Eulemur rufusred-fronted lemur

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Geographic Range

Red-fronted lemurs, Eulemur rufus are found only on the island of Madagascar and are located in two distinct populations on the eastern and western portions of the island. The eastern population is bounded in the north by the Onive and Mangoro Rivers and in the south by the slopes of Andringitra. There is another population on the south-eastern slopes of Andringitra Massif, which shares a 60 km wide hybridization zone with Eulemur cinereiceps around the Iantara River. In the west, red-fronted lemurs are found south of the Fiherenana River near Toliara, and north up to the Betsiboka River. There is also a separate population south of Pic d’Ivohibe. (Garbutt, 2007; Irwin, et al., 2005)

Habitat

Red-fronted lemurs reside in primary and secondary rainforest and the interiors of dry deciduous forest. There are lower densities of this species in edge habitats, (the boundaries of two different habitats, such as a forest and a field), due to the reduced heights and diameters of trees in these areas. Red-fronted lemurs are found at altitudes of 275 to 1670 m above sea level. (Garbutt, 2007; Hoffmann, 2008; Lehman, 2007)

  • Range elevation
    275 to 1670 m
    902.23 to 5479.00 ft

Physical Description

Red-fronted lemurs range from 2.18 to 2.25 kg in mass, and have a mean body length of 378 mm and a tail length of 499 to 508 mm. There is considerable variation in testicle size within males of this species, as some males have a testicular volume that is 2 to 7 times larger than others.

Although there is no sexual dimorphism in size, there are differences in coloration between the sexes. Male red-fronted lemurs have a grizzled grey to grey-brown dorsal pelage and a lighter creamy-grey pelage on the underside. The face, muzzle, and mid-forehead are black, with a thin dark line extending up into and dividing the russet orange crown. Their cheeks and beard are distinctively bushy and white, and they have white eyebrow patches. There is considerable regional variation among females, which have grey-brown to red/orange-brown dorsal pelage and tail and pale grey underparts. Females also have a black face and muzzle with a dividing line extending up to the crown, although their crown is grizzled grey in color. They also have white eyebrow patches and white cheeks, although they are somewhat less bushy than those of the males. (Garbutt, 2007; Glander, et al., 1992)

  • Sexual Dimorphism
  • sexes colored or patterned differently
  • Range mass
    2.18 to 2.25 kg
    4.80 to 4.96 lb
  • Average length
    378 mm
    14.88 in

Reproduction

Red-fronted lemurs in central western Madagascar are polygynous and live in groups with multiple males and females. In each group, resident females interact more frequently with a single "central" male than with other males. Females copulate significantly more frequently with the central male than with other resident males. However, females do not have exclusive mates and copulate with almost all males in the group during their cycle. In general, there is a lack of strong male-female bonds or special relationships in this species. Male red-fronted lemurs possess relatively large testes, likely indicating the importance of sperm competition as a driving force of intrasexual selection. Frequency of infanticide by resident males is reduced due to the discreet estrus cycle and subsequent polygynous mating system of red-fronted lemurs. (Ostner and Kappeler, 1999)

Female red-fronted lemurs are fertile for only 1 to 3 days, but they copulate for a period of several days to weeks before and after the likely days of ovulation. Females are generally synchronous in their breeding intervals and do not show any visible signs of estrus, and therefore are not monopolized by males. Copulation usually occurs during May and June, and births usually occur during early to mid-October. Gestation lasts approximately 120 days. Young weigh approximately 75 g at birth. Females generally give birth to 1 offspring each year.

