Thering-tailed lemur (Lemur catta) is a medium- to larger-sizedstrepsirrhine (wet-nosed)primate and the most internationally recognizedlemur species, owing to its long, black-and-white, ringed tail. It belongs toLemuridae, one of five lemur families, and is the only member of theLemurgenus. Like all lemurs, it is endemic to the island ofMadagascar, where it isendangered. Known locally inMalagasy asmaky ([makʲ]ⓘ, spelledmaki inFrench) orhira, it ranges fromgallery forests to spinyscrub in the southern regions of the island. It isomnivorous, as well as the most adapted to livingterrestrially of the extant lemurs.
The ring-tailed lemur is highly social, living in groups—known as "troops"—of up to 30 individuals. It is also a female-dominant species, a commonality among lemurs. To keep warm and reaffirm social bonds, groups will huddle together. Mutual grooming is another vital aspect of lemur socialization (as with all primates), reaffirming social and familial connections, while also helping rid each other of any potential insects. Ring-tailed lemurs are strictlydiurnal, being active exclusively during daylight hours. Due to this lifestyle, they also sunbathe; the lemurs can be observed sitting upright on their tails, exposing their soft, white belly fur towards the sun. They will often also have their palms open and eyes gently closed. Like other lemurs, this species relies strongly on their sense of smell, andterritorial marking, with scent glands, provides communication signals throughout a group's home range. The glands are located near the eyes, as well as near the anus. The males perform a unique scent-marking behavior calledspur-marking and will participate instink fights by dousing their tails with their pheromones and "wafting" them at opponents. Additionally, lemurs of both sexes will scent-mark trees, logs, rocks or other objects by simply rubbing their faces and bodies onto it, not unlike a domestic cat.
As one of the most vocal primates, the ring-tailed lemur uses numerousvocalizations, including calling for group cohesion and predatoralarm calls. Experiments have shown that the ring-tailed lemur, despite the lack of a large brain (relative tosimiiform primates), can organize sequences, understand basicarithmetic operations, and preferentially select tools based on functional qualities.
Despite adapting to and breeding easily under captive care (and being the most popular species of lemur inzoos worldwide, with more than 2,000 captive-raised individuals), the wild population of ring-tailed lemur is listed asendangered by theIUCN Red List, due tohabitat destruction, local hunting forbushmeat and theexotic pet trade. As of early 2017, the population in the wild is believed to have lowered to as few as 2,000 individuals due to these reasons, making them far more critically endangered. Local Malagasy farmers and logging industries frequently make use ofslash and burn deforestation techniques, with smoke being visible on the horizon on most days in Madagascar, in an effort to accommodate livestock and to cultivate larger fields of crops.[5]
Although the term "lemur" was first intended forslender lorises, it was soon limited to theendemic Malagasy primates, which have been known as "lemurs" ever since.[6] The name derives from theLatin termlemures,[7] which refers to specters or ghosts that wereexorcised during theLemuria festival of ancient Rome.[8] According toCarl Linnaeus's own explanation, the name was selected because of the nocturnal activity and slow movements of the slender loris.[7] Being familiar with the works ofVirgil andOvid and seeing an analogy that fit with his naming scheme, Linnaeus adapted the term "lemur" for these nocturnal primates.[9] However, it has been commonly and falsely assumed that Linnaeus was referring to the ghost-like appearance,reflective eyes, and ghostly cries of lemurs.[7] 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,[10] but this is unlikely given that the name was selected for slender lorises from India.[7] The species name,catta, refers to the ring-tailed lemur's cat-like appearance. Its purring vocalization is similar to that of thedomestic cat.[3]
Following Linnaeus'sspecies description, thecommon name "ring-tailed maucauco" was first penned in 1771 by Welsh naturalistThomas Pennant, who noted its characteristic long, banded tail. (The term "maucauco" was a very common term for lemurs at this time.) The now universal English name "ring-tailed lemur" was first used byGeorge Shaw in his illustrated scientific publication covering theLeverian collection, which was published between 1792 and 1796.[7]
Allmammalianfossils from Madagascar come from recent times.[11] Thus, little is known about the evolution of the ring-tailed lemur, let alone the rest of the lemurclade, which comprises the entireendemic primate population of the island. However,chromosomal andmolecular evidence suggest that lemurs are more closely related to each other than to otherstrepsirrhine primates. For this to have happened, it is thought that a very small ancestral population came to Madagascar via a singlerafting event between 50 and 80 million years ago.[12][11][13] Subsequentevolutionary radiation andspeciation has created the diversity of Malagasy lemurs seen today.[14]
Genetic analysis indicates that ring-tailed lemurs (left) are more closely related to the two genera of bamboo lemurs (Prolemur [center] andHapalemur [right]) than they are to other members of the family Lemuridae.
