Avahis, sifakas, and indris

(Indriidae)

Class Mammalia

Order Primates

Family Indriidae

Thumbnail description
Medium- to large-sized primates with powerful hind limbs and short snouts

Size
Weight: 2.2–16.1 lb (1.0–7.3 kg); head and body length: 10.4–20.5 in (264–520 mm)

Number of genera, species
Extinct: 6 genera, 10 species; Extant: 3 genera, 8–10 species

Habitat
Subtropical spiny desert and its gallery forest, humid moist tropical forest, tropical dry forest

Conservation status
Extinct: 10 species; Critically Endangered: 3 species; Endangered: 5–7 species

Distribution
Throughout remaining forests in Madagascar

Evolution and systematics

There are five families of primates on the island of Madagascar, all lemurs. The family Indriidae has lost three-fifths of its species in the past 1,000 years. The extinct indriids consisted of the subfamilies: the Paleopropithecinae, the sloth lemurs, and the Archaeolemurinae, the baboon lemurs. The extinct lemurs were all larger than the extant lemurs, with body weights ranging from 27–441 lb (12–200 kg). The sloth lemurs (4 genera, 7 species) and baboon lemurs (2 genera, 3 species) were found throughout the north, west, and south of Madagascar. With long forelimbs and curved finger bones, the sloth lemurs climbed slowly and hung from tree branches to feed on leaves and tough vegetation. Body weight ranges are estimated at 22–441 lb (10–200 kg). The baboon lemurs were arboreal and terrestrial quadrupeds, feeding on leaves, tough seeds, and husked fruits. Body weights are estimated at 38–62 lb (17–28 kg).

The living Indriidae is comprised of three genera, including 8–10 species (depending on the authority). The medium-sized (15.4–17.6 lb [7–8 kg]), tailless indri consists of one species Indri indri. Woolly lemurs have been divided into a widespread eastern rainforest species (Avahi laniger) and a western species A. occidentalis. Originally divided into two species, Propithecus verreauxi (a smaller-bodied species in spiny desert and dry tropical forests in western Madagascar) and P. diadema (larger-bodied, eastern rainforest), a third species P. tattersalli, the golden crowned sifaka, was described in 1988. Recent molecular and morphometric evidence suggests that the diademed sifaka group, previously allopatric subspecies, consists of four species (P. perrieri, P. candidus, P. diadema, P. edwardsi). P. tattersalli is found in both wet and dry tropical forest in a limited area near Daraina, in northeastern Madagascar. Based on molecular evidence, it has come under recent controversy as to whether it should remain a distinct species. Paleaopropithecus has been found in limestone caves of the Manamby Plateau, north of Tulear. Forest destruction and human hunting may be partially responsible for the contraction of the range of the extant species and the extinction of Paleopropithecus, Archeolemur, Archaoindris, Babakotia, Hadropithecus, and Mesopropithecus.

Physical characteristics

Indriids are medium- to large-sized prosimians. The extinct species Archeoindris fontoynonti weighed up to 400 lb (181 kg), while the smallest species in the family, the eastern woolly

lemur Avahi laniger, weighs about 2.3 lb (1 kg). Most indriids have tails shorter than their bodies, with the tail of the indri reduced to a few inches (about 5 cm). The extant indriids are magnificent leapers, with hind limbs longer than their forelimbs. Ears are small, bare or tufted, and rounded. The skin of the face is bare, and the snout is foreshortened. The eye color is often brown in woolly lemurs, orange or amber in sifakas, and yellow-green in indris. The fur is short, dense, and of various colors including brown, beige, white, orange, and black; often with head crowns, head ruffs, saddle backs, and eyebrows contrasting colors from the rest of the body. Indriids have five fingers on each of its two forefeet and five toes on each of its two hind feet; all with bare nails, except for the grooming claw on the second digit of their feet. Males have central chest scent glands, and females have anal scent glands.

