Gray mouse lemur
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The gray mouse lemur (Microcebus murinus), grey mouse lemur or lesser mouse lemur is a small lemur, a type of strepsirrhine primate, found only on the island of Madagascar. Weighing Template:Convert, it is the largest of the mouse lemurs (genus Microcebus), a group that includes the smallest primates in the world. The species is named for its mouse-like size and coloration and is known locally (in Malagasy) as tsidy, koitsiky, titilivaha, pondiky, and vakiandry. The gray mouse lemur and all other mouse lemurs are considered cryptic species, as they are nearly indistinguishable from each other by appearance. For this reason, the gray mouse lemur was considered the only mouse lemur species for decades until more recent studies began to distinguish between the species.
Like all mouse lemurs, this species is nocturnal and arboreal. It is very active, and though it forages alone, groups of males and females form sleeping groups and share tree holes during the day. It exhibits a form of dormancy called torpor during the cool, dry winter months, and in some cases undergoes seasonal torpor (or hibernation), which is unusual for primates. 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. In the wild, its natural predators include owls, snakes, and endemic mammalian predators. Predation pressure is higher for this species than among any other primate species, with one out of four individuals taken by a predator each year. This is counterbalanced by its high reproductive rate. Breeding is seasonal, and distinct vocalizations are used to prevent hybridization with species that overlap its range. 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 deforestation, habitat degradation, and live capture for the pet trade, it is considered one of Madagascar's most abundant small native mammals. It can tolerate moderate food shortages by experiencing daily torpor to conserve energy, but extended food shortages due to climate change may pose a significant risk to the species.
EtymologyEdit
The gray or lesser mouse lemur is named for its brownish-gray fur and mouse-like size and appearance. The genus name, Microcebus, derives from the Greek words mikros, meaning "small", and kebos, meaning "monkey". The Latin version of kebos, cebus, is a common suffix used for primate names, despite the fact that the gray mouse lemur is a lemur, and not a monkey. The species name, murinus, means "mouse-like" and derives from the Latin word mus, or "mouse", and the Latin suffix -inus, which means "like".<ref name="1904Palmer">Template:Cite book</ref>
The lemur is known locally by several names in Malagasy, depending upon the region. Around Tôlanaro (Fort Dauphin), it is called pondiky {{#invoke:IPA|main}}. In the northern end of its range, it is known as tsidy {{#invoke:IPA|main}}. Around Morondava, it is referred to as koitsiky {{#invoke:IPA|main}}, titilivaha {{#invoke:IPA|main}}, and vakiandry {{#invoke:IPA|main}}.<ref name="Mittermeier104-107">Mittermeier, R.A.; et al. (2006). "M. murinus", pp. 104–107</ref><ref name="IUCN Lemurs">Template:Cite book</ref> In many cases, these Malagasy names are also used for other visually indistinguishable mouse lemur species that live within its range.<ref name="Mittermeier91-128">Mittermeier, R.A.; et al. (2006). "Mouse lemurs", pp. 91–128</ref>
TaxonomyEdit
As its name implies, the gray mouse lemur is a lemur, a type of primate, and belongs to the suborder Strepsirrhini and infraorder Lemuriformes.<ref name="msw3" /> Within Lemuriformes, it belongs to the family Cheirogaleidae, which contains the mouse lemurs, dwarf lemurs, giant mouse lemurs, fork-marked lemurs, and hairy-eared dwarf lemur. The mouse lemur genus Microcebus includes the smallest primates in the world.<ref name="msw3" /><ref name="Mittermeier104-107" /><ref name="Garbutt" /><ref name="Nowak">Template:Cite book</ref> Phylogenetic analyses of D-loop DNA sequences of various lemur species suggest that the gray mouse lemur may be most closely related to the reddish-gray mouse lemur (M. griseorufus).<ref name="new_Microcebus01">Template:Cite journal</ref>
