Lemur

The lemur dentition is heterodont (having multiple tooth morphologies) and derives from an ancestral primate permanent dentition of 2.1.3.32.1.3.3. Indriids, sportive lemurs, the aye-aye, and the extinct sloth lemurs, monkey lemurs, and koala lemurs have reduced dentitions, having lost incisors, canines, or premolars.[78] The ancestral deciduous dentition is 2.1.32.1.3, but young indriids, aye-ayes, koala lemurs, sloth lemurs, and probably monkey lemurs have fewer deciduous teeth.[57][74]

A six-tooth version of the strepsirrhine toothcomb in a ring-tailed lemur, with canine-like premolars behind it

There are also noticeable differences in dental morphology and tooth topography between lemurs. Indri, for instance, have teeth that are perfectly adapted for shearing leaves and crushing seeds.[63] In the toothcomb of most lemurs, the bottom incisors and canine teeth are procumbent (face forward rather than up) and finely spaced, thus providing a tool for either grooming or feeding.[18][57][78] For instance, indri use their toothcomb not only for grooming, but also to pry out the large seeds from the tough epicarp of Beilschmiedia fruits,[79] while fork-marked lemurs use their relatively long toothcomb to cut through tree bark to induce the flow of tree sap.[52] The toothcomb is kept clean by the sublingua or "under-tongue", a specialized structure that acts like a toothbrush to remove hair and other debris. The sublingua extends below the tip of the tongue and is tipped with keratinized, serrated points that rake between the front teeth.[80][81]

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 eruption.[83] By contrast, anthropoid primates exhibit slower dental development with increased size and slower morphological development.[78] Lemurs are also dentally precocious at birth, and have their full permanent dentition at weaning.[33]

Lemurs generally have thin tooth enamel compared to anthropoid primates. This may result in extra wear and breakage to the anterior (front) teeth due to heavy use in grooming, feeding, and fighting. Little other dental health information is available for lemurs, except that wild ring-tailed lemurs at Berenty Private Reserve occasionally exhibit abscessed maxillary canines (seen as open wounds on the muzzle) and tooth decay, possibly due to the consumption of non-native foods.[78]

The sense of smell, or olfaction, is highly important to lemurs and is frequently used in communication.[2][17][22] Lemurs have long snouts (compared to the short snouts of haplorrhines) that are traditionally thought to position the nose for better sifting of smells,[17] although long snouts do not necessarily translate into high olfactory acuity since it is not the relative size of the nasal cavity that correlates with smell, but the density of olfactory receptors.[84][85] Instead, the long snouts may facilitate better chewing.[85]

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 scent mark with urine as well as scent glands located on the wrists, inside elbow, genital regions, or the neck.[16][65] The scrotal skin of most male lemurs has scent glands.[86] Ruffed lemurs (genus Varecia) and male sifakas have a gland at the base of their neck,[16][52] while the greater bamboo lemur (Prolemur simus) and the ring-tailed lemur have glands inside the upper arms near the axilla.[16] Male ring-tailed lemurs also have scent glands on the inside of their forearms, adjacent to a thorn-like spur, which they use to gouge, and simultaneously, scent-mark tree branches.[52] They will also wipe their tails between their forearms and then engage in "stink fights" by waving their tail at their opponents.[16]

Lemurs (and strepsirrhines in general) are considered to be less visually oriented than the higher primates, since they rely so heavily on their sense of smell and pheromone detection. The fovea on the retina, which yields higher visual acuity, is not well-developed. The postorbital septum (or bony closure behind the eye) in haplorrhine primates is thought to stabilize the eye slightly, allowing for the evolution of the fovea. With only a postorbital bar, lemurs have been unable to develop a fovea.[87] Therefore, regardless of their activity pattern (nocturnal, cathemeral, or diurnal), lemurs exhibit low visual acuity and high retinal summation.[33] Lemurs can see a wider visual field, however, than anthropoid primates due to a slight difference in the angle between the eyes, as shown in the following table:[88]

