Lemur

Clade of primates endemic to the island of Madagascar

For other uses, see Lemur (disambiguation).

"Lemurs of Madagascar" redirects here. For the book, see Lemurs of Madagascar (book).

Lemurs Temporal range: Pleistocene–Present[1][2] PreꞒ Ꞓ O S D C P T J K Pg N ↓
A sample of lemur diversity; 8 of 1500 biological genera are depicted (from top, left to right): Lemur, Propithecus, Daubentonia, †Archaeoindris, Microcebus, Lepilemur, Eulemur, Varecia.
Scientific classification
Kingdom:	Animalia
Phylum:	Chordata
Class:	Mammalia
Order:	Primates
Suborder:	Strepsirrhini
Infraorder:	Lemuriformes
Superfamily:	Lemuroidea Gray 1821
Families
† Archaeolemuridae Cheirogaleidae Daubentoniidae Indriidae Lemuridae Lepilemuridae † Megaladapidae † Palaeopropithecidae
Diversity
About 100 living species
Range of all lemur species[3]

Lemurs (

are active at night

.

Lemurs share resemblance with other

species concept

is used.

Lemurs range in weight from the 30-gram (1.1 oz)

female social dominance

. Most eat a wide variety of fruits and leaves, while some are specialists. Two species of lemurs may coexist in the same forest due to different diets.

Lemur research during the 18th and 19th centuries focused on taxonomy and specimen collection. Modern studies of lemur ecology and behavior did not begin in earnest until the 1950s and 1960s. Initially hindered by political issues on Madagascar during the mid-1970s, field studies resumed in the 1980s. Lemurs are important for research because their mix of ancestral characteristics and traits shared with anthropoid primates can yield insights on primate and human evolution. Many lemur species remain endangered due to habitat loss and hunting. Many lemur species have already gone extinct in the last 2000 years due to human activity, and are collectively referred to as the "subfossil lemurs". These are typically larger than extant lemurs, with the largest, Archaeoindris, being the size of a gorilla. Although local traditions, such as fady, generally help protect lemurs and their forests, illegal logging, economic privation and political instability conspire to thwart conservation efforts. Because of these threats and their declining numbers, the International Union for Conservation of Nature (IUCN) considers lemurs to be the world's most endangered mammals, noting that as of 2013^[update] up to 90% of all lemur species confront the threat of extinction in the wild within the next 20 to 25 years. As an iconic flagship species that exemplifies the biodiverse fauna of Madagascar, however, lemurs have facilitated the emergence of eco-tourism in Madagascar in World Heritage Sites, such as the Rainforests of the Atsinanana in eastern Madagascar. In addition, conservation organizations, such as the Lemur Conservation Foundation and the Duke Lemur Center, increasingly seek to implement community-based approaches, such as encouraging local communities to adopt sustainable agriculture and afforestation initiatives, to expand employment opportunities for ecological programs, preserve lemur habitats as well as promote public awareness and appreciation for lemurs.

Etymology

The name lemur is derived from the Latin lemures,^[5] which refers to specters or ghosts that were exorcised during the Lemuria festival of ancient Rome.^[6][7]

Carl Linnaeus, the founder of modern binomial nomenclature, gave lemurs their name as early as 1758, when he used it in the 10th edition of Systema Naturae. He included three species under the genus Lemur: Lemur tardigradus (the red slender loris, now known as Loris tardigradus), Lemur catta (the ring-tailed lemur), and Lemur volans (the Philippine colugo, now known as Cynocephalus volans).^[8]

Lemures dixi hos, quod noctu imprimis obambulant, hominibus quodanmodo similes, & lento passu vagantur.
[I call them lemurs, because they go around mainly by night, in a certain way similar to humans, and roam with a slow pace.]

Linnaeus, Museum Adolphi Friderici Regis^[9]
in reference to the red slender loris^[10]

Although the term "lemur" was first intended for

nocturnal activity and slow movements of the slender loris.^[10] Being familiar with the works of Virgil and Ovid and seeing an analogy that fit with his naming scheme, Linnaeus adapted the term "lemur" for these nocturnal primates.^[12]

It was noted in 2012 that it has been commonly and falsely assumed that Linnaeus was referring to the ghost-like appearance, reflective eyes, and ghostly cries of lemurs.^[10] It has also been speculated that Linnaeus may also have known that some Malagasy people have held legends that lemurs are the souls of their ancestors,^[13] but this is unlikely given that the name was selected for slender lorises from India.^[10]

