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Range and Conservation Updates for the Critically Endangered Blue-Eyed Black Lemur Eulemur Flavifrons and the Vulnerable Black Lemur Eulemur Macaco

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Range and Conservation Updates for the Critically Endangered Blue-Eyed Black Lemur Eulemur Flavifrons and the Vulnerable Black Lemur Eulemur Macaco Range and conservation updates for the Critically Endangered blue-eyed black lemur Eulemur flavifrons and the Vulnerable black lemur Eulemur macaco J EN C. TINSMAN,CAITLIN L. ESCHMANN,J.SEDERA S OLOFONDRANOHATRA J OCELYN R OMELIUS R ALAINIRINA,MARC H OLDERIED and G RÁINNE M C C ABE Abstract The Critically Endangered blue-eyed black lemur Supplementary material for this article is available at Eulemur flavifrons of north-western Madagascar is one of https://doi.org/./S the most threatened primates. The majority of research and conservation efforts for the species have been restricted to the Sahamalaza Peninsula but there are unstudied and unprotected populations farther inland. The dearth of Introduction information regarding the transition between E. flavifrons and its parapatric sister species, the Vulnerable black lemur adagascar, a biodiversity hotspot (Myers et al., ), . Eulemur macaco, and the possibility of a hybrid population Mis home to endemic species of lemurs, ac- . complicates conservation planning for both species. We counting for % of global primate diversity; however, surveyed forest fragments across both species’ ranges to % of lemur species are threatened by hunting and defor- investigate the boundary between the taxa, whether hybrids estation (Schwitzer et al., ). One of the species most af- persist, and the threats to lemurs in the region. We found fected is the Critically Endangered blue-eyed black lemur E. flavifrons in six fragments and E. macaco in . We never Eulemur flavifrons, which is subject to poaching and habitat observed E. flavifrons and E. macaco inthesamelocation loss as a result of slash-and-burn rice cultivation (tavy), log- and we found no conclusive evidence of hybrids. Three ging and livestock rearing (Andrianjakarivelo, ; Seiler fragments in which E. flavifrons was present were north of et al., ; Andriaholinirina et al., a). The population . the Andranomalaza River, which had previously been con- of the blue-eyed black lemur declined by % during – sidered the barrier between the two species. Based on these (Andriaholinirina et al., a). observations and a literature review, we provide updated Estimates of E. flavifrons numbers have focused mainly ranges, increasing the extent of occurrence (EOO) of E. on the protected population in the Ankarafa Forest of – flavifrons by .% and reducing the EOO of E. macaco by Sahamalaza Iles Radama National Park, where there are – .%. We also evaluate the capacity of protected areas to estimated to be individuals/km (Schwitzer et al., conserve these lemurs. We recommend additional surveys ; Volampeno et al., ). Surveys of the isolated frag- and the implementation of an education programme in ments where E. flavifrons occurs farther inland found this region to help conserve both species. much lower densities, with a mean of individuals/km (Andrianjakarivelo, ). Based on these surveys there Keywords Black lemur, blue-eyed black lemur, geographical are only an estimated ,–, individuals remaining range, Manongarivo Special Reserve, Sahamalaza–Iles (Schwitzer et al., ). A population viability analysis con- Radama National Park, species distribution cluded that the Ankarafa population, which is the largest remaining, could be extirpated by (Volampeno et al., ). The vulnerability of E. flavifrons is partially attribut- ‡ JEN C. TINSMAN* (Corresponding author, orcid.org/0000-0003-2452-4573) able to its unique habitat; the species occurs only in the tran- Columbia University, 116th St and Broadway, New York, New York 10027, USA. E-mail [email protected] sitional, subtropical forest between Madagascar’s western CAITLIN L. ESCHMANN†‡ (Corresponding author) and MARC HOLDERIED School of dry deciduous forests and the humid evergreen rainforests Biological Sciences, University of Bristol, Bristol, UK of the east (Schwitzer et al., ). The plant, amphibian, E-mail [email protected] reptile and mammal communities of the Sahamalaza J. SEDERA SOLOFONDRANOHATRA and JOCELYN ROMELIUS RALAINIRINA University of Peninsula include endemic species that occur nowhere Antananarivo, Antananarivo, Madagascar else on Madagascar (Birkinshaw, ; Schwitzer et al., GRÁINNE MCCABE Bristol Zoological Society, Bristol, UK ; Penny et al., ). *Also at: New York Consortium on Evolutionary Primatology, New York, USA Although not confined to the Sahamalaza Peninsula, E. †Also at: Bristol Zoological Society, College Road, Clifton, Bristol, UK ‡These authors contributed equally to this work. flavifrons has