According to analysis ofamino acid sequences, the branching of the family Lemuridae has been dated to 26.1 ±3.3 mya while rRNA sequences of mtDNA place the split at 24.9 ±3.6 mya. The ruffed lemurs are the first genus to split away (mostbasal) in the family, a view that is further supported by analysis of DNA sequences andkaryotypes.[15] Additionally,Molecular data suggests a deepgenetic divergence andsister group relationship between the true lemurs (Eulemur) and the other two genera:Lemur andHapalemur.[16][17]
The ring-tailed lemur is thought to share closer affinities to thebamboo lemurs of the genusHapalemur than to the other two genera in its family.[18][19][17] This has been supported by comparisons in communication,chromosomes, genetics, and several morphological traits, such as scent gland similarities. However, other data concerningimmunology and other morphological traits fail to support this close relationship. For example,Hapalemur species have short snouts, while the ring-tailed lemur and the rest of Lemuridae have long snouts. However, differences in the relationship between theorbit (eye socket) and the muzzle suggest that the ring-tailed lemur and the true lemurs evolved their elongated faces independently.[16]
The relationship between the ring-tailed lemur and bamboo lemurs is the least understood. Molecular analysis suggests that either the bamboo lemurs diverged from the ring-tailed lemur, making the groupmonophyletic and supporting the current two-genera taxonomy,[17] or that the ring-tailed lemur is nested in with the bamboo lemurs, requiringHapalemur simus to be split off into its own genus,Prolemur.[16]
The karyotype of the ring-tailed lemur has 56 chromosomes, of which four aremetacentric (arms of nearly equal length), four aresubmetacentric (arms of unequal length), and 46 areacrocentric (the short arm is hardly observable). TheX chromosome is metacentric and theY chromosome is acrocentric.[3]
Linnaeus first used the genus nameLemur to describe "Lemur tardigradus" (thered slender loris, now known asLoris tardigradus) in his 1754 catalog of the Museum of King Adolf Frederick. In 1758, his10th edition ofSystema Naturae listed the genusLemur with three included species, only one of which is still considered to be a lemur while another is no longer considered to be a primate. These species include:Lemur tardigradus,Lemur catta (the ring-tailed lemur), andLemur volans (thePhilippine colugo, now known asCynocephalus volans). In 1911,Oldfield Thomas madeLemur catta thetype species for the genus, despite the term initially being used to describelorises. On January 10, 1929, theInternational Commission on Zoological Nomenclature (ICZN) formalized this decision in its publication of Opinion 122.[3][4]
The ring-tailed lemur shares many similarities withruffed lemurs (genusVarecia) andtrue lemurs (genusEulemur), and its skeleton is nearly indistinguishable from that of the true lemurs.[18] Consequently, the three genera were once grouped together in the genusLemur and more recently are sometimes referred to as subfamily Lemurinae (within family Lemuridae). However, ruffed lemurs were reassigned to the genusVarecia in 1962,[20] and due to similarities between the ring-tailed lemur and the bamboo lemurs, particularly in regards to molecular evidence and scent glands similarities, the true lemurs were moved to the genusEulemur byYves Rumpler andElwyn L. Simons (1988) as well asColin Groves and Robert H. Eaglen (1988).[20][3][19] In 1991,Ian Tattersall andJeffrey H. Schwartz reviewed the evidence and came to a different conclusion, instead favoring to return the members ofEulemur andVarecia to the genusLemur. However, this view was not widely accepted and the genusLemur remainedmonotypic, containing only the ring-tailed lemur.[20][19][21] Because the differences in molecular data are so minute between the ring-tailed lemur and both genera of bamboo lemurs, it has been suggested that all three genera be merged.[16]
Because of the difficulty in discerning the relationships within family Lemuridae, not all authorities agree on the taxonomy, although the majority of theprimatological community favors the current classification.[21]
In 1996, researchersSteven Goodman and Olivier Langrand suggested that the ring-tailed lemur may demonstrate regional variations, particularly a high mountain population atAndringitra Massif that has a thicker coat, lighter coloration, and variations in its tail rings.[3][23] In 2001,primatologistColin Groves concluded that this does not represent a locally occurringsubspecies. This decision was later supported by further fieldwork that showed that the differences fell within the normal range of variation for the species. The thicker coat was considered a local adaptation to extreme low temperatures in the region, and the fading of the fur was attributed to increased exposure tosolar radiation. Additional genetic studies in 2000 further supported the conclusion that population did not vary significantly from the other ring-tailed lemur populations on the island.[23][24]
The ring-tailed lemur is astrepsirrhine primate, with a protruding muzzle and a wet nose. Top is the skull.
