Species-specific usage of sleeping sites in two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in northwestern Madagascar

We investigated the sleeping site ecology of two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in northwestern Madagascar during the second half of the dry season with respect to the type, quality, and usage pattern of the sleeping sites, as well as to social sleeping habits and response to potential threats. The type and quality of the sleeping sites differed between the two species. M. murinus used protected wooden shelters (tree holes) more frequently than M. ravelobensis, and M. ravelobensis used a broader variety of less protected sites (e.g., branches, lianas, and leaves) than M. murinus. Whereas male M. murinus usually slept alone, and female M. murinus mostly slept in groups, both sexes of M. ravelobensis slept in mixed-sex sleeping groups. M. murinus relied on crypsis in their sleeping sites, whereas M. ravelobensis regularly showed a flight response to the approach of an observer. This behavioral difference could indicate an adaptation to a higher predation risk in less protected sleeping sites. Whereas female M. murinus showed a high site fidelity, male M. murinus and both sexes of M. ravelobensis frequently changed their sleeping sites, which may also be interpreted as an antipredator strategy. The results are discussed with respect to three possible ecological explanations: interspecies competition, restricted resource availability, and niche differentiation. The latter is the most likely explanation for these interspecific differences.     

Radial maze performance in young and aged grey mouse lemurs (Microcebus murinus)

Young and aged grey mouse lemurs have been tested in an eight-arm radial maze out of which four arms were blind. An access to a nesting box was only feasible from the far end of the fourth arm, free to visit (= positive reinforcement). Both age groups memorized the position of the blind arms with an equal efficiency and learned very quickly to avoid them. However, repeated visits to the free arms already explored during the trial were noticed with the aged grey mouse lemurs, while the young group returned much less. These results corroborate the theory that age would preferably deteriorate working memory and less the reference memory.     

Submaximal leaping in the grey mouse lemur

In arboreal animals such as the grey mouse lemur (Microcebus murinus Miller, 1777), leaping is the most frequent strategy for predator avoidance. The aim of this study was to characterise the locomotor adaptation in response to the structural constraint of the habitat (i.e., position of the landing substrate). Thus, we characterised the push-off phase by inducing the lemurs to leap up to a range of heights from horizontal to their own individual highest performance. Using uniplanar high-frequency cineradiographs collected in a sagittal plane, the relative contributions of the centre of mass (CoM) velocity vector magnitude and orientation to leaping performance were evaluated. The kinematics of the push-off phase showed that for low landing heights, leaping performance was essentially due to hip and knee extensions. Higher leaps seemed to be related to an increase in ankle contribution. At all leaping heights, the proximal-to-distal sequence of the hind limb joints controlled the orientation and magnitude of the M. murinus CoM velocity vector while pushing off. Finally, the analysis of the velocity vector at the onset of take-off suggested that the optimal solution for predator avoidance was to leap for horizontal distance and not for vertical distance.     

Daily energy expenditure of the grey mouse lemur (Microcebus murinus): a small primate that uses torpor

We aimed to investigate the pattern of utilisation of torpor and its impact on energy budgets in free-living grey mouse lemurs (Microcebus murinus), a small nocturnal primate endemic to Madagascar. We measured daily energy expenditure (DEE) and water turnover using doubly labelled water, and we used temperature-sensitive radio collars to measure skin temperature (T _sk) and home range. Our results showed that male and female mouse lemurs in the wild enter torpor spontaneously over a wide range of ambient temperatures (T _a) during the dry season, but not during the rainy season. Mouse lemurs remained torpid between 1.7–8.9 h with a daily mean of 3.4 h, and their T _sk s fell to a minimum of 18.8 °C. Mean home ranges of mouse lemurs which remained normothermic were similar in the rainy and dry season. During the dry season, the mean home range of mouse lemurs showing daily torpor was significantly smaller than that of animals remaining normothermic. The DEE of M. murinus remaining normothermic in the rainy season (122 ± 65.4 kJ day⁻¹) was about the same of that of normothermic mouse lemurs in the dry season (115.5 ± 27.3 kJ day⁻¹). During the dry season, the mean DEE of M. murinus that utilised daily torpor was 103.4 ± 32.7 kJ day⁻¹ which is not significantly different from the mean DEE of animals remaining normothermic. We found that the DEE of mouse lemurs using daily torpor was significantly correlated with the mean temperature difference between T _sk and T _a (r ²=0.37) and with torpor bout length (r ² =0.46), while none of these factors explained significant amounts of variation in the DEE of the mouse lemurs remaining normothermic. The mean water flux rate of mouse lemurs using daily torpor (13.0 ± 4.1 ml day⁻¹) was significantly lower than that of mouse lemurs remaining normothermic (19.4 ± 3.8 ml day⁻¹), suggesting the lemurs conserve water by entering torpor. Thus, this first study on the energy budget of free-ranging M. murinus demonstrates that torpor may not only reflect its impact on the daily energy demands, but involve wider adaptive implications such as water requirements. Accepted: 29 August 2000     

