name = Ruffed lemursMSW3 Groves|pages=Varecia|id=12100059]
Black-and-white Ruffed Lemur
genus = "Varecia"
genus_authority = Gray, 1863
type_species = "Lemur varius"
type_species_authority = É. Geoffroy
( "Lemur macaco variegatus" Kerr, 1792)
subdivision = "Varecia variegata" "Varcia rubra"
range_map_caption=Distribution of "Varecia spp."Mittermeier, p. 304] The ruffed lemurs of the
genus"Varecia" are Strepsirhine primates and the largest extant lemurs within the family Lemuridae.cite book | last = Sussman | first = R.W. | title = Primate Ecology and Social Structure | volume = Vol. 1: Lorises, Lemurs, and Tarsiers | edition = Revised 1st Edition | pages = pp. 195-200 | publisher = Pearson Custom Publishing | origyear = 1999| year = 2003 | isbn=0-536-74363-0] Like all lemurs, they are found only on the island of Madagascar. Formerly recognized as a monotypicgenus, two speciesare now recognized: the Black-and-white Ruffed Lemur, which is further broken into 3 subspecies, and the Red Ruffed Lemur.Mittermeier, p. 303] Garbutt, p. 170-175]
Ruffed lemurs are
diurnaland arboreal quadrupeds, known for leaping through the upper canopyof the seasonal tropical rainforests in eastern Madagascar. They are also the most frugivorous of the Malagasy lemurs, and they are very sensitive to habitat disturbance.Mittermeier, p. 305-323] Ruffed lemurs live in multi-male/multi-female groups and have a complex and flexible social structure, described as fission-fusion. They are highly vocal, and are known for their loud, raucous calls.
Ruffed lemurs are seasonal breeders and highly unusual in their reproductive strategy. They are considered an "evolutionary enigma" in that they are the largest of the extant species in Lemuridae, yet exhibit reproductive traits more common in small, nocturnal lemurs, such as short
gestationperiods (~102 days) and large average litter sizes (~2-3). Ruffed lemurs also build nests for their newborns (the only primates that do so), carry them by mouth, and exhibit an absentee parental system by stashing them while they forage. Infants are altricial, although they develop relatively quickly, traveling independently in the wild after 70 days and attaining full adult size by 6 months.
Threatened by habitat loss and hunting, ruffed lemurs are facing
extinctionin the wild. However, they reproduce readily in captivity, and have been gradually re-introduced into the wild since 1997. Organizations that are involved in ruffed lemur conservation include the Durrell Wildlife Conservation Trust, the Lemur Conservation Foundation (LCF), the Madagascar Fauna Group (MFG), Monkeyland Primate Sanctuary, Wildlife Trust, and the Duke Lemur Center (DLC).
fossilrecord exists in Madagascar until recent times.Mittermeier, p. 23-26] Consequently, little is known about the evolution of ruffed lemurs, let alone the entire order Lemuriformes, which comprises the endemic primate population of the island.
Although there is still much debate about the origins of
lemurs on Madagascar, it is generally accepted that a single rafting event, similar to the one that brought New World monkeys to South America, occurred around 47-54 million years ago and allowed ancestral lemurs to cross the Mozambique Channeland colonize the island,Garbutt, p. 85-86] which had already split from Africa(while joined with Indian subcontinent), approximately 160 million years ago. The resulting founder effectand either non-existent or inferior competition resulted in speciationas the lemur ancestors radiated out to fill open or insufficiently guarded niches. Today, the endemic primate faunaof Madagascar, which includes the ruffed lemurs, remains as some of the few extant representatives of the Strepsirrhine suborder that had once spread throughout Laurasiaand Africa during the Eoceneepoch.
The genus "Varecia" contains 2 species, and 3 subspecies.