Female red-fronted lemurs lactate for 6 months after giving birth. During this period, females and their newborns are spatially isolated from other members of the group. Infant mortality in southeastern Madagascar ranged from 23 and 45 % over a period of 15 years. (Duke Lemur Center, 2012; Ostner and Kappeler, 1999; Overdorff, 1998)

Female red-fronted lemurs reach sexual maturity between 2 and 4 years of age. However, in two groups in southeastern Madagascar, young females (between 2 and 6 years) had a lower probability of reproductive success than females greater than 6 years of age. Reproductive success has also been tied to maternal body weight, with greater infant production and survival when mothers weigh between 2.3 and 2.6 kg. Males reach sexual maturity at 3 to 4.5 years of age. (Overdorff, et al., 1999)

  • Breeding interval
    Red-fronted lemurs breed once yearly.
  • Breeding season
    Red-fronted lemurs mate during May and June.
  • Average number of offspring
    1
  • Average gestation period
    120 days
  • Average weaning age
    6 months
  • Range age at sexual or reproductive maturity (female)
    2 to 4 years
  • Range age at sexual or reproductive maturity (male)
    3 to 4.5 years

Female red-fronted lemurs show strong investment in their offspring and separate themselves and their infants from the social group after birth. Initially, a mother carries her infant on her belly. After approximately 1 month, the infant gains some motile independence and rides on its mother’s back. Infants are weaned at approximately 6 months of age. (Garbutt, 2007)

In Ranomafana National Park in southeastern Madagascar, infant red-fronted lemurs separated themselves from their mothers for the first time at 26 days of age. The infants first gained locomotory independence at 55 days and were rejected by their mothers for riding the following day. They first consumed solid food at 55 days, and at 96 days they were rejected by their mothers for nipple feeding. (Overdorff, 1996)

Male red-fronted lemurs do not carry or provide food for infants. However, they may allow infants to feed alongside them once offspring are independently mobile. Males show some interest in newborns, but generally do not provide any direct infant care. (Overdorff, 1996; Overdorff, 1998)

  • Parental Investment
  • female parental care
  • pre-hatching/birth
    • provisioning
      • female
    • protecting
      • female
  • pre-weaning/fledging
    • provisioning
      • female
    • protecting
      • female
  • pre-independence
    • provisioning
      • female
    • protecting
      • female

Lifespan/Longevity

Red-fronted lemurs generally live 20 to 25 years in the wild, although lifespan in the wild has been estimated to be 30.8 years. (Duke Lemur Center, 2012; Erhart and Overdorff, 2008)

  • Typical lifespan
    Status: wild
    20 to 30.8 years

Behavior

Red-fronted lemurs display cathemeral behavior, whereby their periods of activity are irregularly distributed throughout a span of 24 hours. Generally, they engage in 3.5 times more activity during the day than at night. Their nocturnal activity is correlated with the lunar cycle, with significantly more activity taking place during nights with greater brightness, indicating that light availability is an important factor for the distribution of cathemeral activity. (Kappeler and Erkert, 2003)

Red-fronted lemurs live in social groups, which range from 5 to 18 individuals. Group composition changes frequently; in one population, 2.0 individuals transferred into or out of a group per year. The social structure of red-fronted lemurs is quite flexible. Often groups contain a central male with a surrounding group. Beneficial male-female dyads have been observed under conditions of food scarcity and dietary duress, but are not habitual. Red-fronted lemurs in captivity engage in post-conflict amiable social interactions, such as mutual tongue-licking and grooming, which may function as a form of reconciliation. Furthermore, both male and female red-fronted lemurs participate in inter-group agonistic encounters, which may indicate group alliances against other lemur groups. (Erhart and Overdorff, 2008; Kappeler, 1993; Ostner and Kappeler, 1999; Overdorff, 1996; Overdorff, 1998)

Male red-fronted lemurs between 3 and 4.5 years of age frequently immigrate to new groups and join a new group within 6 to 12 months of emigration. Within the first month of arrival, male immigrants do not encounter aggression from other group members and are not peripheral to the social structure of the group. Once they have immigrated, non-natal males appear to remain in the same social group until old age. However, as males age, they are more likely to become peripheral to the group, while younger non-natal males are socially integrated into the group. In western Madagascar, female red-fronted lemurs have been observed emigrating from the group upon entering puberty at 23 to 26 months of age. (Ostner and Kappeler, 2004; Overdorff, et al., 1999)