In 1777, the English illustrator John Frederick Miller included a hand-coloured plate of the gray mouse lemur in his Icones animalium et plantarum and coined the binomial name Lemur murinus.<ref>Template:Cite book Published in 10 parts with 6 plates in each part. See: Template:Cite journal</ref> The species was moved to the genus Microcebus by the French naturalist Étienne Geoffroy Saint-Hilaire in 1834.<ref>Template:Cite book</ref> M. murinus remained the only species of its genus, as well as the name used for all mouse lemurs on Madagascar, between the first major taxonomic revision in 1931 and an extensive field study conducted in 1972. The field study distinguished the brown mouse lemur, M. rufus—then considered a subspecies—as a distinct, sympatric species in the southeastern part of the island.<ref name="NaturalHistory">Template:Cite book</ref> Upon this revision, the gray mouse lemur was thought to account for all mouse lemurs that lived in the drier parts of the north, west, and south, while the brown mouse lemur represented the eastern rainforest mouse lemurs. More recently, scientific understanding of the distribution and diversity of the mouse lemurs has become much more complex.<ref name="Garbutt" /> Additional field studies, genetic testing, and resulting taxonomic revisions throughout the 1990s and 2000s identified numerous new mouse lemur species, demonstrating that the genus includes at least 17 cryptic species.<ref name="2008MittermeierGroves">Template:Cite journal</ref><ref name="2008Braune pp1–10">Template:Cite journal
- Template:Cite press release</ref><ref name="2006Olivieri">Template:Cite journal</ref><ref name="2008Louis">Template:Cite journal</ref>
Anatomy and physiologyEdit
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,<ref name="Nowak" /> and large, membranous, protruding ears.<ref name="Mittermeier104-107" /><ref name="IUCN Lemurs" /><ref name="Garbutt" /> It has large eyes and a tapetum lucidum to enhance its vision at night.<ref name="Garbutt" /> 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.<ref name="Mittermeier104-107" />
The gray mouse lemur is one of the smallest primates in the world, yet it is also the largest mouse lemur.<ref name="Garbutt">Template:Cite book</ref> Its total length is Template:Convert, with a head-body length of Template:Convert and a tail length of Template:Convert.<ref name="Mittermeier104-107" /> The average weight for this species is Template:Convert,<ref name="Garbutt" /> with ranges of Template:Convert<ref name="Mittermeier104-107" /> and Template:Convert<ref name="Garbutt" /> reported. This is smaller than the world's smallest monkey, the pygmy marmoset, which ranges between Template:Convert.<ref name="Nowak" /> 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 dormancy.<ref name="Garbutt" /> The tail of the gray mouse lemur can increase fourfold in volume during the wet season when it is storing fat. Even in captivity when environmental limitations are not an issue, mouse lemurs have shown a seasonal dietary preference with a greater protein intake during what would be their more active season.<ref name="Fleagle">Template:Cite book</ref>
Researchers have identified differences in the tooth morphology of the first and second molars between the gray mouse lemur and the reddish-gray mouse lemur. In the reddish-gray mouse lemur, the first lower molar (m1) is squared and both the first and second upper molars (M1 and M2) have slight indentations around the middle of the posterior margin. The gray mouse lemur has a more elongated m1 and lacks the aforementioned indentation on M1 and M2.<ref name="2009Muldoon">Template:Cite journal</ref> In terms of its general dentition, the gray mouse lemur shares the same dental formula as all other members of its family, Cheirogaleidae: Template:DentalFormula<ref name="Mittermeier_1stEd">Template:LoM1</ref>
This species has 66 chromosomes,<ref name="PrimateAnatomy13">Template:Cite book</ref> closely resembling the karyotype of the dwarf lemurs (genus Cheirogaleus). Except for the X chromosome, all chromosomes are acrocentric (with the short arm absent or virtually absent).<ref name="2005Dutrillaux">Template:Cite journal</ref> Its genome size is 3.12 picograms (pg).<ref name="PrimateAnatomy13" />
EcologyEdit
Like all other members of the 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 forests, semi-humid deciduous, moist lowland forest, transitional forest, and secondary forests or degraded forests (including plantations) all ranging up to Template:Convert above sea level.<ref name="Mittermeier104-107" /><ref name="IUCN Lemurs" /><ref name="Garbutt" /> 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, lianas and dense foliage.<ref name="IUCN Lemurs" /><ref name="Garbutt" /><ref name="Sussman">Template:Cite book</ref> These lemurs are usually seen on branches less than Template:Convert in diameter.<ref name="Sussman" /> The gray mouse lemur tends to prefer lower levels of the forest and the understory, where branches and vegetation are dense.<ref name="Garbutt" />