The ring-tailed lemur is a relatively large lemur. Its average weight is 2.2 kilograms (4.9 lb).[21] Its head–body length ranges between 39 and 46 cm (15 and 18 in), its tail length is 56 and 63 cm (22 and 25 in), and its total length is 95 and 110 cm (37 and 43 in).[3][21] Other measurements include a hind foot length of 102 and 113 mm (4.0 and 4.4 in), ear length of 40 and 48 mm (1.6 and 1.9 in), and cranium length of 78 and 88 mm (3.1 and 3.5 in).[3]
The species has a slender frame and narrow face, fox-like muzzle.[3] The ring-tailed lemur's trademark—a long, bushy tail—is ringed in alternating black and white transverse bands, numbering 12 or 13 white rings and 13 or 14 black rings and always ending in a black tip.[3][25] The total number of rings nearly matches the approximate number ofcaudal vertebrae (~25).[26] Its tail is longer than its body[25] and is notprehensile. Instead, it is only used for balance, communication, and group cohesion.[21]
Thepelage (fur) is so dense that it can clog electric clippers.[3] Theventral (chest) coat and throat are white or cream. Thedorsal (back) coat varies from gray to rosy-brown, sometimes with a brown pygal patch around the tail region, where the fur grades to pale gray or grayish brown. The dorsal coloration is slightly darker around the neck and crown. The hair on the throat, cheeks, and ears is white or off-white and also less dense, allowing the dark skin underneath to show through.[3][4][21] The muzzle is dark grayish and the nose is black, and the eyes are encompassed by black triangular patches.[3][21] Facial vibrissae (whiskers) are developed and found above the lips (mystacal), on the cheeks (genal), and on the eyebrow (superciliary). Vibrissae are also found slightly above the wrist on the underside of the forearm.[3] The ears are relatively large compared to other lemurs and are covered in hair, which has only small tufts if any.[3][4] Although slight pattern variations in the facial region may be seen between individuals, there are no obvious differences between the sexes.[3]
Unlike most diurnal primates, but like all strepsirrhine primates, the ring-tailed lemur has atapetum lucidum, or reflective layer behind theretina of the eye, that enhancesnight vision.[27] The tapetum is highly visible in this species because the pigmentation of theocular fundus (back surface of the eye), which is present in—but varies between—all lemurs, is very spotty. The ring-tailed lemur also has a rudimentaryfoveal depression on the retina. Another shared characteristic with the other strepsirrhine primates is therhinarium, a moist, naked, glandular nose supported by the upper jaw and protruding beyond the chin. The rhinarium continues down where it divides the upper lip. The upper lip is attached to thepremaxilla, preventing the lip from protruding and thus requiring the lemur to lap water rather than using suction.[3]
Scent glands on a male: the brachial glands on the upper chest (left), and antebrachial gland and spur on the forearm (right)
The skin of the ring-tailed lemur is dark gray or black in color, even in places where the fur is white. It is exposed on the nose, palms, soles, eyelids, lips, and genitalia. The skin is smooth, but the leathery texture of the hands and feet facilitate terrestrial movement. Theanus, located at the joint of the tail, is covered when the tail is lowered. The area around the anus (circumanal area) and theperineum are covered in fur. In males, thescrotum lacks fur, is covered in small, horny spines, and the two sacs of the scrotum are divided. Thepenis is nearly cylindrical in shape andis covered in small spines, as well as having two pairs of larger spines on both sides. Males have a relatively smallbaculum (penis bone) compared to their size. The scrotum, penis, andprepuce are usually coated with a foul-smelling secretion. Females have avulva with a thick, elongatedclitoris that protrudes from thelabia. The opening of theurethra is closer to the clitoris than thevagina,[28] forming a "drip tip".[3]
Females have two pairs ofmammary glands (four nipples), but only one pair is functional.[3][4] The anterior pair (closest to the head) are very close to theaxillae (armpit).[3] Furlessscent glands are present on both males and females. Both sexes have small, dark antebrachial (forearm)glands measuring 1 cm long and located on the inner surface of the forearm nearly 25 cm (9.8 in) above the wrist joint.[3][4][21] (This trait is shared between theLemur andHapalemur genera.[21]) The gland is soft and compressible, bears fine dermal ridges (likefingerprints), and is connected to the palm by a fine, 2 mm–high, hairless strip.[3] However, only the male has a horny spur that overlays this scent gland.[3][4][21] The spur develops with age through the accumulation of secretions from an underlying gland that may connect through the skin through as many as a thousand minusculeducts. The males also have brachial (arm) glands on theaxillary surface of their shoulders (near the armpit). The brachial gland is larger than the antebrachial gland, covered in short hair around the periphery, and has a naked crescent-shaped orifice near the center. The gland secretes a foul-smelling, brown, sticky substance.[3] The brachial gland is barely developed if present at all in females.[3][4] Both sexes also haveapocrine andsebaceous glands in their genital or perianal regions,[29] which are covered in fur.[4]
Its fingers are slender, padded, mostly lacking webbing, and semi-dexterous with flat, human-likenails. The thumb is both short and widely separated from the other fingers. Despite being set at a right angle to the palm, the thumb is not opposable since the ball of the joint is fixed in place. As with all strepsirrhines, the hand is ectaxonic (the axis passes through the fourth digit) rather than mesaxonic (the axis passing through the third digit) as seen in monkeys and apes. The fourth digit is the longest, and only slightly longer than the second digit. Likewise, the fifth digit is only slightly longer than the second. The palms are long and leathery,[3] and like other primates, they have dermal ridges to improve grip.[30] The feet are semi-digitigrade and more specialized than the hands. The big toe is opposable and is smaller than the big toe of other lemurs, which are morearboreal. The second toe is short, has a small terminal pad, and has atoilet-claw (sometimes referred to as agrooming claw) specialized forpersonal grooming, specifically to rake through fur that is unreachable by the mouth.[3] The toilet-claw is a trait shared among nearly all living strepsirrhine primates.[31] Unlike other lemurs, the ring-tailed lemur's heel is not covered by fur.[3]
Like other lemurs, the ring-tailed lemur has a claw-like nail (toilet-claw) on its second toe (left) and dermal ridges on its hands to improve its grip (center). Unlike other lemurs, it lacks fur on its heel (right).
