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The gray mouse lemur (Microcebus murinus, GML) is a nocturnal, arboreal, prosimian primate that is native to Madagascar. Captive breeding colonies of GMLs have been established primarily for noninvasive studies on questions related to circadian rhythms and metabolism. GMLs are increasingly considered to be a strong translational model for neurocognitive aging due to overlapping histopathologic features shared with aged humans. However, little information is available describing the clinical presentations, naturally occurring diseases, and histopathology of aged GMLs. In our colony, a 9 y-old, male, GML was euthanized after sudden onset of weakness, lethargy, and tibial fracture. Evaluation of this animal revealed widespread fibrous osteodystrophy (FOD) of the mandible, maxilla, cranium, appendicular, and vertebral bones. FOD and systemic metastatic mineralization were attributed to underlying chronic renal disease. Findings in this GML prompted periodic colony-wide serum biochemical screenings for azotemia and electrolyte abnormalities. Subsequently, 3 additional GMLs (2 females and 1 male) were euthanized due to varying clinical and serum biochemical presentations. Common to all 4 animals were FOD, chronic renal disease, uterine adenocarcinoma (females only), cataracts, and osteoarthritis. This case study highlights the concurrent clinical and histopathologic abnormalities that are relevant to use of GMLs in the expanding field of aging research.

SummaryThe physiological mechanisms of the responses toward stressors are the core of ecophysiology studies to understand the limits of an organism’s flexibility and better predict the impact of environmental degradation on natural populations. However, little information is available when we question inter-individual variability of these physiological responses, even though they can be particularly important. Some observations of intersexual differences in heterothermy raised the question of a difference in energy management between sexes. Here we assess male and female differences in a mouse lemur model (Microcebus murinus), a highly seasonal Malagasy primate, studying their physiological flexibility toward caloric restriction, and examining the impact on their reproductive success. These animals are adapted for naturally changing food availability and climate conditions, and can express deep torpor, allowing them to spare their energy expenses over the dry and cold season. We monitored body mass and body temperature on 12 males and 12 females over winter, applying a chronic 40% caloric restriction to 6 individuals of each group. Our results showed variability of Tb modulations throughout winter and in response to caloric treatment depending on the sex, as females entered deep torpor regardless of food restriction, while only CR males had a similar response. The use of deep torpor, however, did not translate into better body condition either in females, or in response to CR, and did not clearly affect reproductive success. The favorable captive context potentially buffered the depth of torpor and minimized the positive effects of using torpor on energy savings. However, our results may emphasize the existence of other benefits of heterothermic responses than fat reserves.

The gray mouse lemur (Microcebus murinus, GML) is a nocturnal, arboreal, prosimian primate that is native to Madagascar. Captive breeding colonies of GMLs have been established primarily for noninvasive studies on questions related to circadian rhythms and metabolism. GMLs are increasingly considered to be a strong translational model for neurocognitive aging due to overlapping histopathologic features shared with aged humans. However, little information is available describing the clinical presentations, naturally occurring diseases, and histopathology of aged GMLs. In our colony, a 9 y-old, male, GML was euthanized after sudden onset of weakness, lethargy, and tibial fracture. Evaluation of this animal revealed widespread fibrous osteodystrophy (FOD) of the mandible, maxilla, cranium, appendicular, and vertebral bones. FOD and systemic metastatic mineralization were attributed to underlying chronic renal disease. Findings in this GML prompted periodic colony-wide serum biochemical screenings for azotemia and electrolyte abnormalities. Subsequently, 3 additional GMLs (2 females and 1 male) were euthanized due to varying clinical and serum biochemical presentations. Common to all 4 animals were FOD, chronic renal disease, uterine adenocarcinoma (females only), cataracts, and osteoarthritis. This case study highlights the concurrent clinical and histopathologic abnormalities that are relevant to use of GMLs in the expanding field of aging research.

