Seasonal Adaptations Of Mouse Lemurs Reproduction

Most lemur species are well known for their seasonal reproduction (e.g., Jolly, 1984; Richard and Dewar, 1991; Sterling, 1994; Wright, 1999). Although this is also true for all mouse lemur species studied so far, some intra- and interspecific differences have been detected recently. The onset of female cycling activities has been shown to depend largely on photoperiodic changes but also partly on temperature and body condition (e.g., Perret and Aujard, 2001; Randrianambinina et al., 2003b). Free-living M. murinus females have been observed or suspected to produce one or two litters per year depending on their geographic origin (Figure 2: Martin, 1972, for Mandena; Schmelting et al., 2000, for Ampijoroa; Eberle and Kappeler, 2004a, for Kirindy). Litter size ranges from one to three with twins occurring most frequently. Interestingly, the lack of a second litter in Kirindy cannot easily be explained with the later onset of the rainy season or the smaller amount of rainfall per year in comparison to Ampijoroa, since there are indications for a second litter in M. berthae (co-occurring with M. murinus in Kirindy; Schwab, 2000) that should also be constrained by these factors. Future studies should focus more closely on the reasons for such intraspecific variation.

One mouse lemur species differs clearly from all others with respect to reproductive seasonality and this is M. ravelobensis (Figure 2). Females of this species start cycling as early as late August (before the photoperiodic change to long days)

Figure 2. Seasonal mating activities in mouse lemurs (for references see text).

and estrous females can be continuously trapped until November (Schmelting et al., 2000; Randrianambinina et al., 2003b), when capture success usually drops dramatically for this species, preventing further inspections of their reproductive state. Moreover, lactating M. ravelobensis females can be captured as late as in early April, suggesting at least partial mating activities until mid January (Schmelting et al., 2000; Radespiel, personal observation). These findings indicate prolonged mating activities and no strict estrous synchrony, which contrasts with the reproductive pattern observed so far in all other species. The physiological and photoperiodic basis for the regulation of the early start and extension of mating activities in M. ravelobensis is not yet clear and deserves further attention.

Torpor and Body Mass Variations

Mouse lemurs are well known for seasonal physiological changes that are, for example, expressed in seasonal variations in body mass, general activity, and the ability to enter torpor. Daily torpor has been observed during the cooler months of the year in all mouse lemur species studied so far (e.g., Schmid, 2001, for M. murinus; Randrianambinina et al., 2003b for M. rufus; Radespiel et al., 2003a, for M. ravelobensis; Schmid et al., 2000, for M. berthae). Seasonal torpor, i.e., a prolonged state of reduced body temperature with inactive periods of several days to months, is known only from one population of M. murinus (Kirindy, Schmid and Kappeler, 1998) and from the M. rufus group (Ranomafana: Atsalis, 1999b; Mantadia: Randrianambinina et al., 2003b). The differences between these and the other study sites have been explained as consequences of the respective temperature regimes. Kirindy forest and the eastern mountain rainforests suffer from very low nightly minimum temperatures during the dry season that may impose severe thermoregulatory stress on its inhabitants. Prolonged torpor allows them to save substantial amounts of energy during these harsh months (Schmid, 1999; Schmid and Stephenson, 2003) but on the other hand imposes costs (i.e., loss of body mass) on an individual. It has therefore been argued that only individuals in relatively good body condition (i.e., high body mass of > 50 g) may afford to enter seasonal torpor (Schmid and Kappeler, 1998; Atsalis, 1999b; Randrianambinina et al., 2003b). These seem to be more often females than males with the consequence that populations with seasonal torpor have a seasonally varying sex ratio with a strong excess of males during the cold period of the year (Schmid and Kappeler, 1998; Atsalis, 1999b; Randrianambinina et al., 2003b).

Seasonal variations of body mass have been observed in all mouse lemur species studied (M. murinus: Schmid and Kappeler, 1998; Schmelting, 2000; Lutermann, 2001; M. rufus group: Atsalis, 1999b; Randrianambinina et al., 2003b) independent of their use of seasonal torpor. These variations can be summarized as follows: Animals usually accumulate fat reserves during the (late) rainy season and lose weight during the subsequent dry season. Seasonally torpid individuals lose proportionally more weight than those that stay active and may feed on a daily basis throughout the year. Males seem to increase body mass prior to the onset of the mating season but lose it soon afterwards, possibly as a result of their mate searching strategies which usually involve high locomotor activities.

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