Different Population Dynamics of Microcebus murinus in Primary and Secondary Deciduous Dry Forests of Madagascar

The goal of this study was to identify causes for lower population densities of mouse lemurs (Microcebus murinus) in secondary than in primary dry deciduous forests of western Madagascar. Variations in the abundance of Microcebus murinus are linked to the capacity to enter energy-saving torpor during the dry season. Under natural conditions in primary forest, Microcebus murinus can maintain daily torpor (and possibly hibernation) as long as body temperatures remain below 28°C. Females are more likely to hibernate than males, resulting in skewed sex ratios of captured Microcebus murinus in the primary forest. In the secondary forest the sex ratio of subjects captured during the dry season is more balanced than in primary forest, indicating that fewer females go into torpor in secondary than in primary forest. Secondary forests have fewer large standing or fallen trees that might provide holes as shelter for Microcebus murinus. Ambient temperatures are higher in secondary than in primary forests and higher outside than inside tree holes. These high ambient temperatures might hinder the ability of Microcebus murinus to maintain torpor for prolonged periods in secondary forests. Mouse lemurs from secondary forest have lower body mass than in primary forest. The year-to-year recapture rate is zero in secondary forest and thus significantly lower than in primary forest. This indicates that survival rates are lower in secondary than in primary forests. Thus, secondary forests may be of limited value as buffer zones or even corridors for mouse lemurs.     

Molecular phylogeny of the lemur family cheirogaleidae (primates) based on mitochondrial DNA sequences

Cheirogaleidae currently comprises five genera whose relationships remain contentious. The taxonomic status and phylogenetic position of both Mirza coquereli and Allocebus trichotis are still unclear. The taxonomic status of the recently discovered Microcebus ravelobensis (a sympatric sibling species of Microcebus murinus) and its phylogenetic position also require further examination. A approximately 2.4-kb mitochondrial DNA sequence including part of the COIII gene, complete ND3, ND4L, and ND4 genes, and 5 tRNAs was used to clarify relationships among cheirogaleids. Mirza and Microcebus form a clade representing the sister group of Allocebus, with a clade containing Cheirogaleus major and Cheirogaleus medius diverging first. M. ravelobensis and Microcebus rufus form a subclade within Microcebus, with M. murinus as its sister group. The molecular data support the generic status of Mirza coquereli and species-level divergence of M. ravelobensis. Furthermore, "M. rufus" may well represent more than one species.     

Different competitive potential in two coexisting mouse lemur species in northwestern Madagascar

Interspecific competition has been suggested to influence the biogeographic distribution patterns of species. A high competitive potential could entail species-specific advantages during resource acquisition that could translate into a higher potential for range expansion. We investigated whether differences in the competitive potential of the morphologically similar and partially sympatric gray mouse lemur (Microcebus murinus) and golden-brown mouse lemur (Microcebus ravelobensis) may help to explain differences in their geographic range sizes. We carried out encounter experiments with 14 pairs of captured female mouse lemurs of both species. The experimental dyads were tested in a two-cage arrangement, with individuals being separated from each other outside the experiments. Two days of habituation and four subsequent days of 1-h encounter experiments were conducted, before releasing the animals again in the wild. In general, the M. murinus individuals won significantly more conflicts than their partners. In eight of 14 tested pairs, there was a significant species bias in winning conflicts, and in 87.5% of these dyads, M. murinus was the "dyad winner". A high competitive potential did not depend on body mass. Furthermore, "dyad winners" spent more time feeding (P < 0.05) and were less spatially restricted than "dyad losers". To conclude, our results suggest that the widely distributed M. murinus may indeed have a higher competitive potential than the regional endemic M. ravelobensis, which may, among other possible factors, have enabled this species to expand geographically, despite the presence of other competing congeners.     

