Mouse Lemur Microcebus Murinus Research Articles

Sex-specific patterns of age-related cerebral atrophy in a nonhuman primate Microcebus murinus

Steadily aging populations result in a growing need for research regarding age-related brain alterations and neurodegenerative pathologies. By allowing a good translation of results to humans, nonhuman primates, such as the gray mouse lemur Microcebus murinus, have gained attention in this field. Our aim was to examine correlations between atrophy-induced brain alterations and age, with special focus on sex differences in mouse lemurs. For cerebral volumetric measurements, in vivo magnetic resonance imaging was performed on 59 animals (28♀♀/31♂♂) aged between 1.0 to 11.9 years. Volumes of different brain regions, cortical thicknesses, and ventricular expansions were evaluated. Analyses revealed significant brain atrophies with increasing age, particularly around the caudate nucleus, the thalamus, and frontal, parietal, and temporo-occipital regions. Especially old females showed a strong decline in cingulate cortex thickness and had higher values of ventricular expansion, whereas cortical thickness of the splenium and occipital regions decreased mainly in males. Our study, thus, provides first evidence for sex-specific, age-related brain alterations in a nonhuman primate, suggesting that mouse lemurs can help elucidating the mechanism underlying sex disparities in cerebral aging, for which there is mixed evidence in humans.

A new species of Schoutedenichia Jadin & Vercammen-Grandjean, 1954 from Madagascar and a re-description of S. dutoiti (Radford, 1948) from South Africa (Acariformes: Trombiculidae).

A new chigger mite species, Schoutedenichia microcebi n. sp. is described from the grey mouse lemur Microcebus murinus (J.F. Miller) from Madagascar. The new species is closely related to S. dutoiti (Radford, 1948), a species described from a single specimen collected on a rodent in South Africa. Examination of the holotype and new material on S. dutoiti from South Africa enabled us to re-describe this species and provide new data on its hosts and geographical distribution.

Does Calorie Restriction in Primates Increase Lifespan? Revisiting Studies on Macaques (Macaca mulatta) and Mouse Lemurs (Microcebus murinus)

The effects of calorie restriction have now been studied in two non-human primates, the macaque Macaca mulatta and the mouse lemur Microcebus murinus. The study on lemurs and one of the two studies on macaques have reported a lifespan increase. In this review, I argue that these results are better explained by a lifespan decrease in the control group because of a bad diet and/or overfeeding, rather than by a real lifespan increase in calorie-restricted animals. If these results can be readily translated to humans, it would mean that no beneficial effect of calorie restriction on lifespan can be expected in normal-weight or lean people, but that overweight and/or obese people could benefit to some extent from a decrease in excessive food intake.

Treadmill locomotion of the mouse lemur (Microcebus murinus); kinematic parameters during symmetrical and asymmetrical gaits.

The gaits of the adult grey mouse lemur Microcebus murinus were studied during treadmill locomotion over a large range of velocities. The locomotion sequences were analysed to determine the gait and the various spatiotemporal gait parameters of the limbs. We found that velocity adjustments are accounted for differently by stride frequency and stride length depending on whether the animal showed a symmetrical or an asymmetrical gait. When using symmetrical gaits the increase in velocity is associated with a constant contribution of the stride length and stride frequency; the increase of the stride frequency being always lower. When using asymmetrical gaits, the increase in velocity is mainly assured by an increase in the stride length which tends to decrease with increasing velocity. A reduction in both stance time and swing time contributed to the increase in stride frequency for both gaits, though with a major contribution from the decrease in stance time. The pattern of locomotion obtained in a normal young adult mouse lemurs can be used as a template for studying locomotor control deficits during aging or in different environments such as arboreal ones which likely modify the kinematics of locomotion.

Determinants of pull strength in captive grey mouse lemurs

AbstractGrasping is important for arboreal species as it allows them to hold on to branches. Although grasping has been studied previously in the context of primate origins and as an indicator of age‐induced loss in overall performance, little is known about the proximate determinants of variation in strength. We measured hand pull strength in 62 adult captive individuals of grey mouse lemurs Microcebus murinus of known age. In addition, we measured the body mass and the length of the forearm in each individual. Our results showed that animals with a longer ulna, and animals that weighed more, and had a greater relative body mass had higher pull strength. However, despite the fact that females are bigger than males, differences in pull strength were not significantly different between the two sexes. Although comparative data for other species of vertebrates are scarce, our data suggest that mouse lemurs have relatively high pull strength for their size that may be interpreted as an adaptation to arboreal locomotion.