Although they lack a fovea, some diurnal lemurs have a cone-rich, although less clustered, area centralis.[87] This area centralis has a high rod-to-cone cell ratio in many diurnal species studied thus far, whereas diurnal anthropoids have no rod cells in their fovea. Once again, this suggests lower visual acuity in lemurs than in anthropoids.[89] Furthermore, the rod-to-cone cell ratio can be variable even among diurnal species. For instance, Verreaux's sifaka (Propithecus verreauxi) and the indri (Indri indri) have only a few large cones scattered along their predominantly rod-dominated retina. The eyes of the ring-tailed lemur contain one cone to five rods. Nocturnal lemurs such as mouse lemurs and dwarf lemurs, on the other hand, have retinas made up entirely of rod cells.[16]

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 nictitating membrane, whereas most other primates have a lesser developed plica semilunaris. The nictitating membrane keeps the cornea moist and clean by sweeping across the eye.[91][92]

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]

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 tree sap are consumed by a few lemur species. The exploitation of exudates has been reported in 18 plant species and only in the dry regions in the south and west of Madagascar. Only the Masoala fork-marked lemur (Phaner furcifer) and Coquerel's giant mouse lemur regularly consume tree sap. Bark has never been reported as an important food item in lemur diets, but at least four species eat it: the aye-aye, the red-tailed sportive lemur (Lepilemur ruficaudatus), the common brown lemur (Eulemur fulvus), and Verreaux's sifaka (Propithecus verreauxi). Most bark feeding is directly linked to exudate feeding, except for the aye-aye's bark feeding on Afzelia bijuga (genus Afzelia) at Nosy Mangabe in the northeast.[96]

Soil consumption (geophagy) has also been reported and likely helps with digestion, provides minerals and salts, and helps absorb toxins. Sifakas have been observed eating soil from termite mounds, possibly adding beneficial intestinal flora to aid the digestion of cellulose from their folivorous diet.[64]

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

Lemurs are social and live in groups that usually include fewer than 15 individuals.[2] Observed social organization patterns include "solitary but social", "fission-fusion", "pair bonds", and "multi-male group".[101] Nocturnal lemurs are mostly solitary but social, foraging alone at night but often nesting in groups during the day. The degree of socialization varies by species, gender, location, and season.[29][39] In many nocturnal species, for instance, the females, along with their young, will share nests with other females and possibly one male, whose larger home range happens to overlap one or more female nesting groups. In sportive lemurs and fork-marked lemurs, one or two females may share a home range, possibly with a male. In addition to sharing nests, they will also interact vocally or physically with their range-mate while they forage at night.[39] Diurnal lemurs exhibit many of the social systems seen in monkeys and apes,[2][39] living in relatively permanent and cohesive social groups. Multi-male groups are the most common, just as they are in most anthropoid primates. True lemurs utilize this social system, often living in groups of ten or less. Ruffed lemurs have been shown to live in fission-fusion societies,[39] and Indri forms pair bonds.[101]

Some lemurs exhibit female philopatry, where females stay within their natal range and the males migrate upon reaching maturity, and in other species both sexes will migrate.[2] In some cases, female philopatry may help explain the evolution of female-bonded multi-male groups, such as those of the ring-tailed lemur, Milne-Edwards' sifaka (Propithecus edwardsi), and the Verreaux's sifaka. Their ancestors may have been more solitary, with females that lived in mother-daughter pairs (or dyads). Over time, these dyads may have allied themselves with other neighboring mother-daughter dyads in order to defend more distributed resources in a wide home range. If this is true, then multi-male groups in lemurs may differ fundamentally in their internal structure from those in catarrhine primates (Old World monkeys and apes).[102]

Social grooming serves many functions for social lemurs.

The presence of female social dominance sets lemurs apart from most other primates and mammals;[2][39][43][103] in most primate societies, males are dominant unless females band together to form coalitions that displace them.[104] However, many Eulemur species are exceptions[39][72] and the greater bamboo lemur (Prolemur simus) does not exhibit female dominance.[105] When females are dominant within a group, the way they maintain dominance varies. Ring-tailed lemur males act submissively with or without signs of female aggression. Male crowned lemurs (Eulemur coronatus), on the other hand, will only act submissively when females act aggressively towards them. Female aggression is often associated with, but not limited to, feeding.[106]

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]

