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Hapalemur aureusgolden bamboo lemur

By Dana Kowalsky

Geographic Range

Hapalemur aureus, the golden bamboo lemur, is endemic to the tropical, moist, southeastern rainforests of Madagascar. It was first observed living sympatrically with other lemur species in 1985. Since its discovery, further studies have confirmed the range of H. aureus overlaps with Hapalemur griseus and Prolemur simus, mostly restricted to the south central part of the eastern forests. Several groups live in and around Ranomafana National Park in Madagascar, a park that covers approximately 43,500 square hectares of rainforest. Hapalemur aureus does not seem to be restricted by altitude, as groups have been found throughout an altitude range of 800 to 1300 m within Ranomanafana National Park. In 1993, H. aureus was also found in Andringitra National Park, south of Ranomafana. These two areas are connected by a forest corridor, which is becoming increasingly fragmented. One survey discovered Hapalemur aureus in 4 out of 8 sites along this corridor. There have not been sightings north of Ranomafana or south of Andringitra and a tentative southern limit is placed at the Manampatrana River. (Arrigo-Nelson and Wright, 2003; Goodman, et al., 2001; Irwin, et al., 2005; Meier, et al., 1987; Mutschler and Tan, 2003; Tan, 1999)

Habitat

Golden bamboo lemurs are arboreal primates restricted to bamboo patches in the southeastern Madagascar rainforest. With a diet specializing in giant bamboo (Cathariostachys madagascarensis), it is not surprising to find bamboo as an important habitat requirement for golden bamboo lemurs. A 2003 survey of lemurs in Ranomafana National Park documented a minimum of two C. madagascarensis stands per site. Each bamboo stand averaged 250 by 200 m in four separate sites, and groups golden bamboo lemurs were found living near each one. In the same survey, two other sites with evidence of golden bamboo lemur activity that did not contain C. madagascarensis, had a different species of large-culm bamboo, Arundinaria ambositrensis. Other species of bamboo grass and small-culm bamboo (genus Cephalostachyum) were also found at each site. All types of bamboo species can co-exist within the same area, but small-culm bamboo and grasses were found with the greatest abundance in edge forest habitats and in gaps in the forest created by tree falls. The successful and rapid colonization of bamboo in disturbance areas can often create an overlap of H. aureus habitat with human activities such as logging and agriculture. If these lemurs live near a forest edge habitat, new mothers tend to move into more sheltered, dense, habitats for the first 10 to 14 days after giving birth. (Arrigo-Nelson and Wright, 2003; Mutschler and Tan, 2003; Tan, 1999)

  • Range elevation
    800 to 1300 m
    2624.67 to 4265.09 ft

Physical Description

Bamboo lemur species generally have round heads, large faces, short muzzles, and small ears hidden by fur. They prefer vertical resting postures and their tails are not prehensile. The hands and feet are short and broad with large pads under the tips of toes and fingers. All teeth have a serrated cutting edge, except for the molars. These cutting edges are thought to be an adaptation for a coarse bamboo diet. The specific dental formula for this species has not been recorded; however, the dental formula in the family Lemuridae is I 2/2, C 1/1, PM 3/3, and M 3/3 = 36. As strepsirhines, lemurs possess a dental comb or toothcomb, a forward projection of the lower jaw teeth often used in grooming. Dental peculiarities exist among the premolars of bamboo lemur species, most likely due to their bamboo rich diets. Bamboo lemurs have additional cusps on the upper fourth premolars. These cusps are thought to help in crushing the fibrous plant material that they eat. Golden bamboo lemurs can easily be distinguished from other bamboo lemur species by the pale golden fur on their bellies, inner limbs, cheeks, throat, and surrounding the eyes. Other bamboo lemur species have fur colors ranging from sooty grey coats to rusty brown, with the occasional “olivaceous” hue in Hapalemur griseus. The ears of golden bamboo lemurs have golden-brown tips and are not tufted. The coat is dorsally reddish-brown; darker over the shoulders, back, top of head, and tail. The tail has a darkened tip. Five bamboo lemur species are recognized. Golden bamboo lemurs are the largest, with an adult weight of 1.25 to 1.7 kg. Head-body length is approximately 34 cm, while tail length is about 41 cm, for a total length of 70 to 80 cm. Female and male golden bamboo lemurs are sexually monomorphic. Females have only one pair of mammae, located pectorally. They have a diploid complement of 62 chromosomes, all of which are acrocentric. Golden bamboo lemurs have well-developed brachial glands on the inner upper arm, and an elliptical hairless patch on the lower arm, possibly with a carpal gland. Elbow flexion brings the two glands together. The brachial gland secretes a white, sticky fluid with a strong smell. (Jernvall, et al., 2008; Meier, et al., 1987; Mittermeier, et al., 2006; Mutschler and Tan, 2003; Nowak, 1999; Yamashita, et al., 2009)