Prosimian hemoglobins--V. The primary structures of the alpha-I, alpha-II and beta-hemoglobin chains of Hapalemur griseus, with a note on the classification of Microcebus

1. The duplicated adult hemoglobins were isolated from a mature Hapalemur griseus and the constituent chains prepared. Sequence analysis of the isolated alpha-globins showed that the alpha-I and alpha-II chains differed by a glycine for lysine substitution at position 15. 2. The complete amino acid sequence of the single adult beta-globin of Hapalemur griseus was determined. The beta-globin sequence of Hapalemur griseus clusters with those of other authentic lemurs, and is clearly separated from the sequences characteristic of lorisiform primates. 3. Partial sequence analysis of the beta-globin of Microcebus murinus showed only a single amino acid difference when compared to the Hapalemur globin. 4. Partial sequence analysis of the alpha-globin of Microcebus murinus showed only three amino acid residues that are not found in other lemuriform alpha-globins; two of these are unique to Microcebus among all known prosimian alpha-globin sequences. 5. The Microcebus alpha- and beta-globins are more similar to the homologous lemuriform sequences than they are to lorisiform sequences.     

Microcebus murinus: a useful primate model for human cerebral aging and Alzheimer's disease?

Age-associated dementia, in particular Alzheimer's disease (AD), will be a major concern of the 21st century. Research into normal brain aging and AD will therefore become increasingly important. As for other areas of medicine, the availability of good animal models will be a limiting factor for progress. Given the complexity of the human brain, the identification of appropriate primate models will be essential to further knowledge of the disease. In this review, we describe the features of brain aging and age-associated neurodegeneration in a small lemurian primate, the Microcebus murinus, also referred to as the mouse lemur. The mouse lemur has a relatively short life expectancy, and animals over 5 years of age are considered to be elderly. Among elderly mouse lemurs, the majority show normal brain aging, whereas approximately 20% develop neurodegeneration. This Microcebus age-associated neurodegeneration is characterized by a massive brain atrophy, abundant amyloid plaques, a cytoskeletal Tau pathology and a loss of cholinergic neurons. While elderly mouse lemurs with normal brain aging maintain memory function and social interaction, animals with age-associated neurodegeneration lose their cognitive and social capacities and demonstrate certain similarities with age-associated human AD. We conclude that M. murinus is an interesting primate model for the study of normal brain aging and the biochemical dysfunctions occurring in age-associated neurodegeneration. Mouse lemurs might also become an increasingly important model for the development of novel treatments in this domain.     

Behavioral study in the gray mouse lemur (Microcebus murinus) using compounds considered sweet by humans

This study presents the results from two-bottle preference (TBP) tests performed on the gray mouse lemur (Microcebus murinus), a small Malagasy primate. We found that of 18 compounds considered sweet by humans, M. murinus preferred only six: D-tryptophan, dulcin, fructose, sucrose, SC45647, and xylitol. The animals neither preferred nor rejected acesulfame-K, alitame, aspartame, N-4-cyanophenyl-N'-cyanoguanidineacetate (CCGA), cyanosuosan, cyclamate, monellin, saccharin, suosan, super-aspartame, N-trifluoroacetyl-L-glutamyl-4-aminophenylcarbonitrile (TGC), and thaumatin. Together with previously recorded taste-nerve responses in M. murinus to acesulfame-K, alitame, aspartame, cyclamate, monellin, saccharin, and suosan [Hellekant et al., Chem Senses 18:307-320, 1993b], the current results suggest that these compounds either do not taste sweet to M. murinus or they have an aversive taste component. In this work we also relate these findings to phylogeny.     

Switching from negative to positive density-dependence among populations of a cobble beach plant

Understanding the co-occurrence of ecologically similar species remains a puzzling issue in community ecology. The species-rich mouse lemurs (Microcebus spec.) are distributed over nearly all remaining forest areas of Madagascar with a high variability in species distribution patterns. Locally, many congeneric species pairs seem to co-occur, but only little detailed information on spatial patterns is available. Here, we present the results of an intensive capture-mark-recapture study of sympatric Microcebus berthae and M. murinus populations that revealed small-scale mutual spatial exclusion. Nearest neighbour analysis indicated a spatial aggregation in Microcebus murinus but not in M. berthae. Although the diet of both species differed in proportions of food categories, they used the same food sources and had high feeding niche overlap. Also, forest structure related to the spatial distribution of main food sources did not explain spatial segregation because parts used by each species exclusively did not differ in density of trees, dead wood and lianas. We propose that life history trade-offs that result in species aggregation and a relative increase in the strength of intra-specific over inter-specific competition best explain the observed pattern of co-occurrence of ecologically similar congeneric Microcebus species.     

