Sclater’s Black , Blue-Eyed Black Lemur Eulemur flavifrons (Gray, 1867) (2008)

Christoph Schwitzer, Pierre Moisson, Guy H. Randriatahina, Sylviane Volampeno, Nora Schwitzer & Clément J. Rabarivola

The blue-eyed black lemur or Sclater’s black lemur was rediscovered by science only in 1983 after more than a century of uncertainty about its existence (Koenders et al. 1985; Meier et al. 1996). Its taxonomic validity was thereafter confirmed independently by Rabarivola (1998) and Pastorini (2000). The species was until recently regarded as a subspecies of Eulemur macaco, but was elevated to full species status on the basis of the consistency of the morphological differences between the black lemur and the blue- eyed black lemur and the pairwise genetic distances between macaco and flavifrons of 68–72 bp (which are in the same range as between the former E. fulvus subspecies, i.e., 29–90 bp, according to Pastorini 2000). Furthermore, the fact that the hybrid zone between the two taxa is restricted to just the north-eastern part density of E. flavifrons in eight inventoried forest of the distribution of E. flavifrons (Andrianjakarivelo fragments to be 24 individuals per km2 (range: 4–85 2004; Schwitzer et al. 2005, 2006; Mittermeier et al. ind./km2). A total count in two different fragments 2008) is in favour of this new . of the Ankarafa forest on the Sahamalaza Peninsula Eulemur flavifrons is still one of the least-studied yielded a density of 60 individuals per km2 (Schwitzer of all Eulemur species. The species occurs only in et al. 2005, 2007a). However, the density of the species northwest Madagascar in a very small area of about 2 in Ankarafa seems to be higher than in any other 2,700 km , south of the Andranomalaza, north of the forest in the range of E. flavifrons (Randriatahina and Maevarano, and west of the Sandrakota rivers, where Rabarivola 2004). Extrapolating the two density it inhabits primary and secondary forest fragments estimates of Andrianjakarivelo (2004) and Schwitzer (Koenders et al. 1985; Meyers et al. 1989; Rabarivola et al. (2005) to the total surface of the terrestrial core et al. 1991; Mittermeier et al. 1994). The area of zones of the recently created Sahamalaza – Iles Radama repartition of Eulemur flavifrons lies within a transition National Park (115.8 km2) yields a remaining, severely zone between the humid Sambirano region in the fragmented population of 2780–6950 blue-eyed black north and the western dry deciduous forest region . Eulemr flavifrons was assessed as Critically in the south, harboring semi-humid forests with tree Endangered (CR A2cd) by the International Union for heights of up to 30 m on ferruginous alkalescent and Conservation of Nature (IUCN) at their most recent alkaline soils based on sandstone, basalt or clay (IRNT Red List Assessment in April 2005, based on an 80% 1991a). Average annual precipitation is around 1,600 population reduction during the last 25 years. The mm (IRNT 1991b). principal threats to its survival are forest destruction There is only a small population of Eulemur due to slash-and-burn agriculture and selective flavifrons remaining, the largest part of it living in forest logging, continued hunting and trapping, especially fragments on and adjacent to the Sahamalaza peninsula by the Tsimihety in the eastern part of its distribution, (Mouton 1999). Rakotondratsima (1999) estimates the and live capture for the local pet trade (Gerson 1995; population of the Sahamalaza peninsula to be about Rakotondratsima 1999). Andrianjakarivelo (2004) 450–2,300 individuals and to have declined about found a density of up to 570 traps/km2 in certain areas 35.3% in three years (see also Andriamanandratra where E. flavifrons occurs. 1996). Andrianjakarivelo (2004) found the mean The blue-eyed black lemur’s home range size and