Unlike many species of lemurs, red-fronted lemur social groups are not dominated by females. However, females have feeding priority and are primarily responsible for directing the group to food sources. This control over the content and nutrition of their daily food intake may have a positive impact upon their long-term reproductive success. (Duke Lemur Center, 2012; Erhart and Overdorff, 2008; Glander, et al., 1992)

Due to the low seasonal temperatures of Madagascar and the low basal metabolic rate of red-fronted lemurs, groups respond to cold stress with inactivity and social thermoregulation, or huddling together for warmth. In such circumstances, subordinate males more frequently participate in male-only social thermoregulation. (Ostner, 2002)

  • Average territory size
    1 km^2

Home Range

The home range of red-fronted lemurs is quite large, typically spanning over 100 ha, 50 ha of which are used as a core area. Red-fronted lemurs are averse to habitat change, but move up to 5 km away from their home range in response to dietary stress. (Erhart and Overdorff, 2008; Gould and Overdorff, 2002)

Communication and Perception

Red-fronted lemurs utilize a variety of vocalizations, including grunts and contact calls. These include a nasaly "ohn" sound, which is used to maintain group cohesion, a high pitched territorial "cree," and a "crou," which is an alarm call. Red-fronted lemurs have several different types of alarm calls, including a general alarm call for carnivores and raptors as well as a specific alarm call for raptors.

Red-fronted lemurs also communicate using olfactory cues such as scent marking, rubbing the head against an object or another animal, and sniffing and licking of objects or the genitals of another animal. Prominent males within the group have higher rates of olfactory behavior, and thus higher rates of scent-marking may indicate social status within the group. Hourly rates of olfactory events range from 2.76 to 2.85 for central males, versus 0.59 to 0.87 for other males. Male red-fronted lemurs engage with female scents significantly more often than the reverse. Males occasionally rub their heads on the anogenital region of a female or on an object close to her. (Fichtel, 2004; Garbutt, 2007; Gould and Overdorff, 2002; Ostner and Kappeler, 1999; Smithsonian National Zoological Park, 2012)

Food Habits

Red-fronted lemurs are highly frugivorous, and fruit makes up more than 50 % of their diet. They also consume leaves, flowers, insects, arthropods, and other food items.

In Ranomafana National Park in southeastern Madagascar, red-fronted lemurs spend an average of 173.0 min per day feeding. Daily amount of time feeding is negatively correlated with fruit availability. Red-fronted lemurs initiate on average 21.7 feeding bouts per day and feed for an average of 8.5 min in a given session. Red-fronted lemurs migrate seasonally when the fruit availability is low.

Red-fronted lemurs consume plant material from 104 plant species and acquire fruit from over 50 % of plant species in their diet. The mostly commonly exploited species are Harungana madagascariensis, Gambeya madagascariensis, Chrysophyllum boivinianum, and Ficus pyrifolia, and red-fronted lemurs primarily obtain fruit from these plants. They also consume new and mature leaves and whole flowers from plants.

From October to March, red-fronted lemurs consume insects and millipedes, with a peak consumption period in November. They eat a variety of insects, including walking sticks, red ants, and flies. Red-fronted lemurs can lick red ants from a tree while hanging vertically and grab flies out of the air. Red-fronted lemurs "wash" some species of millipedes before ingesting them. After removing a millipede from a branch, they place one end of the millipede in their mouths and wait for saliva to foam at the corners of their mouths. They proceed to roll the millipede between their hands or on their abdomens and persist in covering the millipede with saliva for another 5 to 6 minutes. They then consume the millipede in five or six bites. Red-fronted lemurs also eat pillbugs, but do not process them.