The biological rhythm can vary from nocturnal in smaller lemurs to diurnal in most larger lemurs. Diurnality is not seen in any other living strepsirrhine.[29] Cathemerality, where an animal is active sporadically both day and night, occurs among some of the larger lemurs. Few if any other primates exhibit this sort of activity cycle,[108] either regularly or irregularly under changing environmental conditions.[2] The most heavily studied cathemeral lemurs are the true lemurs.[43][109] Although the mongoose lemur (E. mongoz) is the best-documented example, every species in the genus studied has shown some degree of cathemeral behavior,[72] although night activity is often restricted by light availability and moon periodicity.[16] This type of behavior was first documented in the 1960s in true lemur species as well as other Lemuridae species, such as ruffed lemurs and bamboo lemurs. Initially described as "crepuscular" (active at dawn and dusk), anthropologist Ian Tattersall stimulated additional research and coined the new term "cathemeral",[108] although many non-anthropologists prefer the terms "circadian" or "diel".[16]

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.[93][111] Unlike other hibernating mammals from temperate regions, which have to awaken regularly for a few days, dwarf lemurs experience five months of continuous deep hibernation (May through September). Before and after this deep hibernation, there are two months (April and October) of transition, where they will forage on a limited basis to reduce demands on their fat reserves.[110] Unlike any other hibernating mammal, the body temperature of hibernating dwarf lemurs will fluctuate with the ambient temperature rather than remaining low and stable.[31][95][110]

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]

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

Locomotor behavior in lemurs, both living and extinct, is highly varied and its diversity exceeds that of anthropoids.[39] Locomotor postures and behaviors have included vertical clinging and leaping (including saltatory behavior), seen in indriids and bamboo lemurs;[39][66] slow (loris-like) arboreal quadrupedal locomotion, once exhibited by Mesopropithecus;[112] fast arboreal quadrupedal locomotion, seen in true lemurs and ruffed lemurs;[39][113] partially terrestrial quadrupedal locomotion, seen in the ring-tailed lemur; highly terrestrial quadrupedal locomotion, once exhibited by monkey lemurs such as Hadropithecus;[39] and sloth-like suspensory locomotion, once exhibited by many of the sloth lemurs, such as Palaeopropithecus.[2][39] The Lac Alaotra gentle lemur (Hapalemur alaotrensis) has even been reported to be a good swimmer.[2] Sometimes these locomotor types are lumped together into two main groups of lemurs, the vertical clingers and leapers and the arboreal (and occasionally terrestrial) quadrupeds.[64]

The jumping prowess of the indriids has been well documented and is popular among ecotourists visiting Madagascar.[114] Using their long, powerful back legs, they catapult themselves into the air and land in an upright posture on a nearby tree, with both hands and feet tightly gripping the trunk.[17] Indriids can leap up to 10 m (33 ft) rapidly from tree trunk to tree trunk,[17][69] an ability referred to as "ricochetal leaping".[79] Verreaux's sifaka (Propithecus verreauxi) manages to do this in the spiny forests of southern Madagascar. It is unknown how it avoids impaling its palms on the thorn-covered trunks of large plants such as Alluaudia.[17] When distances between trees are too great, sifakas will descend to the ground and cross distances more than 100 m (330 ft) by standing upright and hopping sideways with the arms held to the side and waving up and down from chest to head height, presumably for balance.[17][69] This is sometimes described as a "dance-hop".[17]

Lemur communication can be transmitted through sound, sight, and smell (olfaction). The ring-tailed lemur, for instance, uses complex though highly stereotyped behaviors such as scent-marking and vocalizations.[90] Visual signals are probably the least used by lemurs, since they lack many of the muscles used in common primate facial expressions.[88] Given their poor vision, whole-body postures are probably more noticeable. However, the ring-tailed lemur has demonstrated distinct facial expressions including a threat stare, pulled back lips for submission, and pulled back ears along with flared nostrils during scent-marking.[90] This species has also been observed using yawns as threats.[115][116] Their ringed tails also communicate distance, warn off neighboring troops, and help locate troop members.[90] Sifakas are known to exhibit an open-mouth play face[117] as well as a submissive teeth-baring grimace used in agonistic interactions.[70]

Lemurs use scent-marking to communicate. Pictured is a red-bellied lemur rubbing its rump against some smaller branches.