*** Genus "Lemur": the Ring-tailed Lemur
*** Genus "Eulemur": brown lemurs
*** Genus "Varecia": ruffed lemurs
Black-and-white Ruffed Lemur, "Varecia variegata"
***** "Varecia variegata variegata"
***** "Varecia variegata editorum"
***** "Varecia variegata subcincta"
Red Ruffed Lemur, "Varecia rubra"
Hapalemurinae: bamboo lemurs
Changes in taxonomy
Ruffed lemurs, along with several species of brown lemur were once included in the genus "Lemur". However, the ruffed lemurs were reassigned to the genus "Varecia" in 1962.cite book | last = Nowak | first = R.M. | publisher = Johns Hopkins University Press | title = Walker's Mammals of the World | edition = 6th Edition | year = 1999 | isbn = 0801857899 | pages = pp.517]
Initially, the Red Ruffed Lemur and the Black-and-white Ruffed Lemur were recognized as subspecies, "Varecia variegata rubra" and "Varecia variegata variegata" respectively. However, in 2001 both were elevated to species status, a decision that was later supported by genetic research. Furthermore, three subspecies of Black-and-white Ruffed Lemur, which had been published decades earlier, also where recognized: "variegata", "editorum", and "subcincta". However, this is not entirely conclusive.
Subfossilremains of two extinctlemur species were also initially classified under the genus "Varecia". Found at sites in central and southwestern Madagascar,Mittermeier, p. 43] "Varecia insignis" and "Varecia jullyi" were very similar to modern ruffed lemurs, but more robust and assumed to be more terrestrial, and thus more prone to predation by early human settlers. However, more recent studies have shown that these extinct species had a diet similar to that modern ruffed lemurs, and that they were also arboreal in nature. Furthermore, enough differences were demonstrated to merit a new genus, " Pachylemur". These close relatives of ruffed lemurs are now known as " Pachylemur insignis" and " Pachylemur jullyi".
Anatomy and physiology
Ruffed lemurs are the largest extant members of the family Lemuridae, with an average head-body length between convert|43|and|57|cm|in|lk=on|abbr=on and a total length ranging from convert|100|to|120|cm|in|abbr=on, while ranging in weight from convert|3.1|and|4.1|kg|lb|lk=on|abbr=on.cite web |last = Gron |first = KJ |date = 2007-08-17 |title = Primate Factsheets: Ruffed lemur (Varecia) Taxonomy, Morphology, & Ecology |publisher = Wisconsin Primate Research Center (WPRC) |url = http://pin.primate.wisc.edu/factsheets/entry/ruffed_lemur |accessdate = 2008-09-19] The thick, furry tail is longer than the body, averaging convert|60|and|65|cm|in|abbr=on in length and is used primarily for balance while moving through the trees. Ruffed lemurs exhibit neither
sexual dimorphismnor sexual dichromatism, and females posses three pairs of mammary glands.
Ruffed lemurs are characterized by their long,
canine-like muzzle, which includes a significant overbite. The face is mostly black, with furry "rufts" running from the ears to the neck. These rufts are either white ("V. variegata") or deep reddish ("V. rubra") in coloration, depending on the species. Likewise, the coloration of the fluffy fur also varies by species, while the coloration pattern varies by subspecies in the Black-and-white Ruffed Lemur. There are also intermediates in color variation between the two species.
As with all lemurs, the ruffed lemur has special adaptations for grooming, including a
toilet-clawon its second toe and a toothcomb.
Ruffed lemurs are considered
arboreal quadrupeds, with the most common type of movement being above-branch quadrupedalism. While in the canopy leaping, vertical clinging, and suspensory behavior, are also common, while bridging, bimanual movement, and bipedalism are infrequently seen. When moving from tree to tree, ruffed lemurs will look over the shoulder while clinging, launch themselves into the air, and twist mid-air so that their ventral surface lands on the new tree or limb. Suspensory behavior is more common in ruffed lemurs than in other lemur species. When ruffed lemurs come down to the ground, they continue to move quadrupedally, with running taking the form of bounding hops and the tail held high.
arborealand the most frugivorous of the lemurs, they thrive only in primary forestwith large fruiting trees, where they spend most of their time in the upper canopy. By spending the majority of their time in the crown of tall forest trees, they are relatively safe from predators such as the Fossa.
