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Eulemur cinereicepsgray-headed lemur

By Jean Marie Acuna

Geographic Range

Gray-headed lemurs are found in southeastern Madagascar. Also known as white-collared lemurs, their distribution range is restricted within a thin band of rainforest located between the Manampatra River and Mananara River. In 2005 the extent of native habitat in that area was only 270 square miles. (Andriaholinirina, et al., 2014)

Habitat

Gray-headed lemurs spend majority of their time in the upper layers of forests. They are found to inhabit lowland and mid-altitude rainforest, which includes littoral and montane forest habitats. (Andriaholinirina, et al., 2014; Richardson, 2006)

Physical Description

Gray-headed lemurs are medium-sized lemurs with a head-body length of 39 to 40.5 cm and a tail length of 50 to 55 cm. They have a weight range of 2 to 2.5 kg, with no significant differences between male and female weights. Less distinct in females, gray-headed lemurs are known for their bushy white beard or collar. Males tend to have darker gray to brownish-colored bodies with gray heads and faces. Males may often have a dark brown stripe running down the middle of their dorsum and tail. Females, however, have redder-brown bodies with less bushy, reddish-brown beards. Male gray-headed lemurs were also found to have distinctly larger canines than females. Lemur species, in general, are known to have 5 digits on each limb with dental formulas of 2/2, 1/1, 3/3, 3/3 = 36. (Gould and Sauther, 2006; Johnson, et al., 2005; Johnson, 2002; Linton Zoo, 2014; Richardson, 2006; San Diego Zoo, 2014)

  • Sexual Dimorphism
  • sexes colored or patterned differently
  • Range mass
    2 to 2.5 kg
    4.41 to 5.51 lb
  • Range length
    90 to 100 cm
    35.43 to 39.37 in

Reproduction

Little is known about the reproductive biology of gray-headed lemurs. However, it is likely similar to other brown lemurs. Thus, the mating system of gray-headed lemurs may either be monogamous or polygynous. (Nowak, 1999; Richardson, 2006)

Availability of studies for general reproductive behavior of gray-headed lemurs is quite limited. However, closely relative species, such as other brown lemurs, have matings occurring between June and July and parturition between September and November. Gestation period of lemurs is thought to be approximately 126 to 140 days. Females tend to give birth to one offspring, however there is evidence of twins being produced occasionally. (Animal Defenders International, 2014; Linton Zoo, 2014; Richardson, 2006)

  • Breeding interval
    Gray-headed lemurs are likely to breed once yearly.
  • Breeding season
    Breeding season is uknown in gray-headed lemurs.
  • Range number of offspring
    1 (low)

Parental investment is not described in gray-headed lemurs. In many lemur species, infants tend to stay with their mothers until old enough to move on their own. In the first few weeks after parturition, baby lemurs usually cling onto their mother’s chest then gradually transition to riding on their mother’s back. Young lemurs are generally weaned at five to six months old. Males of related lemur species carry their infants regularly as well. (Lonsdorf and Ross, 2012; San Diego Zoo, 2014)

  • Parental Investment
  • altricial
  • pre-fertilization
    • provisioning
    • protecting
      • female
  • pre-hatching/birth
    • provisioning
      • female
    • protecting
      • female
  • pre-weaning/fledging
    • provisioning
      • female
    • protecting
      • male
      • female
  • pre-independence
    • provisioning
      • female
    • protecting
      • male
      • female

Lifespan/Longevity

Gray-headed lemurs are thought to have a maximum lifespan of up to 20 to 25 years in the wild. (Richardson, 2006)

  • Range lifespan
    Status: wild
    20 to 25 years

Behavior

Gray-headed lemurs are arboreal quadrupeds that utilize leaping locomotion. This species partially relies on vertical postures and support use. They live in multi-male/multi-female social systems, with group sizes ranging 4 to 17 individuals. Unlike other lemurs, dominance hierarchies within gray-headed lemurs are not found to exist in either sex. Populations of gray-headed lemurs have also been found to maintain loose, fission-fusion communities. Although rare in mammals, fission-fusion communities are flexible social groups that allow members to change subgroups from time to time. The adaptation of a fission-fusion structure may be due to the poor habitat quality in which white-collared lemurs reside. It is thought to be a response to increased feeding competition when resources within an area are limited. Gray-headed lemurs are also found to exhibit cathermerality (i.e., active during day and night). Cathermerality in lemurs is thought to be an adaptive response towards thermoregulation, feeding competition, and feeding time when resources are scarce. (Gould and Sauther, 2006; Johnson, 2002; Lehmann and Boesch, 2004; Mittermeier, 2006)

Home Range

Home range size in gray-headed lemurs are not reported in the literature.

