Brown Mouse Lemurs (Microcebus rufus) May Lack Opportunities to Learn about Predator Calls.

Diurnal primates commonly modify their behaviour in response to predator vocalizations, but little is known about how nocturnal primates perceive predator calls. Mouse lemurs do not innately perceive predator calls as dangerous but may learn to do so in the wild. I hypothesized that wild brown mouse lemurs (Microcebus rufus) in Ranomafana National Park, Madagascar, differentiate between predator and non-predator vocalizations and exposed 29 adult subjects to calls of 3 sympatric predators (goshawk, fossa and owl), 3 sympatric non-predators and 4 controls. Brown mouse lemurs did not differentiate among stimuli, and there was no evidence that any recording was associated with danger, as neither activity nor spatial preferences changed in response to a stimulus, nor did subjects exhibit obvious behaviours indicative of danger such as flight or position on the branches. The failure to perceive predator calls as dangerous is common among small nocturnal solitary prey species and could be explained by a lack of learning opportunities. In social species acquired behaviours can spread quickly by social learning. Solitary species like mouse lemurs have to individually learn to associate predator calls with danger which is dependent on encounter rates. Unlike diurnal prey mouse lemurs lack the opportunity to observe diurnal raptors and associate their calls with the bird, and owls are proficient predators, which are difficult to observe in a rain forest where they hunt cryptically from perches. While sometimes nocturnal, the fossa is solitary and largely silent, and is also particularly rare at my study site. Cryptic, rare or non-vocal predators provide prey with few opportunities to associate their calls with danger. Mouse lemurs are subject to high predation rates by a wide range of predators and need to balance the costs and benefits of antipredation behaviours. Their cryptic lifestyle and preference for dense vegetation lowers the likelihood of being detected by predators, and they utilize visual and olfactory predator cues to make decisions about risk. Furthermore, their high reproductive output compensates for the high predation rates.

Hygienic personalities in wild grey mouse lemurs vary adaptively with sex.

Detecting the risk of infection and minimizing parasite exposure represent the first lines of host defence against parasites. Individuals differ in the expression of these behavioural defences, but causes of such variation have received little empirical attention. We therefore experimentally investigated the effects of several individual and environmental factors on the expression level of faecal avoidance in the context of feeding, drinking, sleeping and defecating in a wild primate population. We found a strong sex bias in the expression level of anti-parasite behaviours of grey mouse lemurs (Microcebus murinus), with only females strongly avoiding contaminated food, water and nests, and exhibiting selective defecation. Our results further suggest that individuals adapted their protective behaviours according to variation in intrinsic and ecological factors that may influence the cost-benefit balance of behavioural defences. Overall, individuals exhibited high consistency of investment in protective behaviours across behavioural contexts and time, suggesting that grey mouse lemurs exhibit different hygienic personalities. Finally, the global hygienic score was negatively correlated with faecal-orally transmitted parasite richness, suggesting that variation in behavioural defence has fitness consequences. We suggest that integrating inter-individual variation in behavioural defences in epidemiological studies should improve our ability to model disease spread within populations.

Linking cognition with fitness in a wild primate: fitness correlates of problem-solving performance and spatial learning ability.

Linking the cognitive performance of wild animals with fitness consequences is crucial for understanding evolutionary processes that shape individual variation in cognition. However, the few studies that have examined these links revealed differing relationships between various cognitive performance measures and fitness proxies. To contribute additional comparative data to this body of research, we linked individual performance during repeated problem-solving and spatial learning ability in a maze with body condition and survival in wild grey mouse lemurs (Microcebus murinus). All four variables exhibited substantial inter-individual variation. Solving efficiency in the problem-solving task, but not spatial learning performance, predicted the magnitude of change in body condition after the harsh dry season, indicating that the ability to quickly apply a newly discovered motor technique might also facilitate exploitation of new, natural food resources. Survival was not linked with performance in both tasks, however, suggesting that mouse lemurs' survival might not depend on the cognitive performances addressed here. Our study is the first linking cognition with fitness proxies in a wild primate species, and our discussion highlights the importance and challenges of accounting for a species' life history and ecology in choosing meaningful cognitive and fitness variables for a study in the wild.This article is part of the theme issue 'Causes and consequences of individual differences in cognitive abilities'.

