Developmental thermoenergetics of the dasyurid marsupial 'Antechinus stuartii'
Although conception-to-weaning times in dasyurid marsupials are extremely long and neonates very small, little is known about their growth and thermoenergetics. We studied the growth pattern of 'Antechinus stuartii' from birth to after weaning in relation to thermoregulatory capabilities and energetic cost of lactation in the female. Litter size was 1-8 young. Growth rate was slow for age 0-40 days, increased until weaning at about 100 days of age, and then slowed again. At weaning, males were 18% heavier than females (t-test, P<0.001). Energy expenditure of females increased significantly by about 30% during late lactation, compared with early or postlactation. Overall, maternal investment increased with increasing litter size. Total energy expenditure from birth to weaning was 2,373 kJ for small litters (1-3 young) and about 4,580 kJ for large litters (8 young). However, at weaning, young from small litters were about 30% heavier than young from large litters. Ability of young 'A. stuartii' to thermoregulate improved with age. At 60 days age, young were poikilothermic after cold exposure, but by 79 days, physiological thermoregulation was established.
Daily torpor in a pregnant common blossom-bat ('Syconycteris australis': Megachiroptera)
Torpor and reproduction in mammals are widely viewed as mutually exclusive processes. For most mammals, different energetic and hormonal demands appear to require a temporal sequence of torpor and reproduction within the yearly schedule. Torpor is charecterised by a pronounced fall in body temperature and metabolic rate, which results in an overall reduction of energy expenditure (Geiser and Ruf 1995) and in most mammals occurs during the non-reproductive season (Goldman et al. 1986; Barnes 1996). Reproduction, on the other hand, requires an increase of energy expenditure for acquiring, processing and transfer of nutrients to the growing offspring (Hoffman 1964; Goldman et al. 1986; Thompson and Nicoll 1986; Kenagy et al. 1989; Barnes 1996).
The physiological ecology and thermal biology of the western and eastern pygmy-possums ('Cercartetus' spp.)
Much of contemporary knowledge about heterothermy in small mammals has been derived from eutherian species inhabiting seasonally distinct environments in the northern hemisphere. The differences between these species and those living in more unpredictable environments are largely unexplored, leaving gaps in understanding. On the Australian continent, mammals from all three subclasses enter torpor; however studies are limited and most are restricted to laboratory investigations. Of the marsupials, only five species from two families are known to enter prolonged torpor or hibernation (i.e. torpor bouts > 24 h in duration); four pygmy-possums (Burramyidae) and the feathertail glider (Acrobatidae). Nevertheless, this group of marsupials has attracted relatively little attention from ecophysiologists. Therefore, the aim of my thesis was to investigate the physiological ecology, thermal biology and use of torpor in the western pygmy-possum 'Cercartetus concinnus' (13 g) and the eastern pygmy-possum 'C. nanus' (26 g), the two most closely related burramyids. Both species are arboreal, nocturnal and omnivorous/nectarivorous, but inhabit vastly different environments. They are known to enter prolonged torpor in captivity in response to low ambient temperature (Ta), but information about their expression of heterothermy in the wild is restricted to incidental trapping accounts. In this thesis I have combined laboratory studies with work conducted on free-ranging individuals to investigate torpor use, body temperature (Tb), metabolic rate (MR), thermal conductance, ventilation, water economy, activity patterns and habitat use of these species. The comparative analysis of my results has bettered our understanding of how these and other small heterotherms function, survive and persist in their natural habitats.
Cool running: locomotor performance at low body temperature in mammals
Mammalian torpor saves enormous amounts of energy, but a widely assumed cost of torpor is immobility and therefore vulnerability to predators. Contrary to this assumption, some small marsupial mammals in the wild move while torpid at low body temperatures to basking sites, thereby minimizing energy expenditure during arousal. Hence, we quantified how mammalian locomotor performance is affected by body temperature. The three small marsupial species tested, known to use torpor and basking in the wild, could move while torpid at body temperatures as low as 14.8-17.9°C. Speed was a sigmoid function of body temperature, but body temperature effects on running speed were greater than those in an ectothermic lizard used for comparison. We provide the first quantitative data of movement at low body temperature in mammals, which have survival implications for wild heterothermic mammals, as directional movement at low body temperature permits both basking and predator avoidance.