Communication and Perception

Lemur species use vocalization and scent markings as their form of communication. Vocalizations created by lemurs usually vary by species. They rely heavily on their sense of smell. The combination of a dog-like snout and rhinarium allow lemurs to identify danger and locate young when separated. Located on the wrist and/or genital regions, scent glands are used to mark habitat, alert members of intruders, and for mating purposes. (Bradt and Austin, 2014; Feldhamer, et al., 2007; San Diego Zoo, 2014)

Food Habits

Gray-headed lemurs have a highly diverse diet. They primarily feed on fruits with small portions of flowers, leaves, and nectar. These lemurs may occasionally eat fungi but rarely insects. (Gould and Sauther, 2006; Johnson and Wyner, 2000)

  • Animal Foods
  • insects
  • Plant Foods
  • leaves
  • fruit
  • nectar
  • flowers
  • Other Foods
  • fungus

Predation

Data on predation of gray-headed lemurs is lacking. However, their predators are likely to be fossas, hawks, and humans. (Karpanty and Wright, 2007)

Ecosystem Roles

Gray-headed lemurs can play an important role in the maintenance and regeneration of ecosystems. As prominent frugivores, these lemurs may aid in the dispersal of seeds. They may also serve as a source of prey for other animals. (Gould and Sauther, 2006)

Economic Importance for Humans: Positive

Gray-headed lemurs are hunted with the use of slingshots, snares, and shotguns as a source of food for humans. A breeding program is located in the Linton Zoological Gardens, where the species is used for attraction and educational purposes as well. (Andriaholinirina, et al., 2014; Linton Zoo, 2014)

  • Positive Impacts
  • food
  • research and education

Economic Importance for Humans: Negative

There are no known adverse effects of gray-headed lemurs on humans.

Conservation Status

Like all other lemurs, gray-headed lemurs are listed under Appendix I by CITES. Listed as critically endangered by IUCN, gray-headed lemurs have the lowest reported population density (8.7-13.5/km2) among other brown lemur species. Gray-headed lemurs are greatly threatened by continuous hunting and destruction of their already restricted habitat. Ongoing conversion of habitats into agricultural lands and selective logging are the primary causes of lemur habitat destruction. The Manombo Special Reserve and the Agnalazaha Forest are two areas inhabited by gray-headed lemur populations that are now being managed by Missouri Botanical Garden. A high conservation priority is given towards the expansion of the Manombo Special Reserve. In 2009, about a dozen gray-headed lemurs were found in four zoological collections. Only one of the four zoological collections, however, keeps a breeding group of gray-headed lemurs. (Andriaholinirina, et al., 2014; Brenneman, et al., 2012; CITES, 2014; Gould and Sauther, 2006)

Other Comments

In 2008, Johnson et al conducted a study to distinguish Eulemur albocollaris and Eulemur cinereiceps as two separate taxa. However, no evidence was found to support his hypothesis. Thus, Eulemur cinereiceps was given priority as the valid name. Eulemur albocollaris is a junior synonym of Eulemur cinereiceps. (Andriaholinirina, et al., 2014; Johnson, et al., 2008)

Contributors

Jean Marie Acuna (author), University of Alaska Fairbanks, Laura Prugh (editor), University of Washington, 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

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.

food

A substance that provides both nutrients and energy to a living thing.

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.

intertidal or littoral

the area of shoreline influenced mainly by the tides, between the highest and lowest reaches of the tide. An aquatic habitat.

introduced

referring to animal species that have been transported to and established populations in regions outside of their natural range, usually through human action.

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).

motile

having the capacity to move from one place to another.

nocturnal

active during the night

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

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

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.

year-round breeding

breeding takes place throughout the year

References

Andriaholinirina, N., A. Baden, M. Blanco, L. Chikhi, A. Cooke, N. Davies, R. Dolch, G. Donati, J. Ganzhorn, C. Golden, L. Groeneveld, A. Hapke, M. Irwin, S. Johnson, P. Kappeler, T. King, R. Lewis, E. Louis, M. Markolf, V. Mass, R. Mittermeier, R. Nichols, E. Patel, C. Rabarivola, B. Raharivololona, S. Rajaobelina, G. Rakotoarisoa, B. Rakotomanga, J. Rakotonanahary, H. Rakotondrainibe, G. Rakotondratsimba, M. Rakotondratsimba, L. Rakotonirina, F. Ralainasolo, J. Ralison, T. Ramahaleo, J. Ranaivoarisoa, S. Randrianahaleo, B. Randrianambinina, L. Randrianarimanana, H. Randrianasolo, G. Randriatahina, H. Rasamimananana, T. Rasolofoharivelo, S. Rasoloharijaona, F. Ratelolahy, J. Ratsimbazafy, N. Ratsimbazafy, H. Razafindraibe, J. Razafindramanana, N. Rowe, J. Salmona, M. Seiler, S. Volampeno, P. Wright, J. Youssouf, J. Zaonarivelo, A. Zaramody. 2014. "Eulemur cinereiceps" (On-line). The IUCN Red List of Threatened Species. Accessed November 14, 2014 at http://www.iucnredlist.org/details/8205/0.