Indriids have a dental tooth comb and small upper incisors with a reduced dental formula of only two premolars and four, rather than six, teeth in their tooth comb. Indriids retain the primitive primate features of a simple postorbital bar, relatively small brain case, and a well-developed rhinarium. All species of indriid, whether nocturnal or diurnal, have reflective eyes (tapetum lucidum) to increase perception in low light levels. Indriids are uniform in their cranial morphology and have a tympanic ring that lies free in the bulla and a large

stapedial artery. The digestive tract has an enlarged caecum and a large intestine for digesting vegetation.

Distribution

The family is a widespread successful group confined to Madagascar.

Habitat

Indriids are primarily arboreal, and are found in a wide range of ecotypes including primary forests, disturbed forest fragments, spiny desert, and gallery forests.

Behavior

Indriids have various social systems, with woolly lemurs and indris living in monogamous pairs, and sifakas living in

various social configurations including multi-male and multi-female. Predator attacks have been observed on woolly lemurs, indris, and sifakas. Periodic killing of both adult and infant sifakas by the carnivore fossa (Cryptoprocta ferox) has been observed with respect to rainforest sifakas. Hensti's

goshawk, a large raptor, has stalked and pursued woolly lemurs during the day, and remains have been found in the goshawk nest.

Indriids are primarily arboreal, although the Verraux's sifakas from the spiny desert occasionally travel on their hind legs in a bouncy gait for several meters. Woolly lemur families sleep together on low, shaded branches. Sifakas and indris sometimes sleep in pairs high in the trees. Indriids communicate with a variety of vocalizations from long distance piercing whistles (woolly lemurs) to loud clarinet-like duets (indris) to dog-like barking, honking, and sneezing (sifakas). All species communicate through scent marking. Chemicals from chest (males) and anal (females) glands may constitute individual signatures and indicate reproductive condition, sex, or dominance rank in sifakas. Avahis and indris do not have chest glands, but do use perianal glands in scent marking. Sexual dimorphism does not occur in body size or canine length in any indrid, and females are dominant over males in sifakas and indris. Dominance interactions have not been studied in woolly lemurs.

Feeding ecology and diet

Indriids are vegetarians, feeding on young and mature leaves of trees. In addition, rainforest sifakas feed on lianas, parasites, hemiparasites, herbs, and ferns. Sifakas eat three times as many different plant species as sympatric indris. Seeds are an important diet item for sifakas and fat intake is five times higher for sifakas than indris. Woolly lemurs eat leaves that are high in tannins, and are often found at higher densities in disturbed or edge forests. Flowers are a diet item of sifakas. Both sifakas and indris eat soil, often red clay on a weekly basis. It is unknown if woolly lemurs eat soil. Indris occasionally eat bark.

Reproductive biology

Sexual maturity is generally achieved between 3–5 years of age in indris and sifakas. Data concerning sexual maturity of woolly lemurs does not exist. Both males and females emigrate from natal groups after sexual maturity in indris, woolly lemurs, and sifakas. Male and female sifakas may change groups more than once, or occasionally remain in

their natal group for a lifetime. Sifakas are seasonal breeders, mating in December or January. Male testicles begin to increase in size three months before the mating season (when the females come into estrus). Female sifakas have a 10–36 hour interval when they are in estrus, and they may come into estrus 1–3 times each year. In the wild they usually are pregnant after one breeding season. Females have swollen, bright pink vulvas when in estrus. Sifaka mating occurs when a male clasps a female around the waist and thrusts 10–50 times. Indris mate face-to-face, while hanging from a branch. Indris gestate for about six months. The smaller verraux's sifaka has a gestation of five months, while the larger diademed sifaka gestate for six months. A single infant is born fully furred and able to cling. Weights at birth are small, less than 0.2% of the mother's weight. Weaning occurs at about six months of age.