Complete mitochondrial genome of the gray mouse lemur, Microcebus murinus (Primates, Cheirogaleidae)

We report the high-coverage complete mitochondrial genome sequence of the gray mouse lemur Microcebus murinus. The sequencing has been performed on an Illumina Hiseq 2500 platform, with a genome skimming strategy. The total length of this mitogenome is 16 963 bp, containing 13 protein-coding genes, 22 transfer RNA genes, 2 ribosomal RNA genes and 1 non-coding region (D-loop region). The genome organization, nucleotide composition and codon usage are similar to those reported from other primate’s mitochondrial genomes. The complete mitochondrial genome sequence reported here will be useful for comparative genomics studies in primates.

Striking longevity in a hibernating lemur

AbstractBody mass correlates with life span across mammals; larger species tend to live longer than small ones. There are, however, exceptions to this pattern. One metabolic strategy that has been linked to increased longevity is hibernation; that is, small‐bodied hibernating mammals live longer than expected based on their size alone. Hibernation may be beneficial in seasonal and unpredictable habitats because individuals can reduce metabolic rates to conserve energy in times of resource scarcity. On the downside, the extended periods of dormancy hibernating mammals undergo afford them fewer reproductive opportunities per year compared with their similarly sized non‐hibernating relatives. One strategy to compensate for a reduced reproductive rate is to extend reproductive life span. Increased longevity may also be expected if hibernators possess cellular machinery resilient to metabolic stress, which is generally associated with aging. Here we present data on life span and other life‐history variables for four small‐bodied strepsirrhine primates: (1) the fat‐tailed dwarf lemur Cheirogaleus medius, a hibernator; (2) the gray mouse lemur Microcebus murinus, a closely related species, which opportunistically expresses torpor and/or hibernation; (3) the Northern giant mouse lemur Mirza zaza another closely related species, which does not hibernate, but may employ daily torpor; (4) the bushbaby Galago moholi, a non‐lemur, non‐hibernating strepsirrhine that employs torpor only as an emergency response to harsh conditions. We analyzed newly compiled captive data from the developing Duke Lemur Center Database, and report that dwarf lemurs live significantly longer, reproduce longer and show later incidences of both morphologic and reproductive senescence than the other species analyzed. That these correlations hold in captive populations with no predation indicates that intrinsic biologic effects must play some role.

Sexual dimorphism in bite force in the grey mouse lemur

AbstractSexual dimorphism is thought to be the result of sexual selection, food competition and/or niche differentiation, or simply the result of differential growth between the sexes. Despite the fact that sexual dimorphism is common among primates, lemurs are thought to be largely monomorphic. Yet, females of the species Microcebus are known to be larger than males. Here, we investigate if dimorphism in head dimensions is present in a colony of captive grey mouse lemurs Microcebus murinus. Moreover, we test whether any observed shape dimorphism is associated with differences in bite force between the sexes. Our results show that male and female grey mouse lemurs are indeed sexually dimorphic in head dimensions, with females having taller and wider heads than males. Moreover, we confirm previous observations that females are heavier than males. Bite force was principally determined by head dimensions and age in our dataset, and differed between sexes, with females biting harder than males. These data suggest a potential role for niche dimorphism in driving the observed shape and performance dimorphism as female reproductive output may depend upon the ability of animals to obtain resources that are difficult to ingest.