The front, lower dentition includes atoothcomb (4 incisors and 2 canine teeth), while the first premolars resemble canines.
The ring-tailed lemur has adentition of2.1.3.32.1.3.3 × 2 = 36, meaning that on each side of the jaw it has twoincisors, onecanine tooth, threepremolars, and threemolar teeth.[3] Itsdeciduous dentition is2.1.32.1.3 × 2 = 24.[32] Thepermanent teetherupt in the following order: m 1/1 (first molars), i 2/2 (first incisors), i 3/3 (second incisors), C1 (upper canines), m 2/2 (second molars), c1 (lower canines), m 3/3 (third molars), p 4/4 (third premolars), p 3/3 (second premolars), p 2/2 (first premolars).[3]
Its lower incisors (i1 and i2) are long, narrow, and finely spaced while pointing almost straight forward in the mouth (procumbent). Together with the incisor-shaped (incisiform) lower canines (c1), which are slightly larger and also procumbent, form a structure called atoothcomb,[3] a trait unique to nearly all strepsirrhine primates.[33] The toothcomb is used during oral grooming, which involves licking and tooth-scraping. It may also be used for grasping small fruits, removing leaves from the stem when eating, and possibly scraping sap and gum from tree bark. The toothcomb is kept clean using asublingual organ—a thin, flat, fibrous plate that covers a large part of the base of the tongue. The first lower premolar (p2) following the toothcomb is shaped like a canine (caniniform) and occludes the upper canine, essentially filling the role of the incisiform lower canine. There is also adiastema (gap) between the second and third premolars (p2 and p3).[3]
The upper incisors are small, with the first incisors (I1) space widely from each other, yet closely to the second incisors (I2). Both are compressed buccolingually (between the cheek and the tongue). The upper canines (C1) are long, have a broad base, and curve down and back (recurved). The upper canines exhibit slightsexual dimorphism, with males exhibiting slightly larger canines than females. Both sexes use them in combat by slashing with them. There is a small diastema between the upper canine and the first premolar (P2), which is smaller and more caniniform than the other premolars. Unlike other lemurs, the first two upper molars (M1 and M2) have prominent lingual cingulae, yet do not have a protostyle.[3]
The ring-tailed lemur isdiurnal and semi-terrestrial.[34] It is the most terrestrial of lemur species, spending as much as 33% of its time on the ground. However it is still considerablyarboreal, spending 23% of its time in the mid-levelcanopy, 25% in the upper-level canopy, 6% in the emergent layer and 13% in small bushes. Troop travel is 70% terrestrial.[35]
Troop size, home range, and population density vary by region and food availability. Troops typically range in size from 6 to 25, although troops with over 30 individuals have been recorded. The average troop contains 13 to 15 individuals.[18] Home range size varies between 6 and 35 hectares (15 and 86 acres).[36] Troops of the ring-tailed lemur will maintain a territory, but overlap is often high. When encounters occur, they areagonistic, or hostile in nature. A troop will usually occupy the same part of its range for three or four days before moving. When it does move, the average traveling distance is 1 km (0.62 mi).[35]Population density ranges from 100 individuals per 1 km2 (0.39 sq mi) in dry forests to 250–600 individuals per km2 ingallery and secondary forests.[25]
Endemic to southern and southwesternMadagascar, the ring-tailed lemur ranges further into highland areas than other lemurs. It inhabitsdeciduous forests, dryscrub,montane humid forests, andgallery forests (forests along riverbanks). It strongly favors gallery forests, but such forests have now been cleared from much of Madagascar in order to create pasture for livestock.[25][21] Depending on location, temperatures within its geographic range can vary from −12 °C (10 °F)[24] atAndringitra Massif to 48 °C (118 °F) in the spiny forests ofBeza Mahafaly Special Reserve.[38]
This species is found as far east asTôlanaro, inland towards the mountains ofAndringitra on the southeastern plateau, among the spiny forests of the southern part of the island,[25][21] and north along the west coast to the town ofBelo sur Mer.[3] Historically, the northern limits of its range in the west extended to theMorondava River nearMorondava. It can still be found inKirindy Mitea National Park, just south of Morondava, though at very low densities. It does not occur in Kirindy Forest Reserve, north of Morondava. Its distribution throughout the rest of its range is very spotty, with population densities varying widely.[21]
Within the protected regions it is known to inhabit, the ring-tailed lemur issympatric (shares its range) with as many as 24species of lemur, covering every living genus exceptAllocebus,Indri, andVarecia. Historically, the species used to be sympatric with the critically endangered southern black-and-white ruffed lemur (Varecia variegata editorum), which was once found at Andringitra National Park; however, no sightings of the ruffed lemur have been reported in recent years.[39]
List of species sympatric with the ring-tailed lemur[39]