In secondary forest, it is generally observed from ground level up to Template:Convert above ground, yet Template:Convert in the canopy of primary forest.<ref name="IUCN Lemurs" /><ref name="Sussman" /> Studies have found that the species can spend as much as 40% of its time below Template:Convert, 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.<ref name="Sussman" /> The species is more numerous in spiny forest, such as the Andohahela Special Reserve, than in the gallery forest, preferring drier, littoral forest, whereas the brown mouse lemur prefers inland rain forest.<ref name="IUCN Lemurs" />
The limits of the distribution are poorly understood. It is believed to range from the Onilahy River or Lake Tsimanampetsotsa in the south to Ankarafantsika National Park in the north.<ref name="Mittermeier104-107" /><ref name="Garbutt" /> There is also an isolated and disjointed population in the southeastern part of the island, near Tôlanaro and the Andohahela National Park, up to the Mandena Conservation Zone.<ref name="Mittermeier104-107" /><ref name="Garbutt" /> Individuals tend to occupy small home ranges of Template:Convert.<ref name="Garbutt" /> 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.<ref name="Mittermeier104-107" /> In Ankarafantsika National Park, where it coexists with the golden-brown mouse lemur, the gray mouse lemur's relative population density was highest at higher altitudes and in drier habitat, while the golden-brown mouse lemur preferred the opposite.<ref name="2009Rakotondravony">Template:Cite journal</ref> Another study has looked at the coexistence of the gray mouse lemur and Madame Berthe's mouse lemur and found small, exclusive clusters of each species and a high degree of feeding niche overlap.<ref name="2008Dammhahn">Template:Cite journal</ref>
The gray mouse lemur can reach high population densities up to several hundred individuals per square kilometer<ref name="IUCN Lemurs" /><ref name="Garbutt" /> (up to 167 individuals/km2 at Ankarafantsika National Park to 712 individuals/km2 at Kirindy Mitea National Park).<ref name="iucn status 19 November 2021" /> This abundance is not uniform and tends to concentrate in "population nuclei",<ref name="Garbutt" /> 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.<ref name="IUCN Lemurs" />
Mouse lemurs are omnivorous, and favor fruit and insects for the bulk of their diet. The gray mouse lemur may even come down to the ground to catch insect prey,<ref name="IUCN Lemurs" /> though it quickly returns to the protective cover of the understory to consume its catch.<ref name="Sussman" /> Nectar is also a part of the gray mouse lemur's diet, making it a potential pollinator for local plant species.<ref name="Garbutt" /> A single instance of a male cannibalizing an adult female is known.<ref name="2012Hämäläinen">Template:Cite journal
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PredationEdit
Template:Multiple image The most significant predators of the gray mouse lemur are the Madagascar owl and barn owl.<ref name="Mittermeier104-107" /><ref name="Sussman" /> Studies conducted in Beza Mahafaly Reserve and Kirindy Mitea National Park indicate a predation rate of around 25% (percent population taken by predators per year), the highest known for any primate species. However, given the species' high reproductive potential, predation does not appear to have a drastic effect on its populations.<ref name="Sussman" /> Other raptors, such as Henst's goshawk and other owls, also prey upon this species. Snakes, such as Ithycyphus miniatus (a native colubrid snake) and the Madagascar tree boa, as well as mammalian predators, such as the ring-tailed mongoose, narrow-striped mongoose, fossa, and domestic dogs are also known to prey on the gray mouse lemur.<ref name="Garbutt" /><ref name="Sussman" /> Mammalian predators often discover tree holes serving as nests, and enlarge the opening so they can catch and eat the occupant. This puts strong selective pressure on the choice of nest hole opening diameter and deepness.<ref name="Sussman" />
Due to its non-gregarious nature, the gray mouse lemur, like other nocturnal lemurs, primarily defends itself from predators using avoidance strategies,<ref name="Sussman" /> although group defense through the use of alarm calls and predator mobbing has been observed in this species.<ref name="2008Eberle">Template:Cite journal</ref> Studies involving the placement of predator and non-predator fecal odor with captive populations have demonstrated a genetic predisposition for predator recognition through the detection of metabolites from meat digestion. The mouse lemurs were shown to avoid locations where they typically received rewards, as well as exhibit increased activity and anti-predator behavior, when the odor of predator feces were present in that vicinity, but not when the fecal odor of Malagasy non-predators was present.<ref name="2008Sündermann">Template:Cite journal</ref>