Evolutionary history

Main article: Evolution of lemurs

Lemurs are primates belonging to the suborder

subfossils dating to the Late Pleistocene.^[2]

Once part of the supercontinent

rafting events, where very small populations rafted from nearby Africa on tangled mats of vegetation, which get flushed out to sea from major rivers.^[23] This form of biological dispersal can occur randomly over millions of years.^[18][24] In the 1940s, American paleontologist George Gaylord Simpson coined the term "sweepstakes hypothesis" for such random events.^[25] Rafting has since been the most accepted explanation for the lemur colonization of Madagascar,^[26][27] but until recently this trip was thought to be very unlikely because strong ocean currents flow away from the island.^[28] In January 2010, a report demonstrated that around 60 mya both Madagascar and Africa were 1,650 km (1,030 mi) south of their present-day positions, placing them in a different ocean gyre, producing currents that ran counter to what they are today. The ocean currents were shown to be even stronger than today, which would have pushed a raft along faster, shortening the trip to 30 days or less—short enough for a small mammal to survive easily. As the continental plates drifted northward, the currents gradually changed, and by 20 mya the window for oceanic dispersal had closed, effectively isolating the lemurs and the rest of the terrestrial Malagasy fauna from mainland Africa.^[28] Isolated on Madagascar with only a limited number of mammalian competitors, the lemurs did not have to compete with other evolving arboreal mammalian groups, such as squirrels.^[29] They were also spared from having to compete with monkeys, which evolved later. The intelligence, aggression, and deceptiveness of monkeys gave them an advantage over other primates in exploiting the environment.^[5][30]

Distribution and diversity

See also: Subfossil lemur

A life restoration of Babakotia radofilai, a sloth lemur

that became extinct less than two thousand years ago

Lemurs have

Archaeoindris fontoynonti,^[32] lemurs evolved diverse forms of locomotion, varying levels of social complexity, and unique adaptations to the local climate.^[17][33]

Lemurs lack any shared traits that make them stand out from all other primates.

female social dominance, sexual monomorphism, and male–male competition for mates involving low levels of agonism, such as sperm competition.^[35]

Before the arrival of humans roughly 1500 to 2000 years ago, lemurs were found all across the island.

precipitation and is highest in the rainforests of the east coast.^[2] Despite their adaptations for weathering extreme adversity, habitat destruction and hunting have resulted in lemur populations declining sharply, and their diversity has diminished, with the recent extinction of at least 17 species in eight genera,^[29][32][37] known collectively as the subfossil lemurs. Most of the approximately 100 species and subspecies of lemur are either threatened or endangered. Unless trends change, extinctions are likely to continue.^[38]

Until recently, giant lemurs existed on Madagascar. Now represented only by recent or subfossil remains, they were modern forms that were once part of the rich lemur diversity that has evolved in isolation. Some of their adaptations were unlike those seen in their living relatives.[29] All 17 extinct lemurs were larger than the extant (living) forms, some weighing as much as 200 kg (440 lb),^[5] and are thought to have been active during the day.^[39] Not only were they unlike the living lemurs in both size and appearance, they also filled ecological niches that either no longer exist or are now left unoccupied.^[29] Large parts of Madagascar, which are now devoid of forests and lemurs, once hosted diverse primate communities that included more than 20 lemur species covering the full range of lemur sizes.^[40]

Taxonomic classification and phylogeny

Competing lemur phylogenies

Lemuroidea  Daubentoniidae Indriidae Lepilemuridae Cheirogaleidae Lemuridae

Lemuroidea  Daubentoniidae Lepilemuridae Cheirogaleidae Lemuridae † Megaladapidae Indriidae †Palaeopropithecidae †Archaeolemuridae

There are two competing lemur phylogenies, one by Horvath et al. (top)[41] and one by Orlando et al. (bottom).[42] Note that Horvath et al. did not attempt to place the subfossil lemurs.

Main article: Taxonomy of lemurs

For a more comprehensive list, see List of lemur species.