  • Sexual Dimorphism
  • sexes alike
  • Range mass
    1.25 to 1.7 kg
    2.75 to 3.74 lb
  • Average length
    75 cm
    29.53 in

Reproduction

Golden bamboo lemurs are monogamous and mating takes place in July or August. There is some evidence that male testis size increases prior to the breeding season. One study showed a male, captured in May, having a testicular volume of 17.414 cm3. The same male, captured again in October, had a testicular volume of 6.351 cm3. Further studies are needed to investigate this finding. (Glander, et al., 1992; Norosoarinaivo and Tan, 1998; Tan, 1999b; Yamashita, et al., 2009)

Gestation lasts approximately 138 days, and golden bamboo lemurs give birth just once per year, usually to a single offspring. Altricial young are born in December and require several months of maternal care and lactation. Unlike other bamboo lemur species, females nest with their offspring for the first 10 to 14 days in secluded areas of dense vegetation. Weaning takes place when offspring are 6 to 8 months old. (Glander, et al., 1992; Tan, 1999b)

  • Breeding interval
    Golden bamboo lemurs breed once yearly.
  • Breeding season
    Golden bamboo lemurs breed from July to August.
  • Average number of offspring
    1
  • Average gestation period
    138 days
  • Range weaning age
    6 to 8 months
  • Average time to independence
    3 years

Golden bamboo lemurs practice infant parking and oral transport. Mothers leave infants while foraging and can travel as far as 250 meters away. The infant is left for an average time of 200 minutes. There are no published observations of paternal care, but it is a possibility considering the monogamous behavior of this species. Siblings have also been observed to care for infants. Offspring live with their parents as a family group until approximately 3 years of age, after which they disperse. (Norosoarinaivo and Tan, 1998; Tan, 1999b)

  • Parental Investment
  • altricial
  • female parental care
  • pre-fertilization
    • provisioning
    • protecting
      • female
  • pre-hatching/birth
    • provisioning
      • female
    • protecting
      • female
  • pre-weaning/fledging
    • provisioning
      • female
    • protecting
      • female
  • pre-independence
    • provisioning
      • female
    • protecting
      • female
  • extended period of juvenile learning

Lifespan/Longevity

Average lifespan of H. aureus is not yet known. A sister species, Hapalemur griseus, lived in captivity until the age of 23. On average, H. griseus females and males live to 17.1 years and 12.8 respectively. (Hakeem, et al., 1996; Mittermeier, et al., 2006)

Behavior

Golden bamboo lemurs live in small groups, not often exceeding four individuals. Usually the group consists of an adult male and female, with smaller young adults or juveniles. The group is a family, comprised of a monogamous pair and their offspring. Varying accounts list golden bamboo lemurs as diurnal or crepuscular, with a distinct mid-day rest period. The majority of waking hours are spent eating and foraging. (Garbutt, 1999; Meier, et al., 1987; Mittermeier, et al., 2006; Tan, 1999)

