The ecology and evolution of the monito del monte, a relict species from the southern South America temperate forests

Abstract

The arboreal marsupial monito del monte (genus Dromiciops, with two recognized species) is a paradigmatic mammal. It is the sole living representative of the order Microbiotheria, the ancestor lineage of Australian marsupials. Also, this marsupial is the unique frugivorous mammal in the temperate rainforest, being the main seed disperser of several endemic plants of this ecosystem, thus acting as keystone species. Dromiciops is also one of the few hibernating mammals in South America, spending half of the year in a physiological dormancy where metabolism is reduced to 10% of normal levels. This capacity to reduce energy expenditure in winter contrasts with the enormous energy turnover rate they experience in spring and summer. The unique life history strategies of this living Microbiotheria, characterized by an alternation of life in the slow and fast lanes, putatively represent ancestral traits that permitted these cold-adapted mammals to survive in this environment. Here, we describe the ecological role of this emblematic marsupial, summarizing the ecophysiology of hibernation and sociality, updated phylogeographic relationships, reproductive cycle, trophic relationships, mutualisms, conservation, and threats. This marsupial shows high densities, despite presenting slow reproductive rates, a paradox explained by the unique characteristics of its three-dimensional habitat. We finally suggest immediate actions to protect these species that may be threatened in the near future due to habitat destruction and climate change.

Keywords: Australidelphia; climate change; conservation; hibernation; marsupial; seed dispersal.

FIGURE 1

Dromiciops gliroides individuals found nesting together at the San Martin experimental station (Photograph: Roberto F. Nespolo)

FIGURE 2

Updated Dromiciops gliroides distribution, including the new records extending the range to the South (based on Mejías et al., ; Oda et al., 2019)

FIGURE 3

Calibrated fossil phylogeny of Microbiotheria modified from Goin and Abello (2013), showing the closeness of D. gliroides and Microbiotherium. According to these authors, Dromiciops and Microbiotherium are morphologically indistinguishable

FIGURE 4

Dromiciops phylogenetic tree showing the support of two different species: Dromiciops bozinovici in the northern clade (a) and Dromiciops gliroides in the two southern clades (b and c). Colors show the correspondence of genetic distances and the locations in map. Illustrations of both Dromiciops species are shown. This figure was adapted from Quintero‐Galvis et al. (2021)

FIGURE 5

Dromiciops developmental stages. Panels a and b correspond to lactation in the pouch I, panels c and d correspond to lactation in the pouch II, panels e and f correspond to lactation outside the pouch, panel g correspond to juveniles, and panel h correspond to adults. Photos: R. Nespolo

FIGURE 6

Annual cycle of Dromiciops gliroides showing its physiological, tissue, and biochemical changes during torpor and activity periods based on the summary provided in Nespolo et al. (2018). Particular cellular modifications involve tissue and cell protection during torpor, attained by overexpression of genes codifying for molecular chaperones and other pro‐survival mechanisms such as anti‐apoptotic pathways, mechanisms avoiding muscular atrophy and shifts from carbohydrate to fat metabolism (see details in Nespolo et al., 2018). The stages of the cycle were modified from Muñoz‐Pedreros et al. (2005), and detailed in the text (Nespolo, Fontúrbel, et al., 2022)

FIGURE 7

A hypothetical (but realistic) annual budget of energy and activity of a M _B = 40 g (lean mass) Dromiciops gliroides, summarized from descriptions of the reproductive cycle (Muñoz‐Pedreros et al., 2005), seasonal variations in activity, adiposity, and body mass (Celis‐Diez et al., ; Franco et al., 2017), and food availability (Franco et al., ; Quijano, ; di Virgilio et al., 2014). After reproduction, D. gliroides reduce activity and energy expenditure (dashed line) and accumulate almost twice their body size in fat (Franco et al., 2017). Fat accumulation (dotted line) was estimated from body mass fluctuations using quantitative magnetic resonance, which indicated that animals could double their body mass in autumn (Mejías et al., 2022)

FIGURE 8

Photos of hibernating D. gliroides taken from an outdoor facility near Valdivia in May (austral autumn). (a) Four clustered individuals packed to minimize heat loss in a nest (uncovered). (b) A single individual within a typical nest built on bamboo (Chusquea quila) leaves and mosses. (c) A thermography of four clustered individuals showing their body temperature (~5°C, according to the color bar scale to the right). Ambient temperature is 5.2°C. (d) Lateral view of hibernating individuals. Photo credits: panel (a) R. Nespolo, panel (b) C. Mejias, panel (c) E. Oda, panel (d) P. Gutiérrez