Overview

Brief Summary

Biology

Collared brown lemurs live in multimale-multifemale groups of around 3 to 12 individuals, although group sizes of 29 individuals have been observed. Breeding is seasonal with mating occurring between June and July. The gestation period is approximately 120 days, with infants born between September and November (5). A single offspring is usual, although twins have been reported (2). Collared brown lemurs reach sexual maturity between one and two years, and the lifespan in the wild is thought to range between 20 and 25 years (2) (5). This species is cathemeral, meaning it is active at varying times throughout the day and night. Fruit forms the bulk of this lemur's diet (4), although young leaves, flowers, bark, sap, soil, insects, centipedes and millipedes may also be eaten (6).
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Description

This medium-sized lemur has a horizontal posture, which is suited to its predominantly quadrupedal mode of movement (2). These lemurs are also capable of leaping considerable distances, their long furry tails assisting them in maintaining their balance (5). Colouration of this lemur differs between the sexes. Males possess brownish-grey upperparts, with a darker tail and paler brown-grey underparts. The muzzle, forehead and crown are dark slate-grey, this colour gradually becoming paler as it extends down the back of the neck, with a dark stripe continuing down the spinal ridge. The cheeks and beard are thick, bushy and cream to reddish-brown in colour. Females have browner, often redder, upperparts than males, while the underparts are pale creamy-grey. The head and face are grey, with a faint grey stripe extending over the crown. The cheeks are considerably shorter and less bushy than in males. The eyes of both sexes are orange-red (2).
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Distribution

Range Description

This lemur is found in southeastern Madagascar from the southern limits of the Ambatotsirongorongo transitional forest south-west of Tolagnaro (J. Razafindramanana, pers. comm.) north to the Mananara River. The western limits of the range are the forests of the Kalambatritra region. The Mananara River serves as a boundary between this species and E. cinereiceps, except for isolated populations at Midongy du Sud National Park (Irwin et al. 2005) and at Vohipaho, near Vangaindrano (S.E. Johnson, pers. comm.). There are also small populations of this species in littoral forest fragments at the Mandena Conservation Zone, Sainte Luce Conservation zone and Sainte-Luce Private Reserve (Donati et al. 2011). Ranges from sea level to 1,875 m.

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Range

Found in south-eastern Madagascar, from the Mananara River south to the area north of Tolagnaro (2).
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Ecology

Habitat

Habitat and Ecology

Habitat and Ecology

The Collared Brown Lemurs are found in wet forest habitats and they have been studied in the littoral forest fragments of Sainte Luce and Mandena (Donati et al. 2011). This lemur is largely frugivorous with minor proportions of flowers and young leaves in the diet during the year (120 plants species from 45 families, Donati et al. 2007). The most important plant species included in the diet are Syzigium spp., Dypsis spp., and Uapaca spp. Collared lemurs are cathemeral animals, remaining active both day and night throughout the year and their activity is strongly influenced by nocturnal luminosity and photoperiodic variations (Donati and Borgognini-Tarli 2006). In littoral forest fragments ranging areas vary from 20 to 100 hectares depending on habitat type and social groups tend to be multi-male/multi-female with average group size from 2 to 17 depending on habitat degradation (Donati et al. 2011). Groups can include as much as 22 individuals in rainforest areas (G. Donati pers. comm). Females give birth in September/October after a gestation of about 120 days and twins are not rare (G. Donati pers. comm).