Convenience polyandry or convenience polygyny? Costly sex under female control in a promiscuous primate.

Classic sex roles depict females as choosy, but polyandry is widespread. Empirical attempts to understand the evolution of polyandry have often focused on its adaptive value to females, whereas 'convenience polyandry' might simply decrease the costs of sexual harassment. We tested whether constraint-free female strategies favour promiscuity over mating selectivity through an original experimental design. We investigated variation in mating behaviour in response to a reversible alteration of sexual dimorphism in body mass in the grey mouse lemur, a small primate where female brief sexual receptivity allows quantifying polyandry. We manipulated body condition in captive females, predicting that convenience polyandry would increase when females are weaker than males, thus less likely to resist their solicitations. Our results rather support the alternative hypothesis of 'adaptive polyandry': females in better condition are more polyandrous. Furthermore, we reveal that multiple mating incurs significant energetic costs, which are strikingly symmetrical between the sexes. Our study shows that mouse lemur females exert tight control over mating and actively seek multiple mates. The benefits of remating are nevertheless not offset by its costs in low-condition females, suggesting that polyandry is a flexible strategy yielding moderate fitness benefits in this small mammal.

Experimental evidence for olfactory predator recognition in wild mouse lemurs.

Although primates have remarkable olfactory capabilities, their ability for olfactory predator recognition is still understudied. We investigated this cognitive ability in wild gray and golden-brown mouse lemurs (Microcebus murinus and M. ravelobensis) that were confronted with four different olfactory stimuli, derived from two Malagasy predators (fossa and barn owl) and two local nonpredator species (brown lemur and sifaka). The predator response was tested (1) in a systematic cage setup and (2) in a two-way choice experiment with two Sherman traps on platforms in the forest (stimulus trap vs. nonstimulus trap). For part 1, the study animals were housed in cages during habituation and 5 days of experiments. One stimulus was tested per night and was presented underneath a drinking bottle. The changes in the time spent close to the stimulus and the drinking time at the bottle were used as indicators of predator recognition. A timidity score was established by classifying the strength of the antipredator response during the experiment. The study animals spent significantly less time drinking and less time in the stimulus area when confronted with fossa odor compared with the other stimuli. The timidity score was significantly higher during the fossa stimulus compared with the nonpredator and the control stimuli. The two-way choice experiments revealed a complete avoidance of the fossa odor, which was not found with the other stimuli. Thus, wild mouse lemurs showed clear signs of olfactory predator recognition in the case of the fossa in both experiments, but no signs of avoidance to the other presented stimuli. The lack of owl avoidance may be explained by less or no aversive metabolites in the owl stimulus or by lower significance for olfactory recognition of aerial predators. Furthermore, the results showed slight differences between the two mouse lemur species that may be linked to differences in their ecology.

Do solitary foraging nocturnal mammals plan their routes?

Large-brained diurnal mammals with complex social systems are known to plan where and how to reach a resource, as shown by a systematic movement pattern analysis. We examined for the first time large-scale movement patterns of a solitary-ranging and small-brained mammal, the mouse lemur (Microcebus murinus), by using the change-point test and a heuristic random travel model to get insight into foraging strategies and potential route-planning abilities. Mouse lemurs are small nocturnal primates inhabiting the seasonal dry deciduous forest in Madagascar. During the lean season with limited food availability, these lemurs rely on few stationary food resources. We radio-tracked seven lemurs and analysed their foraging patterns. First change-points coincided with out-of-sight keystone food resources. Travel paths were more efficient in detecting these resources than a heuristic random travel model within limits of estimated detection distance. Findings suggest that even nocturnal, solitary-ranging mammals with small brains plan their route to an out-of-sight target. Thus, similar ecological pressures may lead to comparable spatial cognitive skills irrespective of the degree of sociality or relative brain size.

The three-panel runway maze adapted to Microcebus murinus reveals age-related differences in memory and perseverance performances.