From a taxonomic standpoint, the term "lemur" originally referred to the genus Lemur, which currently contains only the ring-tailed lemur. The term is now used in the colloquial sense in reference to all Malagasy primates.^[43]

Lemur taxonomy is controversial, and not all experts agree, particularly with the recent increase in the number of recognized species.^[34][44][45] According to Russell Mittermeier, the president of Conservation International (CI), taxonomist Colin Groves, and others, there are nearly 100 recognized species or subspecies of extant (or living) lemur, divided into five families and 15 genera.^[46] Because genetic data indicates that the recently extinct subfossil lemurs were closely related to living lemurs,^[47] an additional three families, eight genera, and 17 species can be included in the total.^[32][37] In contrast, other experts have labeled this as taxonomic inflation,^[45] instead preferring a total closer to 50 species.^[34]

The classification of lemurs within the suborder Strepsirrhini is equally controversial, although most experts agree on the same phylogenetic tree. In one taxonomy, the infraorder Lemuriformes contains all living strepsirrhines in two superfamilies, Lemuroidea for all lemurs and Lorisoidea for the lorisoids (lorisids and galagos).^[1][48] Alternatively, the lorisoids are sometimes placed in their own infraorder, Lorisiformes, separate from the lemurs.^[49] In another taxonomy published by Colin Groves, the aye-aye was placed in its own infraorder, Chiromyiformes, while the rest of the lemurs were placed in Lemuriformes and the lorisoids in Lorisiformes.^[50]

Although it is generally agreed that the aye-aye is the most basal member of the lemur clade, the relationship between the other four families is less clear since they diverged during a narrow 10 to 12 million-year window between the Late Eocene (42 mya) and into the Oligocene (30 mya).^[20][26] The two main competing hypotheses are shown in the adjacent image.

Competing taxonomic nomenclature for lemurs and their kin

2 infraorders[48]	3 infraorders[49]	4 infraorders[50]
Order Primates Suborder Strepsirrhini Infraorder †Adapiformes Infraorder Lemuriformes Superfamily Lemuroidea Family †Archaeolemuridae Family Cheirogaleidae Family Daubentoniidae Family Indriidae Family Lemuridae Family Lepilemuridae Family †Megaladapidae Family †Palaeopropithecidae Superfamily Lorisoidea Suborder Haplorhini	Order Primates Suborder Strepsirrhini Infraorder †Adapiformes Infraorder Lemuriformes Superfamily Lemuroidea Family †Archaeolemuridae Family Cheirogaleidae Family Daubentoniidae Family Indriidae Family Lemuridae Family Lepilemuridae Family †Megaladapidae Family †Palaeopropithecidae Infraorder Lorisiformes Suborder Haplorhini	Order Primates Suborder Strepsirrhini Infraorder †Adapiformes Infraorder Chiromyiformes Infraorder Lemuriformes Superfamily Cheirogaleoidea Family Cheirogaleidae Superfamily Lemuroidea Family †Archaeolemuridae Family Indriidae Family Lemuridae Family Lepilemuridae Family †Megaladapidae Family †Palaeopropithecidae Infraorder Lorisiformes Suborder Haplorhini

The Sahamalaza sportive lemur

(Lepilemur sahamalazensis) was identified as a distinct species in 2006.

Lemur taxonomy has changed significantly since the first taxonomic classification of lemurs by Carl Linnaeus in 1758. One of the greatest challenges has been the classification of the aye-aye, which has been a topic of debate up until very recently.[5] Until Richard Owen published a definitive anatomical study in 1866, early naturalists were uncertain whether the aye-aye (genus Daubentonia) was a primate, rodent, or marsupial.^[51][52][53] However, the placement of the aye-aye within the order Primates remained problematic until very recently. Based on its anatomy, researchers have found support for classifying the genus Daubentonia as a specialized indriid, a sister group to all strepsirrhines, and as an indeterminate taxon within the order Primates.^[19] Molecular tests have now shown Daubentoniidae is basal to all Lemuriformes,^[19][54] and in 2008, Russell Mittermeier, Colin Groves, and others ignored addressing higher-level taxonomy by defining lemurs as monophyletic and containing five living families, including Daubentoniidae.^[46]

Relationships among lemur families have also proven to be problematic and have yet to be definitively resolved.

koala lemurs (Megaladapidae). Formerly grouped in the same family due to similarities in dentition,^[57] they are no longer considered to be closely related due to genetic studies.^[56][58]

More taxonomic changes have occurred at the genus level, although these revisions have proven more conclusive, often supported by genetic and molecular analysis. The most noticeable revisions included the gradual split of a broadly defined genus Lemur into separate genera for the ring-tailed lemur, ruffed lemurs, and brown lemurs due to a host of morphological differences.^[59][60]

Due to several taxonomic revisions by Russell Mittermeier, Colin Groves, and others, the number of recognized lemur species has grown from 33 species and subspecies in 1994 to approximately 100 in 2008.

cryptic species such as mouse lemurs, the number of recognized lemur species is likely to keep growing.^[34] However, the rapid increase in the number of recognized species has had its critics among taxonomists and lemur researchers. Since classifications ultimately depend on the species concept used, conservationists often favor definitions that result in the splitting of genetically distinct populations into separate species to gain added environmental protection. Others favor a more thorough analysis.^[34][45]