Does Alzheimer disease exist in all primates? Alzheimer pathology in non-human primates and its pathophysiological implications (II)

IntroductionIn the ageing process there are some species of non-human primates which can show some of the defining characteristics of the Alzheimer's disease (AD) of man, both in neuropathological changes and cognitive-behavioural symptoms. The study of these species is of prime importance to understand AD and develop therapies to combat this neurodegenerative disease. DevelopmentIn this second part of the study, these AD features are discussed in the most important non-experimental AD models (Mouse Lemur—Microcebus murinus, Caribbean vervet—Chlorocebus aethiops, and the Rhesus and stump-tailed macaque—Macaca mulatta and M. arctoides) and experimental models (lesional, neurotoxic, pharmacological, immunological, etc.) non-human primates. In all these models cerebral amyloid neuropathology can occur in senility, although with different levels of incidence (100% in vervets; <30% in macaques). The differences between normal and pathological (Alzheimer's) senility in these species are difficult to establish due to the lack of cognitive-behavioural studies in the many groups analysed, as well as the controversy in the results of these studies when they were carried out. However, in some macaques, a correlation between a high degree of functional brain impairment and a large number of neuropathological changes (“possible AD”) has been found. ConclusionsIn some non-human primates, such as the macaque, the existence of a possible continuum between “normal” ageing process, “normal” ageing with no deep neuropathological and cognitive-behavioural changes, and “pathological ageing” (or “Alzheimer type ageing”), may be considered. In other cases, such as the Caribbean vervet, neuropathological changes are constant and quite marked, but its impact on cognition and behaviour does not seem to be very important. This does assume the possible existence in the human senile physiological regression of a stable phase without dementia even if neuropathological changes appeared.

Light Pollution Modifies the Expression of Daily Rhythms and Behavior Patterns in a Nocturnal Primate

Among anthropogenic pressures, light pollution altering light/dark cycles and changing the nocturnal component of the environment constitutes a threat for biodiversity. Light pollution is widely spread across the world and continuously growing. However, despite the efforts realized to describe and understand the effects of artificial lighting on fauna, few studies have documented its consequences on biological rhythms, behavioral and physiological functions in nocturnal mammals. To determine the impacts of light pollution on nocturnal mammals an experimental study was conducted on a nocturnal primate, the grey mouse lemur Microcebus murinus. Male mouse lemurs (N = 8) were exposed 14 nights to moonlight treatment and then exposed 14 nights to light pollution treatment. For both treatments, chronobiological parameters related to locomotor activity and core temperature were recorded using telemetric transmitters. In addition, at the end of each treatment, the 14th night, nocturnal and feeding behaviors were explored using an infrared camera. Finally, throughout the study, body mass and daily caloric food intake were recorded. For the first time in a nocturnal primate, light pollution was demonstrated to modify daily rhythms of locomotor activity and core temperature especially through phase delays and increases in core temperature. Moreover, nocturnal activity and feeding behaviors patterns were modified negatively. This study suggests that light pollution induces daily desynchronization of biological rhythms and could lead to seasonal desynchronization with potential deleterious consequences for animals in terms of adaptation and anticipation of environmental changes.

Proximate determinants of bite force capacity in the mouse lemur

AbstractBoth mating system and diet are thought to drive inter‐individual variation in bite force. Although previously published data suggest that bite force variation may be driven by variation in morphology (e.g. head morphology, body size, muscle size), age and physiology (e.g. fluctuating plasma testosterone levels) in some vertebrates, this remains untested in primates. Here, we explore the proximal determinants of bite force capacity in the grey mouse lemur Microcebus murinus. Our results show that in male grey mouse lemurs, bite force measurements are repeatable across a 1‐month period. Yet, bite forces were independent of fluctuation plasma testosterone levels. Head dimensions and body mass were all positively correlated with bite force. Among these, head width was the best predictor of bite force as has been observed for other vertebrates. Unexpectedly, age was highly significantly and positively correlated with bite force. Whereas older animals generally bit harder, the oldest age group (5.5 years) showed a decline in bite force capacity. These results suggest that bite force in the grey mouse lemur is mostly determined by morphology and age, yet is independent of variation in testosterone. Future studies including a broader age range and animals of different sexes would be of interest to better understand the variation in bite force in this small lemur.