Microcebus murinus, a mouse lemur primate appears to be a valuable model for cerebral aging study and for Alzheimer's disease model since they can develop beta-amyloid plaques with age. Although the biological and biochemical analyses of cerebral aging are well documented, the cognitive abilities of this primate have not been thoroughly characterized. In this study, we adapted a spatial working memory procedure described in rodents, the sequential choice task in the three-panel runway, to mouse lemurs. We analyzed the age-related differences in a procedural memory task in the absence or presence of visual cues. Sixty percent of young adult and 48% of aged lemurs completed the exploratory, choice habituation and testing phases at the beginning of the procedure. Young adult lemurs showed a higher level of perseverative errors compared with aged animals, particularly in the presence of visual stimuli. Over trials, old animals made more reference errors compared to young ones that improved quickly their performances under random level. No significant improvement was observed in young adults and old ones over sessions. This study showed that behavioural performances of M. murinus assessed on the sequential choice task in the three-panel runway markedly differ from the previously reported abilities of rodents. The behavioural response of young adult lemurs was influenced by novelty-related anxiety that contributed to their performance in terms of perseverative errors. Conversely, aged lemurs showed less perseverative errors, a rapid habituation to the three-panel runway maze, but made more memory errors. Overall, these findings demonstrate the feasibility to use the three-panel runway task in assessing memory performance, particularly in aged mouse lemurs.

Hibernation in Malagasy mouse lemurs as a strategy to counter environmental challenge.

The spiny forest of southwestern Madagascar is the driest and most unpredictable region of the island. It is characterized by a pronounced seasonality with high fluctuations in ambient temperature, low availability of food, and a lack of water during the cool dry season and, additionally, by changes in environmental conditions between years. One of the few mammalian species that manages to inhabit this challenging habitat is the reddish-gray mouse lemur (Microcebus griseorufus). The aim of our study was to determine whether this small primate uses continuous hibernation as an energy saving strategy, and if so, to characterize its physiological properties. We measured skin temperature of 16 free-ranging individuals continuously over 3 months during the cool dry season using collar temperature data loggers. Prolonged hibernation was found in three mouse lemurs and was not sex dependent (one male, two females). Skin temperature of hibernating individuals tracked ambient temperature passively with a minimum skin temperature of 6.5 degrees C and fluctuated strongly each day (up to 20 degrees C), depending on the insulation capacity of the hibernacula. Individuals remained in continuous hibernation even at an ambient temperature of 37 degrees C. The animals hibernated continuously during the dry season, and hibernation bouts were only interrupted by short spontaneous arousals. The study emphasizes that hibernation is an important measure to counter environmental challenge for more tropical species than previously thought, including primates. It furthermore provides evidence that tropical hibernation is functionally similar among tropical species.

Spatial memory in the grey mouse lemur (Microcebus murinus).

Wild animals face the challenge of locating feeding sites distributed across broad spatial and temporal scales. Spatial memory allows animals to find a goal, such as a productive feeding patch, even when there are no goal-specific sensory cues available. Because there is little experimental information on learning and memory capabilities in free-ranging primates, the aim of this study was to test whether grey mouse lemurs (Microcebus murinus), as short-term dietary specialists, rely on spatial memory in relocating productive feeding sites. In addition, we asked what kind of spatial representation might underlie their orientation in their natural environment. Using an experimental approach, we set eight radio-collared grey mouse lemurs a memory task by confronting them with two different spatial patterns of baited and non-baited artificial feeding stations under exclusion of sensory cues. Positional data were recorded by focal animal observations within a grid system of small foot trails. A change in the baiting pattern revealed that grey mouse lemurs primarily used spatial cues to relocate baited feeding stations and that they were able to rapidly learn a new spatial arrangement. Spatially concentrated, non-random movements revealed preliminary evidence for a route-based restriction in mouse lemur space; during a subsequent release experiment, however, we found high travel efficiency in directed movements. We therefore propose that mouse lemur spatial memory is based on some kind of mental representation that is more detailed than a route-based network map.

Olfactory predator recognition in predator-naïve gray mouse lemurs (Microcebus murinus).

