Eulemur cinereiceps (A. Grandidier & A. Milne-Edwards, 1890)

Russell A. Mittermeier, Anthony B. Rylands & Don E. Wilson, 2013, Lemuridae, Handbook of the Mammals of the World – Volume 3 Primates, Barcelona: Lynx Edicions, pp. 90-141 : 135

13.

White-collared Brown Lemur

Eulemur cinereiceps

French: Lémur a collier blanc / German: \Wei3wangen-Halsbandmaki / Spanish: Lémur pardo de cabeza gris

Other common names: Gray-headed Brown Lemur, Gray-headed Lemur, White-collared Lemur

Taxonomy. Lemur mongoz var. cinereiceps Grandidier & Milne-Edwards, 1890 ,

Madagascar, probably Farafangana.

There has been much confusion surrounding this species. It was first described in 1890 by A. Grandidier and H. Milne-Edwards in an illustration in their monumental work on Madagascar. The specimens upon which the illustration was based were female, hence the Latin name cinereiceps (gray head). Unfortunately, although the Grandidier plates are excellent, text was produced only for the Indriidae , not for the remaining lemurs. E. Schwarz, in 1931, assigned the cinereiceps name to two specimens in the Paris Museum of Natural History, collected from two localities in south-eastern Madagascar, Farafangana and Solohy. This animal remained in obscurity for a long time, until it was resurrected by C. P. Groves in 1974. Unaware ofthis, Y. Rumpler in 1975 described the White-collared Brown Lemur as Lemur albocollaris , and this name, later changed to E. albocollaris , was used for more than three decades. A recent survey found that the animals living in Farafangana and Solohy were in fact what had usually been referred to as E. albocollaris . This evidence, added to that of Schwarz, seemed to confirm that the cinereiceps of Grandidier and Milne-Edwards was based on females of the species named albocollaris by Rumpler. In 2008, S. Johnson and coworkers reviewed the literature and concluded that, according to Article 23.9.1 of the International Code of Zoological Nomenclature, the senior synonym could not, in this instance, be rejected, and that the correct name of the White-collared Brown Lemur was indeed E. cinereiceps . Consequently, this name has been universally adopted for the brown lemur species from this part of south-eastern Madagascar, and the name E. albocollaris is no longer used. A hybrid zone with E. rufifrons is evident at the Iantara River (headwaters of the Manampatrana) near Andringitra National Park. Although externally very similar, genetic analyses support full species status for both E. cinereiceps and E. collaris , as do field studies in apparent hybrid zones of E. rufifrons and E. cinereiceps . Monotypic.

Distribution. SE Madagascar in a thin strip of forest from just above the Manampatrana River S to the Mananara River, with a small isolated population at Manombo and Agnalazaha on the coast S of Farafangana.

Descriptive notes. Head—body 39-40 cm, tail 50-55 cm; weight 2 kg. The White-collared Brown Lemuris a medium-sized, sexually dichromatic species. In males, the dorsal coat is gray-brown, often with a dark brown stripe running along the spine, and the tail and lower limbs are slightly darker. The ventral coat, head, and face are a paler gray. A dark gray crown turns lighter on the neck and shoulders. Cheeks and cheek ruffs are white or light cream and bushy. Coloration of male White-collared Brown Lemursis very similar to that of the Red-collared Brown Lemur (£. collaris ), except that male White-collared Brown Lemurs have white beards rather than the orange-rufous beards of the Red-collared Brown Lemurs. Female White-collared Brown Lemurs are more reddish overall than males, and they are virtually indistinguishable from female Red-collared Brown Lemurs, the coat being reddish-brown above with lighter underparts. Their faces are uniformly slate-gray, with a short reddish-brown beard that matches the coat color and is not bushy like that of the male.

Habitat. Tropical moist lowland forest from sea level to elevations of 615 m.

Food and Feeding. Diets of theWhite-collared Brown Lemur consist mainly of fruits (almost 70% in one study), supplemented with young leaves, flowers, fungi, and animal prey including centipedes, millipedes, and spiders. Flowers are an especially important food item late in the dry season. In Manombo Special Reserve, 54 plant species in 24 families have been recorded as food resources of the White-collared Brown Lemur . Dietary variety is considerably lower in the dry season than in the wet season. Parts of non-native plants, such as the spicy fruits of Aframomum angustifolium ( Zingiberaceae ), seem to make up almost 25% of the diet in Manombo.

Breeding. There is no information available for this species.

Activity patterns. The White-collared Brown Lemur is cathemeral and arboreal. It remains active both day and night throughout the year. In a recent behavioral study conducted in Manombo Special Reserve, individuals rested more than 40% of the time and engaged in social behaviors more than 30% of the time. Feeding and traveling each accounted for c.12% of total observation time.