Physical performance is crucial for animal survival and fitness. In this context, greater bite forces can provide advantages and may allow an individual to gain access to reproductive partners and/or different food resources. Here, we explored the determinants of bite force in a wild population of the brown mouse lemur (Microcebus rufus). Our objectives were to elucidate (1) if sex, head width, heart rate (as an indicator of overall physical fitness) and body condition drive variation in bite force in this population of wild mouse lemurs; and (2) the relative importance of the ecological niche in determining bite force by comparing results from this wild population with previously published results on bite force, body mass and head width from a laboratory colony of the grey mouse lemur (Microcebus murinus). We captured 32 wild brown mouse lemurs at night in the Ranomafana National Park in Madagascar during the beginning of the rainy season from 1st to 31st October 2016. We measured bite force, heart rate, body mass and head width of all individuals, and assigned sex and body condition (estimated as the unstandardized residual of a regression of body mass against head size). Although maximum bite force was positively correlated with body mass, it was not correlated with body condition. Residual bite force was highly correlated with residual head width and heart rate. The mean bite force of wild brown mouse lemurs was much lower than that of grey mouse lemurs in captivity, but showed similar relationships to head dimension and body mass. Even when corrected by body condition, grey mouse lemurs bit significantly harder than brown mouse lemurs. The difference in bite force between species could be explained by differences in head size and niche divergence with brown mouse lemurs eating mostly soft fruits and grey mouse lemurs eating more hard insects.

The lemurs of Madagascar are threatened by human activities. We present the first molecular detection of canine heartworm (Dirofilaria immitis) in a wild non-human primate, the mouse lemur (Microcebus rufus). Zoonotic D. immitis infection has been associated with clinical pathology that includes serious and often fatal cardiac and pulmonary reactions. With human encroachment and associated increases in free-roaming dog populations in Madagascar, we examined lemurs for zoonotic canid pathogens. D. immitis presents a new potential conservation threat to lemurs. We highlight the need for wide-ranging and effective interventions, particularly near protected areas, to address this growing conservation issue. Keywords: Madagascar conservation, Pathogen spillover, Mosquito-borne disease, Blood parasite, Canine vector-borne diseases, brown mouse lemur, Microcebus rufus

Madagascar is home to the smallest primates in the world, the mouse lemurs (Microcebus species). Twenty-four species of mouse lemur are currently recognised and are found in variable ecosystems, from dry forests and spiny deserts to humid forests. Due to their widespread distribution and the large number of sympatric species, mouse lemurs can be used as a model to understand the linkages among species richness, population density, and habitat. As all lemurs are threatened by habitat loss and fragmentation, this information can also be used to inform conservation management. We hypothesise that on an island-wide scale, we will find higher population densities in western dry forests than in eastern humid forests because the western dry forests exhibit lower species richness, more sympatric habitat use, and lower resource stability than the eastern humid forests. We conducted a literature review of population density estimates of known mouse lemur species, and used those data to conduct a meta-analysis and estimate overall average population density by geographic region. Our findings suggest that mouse lemur species living in western dry forest generally exhibit higher densities than those in eastern humid forests. This may be partly explained by higher habitat fragmentation in western dry forests, where species co-occur, but is likely to be a function of the magnitude and variability in seasonally available resources in each forest type. Higher seasonality results in less constant food availability and lower levels of environmental predictability, fostering species capable of coping with environmental change and maintaining high densities throughout periods of resource paucity. Our study highlights the importance of conducting Microcebus population density research that adheres to standardised methodological approaches. We point to the need for population density estimates for several species for which data are lacking. Such knowledge is important to assess the conservation status of these species, but also to enhance our ability to identify the macro-biogeographical and local ecological drivers of interspecific and intraspecific variability in population density.

Systematic genetic studies of a handful of diverse organisms over the past 50 years have transformed our understanding of biology. However, many aspects of primate biology, behavior, and disease are absent or poorly modeled in any of the current genetic model organisms including mice. We surveyed the animal kingdom to find other animals with advantages similar to mice that might better exemplify primate biology, and identified mouse lemurs (Microcebus spp.) as the outstanding candidate. Mouse lemurs are prosimian primates, roughly half the genetic distance between mice and humans. They are the smallest, fastest developing, and among the most prolific and abundant primates in the world, distributed throughout the island of Madagascar, many in separate breeding populations due to habitat destruction. Their physiology, behavior, and phylogeny have been studied for decades in laboratory colonies in Europe and in field studies in Malagasy rainforests, and a high quality reference genome sequence has recently been completed. To initiate a classical genetic approach, we developed a deep phenotyping protocol and have screened hundreds of laboratory and wild mouse lemurs for interesting phenotypes and begun mapping the underlying mutations, in collaboration with leading mouse lemur biologists. We also seek to establish a mouse lemur gene “knockout” library by sequencing the genomes of thousands of mouse lemurs to identify null alleles in most genes from the large pool of natural genetic variants. As part of this effort, we have begun a citizen science project in which students across Madagascar explore the remarkable biology around their schools, including longitudinal studies of the local mouse lemurs. We hope this work spawns a new model organism and cultivates a deep genetic understanding of primate biology and health. We also hope it establishes a new and ethical method of genetics that bridges biological, behavioral, medical, and conservation disciplines, while providing an example of how hands-on science education can help transform developing countries.