Home Range

A study of two separate family groups of golden bamboo lemurs over a two-year period showed their mean home range to be 26 hectares. Another group, an adult pair and two offspring, had a home range of 80 hectares. Territoriality has not been documented in Hapalemur aureus. But the presence of a brachial gland and subsequent reports of scent marking in a sister species, Hapalemur griseus griseus, suggests they may be territorial. (Tan, 1999; Wright and Randrimanantena, 1989)

Communication and Perception

Golden bamboo lemurs are highly vocal, with at least two distinct calls. They were first recorded as performing a “hard grunt” and a loud call at night. One call is described as a quiet “resonant wuulp with inquisitive inflection.” This sound possibly serves as a contact call between members of the family group, as it is sometimes responded to and repeated by others. A longer call is described as a loud, sharp, throaty honk that decreases in volume as it is repeated. This longer call appears to be delivered by only one member of the group and is often heard along with the "wuulp" call. This second call may have a territorial function. Golden bamboo lemurs, like other lemurs, have binocular vision. The function of the brachial gland in Hapalemur aureus is not yet known. Lesser bamboo lemurs use scent-marking, vocal displays, and chasing in territory defense. Ring-tailed lemurs participate in territoriality via scent marking. They excrete a fatty substance from their brachial glands, which is rubbed onto its long tail for scent dispersal. The excretions of the brachial gland in golden bamboo lemurs are likely used in a similar way. (Garbutt, 1999; Meier, et al., 1987; Mutschler and Tan, 2003; Nowak, 1999)

Food Habits

Golden bamboo lemur diet is primarily composed of Madagascar giant bamboo, but Cephalostachyum viguieri, Arundinaria ambositrensis, and other bamboo grasses are also consumed. Bamboo is consumed year round, as is the consumption of small amounts of soil and fungi. Although approximately 78% of golden bamboo lemur diet is giant bamboo, this species has been observed to eat other bamboo and grass species (10%), bamboo foliage (3%), fruit (4%), and other (5%). Small instances of frugivory are opportunistic. Golden bamboo lemurs prefer to consume young growth of giant bamboo, such as the leaf base, shoots, and pith, discarding more mature growth. New growth bamboo has a lower energy cost during the mastication and is more easily digested. It also has higher concentration of protein. Young shoots are only seasonally available. Golden bamboo lemurs consume varying parts of bamboo when the young shoots are less abundant during different seasons. Previously, it was proposed that niche partitioning explained the preference of different bamboo portions in Hapalemur aureus and two other species of bamboo lemurs that live sympatrically: Hapalemur griseus and Prolemur simus. These species appeared to select alternate portions of bamboo plants. Subsequent studies cast doubt on the degree of niche partitioning after finding overlap in the diets of all three species. Ironically, the most protein-rich part of bamboo is also the most deadly; giant bamboo shoots contain high amounts of cyanide. Because golden bamboo lemurs specifically target these shoots for consumption, they are estimated to ingest about 500 g of bamboo daily, which contains approximately 12 times the lethal dose of cyanide in comparable mammals. More recent studies suggest the cyanide concentration in Cathariostachys madagascariensis shoots to be up to four times higher than originally estimated. A positive test for cyanide has been found in the urine of H. aureus, but only rarely in fecal samples. This result suggests cyanide is absorbed by the gastrointestinal tract with the kidneys involved in its excretion. It takes more than 20 hours for complete digestion and elimination of fecal matter. The means by which they avoid cyanide poisoning is unknown. (Ballhorn, et al., 2009; Glander, et al., 1989; Tan, 1999; Yamashita, et al., 2010; Yamashita, et al., 2009)

  • Plant Foods
  • leaves
  • wood, bark, or stems
  • fruit

Predation

Direct hunting by humans is the most widely reported type of predation on golden bamboo lemurs. Two types of hunting have been reported: projectile, usually using spears, slings and blowguns; and trapping, involving snares. (Garbutt, 1999; Irwin, et al., 2005; Mittermeier, et al., 2006; Mutschler and Tan, 2003)

Ecosystem Roles

The ecosystem role of Hapalemur aureus has not been studied. Frugivorous lemurs have been implicated as important vectors for seed dispersal in Malagasy rainforests, but it is unknown what, if any, role they may play in propagation of bamboo. (Dew and Wright, 1998)

Economic Importance for Humans: Positive

Golden bamboo lemurs are part of the fascinating and unique endemic lemur fauna of Madagascar.

