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Torpor and reproduction in mammals and birds are widely viewed as mutually exclusive processes because of opposing energetic and hormonal demands. However, the reported number of heterothermic species that express torpor during reproduction is ever increasing, to some extent because of recent work on free-ranging animals. We summarize current knowledge about those heterothermic mammals that do not express torpor during reproduction and, in contrast, examine those heterothermic birds and mammals that do use torpor during reproduction. Incompatibility between torpor and reproduction occurs mainly in high-latitude sciurid and cricetid rodents, which live in strongly seasonal, but predictably productive habitats in summer. In contrast, torpor during incubation, brooding, pregnancy, or lactation occurs in nightjars, hummingbirds, echidnas, several marsupials, tenrecs, hedgehogs, bats, carnivores, mouse lemurs, and dormice. Animals that enter torpor during reproduction often are found in unpredictable habitats, in which seasonal availability of food can be cut short by changes in weather, or are species that reproduce fully or partially during winter. Moreover, animals that use torpor during the reproductive period have relatively low reproductive costs, are largely insectivorous, carnivorous, or nectarivorous, and thus rely on food that can be unpredictable or strongly seasonal. These species with relatively unpredictable food supplies must gain an advantage by using torpor during reproduction because the main cost is an extension of the reproductive period; the benefit is increased survival of parent and offspring, and thus fitness.

Metabolic rates of mammals presumably increased during the evolution of endothermy, but molecular and cellular mechanisms underlying basal metabolic rate (BMR) are still not understood. It has been established that mitochondrial basal proton leak contributes significantly to BMR. Comparative studies among a diversity of eutherian mammals showed that BMR correlates with body mass and proton leak. Here, we studied BMR and mitochondrial basal proton leak in liver of various marsupial species. Surprisingly, we found that the mitochondrial proton leak was greater in marsupials than in eutherians, although marsupials have lower BMRs. To verify our finding, we kept similar-sized individuals of a marsupial opossum (Monodelphis domestica) and a eutherian rodent (Mesocricetus auratus) species under identical conditions, and directly compared BMR and basal proton leak. We confirmed an approximately 40 per cent lower mass specific BMR in the opossum although its proton leak was significantly higher (approx. 60%). We demonstrate that the increase in BMR during eutherian evolution is not based on a general increase in the mitochondrial proton leak, although there is a similar allometric relationship of proton leak and BMR within mammalian groups. The difference in proton leak between endothermic groups may assist in elucidating distinct metabolic and habitat requirements that have evolved during mammalian divergence.

Metabolic rate and evaporative water loss (EWL) were measured for a small, arid-zone marsupial, the stripe-faced dunnart (Sminthopsis macroura), when normothermic and torpid. Metabolic rate increased linearly with decreasing ambient temperature (T(a)) for normothermic dunnarts, and calculated metabolic water production (MWP) ranged from 0.85+/-0.05 (T(a)=30 degrees C) to 3.13+/-0.22 mg H2O g(-1) h(-1) (T(a)=11 degrees C). Torpor at T(a)=11 and 16 degrees C reduced MWP to 24-36% of normothermic values. EWL increased with decreasing T(a), and ranged from 1.81+/-0.37 (T(a)=30 degrees C) to 5.26+/-0.86 mg H2O g(-1) h(-1) (T(a)=11 degrees C). Torpor significantly reduced absolute EWL to 23.5-42.3% of normothermic values, resulting in absolute water savings of 50-55 mg H2O h(-1). The relative water economy (EWL/MWP) of the dunnarts was unfavourable, remaining >1 at all T(a) investigated, and did not improve with torpor. Thus torpor in stripe-faced dunnarts results in absolute, but not relative, water savings.

Telomerase activity was examined in two species of bat, Hipposideros armiger and Rousettus leschenaultia , which have similar body mass and lifespan but differ in use of hibernation. We found that telomerase activity was present in all tissues sampled, but it was greater in metabolically active tissues such as liver, spleen, and kidney. Of special interest is the raised activity found in the heterothermic bat H. armiger , and the hibernating bats having raised values for spleen, heart, and kidney. These findings show that maintenance of high levels of telomerase is an essential part of the regulation of cellular activities during hibernation.

The marsupial genus Antechinus is a group of small carnivorous marsupials from the order Dasyuromorphia (Family Dasyuridae) and is found in eastern Australia. The life history of all species in the genus is characterized by a complex, but highly synchronized life cycle in both sexes, culminating in a short mating period followed by total male mortality (semelparity). The breeding season is defined by a specific rate of increase in photoperiod, which is different for each species. In Antechinus spp., male mortality is due to the effects of high free testosterone and cortisol levels on many organ systems. Unusually, spermatogenesis is complete before testosterone levels begin to rise at the winter solstice. In males, low sperm counts have been compensated for by high proportions of sperm reaching the isthmus of the female reproductive tract and long-term storage in the crypts. The females survive to rear their young and may mate again in their second year. Gestation lasts from 26 to 34 days, depending on the species. However, developmental arrest can occur at several stages during embryogenesis, elongating the apparent gestation duration by several days. Several species have strong female sex biases in their litters. The high degree of life history synchrony and the cascade of endocrine-driven physiological events that result in male death are unusual physiological characteristics for mammals. Suggestions why semelparity may have evolved in Antechinus are discussed.