In western Madagascar, sympatric ring-tailed lemurs andred-fronted lemurs (Eulemur rufifrons) have been studied together. Little interaction takes place between the two species. While the diets of the two species overlap, they eat in different proportions since the ring-tailed lemur has a more varied diet and spends more time on the ground.[35]
The ring-tailed lemur is an opportunisticomnivore primarily eating fruits and leaves, particularly those of thetamarind tree (Tamarindus indica), known natively askily.[25][35] When available, tamarind makes up as much as 50% of the diet, especially during the dry, winter season.[25] The ring-tailed lemur eats from as many as three dozen different plant species, and its diet includes flowers, herbs, bark and sap. It has been observed eating decayed wood,earth, spider webs, insect cocoons,arthropods (spiders, caterpillars, cicadas and grasshoppers) and smallvertebrates (birds and chameleons).[25] During the dry season it becomes increasingly opportunistic.[40]
Ring-tailed lemurs live in groups known as "troops," which are classified asmulti-male groups, with amatriline as the core group.[41][42][43] As with most lemurs, females socially dominate males in all circumstances, including feeding priority. Dominance is enforced by lunging, chasing, cuffing, grabbing and biting. Young females do not always inherit their mother's rank and young males leave the troop between three and five years of age.[35][43] Both sexes have separate dominance hierarchies; females have a distinct hierarchy while male rank is correlated with age. Each troop has one to three central, high-ranking adult males who interact with females more than other group males and lead the troop procession with high-ranking females. Recently transferred males, old males or young adult males that have not yet left their natal group are often lower ranking. Staying at the periphery of the group they tend to be marginalized from group activity.[43]
The ring-tailed lemur will sit facing the sun to warm itself in the mornings.
For males, social structure changes can be seasonal. During the six-month period between December and May a few males migrate between groups. Established males transfer on average every 3.5 years,[35] although young males may transfer approximately every 1.4 years. Group fission occurs when groups get too large and resources become scarce.[43]
In the mornings the ring-tailed lemur sunbathes to warm itself. It faces the sun sitting in what is frequently described as a "sun-worshipping" posture orlotus position. However, it sits with its legs extended outward, not cross-legged, and will often support itself on nearby branches. Sunning is often a group activity, particularly during the cold mornings. At night, troops will split into sleeping parties huddling closely together to keep warm.[43]
Despite beingquadrupedal the ring-tailed lemur can rear up and balance on its hind legs, usually for aggressive displays. When threatened, the ring-tailed lemur may jump in the air and strike out with its short nails and sharp uppercanine teeth in a behavior termedjump fighting. This is extremely rare outside of the breeding season when tensions are high and competition for mates is intense. Other aggressive behaviors include athreat-stare, used to intimidate or start a fight, and a submissive gesture known aspulled-back lips.[43]
Border disputes with rival troops occur occasionally and it is the dominant female's responsibility to defend the troop's home range. Agonistic encounters include staring, lunging approaches and occasional physical aggression, and conclude with troop members retreating toward the center of the home range.[43]
Male ring-tailed lemurs will scent-mark saplings and branches by spur-marking.
Olfactory communication is critically important for strepsirrhines like the ring-tailed lemur. Males and femalesscent mark both vertical and horizontal surfaces at the overlaps in their home ranges using theiranogenital scent glands. The ring-tailed lemur will perform a handstand to mark vertical surfaces, grasping the highest point with its feet while it applies its scent.[43] Use of scent marking varies by age, sex and social status.[44] Male lemurs use their antebrachial and brachial glands to demarcate territories and maintain intragroup dominance hierarchies. The thorny spur that overlays the antebrachial gland on each wrist is scraped against tree trunks to create grooves anointed with their scent. This is known asspur-marking.[43]
In displays of aggression, males engage in a social display behaviour calledstink fighting, which involves impregnating their tails with secretions from the antebrachial and brachial glands and waving the scented tail at male rivals.[45]
Ring-tailed lemurs have also been shown tomark using urine. Behaviorally, there is a difference between regular urination, where the tail is slightly raised and a stream of urine is produced, and the urine-marking behavior, where the tail is held up in display and only a few drops of urine are used.[46][47] The urine-marking behavior is typically used by females to mark territory, and has been observed primarily at the edges of the troop's territory and in areas where other troops may frequent.[48] The urine marking behavior also is most frequent during the mating season, and may play a role in reproductive communication between groups.[46]
Ring-tailed lemurs are some of the most vocal primates.