During the day, when they are most vulnerable, individuals shelter inside tree holes, sometimes forming nests. They may use three to nine different tree holes within their home range, yet individuals may use one particular hole for up to five consecutive days.<ref name="Mittermeier104-107" /><ref name="Garbutt" /> Mouse lemurs tend to prefer tree hollows, but also commonly make spherical constructions out of leaves. Nests are usually found in tree holes with a minimum diameter of Template:Convert, with a median of Template:Convert, suggesting that this range in diameter of tree holes may be crucial for maintaining a healthy habitat.<ref name="IUCN Lemurs" /> The gray mouse lemur also spends most of its time in dense vegetation, limiting its visibility and accessibility to predators. Furthermore, it has a high reproductive rate to counter losses to predation.<ref name="Sussman" />
BehaviorEdit
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.<ref name="Garbutt" /> It usually forages alone at night, but may sleep in groups during the day, the composition of which depends on gender and season.<ref name="IUCN Lemurs" /> Tree holes can be shared with up to 15 other individuals,<ref name="Garbutt" /> although males tend to sleep alone while females tend to share nests.<ref name="Mittermeier104-107" />
All mouse lemurs are highly active at night,<ref name="Nowak" /> often scurrying like mice and leaping over Template:Convert,<ref name="Sussman" /> using the tail as a balancing organ.<ref name="Nowak" /> When moving among the terminal branches of bushes and trees, they grip using all four feet and move with four legs.<ref name="Nowak" /><ref name="Sussman" /> When on the ground, either to catch insects or cross short open areas, mouse lemurs hop like a frog.<ref name="Nowak" /> When hunting, the grey mouse lemur is known to catch invertebrates and small vertebrates with quick hand grasps.<ref name="Fleagle" />
In the dry season, the gray mouse lemur faces the challenge of exploiting sparsely distributed feeding resources efficiently. Results of a recent study on this showed that the gray mouse lemur does not move around randomly, but rather use spatial cues to find food resources in the absence of sensory cues, and that they seem to reuse common, highly efficient routes with regard to travel distance. It is believed that rather than using a route-based network, the gray mouse lemur has some sense of mental representation of their spatial environment, which they use to find and exploit food resources.<ref>Template:Cite journal</ref>
Foraging behavior is often slow, with height and direction changing continuously. Predation of insects occurs primarily on the ground.<ref name="IUCN Lemurs" /> Before descending, the ear pinnae 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.<ref name="Sussman" /> Studies with captive gray mouse lemurs have shown that vision is primarily used for prey detection, although the other senses certainly play a role in foraging.<ref name="2008Piep">Template:Cite journal</ref>
The gray mouse lemur is omnivorous,<ref name="Garbutt" /> feeding primarily on fruit and invertebrates.<ref name="IUCN Lemurs" /><ref name="Sussman" /> Local populations appear to specialize on locally available fruit. At both Marosalaza and Mandena, beetles are the primary insect prey, although moths, praying mantids, 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.<ref name="Sussman" /> 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.<ref name="Mittermeier104-107" /><ref name="IUCN Lemurs" /><ref name="Garbutt" /> Its diet is seasonally varied and diverse in content, giving it a very broad feeding niche compared to other species such as the Madame Berthe's mouse lemur. Therefore, it is affected more by food availability than by niche partitioning where sympatry occurs.<ref name="2008Dammhahn_01">Template:Cite journal</ref>
DormancyEdit
As with all members of the mouse lemur genus, the gray mouse lemur is known to enter short states of daily torpor, particularly during the cool, dry Southern Hemisphere winter.<ref name="Mittermeier91-128" /><ref name="NaturalHistory" /><ref name="Lemurs_Chap10">Template:Cite book</ref> This rare trait in primates,<ref name="2009Schmid">Template:Cite journal</ref> coupled with the ease of observing the species within its wide geographic distribution<ref name="Mittermeier104-107" /> and its good representation in captivity,<ref name="ISIS">{{#invoke:citation/CS1|citation |CitationClass=web }}</ref> makes it a popular subject for research as a model organism.