Olfaction is particularly important to lemurs,[2] except for the indri, which lacks most common lemur scent glands and has a greatly reduced olfactory region in the brain.[79] Olfaction can communicate information about age, sex, reproductive status, as well as demarcate the boundaries of a territory. It is most useful for communication between animals that rarely encounter each other.[51] Small, nocturnal lemurs mark their territories with urine, while the larger, diurnal species use scent glands located on various parts of their anatomy. The ring-tailed lemur engages in "stink fights" by rubbing its tail across scent glands on its wrists, and then flicking its tail at other male opponents. Some lemurs defecate in specific areas, otherwise known as latrine behavior. Although many animals exhibit this behavior, it is a rare trait among primates. Latrine behavior can represent territorial marking and aid in interspecies signaling.[16]

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]

All lemurs experience some predation pressure.[121] Common defenses against predation include the use of alarm calls and predator mobbing,[122] mostly among diurnal lemurs.[39] The leaping abilities of lemurs may have evolved for predator avoidance rather than for travel, according to a study in kinematics.[123] Nocturnal lemurs are difficult to see and track at night and decrease their visibility by foraging alone. They also try to avoid predators by using concealing sleeping locations, such as nests, tree holes, or dense vegetation,[39] Some may also avoid areas frequented by predators by detecting the smell of their feces[124] and alternating between multiple sleeping locations.[31] Even torpor and hibernation states among cheirogaleids may be partly due to high levels of predation.[121] Infants are protected while foraging by either leaving them in the nest or by stashing them in a hidden location, where the infant remains immobile in the absence of the parent.[39]

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]

Except for the aye-aye and the Lac Alaotra gentle lemur, lemurs are seasonal breeders[2][43] with very short mating and birth seasons influenced by the highly seasonal availability of resources in their environment. Mating season usually last less than three weeks each year,[39] and the female vagina opens up only during a few hours or days of her most receptive time of estrus.[86] These narrow windows for reproduction and resource availability appear to relate to their short gestation periods, rapid maturation, and low basal metabolic rates, as well as the high energy costs of reproduction for females. This may also relate to the relatively high mortality rate among adult females and the higher proportion of adult males in some lemur populations—both unusual traits among primates. In both the aye-aye and Lac Alaotra gentle lemur, birth (parturition) occurs over a six-month period.[2]

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.

Scent factors heavily into lemur reproduction. Scent-marking activity escalates during the mating season. Pheromones may coordinate reproductive timing for females coming into estrus.[86] Mating can be either monogamous or promiscuous for both males and females, and mating can include individuals from outside the group.[2][39] Monogamous lemurs include the red-bellied lemur (Eulemur rubriventer) and the mongoose lemur (E. mongoz), although the mongoose lemur has been observed mating outside of its pair bond.[39] Monogamy is most common among nocturnal species, although some exhibit scramble competition, sexual suppression of subordinates, or competitions between males that avoid direct fighting.[33] In mouse lemurs, males utilize sperm plugs, developed enlarged testes during the mating season, and develop size dimorphism (likely due to the enlarged testes). These indicate a mating system known as scramble competition polygyny, where males cannot defend females or the resources that might attract them.[125]

The gestation period varies within lemurs, ranging from 9 weeks in mouse lemurs and 9–10 weeks in dwarf lemurs to 18–24 weeks in other lemurs.[86] The smaller, nocturnal lemurs, such as mouse lemurs, giant mouse lemurs, and dwarf lemurs, usually give birth to more than one infant, whereas the larger, nocturnal lemurs, such as fork-marked lemurs, sportive lemurs, and the aye-aye usually have one offspring.[29] Dwarf and mouse lemurs have up to four offspring, but both average only two. Ruffed lemurs are the only large, diurnal lemurs to consistently give birth to two or three offspring. All other lemurs have single births. Multiple births in lemurs are normally fraternal, and are known to occur in every five to six births in species such as the ring-tailed lemur and some Eulemur.[86]

After the offspring are born, lemurs either carry them around or stash them while foraging. When transported, the infants either cling to the mother's fur or are carried in the mouth by the scruff. In some species, such as bamboo lemurs, infants are carried by mouth until they are able to cling to their mother's fur.[126] Species that park their offspring include nocturnal species (e.g. mouse lemurs, sportive lemurs, and dwarf lemurs), bamboo lemurs, and ruffed lemurs.[29][126] In the case of the ruffed lemurs, the young are altricial and the mothers build nests for them, much like the smaller, nocturnal lemur species.[2] Woolly lemurs are unusual for nocturnal lemurs because they live in cohesive family groups and carry their single offspring with them rather than parking them.[66][67] Alloparenting (multiple or group parenting) has been reported in all lemur families except the sportive lemurs and aye-aye. Allonursing is also known to occur in several lemur groups.[127] Even males have been observed caring for infants in species such as the red-bellied lemur, mongoose lemur,[72] eastern lesser bamboo lemur, silky sifaka,[127] fat-tailed dwarf lemur,[128] and ruffed lemurs.[129]