Marsupials, unlike placental mammals, are believed to be unable to increase heat production and thermal performance after cold-acclimation. It has been suggested that this may be because marsupials lack functional brown fat, a thermogenic tissue, which proliferates during cold-acclimation in many placentals. However, arid zone marsupials have to cope with unpredictable, short-term and occasionally extreme changes in environmental conditions, and thus they would benefit from an appropriate physiological response. We therefore investigated whether a sequential two to four week acclimation in Sminthopsis macroura (body mass approx. 25 g) to both cold (16 degrees C) and warm (26 degrees C) ambient temperatures affects the thermal physiology of the species. Cold-acclimated S. macroura were able to significantly increase maximum heat production (by 27%) and could maintain a constant body temperature at significantly lower effective ambient temperatures (about 9 degrees C lower) than when warm-acclimated. Moreover, metabolic rates during torpor were increased following cold-acclimation in comparison to warm-acclimation. Our study shows that, despite the lack of functional brown fat, short-term acclimation can have significant effects on thermoenergetics of marsupials. It is likely that the rapid response in S. macroura reflects an adaptation to the unpredictability of the climate in their habitat.

The cyto- and chemoarchitecture of the cerebral cortex has been examined in three small (mouse-sized) polyprotodont marsupial carnivores from Australia (the stripe-faced dunnart, Sminthopsis macroura; the brown antechinus, Antechinus stuartii; and the red-tailed phascogale, Phascogale calura) in order to compare the cortical topography of these marsupials with that of diprotodontids, didelphids and eutherians. All three species studied had similar cortical cytoarchitecture. The isocortical surface was dominated by primary somatosensory (S1) and visual (V1) areas. Putative secondary sensory areas (S2, V2M, V2L) were also identified. The primary somatosensory cortex demonstrated clumps of granule cells in the presumptive mystacial field, whereas the primary visual area showed a distinctive chemical signature of intense calbindin immunoreactivity in layer IV. On the other hand, the primary auditory area was small and indistinct, but flanked by a temporal association area (TeA). A cytoarchitecturally distinct primary motor cortex (M1) with prominent pyramidal neurons in layer V and poor layer IV was identified medially to S1, and at rostral levels a putative secondary motor area was identified medial to M1. Transitional areas between isocortex and allocortical regions showed many cyto- and chemoarchitectural similarities to those reported for eutherian (and in particular rodent) cortex. Medially, two cingulate regions were found at rostral levels, with dysgranular and granular ‘retrosplenial’ areas identified caudally. Laterally, granular and agranular areas surrounded the rostral rhinal fissure, to be replaced by ectorhinal and perirhinal areas caudally. The findings indicate that the cyto- and chemoarchitectural features which characterize the iso- and allocortex in these small marsupial carnivores are similar to those reported in didelphids and eutherians and our findings suggest the existence of putative dedicated motor areas medial to the S1 field.

Photoperiod and dietary lipids both influence thermal physiology and the pattern of torpor of heterothermic mammals. The aim of the present study was to test the hypothesis that photoperiod-induced physiological changes are linked to differences in tissue fatty acid composition of deer mice, Peromyscus maniculatus (~18-g body mass). Deer mice were acclimated for >8 weeks to one of three photoperiods (LD, light/dark): LD 8:16 (short photoperiod), LD 12:12 (equinox photoperiod), and LD 16:8 (long photoperiod). Deer mice under short and equinox photoperiods showed a greater occurrence of torpor than those under long photoperiods (71, 70, and 14%, respectively). The duration of torpor bouts was longest in deer mice under short photoperiod (9.3 ± 2.6 h), intermediate under equinox photoperiod (5.1 ± 0.3 h), and shortest under long photoperiod (3.7 ± 0.6 h). Physiological differences in torpor use were associated with significant alterations of fatty acid composition in ~50% of the major fatty acids from leg muscle total lipids, whereas white adipose tissue fatty acid composition showed fewer changes. Our results provide the first evidence that physiological changes due to photoperiod exposure do result in changes in lipid composition in the muscle tissue of deer mice and suggest that these may play a role in survival of low body temperature and metabolic rate during torpor, thus, enhancing favourable energy balance over the course of the winter.

Antechinus stuartii has one highly synchronized mating period which occurs at the same time each year. An analysis of the time of reproduction in 162 populations of A. stuartii shows that the onset of the mating period is correlated with the rate of change of photoperiod, rather than with critical photoperiodic length. The rate of change of photoperiod is different for two designated forms of this species and can be used as a predictor of these animals' reproductive timing. A rate of change model further explains the rigid and highly synchronized nature of the mating period and, by providing a mechanism for reproductive isolation, offers an explanation for the evolution of the two forms of this species.

Altricial mammals and birds become endothermic at about half the size of adults and presumably would benefit energetically from entering torpor at that time. Because little is known about torpor during development in endotherms, we investigated whether after the establishment of endothermic thermoregulation (i.e. the ability to maintain a high body temperature during cold exposure), Sminthopsis macroura, a small (~25 g) insectivorous marsupial, is capable of entering torpor and whether torpor patterns change with growth. Endothermic thermoregulation was established when the nest young reached a body mass of ~10 g, and they were capable of entering torpor early during development at ~10-12 g, lending some support to the view that torpor is a phylogenetically old mammalian trait. Torpor bout length shortened significantly and the minimum metabolic rate during torpor increased as juveniles approached adult size, and consequently total daily energy expenditure increased steeply with age. Relationships between total daily energy expenditure and body mass during development of S. macroura (slope ~1.3) differed substantially from the relationship between basal metabolism and body mass in adult endotherms (slope ~0.75) suggesting that the energy expenditure-size relationship during the development differs substantially from that in adults under thermo-neutral conditions. Our study shows that while torpor can substantially reduce energy expenditure during development of endotherms and hence is likely important for survival during energy bottlenecks, it also may enhance somatic growth when food is limited. We therefore hypothesize that torpor during the development in endotherms is far more widespread than is currently appreciated.