Olfactory cues of predators, such as feces, are known to elicit antipredator responses in animals (e.g., avoidance, activity). To date, however, there is little information on olfactory predator recognition in primates. We tested whether the odor of feces of different predator categories (historical Malagasy predators and introduced predators) and of Malagasy nonpredators (control) induces antipredator behavior in captive born, predator-naïve gray mouse lemurs. In an olfactory predator experiment a mouse lemur was exposed to a particular odor, fixed at a preferred location, where the animal was trained to get a reward. The behavior of the mouse lemur toward the respective stimulus category was videotaped and quantified. Results showed that mouse lemurs avoided the place of odor presentation when the odor belonged to a predator. They reacted with a significantly enhanced activity when exposed to odors of carnivores compared to those of nonpredatory controls. These findings are in favor of a genetic predisposition of olfactory predator recognition that might be based on the perception of metabolites from meat digestion.

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.

Context-specific calls signal infants' needs in a strepsirrhine primate, the gray mouse lemur (Microcebus murinus).

The presence of context-specific communication sounds, structurally different call types related to particular situations and potentially expressing distinct emotions of the caller, were not systematically studied in infants of strepsirrhine primates. We exposed suckling's of gray mouse lemurs (Microcebus murinus) in an infant separation paradigm to three distinct contexts (isolation, threat-induced, grooming). An audio-videographic analysis of sound-correlated infant behaviors and a simultaneous multiparametric sound analysis revealed context-specific calls. Peak frequency predicted their acoustic classification best. Findings provided first evidence for a strepsirrhine primate that infant communication sounds may express distinct contexts and thereby infant's need reliably.

Social organization of the golden brown mouse lemur (Microcebus ravelobensis).

Our study provides the first data on the social organization of the golden brown mouse lemur, a nocturnal primate discovered in northwestern Madagascar in 1994. The study was carried out in two 6-month field periods during the dry season, covering time before and during the mating season. The spatial and temporal distributions of the sexes in the population were investigated by mark/recapture and radiotelemetry. Focal observations and the determination of sleeping associations provided further insights into the sociality of this solitary forager. High intra- and intersexual home-range overlaps occurred throughout the study. In general, individuals of both sexes had spatial access to more than one conspecific of the same and the opposite sex. We found no indication for spatial monopolization of females by certain males. These results suggest a dispersed multimale/multifemale system with a promiscuous mating pattern. Individuals showed temporal stability in their home range locations and interacted regularly with conspecifics. Five sleeping groups were identified during the study period: one female group and four mixed-sex groups. Even though sleeping sites were changed frequently, sleeping-group compositions remained stable over time. Thermoregulatory constraints are the most likely explanation for sleeping-group composition with members of both sexes in this species. Mixed-sex sleeping groups can be described as the basic social unit within this dispersed multimale/multifemale society.

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.

The hidden matrilineal structure of a solitary lemur: implications for primate social evolution.

Kin selection affects many aspects of social behaviour, especially in gregarious animals in which relatives are permanently associated. In most group-living primates with complex social behaviour, females are philopatric and organized into matrilines. Models of primate social evolution assume that females in solitary primates are also organized into matrilines. We examined the genetic structure and the mating system of a population of Coquerel's dwarf lemur (Mirza coquereli), a solitary primate from Madagascar, to test this assumption. Our genetic and behavioural analyses revealed that this population of solitary individuals is indeed structured into matrilines, even though this pattern was not predicted by behavioural data. Specifically, females sharing a mitochondrial DNA haplotype were significantly clustered in space and the average genetic and geographical distances among them were negatively correlated. Not all females were philopatric, but there is no evidence for the successful settlement of dispersing females. Although not all adult males dispersed from their natal range, they were not significantly clustered in space and all of them roamed widely in search of oestrous females. As a result, paternity was widely spread among males and mixed paternities existed, indicating that scramble competition polygyny is the mating system of this species. Our data therefore revealed facultative dispersal in both sexes with a strong bias towards female philopatry in this primitive primate. We further conclude that complex kinship structures also exist in non-gregarious species, where their consequences for social behaviour are not obvious.

Colony specificity in a social call of mouse lemurs (Microcebus ssp.).