On rare occasions, red-fronted lemurs ingest dirt, mushrooms, leaf petioles, feces, and bark. The dirt consumed is either red clay, acquired from trails, or black soil, acquired from the banks of stream beds. Coprophagy was observed when an individual in the group defecated on a branch and another individual picked up the feces and consumed it.

Adult red-fronted lemurs also regurgitate and re-swallow food. They accomplish this by tilting their head back, pointing their nose vertically, vomiting, and then swallowing the vomitus. This regurgitation activity takes place during rest periods after feeding on unripe fruit and mature leaves and may be a tactic to re-digest some food materials more efficiently.

When obtaining water, red-fronted lemurs drink from both terrestrial and arboreal sources, such as streams, puddles, and hollow portions of fallen trees. (Overdorff, 1993)

  • Animal Foods
  • insects
  • terrestrial non-insect arthropods
  • Plant Foods
  • leaves
  • wood, bark, or stems
  • fruit
  • flowers
  • Other Foods
  • dung

Predation

Known predators of red-fronted lemurs in Ranomafana National Park include fossa (Cryptoprocta ferox), Madagascar harrier-hawks (Polyboroides radiatus), and Henst’s goshawks (Accipiter henstii).

When red-fronted lemurs first hear vocalizations of predators, they increase vigilance and decrease activity levels for approximately one hour. Upon hearing the vocalization of an aerial predator, individuals search the sky, move lower in the canopy, and emit an alarm call or flee. On observing a terrestrial predator, individuals move higher in the canopy, heighten vigilance, and emit an alarm call.

There is no evidence to support that living in large social groups is a successful anti-predator strategy in red-fronted lemurs. Although large groups include more alert individuals or provide a sort of "dilution effect," a large group is noisy and may easily attract predators. (Karpanty and Wright, 2007)

Ecosystem Roles

Across Madagascar, Eulemur rufus is sympatric with many other species of lemurs. In the western region of the island, E. rufus and Propithecus verreauxi share the same predators and have similar responses to predator recognition. The two species are able to understand conspecific aerial and general alarm calls in response to predators and have a mutually beneficial relationship of predator warning.

In both dry deciduous forests and rainforests, red-fronted lemurs are also important contributors to seed dispersal. (Fichtel, 2004; Garbutt, 2007)

Red-fronted lemurs in Tsiombokibo Forest in western Madagascar are parisitized by Lemurostrongylus spp. and Trichurus spp. Mites of the family Laelapidae have been found on the facial region and ears of red-fronted lemurs and do not appear to cause itching or irritation. (Junge and Louis, 2005)

  • Ecosystem Impact
  • disperses seeds
Commensal/Parasitic Species

Economic Importance for Humans: Positive

Red-fronted lemurs may contribute to tourism or indirect economic investment in Madagascar due to the unique presence of lemurs on the island.

Economic Importance for Humans: Negative

There are no known adverse effects of red-fronted lemurs on humans.

Conservation Status

In 2000, Eulemur rufus was classified as a species of lower risk/near threatened by the IUCN. Currently, the species is provisionally listed as Data Deficient, due to previous conflation of E. rufus and E. rufifrons in population studies. However, due to threats, it is likely that E. rufus will be listed as near threatened or vulnerable in the future. Historically, these threats have included selective logging and use of forest products within lemur habitat, reducing habitat and causing dietary stress. This species is listed on Appendix I of CITES. (Erhart and Overdorff, 2008; Hoffmann, 2008)

Other Comments

Eulemur rufus was once considered a subspecies of E. fulvus, which contained 5 to 6 other subspecies. In 2001, Groves re-classified all of the subspecies to full species based on distinct external appearances, craniodental morphology, and genetic evidence. Additionally, E. rufifrons was recently separated from E. rufus based on morphological and genetic data. These species, however, may require further taxonomic revision as additional data is gathered on the lemurs of Madagascar. (Groves, 2001; Groves, 2007; Mittermeier, et al., 2008; Pastorini, et al., 2003)

Contributors

Amelie Peisl (author), Yale University, Eric Sargis (editor), Yale University, Rachel Racicot (editor), Yale University, Gail McCormick (editor), Animal Diversity Web Staff.