Conservation status

IUCN conservation status is Endangered for all living indriid species except for the Critically Endangered forms of Propithecus perrieri, Propithecus diadema, and Propithecus candidus.

Significance to humans

Sifakas and indris are often protected from traditional hunting by "fadys" (taboos). Malagasies recognize the human qualities of their hands and faces and therefore do not kill them as they are considered spirits of the ancestors.

Species accounts

List of Species

Eastern woolly lemur

Avahi laniger

subfamily

Indriinae

taxonomy

Avahi laniger Jourdan, 1834, Madagscar.

other common names

Malagasy: Avahy, ampongy, fotsifaka, fotsife.

physical characteristics

Woolly lemurs are small, nocturnal lemurs, well camouflaged in beige, brown, and gray fur. Their ears are small and furred. Their noses are broad, black, and wet. Nocturnal, medium-small lemurs adopt a vertical posture. The fur is woolly and dense. The muzzle is short and dark and the head rounded with large brown eyes, accented with beige eyebrows. The fur on the thighs is bright white—like splotches of sunlight or moonlight. The head and body length is 9.8–11.6 in (250–295 mm); tail length is 12.4–14.6 in (315–370 mm), and weight is 2.0–2.9 lb (0.9–1.3 kg).

distribution

The eastern woolly lemur is found throughout the eastern rainforest, from the Marojejy Massif in the north to the Andohahela Massif in the south. A remnant population occurs in the central forest of Ambohitantely Special Reserve.

habitat

Primary and secondary forests.

behavior

Nocturnal. The animal lives in monogamous pairs and offspring with a group size of 3–5. The family group sleeps throughout the day, huddled on a horizontal branch, usually near a tree trunk about 3–8 ft (0.9–2.4 m) from the ground. Activity begins just after dusk with the family group foraging within 80 ft (25 m) of one another. During the night the family spends 40% of the night in close contact, grooming or resting over 60% of the time. Feeding occupies about 22% of their time, with traveling about 14%. Woolly lemurs communicate to one another with a long, high-pitched whistle, especially during the bright moon, and a neighboring group will respond with an answering whistle. Alarm screams are heard when an individual is chased by a raptor, but woolly lemurs are silent and still when approached, and do not mob. Woolly lemurs do not have obvious glands that secrete scent, which is unusual for a nocturnal primate. They may use anogenital glands to communicate, but this has not been documented to date. Grooming of family members occurs at dawn and dusk. The family returns to its sleep tree just before dawn.

feeding ecology and diet

Magnificent leapers, the woolly lemurs vertically cling and leap from trunk to trunk, then climb up to the canopy of trees to eat young leaves. Obligate leaf-eaters, the woolly lemurs are known to eat over 20 species of leaves but prefer the leaves of Dombeya and Harungana, both abundant tree species found in the edge or second growth forests. Leaves containing tannins are preferred diet items. They also have been seen to eat flowers.

reproductive biology

A pair occupies a home range of between 2.5–4.9 acres (1–2 hectares). Woolly lemurs live in monogamous pairs with one infant born each year. Breeding is seasonal with infants born in August and September. The gestation period is unknown, although it may be 4–5 months. The infant clings ventrally to the mother for the first week and then rides on her back up to three months after birth. In one instance, a father has been seen to carry a two-month old infant on his back. The infant develops quickly. By three months of age the infant weighs 45% of adult weight, and has a full set of adult teeth.

conservation status

Endangered.

significance to humans

Humans threaten to destroy their habitat.