Movements, Home range and Social organization. Information regarding the natural history of the White-collared Brown Lemur comes largely from studies conducted in the forests of Vevembe. Social groups tend to be multimale-multifemale and relatively large, and they regularly exhibit fission-fusion. When resources are abundant in the wet season, it occurs in larger groups. Groups split into smaller units at times of food scarcity to avoid conflict over access to limited resources. Female dominance has not been observed. Densities are 8-7 ind/km? in Agnalazaha, 10-9 ind/km? in Vevembe, and 13-5 ind/km?in Manombo.

Status and Conservation. CITES Appendix I. Classified as Endangered on The IUCN Red List, but a subsequent review has concluded that it should be critically endangered. At the IUCN/SSC Lemur Red-Listing Workshop held in July 2012, E. cinereiceps was indeed assessed as critically endangered. The White-collared Brown Lemur has the most restricted distribution of any species of Fulemur. It occurs in a largely continuous inland forest block (Vevembe) and some small coastal fragments (Manombo, Agnalazaha); satellite imagery shows that total habitat remaining within its distribution is little more than 700 km? In 1997, a powerful cyclone reduced the total population of White-collared Brown Lemurs by ¢.50%. It has apparently hybridized extensively with the Red-fronted Brown Lemur in the northern part of its range, ¢.50% ofits total distribution, and coastal populations have suffered a significant genetic bottleneck. Effective population size (i.e. number of breeding individuals) falls well below total population estimates. In recognition of these factors, the White-collared Brown Lemur (under the name E. albocollaris ) was listed as one of the world’s 25 Most Endangered Primates in 2004 and 2006. Principal threats to its survival are habitat loss due to slashand-burn agriculture and logging, and hunting with snares, shotguns, and slingshots. Apparently, it is easily baited and trapped during the fruiting season of the strawberry guava ( Psidium cattleianum, Myrtaceae ). On the coast, the White-collared Brown Lemur numbers only in the low hundreds. The only protected areas in which it occurs are the Manombo Special Reserve and nearby Agnalazaha Forest, which is now being managed by the Missouri Botanical Garden. Unfortunately, these two areas represent less than 5% of the total remaining habitat within its distribution. It also occurs in two unprotected forests, Vevembe and Lambohazo, west of Vondrozo, both of which could be added to existing parks and reserves. Expansion of the Manombo Special Reserve to include the neighboring classified forest is a high conservation priority, as is preservation of the existing hybrid zone. A detailed search of remaining forests in the immediate Farafangana region is also a high priority, because protected areas in the broader region surrounding Farafangana all seem to harbor the White-collared Brown Lemur . Conservation International is presently initiating programs for the management of the Fandriana-Vondrozo forest corridor. This will be critical for the long-term survival of the White-collared Brown Lemur because the vast majority of populations are found within this corridor and few are presently protected. The overall population estimate is less than 1000 individuals.

Bibliography. Bradley et al. (1997), Brenneman et al. (2012), Delmore et al. (2009, 2011), Djletati et al. (1997), Garbutt (2007), Groves (1974), Irwin et al. (2005), Johnson (2002), Johnson & Overdorff (1999), Johnson & Wyner (2000), Johnson et al. (2005, 2008, 2009, 2011), Mittermeier et al. (2010), Petter & Petter-Rousseaux (1979), Ralainasolo et al. (2008), Rumpler (1975), Schwarz (1931), Sterling & Ramaroson (1996), Tattersall (1982, 1986b), Wyner, Absher et al. (1999), Wyner, Johnson et al. (2002).

Figures

8. Brown (Lemur Fulemurfulvus), 9. Rufous Brown Lemur (Eulemur rufus), 10. Red-fronted Brown Lemur (FEulemur rufifrons), 11. White-fronted Brown Lemur (Eulemur albifrons), 12. Sanford’s Brown Lemur (Fulemur sanfordi), 13. White-collared Brown Lemur (Eulemur cinereiceps), 14. Red-collared Brown Lemur (Eulemur collars), 15. Black Lemur (Eulemur macaco), 16. Blue-eyed Black (Lemur Eulemurflavifrons), 17. Crowned Lemur (Eulemur coronatus), 18. Red-bellied Lemur (Eulemur rubriventer), 19. Mongoose Lemur (Eulemur mongoz)

Distribution. SE Madagascar in a thin strip of forest from just above the Manampatrana River S to the Mananara River, with a small isolated population at Manombo and Agnalazaha on the coast S of Farafangana.