Nocturnal primate species are often difficult to discriminate by gross visual bodily characteristics. This is also true for the world's smallest primate taxon, the Malagasy mouse lemurs. Recent findings imply that this taxon contains sibling species that can be diagnosed noninvasively by their species-specific advertisement call. We used comparative bioacoustics in order to explore variation of this call type and to assess species status of three European colonies. Acoustic variation was compared within and between colonies as well as with known species-specific differences. It was further related to morphological and genetic variations to investigate in how far it covaries with them. Results show that acoustic and genetic differences revealed by random amplified polymorphic DNA (RAPD) fingerprinting separated colonies reliably, but were on a different level than known species-specific differences. A Mantel test showed that acoustic differences were weakly correlated to genetic, but not to morphological differences. Our study is the first to reveal that both acoustic signaling and genetics clearly establish the species status for nocturnal primate populations. It also suggests that acoustic traits change at a more obvious and rapid pace than morphology in isolated populations, and may be used as an indication of conditions that may favor the evolution of subspecies.

Female dominance in captive gray mouse lemurs (Microcebus murinus).

Female dominance or female feeding priority seem to be characteristic for many lemur species, but are rare traits in other primates and mammals in general. The nocturnal lemur species, however, are underrepresented in the quantitative studies on social dominance. The aim of this study is to investigate the pattern of intersexual dominance relationships in the gray mouse lemur (Microcebus murinus), a species that is generally thought to possess a number of ancestral lemur traits. The context, distribution, and outcome of intersexual conflicts are analyzed in four captive groups of gray mouse lemurs. Intersexual conflicts occurred in the study groups in different behavioral contexts and were mostly spatial interactions (chasing/fleeing, approach/avoidance). The majority of conflicts were decided, and were in all but one case won by females. This is the first evidence suggesting unconditional female dominance in a cheirogaleid primate. The existence of female dominance in most families of the Lemuriformes suggests it is an ancient trait that evolved in their common ancestor.

Mating system of Microcebus murinus.

Microcebus murinus, a small nocturnal lemur from Madagascar, has retained features of ancient primates. Based on these ancestral traits, its social organization has often been used as a model for early primate social systems. In captivity it breeds polygynously, i.e., one male mates with several females, while females usually copulate only with the dominant male. The present project tested whether or not sexual size dimorphism, spatial distribution, and relative testis size of M. murinus correspond with predictions of the sexual selection theory concerning polygynous mating systems. The study was combined with a mark-recapture study and radio tracking of 12 animals in 1993 in a dry deciduous forest of western Madagascar at the end of the dry season. Large overlapping home ranges in males, lack of sexual size dimorphism, and relatively large testes suggest a multi-male mating system, i.e., one that is promiscuous rather than polygynous.

Age-related effects on reproductive function and sexual competition in the male prosimian primate, Microcebus murinus.

In the male lesser mouse lemur (Microcebus murinus), a polygamous long-day breeder of which the life span may reach 12-14 years, the effects of aging on socio-sexual relationships were studied on 44 captive animals of various ages. In this primate, new dominance relationships must be established at the beginning of each breeding season. During the breeding season induced by exposure to artificial long days, preoestrous females were introduced into cages of paired males to elicit sexual competition. Sexual behaviors, social interactions through chemical signals, and dominance relationships were recorded in paired males either of similar age (young or aged pairs), or of mixed ages. In all pairs, competition for priority access to females always occurred and dominance relationships were established unrelated to body weight. Although aged animals exhibited significantly less number of sexual and aggressive behaviors, they outranked younger males excepted when reaching oldest age. Independent of male's age, the typical pattern of seasonal rhythm of testosterone was observed, but aged males demonstrated a significant reduction in mean hormonal levels (25.5 +/- 2.8 ng/mL, n = 8) compared to young animals (50 +/- 2.7 ng/mL, n = 8). Moreover, their hormonal response to photoperiod was phase-shifted leading to reduced testosterone values when females entered oestrus. Despite the fact that testosterone levels and sexual behaviors decreased with aging in this primate, older males reached a dominant position, increasing thus their reproductive success.