Torpor in free-ranging antechinus: does it increase fitness?

Abstract

Antechinus are small, insectivorous, heterothermic marsupial mammals that use torpor from late summer to early winter and reproduce once a year in late winter/early spring. Males die after mating, most females produce only a single litter, but some survive a second winter and produce another litter. As it is not known how these females manage to survive the second winter after the energetically demanding reproductive period and then reproduce a second time, we aimed to provide the first data on thermal biology of free-ranging antechinus by using temperature telemetry. Male Antechinus stuartii and Antechinus flavipes rarely entered torpor in autumn/early winter in the wild, expressing only shallow bouts of <2 h. Female A. stuartii used torpor extensively, employing bouts up to 16.7 h with body temperatures as low as 17.8 °C. Interestingly, although first and second year females used similar torpor patterns, torpor occurrence was almost twofold in second year (93 % of days) than first year females (49 %), and the proportion of the overall monitoring period animals spent torpid was 3.2-fold longer in the former with a corresponding shorter activity period. Our study suggests that intensive use of torpor is crucial for second year females for autumn and winter survival and production of a second litter. We provide the first evidence of an age-related pattern in daily torpor expression in free-ranging mammals and show that torpor use is a complex process that is affected not only by the current energy availability and thermal conditions but also by the reproductive history and age of individuals.

A new cue for torpor induction: charcoal, ash and smoke

“…Yellow-footed antechinus are known to survive forest fires in situ and the survivors were found nesting in crevices in large rocky outcrops after a devastating wildfire (Matthews et al, 2016). Importantly, yellow-footed antechinus employed more torpor in this denuded landscape than in a laboratory study (Geiser, 1988) and also in free-ranging individuals (Rojas et al, 2014). Similar field observations with an increase in torpor use were also made for brown antechinus (Antechinus stuartii) and echidnas (Tachyglossus aculeatus) after management burns (Nowack et al, 2016a;Stawski et al, 2016).…”

“…Therefore, in dunnarts it is likely that the torpor-inducing stimuli of low T a and food restriction might already elicit a maximal torpor response to save energy and further augmentation is not possible. Yellow-footed antechinus, in contrast, do not employ torpor as often as dunnarts and, importantly, do not always do so in response to food restriction (Geiser, 1988;Rojas et al, 2014). Therefore, the response of antechinus to a charcoal/ash substrate by increasing torpor use suggests that they might adjust thermal biology on a finer scale and incorporate more subtle cues than just food restriction alone.…”

“…Additionally, as T b regulation involves the hypothalamus (Heller et al, 1977;Seebacher, 2009), a fast adjustment to the thermal physiology of the animal can be made, as the presence of these products of fire will herald a potential reduction in food availability. The additional acute cue of food restriction will further amplify this response, resulting in enhanced torpor expression in a species that does not enter torpor every day (Geiser, 1988;Rojas et al, 2014). Such a response is particularly pertinent in the forest habitat where antechinus are found (Kelly, 2006;Crowther, 2013) and where a charcoal and ash substrate will be present in large amounts after a fire, accompanied by a reduction in food resources and ground cover and increasing predation pressure .…”

“…Antechinus are semi-arboreal, with nests often located in rock fissures, underground burrows or high in trees, and forage predominantly on arthropods on the ground and also in trees (Dickman, 1980;Marchesan and Carthew, 2004;Lada et al, 2007). While antechinus can use torpor, they usually do not employ torpor every day and often only in response to adverse conditions, and generally females are more likely to use torpor than males (Geiser, 1988;Rojas et al, 2014). Conversely, both male and female arid-zone dunnarts use torpor frequently throughout the year and even express spontaneous torpor (food ad libitum) under laboratory conditions (Warnecke et al, 2008;Stawski et al, 2015).…”

The importance of mammalian torpor for survival in a post-fire landscape

“…As data on the physiological and behavioural mechanisms used by animals to survive changes in climate and fires are scant [13,15], we used this opportunity to test the hypothesis that the use of torpor for energy conservation is an important post-fire survival strategy for the most common terrestrial mammal in the study area, the brown antechinus (Antechinus stuartii; body mass 18-60 g). Antechinus are daily heterotherms and because use of torpor is more pronounced in females than males [16], we focused on females and predicted that they would increase torpor use and decrease activity after the fire.…”