales, interpretation of their immune profile at different age stages was then attempted. During the breeding season, males developed a stress leukogram characterized by a marked lymphopenia, further aggravated by a severe leukopenia after the breeding season. To determine whether these changes were limited to the peripheral blood or had more profound implications, histopathology of the spleen was performed opportunistically. Adult males showed white pulp atrophy, at various degrees. The atrophy was mainly lymphoid and more severe in 1.5-year-old males than in 3.5-year-old females. These results suggest that captive males undergo accelerated immunosenescence. Conclusions Functional studies are now needed to characterize the underlying mechanisms leading to immunosenescence in marsupials. Semelparous dasyurids present great potential for studying the effects of sex and stress on immunity in marsupials. Characterization of these immune-endocrine interactions may help refine veterinary treatment plans, husbandry protocols and conservation programs to maintain the health of captive and wild populations.
... Below thermoneutrality the 'gain' of the physiological system can result in actual T b being below setpoint T b , a differential that increases as T a falls. Both the setpoint T b and the gain vary between species, for example the mean thermolability for dasyurids is 0.064  0.018 °C °C -1 ) but for arboreal dasyurid Phascogale calura thermolability is 0.26  0.04 °C °C -1 (Pusey et al. 2013). Thermolability is rarely reported for birds, even though the high resting T b of birds means significant energy savings can still be made with small T b reductions (Willis & Brigham 2003). ...
... Even though the T b decrease was small, it still provided appreciable energy savings, as on a typical winter night a treecreeper saved 1.19 kJ, equivalent to metabolic input required for 41 minutes at T a = 10 °C. Although interspecific differences in thermolability have been reported (Pusey et al. 2013), how variations in the 'gain' of the thermoregulatory physiology system and hence thermolability fit in as part of broader thermoregulatory strategies is not understood. The construction of metrics such as Thermoregulatory Scope and Heterothermy Index (Boyles et al. 2011a;Boyles et al. 2013) have helped describe the continuum of thermoregulatory responses and facilitate broadscale comparison that is inclusive of smaller ∆T b /∆T a changes, but recognition and understanding of the adaptive mechanisms driving these small responses is still lacking. ...
Thesis
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Four sedentary, insectivorous, Australian passerines (White-browed Babbler, Rufous Treecreeper, Western Yellow Robin, and Australian Magpie) meet energetic requirements under challenging environmental conditions without using mechanisms such as torpor. Instead at low ambient temperature they maintain body temperature just below normothermia by increasing metabolic rate and lowering thermal conductance, a typical endothermic response. Free-ranging birds utilise behavioural strategies like communal roosting and sheltered roost sites to aid thermoregulation, but these are not essential to maintain homeothermy.
... We compared basal values (measured at T a = 30°C) for species nested in habitat by nested ANOVA, using StatistiXL v 1.6, and calculated the PRWE for each species using least squares linear regression of RWE against T a . ANCOVA was used to compare the thermolability of the four antechinus species, calculated as the slope of T b against T a from T a = 10-30 o C. For all comparisons between species, physiological variables were corrected for body mass effects using allometric scaling exponents for marsupials (0.533 for T b , 0.737 for BMR, 0.564 for C wet and C dry and 0.736 for EWL), calculated from the data of Withers et al., 23 Warnecke et al. 42 and Pusey et al. 43 We compared standard T b , BMR, standard EWL and standard C wet (measured at T a = 30°C) of our four species of antechinus to the 95% prediction limits 44 for the log-transformed allometric relationships for other marsupials (using the dataset of Warnecke et al. 42 with additional data from Withers et al., 23 Withers and Cooper, 37 Pusey et al. 43 and Tomlinson et al., 45 using both conventional least-squares regression and phylogenetically-informed regression, after rendering the data independent of phylogeny using autoregression 46,47 and the phylogenetic trees of Bininda-Emonds et al. 48 ...