Systems
  • Terrestrial
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Tropical moist lowland and montane forest (4). Collared brown lemurs are arboreal and spend most of their time in the upper layers of the forest (6).
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Conservation

Conservation Status

IUCN Red List Assessment


Red List Category
EN
Endangered

Red List Criteria
A2cd+3cd+4cd

Version
3.1

Year Assessed
2014

Assessor/s
Andriaholinirina, N., Baden, A., Blanco, M., Chikhi, L., Cooke, A., Davies, N., Dolch, R., Donati, G., Ganzhorn, J., Golden, C., Groeneveld, L.F., Hapke, A., Irwin, M., Johnson, S., Kappeler, P., King, T., Lewis, R., Louis, E.E., Markolf, M., Mass, V., Mittermeier, R.A., Nichols, R., Patel, E., Rabarivola, C.J., Raharivololona, B., Rajaobelina, S., Rakotoarisoa, G., Rakotomanga, B., Rakotonanahary, J., Rakotondrainibe, H., Rakotondratsimba, G., Rakotondratsimba, M., Rakotonirina, L., Ralainasolo, F.B., Ralison, J., Ramahaleo, T., Ranaivoarisoa, J.F., Randrianahaleo, S.I., Randrianambinina, B., Randrianarimanana, L., Randrianasolo, H., Randriatahina, G., Rasamimananana, H., Rasolofoharivelo, T., Rasoloharijaona, S., Ratelolahy, F., Ratsimbazafy, J., Ratsimbazafy, N., Razafindraibe, H., Razafindramanana, J., Rowe, N., Salmona, J., Seiler, M., Volampeno, S., Wright, P., Youssouf, J., Zaonarivelo, J. & Zaramody, A.

Reviewer/s
Schwitzer, C. & Molur, S.

Contributor/s

Justification

Listed as Endangered as the species is suspected to have undergone a population decline of ≥50% over a period of 24 years (three generations), due primarily to continuing decline in area, extent and quality of habitat caused by charcoal production and slash-and-burn agriculture, and exploitation through unsustainable levels of hunting. Ilmenite mining is also threatening this species. These causes have not ceased, and will to a large extent not be easily reversible. The population is predicted to decline in the future at the same rate over three generations (24 years).


History
  • 2000
    Vulnerable
  • 1996
    Vulnerable
  • 1994
    Vulnerable
    (Groombridge 1994)
  • 1990
    Vulnerable
    (IUCN 1990)
  • 1990
    Vulnerable
    (IUCN 1990)
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Status

Classified as Vulnerable (VU A1cd, B1+2bc) on the IUCN Red List 2004 (1), although classified here as a subspecies (Eulemur fulvus collaris) of the brown lemur (Eulemur fulvus), which is also listed under Appendix I of CITES (3). Recent scientific thought is that the collared brown lemur should be elevated to species status, as Eulmur collaris (4).
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Population

Population

In littoral forest fragments densities of this species are high (74 to 139 individuals/km2)(Ganzhorn et al. 2007, T. Nguyen pers. comm.). In Midongy du Sud, densities were recorded at 14 individuals/km2 (Irwin et al. 2005). In Andoahela National Park and Tsitongambarika densities recorded are respectively 8 and 11 individuals/km2 (G. Donati pers. comm.).


Population Trend
Decreasing
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Threats

Major Threats

The principal threat to the survival of E. collaris is habitat destruction, due to charcoal production and slash-and-burn agriculture (Bollen and Donati 2006). It is also widely hunted for food and trapped occasionally for the local pet trade. Ilmenite mining is also threatening the remaining populations in littoral forest fragments.

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Habitat destruction remains the primary threat to this lemur, largely as a result of the explosive growth in the human population on Madagascar (5). Hunting and trapping for food or the pet trade also constitute a significant threat to the collared brown lemur (2).
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Management

Conservation Actions

Conservation Actions

This species is listed on Appendix I of CITES. It is reported to occur in two national parks (Andohahela and Midongy du Sud), the Kalambatritra Special Reserve, The Tsitongambarika Protected Area, Mandena and Sainte Luce Conservation Zones, and Sainte Luce Private Reserve. An introduced population of E. collaris/E. rufifrons hybrids is present in the Berenty Private Reserve (Donati et al. 2009). As of 2009, there were 37 Collared Brown Lemurs reported in zoological collections in Europe and North America (ISIS 2009).