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.     

Developmental morphology of the solum nasi in the mouse lemur (Microcebus murinus)

The solum nasi of Microcebus murinus is characterized by the presence of a zona annularis, continuity between the anterior transverse lamina and the paraseptal cartilage, a continuous paraseptal cartilage, a palatine cartilage and a posterior transverse lamina. It lacks a fibula reuniens and possibly a cartilage of the nasopalatine duct as well as a palatine papillary cartilage. The morphology in M. murinus closely resembles that seen in Tupaia and Galago. This affinity results from the retention of primitive traits. However, Galago is reported to lack a zona annularis, thus displaying a specialization not shared with M. murinus. Therefore, the zona annularis provides a useful trait for distinguishing between the ontogenies of M. murinus and Galago.     

Cytogenetic study of the endemic Malagasy lemurs subfamily Cheirogaleinae Gregory 1915

Karyotypes were determined on 27 lemurs from six species of what has been called the “subfamily” of Cheirogaleinae : Microcebus murinus murinus (2), M. murinus rufus (2), M. coquereli (5), Phaner furcifer (6), Cheirogaleus medius (9), and C. major (3). The cytogenetic study of these animals reveals that this “subfamily” contains in fact two groups, (a) — Microcebus and Cheirogaleus, and (b) — Phaner. The karyotype of the first two genera has a fundamental number (FN) equal to 66 and the karyotype of the third genus has an FN equal to 62. This result and the fact that Phaner has a particular scent-marking gland, knuckle pads, and finger prints markedly different from those of other genera agree with the view that this animal belongs to a special subfamily, Phanerinae, while the two other genera constitute the subfamily of Cheirogaleinae. These two subfamilies constitute the family of Cheirogaleidae.     

Brown fat and nonshivering thermogenesis in the gray mouse lemur (Microcebus murinus)

The gray mouse lemur Microcebus murinus is a rare example of a primate exhibiting daily torpor. In captive animals, we examined the metabolic rate during arousal from torpor and showed that this process involved nonshivering thermogenesis (NST). Under thermoneutrality (28 degrees C), warming-up from daily torpor (body temperature <33 degrees C) involved a rapid (<5 min) increase of O(2) consumption that was proportional to the depth of torpor (n = 8). The injection of a beta-adrenergic agonist (isoproterenol) known to elicit NST induced a dose-dependent increase in metabolic rate (n = 8). Moreover, maximum thermogenesis was increased by cold exposure. For the first time in this species, anatomic and histological examination using an antibody against uncoupling protein (UCP) specifically demonstrated the presence of brown fat. With the use of Western blotting with the same antibody, we showed a likely increase in UCP expression after cold exposure, suggesting that NST is also used to survive low ambient temperatures in this tropical species.     

Relationship Between Microhabitat Structure and Distribution of Mouse Lemurs (Microcebus spp.) in Northwestern Madagascar

Understanding processes affecting the distribution and abundance of organisms is a central issue in ecology and conservation biology. In northwestern Madagascar, we found an uneven distribution pattern of the golden-brown mouse lemur (Microcebus ravelobensis) and the grey mouse lemur (M. murinus). In one area (JBA) the two species lived sympatrically, whereas in another forest area (JBB) Microcebus ravelobensis occurred exclusively. To investigate whether differences in forest structure may explain this uneven distribution, we conducted a microhabitat analysis and related it to specific distribution. In JBA the habitat of Microcebus ravelobensis was characterized by a higher percentage of trees with many lianas and a higher cover of the herb layer, whereas that of M. murinus had a higher number of trees with a diameter at breast height (DBH) >10 cm. The comparison of the forest structure of the microhabitats of the two species between JBA and JBB revealed further differences. The cover of the overstory, the percentage of trees without lianas and the number of larger trees (DBH >10 cm) among the microhabitats were higher for Microcebus murinus in JBA than for M. ravelobensis in JBB whereas the microhabitats of M. ravelobensis at the two sites did not differ concerning these vegetation structures. Differences between the two species coincide with those of resources important for survival. Our results indicate the importance of microhabitat analyses for the understanding of distribution patterns of species and for successful conservation planning.     