... We compared basal values (measured at T a = 30°C) for species nested in habitat by nested ANOVA, using StatistiXL v 1.6, and calculated the PRWE for each species using least squares linear regression of RWE against T a . ANCOVA was used to compare the thermolability of the four antechinus species, calculated as the slope of T b against T a from T a = 10-30 o C. For all comparisons between species, physiological variables were corrected for body mass effects using allometric scaling exponents for marsupials (0.533 for T b , 0.737 for BMR, 0.564 for C wet and C dry and 0.736 for EWL), calculated from the data of Withers et al., 23 Warnecke et al. 42 and Pusey et al. 43 We compared standard T b , BMR, standard EWL and standard C wet (measured at T a = 30°C) of our four species of antechinus to the 95% prediction limits 44 for the log-transformed allometric relationships for other marsupials (using the dataset of Warnecke et al. 42 with additional data from Withers et al., 23 Withers and Cooper, 37 Pusey et al. 43 and Tomlinson et al., 45 using both conventional least-squares regression and phylogenetically-informed regression, after rendering the data independent of phylogeny using autoregression 46,47 and the phylogenetic trees of Bininda-Emonds et al. 48 ...
Article
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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 four Antechinus species, two from alpine habitats and two 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.
... Serum from a male animal was chosen to optimise the assay to avoid possible biological variation in female serum due to reproductive status. Serum (50 μL) from the one male RTP was incubated at 34.7°C (Pusey et al. 2013), and a further 50 μL serum was incubated at 56°C for 1 h to inactivate serum complement and act as a negative control. After incubation, the haemolytic assay was performed in 96well (eight rows by 12 columns) round (U) bottom assay plates by transferring 25 μL of serum into columns 1 and 2 of the plate and 25 μL of GVBS to columns 2 to 12. ...
... However, there was a slight decrease in RbE haemolysis from temperatures 30 to 40°C when reacted with female RTP serum, indicating that RbE lysis was complete at approximately 30°C for female RTPs. The optimal incubation temperature between 30 and 40°C was expected in RTPs as these animals have a body temperature of 34.7°C (Pusey et al. 2013), and a functional alternative complement pathway is expected to function best in the animals' regular physiological body temperature. ...
Article
Very few assays that are used to assess the status of mammalian immunity have proved useful for assessment of marsupial health and/or diagnosis of disease. This is largely due to the lack of species cross-reactive reagents that underpin such experiments. To begin to address this deficit, we describe the activation of classical and alternative complement pathways of red-tailed phascogales (RTP; Phascogale calura). Using standard haemolytic assays, the existence of both complement pathways were established in RTP serum based on its ability to lyse unsensitised rabbit erythrocytes (RbE) and sensitised sheep erythrocytes (SE), respectively. The alternative complement pathway assays were conducted using pooled serum of male and female RTPs, and the remaining RTP sera were opportunistically used to test the presence of a functional classical complement system in individual animals, a first in non-eutherian animals. Observations from this study suggest that the activation of these two complement pathways in RTPs are comparable to that seen in other mammals. Since this assay was able to be used on very small samples of blood, it could serve as a useful tool to gather data for comparative immunological studies and to further our knowledge of the mechanisms of immunity available to marsupial young.
... Standard physiological traits (body mass, basal metabolic rate; BMR, T b , EWL, C wet , C dry and PRWE) of WRPs were compared with those of other marsupials in general, and other folivorous marsupials (pseudocheirid and phalangerid possums, the koala [Phascolarctos cinereus] and Matschie's tree kangaroo [Dendrolagus matschiei]; N = 14) specifically, using the dataset of supplemented with additional data (McNab 1988;Krockenberger et al. 2012;Withers et al. 2012;Pusey et al. 2013;Cooper et al. 2016Cooper et al. , 2018Genoud et al. 2018;Turner 2020). Datasets for each variable ranged from N = 29 for PRWE to N = 85 for BMR. ...
Article
Extreme weather events (e.g. heatwaves and droughts) can expose animals to environmental conditions outside of their zones of physiological tolerance, and even resistance, and impact long-term viability of populations and species. We examined the thermal and hygric physiology of the critically endangered western ringtail possum (Pseudocheirus occidentalis), a member of a family of marsupial folivores (Pseudocheiridae) that appear particularly vulnerable to environmental extremes. Basal metabolic rate and other standard physiological variables measured at an ambient temperature of 30°C conformed to values for other marsupials. At lower temperatures, body temperature decreased slightly, and metabolic rate increased significantly at 5°C. At higher temperatures, possums experienced mild hyperthermia and increased evaporative heat loss by licking rather than panting. Their point of relative water economy (–8.7°C) was more favourable than other pseudocheirid possums and the koala (Phascolarctos cinereus). We predict that western ringtail possums should tolerate low ambient temperatures well and be more physiologically tolerant of hot and dry conditions than common (Pseudocheirus peregrinus) and particularly green (Pseudochirops archeri) ringtail possums, and koalas. Our physiological data can be incorporated into mechanistic species distribution models to test our hypothesis that western ringtail possums should physiologically tolerate the climate of habitat further inland than their current distribution, and withstand moderate impacts of climate change in the south-west of Western Australia.