The gray mouse lemur is unique among the mouse lemurs studied so far because it is the only species to exhibit prolonged seasonal torpor, but this behavior has only been observed to occur in one locality.<ref name="Lemurs_Chap10" /> Activity patterns can differ noticeably between sexes as well as populations. At the Ampijoroa Forestry Station in Ankarafantsika National Park, males and females exhibit daily, rather than seasonal torpor.<ref name="Mittermeier104-107" /><ref name="NaturalHistory" /> 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. However, males 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.<ref name="Mittermeier104-107" /><ref name="Garbutt" /><ref name="NaturalHistory" /> The use of alternative energy-saving strategies under the same environmental conditions was observed directly in 2008, providing the first physiological confirmation from the field.<ref name="2009Schmid" /> This pattern of seasonal versus daily torpor may relate to the seasonality of the region,<ref name="Sussman" /> since Kirindy is the only location west of the eastern mountain rainforests that experiences very low temperatures at night during the winter months. By entering extended torpor, sometimes referred to as hibernation, this would reduce the thermoregulatory stress in females,<ref name="Lemurs_Chap10" /> whereas males remain more active in preparation for the upcoming mating season.<ref name="Mittermeier104-107" /> No difference in mortality has been shown between hibernating females and active males.<ref name="2008Kraus">Template:Cite journal</ref>
During torpor, the gray mouse lemur's metabolic rate slows and its body temperature drops to the ambient temperature, as low as Template:Convert. During the cooler months of May though August, the species selects tree holes closer to ground level, where ambient temperatures remain more stable. This allows them to remain in torpor longer, and to conserve metabolic resources.<ref name="Garbutt" /> One study showed that during the breeding season, both males and females reduced their energy expenditure by 20% when they nested in pairs, and a maximal energetic benefit of 40% was achieved when three mouse lemurs nested together. Even during the nonbreeding season, maximal energetic gain was observed two or more animals nested together, because resting metabolic rate was already decreased.<ref>Template:Cite journal</ref>
While the gray mouse lemur is found in both primary and secondary deciduous forests, they have lower population densities in secondary forests. This is because variations in gray mouse lemur abundance are linked to their capacity to enter torpor during the dry season, especially for females, which tend to hibernate longer than males. In primary forests, they can maintain daily torpor or hibernation as long as their body temperatures remain below Template:Convert, but in secondary forests that have fewer large trees, temperatures are higher and inhibit the gray mouse lemur's ability to maintain torpor for prolonged periods of time. In addition, the gray mouse lemur in secondary forests tend to have a lower body mass than those in primary forests, as well as lower survival rates. This is likely because those with lower body mass are less likely to enter torpor, and therefore expend around 40% more energy than those that do maintain torpor.<ref>Template:Cite journal</ref>
This unusual ability for a primate to exhibit dormancy, in addition to the diminutive size, has led researchers to speculate that ancestral lemurs, and possibly ancestral primates, may have shared some traits with mouse lemurs. Consequently, the gray mouse lemur has once again been used as a model organism for studying lemur and primate evolution.<ref name="Lemurs_Chap10" /> For example, lemurs are thought to have colonized Madagascar by rafting to the island around 60 million years ago according to molecular phylogenetic studies.<ref name="Mittermeier23-26">Mittermeier, R.A.; et al. (2006) "Chapter 1: Origin of the lemurs", pp. 23–26</ref><ref name="2004YoderYang">Template:Cite journal</ref> Before the discovery that ocean currents were the opposite of what they are today, thus favoring such an event,<ref name="2010AliHuber">Template:Cite journal
- Template:Cite press release</ref> it was thought that it would have taken too long for any animal not capable of entering a state of dormancy to survive the trip. Therefore, the mouse lemurs, such as the gray mouse lemur, were thought to have shared this plesiomorphic (ancestral) trait with the ancestral lemurs.<ref name="Lemurs_Chap10" />
Social systemsEdit