The ring-tailed lemur is one of the most vocal primates and has a complex array of distinctvocalizations used to maintain group cohesion during foraging and alert group members to the presence of a predator. Calls range from simple to complex. An example of a simple call is the purr (listenⓘ), which expresses contentment. A complex call is the sequence of clicks, close-mouth click series (CMCS), open-mouth click series (OMCS) and yaps (listenⓘ) used duringpredator mobbing. Some calls have variants and undergo transitions between variants, such as an infant "whit" (distress call) transitioning from one variant to another (listenⓘ).[49]
The most commonly heard vocalizations are the moan (listenⓘ) (low-to-moderate arousal, group cohesion), early-high wail (listenⓘ) (moderate-to-high arousal, group cohesion), and clicks (listenⓘ) ("location marker" to draw attention).[49]
In the wild, females typically give birth to a single offspring.
The ring-tailed lemur ispolygynandrous,[35] although the dominant male in the troop typically breeds with more females than other males. Fighting is most common during the breeding season.[50] A receptive female may initiate mating by presenting her backside, lifting her tail, and looking at the desired male over her shoulder. Males may inspect the female's genitals to determine receptiveness. Females typically mate within their troop, but may seek outside males.[51][35]
The breeding season runs from mid-April to mid-May.Estrus lasts 4 to 6 hours,[18] and females mate with multiple males during this period.[35] Within a troop, females stagger their receptivity so that each female comes into season on a different day during the breeding season, reducing competition for male attention.[52] Females lactate during the wet season, from December through April, when resources are readily available. Females gestate during the dry season, from May through September, when resources are low. Females give birth during seasons where resources, such as flowers, are in peak.[53]Gestation lasts for about 135 days, andparturition occurs in September or occasionally October. In the wild, one offspring is the norm, although twins may occur. Ring-tailed lemur infants have a birth weight of 70 g (2.5 oz) and are carried ventrally (on the chest) for the first 1 to 2 weeks, then dorsally (on the back).[18]
The young lemurs begin to eat solid food after two months and are fully weaned after five months. Sexual maturity is reached between 2.5 and 3 years.[50] Male involvement in infant rearing is limited, although the entire troop, regardless of age or sex, can be seen caring for the young.Alloparenting between troop females has been reported. Kidnapping by females andinfanticide by males also occur occasionally.[43] Due to harsh environmental conditions, predation and accidents such as falls, infant mortality can be as high as 50% within the first year and as few as 30% may reach adulthood.[18] The longest-lived ring-tailed lemur in the wild was a female at the Berenty Reserve who lived for 20 years.[25] In the wild, females rarely live past the age of 16, whereas the life expectancy of males is not known due to their social structure. The longest-lived male was reported to be 15 years old. The maximum lifespan reported in captivity was 27 years.[3]
Historically, the studies oflearning andcognition in non-human primates have focused onsimians (monkeys and apes), while strepsirrhine primates, such as the ring-tailed lemur and its allies, have been overlooked and popularly dismissed as unintelligent.[54] A couple of factors stemming from early experiments have played a role in the development of this assumption. First, theexperimental design of older tests may have favored the natural behavior and ecology of simians over that of strepsirrhines, making the experimental tasks inappropriate for lemurs. For example, simians are known for their manipulative play with non-food objects, whereas lemurs are only known to manipulate non-food objects in captivity.[55] This behavior is usually connected with food association. Also, lemurs are known to displace objects with their nose or mouth more so than with their hands.[54] Therefore, an experiment requiring a lemur to manipulate an object without prior training would favor simians over strepsirrhines. Second, individual ring-tailed lemurs accustomed to living in a troop may not respond well to isolation for laboratory testing. Past studies have reported hysterical behavior in such scenarios.[56]
The notion that lemurs are unintelligent has been perpetuated by the view that theneocortex ratio (as a measure of brain size) indicates intelligence.[57] In fact,primatologistAlison Jolly noted early in her academic career that some lemur species, such as the ring-tailed lemur, have evolved a social complexity similar to that ofcercopithecine monkeys, but not the corresponding intelligence.[58] After years of observations of wild ring-tailed lemur populations at theBerenty Reserve in Madagascar and as well as baboons in Africa, Jolly concluded that this highly social lemur species does not demonstrate the equivalent social complexity of cercopithecine monkeys, despite general appearances.[59]