Milne-Edwards's sifaka

Propithecus edwardsi

subfamily

Indriinae

taxonomy

Propithecus edwardsi (A. Grandidier, 1871), Madagascar.

other common names

Malagasy: Simpona, simpony.

physical characteristics

The face is reduced and the muzzle is shortened. Adult females and males do not show differences in weight, canine size, or coloration. Long legs, broad hands and feet, and a vertical clinging and leaping locomotion characterize sifakas. The tail is about the same length as the body. The tooth comb is used for grooming fur by both males and females. Milne-Edwards's sifakas are black with a whitish beige back saddle patch. Sifaka noses are broad, black, and not furred. Sifaka eye color ranges from amber to orange to brown. The tail is the same length and color as the body.

distribution

Milne-Edwards's sifakas are found in southeastern mountain rainforests in Madagascar from Pic Ivohibe in the south until Kiriasy, south of the Onive River. This species is not seen on the coast or in elevations less than 1,310 ft (400 m). Although abundant in Ranomafana National Park, it is rare at Andingitra National Park and very rare in forests north of Ranomafana National Park.

habitat

Primary and secondary moist, humid forests in elevations higher than 1,310 ft (400 m).

behavior

Diurnal. It lives in groups of 3–9, composed of multi-male, multi-female, one-male, or one-female. Females are dominant to males in both feeding and social situations. The group sleep huddled together on a broad horizontal branch about 49–82 ft (15–25 m) high off the ground. If the group is large, paired individuals sleep in nearby trees. The same sleep trees are used over time, but usually not on consecutive nights. During the day the family spends over 45% of the day in close contact, grooming or resting. Feeding occupies about one-third of their time, with 15% of time traveling. In contrast to indris, sifakas do not give daily long calls. Milne-Edwards's sifakas have over seven discrete calls. Lost individuals give long, warbling whistles that are answered by group members. Quieter contact moos are given among group members to indicate position and propose group movement. Alarm calls alerting for aerial predators are loud, raucous barking by all group members. Often males first sight a hawk or eagle, give the alarm bark, and the females and infants drop to the ground for protection. In contrast, a short staccato "zusss" call warns the group of proximity of terrestrial predators. Sifaka males have chest glands that secrete scent, and are used to scent mark over the anogenital marks that females rub on vertical tree trunks. He also urinates over her mark. Scent marking by both males and females occurs year round, and may indicate territorial marking. Frenzied scent marking bouts indicate that the breeding season is near.

feeding ecology and diet

Milne-Edwards's sifakas primarily eat vegetation including young leaves from trees and vines and seeds from fleshy fruits. Flowers, fruit pulp, mature leaves, and soil are also consumed regularly. Homopteran insects are consumed by Milne-Edwards's sifakas in December. Sifaka individuals often eat 25–30 plant species per day, and over 150 plant species within a year.

reproductive biology

Milne-Edwards's sifakas live in monogamous pairs, harems, multi-male, multi-female groups and in polyandrous groups. Breeding is seasonal, and males' testicles begin to expand three months before the mating in December to January. During estrus the female's vulva becomes swollen and pink. Milne-Edwards' sifakas mate 3–4 times within a 10-hour period with the male mounting the female from the back. Females may mate with one or more males in the group. The gestation period is six months, and infants are born in May or June. One infant is born per mother on average every second year. Newborn infants weigh about 4.4 oz (125 g) and are 0.2% of the weight of the mother. The infant clings ventrally to the mother for the first four weeks and then rides on her back for five months. Males help transport older infants about 10% of the time, and defend the group against attacks by large raptors. Females are dominant in feeding and social situations. Infant mortality is high (over 50%).

conservation status

Endangered.

significance to humans

In the Ranomafana region it is fady (taboo) to eat sifakas because they resemble humans.

Indri

Indri indri

subfamily

Indriinae

taxonomy

Indri indri E. Geoffroy and G. Cuvier, 1796, Madagascar.

other common names

Malagasy: Amboanala, babakoto, endrina.

physical characteristics

Body length is about 23.6 in (600 mm), tail length is about 2.0 in (50 mm), and weight is 13.2–16.5 lb (6.0–7.5 kg).

distribution

The indri occurs from forests north of the Mangoro River to near Sambava, but excluding the Masoala peninsula.

habitat

Primary and secondary lowland and mid-altitude humid moist forests.