Economic Importance for Humans: Negative

There are no adverse impacts of golden bamboo lemurs on humans. (Garbutt, 1999; Mutschler and Tan, 2003)

Conservation Status

The most recent IUCN Red List assessment (2008) concluded that golden bamboo lemurs are endangered due to their small range and habitat fragmentation. The species is very rare, restricted to the southeastern rainforest in Madagascar near areas of bamboo growth. Recent surveys have identified two regions in which the forest corridor between Ranomafana and Andringitra have become discontinuous. This creates a barrier to migration and gene flow. A 2005 survey estimated the population to be 5,916 individuals evenly distributed throughout the area. Even distribution is likely an unrealistic assumption, so the population is estimated at 25% less than this calculated value. Other sources suggest the population to be as low as 1,000 individuals. (Garbutt, 1999; Glander, et al., 1989; Irwin, et al., 2005; Sussman, 2002)

Other Comments

Golden bamboo lemurs were first discovered in 1985 in Ranomafana National Park in southeastern Madagascar and first described in 1987. (Fausser, et al., 2002; Meier, et al., 1987; Pastorini, et al., 2002)

Contributors

Dana Kowalsky (author), University of Manitoba, Jane Waterman (editor), University of Manitoba, Tanya Dewey (editor), University of Michigan-Ann Arbor.

Glossary

Ethiopian

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

World Map

acoustic

uses sound to communicate

altricial

young are born in a relatively underdeveloped state; they are unable to feed or care for themselves or locomote independently for a period of time after birth/hatching. In birds, naked and helpless after hatching.

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.
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

folivore

an animal that mainly eats leaves.

herbivore

An animal that eats mainly plants or parts of plants.

island endemic

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

iteroparous

offspring are produced in more than one group (litters, clutches, etc.) and across multiple seasons (or other periods hospitable to reproduction). Iteroparous animals must, by definition, survive over multiple seasons (or periodic condition changes).

monogamous

Having one mate at a time.

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.

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

sedentary

remains in the same area

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

temperate

that region of the Earth between 23.5 degrees North and 60 degrees North (between the Tropic of Cancer and the Arctic Circle) and between 23.5 degrees South and 60 degrees South (between the Tropic of Capricorn and the Antarctic Circle).

terrestrial

Living on the ground.

territorial

defends an area within the home range, occupied by a single animals or group of animals of the same species and held through overt defense, display, or advertisement

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

viviparous

reproduction in which fertilization and development take place within the female body and the developing embryo derives nourishment from the female.

References

Arrigo-Nelson, S., P. Wright. 2003. Survey results from Ranomafana National Park: new evidence for the effects of habitat preference and disturbance of Hapalemur. Folia Primatol, 75: 331-334.

Ballhorn, D., S. Kautz, F. Rakotoarivelo. 2009. Quantitative variability of cyanogenesis in Cathariostachys madagascariensis – the main food plant of bamboo lemurs in southeastern Madagascar. Am J Primatol, 71: 305-315.

Dew, L., P. Wright. 1998. Frugivory and Seed Dispersal by Four Species of Primates in Madagascar's Eastern Rain Forest. Biotropica, 30/3: 425-437.

Fausser, J., P. Prosper, G. Donati, B. Ramanamanjato, Y. Rumpler. 2002. Phylogenetic relationships between Hapalemur species and subspecies based on mitochondrial DNA sequences. BMC Evol Biol, 2: 1-9. Accessed November 01, 2013 at http://www.biomedcentral.com/1471-2148/2/4.