Regardless, research has continued to illuminate the complexity of the lemur mind, with emphasis on the cognitive abilities of the ring-tailed lemur. As early as the mid-1970s, studies had demonstrated that they could be trained throughoperant conditioning using standardschedules of reinforcement. The species has been shown to be capable of learning pattern, brightness, and object discrimination, skills common amongvertebrates. The ring-tailed lemur has also been shown to learn a variety of complex tasks often equaling, if not exceeding, the performance of simians.[54]
More recently, research at theDuke Lemur Center has shown that the ring-tailed lemur can organize sequences in memory and retrieve ordered sequences without language.[60] The experimental design demonstrated that the lemurs were using internal representation of the sequence to guide their responses and not simply following a trained sequence, where one item in the sequence cues the selection of the next.[60] But this is not the limit of the ring-tailed lemur's reasoning skills. Another study, performed at theMyakka City Lemur Reserve, suggests that this species along with several other closely related lemur species understand simple arithmetic operations.[61]
Since tool use is considered to be a key feature of primate intelligence, the apparent lack of this behavior in wild lemurs, as well as the lack of non-food object play, has helped reinforce the perception that lemurs are less intelligent than their simian cousins.[55] However, another study at the Myakka City Lemur Reserve examined the representation of tool functionality in both the ring-tailed lemur and thecommon brown lemur and discovered that, like monkeys, they used tools with functional properties (e.g., tool orientation or ease of use) instead of tools with nonfunctional features (e.g., color or texture). Although the ring-tailed lemur may not use tools in the wild, it can not only be trained to use a tool, but will preferentially select tools based on their functional qualities. Therefore, the conceptual competence to use a tool may have been present in the common primate ancestor, even though the use of tools may not have appeared until much later.[62]
In addition to being listed asendangered in 2014 by the IUCN,[1] the ring-tailed lemur has been listed since 1977 byCITES underAppendix I,[2] which makes trade of wild-caught specimens illegal. Although there are more endangered species of lemur, the ring-tailed lemur is considered aflagship species due to its recognizability.[63] As of 2017, only about 2,000 ring-tailed lemurs are estimated to be left in the wild, making the threat of extinction far more serious for them than previously believed.[5]
Three factors threaten ring-tailed lemurs. First and foremost ishabitat destruction. Starting nearly 2,000 years ago with the introduction of humans to the island, forests have been cleared to produce pasture and agricultural land.[63] Extraction of hardwoods for fuel and lumber, as well mining andovergrazing, have also taken their toll. Today, it is estimated that 90% of Madagascar's original forest cover has been lost.[64] Rising populations have created even greater demand in the southwest portion of the island for fuel wood,charcoal, and lumber. Fires from the clearing of grasslands, as well as slash-and-burn agriculture destroy forests. Another threat to the species is harvesting either for food (bushmeat),fur clothing orpets. Finally, periodic drought common to southern Madagascar can impact populations already in decline. In 1991 and 1992, for example, a severe drought caused an abnormally high mortality rate among infants and females at theBeza Mahafaly Special Reserve. Two years later, the population had declined by 31% and took nearly four years to start to recover.[63]
The ring-tailed lemur resides in several protected areas within its range, each offering varying levels of protection. At the Beza Mahafaly Special Reserve, a holistic approach toin-situ conservation has been taken. Not only does field research and resource management involve international students and local people (including school children), livestock management is used at the peripheral zones of the reserve andecotourism benefits the local people.[63]
Outside of its diminishing habitat and other threats, the ring-tailed lemur reproduces readily and has fared well in captivity. For this reason, along with its popularity, it has become the most populous lemur inzoos worldwide, with more than 2500 in captivity as of 2009. It is also the most common of all captive primates.[21]Ex situ facilities actively involved in the conservation of the ring-tailed lemur include theDuke Lemur Center inDurham, North Carolina, theLemur Conservation Foundation in Myakka City, Florida, and theMadagascar Fauna Group headquartered at theSaint Louis Zoo. Due to the high success of captive breeding, reintroduction is a possibility if wild populations were to crash. Although experimental releases have met success onSt. Catherines Island in Georgia, demonstrating that captive lemurs can readily adapt to their environment and exhibit a full range of natural behaviors, captive release is not currently being considered.[63]
Ring-tailed lemur populations can also benefit from drought intervention, due to the availability of watering troughs and introduced fruit trees, as seen at theBerenty Private Reserve in southern Madagascar.[63] However, these interventions are not always seen favorably, since natural population fluctuations are not permitted. The species is thought to have evolved its highfecundity due to its harsh environment.[63]