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 development of small primate models for aging research

Nonhuman primate (NHP) aging research has traditionally relied mainly on the rhesus macaque. But the long lifespan, low reproductive rate, and relatively large body size of macaques and related Old World monkeys make them less than ideal models for aging research. Manifold advantages would attend the use of smaller, more rapidly developing, shorter-lived NHP species in aging studies, not the least of which are lower cost and the ability to do shorter research projects. Arbitrarily defining "small" primates as those weighing less than 500 g, we assess small, relatively short-lived species among the prosimians and callitrichids for suitability as models for human aging research. Using the criteria of availability, knowledge about (and ease of) maintenance, the possibility of genetic manipulation (a hallmark of 21st century biology), and similarities to humans in the physiology of age-related changes, we suggest three species--two prosimians (Microcebus murinus and Galago senegalensis) and one New World monkey (Callithrix jacchus)--that deserve scrutiny for development as major NHP models for aging studies. We discuss one other New World monkey group, Cebus spp., that might also be an effective NHP model of aging as these species are longer-lived for their body size than any primate except humans.     

Habitat separation of sympatric Microcebus spp. in the dry spiny forest of south-eastern Madagascar

We investigated whether or not habitat structure contributes to the separation of two sister species of lemurs and their hybrids. For this, we studied Microcebus murinus and M. griseorufus along a continuous vegetation gradient where populations of the two species occur in sympatry or in allopatry. In allopatry, the two species are generalists without any sign of microhabitat selectivity. In sympatry, both species differed significantly and discriminated against certain habitat structures: M. murinus was found in microhabitats with larger trees than average while M. griseorufus utilized microhabitats with smaller trees. Hybrids between the two species did not show any significant discrimination for or against microhabitat structure and did not differ in their habitat utilization from either parent species. Both species can go into torpor and hibernation. M. griseorufus is seen more frequently during the cool dry season than M. murinus. We assume that M. murinus goes into extended torpor or hibernation more frequently than M. griseorufus. We interpret the different occurrence of large-sized trees in microhabitats of M. murinus as a prerequisite for M. murinus to be able to spend extended periods of time in tree holes that are isolated and allow hibernation at reduced temperature levels.     

Soluble aggregates of the amyloid-beta protein selectively stimulate permeability in human brain microvascular endothelial monolayers

Cerebral amyloid angiopathy associated with Alzheimer's disease is characterized by cerebrovascular deposition of the amyloid-beta protein (Abeta). Abeta elicits a number of morphological and biochemical alterations in the cerebral microvasculature, which culminate in hemorrhagic stroke. Among these changes, compromise of the blood-brain barrier has been described in Alzheimer's disease brain, transgenic animal models of Alzheimer's disease, and cell culture experiments. In the current study, presented data illustrates that isolated soluble Abeta(1-40) aggregates, but not unaggregated monomer or mature fibril, enhance permeability in human brain microvascular endothelial monolayers. Abeta(1-40)-induced changes in permeability are paralleled by both a decrease in transendothelial electrical resistance and a re-localization of the tight junction-associated protein zonula occludin-1 away from cell borders and into the cytoplasm. Small soluble Abeta(1-40) aggregates are confirmed to be the most potent stimulators of endothelial monolayer permeability by establishing an inverse relationship between average aggregate size and stimulated changes in diffusional permeability coefficients. These results support previous findings demonstrating that small soluble Abeta(1-40) aggregates are also primarily responsible for endothelial activation, suggesting that these same species may elicit other changes in the cerebrovasculature associated with cerebral amyloid angiopathy and Alzheimer's disease.     

Food prehension and manipulation in Microcebus murinus (Prosimii, Cheirogaleidae)

Among primates, apes and monkeys are known to use their hands and to exhibit independent control of their fingers. In comparison, Prosimii are thought to have less digital individualization and to use their mouth more commonly for prehension. Unfortunately, prehension and manipulation studies in Prosimii have been conducted in conditions constraining the subject to grasp with the hand. Moreover, the effect of food size remains unexplored, even though it could affect the use of the hands versus the mouth. Thus, whether prosimians use the hand or the mouth to grasp and manipulate food items of different sizes in unconstrained conditions remains unclear. To address this question, we characterized the eating and manipulation patterns of Microcebus murinus in unconstrained conditions, using three food sizes. The results showed that M. murinus showed (i) an eating pattern similar to that of rodents, with smaller food items being grasped with the mouth, (ii) a greater tendency to use the hands for prehension of larger foods, and (iii) plasticity during food manipulation similar to that which has been observed in rodents. These results are discussed in the framework of grasping in mammals and are used to discuss the origins of prehension in primates.     