Animal Defenders International, 2014. "Primates: Lemur" (On-line). Save the Primates. Accessed November 15, 2014 at http://www.savetheprimates.org/primatefacts/primates/lemur.

Bradt, H., D. Austin. 2014. Madagascar, 11th edition. England: Bradt Travel Guides Ltd.

Brenneman, R., S. Johnson, C. Bailey, C. Ingraldi, K. Delmore, T. Wyman, H. Andriamaharoa, F. Ralainasolo, J. Ratsimbazafy, E. Louis, Jr.. 2012. Population genetics and abundance of the Endangered grey-headed lemur Eulemur cinereiceps in south-east Madagascar: assessing risks for fragmented and continuous populations. Oryx, 46/02: 298-307.

CITES, 2014. "Appendices I, II and III" (On-line pdf). Convention on International Trade in Endangered Species of Wild Fauna and Flora. Accessed November 14, 2014 at http://www.cites.org/sites/default/files/eng/app/2014/E-Appendices-2014-09-14.pdf.

Feldhamer, G., L. Drickamer, S. Vessey, J. Merritt, C. Krajewski. 2007. Mammalogy: Adaptation, Diversity, Ecology. Baltimore, Maryland: The Johns Hopkins University Press.

Gould, L., M. Sauther. 2006. Lemurs: Ecology and Adaptation. New York, NY: Springer Science & Business Media, LLC.

Johnson, S. 2002. Ecology and Speciation in Brown Lemurs: White-collared Lemurs ( Eulemur albocollaris ) and Hybrids ( Eulemur albocollaris X Eulemur fulvus rufus ) in Southeastern Madagascar. Austin, Texas: PhD Dissertation, The University of Texas at Austin. Accessed November 13, 2014 at http://www.lib.utexas.edu/etd/d/2002/johnsonse026/johnsonse026.pdf.

Johnson, S., A. Gordon, R. Stumpf, D. Overdoff, P. Wright. 2005. Morphological Variation in Populations of Eulemur albocollaris and E. fulvus rufus. International Journal of Primatology, 26: 1399-1416. Accessed November 13, 2014 at http://www.albany.edu/~ag856732/Johnsonetal2005IJP.pdf.

Johnson, S., R. Lei, S. Martin, M. Irwin, E. Louis. 2008. Does Eulemur cinereiceps Exist? Preliminary Evidence From Genetics and Ground Surveys in Southeastern Madagascar. American Journal of Primatology, 70: 372–385. Accessed December 08, 2014 at http://onlinelibrary.wiley.com/doi/10.1002/ajp.20501/pdf.

Johnson, S., Y. Wyner. 2000. Notes on the biogeography of Eulemur fulvus albocollaris. Lemur News, 5: 25-28. Accessed December 05, 2014 at http://www.aeecl.org/lemurnews/lemurnews2000_5.pdf.

Karpanty, S., P. Wright. 2007. Predation on Lemurs in the Rainforest of Madagascar by Multiple Predator Species: Observations and Experiments. Pp. 77-99 in S Gursky-Doyen, K Nekaris, eds. Primate Anti-Predator Strategies. New York, NY: Springer Science & Business Media, LLC.

Lehmann, J., C. Boesch. 2004. To fission or to fusion: effects of community size on wild chimpanzee ( Pan troglodytes verus ) social organisation. Behavioral Ecology and Sociobiology, 5: 207-216. Accessed December 06, 2014 at http://www.eva.mpg.de/primat/staff/boesch/pdf/behav_eco_soc_fiss_fus.pdf.

Linton Zoo, 2014. "White Collared Lemur (Eulemur cinereiceps)" (On-line). Linton Zoological Gardens. Accessed November 15, 2014 at http://www.lintonzoo.com/Documents/Animal%20information/White%20Collared%20Lemur.pdf.

Lonsdorf, E., S. Ross. 2012. Socialization and Development of Behavior. Pp. 245-268 in J Mitani, J Call, P Kappeler, R Palombit, J Silk, eds. The Evolution of Primate Societies. Chicago: University of Chicago Press.

Mittermeier, R. 2006. Lemurs of Madagascar. Washington, D.C.: Conservation International.

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

Richardson, M. 2006. "White-collared brown lemur (Eulemur cinereiceps)" (On-line). Wildscreen Arkive. Accessed November 13, 2014 at http://www.arkive.org/white-collared-brown-lemur/eulemur-cinereiceps/.

San Diego Zoo, 2014. "Mammals: Lemur" (On-line). San Diego Zoo Animals. Accessed December 06, 2014 at http://animals.sandiegozoo.org/animals/lemur.

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