The “conservative” reproduction of Dromiciops
Although the basic biology of Dromiciops has been historically
considered poorly known, this situation has drastically changed in the
last decades, as several populations have been studied in detail by
Latin American researchers (e.g., Balazote-Oliver et al., 2017;
Celis-Diez et al., 2012; Fontúrbel, Franco, Rodríguez-Cabal, Rivarola,
& Amico, 2012; Franco, Quijano, & Soto-Gamboa, 2011; Kelt, Meserve,
Patterson, & Lang, 1999; Meserve, 1981; Meserve, Lang, & Patterson,
1988; Patterson, Meserve, & Lang, 1989). Inappropriate capture methods
(Fontúrbel, 2010; Fontúrbel & Jiménez, 2009), but also lack of
knowledge about its seasonal activity patterns led to a large
underestimation of its densities (Fontúrbel & Jiménez, 2011; Franco et
al., 2011; Nespolo, Verdugo, Cortes, & Bacigalupe, 2010). For example,
captive D. gliroides individuals seem to be more active during
summer than during other seasons (Aizen, 2003; Kelt & Martínez, 1989),
but only recently, several authors have studied Dromiciopsactivity in the field. For instance, Fontúrbel, Candia, and Botto-Mahan
(2014) found that this species presents a nocturnal activity (from 19:00
h to 07:00 h), with a significant monthly variation related to resource
abundance and distribution, closely related to fleshy fruit availability
(di Virgilio et al., 2014; Fontúrbel, Salazar, & Medel, 2017b).
Historical descriptions (Hershkovitz, 1999; Mann, 1978; Muñoz-Pedreros,
Lang, Bretos, & Meserve, 2005) indicate that Dromiciops is
relatively long-lived, with reports of 5–6 years-old individuals
captured in the field (Balazote-Oliver et al., 2017). According to
Muñoz-Pedreros et al. (2005), D. gliroides reproductive cycle is
divided into seven stages. They attain sexual maturity at the second
year of age and start reproducing in August-September (stage I: pair
formation), then producing 1–4 pups (females have four nipples) that
develop in the uterus for about a month (stage II: intra-uterine
development), and approximately in early November they migrate to the
marsupium (stage III: parturition) and start lactation (stage IV:
intra-marsupium development). Most Australian marsupials are
characterised by secreting milk of different compositions from different
mammary glands, in close concordance to the development stage of the
young (Pharo, 2019; Renfree, 1981), which is unknown for this
marsupial. During the austral summer (December–January), pouched
young abandon the marsupium for short exploratory excursions. However,
they do not stop suckling and use the nest as a centre for home-range
activities (stage V: extra-marsupium development) (Figure 4). Finally,
juveniles join family excursions during February (stage VI: nocturnal
family excursions), coinciding with the elevated trapping success
usually reported. Then, juveniles become independent in March (Stage
VII: juvenile independence) and start preparing for hibernation (see
below). A summary of Dromiciops annual cycle is presented in
Figure 5.
<Figures 4 and 5 about here>
This extended Dromiciops breeding (i.e., 20 days of gestation and
70 days lactating), which is also energetically very extenuating and
energy consuming, is combined with a low reproductive output. For
instance, a female Dromiciops individual can produce a maximum of
four offspring in a single reproductive event each year and become
fertile at the second year. This represents a reproductive output of two
new individuals per year (Nespolo 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. This translates into a (a maximum) reproductive output of 16
individuals per year, eight times the value for Dromiciops(assuming only one breeding period per year). Similarly, the poorly
known sympatric marsupial Rhyncholestes raphanurus(Caenolestidae) has been described to have continuous reproduction at
any moment of the year, with a maximum litter size of seven young
individuals (Iriarte, 2008). Reproduction in Dromiciops is
followed by a fattening period in which animals forage frenetically to
gain weight for hibernation, which starts in autumn. The peak of energy
expenditure occurs during lactation, which is the longest recorded in
marsupials and in Dromiciops extends from December to January. 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.