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]

Lemurs have traditionally been regarded as being less intelligent than anthropoid primates,[130] with monkeys and apes often described as having more cunning, guile, and deceptiveness.[17] Many lemur species, such as sifakas and the ring-tailed lemur, have scored lower on tests designed for monkeys while performing as well as monkeys on other tests.[17][107] These comparisons may not be fair since lemurs prefer to manipulate objects with their mouths (rather than their hands) and only take interest in objects when in captivity.[107] Recent studies have shown that lemurs exhibit levels of technical intelligence on par with many other primates, although they manipulate objects less often.[131] Tool use has not been witnessed by lemurs in the wild, although in captivity the common brown lemur and the ring-tailed lemur have been demonstrated to be able to understand and use tools.[16]

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]

The greatest concern facing lemur populations is habitat destruction and degradation.[39][144] Deforestation takes the form of local subsistence use, such as slash and burn agriculture (referred to as tavy in Malagasy), the creation of pasture for cattle through burning, and legal and illegal gathering of wood for firewood or charcoal production; commercial mining; and the illegal logging of precious hardwoods for foreign markets.[39][143] After centuries of unsustainable use, as well as rapidly escalating forest destruction since 1950,[136] less than 60,000 km² (23,000 sq mi) or 10% of Madagascar's land area remains forested. Only 17,000 km² (6,600 sq mi) or 3% of the island's land area is protected and due to dire economic conditions and political instability, most of the protected areas are ineffectively managed and defended.[143][145] Some protected areas were set aside because they were naturally protected by their remote, isolated location, often on steep cliffs. Other areas, such as the dry forests and spiny forests of the west and south, receive little protection and are in serious danger of being destroyed.[39]

Some species may be in risk of extinction even without complete deforestation, such as ruffed lemurs, which are very sensitive to habitat disturbance.[62] If large fruit trees are removed, the forest may sustain fewer individuals of a species and their reproductive success may be affected for years.[97] Small populations may be able to persist in isolated forest fragments for 20 to 40 years due to long generation times, but in the long term, such populations may not be viable.[153] Small, isolated populations also risk extirpation by natural disasters and disease outbreaks (epizootics). Two diseases that are lethal to lemurs and could severely impact isolated lemur populations are toxoplasmosis, which is spread by feral cats, and the herpes simplex virus carried by humans.[154]

Climate change and weather-related natural disasters also threaten lemur survival. For the last 1000 years, western and highland regions have been growing significantly drier, but in the past few decades, severe drought has become much more frequent. There are indications that deforestation and forest fragmentation are accelerating this gradual desiccation.[97] The effects of drought are even felt in the rainforests. As annual rainfall decreases, the larger trees that make up the high canopy suffer increased mortality, failure to fruit, and decreased production of new leaves, which folivorous lemurs prefer. Cyclones can defoliate an area, knock down canopy trees, and create landslides and flooding. This can leave lemur populations without fruit or leaves until the following spring, requiring them to subsist on crisis foods, such as epiphytes.[155]

Lemurs are hunted for food by the local Malagasy, either for local subsistence[5][143] or to supply a luxury meat market in the larger cities.[156] Most rural Malagasy do not understand what "endangered" means, nor do they know that hunting lemurs is illegal or that lemurs are found only in Madagascar.[157] Many Malagasy have taboo, or fady, about hunting and eating lemurs, but this does not prevent hunting in many regions.[2] Even though hunting has been a threat to lemur populations in the past, it has recently become a more serious threat as socioeconomic conditions deteriorate.[143] Economic hardships have caused people to move around the country in search of employment, leading local traditions to break down.[62][144][157] Drought and famine can also relax the fady that protect lemurs.[62] Larger species, such as sifakas and ruffed lemurs, are common targets, but smaller species are also hunted or accidentally caught in snares intended for larger prey.[5][144] Experienced, organized hunting parties using firearms, slings and blowguns can kill as many as eight to twenty lemurs in one trip. Organized hunting parties and lemur traps can be found in both non-protected areas and remote corners of protected areas.[62] National parks and other protected areas are not adequately protected by law enforcement agencies.[157] Often, there are too few park rangers to cover a large area, and sometimes terrain within the park is too rugged to check regularly.[158]