behavior

Strictly diurnal. Group size varies from 2–6 and is normally comprised of adult pair and offspring. Females are dominant over males in feeding and social situations. The pair gives morning clarinet-like calls that can be heard up to 2 mi (3 km). The number of calls increases prior to and during the mating season. Home ranges are 20–74 acres (8–30 hectares), with the daily path length from 980–2,300 ft (300–700 m). Indris leap through the forest with spectacular bounds of up to 33 ft (10 m) between vertical trunks. Indris have no scent glands located on the chest, head, or arms. Salivary scent marks transmitted by mouth rubbing has been observed. Anogenital glands are used for scent marking during the mating season. Indris rest frequently and daily activity ranges from 4–11 hours depending on the time of the year.

feeding ecology and diet

The annual diet of Indri consists of 70–82% immature leaves from trees, 10–22% fruit, 6% flowers, and the remainder from mature leaves, bark, galls, and soil. Seventy-nine plant species are consumed during the year at mid-elevation forest, less than half of the number of species consumed by sympatric diademed sifakas. In low-elevation forest the indri feed on over 42 plant species. The indri has a long small intestine and enlarged caecum for digestion of vegetation. Females spend significantly more time feeding than males, although the number of feeding bouts per day is equal for males and females. Foliage from the Laurel family is the most frequently eaten by indri populations both in mid-altitude montane and low-altitude coastal rain-forests.

reproductive biology

Monogamous. Indris do not reach sexual maturity until 7–9 years of age, and females give birth every 2–3 years. Mating occurs between December and March with a single offspring born between April and August. Indri mate face-to-face, hanging from a branch. The gestation is between 120–150 days. The infant is born furred, able to cling, but very small in size. The infant rides on the ventrum of the mother until four months when it transfers to the mother's back. The offspring is capable of moving independently at eight months.

conservation status

Endangered.

significance to humans

Local taboo restricts harming or hurting the indri. Local legend says an indri howls at dawn to mourn the loss of its tail stolen by black and white ruffed lemurs.

Greater sloth lemur

Palaeopropithecus ingens

subfamily

Palaeopropithecinae

taxonomy

Palaeopropithecus ingens Grandidier, 1899, Madagascar.

other common names

None known.

physical characteristics

Its estimated body weight is 121 lb (55 kg). It is dentally similar to the extant sifakas with long, narrow molars, and well-developed shearing crests. It has small, vertical lower incisors with no tooth comb. The skull is similar to living indriids, but more robustly built, with a longer snout, and a heavily buttressed nasal region suggesting prehensile lips. The forelimbs are considerably longer than the hind limbs, and it has very long, curved phalanges and very mobile joints. Extremely suspensory, its locomotor abilities have been compared to sloths or orangutans.

distribution

Sloth lemurs went extinct within the last few thousand years, but before that were widely distributed throughout Madagascar. Paleaopropithecus, the most sloth-like of the sloth lemurs was widespread throughout all Madagascar, with this species found in Andranomena, Analabe in the west, and Ankarana massif in the north. Paleaopropithecus have been found in limestone caves of the Manamby Plateau, north of Tulear.

habitat

Primary and secondary forests.

behavior

From the morphology, it is predicted that they were slow moving, commonly climbing and suspending themselves in trees.

feeding ecology and diet

Highly folivorous.

reproductive biology

Nothing is known.

conservation status

Extinct.

significance to humans

Scientists have indications from cut marks on bones that early humans hunted subfossil lemurs. Climate changes suggest humans and perhaps wildfires destroyed their habitat.