Seasonal variations in gastrointestinal parasites excreted by the gray mouse lemur Microcebus murinus in Madagascar

We describe seasonal variations in gastrointestinal parasites found in feces of the gray mouse lemur Microcebus murinus. Our study was carried out in the evergreen littoral forest of Mandena, Madagascar. Fecal samples from M. murinus caught during monthly trapping sessions were screened for eggs and larvae of intestinal parasites. Gastrointestinal parasite infection of M. murinus was charac- terized by parasite species richness, the prevalence of parasites, and the intensity of infection expressed as the number of parasite eggs, larvae, and cysts per g feces. We used a modification of the McMaster flotation egg counting technique to quantify parasite egg shedding. Parasite excretions changed season- ally when analyzed on the level of individual hosts. The number of parasite species and the abundance of parasite eggs and larvae in Microcebus feces were higher during the hot season than during the cold season. Reduced parasite excretion during the cold season could be due to environmental factors or to the ability of M. murinus to enter torpor and hibernation during the cold season, which might lead to re- duced metabolism of intestinal parasites and might thus result in reduced shedding of eggs. No such variation was found when the analyses were based on samples of unknown origin.

Torpor and energetic consequences in free-ranging grey mouse lemurs (Microcebus murinus): a comparison of dry and wet forests

Many endotherms save energy during food and water shortage or unpredictable environment using controlled reductions in body temperature and metabolism called torpor. In this study, we measured energy metabolism and water turnover in free-ranging grey mouse lemurs Microcebus murinus (approximately 60 g) using doubly labelled water during the austral winter in the rain forest of southeastern Madagascar. We then compared patterns of thermal biology between grey mouse lemurs from the rain forest and a population from the dry forest. M. murinus from the rain forest, without a distinct dry season, entered daily torpor independent of ambient temperature (T (a)). There were no differences in torpor occurrence, duration and depth between M. murinus from the rain and dry forest. Mouse lemurs using daily torpor reduced their energy expenditure by 11% in the rain forest and by 10.5% in the dry forest, respectively. There was no significant difference in the mean water flux rates of mouse lemurs remaining normothermic between populations of both sites. In contrast, mean water flux rate of individuals from the dry forest that used torpor was significantly lower than those from the rain forest. This study represents the first account of energy expenditure, water flux and skin temperature (T (sk)) in free-ranging M. murinus from the rain forest. Our comparative findings suggest that water turnover and therefore water requirement during the austral winter months plays a more restricting role on grey mouse lemurs from the dry forest than on those from the rain forest.

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.

Sensory ecology of prey rustling sounds: acoustical features and their classification by wild Grey Mouse Lemurs

Summary 1 Predatory mammals and birds from several phylogenetic lineages use prey rustling sounds to detect and locate prey. However, it is not known whether these rustling sounds convey information about the prey, such as its size or profitability, and whether predators use them to classify prey accordingly. 2 We recorded rustling sounds of insects in Madagascar walking on natural substrate and show a clear correlation between insect mass and several acoustic parameters. 3 In subsequent behavioural experiments in the field, we determined whether nocturnal animals, when foraging for insects, evaluate these parameters to classify their prey. We used field-experienced Grey Mouse Lemurs Microcebus murinus in short-term captivity. Mouse Lemurs are generally regarded as a good model for the most ancestral primate condition. They use multimodal sensorial information to find food (mainly fruit, gum, insect secretions and arthropods) in nightly forest. Acoustic cues play a role in detection of insect prey. 4 When presented with two simultaneous playbacks of rustling sounds, lemurs spontaneously chose the one higher above their hearing threshold, i.e. they used the rustling sound's amplitude for classification. We were not able, despite attempts in a reinforced paradigm, to persuade lemurs to use cues other than amplitude, e.g. frequency cues, for prey discrimination. 5 Our data suggests that Mouse Lemurs, when foraging for insects, use the mass–amplitude correlation of prey-generated rustling sounds to evaluate the average mass of insects and to guide their foraging decisions.