18 use differs between primary and secondary forest The European captive population of the subspecies fragments, indicating that it is somewhat able to adapt is being managed in a European Endangered Species to different types of habitat. Larger home ranges and Programme (EEP) coordinated by Mulhouse Zoo. lower densities of E. flavifrons in secondary forest as compared to primary forest, however, suggest that References the former is less suitable habitat for the species (Schwitzer et al. 2007a). During a 12-month study, E. Andriamanandratra, A. N. 1996. Proposition pour un flavifrons consumed parts of 72 different plant species nouveau parc national dans la région du Nord-Ouest from 35 families; 52.3% of these were fruits and 47.7% de Madagascar: un commencement intégratif. Report to AEECL. Parc Zoobotanique et Botanique, Mulhouse. were leaves. The also fed on flowers, insects, 51pp. insect exudates and fungi (Polowinsky and Schwitzer Andrianjakarivelo, V. 2004. Exploration de la zone en dehors in press). Eulemur flavifrons exhibits a bimodal activity de la peninsule Sahamalaza pour l’évaluation rapide de pattern, which peaks during the morning and evening la population d’E. m. flavifrons. Unpublished report to twilight. It shows activity bouts during the day and the Wildlife Conservation Society (WCS), Antananarivo. night year-round. Nocturnal illumination and the 31pp. proportion of illuminated lunar disc are positively Gerson, J. S. 1995. The status of Eulemur macaco flavifrons at associated with the amount of nocturnal activity. Total two localities in northwestern Madagascar. American daily activity, as well as nocturnal activity, is higher in Journal of Physical Anthropology Suppl. 20: 98. Abstract. Koenders, L., Y. Rumpler, J. Ratsirarson and A. Peyrieras. secondary forest than in primary forest (Schwitzer et 1985. Lemur macaco flavifrons (Gray, 1867): a rediscovered al. 2007b). subspecies of . Folia Primatologica 44: 210–215. Blue-eyed black lemur groups are multi-male Lernould, J.-M. 2002. Un programme international de multi-female, ranging in size from 6 to 10 individuals, recherche et de conservation pour le lémur aux yeux including 4 to 7 adults (G. H. Randriatahina and J. J. turquoise (Eulemur macaco flavifrons). Lemur News 7: Roeder in prep.). Both sexes disperse, but only males 30–33. have been seen moving into a foreign social group. Madagascar, IRNT. 1991a. Carte des ressources en sols. The sex ratio at birth varies strongly between years Feuille SC 38 L. Antananarivo: FTM. Projet Inventaire and could be male-biased (G. H. Randriatahina and J. des Ressources Naturelles Terrestres de Madagasikara. 1p. J. Roeder in prep.). Births occur between late August Madagascar, IRNT. 1991b. Carte des ressources en eaux. and October, at the end of the dry season. During two Feuille SC 38 L. Antananarivo: FTM. Projet Inventaire des successive birth seasons, infant mortality was 22.7%. Ressources Naturelles Terrestres de Madagasikara.1p. Infants start to become independent at around eleven Meier, B., A. Lonina and T. Hahn. 1996. Expeditionsbericht weeks of age (S. Volampeno in prep.). Sommer 1995 – Schaffung eines neuen Nationalparks in Parts of the Sclater’s black lemur’s range officially Madagaskar. Zeitschrift des Kölner Zoo 39(2): 61–72. received protected area status in June 2007 (Parc Meyers, D. M., C. Rabarivola and Y. Rumpler. 1989. National Sahamalaza – Iles Radama), including the Distribution and conservation of Sclater’s lemur: Sahamalaza Peninsula and some mainland forests implications of a morphological cline. Primate Conservation (10): 77–81. to the north and east (Moisson et al. 1999; Lernould Mittermeier R. A., I. Tattersall, W. R. Konstant, D. M. Meyers 2002; Schwitzer and Lork 2004; Schwitzer et al. and R. B. Mast. 1994. Lemurs of Madagascar. Conservation 2006). The Sahamalaza Peninsula is also a UNESCO International Tropical Field Guide Series, Conservation Biosphere Reserve. The Association Européenne pour International, Washington, DC. l’Etude et la Conservation des Lémuriens (AEECL) is Mittermeier, R. A., J. U. Ganzhorn, W. R. Konstant, K. a consortium of European zoos that have joined Glander, I. Tattersall, C. P. Groves, A. B. Rylands, A. forces to conserve Madagascar’s lemurs, with the Hapke, J. Ratsimbazafy, M. I. Mayor, E. E. Louis Jr., Y. involvement of representatives of local communities Rumpler, C. Schwitzer and R. M. Rasoloarison. 2008. from the Sahamalaza Peninsula and representatives Lemur diversity in Madagascar. International Journal of Primatology 29: 1607–1656. of WCS and several other environmental institutions. Moisson, P., Y. Rumpler, J.-M. Lernould and G. Nogge. AEECL implemented a natural resource management 1999. Creation of a natural reserve for Eulemur macaco programme in Sahamalaza in December 2000 in order flavifrons in the north-west of Madagascar: an update. to protect the remaining lemur habitat and to improve Folia Primatologica 70(4): 201. Abstract. the living standards of the local human population. Moisson, P. and C. Prieur. 2008. European studbook for AEECL also maintains a field station in Sahamalaza, Sclater’s lemur (Eulemur macaco flavifrons), n°5. Parc which serves as a basis for studying the conservation Zoologique et Botanique, Mulhouse. 25pp. ecology of E. flavifrons and of other lemur species in Mouton, E. 1999. Mission de terrain sur la presqu’île the area. de Sahamalaza (Nord-ouest Madagascar). Rapport préliminaire pour la création d’une aire protégée. Parc As of 2008, there were 30 blue-eyed black lemurs Zoologique et Botanique, Mulhouse. 23pp. living in European zoos (Moisson and Prieur 2008). Pastorini, J. 2000. Molecular Systematics of Lemurs. PhD

