The Physiological Ecology of the Enigmatic Colocolo Opossum, the Monito del Monte (genusDromiciops), and Its Role as a Bioindicator of the Broadleaf Biome

Abstract

Physiological ecology explains why some physiological designs are so intimately associated with a given environment. Here we present the case of the monito del monte (Dromiciops gliroides), an arboreal marsupial adapted to the southernmost relict fragment of the broadleaf forest biome in South America. Dromiciops is considered the last living representative genus of the order Microbiotheria, whose ancestors are known to have colonized Australia through an Antarctic bridge in the Cretaceous (65 mya). These marsupials survive almost exclusively in well-grown, undisturbed broadleaf forests, where densities are high (10–20 ind per ha), compared with other sympatric mammals (e.g. rodents). However, monitos show the typical long breeding period of Australidelphians (∼3.5 months), small litter size (1–4 pups), long lactation (∼70 days), extended parental care (1 year), and long generation time (2 years). Here we posit that the ecological success of monitos is explained by Microbiotheriid autoecological adaptations to the ecological niche provided by the broadleaf forest biome, retained until today by Dromiciops. These marsupial adaptations maximized survival, rather than reproductive output; and are characterized by omnivory-frugivory, nocturnal-arboreal habits, and sociality with nestling behavior. In addition, the unique opportunistic hibernation capacity of this marsupial allows it to shut down its metabolism in times of low trophic supply, promoting the efficient use of energy during periods of scarcity. In summary, Dromiciops (and probably, Microbiotherians) exhibits an investment strategy in viability and survival, which promoted longevity in the arboreal, cold, and seasonal niche of the forest.

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

“…In terms of the allometric predictions for life histories in marsupials, given by the equation: age at first reproduction =5.75* M B 0.10 provided by Hamilton et al (2011), a 30 g marsupial such as Dromiciops should have an age of first reproduction of 243 days (but it attains sexual maturity at 720 days). A similar computation for a maximum lifetime (=0.041* M B 0.20 , Hamilton et al, 2011) gives 2.5 years (but in Dromiciops , this parameter is above 4–5 years; Nespolo, Saenz‐Agudelo, et al, 2022). Then, the high observed densities of Dromiciops can only be explained by low mortality and an extended reproductive period during their lifetime, which can only be achieved in a large and spatially complex three‐dimensional habitat that serves as a refuge, such as mature temperate rainforests.…”

“…Hence, the small living Microbiotherids, with an verage reproductive output of two individuals per year (Nespolo, Saenz-Agudelo, et al, 2022), fall in the "slow" extreme. In terms of the allometric predic- Hershkovitz (1999) proposed that Microbiotheriids' life history is intimately associated with a combination of Nothofagus trees and Chusquea native bamboos (i.e., the Chusquea-Nothofagus-Microbiotheria association, CNF), which allowed them to build their sophisticated and impermeable nests that, in turn, are fundamental for hibernating in such a humid and cold forest.…”

“…However, they do not stop suckling and use the nest as a center for homerange activities (stage V: extra-marsupium development) (Figure 5). (Nespolo, Saenz-Agudelo, et al, 2022). In comparison, opossums (Thylamys elegans, for instance, which is sympatric with D. bozinovici in its northern distribution range) produce up to 16 individuals per reproductive event, which attain sexual maturity at the first year.…”

“…For instance, a female Dromiciops individual can produce a maximum of four offspring in a single reproductive event each year, which become fertile at the second year. This represents a maximum reproductive output of two new individuals per year (Nespolo, Saenz‐Agudelo, et al, 2022). In comparison, opossums ( Thylamys elegans , for instance, which is sympatric with D .…”

“…Reproduction in Dromiciops is followed by a fattening period in which animals forage frenetically to gain weight for hibernation, which starts in autumn (Nespolo, Fontúrbel, et al, 2022). The peak of energy expenditure occurs during lactation, the longest recorded in marsupials and in Dromiciops extends from December to January (Nespolo, Fontúrbel, et al, 2022; Nespolo, Saenz‐Agudelo, et al, 2022). To compensate for the high energy expenditure of this extravagant way of life, Dromiciops must reduce energy expenditure in the cold period, which is achieved by hibernation.…”