Heterothermy as the Norm, Homeothermy as the Exception: Variable Torpor Patterns in the South American Marsupial Monito del Monte (Dromiciops gliroides)

Abstract

Hibernation (i.e., multiday torpor) is considered an adaptive strategy of mammals to face seasonal environmental challenges such as food, cold, and/or water shortage. It has been considered functionally different from daily torpor, a physiological strategy to cope with unpredictable environments. However, recent studies have shown large variability in patterns of hibernation and daily torpor ("heterothermic responses"), especially in species from tropical and subtropical regions. The arboreal marsupial "monito del monte" (Dromiciops gliroides) is the last living representative of the order Microbiotheria and is known to express both short torpor episodes and also multiday torpor depending on environmental conditions. However, only limited laboratory experiments have documented these patterns in D. gliroides. Here, we combined laboratory and field experiments to characterize the heterothermic responses in this marsupial at extreme temperatures. We used intraperitoneal data loggers and simultaneous measurement of ambient and body temperatures (T _A and T _B, respectively) for analyzing variations in the thermal differential, in active and torpid animals. We also explored how this differential was affected by environmental variables (T _A, natural photoperiod changes, food availability, and body mass changes), using mixed-effects generalized linear models. Our results suggest that: (1) individuals express short bouts of torpor, independently of T _A and even during the reproductive period; (2) seasonal torpor also occurs in D. gliroides, with a maximum bout duration of 5 days and a mean defended T _B of 3.6 ± 0.9°C (one individual controlled T _B at 0.09°C, at sub-freezing T _A); (3) the best model explaining torpor occurrence (Akaike information criteria weight = 0.59) discarded all predictor variables except for photoperiod and a photoperiod by food interaction. Altogether, these results confirm that this marsupial expresses a dynamic form of torpor that progresses from short torpor to hibernation as daylength shortens. These data add to a growing body of evidence characterizing tropical and sub-tropical heterothermy as a form of opportunistic torpor, expressed as daily or seasonal torpor depending on environmental conditions.

Keywords: Dromiciops gliroides; Microbiotheria; heterothermia; hibernation; non-Holarctic heterotherms; passive cooling; torpor.

Figure 1

A thermoregulatory polygon of a hibernator, showing the metabolic curve of torpor and the critical body temperature where animals start thermoregulating in torpor (T_Bmin; see text for details, modified from Rezende and Bacigalupe, 2015).

Figure 2

(A) torpid pups (n = 2, approximate age: 3 weeks) found in a torpid female (M_B = 25 g) on December 18, 2020, in the field, with T_A = 25°C and T_B of the female = 25.1°C. Pups were not moving. (B) shows another view, and (C) shows the cluster of torpid individuals found this day (red arrow denotes the examined female). All these animals were found active the next day.

Figure 3

Natural photoperiodic changes during the study period in the outdoor enclosures.

Figure 4

Percentage of torpid D. gliroides (n = 25) in a field study using outdoor enclosures. Torpor incidence was recorded weekly.

Figure 5

(A) Summer experiments in climatic chambers showing short torpor episodes at T_A = 20°C, (B) summer experiment in climatic chambers showing torpor episodes at T_A = 15°C, (C) a representative record of one heterothermic individual during winter (August), showing a few multiday torpor episodes of several days and frequent periodic arousals, (D) statistics of the outdoor experiment showing a high frequency of short torpor episodes of 10 h, and some long, multiday torpor episodes of 100–125 h (detailed statistics are shown in Table 1; colors represent different individuals).

Figure 6

Thermal differential (T_B − T_A) in six monitos. The first four animals (A–D) are from the outdoor experiment, and the last two (E,F) were from the ramp experiment, showing torpor at sub-freezing T_As (see the details in Figure 8). T_Bmin denotes the temperature at which animals start thermoregulating.

Figure 7

Summaries of calculated RMRs from Figure 5, using Newton’s equation for passive cooling: RMR = C_min(T_B − T_A), where C_min = 3.4848 Jg⁻¹ h⁻¹°C⁻¹ (Bozinovic et al., 2004), comparing the metabolic variability obtained in a climatic chamber (A) ramp experiments and in the field (B) outdoor experiments. (C) Shows the ambient and body temperature of a representative individual during the outdoor experiment.

Figure 8

The ramping experiment, where two D. gliroides (A,B; without food access), with intraperitoneal data loggers were gradually exposed first to diminishing temperatures from 5°C to −2.4°C (rate: 1°C day⁻¹). At day 8, T_A was elevated gradually at a similar rate until 28°C, and food was provided ad libitum. The spikes in T_A are because chamber openings. The elevation of T_A between the sixth and seventh day occurred because of the freezing of the climatic chamber compressor.