Contest versus scramble competition for mates: The composition and spatial structure of a population of gray mouse lemurs (Microcebus murinus) in North-west Madagascar

The modes of intrasexual competition interacting in many dispersed societies of nocturnal solitary foragers are still poorly understood. In this study we investigate the spatial structure within a free-living population of gray mouse lemurs (Microcebus murinus) in order to test for the first time the predictions from two contrasting models of male intrasexual competition on the population level. The contest competition model predicts an uneven distribution of the sexes in a population nucleus with a female biased sex ratio in the center and a male biased sex ratio in the periphery. In contrast the scramble competition model predicts males and females being distributed evenly throughout their habitat with a constant sex ratio. Nine capture/recapture periods within three consecutive mating seasons revealed a continuous male biased sex ratio in the adult population with even trapping rates for the sexes. The male biased sex ratio could either be explained with postnatal female biased mortality or with a male biased natal sex ratio. This male biased sex ratio was apparent in all parts of the study site, indicating that the population was not subdivided into a female biased core and a male biased periphery. Furthermore, the majority of adult males have been captured at the same site as or in vicinity to females. Consequently, a large proportion of males had spatial access to females during the mating season. No signs of monopolization of females by certain dominant males could be detected. These data support the predictions from the scramble competition model and the concept of a promiscuous mating system for this species.     

First experimental evidence for female mate choice in a nocturnal primate

Female mate choice can be hypothesised in most nocturnal primates, since females show a higher investment in their offspring than males. The aim of this experimental study was to investigate if female grey mouse lemurs perform mate choice and whether age, relatedness (to the male), or male advertisement call activity systematically influence their decisions. A two-way mate choice design was developed in which females could choose between two males. Mate choice was deduced from the time spent in proximity to the males and from mating behaviour. During oestrus 12 of 17 females participated actively in the experiment and all of them showed either a significant spatial (n=11) or behavioural (n=1) preference for one male. In four cases copulations were observed. The influence of age on female mate choice was not statistically significant. In the cases with copulations, however, females mostly preferred the older male. This might indicate a preference for older age as an indicator of experience, fitness, and/or status. The influence of relatedness on female mate choice could not be definitely clarified. However, results imply a mechanism of kin recognition on the basis of familiarity. In the majority of choices, females preferred the male with higher trill call activity. Since trill call activity correlates with the relative dominance status of males, these results suggest an importance of the male dominance status for female mate choice in grey mouse lemurs. Altogether our findings indicate that females use a complex of different cues to choose their mates.     

The costs of risky male behaviour: sex differences in seasonal survival in a small sexually monomorphic primate

Male excess mortality is widespread among mammals and frequently interpreted as a cost of sexually selected traits that enhance male reproductive success. Sex differences in the propensity to engage in risky behaviours are often invoked to explain the sex gap in survival. Here, we aim to isolate and quantify the survival consequences of two potentially risky male behavioural strategies in a small sexually monomorphic primate, the grey mouse lemur Microcebus murinus: (i) most females hibernate during a large part of the austral winter, whereas most males remain active and (ii) during the brief annual mating season males roam widely in search of receptive females. Using a 10-year capture-mark-recapture dataset from a population of M. murinus in Kirindy Forest, western Madagascar, we statistically modelled sex-specific seasonal survival probabilities. Surprisingly, we did not find any evidence for direct survival benefits of hibernation-winter survival did not differ between males and females. By contrast, during the breeding season males survived less well than females (sex gap: 16%). Consistent with the 'risky male behaviour' hypothesis, the period for lowered male survival was restricted to the short mating season. Thus, sex differences in survival in a promiscuous mammal can be substantial even in the absence of sexual dimorphism.     