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Conservation

The collared brown lemur is known to occur naturally in only two national parks, Andohahela and Midongy du Sud, but has also been introduced into two private reserves, Kalambatritra Special Reserve and St. Luce Private Reserve (4). Captive bred populations also exist in institutions worldwide (5). The fate of the collared brown lemur will most probably be determined by the future of its forest habitat, which needs to be better preserved if the survival of this lemur is to be safeguarded.
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Wikipedia

Collared brown lemur

The collared brown lemur (Eulemur collaris), also known as the red-collared brown lemur or red-collared lemur, is a medium-sized strepsirrhine primate and one of twelve species of brown lemur in the Lemuridae family. It is only found in south-eastern Madagascar. Like most species of lemur, it is arboreal, moving quadrupedally and occasionally leaping from tree to tree. Like other brown lemurs, it lives in social groups, primarily eats fruit, is active both day and night, exhibits sexual dichromatism, and does not demonstrate female dominance. The species is listed as Vulnerable by the International Union for Conservation of Nature (IUCN) and is threatened primarily by habitat loss.

Taxonomy[edit]

Together with the twelve other true lemurs (genus Eulemur),[3] the collared brown lemur (E. collaris) is a type of lemur belonging to the family Lemuridae. Collectively, lemurs (infraorder Lemuriformes) are classified as strepsirrhine primates. Originally listed as a subspecies of the common brown lemur (E. fulvus), the collared brown lemur was promoted to full species status in 2001 by biological anthropologist Colin Groves.[1]

Anatomy and physiology[edit]

An adult collared brown lemur can reach a head-body length of 39 and 40 cm (15 and 16 in) and have a tail length of 50 and 55 cm (20 and 22 in) for an overall length of 89 and 95 cm (35 and 37 in). It has an average body weight of 2.25 and 2.5 kg (5.0 and 5.5 lb), making it a medium-sized lemur.[4][5] The only form of sexual dimorphism exhibited by the collared brown lemur is dichromatism. The following table illustrates the coloration differences between the sexes:

Differences in coloration between sexes in the collared brown lemur[4][5]
MaleFemale
Dorsal coatBrownish-grayBrowner and more rufous than the male's
Ventral coatPaler grayPale creamy-gray
TailDarker gray with a dark stripe along the spineSame as dorsal coat
Face and headMuzzle, face and crown are dark gray to black; creamy to gray-colored eyebrow patches vary between individualsGray, with faint gray stripe extending over crown
CheeksCreamy to rufous-brown cheeks and beard are thick and bushyRufous-brown, but less prominent than the male's
Eyesorange-redorange-red
Illustration of female (top) and male (bottom) heads, seen from the right. Female is mostly gray with some rufous-brown coloration on the cheeks. Males has mostly dark gray or black muzzle, face, and crown; as well as thick and bushy rufous-brown cheeks and beard. Both have big ears and a long snout
Collared brown lemurs:
Female (top) and male (bottom)
(Illustration from 1892)

In the wild, the collared brown lemur's range does not overlap with other brown lemurs, so it is rarely confused with other species.[5] However, in captivity it can be easily confused with the gray-headed lemur (Eulemur cinereiceps) due to similar coloration. The male collared brown lemur can be distinguished by their cream-colored or rufous beards, whereas the male gray-headed lemur has a white beard. Females of these two species are nearly indistinguishable, even though genetic analyses support full species status for both taxa.[4]

Ecology[edit]

Found in tropical moist lowland and montane forests in southeastern Madagascar, the collared brown lemur occurs west to the forests of Kalambatritra and in the south from Tôlanaro north to the Mananara River.[2][4][5] The Mananara River is the boundary between the ranges of the collared brown lemur and the Gray-headed Lemur to the north. The collared brown lemur can be seen in the Mandena Conservation Zone, Saint Luce Private Reserve, and Andohahela National Park.[4]