... Furthermore, across both subfamilies the more arid-dwelling species have lower BMR, and hence appear more energetically conservative than more mesically-distributed species. This is consistent with patterns of thermolability previously reported for small Australian mammals from arid ecosystems Pusey et al., 2013;Tomlinson et al., 2007Tomlinson et al., , 2012aWithers and Cooper, 2009). What is not clear is whether this greater tolerance of thermolability and less precise thermoregulation is an adaptation that facilitates energy conservation, or a constraint implied by a limited energy budget (Tomlinson et al., 2012a). ...
... Phascogales for a subsequent translocation in 2010 were sourced from a physiological study at Curtin University (Pusey et al. 2013). They had been wild-caught from a private remnant south of Narrogin in April 2010, but held for about six weeks before translocation. ...
Article
Red-tailed phascogales (Phascogale calura) were reintroduced to Wadderin Sanctuary in the eastern wheatbelt of Western Australia in April 2009 with individuals sourced from remnant native vegetation on farmland some 180km to the west. Their establishment was monitored initially by radio-telemetry and trapping, and subsequently by the checking of nest boxes both within and outside the sanctuary. Translocated phascogales established well and bred successfully in their first season. Phascogales remain extant at Wadderin more than five years after release and appear to be abundant and to occupy all available habitat. They have spread beyond the fenced sanctuary to adjoining woodland and to shrubland and woodland habitat in a remnant 1.4km away. Comparison with two other reintroductions of this species (one apparently successful, one not) suggests management and habitat factors that may have contributed to the outcomes.
Article
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The mountain pygmy possum (Burramys parvus) is an endangered marsupial restricted to boulder fields in the Australian Alps, where it hibernates under the snow during winter. Understanding its habitat requirements is essential for conservation, so we examine here ecological implications of the thermal consequences of maintaining water balance during the hibernation season. Hibernating mountain pygmy possums arousing to consume water must either drink liquid water or consume snow. If they drink water, then the energy required to warm that water to body temperature (4.18 J g-1 oC−1) increases linearly with mass ingested. If they eat snow, then the energy required melt the snow (latent heat of fusion = 332 J g−1) and then warm it to body temperature is much higher than just drinking. For mountain pygmy possums, these energetic costs are a large proportion (up to 19%) of their average daily metabolic rate during the hibernation period and may dramatically shorten it. If mountain pygmy possums lose water equivalent to 5% of body mass before arousing to rehydrate, then the potential hibernation period is reduced by 30 days for consuming snow compared with 8.6 days for drinking water. The consequences of ingesting snow rather than liquid water are even more severe for juvenile possums. A reduction in the hibernation period can impact on the overwinter survival, a key factor determining demographics and population size. Therefore, habitats with subnivean access to liquid water during winter, such as those with subterranean streams running under boulder fields, may be of particular value.
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Hibernation and daily torpor (i.e. temporal heterothermy) have been reported in many marsupial species of diverse families and are known to occur in ∼15% of all marsupials, which is a greater proportion than the percentage of heterothermic placentals. Therefore, we aimed to gather data on heterothermy, including minimal body temperature, torpor metabolic rate and torpor bout duration for marsupials, and relate these physiological variables to phylogeny and other physiological traits. Data from published studies on 41 marsupial species were available for the present analysis. Heterothermic marsupials ranged from small species such as planigales weighing 7 g to larger species such as quolls weighing up to 1000 g. We used the marsupial phylogeny to estimate various heterothermic traits where the current dataset was incomplete. The torpor metabolic rate in relation to basal metabolic rate (%) ranged from 5.2 to 62.8% in daily heterotherms and from 2.1 to 5.2% in marsupial hibernators, and was significantly correlated with the minimum body temperature in daily heterotherms (R 2 = 0.77, P < 0.001), but not in hibernators (R 2 = 0.10, P > 0.05). The mean torpor bout duration ranged from 2 to 15 h in daily heterotherms and from 85 to 342 h in hibernators, and decreased significantly with increasing minimum body tempera-ture in daily heterotherms (R 2 = 0.31, P < 0.001), but was not significant in hiber-nators. Our results show that phylogeny has a significant influence on nearly all analysed individual traits and relationships between traits in daily heterotherms (n = 35), but not in hibernators (n = 6). However, allometric analyses show that many of the physiological parameters scale differently between hibernators and daily heterotherms.