Although not as significant as deforestation and hunting, some lemurs, such as crowned lemurs and other species that have successfully been kept in captivity, are occasionally kept as exotic pets by Malagasy people.[52][136] Bamboo lemurs are also kept as pets,[136] although they only survive for up to two months.[159] Live capture for the exotic pet trade in wealthier countries is not normally considered a threat due to strict regulations controlling their export.[136][144]

Rosewood is logged illegally from national parks, such as Marojejy.

Lemurs have drawn much attention to Madagascar and its endangered species. In this capacity, they act as flagship species,[62][136] the most notable of which is the ring-tailed lemur, which is considered an icon of the country.[60] The presence of lemurs in national parks helps drive ecotourism,[136] which especially helps local communities living in the vicinity of the national parks, since it offers employment opportunities and the community receives half of the park entrance fees. In the case of Ranomafana National Park, job opportunities and other revenue from long-term research can rival that of ecotourism.[160]

Rice paddies have gradually replaced lemur habitat, particularly in the central part of the island.

Starting in 1927, the Malagasy government has declared all lemurs as "protected"[71] by establishing protected areas that are now classified under three categories: National Parks (Parcs Nationaux), Strict Nature Reserves (Réserves Naturelles Intégrales), and Special Reserves (Réserves Spéciales). There are currently 18 national parks, 5 strict nature reserves, and 22 special reserves, as well as several other small private reserves, such as Berenty Reserve and Sainte Luce Private Reserve, both near Fort Dauphin.[136] All protected areas, excluding the private reserves, comprise approximately 3% of the land surface of Madagascar and are managed by Madagascar National Parks, formerly known as l'Association Nationale pour la Gestion des Aires Protégées (ANGAP), as well as other non-governmental organizations (NGOs), including Conservation International (CI), the Wildlife Conservation Society (WCS), and the World Wide Fund for Nature (WWF).[136][145] Most lemur species are covered by this network of protected areas, and a few species can be found in multiple parks or reserves.[145]

Conservation is also facilitated by the Madagascar Fauna Group (MFG), an association of nearly 40 zoos and related organizations, including the Duke Lemur Center, the Durrell Wildlife Conservation Trust, and the Saint Louis Zoological Park. This international NGO supports Madagascar's Parc Ivoloina, helps protect Betampona Reserve and other protected areas, and promotes field research, breeding programs, conservation planning, and education in zoos.[161] One of their major projects involved the release of captive black-and-white ruffed lemurs, designed to help restock the dwindling population within Betampona Reserve.[161][162]

Habitat corridors are needed for linking these protected areas so that small populations are not isolated.[145] In September 2003 in Durban, South Africa, Madagascar's former president Marc Ravalomanana promised to triple the size of the island's protected areas in five years.[143] This became known as the "Durban Vision".[136] In June 2007, the World Heritage Committee included a sizable portion of Madagascar's eastern rainforests as a new UNESCO World Heritage Site.[34]

Debt relief may help Madagascar protect its biodiversity.[152] With the political crisis in 2009, illegal logging has proliferated and now threatens rainforests in the northeast, including its lemur inhabitants and the ecotourism that the local communities rely upon.

Captive lemur populations are maintained locally and outside of Madagascar in varied zoological conservatories and research centers, although the diversity of species is limited. Sikafas, for instance, do not survive well in captivity, so few facilities have them.[2][63] The largest captive lemur population can be found at the Duke Lemur Center (DLC), whose mission includes non-invasive research, conservation (e.g. captive breeding), and public education.[136] Another large lemur colony includes the Myakka City Lemur Reserve run by the Lemur Conservation Foundation (LCF), which also hosts lemur research.[163] In Madagascar, Lemurs' Park is a free-range, private facility southwest of Antananarivo that exhibits lemurs for the public while also rehabilitating captive-born lemurs for reintroduction into the wild.[164]