In its environment, the collared brown lemur acts as a seed disperser, and is especially critical for the dispersal of large-seeded fruiting trees within its range.[6] However, there is no evidence that these relationships are coevolutionary and instead these lemurs may be the last remaining seed dispersers for these tree species following the extinction of larger frugivorous birds and subfossil lemurs.[7]

Behavior[edit]

Very little is known about this species. It is thought to primarily eat fruit, like most other true lemurs.[4] It is also cathemeral (active both day and night throughout the year), a trait seen in some other members of its genus.[4][5] Research has suggested that metabolic dietary-related needs are the leading factor behind this behavior, although the specific hours of this activity pattern can shift based on lunar luminosity and seasonal changes in the photoperiod (day length).[8] Previous studies had ruled out effects of predators on the expression of this trait, and instead pointed to fruit availability and fiber intake as more important factors.[9]

The collared brown lemur tends to live in social groups that are multi-male/multi-female,[4] with groups ranging in size from three to seven.[5] Population densities are estimated at 14 individuals/km2, and it appears to be common within its range.[4] Females give birth to one offspring between October and December, and male involvement with the young has been observed.[5] Female dominance, a common behavioral trait in many lemur species but uncommon in most true lemurs, has not been observed in this species.[4][10]

Brown lemurs at Berenty (hybrid E. fulvus x collaris) [11] show linear hierarchy, adult female dominance, and the presence of conciliatory behavior after aggressions.[12] Additionally, stress levels (measured via self-directed behaviors) decrease at the increase of the hierarchical position of individuals within the social group and reconciliation is able to bring stress down to the baseline levels.[13]

Conservation status[edit]

Male collared brown lemur sits on a rock behind a female, who swats and eats plant material
Populations of collared brown lemur have successfully been maintained in captivity.

The collared brown lemur was listed as Vulnerable (VU A2cd) in the 2008 IUCN Red List assessment.[2] Its greatest threat is habitat loss from slash-and-burn agriculture and charcoal production. It is also hunted for food and captured for the local pet trade.[4] Populations of the collared brown lemur have been successfully sustained in captivity as a safeguard against their extinction.[14]

A small group of collared brown lemurs was introduced in the 1980s into the Berenty Private Reserve and has since hybridized with introduced red-fronted lemurs.[4]

References[edit]

