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The Gray Mouse Lemur (Microcebus murinus) is a small Strepsirrhine primate, found only on the island of Madagascarmarker. Weighing , it is the largest mouse lemur, yet smaller than the world's smallest monkey, the Pygmy Marmoset, which ranges between . Its genus, Microcebus, includes the smallest primates in the world.

The Gray Mouse Lemur is named for its mouse-like size and coloration. It is known locally (in Malagasy) as Tsidy, Koitsiky, Titlivaha, Pondiky, and Vakiandri.

Like all mouse lemurs, this species is nocturnal and arboreal. It is very active, and although it forages alone, groups of males and females will form sleeping groups and share tree holes during the day. The Gray Mouse Lemur can be found in several types of forest throughout western and southern Madagascar. Its diet consists primarily of fruit, insects, flowers, and nectar.

Gestation lasts approximately 60 days, and typically two young are born. The offspring are usually independent in two months, and can reproduce after one year. The Gray Mouse Lemur has a reproductive lifespan of five years, although captive individuals have been reported to live up to 15 years. Although threatened by slash-and-burn agriculture and live capture for the pet trade, wild populations can remain healthy under the right conditions. It is considered one of Madagascar's most abundant small native mammals.

Etymology

The Gray Mouse Lemur is named for its brownish-gray fur and mouse-like size and appearance. The genus name, Microcebus, derives from the Greek word mikros, meaning small, and the Greek word, kebos, meaning monkey. The Latin version of Kebos, cebus, is a common suffix used for primates, despite the fact that the Gray Mouse Lemur is a lemur, and not a monkey. The species name, murinus, is Latin for "gray-mouse-colored" and derives from the Latin word mus, or "mouse."

It is known locally (in Malagasy) as Tsidy, Koitsiky, Titlivaha, Pondiky, and Vakiandri.

Taxonomy

First described in 1777 by John Frederick Miller, the Gray Mouse Lemur is a primate and belongs to the suborder Strepsirrhini and infraorder Lemuriformes. Within Lemuriformes, the Gray Mouse Lemur belongs to the family Cheirogaleidae, which contains the dwarf lemurs and mouse lemurs. The Gray Mouse Lemur is a member of the genus Microcebus, which includes most of the mouse lemurs, including the smallest primates in the world. According to D-loop DNA sequence data, the Gray Mouse Lemur may be most closely related to the Reddish-gray Mouse Lemur (M. griseorufus).

Anatomy and physiology

The Gray Mouse Lemur shares many traits with other mouse lemurs, including soft fur, a long tail, long hind limbs, a dorsal stripe down the back (not always distinct), a short snout, rounded skull, prominent eyes, and large, membranous, protruding ears. It has large eyes and a tapetum lucidum to enhance its vision at night. The dorsal coat is brownish-gray with various reddish tones, the flanks are light gray to beige, and the ventral fur has discrete dull beige or whitish-beige patches along portions of the belly. On the rounded face, there is a pale white patch above the nose and between the eyes; some individuals have dark orbital markings. The furred portions of the hands and feet are off-white.

The Gray Mouse Lemur is one of the smallest primates in the world, yet it is also the largest mouse lemur. Its total length is , with a head-body length of and a tail length of . The average weight for this species is , with ranges of and reported. This is smaller than the world's smallest monkey, the Pygmy Marmoset, which ranges between . Weight varies by season, with both sexes building fat reserves, up to 35% of their body weight, in the tail and hind legs prior to the dry season and periods of estivation.


Ecology

Like all other members of its family, Cheirogaleidae, the Gray Mouse Lemur is nocturnal and arboreal. It inhabits lowland tropical dry forest, sub-arid thorn scrub, gallery forest, spiny forest, eastern littoral forest, dry deciduous forest, semi-humid deciduous, moist lowland forest, transitional forest, and secondary forests or degraded forests (including plantations) all ranging up to above sea level. The species is more common in secondary forest than in primary forest, particularly bush and scrub habitat, where it occupies a "fine branch" niche, restricting the vertical range to fine branches, fine terminal supports, lianes and dense foliage. These lemurs are usually seen on branches less than in diameter. The Gray Mouse Lemur tends to prefer lower levels of the forest and the understory, where branches and vegetation are dense.

In secondary forest, it is generally observed at above ground, yet in the canopy of primary forest. Studies have found that the species can spend as much as 40% of its time below , with 70% of its time spent at this level during the end of the dry season, when plant food is limited and insects compose a larger percentage of the diet. The species is more numerous in spiny forest, such as the Andohahela Special Reservemarker, than in the gallery forest, preferring drier, littoral forest, whereas the Brown Mouse Lemur prefers inland rain forest.

The limits of the distribution are poorly understood. It is believed to range from the Onilahy Rivermarker or Lake Tsimanampetsotsamarker in the south to Ankarafantsika National Park in the north There is also an isolated and disjointed population in the southeastern part of the island, near Tôlanaromarker and the Andohahela National Park, up to the Mandena Conservation Zone. Individuals tend to occupy small home ranges of . The Gray Mouse Lemur is also sympatric with the Reddish-gray Mouse Lemur, Golden-brown Mouse Lemur, Madame Berthe's Mouse Lemur, and several other cheirogaleid lemurs.