Garbutt, N. 1999. Mammals of Madagascar. New Haven and London: Yale University Press.

Glander, K., P. Wright, D. Seigler, V. Randrianasolo, B. Randrianasolo. 1989. Consumption of cyanogenic bamboo by a newly discovered species of bamboo lemur. Am J Primatol, 19: 119-124.

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

Goodman, S., V. Razafindratsita, H. Schutz, R. Ratsimbazafy. 2001. Inventaire Biologique du Parc National de Ranomafana et du couloir forestier qui relie au Parc National d'Andringitra. Pp. 231-243 in S Goodman, V Razafindratsita, eds. Les Lemuriens. Antananarivo, Madagascar: CIDST.

Hakeem, A., R. Sandoval, M. Jones, J. Allman. 1996. Brain and life span in primates. Pp. 78-104 in J Birren, ed. Handbook of the Psychology of Aging. Waltham, MA: Academic Press.

Irwin, M., S. Johnson, P. Wright. 2005. The state of lemur conservation in south-eastern Madagascar: population and habitat assessments for diurnal and cathemeral lemurs using surveys, satellite imagery and GIS. Oryx, 39/2: 204-218.

Jernvall, J., C. Gilbert, P. Wright. 2008. Peculiar tooth homologies of the greater bamboo lemur (Prolemus simus). Pp. 335-342 in C Gilbert, J Fleagle, eds. Elwyn Simons: A Search for Origins. Helinski, Finland: Springer.

Meier, B., R. Albignac, A. Peyieras, Y. Rumpler, P. Wright. 1987. A new species of Hapalemur primates from southeast Madagascar. Folia Primatol, 48: 211-215.

Mittermeier, R., W. Konstant, F. Hawkins, E. Louis, O. Langrand, J. Ratsimbazafy, R. Rasoloarison, J. Ganzhorn, S. Rajaobelina, I. Tattersall, D. Meyers. 2006. Lemurs of Madagascar. Washington, DC: Conservation International.

Mutschler, T., C. Tan. 2003. Hapalemur, bamboo or gentle lemurs. Pp. 1324-1328 in S Goodman, J Benstead, eds. The Natural History of Madagascar. Chicago: University of Chicago Press.

Norosoarinaivo, J., C. Tan. 1998. Infant care in Hapalemur aureus, Ranomafana National Park, Madagascar. Congress of the International Primatological Society (abstracts), 17: 384.

Nowak, R. 1999. Walker's Mammals of the World, Sixth Edition, Volume I. Baltimore and London: The Johns Hopkins University Press.

Pastorini, J., M. Forstner, R. Martin. 2002. Phylogenetic relationships of gentle lemurs (Hapalemur). Evol Primatol, 1: 150-154.

Stewart, I. 1988. Discovery of a new species of lemur. Nature, 333: 206.

Sussman, R. 2002. Adaptive array of lemurs of Madagascar revisited. Evol Anthropol, 1: 75-78.

Tan, C. 1999. Group composition, home range size, and diet of three sympatric bamboo lemur species (genus Halaplemur) in Ranomafana National Park, Madagascar. Intl J Primatol, 20/4: 547-566.

Tan, C. 1999b. Life history and infant rearing strategies of three Hapalemur species. Primate Report, 54/1: 33.

Wright, P., M. Randrimanantena. 1989. Comparative ecology of three sympatric bamboo lemurs in Madagascar. Am J Phys Anthropol, 78: 327.

Yamashita, N., C. Tan, C. Vinyard, C. Williams. 2010. Semi-quantitative tests of cyanide in foods and excreta of three Hapalemur species in Madagascar. American Journal of Primatology, 72: 56-61.

Yamashita, N., C. Vineyard, C. Tan. 2009. Food mechanical properties in three sympatric species of Hapalemur in Ranomafana National Park, Madagascar. Am J Phys Anthropol, 139: 368-381.

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