  1. ^ a b Groves, C. P. (2005). "Eulemur collaris". In Wilson, D. E.; Reeder, D. M. Mammal Species of the World (3rd ed.). Baltimore: Johns Hopkins University Press. OCLC 62265494. ISBN 0-801-88221-4. 
  2. ^ a b c Andriaholinirina, N., Baden, A., Blanco, M., Chikhi, L., Cooke, A., Davies, N., Dolch, R., Donati, G., Ganzhorn, J., Golden, C., Groeneveld, L.F., Hapke, A., Irwin, M., Johnson, S., Kappeler, P., King, T., Lewis, R., Louis, E.E., Markolf, M., Mass, V., Mittermeier, R.A., Nichols, R., Patel, E., Rabarivola, C.J., Raharivololona, B., Rajaobelina, S., Rakotoarisoa, G., Rakotomanga, B., Rakotonanahary, J., Rakotondrainibe, H., Rakotondratsimba, G., Rakotondratsimba, M., Rakotonirina, L., Ralainasolo, F.B., Ralison, J., Ramahaleo, T., Ranaivoarisoa, J.F., Randrianahaleo, S.I., Randrianambinina, B., Randrianarimanana, L., Randrianasolo, H., Randriatahina, G., Rasamimananana, H., Rasolofoharivelo, T., Rasoloharijaona, S., Ratelolahy, F., Ratsimbazafy, J., Ratsimbazafy, N., Razafindraibe, H., Razafindramanana, J., Rowe, N., Salmona, J., Seiler, M., Volampeno, S., Wright, P., Youssouf, J., Zaonarivelo, J. & Zaramody, A. (2014). "Eulemur collaris". IUCN Red List of Threatened Species. Version 2014.1. International Union for Conservation of Nature. Retrieved 2014-06-16. 
  3. ^ Mittermeier, R.; Ganzhorn, J.; Konstant, W.; Glander, K.; Tattersall, I.; Groves, C.; Rylands, A.; Hapke, A.; Ratsimbazafy, J.; Mayor, M.; Louis, E.; Rumpler, Y.; Schwitzer, C.; Rasoloarison, R. (2008). "Lemur Diversity in Madagascar". International Journal of Primatology 29 (6): 1607–1656. doi:10.1007/s10764-008-9317-y. 
  4. ^ a b c d e f g h i j k l Mittermeier, R.A.; Konstant, W.R.; Hawkins, F.; Louis, E.E.; Langrand, O.; Ratsimbazafy, J.; Rasoloarison, R.; Ganzhorn, J.U.; Rajaobelina, S.; Tattersall, I.; Meyers, D.M. (2006). Lemurs of Madagascar. Illustrated by S.D. Nash (2nd ed.). Conservation International. pp. 278–279. ISBN 1-881173-88-7. 
  5. ^ a b c d e f g Garbutt, N. (2007). Mammals of Madagascar, A Complete Guide. A&C Black Publishers. pp. 164–165. ISBN 978-0-300-12550-4. 
  6. ^ Bollen, A.; Van Elsacker, L.; Ganzhorn, J.U. (2004). "Relations between fruits and disperser assemblages in a Malagasy littoral forest: a community-level approach". Journal of Tropical Ecology (Cambridge University Press) 20 (6): 599–612. doi:10.1017/S0266467404001853. 
  7. ^ Bollen, A.; Van Elsacker, L.; Ganzhorn, J.U. (2004). "Tree dispersal strategies in the littoral forest of Sainte Luce (SE-Madagascar)". Oecologia (Springer Berlin / Heidelberg) 139 (4): 604–616. doi:10.1007/s00442-004-1544-0. PMID 15095087. 
  8. ^ Donatia, G.; Baldib, N.; Morellib, V.; Ganzhorn, J.U.; Borgognini-Tarli, S.M. (2009). "Proximate and ultimate determinants of cathemeral activity in brown lemurs". Animal Behaviour 77 (2): 317–325. doi:10.1016/j.anbehav.2008.09.033. 
  9. ^ Donati1, G.; Bollen, A.; Borgognini-Tarli, S.M.; Ganzhorn, J.U. (2007). "Feeding over the 24-h cycle: dietary flexibility of cathemeral collared lemurs (Eulemur collaris)". Behavioral Ecology and Sociobiology (Springer Berlin / Heidelberg) 61 (8): 1237–1251. doi:10.1007/s00265-007-0354-x. 
  10. ^ Sussman, R. (1999). Primate Ecology and Social Structure Volume 1: Lorises, Lemurs and Tarsiers. Pearson Custom Publishing. p. 214. ISBN 0-536-02256-9. 
  11. ^ Alison Jolly, Naoki Koyama, Hantanirina Rasamimanana, Helen Crowley, and George Williams (2006). "Berenty Reserve: a research site in southern Madagascar". In A. Jolly, R. W. Sussman, N. Koyama & H. Rasamimanana. Ringtailed Lemur Biology: Lemur catta in Madagascar. pp. 32–42. ISBN 0-387-32669-3. 
  12. ^ Norscia, I., Palagi, E. (2010). "Do wild brown lemurs reconcile? Not always". Journal of Ethology. doi:10.1007/s10164-010-0228-y. 
  13. ^ Palagi, E., Norscia, I. (2010). "Scratching around stress: hierarchy and reconciliation make the difference in wild brown lemurs Eulemur fulvus". Stress. doi:10.3109/10253890.2010.505272. 
  14. ^ "ISIS Species Holdings, Eulemur collaris". International Species Information System (ISIS). 2010. Retrieved 26 February 2010. 
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