one of the smallest geographical ranges of Received November . Revision requested February . the genus Eulemur (Volampeno et al., ). Its estimated Accepted June . First published online August . extent of occurrence (EOO; i.e. the smallest, continuous Oryx, 2020, 54(6), 819–827 © 2019 Fauna & Flora International doi:10.1017/S0030605318000868 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.42, on 25 Sep 2021 at 10:16:37, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318000868 820 J. C. Tinsman et al. FIG. 1 Previous extent of occurrence polygons for Eulemur macaco and Eulemur flavifrons, from IUCN (used with permission). All known occurrence records for E. flavifrons, E. macaco and putative hybrids, and for Eulemur fulvus, in the area are noted. area encompassing all known or projected occurrences of The first report of phenotypic variation was by Meyers a species; IUCN, )is, , km (Andriaholinirina et al. (), who observed two distinct groups of lemurs un- et al., a). Its area of occupancy (AOO; i.e. the area of like typical E. flavifrons or E. macaco. The first group was at suitable habitat that is actually occupied within a species’ Beraty: individuals had light brown eyes and short ruffs of EOO; IUCN, ) must be even smaller, although it had hair around their ears, characteristics that are intermediate not been estimated previously. between E. flavifrons and E. macaco. The second group was The EOO of E. flavifrons is bounded by the Mozambique at Ambodivoahangy: individuals had darker eyes and redder Channel to the west and the Maevarano River to the south coats than is typical of Sahamalaza E. flavifrons. However, (Koenders et al., ; Petter & Andriatsarafara, ; when Andrianjakarivelo () visited Ambodivoahangy Randriatahina & Rabarivola, ; Schwitzer & Lork, he found animals that ‘greatly resembled’ E. flavifrons. ; Andriaholinirina et al., a; Fig. ). It extends east Goodman and Schütz () surveyed the eastern slopes of to the Sandrakota River and Manongarivo Special Reserve, Manongarivo Special Reserve, north of Ambodivoahangy, which comprises , ha of protected Sambirano rainfor- and identified groups containing both E. macaco and ‘hy- est (MEF & MNP, ). Previous studies have identified the brid’ individuals but did not detail their criteria for these Andranomalaza River, also called the Maitsomalaza in the distinctions. Their assessment was complicated by the local Sakalava dialect, as the boundary between E. flavifrons presence of E. fulvus in that area, which may be perceived and its parapatric sister species, the black lemur Eulemur as having a reddish coat (Goodman & Schütz, ). macaco (Koenders et al., ; Andriaholinirina et al., Updated assessments of the lemurs in this region are ne- a). However, there is conflicting evidence regarding cessary to establish effective conservation initiatives for these whether the lemurs between the Andranomalaza River two species (Rakotonirina et al., , ). They could and the more northern Manongarivo River are hybrids, also improve estimates of the species’ ranges, especially intermediate-appearing forms on a phenotypic cline, or considering the area has not been assessed since typical members of either species (Meyers et al., ; (Schwitzer et al., ). We investigated the presence and Rabarivola et al., ; Andrianjakarivelo, ;Randriatahina phenotypes of Eulemur species from Sahamalaza–Iles & Rabarivola, ). Radama National Park to Manongarivo Special Reserve, Oryx, 2020, 54(6), 819–827 © 2019 Fauna & Flora International doi:10.1017/S0030605318000868 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.42, on 25 Sep 2021 at 10:16:37, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318000868 Lemur conservation updates 821 FIG. 2 Updated extent of occurrence polygons for E. flavifrons and E. macaco based on field work conducted in this study (triangles) and previous published studies (circles). Numbers correspond to numbering of forest fragments in Table . and the threats to their survival, to () establish the contin- We followed the lemurs until they settled down to sleep, ued existence of E. flavifrons outside protected habitat, which enabled us to observe them more closely. We re- () locate the purported contact zone between E. flavifrons corded locations of all observed Eulemur spp. with a GPS and E. macaco, and () understand anthropogenic pressures and noted key morphological features (eye colour, presence in and around the protected areas in this region. We provide of ruffs) to distinguish between E. flavifrons and E. macaco. updated EOOs and new AOOs for both species, and report Evidence of tavy, livestock incursions, traps and hunting on the status of the lemurs between the Manongarivo and was also noted. Andranomalaza Rivers. In addition to field surveys we reviewed the literature for occurrence records of E. flavifrons
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