Baboon lemur

Archeolemur edwardsi

subfamily

Palaeopropithecinae

taxonomy

Archaeolemur edwardsi Filhol, 1895, Madagascar.

other common names

Malagasy: Kadoky.

physical characteristics

Its estimated body weight is 49 lb (22 kg). Males and females had the same body size. Tooth eruption patterns, including rapid eruption of adult dentition, are reminiscent of the living indris, sifakas, and woolly lemurs. The anterior premolar is caniniform, and the entire premolar row formed a long cutting edge. The broad molars had low, rounded cusps arranged in a bilophodont pattern similar to Old World monkeys. Cranially it is similar to living indrids. Short limbs relative to trunk length are reminiscent of both terrestrial and arboreal quadrapeds.

distribution

From north to south to west subfossil sites throughout Madagascar. This was the most widespread species of subfossil lemurs.

habitat

Primary and secondary forests and woodlands throughout Madagascar.

behavior

From the morphology, it is predicted that the baboon lemurs fed on leaves and hard fruits, and traveled both on the ground and in the trees.

feeding ecology and diet

Projecting from morphology, baboon lemurs had a diverse diet including fruit, seeds, and invertebrates. The teeth of Archaeolemur appear specialized for processing foods requiring considerable preparation previous to processing, such as fruits with tough outer coverings or the seeds within them. It has been suggested that it ate seeds of baobab trees, which facilitated seed dispersal. High foliage consumption is supported by data on molar microwear.

reproductive biology

Nothing is known.

conservation status

Extinct.

significance to humans

Scientists have indications from cut marks on bones that early humans hunted them. Climate changes suggest humans and perhaps wildfires destroyed their habitat.

Resources

Books

Fleagle, John G. Primate Adaptation and Evolution, 2nd ed. San Diego, CA: Academic Press, 1999.

Garbutt, Nick. Mammals of Madagascar. New Haven, CT: Yale University Press, 1999.

Godfrey, L. R., W. L. Jungers, K. E. Reed, E. L. Simons, and P. S. Chatrath. "Subfossil Lemurs Inferences about Past and Present Primate Communities in Madagascar." In Natural Change and Human Impact in Madagascar, edited by S. M. Goodman and B. D. Patterson. Washington, DC: Smithsonian Institution Press, 1997.

Mittermeier, Russell A., Ian Tattersall, William R. Konstant, David M. Meyers, and Roderic B. Mast. Lemurs of Madagascar. Chicago, IL: University of Chicago Press, 1994.

Rowe, Noel. The Pictorial Guide to the Primates. New York: Pogonias Press, 1996.

Simons, E. L. "Lemurs: Old and New." In Natural Change and Human Impact in Madagascar, edited by S. M. Goodman and B. D. Patterson. Washington, DC: Smithsonian Institution Press, 1997.

Periodicals

Pochron, S. T., and P. C. Wright. "Flexibility in Mating Systems in a Prosimian Primate." Behavioral Ecology and Sociobiology (2003): 31–42.

Pollock, J. I. "The Song of the Indris (Indri indri: Primates: Lemuroidea): Natural History, Form, and Function." International Journal of Primatology 7 (1986): 225–264.

Simons, E. L., D. A. Burney, P. S. Chatrath, L. R. Godfrey, W. L. Jungers, and B. Rakotosaminmanana. "AMS14 Dates on Extinct Lemurs from Caves in the Ankarana Massif of Northern Madagscar." Quartenary Research 42 (1995): 249–254.

Wright, P. C. "Lemur Traits and Madagascar Ecology: Coping with an Island Environment." Yearbook of Physical Anthropology 42 (1999): 31–42.

Organizations

Duke University Primate Center, Division of Fossil Primates. 1013 Broad Street, Durham, NC 27705 United States. Phone: (919) 416-8420. Fax: (919) 416-8584. Web site: <http://www.fossils.duke.edu/>.

Institute for the Conservation of Tropical Environments. N-543 SBS Bldg., SUNY at Stony Brook, Stony Brook, NY 11794-4364 United States. Phone: (631) 632-9440. Fax: (631) 632-7692. E-mail: [email protected] Web site: <http://naples.cc.sunysb.edu/CAS/icteweb.nsf>.

Patricia Wright, PhD