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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