Ruffed lemurs are active primarily during the day (
diurnal), during which time they feed primarily on fruits and nectar, often utilizing suspensory postures while feeding. The seeds of the fruit they eat pass through their digestive tract and are propagated throughout the rainforests in their feces, helping to ensure new plant growth and a healthy forest ecosystem. These lemurs are also known to be significant pollinators of the Traveller's Tree ("Ravenala madagascariensis"). Without destroying the inflorescence, they lick the nectar from deep inside the flower using their long muzzles and tongues, collecting and transferring pollen on their snouts and fur from plant to plant. This relationship is thought to be a result of co-evolution.
Geographic range and habitat
Like all lemurs, this genus is found only on the island of Madagascar off the southeastern coast of
Africa. Confined to the island's seasonal eastern tropical rainforests, it is uncommon to rare throughout its range, which historically ran from the Masoala Peninsula in the northeast to the Mananara River in the south. Today, the Black-and-white Ruffed Lemurhas a much larger, though very patchy, distributed range than the Red Ruffed Lemur, extending from slightly northwest of Maroantsetra, on Antongil Bay, in the north down the coast to the Mananara River near Vangaindranoin the south. Additionally, a concentrated population of Black-and-white Ruffed Lemurs, of the subspecies "Varecia variegata subcincta", can also be found on the island reserve of Nosy Mangabein Antongil Bay. It is suspected that this population was introduced to the island in the 1930's. The Red Ruffed Lemur, on the other hand, has a very restricted range on the Masoala Peninsula.
confluenceof the Vohimara and Antainambalana Rivers may have been a zone of hybridization between these two species, although no conclusive results have indicated current interbreeding. In general, the Antainambalana River appears to isolate the Red Ruffed Lemurs from the neighboring subspecies of Black-and-white Ruffed Lemur, "V. v. subcincta". The subspecies "V. v. variegata" can be found further south, and "V. v. editorum" is the southernmost subspecies. The ranges of these two southern subspecies overlap and intermediate forms are reported to exist, although this has not been confirmed.
The rainforests in which these animals live are seasonal, with two primary seasons: the hot, wet season (November through April), the cool, dry season (May through October). The primary habitat for both species, regardless of season, is in the crowns of trees, spending the majority of their time convert|15|and|25|m|ft|abbr=on above ground. With the seasonal availability of resources being similar, regardless of location, there is little to no difference in tree usage between species. From September through April, more fruit is available, so females prefer the
lianas in the crowns of trees. Also, both sexes utilize the lower, major branches during the hot, rainy season. The tree crowns are predominantly used from May through August, when young leaves and flowers are in abundance.
The following lemur species can be found within the same geographic range as ruffed lemurs:
* Greater Dwarf Lemur ("Cheirogaleus major")
* Eastern Lesser Bamboo Lemur ("Hapalemur griseus griseus")
* Weasel Sportive Lemur ("Lepilemur mustelinus")
* Diademed Sifaka ("Propithecus diadema")
* Common Brown Lemur ("Eulemur fulvus")
* Red-bellied Lemur ("Eulemur rubriventer")
* Eastern Woolly Lemur ("Avahi laniger")
* Indri ("Indri indri")
* Brown Mouse Lemur ("Microcebus rufus")
* Aye-aye ("Daubentonia madagascariensis")
* White-headed Lemur ("Eulemur albifrons")
Ruffed lemurs are known to either demonstrate feeding dominance or divide resources by using different forest strata. They are dominant over Red-bellied Lemurs, while Eastern Lesser Bamboo Lemurs avoid encountering them all together. White-headed Lemurs, on the other hand, utilize the
understoryand lower canopy, below convert|15|m|ft|abbr=on, while the ruffed lemurs utilize the upper canopy, above convert|15|m|ft|abbr=on. Play has even been observed between infant ruffed lemurs and White-headed Lemurs.