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Most of the variation (98.8 %) in basal rate of metabolism (BMR) in 70 species of marsupials is correlated with body mass, although lowland species have higher basal rates than highland species and burrowers have lower basal rates than non-burrowers. These factors collectively account for 99.2 % of the variation in marsupial BMR. Marsupials differ in BMR from eutherians by having no species with a high basal rate by general mammalian standards, even when consuming vertebrates or grass, food habits that are associated with very high basal rates in eutherians. The absence of high basal rates in marsupials reflects the absence of a correlation of rate of reproduction with basal rate, a correlation present in eutherians. These differences have two consequences: (1) marsupials are less tolerant of cold environments than eutherians, and (2) marsupials coexist with eutherians only when both have food habits associated with low basal rates and therefore when eutherians have reduced rates of reproduction. In Australia and South America marsupial carnivores diversified in the absence of eutherian equivalents. The importation to mainland Australia of dingos by humans appears to have been the immediate cause for the extinction of thylacines, Tasmanian devils, and eastern quolls. Carnivorous marsupials in South America were replaced by eutherians with the completion of the Panamanian land bridge. Macropods, which have lower basal rates than eutherian grazers, survive in central Australia probably because of their adjustment to xeric environments, whereas introduced domestic stock require the provision of water by humans.
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Most studies on torpor in mammals and birds have been conducted in the laboratory. We compared whether patterns of torpor of several mammals and birds differ between the laboratory and field. Our comparison shows that in most species patterns of torpor in the laboratory differ substantially from those in the field. Some species, even if they use torpor extensively in the field. appear most reluctant to enter torpor in captivity. Moreover, torpor in the field is often more frequent, deeper, and longer than in captivity. Our comparison suggests that laboratory studies are likely to underestimate use and depth of torpor in the wild and thus may underestimate its impact on energy expenditure and survival.
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Basal metabolic rate in mammals increases allometrically with body weight, irrespective of the taxonomic level chosen for analysis. Species' deviations from the allometric curve (relative basal metabolic rates) are associated with differences in diet, habitat and taxonomic affinity. When correlations with taxonomy are controlled for, the only consistently significant association that remains is the higher relative basal metabolic rates of vertebrate eaters.
Article
Stripe-faced dunnarts (Sminthopsis macroura) and Ooldea dunnarts (S. ooldea) were acclimated for 2 weeks to ambient temperature (T(a)) regimes of 12-22°C, 18-28°C and 25-35°C, and then measured for standard, basal (BMR) and maximum (MMR) metabolic rate using flow-through respirometry. Sminthopsis macroura maintained a stable body temperature under all experimental T(a) and acclimation regimes. Although its BMR was not statistically different between the three acclimation regimes, the lower end of the thermoneutral zone (TNZ) shifted from 30°C under the 18-28°C and 12-22°C acclimation regimes to 35°C under the 25-35°C acclimation regime. MMR increased significantly at the cooler acclimation regimes. EWL increased at T(a)=35°C, compared with lower T(a), in all acclimation regimes, but an increase in evaporative water loss (EWL) at T(a)=10°C observed in cool acclimations did not occur at the 25-35°C regime. In contrast, S. ooldea had variable body temperature between experimental T(a) in all acclimation regimes, but no acclimational shift in TNZ, which was between 30 and 35°C. Neither BMR nor MMR was affected by exposure to the three acclimation regimes. EWL did not change across T(a) or with acclimation regime. Sminthopsis macroura was flexible in many aspects of its thermoregulation (involving energy and water balance) in response to thermal acclimation, presumably allowing it to balance its energy and water requirements over a broad range of climatic conditions. Sminthopsis ooldea seems to have an inflexible energetic and water balance in response to thermal acclimation, but has low nominal expenditure of either resource on thermoregulation because it thermoregulates less precisely than S. macroura. It seems that S. ooldea is adapted to a more narrow, stable climate.