19 dissertation, Universität Zürich, Zürich. 183pp. Polowinsky, S. Y. and C. Schwitzer. In press. Nutritional ecology of the blue-eyed black lemur (Eulemur flavifrons): Integrating in situ and ex situ research to assist the conservation of a critically endangered species. In: Zoo Nutrition Vol. IV, M. Clauss et al. (eds.). Filander Verlag, Fuerth. Rabarivola, C. 1998. Etude génétique comparative de populations insulaires et “continentales” de Eulemur macaco. Utilisation simultanée des dermatoglyphes, de marqueurs sanguins et de l’ADN (RAPD) pour étudier la différenciation de E. macaco en deux sous-espèces: E. m. macaco et E .m. flavifrons. Doctoral thesis, Université d’Antananarivo, Antananarivo. Rabarivola, C., D. Meyers and Y. Rumpler. 1991. Distribution and morphological characters of intermediate forms between the black lemur (Eulemur macaco macaco) and Sclater’s lemur (Eulemur macaco flavifrons). 32(2): 269–273. Rakotondratsima, M. 1999. Etude quantitative de Eulemur macaco flavifrons dans la presqu’île Radama. In: Wildlife Conservation Society Madagascar Country Program: Evaluation de l’état de l’environnement naturel terrestre de la presqu’île Radama, pp.15–29. The Wildlife Conservation Society (WCS), Antananarivo. Randriatahina, G. H. and J. C. Rabarivola. 2004. Inventaire des lémuriens dans la partie nord-ouest de Madagascar et distribution d’Eulemur macaco flavifrons. Lemur News 9: 7–9. Schwitzer, C. and A. Lork. 2004. “Projet Sahamalaza – Iles Radama“: Ein internationales Schutzprojekt für den Sclater’s Maki (Eulemur macaco flavifrons Gray, 1867). Zeitschrift des Kölner Zoo 47(2): 75–84. Schwitzer. C., N. Schwitzer, G. H. Randriatahina, C. Rabarivola and W. Kaumanns. 2005. Inventory of the Eulemur macaco flavifrons population in the Sahamalaza protected area, northwestern Madagascar, with notes on an unusual colour variant of E. macaco. Primate Report Special Issue 72–1: 39-40. Abstract. Schwitzer, C., N. Schwitzer, G. H. Randriatahina, C. Rabarivola and W. Kaumanns. 2006. “Programme Sahamalaza”: New perspectives for the in situ and ex situ study and conservation of the blue-eyed black lemur (Eulemur macaco flavifrons) in a fragmented habitat. In: Proceedings of the German-Malagasy Research Cooperation in Life and Earth Sciences, C. Schwitzer, S. Brandt, O. Ramilijaona, M. Rakotomalala Razanahoera, D. Ackermand, T. Razakamanana and J. U. Ganzhorn (eds.), pp.135–149. Concept Verlag, Berlin. Schwitzer, N., G. H. Randriatahina, W. Kaumanns, D. Hoffmeister and C. Schwitzer. 2007. Habitat utilization of blue-eyed black lemurs, Eulemur macaco flavifrons (Gray, 1867), in primary and altered forest fragments. Primate Conservation (22): 79–87. Schwitzer, N, W. Kaumanns, P. C. Seitz and C. Schwitzer C. 2007. Cathemeral activity patterns of the blue-eyed black lemur Eulemur macaco flavifrons in intact and degraded forest fragments. Endangered Species Research 3: 239–247.

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