Ruffed lemurs, on average, spend 28% of the day feeding, 53% resting, and 19% traveling, although differences in resting and feeding durations have been observed between males and females, with females resting less and feeding more. They are diurnal, although peak activity occurs during the early morning and late afternoon or evening, resting usually occurs around midday. When resting, ruffed lemurs often sit hunched or upright. They are also frequently seen lying prone over a branch or sunbathing in a
supine positionwith the limbs outstretched. When feeding, they will often hang upside-down by their hind feet, a type of suspensory behavior, which allows them to reach fruits and flowers.
Being highly arboreal, they spend the majority of their time in the high canopy throughout the day. Ruffed lemurs spend the majority of their time between convert|15|to|20|m|ft|abbr=on above the forest floor, followed by convert|20|to|25|m|ft up, and are least frequently seen at convert|10|to|15|m|ft. During the hot season, they will relocate to the lower canopy to help regulate their body temperature. During the cold season, ruffed lemurs are least active and may dedicate 2% of their resting time to sunbathing in order to warm up.
Long-term field research has shown that range size, group size, social systems, and territorial behavior vary widely, and may be greatly affected by food distribution and quality. It is generally agreed that the ruffed lemur social system is multi-male/multi-female with a
fission-fusion society,cite web |last = Gron |first = KJ |date = 2007-08-17 |title = Primate Factsheets: Ruffed lemur (Varecia) Behavior |publisher = Wisconsin Primate Research Center (WPRC) |url = http://pin.primate.wisc.edu/factsheets/entry/ruffed_lemur/behav |accessdate = 2008-09-19] although some populations of Black-and-white Ruffed Lemur have been reported as monogamous. This social flexibility is suspected to improve survivability despite an inflexible feeding ecology.
Being the most frugivorous members of the family Lemuridae, consuming an average of 74-90% fruit, ruffed lemurs also consume nectar (4-21%), and supplement the rest of their diet with young leaves (3-6%), mature leaves (1%), flowers (3-6%), and some seeds. Ruffed lemurs have also been reported to come to the ground to eat fungi and exhibit
The majority of their diet is made up of relatively few common plant species, with a few species providing more than 50% of the diet. Fig species of the genus
Ficus, for example, account for 78% of the fruit consumed by Red-ruffed Lemurs on the Masoala Peninsula. Although plant species and diets vary by location, the most common food plants reported from the field include the following:
* Ravensara (Family
However, fruit trees do not appear to be selected by species, but by availability and accessibility of edible fruit. And despite predominance of a few plant species in the ruffed lemur diet, the remainder of their diet consists of between 80 and 132 other species from 36 plant families.
The availability of food reflects the seasonal nature of the forests in which they live. During the hot season, fruit, flowers, and young leaves are more abundant, whereas the cold wet season offers more young leaves and flowers. Despite this, the diet changes little between seasons, except that females will consume more high-protein, low-fiber items, such as young leaves and flowers, during pregnancy and lactation in order to offset the energy costs of reproduction. Nectar is only available sporadically, yet constitutes a major food source when the flowers bloom. The nectar of the Traveller's Tree ("
Ravenala madagascariensis") is a favorite among ruffed lemurs.
The social organization of ruffed lemurs is widely variable in both group organization and group composition, although no notable difference can be seen between the two species. Ruffed lemurs are typically described as multi-male/multi-female groups with a fission-fusion social structure, although this can vary by season and locality.