The Gray Mouse Lemur can reach high population densities up to several hundred individuals per square kilometer (up to 167 individuals/km2 at Ankarafantsika National Park to 712 individuals/km2 at Kirindy Mitea National Park). This abundance is not uniform and tends to concentrate in "population nuclei"', suggesting that it is difficult to accurately estimate population densities when extrapolating from a small area (from various studies) to a large area. The difficulty in finding individuals during some times of the year, particularly during the dry periods, can further complicate the problem of estimating population densities.

Mouse lemurs are omnivorous, favoring fruit and insects for the bulk of its diet. The Gray Mouse Lemur may even come down to the ground to catch insect prey, although it will quickly return to the protective cover of the understory to consume its catch. Nectar is also a part of the Gray Mouse Lemur's diet, making it a potential pollinator for local plant species.

Predation

The most significant predator of the Gray Mouse Lemur are the Madagascar Long-eared Owl and Barn Owl. Studies in Beza Mahafaly Reservemarker and Kirindy Mitea National Park indicate an approximate predation rate of 25% (percent population taken by predator per year), the highest known for any primate species. However, given its high reproductive potential, predation does not appear to drastically affect its populations. Other raptors, such as the Henst's Goshawk, and owls prey upon this species. Snakes, such as Ichythcyphys miniatus (a native colubrid snake), Madagascar tree boa, as well as mammalian predators, such as the Ring-tailed Mongoose, Narrow-striped Mongoose, Fossa, and domestic dog are also prey upon the Gray Mouse Lemur. Mammalian predators often discover tree holes serving as nests and then enlarge the opening in order to obtain and eat the occupant, resulting in strong selective pressure affecting the choice of nest hole opening diameter and deepness.

Due to its non-gregarious nature, the Gray Mouse Lemur, like other nocturnal lemurs, defends itself from predators using strategies that do not involve direct defense or social facilitation. First, individuals take shelter inside tree holes within their range during the day when they are most vulnerable, sometimes forming nests. Individuals use between three and nine different tree holes within their range, yet stay within one particular hole for up to five consecutive days. Tree hollows tend to be preferred, but spherical constructions made of leaves are also common. Nests are usually found in tree holes with a minimum diameter of , with a median of , suggesting that this range in diameter of tree holes my be crucial for maintaining a healthy habitat for this species. The Gray Mouse Lemur also spends most of its time in dense vegetation, limiting its visibility and accessibility. Furthermore, it has a high reproductive rate to counter losses to predation.

Behavior

The Gray Mouse Lemur is nocturnal, sleeping during the day in tree holes lined with leaf-litter or purpose-built spherical nests constructed from dead leaves, moss and twigs. It usually forages alone at night, but may sleep in groups during the day, the composition of which depends on gender and season. Tree holes can be shared with up to 15 other individuals, although males tend to sleep alone while females tend to share nests.

All mouse lemurs are agile and highly active at night,, often scurrying like mice and leaping over , using the tail as a balancing organ. When moving among the terminal branches of bushes and trees, they grip using all four feet and move with four legs. When on the ground, either to catch insects or cross short open areas, mouse lemurs hop like a frog.

Foraging behavior is often slow, with height and direction changing continuously. Predation of insects occurs primarily on the ground. Before descending, the ear pinna move alternately to help pinpoint the precise location of their prey. Insects are captured during a rapid dash across the leaf litter and are transported by mouth up into the relative safety of the branches.

Activity patterns differ noticeably between populations and sexes. At Ankarafantsika National Park, males and females exhibit daily, rather than seasonal torpor. At Kirindy Forest, both sexes share the same daily torpor, yet during the dry season (April/May through September/October), females become completely inactive for several weeks or up to five months to conserve energy and reduce predation. Males, however, rarely remain inactive for more than a few days and become extremely active before the females revive from torpor, allowing them to establish hierarchies and territories for the breeding season. This pattern of seasonal versus daily torpor may relate to the seasonality of the region.

During torpor, the Gray Mouse Lemur's metabolic rate slows and its body temperature drops to the ambient temperature, as low as . From May though August, during the cooler winter months, the species selects tree holes closer to ground level, where ambient temperatures remain more stable. This allows them to remain in torpor longer, conserving metabolic resources.

Diet

The Gray Mouse Lemur is omnivorous, feeding primarily on fruit and invertebrates. Local populations appear to specialize on locally available fruit. At both Marosalaza and Mandena, beetles are the primary insect prey, although moths, praying mantid, fulgorid bugs, crickets, cockroaches, and spiders are also eaten. Less than half the diet consists of insects, with fruit making up a slightly larger fraction. This lemur also consumes flowers, gums and nectar from Euphorbia and Terminalia trees, leaves (Uapaca sp.), exudates (Homopteran larvae secretions), and small vertebrates such as tree frogs, geckos, and chameleons.