Summer and winter torpor use by a free-ranging marsupial
Torpor is usually associated with low ambient temperatures (Ta) in winter, but in some species it is also used in summer, often in response to limited food availability. Since the seasonal expression of torpor of both placental and marsupial hibernators in the wild is poorly documented by quantitative data, we investigated torpor and activity patterns of the eastern pygmy-possum 'Cercartetus nanus' (17.4 g) over two seasons. We used radio telemetry to track animals during winter (n=4) and summer (n=5) in a warm-temperate habitat and found that torpor was used in both seasons. In winter all animals entered periods of short-term hibernation (from 5 to 20 days) containing individual torpor bouts of up to 5.9 days. In summer, torpor bouts were always <1 day in duration, only used by males and were not related to daily mean Ta. Pygmy-possums entered torpor at night as Ta cooled, and rewarmed during the afternoon as Ta increased. Individuals interspersed torpor bouts with nocturnal activity and the percentage of the night animals were active was the same in summer and winter. Our study provides the first information on torpor patterns in free-ranging 'C. nanus', and shows that the use of torpor throughout the year is important for energy management in this species.
Dietary fats and body lipid composition in relation to hibernation in free-ranging echidnas
Laboratory studies have shown that high levels of dietary unsaturated fatty acids prolong torpor and lower body temperatures in hibernating herbivorous rodents, which may in turn improve winter survival. The importance of nutritional ecology in relation to hibernation in insectivorous hibernators is unknown. We therefore studied fatty acid composition of dietary insects and the depot fat of echidnas Tachyglossus aculeatus (Monotremata) during the pre-hibernation season and compared depot fat fatty acid composition before and after hibernation. Echidna depot fat fatty acid composition during the pre-hibernation season was almost identical to that of the most abundant prey species, the ant Iridomyrmex sp. Oleic acid (C18:1) was by far the most common fatty acid in both Iridomyrmex sp. (60%) and echidna depot fat (62%). After about 5 months of hibernation and an 18% loss of body mass, echidna fatty acid composition had changed significantly. The percentage of the monounsaturated oleic acid (C18:1) and palmitoleic acid (C16:1) had declined, whereas that of the saturated fatty acids (C12:0, C16:0, C18:0) and the polyunsaturated linoleic acid (C18:2) had increased. Our study suggests that, unlike herbivorous rodent hibernators, echidnas rely to a large extent on monounsaturated fatty acids as fuel for hibernation, reflecting the most common fatty acid in their food. Moreover, it appears that the high concentration of monounsaturated fatty acids compensates for the moderate availability of polyunsaturates and enables them to hibernate at low body temperatures.
Thermal biology, torpor and behaviour in sugar gliders: a laboratory-field comparison
Most studies on animal physiology and behaviour are conducted in captivity without verification that data are representative of free-ranging animals. We provide the first quantitative comparison of daily torpor, thermal biology and activity patterns, conducted on two groups of sugar gliders ('Petaurus breviceps', Marsupialia) exposed to similar thermal conditions, one in captivity and the other in the field. Our study shows that activity in captive gliders in an outdoor aviary is restricted to the night and largely unaffected by weather, whereas free-ranging gliders omit foraging on cold/wet nights and may also forage in the afternoon. Torpor occurrence in gliders was significantly lower in captivity (8.4% after food deprivation; 1.1% for all observations) than in the field (25.9%), mean torpor bout duration was shorter in captivity (6.9 h) than in the field (13.1 h), and mean body temperatures during torpor were higher in captivity (25.3°C) than in the field (19.6°C). Moreover, normothermic body temperature as a function of air temperature differed between captive and free-ranging gliders, with a >3°C difference at low air temperatures. Our comparison shows that activity patterns, thermal physiology, use of torpor and patterns of torpor may differ substantially between the laboratory and field, and provides further evidence that functional and behavioural data on captive individuals may not necessarily be representative of those living in the wild.