Anatomy and physiology

Lemurs vary greatly in size. They include the smallest primates in the world and, until recently, also included some of the largest. They currently range in size from about 30 g (1.1 oz) for

Archaeoindris fontoynonti.^[5][32]

toilet-claw

on the second toe and nails on all other toes

A six-tooth version of the strepsirrhine toothcomb in a ring-tailed lemur

, with canine-like premolars behind it

Only the aye-aye, the extinct giant aye-aye, and the largest of the extinct giant sloth lemurs lack a functional strepsirrhine toothcomb.^[78][76] In the case of the aye-aye, the morphology of the deciduous incisors, which are lost shortly after birth, indicates that its ancestors had a toothcomb. These milk teeth are lost shortly after birth^[82] and are replaced by open-rooted, continually growing (hypselodont) incisors.^[78]

The toothcomb in lemurs normally consists of six teeth (four incisors and two canines), although indriids, monkey lemurs, and some sloth lemurs only have a four-tooth toothcomb due to the loss of either a canine or an incisor.^[18][78] Because the lower canine is either included in the toothcomb or lost, the lower dentition can be difficult to read, especially since the first premolar (P2) is often shaped like a canine (caniniform) to fill the canine's role.^[57] In folivorous (leaf-eating) lemurs, except for indriids, the upper incisors are greatly reduced or absent.^[57][78] Used together with the toothcomb on the mandible (lower jaw), this complex is reminiscent of an ungulate browsing pad.^[78]

Lemurs are unusual among primates for their rapid dental development, particularly among the largest species. For example, indriids have relatively slow body growth but extremely fast tooth formation and

Lemurs generally have a wet nose, or rhinarium

, as well as a longer snout than anthropoid primates.

The wet nose, or rhinarium, is a trait shared with other strepsirrhines and many other mammals, but not with haplorrhine primates.^[52] Although it is claimed to enhance the sense of smell,^[65] it is actually a touch-based sense organ that connects with a well-developed vomeronasal organ (VNO). Since pheromones are usually large, non-volatile molecules, the rhinarium is used to touch a scent-marked object and transfer the pheromone molecules down the philtrum (the nasal mid-line cleft) to the VNO via the nasopalatine ducts that travel through the incisive foramen of the hard palate.^[16]

To communicate with smell, which is useful at night, lemurs will

Since cone cells make color vision possible, the high prevalence of rod cells in lemur eyes suggest they have not evolved color vision.^[16] The most studied lemur, the ring-tailed lemur, has been shown to have blue-yellow vision, but lacks the ability to distinguish red and green hues.^[90] Due to polymorphism in opsin genes, which code for color receptivity, trichromatic vision may rarely occur in females of a few lemur species, such as Coquerel's sifaka (Propithecus coquereli) and the red ruffed lemur (Varecia rubra). Most lemurs, therefore, are either monochromats or dichromats.^[16]

Aye-ayes exhibit eyeshine because they have a reflective layer of tissue in the eye, called a tapetum lucidum

.

Most lemurs have retained the tapetum lucidum, a reflective layer of tissue in the eye, which is found in many vertebrates.^[43] This trait is absent in haplorrhine primates, and its presence further limits the visual acuity in lemurs.^[33][89] The strepsirrhine choroidal tapetum is unique among mammals because it is made up of crystalline riboflavin, and the resulting optical scattering is what limits visual acuity.^[89] Although the tapetum is considered to be ubiquitous in lemurs, there appear to be exceptions among true lemurs, such as the black lemur and the common brown lemur, as well as the ruffed lemurs.^[16][33][89] Since the riboflavins in the tapetum have a tendency to dissolve and vanish when processed for histological investigation, however, the exceptions are still debatable.^[16]

Lemurs also have a third eyelid known as a

Lemurs have low basal metabolic rates (BMR), which helps them to conserve energy during the dry season, when water and food are scarce.^[2][68] They can optimize their energy use by lowering their metabolic rate to 20% below the values predicted for mammals of similar body mass.^[93] The red-tailed sportive lemur (Lepilemur ruficaudatus), for instance, reportedly has one of the lowest metabolic rates among mammals. Its low metabolic rate may be linked to its generally folivorous diet and relatively small body mass.^[68] Lemurs exhibit behavioral adaptations to complement this trait, including sunning behaviors, hunched sitting, group huddling, and nest sharing, in order to reduce heat loss and conserve energy.^[93] Dwarf lemurs and mouse lemurs exhibit seasonal cycles of dormancy to conserve energy.^[93] Before dry season, they will accumulate fat in white adipose tissue located at the base of the tail and hind legs, doubling their weight.^[31][94][95] At the end of the dry season, their body mass may fall to half of what it was prior to the dry season.^[31] Lemurs that do not experience states of dormancy are also able to shut down aspects of their metabolism for energy conservation.^[93]

