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.
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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.