In a study done at Masoala Peninsula on Red ruffed lemurs three levels of organization were identified and defined: communities, core groups, and subgroups. Communities are individuals that affiliated regularly with each other, but rarely with conspecifics outside of the community. Although the entire multi-male/multi-female community lives within a discrete home range, all individuals are never seen in the same location at the same time. Instead, individuals form dispersed social networks, known as core groups, within the community. Core groups are individuals that shared the same core area within a community territory throughout the year. Core groups typically consist of two reproductive females, as well as reproductive males and subadults, ranging in size from 2 individuals to 9. Females within the groups are cooperative, but male encounters are often agonistic. Subgroups, on the other hand, vary daily in size, composition, and duration, and consist of associated individuals from either the same core group or different core groups, depending on the season. It is from the consistent, daily changes in these subgroups that occur throughout the year, as well as the seasonal formations of core groups in core areas, that demonstrate the fission-fusion nature of ruffed lemur social structure.
In another study done at
Nosy Mangabeon Black-and-white Ruffed Lemurs a fourth level or organization was defined: affiliates. Affiliates were individuals with more persistent social bonds and more frequent interactions, usually within a core group, but sometimes also between core groups within a subgroup. Adult females typically had many affiliates, whereas adult males rarely interacted with conspecifics, living a more solitary existence.
Past studies have reported other social organizations in ruffed lemurs including monogamous
pair bonding. However, this may have been due to the use of short-term, seasonal field studies instead of yearlong studies that take into consideration the effects that changing seasons have on ruffed lemur communities. For instance, during the cold, rainy season, which corresponds with the breeding season, interactions between core groups within a community are significantly reduced. During this time small subgroups form consisting of a mature female, a mature male, and sometimes offspring. This can be misinterpreted as monogamous pair bonding.
Not only group composition, but ranging behavior can also exhibit seasonal variability. During the hot, wet season females range widely, either alone or in groups of up to 6 individuals. In the cool, dry season, smaller core groups stabilize in order to occupy concentrated areas. Therefore, during seasons when fruit is abundant subgroups are larger while scarcity is met with more solitary behavior. This suggests that although their feeding ecology is inflexible, being tied to widely distributed, patchy, and sometimes scarce fruit, ruffed lemurs instead adapt the social system in order to survive.
In terms of dominance the ruffed lemur's social structure is not as clear-cut as other lemur societies where female dominance is the norm. Although it is historically reported that "males were subordinate to females," especially with captive and free-ranging ruffed lemur populations demonstrating this, wild populations cannot be definitively labeled as matriarchal due to inter-group variation.
There are also social difference between males and females. Females typically have many affiliates and bond strongly with other females both within and outside their core areas, but do not affiliate with individuals outside the community range, except during mating season. Males, on the other hand, are more solitary, interact with only a couple conspecifics, have weak social bonds with other males, and rarely associate with others outside their core group. Furthermore, field studies suggests that only females play a role in communal home range defense. Males may scent-mark and remain relatively silent, but otherwise show little involvement during disputes.
Community range or territory size can vary widely, from convert|16|to|197|ha|km2 sqmi|abbr=on while group size can range from a single pair to 31 individuals.
Population densityis also noticeably variable. These wide ranges can be attributed to differing levels of protection and degree of environmental degradation, with better protection and a less degraded environment resulting in higher population density and more moderately sized community ranges. (The duration and seasonality of the studies involved may also have contributed to low group size estimates and community ranges. A study at the Betampona Reserve, for instance, observed monogamous pairs with 2 to 5 infants maintaining ranges of 16-43 ha.) Core areas at Ambatonakolahyconstituted approximately 10% of the overall community range and showed a close relationship with the location of the largest fruiting trees.
The average daily traveling distance for ruffed lemurs varies between convert|436|to|2250|m|ft, averaging convert|1129|m|ft per day. However, activity patterns within the community range varies by gender and season. Males generally stay within a core area all year, whereas females only confine themselves to a core area during the cold, wet season, then expand their range throughout the community range during the hot, rainy season. Females expand their traveling range slightly after giving birth, still staying within the core area, but gradually range further in December when they begin stashing their infants with other community members while they look for food. Females range the furthest later during the hot, rainy season. Both activity level and reproductive activity can be summarized in the following table.