Behaviour

Lemur behaviour is as variable as lemur morphology. Differences in diet, social systems, activity patterns, locomotion, communication, predator avoidance tactics, breeding systems, and intelligence levels help define lemur taxa and set individual species apart from the rest. Although trends frequently distinguish the smaller, nocturnal lemurs from the larger, diurnal lemurs, there are often exceptions that help exemplify the unique and diverse nature of these Malagasy primates.

Diet

Mouse lemurs

primarily eat fruit, although their diet also includes insects.

Lemur diets are highly variable and demonstrate a high degree of plasticity,[96] although general trends suggest that the smallest species primarily consume fruit and insects (omnivory), while the larger species are more herbivorous, consuming mostly plant material.^[39] As with all primates, hungry lemurs might eat anything that is edible, whether or not the item is one of their preferred foods.^[16] For instance, the ring-tailed lemur eats insects and small vertebrates when necessary^[39][59] and as a result it is commonly viewed as an opportunistic omnivore.^[78] Coquerel's giant mouse lemur (Mirza coquereli) is mostly frugivorous, but will consume insect secretions during the dry season.^[39]

A common assumption in mammalogy is that small mammals cannot subsist entirely on plant material and must have a high-calorie diet in order to survive. As a result, it was thought that the diet of tiny primates must be high in protein-containing insects (insectivory). Research has shown, however, that mouse lemurs, the smallest living primates, consume more fruit than insects, contradicting the popular hypothesis.^[16][39]

Plant material makes up the majority of most lemur diets. Members of at least 109 of all known plant families in Madagascar (55%) are exploited by lemurs. Since lemurs are primarily arboreal, most of these exploited species are woody plants, including trees, shrubs, or lianas. Only the ring-tailed lemur, the bamboo lemurs (genus Hapalemur), and the black-and-white ruffed lemur (Varecia variegata) are known to consume herbs. While Madagascar is rich in fern diversity, these plants are rarely eaten by lemurs. One possible reason for this is that ferns lack flowers, fruits, and seeds—common food items in lemur diets. They also occur close to the ground, while lemurs spend most of their time in the trees. Lastly, ferns have an unpleasant taste due to the high content of tannins in their fronds. Likewise, mangroves appear to be rarely exploited by lemurs due to their high tannin content.^[96] Some lemurs appear to have evolved responses against common plant defenses, however, such as tannins and alkaloids.^[79] The golden bamboo lemur (Hapalemur aureus), for instance, eats giant bamboo (Cathariostachys madagascariensis), which contains high levels of cyanide. This lemur can consume twelve times the typically lethal dose for most mammals on a daily basis; the physiological mechanisms that protect it from cyanide poisoning are unknown.^[2] At the Duke Lemur Center (DLC) in the United States, lemurs that roam the outdoor enclosures have been observed eating poison ivy (Taxicodendron radicans), yet have shown no ill effects.^[64]

Up to 95% of the greater bamboo lemur's diet consists of bamboo.^[59]

Many of the larger lemur species consume leaves (folivory),^[96] particularly the indriids.^[66] However, some smaller lemurs such as sportive lemurs (genus Lepilemur) and woolly lemurs (genus Avahi) also primarily eat leaves, making them the smallest primates that do so.^[68] The smallest of the lemurs generally do not eat much leaf matter.^[96] Collectively, lemurs have been documented consuming leaves from at least 82 native plant families and 15 alien plant families. Lemurs tend to be selective in their consumption of the part of the leaf or shoot as well as its age. Often, young leaves are preferred over mature leaves.^[96]