Glossary

Ethiopian

living in sub-Saharan Africa (south of 30 degrees north) and Madagascar.

World Map

acoustic

uses sound to communicate

arboreal

Referring to an animal that lives in trees; tree-climbing.

bilateral symmetry

having body symmetry such that the animal can be divided in one plane into two mirror-image halves. Animals with bilateral symmetry have dorsal and ventral sides, as well as anterior and posterior ends. Synapomorphy of the Bilateria.

chemical

uses smells or other chemicals to communicate

crepuscular

active at dawn and dusk

diurnal
  1. active during the day, 2. lasting for one day.
ecotourism

humans benefit economically by promoting tourism that focuses on the appreciation of natural areas or animals. Ecotourism implies that there are existing programs that profit from the appreciation of natural areas or animals.

endothermic

animals that use metabolically generated heat to regulate body temperature independently of ambient temperature. Endothermy is a synapomorphy of the Mammalia, although it may have arisen in a (now extinct) synapsid ancestor; the fossil record does not distinguish these possibilities. Convergent in birds.

female parental care

parental care is carried out by females

forest

forest biomes are dominated by trees, otherwise forest biomes can vary widely in amount of precipitation and seasonality.

frugivore

an animal that mainly eats fruit

herbivore

An animal that eats mainly plants or parts of plants.

island endemic

animals that live only on an island or set of islands.

motile

having the capacity to move from one place to another.

native range

the area in which the animal is naturally found, the region in which it is endemic.

nocturnal

active during the night

polygynandrous

the kind of polygamy in which a female pairs with several males, each of which also pairs with several different females.

polygynous

having more than one female as a mate at one time

rainforest

rainforests, both temperate and tropical, are dominated by trees often forming a closed canopy with little light reaching the ground. Epiphytes and climbing plants are also abundant. Precipitation is typically not limiting, but may be somewhat seasonal.

scent marks

communicates by producing scents from special gland(s) and placing them on a surface whether others can smell or taste them

seasonal breeding

breeding is confined to a particular season

sexual

reproduction that includes combining the genetic contribution of two individuals, a male and a female

social

associates with others of its species; forms social groups.

tactile

uses touch to communicate

terrestrial

Living on the ground.

tropical

the region of the earth that surrounds the equator, from 23.5 degrees north to 23.5 degrees south.

visual

uses sight to communicate

References

Duke Lemur Center, 2012. "Red Fronted Lemur" (On-line). Duke Lemur Center. Accessed July 19, 2012 at http://lemur.duke.edu/red-fronted-brown-lemur/.

Erhart, E., D. Overdorff. 2008. Population demography and social structure changes in Eulemur fulvus rufus from 1988 to 2003. American Journal of Physical Anthropology, 136: 183-193.

Fichtel, C. 2004. Reciprocal recognition of sifaka (Propithecus verreauxi verreauxi) and redfronted lemur (Eulemur fulvus rufus) alarm calls. Animal Cognition, 7: 45-52.

Garbutt, N. 2007. Mammals of Madagascar: A Complete Guide. New Haven: Yale University Press.

Glander, K., P. Wright, P. Daniels, A. Merenlender. 1992. Morphometrics and testicle size of rain forest lemur species from southeastern Madagascar. Journal of Human Evolution, 22: 1-17.

Gould, L., D. Overdorff. 2002. Adult male scent-marking in Lemur catta and Eulemur fulvus rufus. International Journal of Primatology, 23: 575-586.

Groves, C. 2001. Primate Taxonomy. Washington, DC: Smithsonian Books.

Groves, C. 2007. Red-fronted lemurs are not the same as red lemurs. Australasian Primatology, 18: 23.