Cardiorespiratory function and metabolism of heterothermic bats
Bats are fascinating in their ability to maintain coordinated cardiorespiratory function at the extremes of metabolism- during flight and torpor. As the only mammals capable of powered flight, bats have developed relatively large and highly efficient hearts and lungs compared to their non-flying counterparts. In addition to this expensive form of locomotion, bats must cope with high heat loss associated with their high surface area to volume ratios because of their small size. To balance these energetic challenges many bats are capable of entering torpor where metabolic rate (MR), cardiac function and body temperature (Tb) are substantially reduced. Torpor use is essential to many bats, can occur almost daily in some species and is often expressed throughout the year. There are two forms of torpor exhibited by heterothermic mammals including bats; daily heterothermy, which consists of short term daily torpor <24h or longer multiday hibernation, which comprises longer multiday torpor bouts punctuated by periodic spontaneous arousals. Previous work on torpor physiology in bats has primarily been undertaken on the thermal energetics of northern hemisphere temperate zone insectivorous species that hibernate in thermally stable environments such as caves or houses. On the other hand, many tree-dwelling bats in Australia enter torpor in thermally labile roosts under tree bark or among exposed foliage and can experience large fluctuations in ambient temperature (Ta). Although the cardiorespiratory system is central to the coordination and maintenance of torpor, as its role in the circulation of blood gases and hormones directly impact on thermoregulation, to date there has been limited investigation of cardiac function in heterothermic bats. Therefore, I aimed to determine the patterns of cardiorespiratory function during torpor in two species of Australian bats that use either hibernation, Gould’s long-eared bat ('Nyctophilus gouldi' Vespertilionidae), or daily torpor, common blossom bat ('Syconycteris australis' Pteropodidae). I also examined the influence of Ta on the relationships between heart rate (HR), ventilation rate (VR), oxygen consumption (V̇O₂) and subcutaneous temperature (Tsub), either at a constant Ta or an increasing Ta profile.
Torpor in Australian birds
Energy-conserving torpor is characterized by pronounced reductions in body temperature and metabolic rate and, in Australian birds, is known to occur in the Caprimulgiformes (spotted nightjar, Australian owlet-nightjar, tawny frogmouth), Apodiformes (white-throated needletail) and the Passeriformes (dusky woodswallow). Anecdotal evidence suggests that it also may occur in the white-fronted honeyeater, crimson chat, banded whiteface, red-capped robin, white-backed swallow, mistletoebird, and perhaps welcome swallow. Daily torpor (bouts lasting for several hours) appears to be the most common pattern, although anecdotal evidence indicates that white-backed swallows can undergo prolonged torpor. Diurnal birds enter torpor only during the night but nocturnal birds may use it by the day and/or night, and often in more than one bout/day. Body temperatures fall from ~38–41°C during activity to ~29°C during torpor in spotted nightjars, tawny frogmouths, dusky woodswallows and white-throated needletails, and to ~22°C in Australian owlet-nightjars. In the spotted nightjar, a reduction in Tb by ~10°C resulted in a 75% reduction in metabolic rate, emphasizing energy conservation potential. Since torpor is likely to be more crucial for the survival of small birds, a detailed understanding of its use is important, not only for physiologists but also ecologists and wildlife managers. It is thus disappointing that so much information on torpidity in Australian birds is anecdotal, and that so little effort has been made to characterize its patterns and quantify the resulting energy savings and survival benefits for birds in the wild.
Torpor and thermal energetics in Australian arid zone bats
In spite of challenging and unpredictable environmental conditions, bats are among the most successful groups of Australian arid zone mammals. Yet knowledge about the thermal biology and energetics of desert bats is scarce. I used temperature-telemetry to obtain data on the thermal physiology, torpor patterns, thermoregulatory behaviour, foraging activity and roosting ecology of desert bats under natural conditions in relation to climate and season. The study species were the inland freetail bat ('Mormopterus species' 3, body mass, BM, 9 g, henceforth 'Mormopterus'), the little broad-nosed bat ('Scotorepens greyii', BM 6 g) and the inland broad-nosed bat ('Scotorepens balstoni', BM 9 g). The study was conducted at Sturt National Park (New South Wales, Australia) over three summers (2010-13), two winters (2011-12) and one spring (2011). In addition, I used flow-through respirometry to collect data on the thermal, metabolic and hygric physiology of 'Mormopterus' and 'S. greyii' over air temperatures (Ta) from 5 to 42°C during summer 2013.