Many lemurs that eat leaves tend to do so during times of fruit scarcity, sometimes suffering weight loss as a result.^[97] Most lemur species, including most of the smallest lemurs and excluding some of the indriids, predominantly eat fruit (frugivory) when available. Collectively, lemurs have been documented consuming fruit from at least 86 native plant families and 15 alien plant families. As with most tropical fruit eaters, the lemur diet is dominated by fruit from Ficus (fig) species.^[96] In many anthropoid primates, fruit is a primary source of vitamin C, but unlike anthropoid primates, lemurs (and all strepsirrhines) can synthesize their own vitamin C.^[98] Historically, captive lemur diets high in vitamin C-rich fruits have been thought to cause hemosiderosis, a type of iron overload disorder, since vitamin C increases iron absorption. Although lemurs in captivity have been shown to be prone to hemosiderosis, the frequency of the disease varies across institutions and may depend on the diet, husbandry protocols, and genetic stock. Assumptions about the problem need to be tested separately for each species.^[99] The ring-tailed lemur, for instance, seems to be less prone to the disorder than other lemur species.^[100]

Only eight species of lemur are known to be seed predators (granivores), but this may be under-reported since most observations only report fruit consumption and do not investigate whether the seeds are consumed as well. These lemurs include some indriids, such as the diademed sifaka (Propithecus diadema), the golden-crowned sifaka (Propithecus tattersalli), the indri,^[2][70] and the aye-aye. The aye-aye, which specializes in structurally defended resources, can chew through Canarium seeds, which are harder than the seeds that New World monkeys are known to break open.^[51] At least 36 genera from 23 families of plants are targeted by lemur seed predators.^[96]

Inflorescences (clusters of flowers) of at least 60 plant families are eaten by lemurs ranging in size from the tiny mouse lemurs to the relatively large ruffed lemurs. If the flowers are not exploited, sometimes the nectar is consumed (nectarivory) along with the pollen (palynivory). At least 24 native species from 17 plant families are targeted for nectar or pollen consumption.^[96]

Bark and plant exudates such as

Dwarf lemurs

are solitary but social, foraging alone but often sleeping in groups.

Social grooming serves many functions for social lemurs.

There have been many hypotheses that have attempted to explain why lemurs exhibit female social dominance while other primates with similar social structures do not,[2]^[103] but no consensus has been reached after decades of research. The dominant view in the literature states that female dominance is an advantageous trait given the high costs of reproduction and the scarcity of resources available.^[103] Indeed, female dominance has been shown to be linked to increased maternal investment.^[104] However, when reproductive costs and extreme seasonality of resources were compared across primates, other primates demonstrated male dominance under conditions that were similar to or more challenging than those faced by lemurs. In 2008, a new hypothesis revised this model using simple game theory. It was argued that when two individuals were equally matched in fighting capacity, the one with the most need would win the conflict since it would have the most to lose. Consequently, the female, with higher resource needs for pregnancy, lactation, and maternal care, was more likely to win in resource conflicts with equally sized males. This, however, assumed monomorphism between sexes.^[103] The following year, a new hypothesis was proposed to explain monomorphism, stating that because most female lemurs are only sexually receptive for a day or two each year, males can utilize a more passive form of mate guarding: copulatory plugs, which block the female reproductive tract, preventing other males from successfully mating with her, and thus reducing the need for aggression and the evolutionary drive for sexual dimorphism.^[35]

In general, levels of agonism (or aggression) tend to correlate with relative canine height. The ring-tailed lemur has long, sharp upper canine teeth in both sexes, and it also exhibits high levels of agonism. The Indri, on the other hand, has smaller canines and exhibits lower levels of aggression.^[33] When neighboring groups of the same species defend their territories, the conflict can take the form of ritualized defense. In sifakas, these ritualized combats involve staring, growling, scent-marking, and leaping to occupy certain sections of the tree. The indri defends its home range with ritualized "singing" battles.^[2]

Like other primates, lemurs groom socially (allogroom) to ease tensions and solidify relationships. They groom in greeting, when waking up, when settling in for sleep, between mother and infant, in juvenile relations, and for sexual advances.^[107] Unlike anthropoid primates, who part the fur with the hands and pick out particles with the fingers or mouth, lemurs groom with their tongue and scraping with their toothcomb.^[2][107] Despite the differences in technique, lemurs groom with the same frequency and for the same reasons as anthropoids.^[107]

Activity patterns

The

In order to conserve energy and water in their highly seasonal environment,[93]^[110] mouse lemurs and dwarf lemurs exhibit seasonal behavioral cycles of dormancy where the metabolic rate and body temperature are lowered. They are the only primates known to do so.^[93] They accumulate fat reserves in their hind legs and the base of their tail before the dry winter season, when food and water are scarce,^[31][94] and can exhibit daily and prolonged torpor during the dry season. Daily torpor constitutes less than 24 hours of dormancy, whereas prolonged torpor averages two weeks in duration and signals hibernation.^[93] Mouse lemurs have been observed experiencing torpor that lasts for several consecutive days, but dwarf lemurs are known to hibernate for six to eight months every year,^[29][31][95] particularly on the west coast of Madagascar.^[110]

Dwarf lemurs are the only primates known to hibernate for extended periods.