The gray mouse lemur is described as solitary but social,<ref name="Sussman" /> foraging alone at night, but frequently sleeping in groups during the day.<ref name="IUCN Lemurs" /><ref name="Garbutt" /> This social pattern 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.<ref name="Mittermeier104-107" /><ref name="IUCN Lemurs" /><ref name="Garbutt" /> 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.<ref name="Nowak" /> During the breeding season (September through October), males and females may sleep in the same tree hole.<ref name="Garbutt" /><ref name="Nowak" /> 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.<ref name="IUCN Lemurs" />
Research has shown that home ranges for the gray mouse lemur are usually small, possibly less than Template:Convert.<ref name="IUCN Lemurs" /> Males typically travel further at night and have home ranges that are twice as large as those of females,<ref name="Mittermeier104-107" /><ref name="IUCN Lemurs" /> often overlapping with one another, and always overlapping with at least one female's home range.<ref name="Garbutt" /><ref name="Nowak" /> Male home ranges increase threefold during the breeding season.<ref name="Mittermeier104-107" /><ref name="Garbutt" />
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.<ref name="IUCN Lemurs" /> Genetic studies indicate that females arrange themselves spatially in clusters ("population nuclei") of related individuals, while males tend to emigrate from their natal group.<ref name="Mittermeier104-107" /> Research has shown that females in this species may maintain smaller ranges and associate more closely with other females than in some other mouse lemur species due to a more opportunistic feeding niche and, in the case of populations at Kirindy, the use of extended, seasonal torpor.<ref name="2009Dammhahn">Template:Cite journal</ref>
CommunicationEdit
{{#invoke:Listen|main}} Vocalizations and scent are the primarily modes of communication within this species. Home ranges are scent marked with urine and feces.<ref name="Nowak" /> 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).<ref name="Nowak" /><ref name="EncycMammals">Template:Cite encyclopedia</ref> These include calls for seeking contact, mating, distant communication, alarm, and distress.<ref name="Nowak" />
Like other mouse lemurs, the gray mouse lemur uses what has been described as a harmonic whistle call that is lower in frequency and shorter in duration than its close relative, the brown mouse lemur. In addition, it has been found that the types of vocalizations emitted by the gray mouse lemur can be dependent upon the environment. In the more open dry forest habitats favored by the gray mouse lemur, trill calls are more common and effective since they carry faster and are less likely to be masked by the wind, while chirp calls are more common in the brown mouse lemur, which favors closed rain forest habitats.<ref>Template:Cite journal</ref>
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 much like a bird song in terms of its ordered sequence of broadband frequency modulated syllables, ranging between 13 and 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.<ref name="EncycMammals" />
Because mouse lemurs are cryptic species, and therefore visually indistinguishable, their social calls help individuals select mates of their own species. This differentiated signaling and recognition system has promoted species cohesiveness through premating isolation, and helped researchers distinguish and identify species.<ref name="2008Braune p19">Template:Cite journal</ref>
Breeding and reproductionEdit
The mating system is described as multi-male and 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.<ref name="Sussman" /> During the breeding season, male testes increase significantly in size,<ref name="Mittermeier104-107" /> facilitating sperm competition due to female promiscuity. Studies with the gray mouse lemur have shown that the optimal insemination period, during which a male is most likely to sire offspring, occurs early during a female's receptivity.<ref name="2007Eberle">Template:Cite journal</ref> Only during the mating season does male mortality rise above that of female mortality.<ref name="2008Kraus" />
Although the gray mouse lemur displays multi-male, multi-female mating patterns, studies have shown that females do exhibit indirect mate selection (a form of selected polyandry). During the study, females would mate with 1–7 males up to 11 times during their single night of receptivity, but would avoid or counteract males that attempted to monopolize mating. Dominant males that attempt to monopolize tend to be larger and heavier individuals. Female selection however, has been shown to help increase genetic diversity among offspring.<ref>Template:Cite journal</ref>