Social systems

The Gray Mouse Lemur is described as solitary but social, foraging alone at night, but frequently sleeping in groups during the day. This varies by gender, season, and location. Females tend to share nests with other females and their offspring, whereas males tend to sleep alone or in pairs outside of the breeding season. Groups of females sharing a nest can be relatively stable, consisting of two to nine individuals, although a male may be found with a group of females outside the breeding season. During the breeding season (September through October), males and females may sleep in the same tree hole. Mixed sex groups can be common at this time, with single males sharing nest sites with three to seven females or single females sharing nest sites with one to three males.

Research has shown that home ranges for the Gray Mouse Lemur are likely to be small, possibly less than . Males typically travel further at night and have home ranges that are twice as large as those of females, often overlapping with one another, and always overlapping with at least one female's home range. Male home ranges increase threefold during the breeding season, and ranges are scent-marked with urine and feces.

Female home ranges overlap less than those of males, although localized concentrations, or "population nuclei" tend to form in some areas, where the sex ratio favors females to males by three or four to one at the nucleus core. Genetic studies indicate that females arrange themselves spatially in clusters ("population nuclei") of related individuals, while males tend to emigrate from their natal group.

Communication

Vocalizations and scent are the primarily modes of communication within this species. Home ranges are scent mark with urine and feces. Vocalizations are complex and very high-pitched (ranging from 10 to 36 kHz), sometimes beyond the range of human hearing (0.02 to 20 kHz). These include calls for seeking contact, mating, distant communication, alarm, and distress.

As with other social mammals, the calls reveal the sex and identity of the individual. Dialects have also been detected between communities. The male trill call, part of the male mating display, is very like a bird song in terms of its ordered sequence of broadband frequency modulated syllables, ranging between 13 to 35 kHz in pitch and lasting 0.3 to 0.9 seconds, repeating up to 1.5 times per minute. Each locality has its own theme of trill calls that is distinct from those of neighboring communities, and resident males produce individually distinct trill calls within that theme. These calls are not genetically programmed. During play, young males produce early attempts at the trill call which show high degrees of variability. Research has shown that the male mouse lemurs consciously manipulate the dialect to resemble those of their neighbors, when transferred from their home to a new neighborhood. This may reduce aggression and foster social acceptance for emigrant males as they transfer from their natal group upon maturity.

Breeding and reproduction

The mating system is described as multi-male/multi-female. Males establish dominance hierarchies prior to the mating season, however, some studies in the wild have shown no male aggression or visible competition for receptive females. Males in captivity become highly aggressive and form strict dominance hierarchies. These captive males may show the highest plasma testosterone levels found in mammals, and even the odor of a dominant male can lower the testosterone levels and sexually inhibit a subordinate male.

The females are receptive for 45 to 55 days between September and October, with estrus lasting 1 to 5 days. During the breeding season, male testes increase significantly in size. Females advertise estrus by distinctive high-frequency calls and scent-marking. Gestation lasts 54 to 68 days, averaging 60 days, typically resulting in 2 or 3 offspring weighing each.

Infants are born in a leaf nest or tree hole in November prior to the onset of the rainy season. Weaning occurs after 25 days, and the infants are either left in the nest or carried in the mother's mouth and deposited on a branch while she forages. Infant mouse lemurs do not cling to the mother's fur. Independence is attained in 2 months, while sexual maturity is reached at 10 to 29 months in females and 7 to 19 months in males. Closely related females remain loosely associated after maturation (female philopatry), whereas males disperse from their natal area. In the wild, the Gray Mouse Lemur's reproductive lifespan is no more than 5 years, although captive specimens have reportedly lived as long as 15 years and 5 months.

Conservation status

The Gray Mouse Lemur was listed in Appendix 1 by the Convention on International Trade in Endangered Species (CITES) in 1975, declaring it as threatened with extinction and prohibiting international trade of specimens except for non-commercial use, such as scientific research. As of 2009, the species was no longer listed under Appendix 1. The 2008 International Union for Conservation of Nature (IUCN) Red List assessment lists it as a species of Least Concern (LC) with a decreasing population trend. Its greatest threats are habitat loss from slash-and-burn agriculture and cattle-grazing, as well as live capture for the local pet trade in the northern and southern parts of its range. Although this species inhabits secondary forests, studies have shown that decreased habitat quality adversely affects its populations since fewer tree holes offer fewer opportunities to conserve energy, increasing stress and mortality. Studies in the late 1960's and 1970's showed that heavy logging between 1968 and 1970 seemed to result in decreased body weight, the use of smaller trees for nesting sites, and a smaller maximum female nesting group size (down to 7 from 15).

The Gray Mouse Lemur is considered to be one of Madagascar's most abundant small native mammals, found in seven national parks, five special reserves, the Berenty Private Reservemarker, and other privately-protected forests within the Mandena Conservation Zone.

This species of mouse lemur breeds very well in captivity, although it is not commonly displayed in zoos like some larger, diurnal lemurs. In 1989, more than 370 individuals were housed by 14 International Species Information System (ISIS) and non-ISIS institutions across the United States and Europe, 97% of which were captive born. In March 2009, 167 were registered at 29 ISIS institutions, including the Duke Lemur Center.

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