Other lemurs that do not exhibit dormancy conserve energy by selecting thermoregulated microhabitats (such as tree holes), sharing nests, and reducing exposed body surfaces, such as by hunched sitting and group huddling. Also, the ring-tailed lemur, ruffed lemurs, and sifakas are commonly seen sunning, thus using solar radiation to warm their bodies instead of metabolic heat.^[93]

Locomotion

Sifakas

are specially adapted to vertical clinging and leaping, so they must hop sideways to move on the ground.

Lemurs use scent-marking to communicate. Pictured is a red-bellied lemur

rubbing its rump against some smaller branches.

Compared to other mammals, primates in general are very vocal, and lemurs are no exception.[16] Some lemur species have extensive vocal repertoires, including the ring-tailed lemur and ruffed lemurs.^[90][118] Some of the most common calls among lemurs are predator alarm calls. Lemurs not only respond to alarm calls of their own species, but also alarm calls of other species and those of non-predatory birds. The ring-tailed lemur and a few other species have different calls and reactions to specific types of predators.^[39] With mating calls, it has been shown that mouse lemurs that cannot be discerned visually respond more strongly to the calls of their own species, particularly when exposed to the calls of other mouse lemurs that they would encounter normally within their home range.^[73] Lemur calls can also be very loud and carry long distances. Ruffed lemurs use several loud calls that can be heard up to 1 km (0.62 mi) away on a clear, calm day.^[118] The loudest lemur is the indri, whose calls can be heard up to 2 km (1.2 mi) or more^[52][63] and thus communicate more effectively the territorial boundaries over its 34 to 40 hectares (0.13 to 0.15 sq mi) home range.^[79] Both ruffed lemurs and the indri exhibit contagious calling, where one individual or group starts a loud call and others within the area join in.^[63][118] The song of the indri can last 45 seconds to more than 3 minutes and tends to coordinate to form a stable duet comparable to that of gibbons.^[63][68]

Tactile communication (touch) is mostly used by lemurs in the form of grooming, although the ring-tailed lemur also clumps together to sleep (in an order determined by rank), reaches out and touches adjacent members, and cuffs other members. Reaching out and touching another individual in this species has been shown to be a submissive behavior, done by younger or submissive animals towards older and more dominant members of the troop. Allogrooming, however, appears to occur more frequently between higher ranking individuals, a shared trait with other primate species.^[119] Unlike anthropoid primates, lemur grooming seems to be more intimate and mutual, often directly reciprocated. Anthropoids, on the other hand, use allogrooming to manage agonistic interactions.^[120] The ring-tailed lemur is known to be very tactile, spending between 5 and 11% of its time grooming.^[119]

Sample lemur vocalizations
Indri duet The wailing "song" of the indri Gray mouse lemur alarm call High-frequency, fast-paced squeaks emitted when startled Problems playing these files? See media help.	Ring-tailed lemur cackle A defensive but confrontational vocalization Ruffed lemur roar/shriek chorus An intergroup spacing call Problems playing these files? See media help.

Predator avoidance

Lemur alarm calls

Three types of clicks followed by loud yaps

Mammalian predator alert by a ring-tailed lemur

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High-amplitude, pulsed squawks

Mammalian predator alert by a ruffed lemur

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All lemurs experience some predation pressure.

Diurnal lemurs are visible during the day, so many live in groups, where the increased number of eyes and ears helps aid in predator detection. Diurnal lemurs use and respond to alarm calls, even those of other lemur species and non-predatory birds. The ring-tailed lemur has different calls and reactions to different classes of predators, such as predatory birds, mammals, or snakes.[39] Some lemurs, such as the indri, use crypsis to camouflage themselves. They are often heard but difficult to see in the trees due to the dappled light, earning them the reputation of being "ghosts of the forest".^[79]

Reproduction

Except for the aye-aye and the Lac Alaotra gentle lemur, lemurs are seasonal breeders

Lemurs time their mating and birth seasons so that all weaning periods are synchronized to match the time of highest food availability.^[86][97] Weaning occurs either before or shortly after the eruption of the first permanent molars in lemurs.^[33] Mouse lemurs are able to fit their entire breeding cycle into the wet season, whereas larger lemurs, such as sifakas, must lactate for two months during the dry season.^[97] Infant survival in some species, such as Milne-Edwards' sifaka, has been shown to be directly impacted by both environmental conditions and the rank, age, and health of the mother. The breeding season is also affected by geographical location. For example, mouse lemurs give birth between September and October in their native habitat in the Southern Hemisphere, but from May through June in the captive settings in the Northern Hemisphere.^[86]

Woolly lemurs

are nocturnal and typically give birth to one offspring, which they carry with them while foraging.