MHC Variability of a Small Lemur in the Littoral Forest Fragments of Southeastern Madagascar

Habitat fragmentation inhibits gene flow between populations often resulting in a loss of genetic diversity with possible negative effects on fitness parameters. In vertebrates, growing evidence suggests that such genetic diversity is particularly important at the level of the major histocompatibility complex (MHC) because its gene products play an important role in immune functions. Diversity in the MHC is assumed to improve population viability. Here, we investigated the impact of forest fragmentation on the genetic variability of one of the functionally important parts of the MHC, DRB exon 2, of the endemic mouse lemur Microcebus murinus by comparing populations inhabiting two littoral forest fragments of different size in southeastern Madagascar. Twelve different alleles of DRB exon 2 were found in 145 individuals of M. murinus with high levels of sequence divergence between alleles. In both subpopulations, levels of genetic diversity were high, and the genetic analyses revealed only limited effects of fragmentation. Significantly more non-synonymous than synonymous substitutions were found in the functionally important antigen recognition and binding sites indicating selection processes maintaining MHC polymorphism. This is the first study on MHC variation in a free-ranging Malagasy lemur population.

Female dominance in competition for gum trees in the Grey Mouse Lemur Microcebus murinus

Chez les mammifères, les femelles sont généralement plus limitées par les ressources alimentaires que les mâles, du fait de leur plus grand investissement dans la reproduction. Dans une forêt sèche décidue de l’ouest de Madagascar, le poids corporel, la distribution spatiale, les comportements alimentaires et sociaux de Microcèbes gris (Microcebus murinus) ont été suivis pendant la période d’engraissement automnal (mars-avril) à l’aide de captures-recaptures d’animaux marqués et d’observations comportementales. Seuls quelques animaux (23 %) ont pris du poids et les femelles étaient en général plus lourdes que les mâles. La distribution spatiale des captures des animaux des deux sexes s’est superposée à celle des arbres à gomme, lesquels sont apparus comme une ressource-clef à cette période (75 % du régime). De plus, les femelles étaient d’autant plus lourdes qu’elles étaient capturées près des arbres à gomme, alors que cette corrélation n’a pas été retrouvée chez les mâles. Une exclusion spatiale des captures de mâles et de femelles a également été observée. En fait, une compétition locale pour les ressources, confirmée par les observations comportementales, semble expliquer le poids corporel élevé d’animaux dominants, c’est-à-dire en particulier des femelles. La mise en réserve de graisse corporelle pourrait affecter à la fois la survie à la saison sèche et le succès reproducteur à la saison des pluies suivante. Ainsi, la compétition alimentaire à l’automne pourrait avoir des conséquences importantes sur l’organisation socio-spatiale du Microcèbe gris en produisant une grande variabilité intra-et inter-sexuelle.

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.

Topographical localization of lipofuscin pigment in the brain of the aged fat‐tailed dwarf lemur Cheirogaleus Medius and grey lesser mouse lemur Microcebus Murinus: Comparison to iron localization

Topographical localization of lipofuscin pigment in the brain of the aged fat‐tailed dwarf lemur Cheirogaleus Medius and grey lesser mouse lemur Microcebus Murinus: Comparison to iron localization

Topographical localization of iron in brains of the aged fat‐tailed dwarf lemur Cheirogaleus medius and gray lesser mouse lemur Microcebus murinus

Iron deposits in the human brain are characteristic of normal aging but have also been implicated in various neurodegenerative diseases. Among nonhuman primates, strepsirhines are of particular interest because hemosiderosis has been consistently observed in captive aged animals. In particular, the cheirogaleids, because of their small size, rapid maturity, fecundity, and relatively short life expectancy, are a useful model system for the study of normal and pathological cerebral aging. This study was therefore undertaken to explore iron localization in the brain of aged cheirogaleids (mouse and dwarf lemurs) with histochemistry and magnetic resonance microscopy. Results obtained with both techniques were comparable. There was no difference between old animals in the two species. The young animals (3 years old) showed no iron deposits. In the old animals (8–15 years old), iron pigments were mainly localized in the globus pallidus, the substantia nigra, the neocortical and cerebellar white matter, and anterior forebrain structures, including the nucleus basalis of Meynert. This distribution agrees with previous findings in monkeys and humans. In addition, we observed iron in the thalamus of these aged nonhuman primates. Microscopic NMR images clearly reveal many features seen with the histochemical procedure, and magnetic resonance microscopy is a powerful method for visualizing age-related changes in brain iron. Am. J. Primatol. 45:291–299, 1998. © 1998 Wiley-Liss, Inc.