Tree Holes Used for Resting by Gray Mouse Lemurs (Microcebus murinus) in Madagascar: Insulation Capacities and Energetic Consequences

I studied the insulation capacity of tree holes used by gray mouse lemurs (Microcebus murinus) in a primary dry deciduous forest in western Madagascar during the cool dry season. Tree holes had an insulating effect, and fluctuations of air temperatures were less extreme inside the holes than outside them. The insulation capacity of the tree holes peaked between 0800 and 1100 hr, when ambient temperatures ranged between 25 and 30°C. To compare tree holes, I calculated the mean difference between the internal temperature )(T_i ) and the external temperature (T_e ) for each tree hole. Thus large differences indicate good insulation capacities. The mean difference of tree holes in living trees was significantly larger than that of tree holes in dead trees, which shows that insulation in living trees is more effective. During the dry season, the insulation capacity of tree holes in living trees decreased and was lowest in July, whereas the insulation capacity of holes in dead trees remained approximately constant. Physiological studies under natural temperature and light condition in Microcebus murinus reveal that daily torpor saves around 40% of the daily energy expenditure compared to normothermia. However, torpor can be maintained only up to the threshold body and ambient temperature of 28°C, whereat Microcebus murinus have to terminate torpor actively. By occupying insulating tree holes, mouse lemurs may stay longer in torpor, which increases their daily energy savings by an extra 5%.     

A preliminary study of spatial distribution and mating system of pygmy mouse lemurs (Microcebus cf. myoxinus)

According to current hypotheses on the evolution of life history traits and social systems of Malagasy lemurs, nocturnality is associated with a solitary lifestyle and a polygynous or promiscuous mating system. Recent studies, however, have indicated that this may not be true of all lemurs. The goal of this study was to investigate the sociality and the mating system of pygmy mouse lemurs (Microcebus cf myoxinus), which are the smallest known primates, and which retain characteristics of the most primitive primates. I compared my findings with data on the sympatric Microcebus murinus and Cheirogaleus medius. Observational, morphometric and spatial distribution data were obtained by a radiotracking study in 1994, and from a capture-recapture study conducted during 1995/96. Pygmy mouse lemurs usually slept alone in a tangle of vegetation. During the mating season, sleeping sites of males were distributed over a much broader area than were female sites, indicating that male home ranges are larger than those of females. The home ranges of males overlapped during the mating season, and males occasionally roamed over long distances during a single night. Pygmy mouse lemurs forage primarily alone. Analysis of estrus stages indicate that female cycles are unsynchronized during the mating season. There was a lack of sexual dimorphism in body size but not in body mass. Males were heavier than females during the reproductive season but lighter than females the rest of the year. Testes of males varied in size seasonally and enlarged significantly during the mating season. The presence of a vaginal sperm plug in a female indicated the importance of preventing additional matings in this species. Thus pygmy mouse lemurs follow the predictions derived from sexual selection theory for multi-male mating systems with promiscuous matings and male sperm competition.     

Cytogenetics of two Lorisidae (Nycticebus coucang and Perodicticus potto). Comparison with the lemurs and the simians (author's transl)]

The karyotypes of two Lorisidae (Prosimians) Nycticebus coucang and Perodicticus potto have been studied, using many banding techniques. These karyotypes are compared with each other and also with those of Microcebus murinus (Lemur) and of Cebus capucinus (Simian, platyrrhine). The karyotype of M. murinus appears ancestral to the other. That of the Lorisidae cannot be an intermediatry stage between the karyotypes of the lemurs and of the simians. An important part (12 p. cent) of the genome of N. coucang is comprised of heterochromatin ; it and the juxta centromeric heterochromatin stain negatively with C-banding techniques. C-banding therefore is insufficient to delineate constitutive heterochromatin, late replication being the only universal criterion.