Yet another trait that sets most lemurs apart from anthropoid primates is their long lifespan together with their high infant mortality.[97] Many lemurs, including the ring-tailed lemur, have adapted to a highly seasonal environment, which has affected their birthrate, maturation, and twinning rate (r-selection). This helps them to recover rapidly from a population crash.^[90] In captivity, lemurs can live twice as long as they do in the wild, benefiting from consistent nutrition that meets their dietary requirements, medical advancements, and improved understanding of their housing requirements. In 1960, it was thought that lemurs could live between 23 and 25 years. We now know that the larger species can live for more than 30 years without showing signs of aging (senescence) and still be capable of reproduction.^[86]

Cognitive abilities and tool use

Lemurs have traditionally been regarded as being less intelligent than anthropoid primates,

A few lemurs have been noted to have relatively large brains. The extinct Hadropithecus was as large as a large male baboon and had a comparably sized brain, giving it the largest brain size relative to body size among all prosimians.^[132] The aye-aye also has a large brain-to-body ratio, which may indicate a higher level of intelligence.^[43] However, despite having a built-in tool in the form of its thin, elongated middle finger, which it uses to fish for insect grubs, the aye-aye has tested poorly in the use of extraneous tools.^[16]

Ecology

See above: Diet, Metabolism, Activity patterns, and Locomotion

The fossa (above) and the Madagascar harrier-hawk (below) are predators of many lemur species.^[121]

Madagascar not only contains two radically different climatic zones, the rainforests of the east and the dry regions of the west,^[2] but also swings from extended drought to cyclone-generated floods.^[133] These climatic and geographical challenges, along with poor soils, low plant productivity, wide ranges of ecosystem complexity, and a lack of regularly fruiting trees (such as fig trees) have driven the evolution of lemurs' immense morphological and behavioral diversity.^{[15][2][33][97]} Their survival has required the ability to endure the persistent extremes, not yearly averages.^[133]

Lemurs have either presently or formerly filled the ecological niches normally occupied by monkeys, squirrels, woodpeckers, and grazing ungulates.^[17] With the diversity of adaptations for specific ecological niches, habitat selection among lemur families and some genera is often very specific, thus minimizing competition.^[2] In nocturnal lemurs from the more seasonal forests in the west, up to five species can coexist during the wet season due to high food abundance. However, to endure the extreme dry season, three of the five species utilize different dietary patterns and their underlying physiological traits to allow them to coexist: fork-marked lemurs feed on tree gum, sportive lemurs feed on leaves, and giant mouse lemurs sometimes feed on insect secretions. The other two species, the gray mouse lemur and the fat-tailed dwarf lemur (Cheirogaleus medius), avoid competition through reduced activity. The gray mouse lemur uses bouts of torpor, while the fat-tailed dwarf lemur hibernates completely.^[29] Similarly, on the east coast entire genera focus on specific food to avoid too much niche overlap. True lemurs and ruffed lemurs are frugivorous, indriids are folivorous, and bamboo lemurs specialize in bamboo and other grasses. Once again, seasonal dietary differences as well as subtle differences in substrate preferences, forest strata used, activity cycle, and social organization enable lemur species to coexist, although this time the species are more closely related and have similar niches.^[2] A classic example involves resource partitioning between three species of bamboo lemur that live in close proximity in small forested areas: the golden bamboo lemur, the greater bamboo lemur, and the eastern lesser bamboo lemur (Hapalemur griseus). Each utilizes either different species of bamboo, different parts of the plant, or different layers in the forest.^[17][57] Nutrient and toxin content (such as cyanide) help regulate food selection,^[2] though seasonal food preferences are also known to play a role.^[57]

Dietary regimes of lemurs include

Similarities that lemurs share with anthropoid primates, such as diet and social organization, along with their own unique traits, have made lemurs the most heavily studied of all mammal groups on Madagascar.[2]^[62] Research often focuses on the link between ecology and social organization, but also on their behavior and morphophysiology (the study of anatomy in relation to function).^[2] Studies of their life-history traits, behavior and ecology help understanding of primate evolution, since they are thought to share similarities with ancestral primates.

Lemurs have been the focus of