The well-known "roar/shriek chorus" is spontaneous, occurring most often during period of high activity, as well as being contagious, involving communal participation including infants 3 to 4 months old. "Abrupt roars" are also more common during high activity and aside from alerting group members to the presence of an avian predator, they probably also help maintain contact with individuals outside of visual range or indicate an aggressive/defensive response to a disturbance. In the wild, both of these calls are emitted more during the hot, rainy season due to heighten activity. All high-amplitude calls are delivered with from a "taut" body posture.
Medium-amplitude calls operate over a shorter range or often involve moderately arousing situations, such as frustration or submission. Low-amplitude calls also generally operate over a short range, yet also cover a wider range of aggravation levels.
Whines are highly variable between individual ruffed lemurs. "Cough", "Grumble", "Squeak", and "Squeal" have only been observed and researched in the wild.
The calls of ruffed lemurs vary only slightly between the two species. In fact, in captivity, it has been documented that Red Ruffed Lemurs understand and even join in the alarm calls of Black-and-white Ruffed Lemurs. One minor difference between the vocal repertoires of these two species is in the pulse rate and frequency of the "pulsed squawk", which is much faster and higher in Red Ruffed Lemurs than Black-and-White Ruffed Lemurs and is even detectible by the human ear. The difference in this vocalization is only interspecific, showing no signs of significant sexual dimorphism within each species.
Furthermore, Red Ruffed Lemurs do not appear to produce a bona fide "wail" vocalization. In Black-and-white Ruffed Lemurs, "pulsed squawks" sometimes slow down as the group calms down, and integrate with the "wail", creating "pulsed squawk-wail intermediates" Audio2|Varecia_ pulsed_squawk-wail1.ogg. Red Ruffed Lemurs also produce "pulsed squawk-wail intermediate" sounds, but they do not exhibit long, drawn-out "wails" like the Black-and-white Ruffed Lemurs.
Breeding and reproduction
Contrary to initial reports of monogamy, ruffed lemurs in the wild exhibit seasonal polygamous breeding behavior, with both males and females mating with more than one partner within a single season. Mating is not restricted to just community members, but also involves members of neighboring communities. Females mate primarily with males with whom they had affiliative relations prior to mating season, although some matings occurred with roaming males from other communities.
Shortly before mating season begins, females exhibit swelling of the sex skin, which reaches its peak around the middle of their 14.8 day
estrous cycle. Male sexual physiology also undergoes its own change, with testicular volume increasing during mating season, peaking around the time of breeding. Aggression also increases during the mating season, both between members of the same sex and by females towards the male attempting to mate with her. Females have been observed grappling, cuffing, and biting the male during copulation. Either sex may approach the other when the female is in estrus. Initially, however, they may "roar-shriek" with each other. When a male approaches a female he often lowers his head and squeals, inspecting the female's genitalia by licking or sniffing, scent-marking, and offering a submissive chattering vocalization. When a female approaches a male, she may posture herself for mounting. Mating pairs often copulate many times during the course of a mating bout.
The mating season lasts from May through July, during the cold, rainy season, resulting in birth and peak
lactationcoinciding with the time that fruit is the most plentiful. The gestationperiod of ruffed lemurs is the shortest of the family Lemuridae, averaging 102 days (with a range of 90 to 106 days). Gestation in the wild last slighlty longer than in captivity, averaging 106 days. Just like the mating season, parturitionis also seasonal, synchronized to the end of the cold, dry season and the start of the productive hot, rainy season.
In addition to an abnormally short gestation period, ruffed lemurs share another feature with small, nocturnal lemurs by producing the largest litters of the family Lemuridae. Litters typical include two or three infants, although up to five have been reported. Birth weights in captivity average between convert|83|to|101.7|g|oz|abbr=on and range from convert|70|to|140|g|oz. Ruffed lemur infants are considered to be
altricial, and are born with their eyes open and full coat of fur.