All habitats of Madagascar go through a dry season from April to September each year, resulting in a period of fruit scarcity lasting up to 6 months and creating selection pressure for adaptation to fluctuations in resources. Some Cheirogaleid lemurs, including mouse lemurs (Microcebus), use daily torpor and long-term hibernation during this period, saving energy through inactivity. Capture–recapture studies in some mouse lemur populations have suggested a pattern of biased sex ratio throughout the winter as a result of females hibernating while most males remain active. We studied winter activity in a captive population of Microcebus lehilahytsara, Goodman’s mouse lemur, in a large enclosure at Zoo Zurich, Switzerland using capture–recapture methods to determine how this behavior varies with sex and age, and what this pattern suggests about the ultimate cause of torpor use in this clade. Our results suggest that Goodman’s mouse lemurs use torpor to avoid seasonal food shortage, even though they experience less extreme seasonal variability of food availability than western dry forest mouse lemurs. Male and female Goodman’s mouse lemurs are equally capable of winter torpor, and most remaining active individuals are young that have not sufficiently fattened. This suggests that the “ideal” winter behavior for both males and females is torpor, which ultimately avoids periods of seasonal food scarcity.

Mouse lemurs (Microcebus) are solitary, experience heavy predation, and use torpor to conserve energy, so an individual's choice of daytime sleeping site can have a major impact on its fitness. Sharing a sleeping site may strengthen social bonds or insulate against fluctuating ambient temperatures. Changing sites often may prevent tracking by predators. Choosing a site in a hole in an old, thick tree may allow for longer and deeper torpor. The aim of this paper is to provide a preliminary characterization of sleeping site selection and use in Microcebus rufus, the brown mouse lemur. We trapped mouse lemurs in disturbed forests in the peripheral zone of Ranomafana National Park, Madagascar, and tracked 7 individuals using temperature-sensitive radiocollars. Radiotracked individuals shared sleeping sites concurrently and serially and slept in same-sex and mixed-sex groups. They slept in tree holes as well as in piles of leaves on branches. Radiotracked individuals tended to use higher-diameter at breast hei...

Aim The factors that set species range limits underlie many patterns in ecology, evolution, biogeography and conservation. These factors have been the subject of several reviews, but there has been no systematic review of the causes of warm-edge limits (low elevations and latitudes). Understanding these causes is urgent, given that the factors that set these limits might also drive extinction at warm edges as global climate changes. Many authors have suggested that warm-edge limits are set by biotic factors (particularly competition) whereas others have stressed abiotic factors (particularly temperature). We synthesize the known causes of species’ warm-edge range limits, with emphasis on the underlying mechanisms (proximate causes).

Anthropogenic climate change is predicted to be a major cause of species extinctions in the next 100 years. But what will actually cause these extinctions? For example, will it be limited physiological tolerance to high temperatures, changing biotic interactions or other factors? Here, we systematically review the proximate causes of climate-change related extinctions and their empirical support. We find 136 case studies of climatic impacts that are potentially relevant to this topic. However, only seven identified proximate causes of demonstrated local extinctions due to anthropogenic climate change. Among these seven studies, the proximate causes vary widely. Surprisingly, none show a straightforward relationship between local extinction and limited tolerances to high temperature. Instead, many studies implicate species interactions as an important proximate cause, especially decreases in food availability. We find very similar patterns in studies showing decreases in abundance associated with climate change, and in those studies showing impacts of climatic oscillations. Collectively, these results highlight our disturbingly limited knowledge of this crucial issue but also support the idea that changing species interactions are an important cause of documented population declines and extinctions related to climate change. Finally, we briefly outline general research strategies for identifying these proximate causes in future studies.