The ring-tailed lemur is known locally in Malagasy asmaky (pronounced[ˈmakʲi̥], and spelledmaki in French) orhira (pronounced[ˈhirə] or colloquially[ˈir]). Being the most widely recognized endemic primate on the island, it has been selected as the symbol forMadagascar National Parks (formerly known as ANGAP).[21] TheMaki brand, which started by selling T-shirts in Madagascar and now sells clothing across the Indian Ocean islands, is named after this lemur due to its popularity, even though the company's logo portrays the face of asifaka and its name uses the French spelling.[65]
The first mention of the ring-tailed lemur in Western literature came in 1625 when English traveller and writerSamuel Purchas described them as being comparable in size to a monkey and having a fox-like long tail with black and white rings.[3]Charles Catton included the species in his 1788 bookAnimals Drawn from Nature and Engraved in Aqua-tinta, calling it the "Maucauco" and regarding it as a type of monkey.[66]
The species was further popularized by theAnimal Planet television seriesLemur Street,[67][68] as well as by the characterKing Julien in the animatedMadagascar film and TV franchise.[69] The ring-tailed lemur was also the focus of the 1996Nature documentaryA Lemur's Tale, which was filmed at the Berenty Reserve and followed a troop of lemurs. The troop included a special infant named Sapphire, who was nearlyalbino, with white fur, bright blue eyes, and the characteristic ringed tail.[70]
A Ring-tailed lemur played a role in the 1997 comedy filmFierce Creatures, starringJohn Cleese, who has a passion for lemurs.[71][72] Cleese later hosted the 1998BBC documentaryIn the Wild: Operation Lemur with John Cleese, which tracked the progress of areintroduction ofblack-and-white ruffed lemurs back into theBetampona Reserve in Madagascar. The project had been partly funded by Cleese's donation of the proceeds from the London premier ofFierce Creatures.[72][73]
^Type species was designated asCatta mococo (=Lemur catta Linnaeus, 1758).[3]
^Type species was designated asMaki mococo (=Lemur catta Linnaeus, 1758).[3][4]
^The synonymMococo is sometimes omitted because it was technically a vernacular term for the genusProsimia.[4]René Primevère Lesson named the type species for this genus asProsimia catta (=Lemur catta Linnaeus, 1758) in the same year (1878).[3]
^Muirhead (1819) credited the nameMaki mococo toAnselme Gaëtan Desmarest (1817), although it was actually used as a vernacular name.[3][4]
^The pale fork-marked lemur found at Zombitse-Vohibasia National Park may instead be a new species.[39]
^Drea, Christine M.; Weil, Anne (2008). "External genital morphology of the ring-tailed lemur (Lemur catta): Females are naturally masculinized".Journal of Morphology.269 (4):451–463.doi:10.1002/jmor.10594.PMID17972270.S2CID29073999.
^Howarth, C. J.; Wilson, J. M.; Adamson, A. P.; Wilson, M. E.; Boase, M. J. (1986). "Population ecology of the ring-tailed lemur,Lemur catta, and the white sifaka,Propithecus verreauxi verreauxi, at Berenty, Madagascar, 1981".Folia Primatologica.47 (1):39–48.doi:10.1159/000156262.PMID3557229.
^D. L. Hart (May 2000).Primates as prey: ecological, morphological and behavioral relationships between primate species and their predators. Washington University Department of Anthropology.
^Sussman, R.W. (1991). "Demography and social organization of free-rangingLemur catta in the Beza Mahafaly Reserve, Madagascar".American Journal of Physical Anthropology.84 (1):43–58.doi:10.1002/ajpa.1330840105.
^Palagi, E.; Norscia, I. (2005). "Multimodal signaling in wildLemur catta: Economic design and territorial function of urine marking".American Journal of Physical Anthropology.139 (2):182–192.doi:10.1002/ajpa.20971.PMID19051254.
^abMacedonia, J.M. (1993). "The vocal repertoire of the ring-tailed lemur (Lemur catta)".Folia Primatologica.61 (4):186–217.doi:10.1159/000156749.PMID7959437.
^abAnderson, R. (1999)."Lemur catta". Animal Diversity Web. Retrieved2008-04-18.
^Sauther, Michelle L. (1993). "Resource Competition in Wild Populations of Ringtailed Lemurs (Lemur Catta): Implications for Female Dominance". In Kappeler, P. M.; Ganzhorn, J. U. (eds.).Lemur Social Systems and Their Ecological Basis. Boston, MA: Springer. pp. 135–152.doi:10.1007/978-1-4899-2412-4_10.ISBN978-1-4899-2414-8.
Gould, L.; Sauther, M. (2007). "Lemuriformes". In Campbell, C.; Fuentes, A.; MacKinnon, K.; Stumpf, R.M.; Bearder, S. (eds.).Primates in Perspective. Oxford University Press. p. 53.ISBN978-0-19-517133-4.
Gouzoules, H.; Gouzoules, S. (2007). "The Conundrum of Communication". In Campbell, C.; Fuentes, A.; MacKinnon, K.; Stumpf, R.M.; Bearder, S. (eds.).Primates in Perspective. Oxford University Press. p. 624.ISBN978-0-19-517133-4.
Goodman, S.M.; Rakotoarisoa, S.V.; Wilmé, L. (2006). "The Distribution and Biogeography of the Ringtailed Lemur (Lemur catta) in Madagascar". In Jolly, A.; Sussman, R.W.; Koyama, N.; Rasamimanana, H. (eds.).Ringtailed Lemur Biology. Springer. pp. 3–15.ISBN978-0-387-32669-6.
Jolly, A.; Sussman, R.W. (2006). "Chapter 2: Notes on the History of Ecological Studies of Malagasy Lemurs". In Gould, L.; Sauther, M.L. (eds.).Lemurs: Ecology and Adaptation. Springer. pp. 19–39.ISBN978-0-387-34585-7.
Sussman, R.W. (1999).Primate Ecology and Social Structure. Vol. 1: Lorises, Lemurs and Tarsiers. Pearson Custom Pub. pp. 154–173.ISBN978-0-536-02256-1.
Tattersall, I. (1982).The Primates of Madagascar. Columbia University Press. pp. 43–46.ISBN978-0-231-04704-3.
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