Compatibility counts: MHC-associated mate choice in a wild promiscuous primate

The mechanisms and temporal aspects of mate choice according to genetic constitution are still puzzling. Recent studies indicate that fitness is positively related to diversity in immune genes (MHC). Both sexes should therefore choose mates of high genetic quality and/or compatibility. However, studies addressing the role of MHC diversity in pre- and post-copulatory mate choice decisions in wild-living animals are few. We investigated the impact of MHC constitution and of neutral microsatellite variability on pre- and post-copulatory mate choice in both sexes in a wild population of a promiscuous primate, the grey mouse lemur (Microcebus murinus). There was no support for pre-copulatory male or female mate choice, but our data indicate post-copulatory mate choice that is associated with genetic constitution. Fathers had a higher number of MHC supertypes different from those of the mother than randomly assigned males. Fathers also had a higher amino acid distance to the females' MHC as well as a higher total number of MHC supertypes and a higher degree of microsatellite heterozygosity than randomly assigned males. Female cryptic choice may be the underlying mechanism that operates towards an optimization of the genetic constitution of offspring. This is the first study that provides support for the importance of the MHC constitution in post-copulatory mate choice in non-human primates.     

Wild mouse lemurs revisit artificial feeding platforms: implications for field experiments on sensory and cognitive abilities in small primates

Dealing effectively with space to find important resources in a natural environment is a fundamental ability necessary for survival. Evidence has already been provided that wild gray mouse lemurs revisit stationary feeding sites regularly. In this study, we explore to what extent two sympatric mouse lemur species, Microcebus murinus and M. ravelobensis, revisited artificial feeding sites during a period of food scarcity. As the tested populations are marked with individual transponders, we built up artificial feeding platforms equipped with a transponder reader at nine different locations where mouse lemurs had been previously caught. We baited them with a liquid reward and recorded the visitors' ID, the time and frequency of their visits, as well as all encounters that occurred on the platforms. Only mouse lemurs visited platforms and a total of sixteen individuals across both species were identified. Mouse lemurs visited a platform with a frequency of 2.02 (+/-0.95, range: 1-3.4) times in a night and they revisited it on several consecutive nights following their first visit (percentage of revisits 90.6%+/-11.7, range: 73.3-100%). First visits on a platform occurred on average 44 min (+/-35; range: 13-131) after sunset. We identified encounters between mouse lemurs on platforms: all of them were agonistic and within a species. Within a dyad, chasers were significantly heavier than chasees (N=7 dyads). Our design of platform experiments offers the advantage of observing wild individually known small primates in their natural environment and of setting up controlled experiments to gain insight into their sensory and cognitive abilities.     

Nest sites as limiting resources for cavity‐nesting birds in mature forest ecosystems: a review of the evidence

ABSTRACT Assumptions that populations of cavity‐nesting birds are limited by access to nest sites have largely been based on anecdotal reports or correlative data. Nest‐box‐addition experiments or tree‐cavity‐blocking experiments are potentially rigorous ways to investigate how densities of breeding birds are affected by access to nest cavities. Experimental evidence indicates that natural tree holes are limited in human‐altered landscapes, but the possibility that cavity nests are limited in old growth (unmanaged) forests is less clear. I reviewed 31 nest‐cavity‐removal or addition experiments conducted with 20 species of cavity‐nesting birds in mature forests. Of these 31 experiments conducted with a variety of different species of birds, only 19% reported statistically significant changes in breeding densities. However, none of these studies included data about the reproductive history of individuals colonizing the boxes (i.e., whether birds using the boxes would have otherwise been floaters or that birds excluded from blocked cavities on the plots did not simply move elsewhere), so they provided no strong evidence that the number of breeding pairs was limited by availability of nest sites at the population scale. Although some studies indicate that nest sites are limited at local (plot) scales in old growth forests, there is still little empirical evidence for nest‐site limitation at the population‐ and landscape‐level in mature, unmanaged forests. I review the challenges in designing and interpreting box‐addition experiments and highlight the main gaps in knowledge that should be targeted in the future.