The gray mouse lemur is considered overall sexually monomorphic, but seasonally fluctuating sexual dimorphism in terms of body mass has been recorded. While the body mass of both sexes fluctuates over the year as a function of food availability, being highest in the rainy season, the differing behavioral repertoires of the sexes lead to sex-specific patterns in this fluctuation. For example, male body mass increases prior to the mating season due to a substantial increase in testes volume that likely enhances the males' success in sperm competition.<ref>Template:Cite journal</ref><ref>Template:Cite journal</ref>
The females are receptive for 45 to 55 days between September and October, with estrus lasting 1 to 5 days.<ref name="Mittermeier104-107" /><ref name="Garbutt" /><ref name="Nowak" /> Females advertise estrus by distinctive high-frequency calls and scent-marking.<ref name="Garbutt" /> Gestation lasts 54 to 68 days,<ref name="Nowak" /> averaging 60 days, typically resulting in 2 or 3 offspring weighing Template:Convert each.<ref name="Mittermeier104-107" /><ref name="IUCN Lemurs" /><ref name="Garbutt" /><ref name="Nowak" /> Infants are born in a leaf nest or tree hole in November prior to the onset of the rainy season.<ref name="Garbutt" /> Weaning occurs after 25 days,<ref name="Nowak" /> and the infants are either left in the nest or carried in the mother's mouth and deposited on a branch while she forages.<ref name="Garbutt" /><ref name="Sussman" /> Infant mouse lemurs do not cling to the mother's fur. Independence is attained in 2 months,<ref name="IUCN Lemurs" /><ref name="Garbutt" /> while sexual maturity is reached at 10 to 29 months in females and 7 to 19 months in males.<ref name="IUCN Lemurs" /><ref name="Nowak" /> 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,<ref name="Garbutt" /> although captive specimens have reportedly lived as long as 15 years and 5 months,<ref name="Nowak" /> or even as long as 18.2 years.<ref>Template:Cite book</ref>
The gray mouse lemur uses cooperative breeding as a form of family insurance. The female regularly transfers her offspring to other females' nests—and likewise grooms and cares for offspring other than her own. While this can have a high physiological cost on a lactating female that is already expending a lot of energy, it can be beneficial overall to insuring survival among closely related groups with high mortality risk. A study that took place over three breeding seasons showed that closely related females form breeding groups mainly when there is a shortage of suitable roosts; when there is an advantage of a communal nest for defense, or when there are thermoregulatory benefits. In the event of offspring adoption, when a parent dies and a closely related female takes over care, it is believed that this is beneficial to groups with high mortality risk.<ref>Template:Cite journal</ref>
Conservation statusEdit
The gray mouse lemur was listed in Appendix 1 by the Convention on International Trade in Endangered Species (CITES) in 1975,<ref name="CITES_old">{{#invoke:citation/CS1|citation |CitationClass=web }}Template:Dead link</ref> declaring it as threatened with extinction and prohibiting international trade of specimens except for non-commercial use, such as scientific research.<ref name=CITES>{{#invoke:citation/CS1|citation |CitationClass=web }}</ref> 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.<ref name="iucn status 19 November 2021" />
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.<ref name="iucn status 19 November 2021" /><ref name="Mittermeier104-107" /> One study found nine species of parasites in the fecal matter of the gray mouse lemur living in forests that suffered degradation and fragmentation. In small fragments of good quality forest, as well as forests with high levels of degradation, the gray mouse lemur showed a higher prevalence of parasitic nematodes and protozoans than those in larger good quality forest fragments.<ref>Template:Cite journal</ref> Studies in the late 1960s and 1970s 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).<ref name="IUCN Lemurs" /> There is also a concern that although daily torpor can help conserve energy and resources during moderate food shortages, extended food shortages brought about by climate change could create too much stress and severely impact the survivability of the species.<ref name="2010Giroud">Template:Cite journal</ref><ref name="2008Giroud">Template:Cite journal</ref>
The gray mouse lemur is considered one of Madagascar's most abundant small native mammals, found in seven national parks, five special reserves, the Berenty Private Reserve, and other privately protected forests within the Mandena Conservation Zone.<ref name="Mittermeier104-107" />
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.<ref name="IUCN Lemurs" /> In March 2009, 167 were registered at 29 ISIS institutions, including the Duke Lemur Center.<ref name="iucn status 19 November 2021" /><ref name="ISIS" />
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