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Abstract
Hibernation and daily torpor are physiological strategies to cope with energetic challenges
that occur in many mammalian and avian taxa, but no reliable information exists about
daily torpor or hibernation for any xenarthran. Our objective was to determine whether
the pichi (Zaedyus pichiy), a small armadillo (Xenarthra, Dasypodidae) that inhabits
arid and semi-arid habitats in central and southern Argentina and Chile, enters shallow
daily torpor or prolonged deep hibernation during winter when environmental temperature
and food availability are low. We studied body temperature changes during winter in
semi-captive pichis by means of temperature dataloggers implanted subcutaneously.
All individuals entered hibernation, characterized by torpor events of 75+/-20 h during
which the subcutaneous temperature (T(sc)) decreased to 14.6+/-2.1 degrees C. These
events were interrupted by periods of euthermia of 44+/-38 h with a T(sc) of 29.1+/-0.7
degrees C. After the hibernation season, daily torpor bouts of 4 to 6 h occurred irregularly,
with T(sc) dropping to as low as 24.5 degrees C. We conclude that the pichi is a true
hibernator and can enter daily torpor outside of the hibernation season.
Daily torpor and hibernation are the most powerful measures of endotherms to reduce their energy expenditure. During entrance into these torpid states metabolic rate is suppressed to a fraction of euthermic metabolism, paralleled by reductions in ventilation and heart rate. Body temperature gradually decreases towards the level of ambient temperature. In deep torpor body temperature as well as metabolic rate are controlled at a hypothermic and hypometabolic level. Torpid states are terminated by an arousal where metabolic rate spontaneously returns to normal levels again and euthermic body temperature is established by a burst of heat production. In recent years some of the cellular mechanisms which contribute to hypometabolism have been disclosed. Transcription, translation, as well as protein synthesis are largely suppressed. Cell proliferation in highly proliferating epithelia like the intestine is suspended. ATP production from glucose is reduced and lipids serve as the major substrate for remaining energy requirements. All these changes are rapidly reverted to normometabolism during arousal. Hibernation and daily torpor are found in small mammals inhabiting temperate as well as tropical climates. It indicates that this behaviour is not primarily aimed for cold defense, instead points to a general role of hypometabolism, as a measure to cope with a timely limited or seasonal bottleneck of energy supply.
Many elements of mammalian and avian thermoregulatory mechanisms are present in reptiles, and the changes involved in the transition to endothermy are more quantitative than qualitative. Drawing on our experience with reptiles and echidnas, we comment on that transition and on current theories about how it occurred. The theories divide into two categories, depending on whether selection pressures operated directly or indirectly on mechanisms producing heat. Both categories of theories focus on explaining the evolution of homeothermic endothermy but ignore heterothermy. However, noting that hibernation and torpor are almost certainly plesiomorphic (=ancestral, primitive), and that heterothermy is very common among endotherms, we propose that homeothermic endothermy evolved via heterothermy, with the earliest protoendotherms being facultatively endothermic and retaining their ectothermic capacity for "constitutional eurythermy." Thus, unlike current models for the evolution of endothermy that assume that hibernation and torpor are specialisations arising from homeothermic ancestry, and therefore irrelevant, we consider that they are central. We note the sophistication of thermoregulatory behavior and control in reptiles, including precise control over conductance, and argue that brooding endothermy seen in some otherwise ectothermic Boidae suggests an incipient capacity for facultative endothermy in reptiles. We suggest that the earliest insulation in protoendotherms may have been internal, arising from redistribution of the fat bodies that are typical of reptiles. We note that short-beaked echidnas provide a useful living model of what an (advanced) protoendotherm may have been like. Echidnas have the advantages of endothermy, including the capacity for homeothermic endothermy during incubation, but are very relaxed in their thermoregulatory precision and minimise energetic costs by using ectothermy facultatively when entering short- or long-term torpor. They also have a substantial layer of internal dorsal insulation. We favor theories about the evolution of endothermy that invoke direct selection for the benefits conferred by warmth, such as expanding daily activity into the night, higher capacities for sustained activity, higher digestion rates, climatic range expansion, and, not unrelated, control over incubation temperature and the benefits for parental care. We present an indicative, stepwise schema in which observed patterns of body temperature are a consequence of selection pressures, the underlying mechanisms, and energy optimization, and in which homeothermy results when it is energetically desirable rather than as the logical endpoint.
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