Article
Total body plethysmography can be used to measure ventilation of hibernating mammals and poikilothenns where other methods are inapplicable as they involve handling the animals excessively. Pressure in a closed chamber containing the animal is recorded as it changes with cyclic variations of temperature and vapor pressure of the inspired and expired gas. In the plethysmograph developed for use with hibemators and poikilothenns, the difference between ambient and body temperature must be small (3–4° C), and the apparatus has been specially designed to eliminate thermal drifts and vibrational noise. Theoretical study of the method shows that simple equations based on isothermal transformations may be applied in physiological (adiabatic) conditions with certain restrictions. The sign of the pressure variation caused by inspiration is the same as that of the body-to-ambience temperature difference. Ventilation of hibernating marmots and of turtles measured with this plethysmograph is briefly described.
1.1. The effects of body size, food habits and limits of endothermy on the energetics of seventeen species of South American ericetid rodents were examined. The combination of mixed diets, together with close to the expected basal rates of heat production, allows most cricetids studied to maintain effective endothermy; but those that have low basal metabolic rates and small sizes show a state of torpor.2.2. Our observations do not support the hypothesis that the absence of torpor in South American ericetid rodents is due to phylogenetic characteristics.3.3. The high ecological diversity, as well as the variety of life modes of these rodents, is explained on an energetic basis.
1.1. No single equation adequately describes the allometric relation between body mass and BMR for mammals.2.2. Least squares regression of log-transformed data for 248 eutherian species results in a line with a slope (−0.30) significantly different from that of Kleiber's line (−0.25).3.3. Interordinal comparisons of least squares regressions of log-transformed BMR and mass suggest that the Insectivora have a significantly steeper slope to their allometric relationship than do most other orders, while the non-insectivore orders are statistically homogeneous with respect to slope.4.4. With respect to elevation, Edentata have the lowest BMRs; Marsupialia, Primates and Chiroptera are indistinguishable from each other but above the edentates; Primates, Chiroptera, Rodentia, Lagomorpha and Carnivora form the next highest homogeneous grouping; and Artiodactyla have the highest BMRs, significantly greater than all but Lagomorpha and Carnivora.5.5. Analysis of intraordinal variation within the Rodentia suggests significant heterogeneity among families in BMR-mass allometry.
Article
We present here the first physiological data for the sandhill dunnart (Sminthopsis psammophila), the second largest (35–44 g) sminthopsine dasyurid marsupial, and report torpor for this species. Their thermoneutral body temperature (34.4 °C), thermolability below thermoneutrality (0.062 °C °C− 1), and mild hyperthermia above thermoneutrality (35.5 °C) are typical of small dunnarts, and dasyurids. Basal metabolic rate (0.80 mL O2 g− 1 h− 1) is as predicted from mass. Sandhill dunnarts generally conform to the Scholander–Irving model of endothermy, although metabolism increases less than expected and extrapolates to a higher than actual body temperature. Wet (0.22 mL O2 g− 1 h− 1 C− 1) and dry (2.8 J g− 1 h− 1 °C− 1) thermal conductances were as predicted. Thermoneutral evaporative water loss (1.6 mg g− 1 h− 1) was only 54% of expected, but this is not significantly different, and more likely reflects variability in the marsupial dataset than an adaptation. Relative water economy resembles that of other small marsupials, rodents and birds, with a point of relative economy of 18 °C. Respiratory ventilation closely matches metabolic rate, with minute volume increased at low ambient temperatures by increased breathing rate rather than tidal volume; oxygen extraction was constant at about 17%, except during hyperthermia above the thermoneutrality. Torpor conferred significant energetic and hygric benefits. We found no evidence of deviation from allometrically- and phylogenetically-based expectations despite the sandhill dunnart's arid habitat and large (for a dunnart) body mass.
Article
There is no empirical evidence for the claim that basal or active daily metabolic rates contribute to taxonomic variation in mammalian or eutherian life hisotries when body-size effects are controlled for. There is also no empirical evidence for the claim that dietary differences contribute to taxonomic variation in mammalian or eutherian metabolic rates when body-size effects are controlled for.
