Daily, seasonal, and “hot” torpor in Dromiciops
The seasonal regulation of energy balance is a key concept in mammalian life histories (Harvey, Pagel, & Rees, 1991), and hibernation—a distinctive characteristic of Dromiciops —represents the evolution of “slow” life histories (Turbill, Bieber, & Ruf, 2011).Dromiciops spend six months a year in this lethargic condition, constraining the activity period to spring and summer (Figure 5). In eutherian hibernators, there is a marked cycle of adiposity, where animals accumulate fat during summer to be consumed during hibernation, without ingesting any food during this period (Humphries, Kramer, & Thomas, 2003; Humphries, Thomas, & Speakman, 2002; Toien et al., 2011). In Dromiciops , this cycle is unclear as they ingest food whenever they find it, which can happen even during interbout arousals when hibernating (Franco, Contreras, Place, Bozinovic, & Nespolo, 2017; Nespolo et al., 2020). In this section, we discuss distinctive aspects of seasonality and energetics of D. gliroides : its capacity for daily, seasonal torpor and aestivation (torpor in response to hot and dry conditions).
Hibernation (also known as “seasonal torpor”; Geiser & Ruf, 1995) was first described in placental mammals of the northern hemisphere (e.g., squirrels, marmots, hamsters, bears; Melvin & Andrews, 2009), where a clear pattern of seasonal metabolic depression in autumn and winter is distinguished from continuous periods of activity in spring and summer (Geiser, Currie, O’Shea, & Hiebert, 2014; Heldmaier, Ortmann, & Elvert, 2004). This is functionally different from daily torpor, which consists of short and shallow bouts of metabolic depression of a few hours that occur at any moment of the year and is characteristic of several bat and marsupial species (Geiser, 2013; Ruf & Geiser, 2015).Dromiciops seems to do both, as was confirmed recently by a set of experiments under semi-natural enclosures, indicating that in winter, animals experience seasonal torpor with multiday torpor episodes lasting 5 to 10 days, which together represents a net energy savings of 90% compared to animals that did not hibernate (Mejías, Sabat, Franco, Bozinovic, & Nespolo, 2022). This complemented older studies indicating that Dromiciops experiences a dynamic form of torpor, including daily torpor of a few hours, at any moment of the year, whenever food or water is scarce (Nespolo, Fontúrbel, et al., 2021). A novel aspect ofDromiciops torpor was recently revealed when animals under hot torpor (also known as aestivation: metabolic depression under hot and dry conditions) were discovered in the field (Nespolo, Fontúrbel, et al., 2021). These authors described torpor in summer, with temperatures were above 25ºC and water was scarce. The same study described torpor in females with pups at the marsupium (pups were also in torpor, see Fig 2 in Nespolo, Fontúrbel, et al., 2021). When entering into winter torpor, animals experience a metabolic shut-down followed by passive cooling, to a limit of about –0.5ºC in the tissues, and then they start thermoregulating in torpor in order to avoid freezing (Mejías et al., 2022; Nespolo, Fontúrbel, et al., 2021). The whole transition from normothermia to torpor lasts 4-6 hours (Cortés, Franco, Moreno-Gómez, Barrientos, & Nespolo, 2014), and happens in the nest, normally in groups of two to five individuals (Franco et al., 2011; Nespolo, Fontúrbel, et al., 2021), but arousal can be as rapid as in 30–150 minutes, depending on ambient temperature (Mejías et al., 2022; Nespolo, Fontúrbel, et al., 2021). These costly rewarming events are bursts of aerobic activity that could account for 25% of the energy consumed during hibernation (Mejías et al., 2022). Rewarming during hibernation have a typical frequency in winter of about twice a month (Nespolo, Fontúrbel, et al., 2021; Nespolo, Mejías, et al., 2021), which explains why long-term energy savings during hibernation (90%) are lower than the energy reduction estimated from a single torpor bout (96%, see Mejías et al., 2022). The extreme capacity to endure under-zero temperatures of hibernating Dromiciops explains its presence in high Andean locations such as Altos de Lircay at the northern edge of the distribution (Mejías et al., 2021), Llao Llao in Argentina (Rodriguez-Cabal, Amico, Novaro, & Aizen, 2008) or Futaleufú at the southern limit (Oda et al., 2019). The seasonal cycle of hibernation-activity of Dromiciops define an annual energy budget with profits and loss, that the animal modulates precisely in order to give an overall positive balance (Figure 6).
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