Hoffmann, M. 2008. "Eulemur rufus" (On-line). In: IUCN 2012. IUCN Red List of Threatened Species. Version 2012.1. Accessed April 09, 2012 at http://www.iucnredlist.org/apps/redlist/details/8209/0.

Irwin, M., S. Johnson, P. Wright. 2005. The state of lemur conservation in south-eastern Madagascar: population and habitat assessment for diurnal and cathemeral lemurs using surveys, satellite imagery and GIS. Oryx, 39: 204-218.

Junge, R., E. Louis. 2005. Biomedical evaluation of two sympatric lemur species (Propithecus verreauxi deckeni and Eulemur fulvus rufus) in Tsiombokibo Classified Forest, Madagascar. Journal of Zoo and Wildlife Medicine, 36: 581-589.

Kappeler, P. 1993. Reconciliation and post-conflict behavior in ring-tailed lemurs, Lemur catta and redfronted lemurs, Eulemur fulvus rufus. Animal Behavior, 45: 901-915.

Kappeler, P., H. Erkert. 2003. On the move around the clock: correlates and determinants of cathemeral activity in wild redfronted lemurs (Eulemur fulvus rufus). Behavioral Ecology and Sociobiology, 54: 359–369.

Karpanty, S., P. Wright. 2007. Predation on lemurs in the rainforest of Madagascar by multiple predator species: observations and experiments. Developments in Primatology: Progress and Prospects, 2: 77-99.

Lehman, S. 2007. Spatial variations in Eulemur fulvus rufus and Lepilemur mustelinus densities in Madagascar. Folia Primatologica, 78: 46-55.

Mittermeier, R., J. Ganzhorn, W. Konstant, K. Glander, I. Tattersall, C. Groves, A. Rylands, A. Hapke, J. Ratsimbazafy, M. Mayor, E. Louis, Y. Rumpler, C. Schwitzer, R. Rasoloarison. 2008. Lemur Diversity in Madagascar. International Journal of Primatology, 29: 1607-1656.

Ostner, J. 2002. Social Thermoregulation in Redfronted Lemurs (Eulemur fulvus rufus). Folia Primatologica, 73: 175-180.

Ostner, J., P. Kappeler. 1999. Central males instead of multiple pairs in redfronted lemurs, Eulemur fulvus rufus (Primates, Lemuridae)?. Animal Behavior, 58: 1069-1078.

Ostner, J., P. Kappeler. 2004. Male life history and the unusual adult sex ratios of redfronted lemur, Eulemur fulvus rufus, groups. Animal Behavior, 67: 249-259.

Overdorff, D. 1998. Are Eulemur species pair-bonded? Social organization and mating strategies in Eulemur fulvus rufus from 1988–1995 in southeast Madagascar. American Journal of Physical Anthropology, 105: 153-166.

Overdorff, D. 1996. Ecological correlates to social structure in two lemur species in Madagascar. American Journal of Physical Anthropology, 100: 487-506.

Overdorff, D. 1993. Similarities, differences, and seasonal patterns in the diets of Eulemur rubriventer and Eulemur fulvus rufus in the Ranomafana National Park, Madagascar. International Journal of Primatology, 14: 721-753.

Overdorff, D., A. Merenlender, P. Talata, A. Telo, Z. Forward. 1999. Life History of Eulemur fulvus rufus From 1988–1998 in Southeastern Madagascar. American Journal of Physical Anthropology, 108: 295-310.

Pastorini, J., U. Thalmann, R. Martin. 2003. A molecular approach to comparative phylogeography of extant Malagasy lemurs. Proceedings of the National Academy of Sciences of the United States of America, 100: 5879-5884.

Smithsonian National Zoological Park, 2012. "Red-fronted Lemurs" (On-line). Smithsonian National Zoological Park. Accessed July 19, 2012 at http://nationalzoo.si.edu/Animals/Primates/Facts/FactSheets/Lemurs/RedFrontedlemur/default.cfm.