Article
Giles' planigale (Planigale gilesi) is among the smallest extant marsupials and inhabits deep soil cracks in arid floodplains. We examined whether its physiology shows specific adaptations to its extreme habitat. Metabolic rate, body temperature, evaporative water loss and thermal conductance were measured for eight planigales (average mass 9 g) exposed to four different ambient temperatures ranging from 10 degrees C to 32 degrees C. Water economy and respiratory variables were measured for the first time in this species. All of these standard physiological variables conformed to allometrically-predicted values for a marsupial. All variables were significantly affected by ambient temperature, except tidal volume and dry thermal conductance. Metabolic rate increased substantially at low ambient temperatures, as required to maintain a relatively constant body temperature of about 32-34 degrees C. This increased oxygen demand was accommodated by increased ventilation rather than increased oxygen extraction. Planigales had a comparatively high point of relative water economy of 19.1 degrees C, consistent with their small body size and arid habitat. Torpor reduced energy expenditure by 79% and evaporative water loss by 62%. Our study suggests that torpor use, along with behavioural adaptations, suffice for P. gilesi to live underground in arid habitats without further physiological adaptations.
Article
The chuditch is a large carnivorous dasyurid marsupial. Historically it had one of the widest geographical distributions of all marsupials, encompassing much of arid Australia, but it is now restricted to the mesic south-west of Western Australia. It is therefore of interest to determine if its physiology better reflects adaptation to its historically arid or present mesic habitat. The basic physiological parameters of the chuditch conform to other marsupials. Body mass of males (1385 g) was >400% of that predicted by phylogeny and this may be related to its carnivorous diet. Body temperature was 33.9 degrees C at ambient temperatures < or = thermoneutrality, with hyperthermia occurring above thermoneutrality. Basal metabolic rate was 0.361 mL O(2) g(-1) h(-1) at an ambient temperature of 31 degrees C. Metabolic rate increased below the thermoneutral zone by 0.038 mL O(2) g(-1) h(-1) degrees C(-1), and above the thermoneutral zone to 0.444+/-0.059 mL O(2) g(-1) h(-1) at 33.3 degrees C. Standard evaporative water loss was 0.498+/-0.071 mg g(-1) h(-1) at an ambient temperature of 26.0 degrees C, and increased at higher ambient temperatures due to panting and licking. Changes in wet thermal conductance largely reflected changes in evaporative heat loss, and dry thermal conductance increased at high ambient temperature due in part to posture change. Ventilatory parameters were consistent with metabolic demands in and below thermoneutrality, and suggested augmented evaporative heat loss above the thermoneutral zone. Chuditch had a high point of relative water economy of 22.6 degrees C, indicating favourable water economy at even moderate ambient temperatures, due to its low evaporative water loss rather than high metabolic water production. Chuditch were physiologically more similar to marsupials from arid rather than mesic habitats, better reflecting their historical distribution than their current geographical range.
Article
Zoogeographical effects on the basal metabolic rate (BMR) of 487 mammal species were analyzed using conventional and phylogenetically independent ANCOVA. Minimal BMR variance occurred at a "constrained body mass" of 358 g, whereas maximum variance occurred at the smallest and largest body masses. Significant differences in BMR were identified for similar-sized mammals from the six terrestrial zoogeographical zones (Afrotropical, Australasian, Indomalayan, Nearctic, Neotropical, and Palearctic). Nearctic and Palearctic mammals had higher basal rates than their Afrotropical, Australasian, Indomalayan, and Neotropical counterparts. Desert mammals had lower basal rates than mesic mammals. The patterns were interpreted with a conceptual model describing geographical BMR variance in terms of the influence of latitudinal and zonal climate variability. Low and high basal rates were explained in unpredictable and predictable environments, respectively, especially in small mammals. The BMR of large mammals may be influenced in addition by mobility and predation constraints. Highly mobile mammals tend to have high BMRs that may somehow facilitate fast running speeds, whereas less mobile mammals are generally dietary specialists and are often armored. The model thus integrates physiological and ecological criteria and makes predictions concerning body size and life-history evolution, island effects, and locomotor energetics.