Habitat fragmentation is one of the major types of anthropogenic change, though fragmented landscapes predate human intervention. At present, the Central Highlands of Madagascar are covered by extensive grasslands interspersed with small discrete forest patches of unknown antiquity. Ankafobe, an actively protected site, comprises two such fragments of 12 and 30 ha, respectively, known to harbor three lemur species and other endemic wildlife. At this location, we conducted a survey of resident Goodman’s mouse lemurs, Microcebus lehilahytsara, to determine baseline behavioral and ecological conditions for this isolated population. By studying primates in forest fragments, investigators can characterize the effects of shrinking habitats and decreasing connectivity on species diversity and survival, thus providing a glimpse into the potential resilience of species in the face of anthropogenic disturbance. Investigating the behavioral ecology of Goodman’s mouse lemurs across their geographic range could help us understand their metabolic and ecological flexibility and predict species long-term survival prospects. We conducted night transect walks, using capture techniques and telemetry, to track eight radio-collared individuals. Preliminary density estimates based on a limited number of sightings (n = 18) were 2.19 ind/ha, and home range assessments ranged between 0.22 and 3.67 ha. Mouse lemurs traveled an average of 425 m nightly during the 5-h tracking periods and primarily fed on fruits of the mistletoe Bakerella clavata. The finding that Goodman’s mouse lemurs apparently thrive in the seasonally cold and arid forest fragments in the Central Highlands indicates that they may be among the most tolerant and adaptable lemur species in Madagascar. These results point towards an exciting research program that focuses on ecological tolerance as a mechanism for long-term species survival.
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Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:227–267
Andriambeloson J-B, Greene LK, Blanco MB (2020) Prolonged Torpor in Goodman’s Mouse Lemur (Microcebus lehilahytsara) from the high-altitude forest of Tsinjoarivo, Central-Eastern Madagascar. Folia Primatol 91:697–710. https://doi.org/10.1159/000509102
Andriatsitohaina B, Ramsay MS, Kiene F, Lehman SM, Rasoloharijaona S, Rakotondravony R, Radespiel U (2019) Ecological fragmentation effects in mouse lemurs and small mammals in northwestern Madagascar. Am J Primatol. https://doi.org/10.1002/ajp.23059
Andriatsitohaina B, Romero-Mujalli D, Ramsay MS et al (2020) Effects of habitat edges on vegetation structure and the vulnerable golden-brown mouse lemur (Microcebus ravelobensis) in northwestern Madagascar. BMC Ecol 20:69. https://doi.org/10.1186/s12898-020-00337-z
Arroyo-Rodríguez V, Cuesta-del Moral E, Mandujano S, Chapman CA, Reyna-Hurtado R, Fahrig L (2013) Assessing habitat fragmentation effects on primates: the importance of evaluating questions at the correct scale. In: Marsh LK, Chapman CA (eds) Primates in Fragments: Complexity and Resilience. Springer, New York, pp 13–28
Atsalis S (1999) Diet of the brown mouse lemur (Microcebus rufus) in Ranomafana National Park, Madagascar. Int J Primatol 20:193–229
Atsalis S (2008) A Natural History of the Brown Mouse Lemur. Pearson Prentice Hall, New Jersey
Benchimol M, Peres CA (2014) Predicting primate local extinctions within “real-world” forest fragments: a pan-neotropical analysis. Am J Primatol 76:289–302. https://doi.org/10.1002/ajp.22233
Blanco MB (2010) Reproductive biology of mouse and Dwarf Lemurs of Eastern Madagascar, with an emphasis on brown mouse Lemurs (Microcebus rufus) at Ranomafana National Park, a Southeastern Rainforest. Dissertation, University of Massachusetts, Amherst
Blanco MB, Godfrey LR (2014) Hibernation patterns of dwarf lemurs in the high altitude forest of eastern Madagascar. In: Gursky S, Krzton A, Grow N (eds) High altitude primates. Springer, New York, pp 23–42
Blanco MB, Andriantsalohimisantatra AA, Rivoharison TV, Andriambeloson J-B (2017) Evidence of prolonged torpor in Goodman’s mouse lemurs at Ankafobe forest, central Madagascar. Primates 1:1–7
Bohr YE-MB, Giertz P, Ratovonamana YR, Ganzhorn JU (2011) Gray-brown mouse lemurs (Microcebus griseorufus) as an example of distributional constraints through increasing desertification. Int J Primatol 32:901–913. https://doi.org/10.1007/s10764-011-9509-8
Bond W (2008) What limits trees in C4 grasslands and savannas? Annu Rev Ecol Evol S 39:641–659
Bond W, Silander J, Ranaivonasy J, Ratsirarson J (2008) The antiquity of Madagascar’s grasslands and the rise of C4 Grassy Biomes. J Biogeogr 35:1743–1758
Burney DA (1996) Climate change and fire ecology as factors in the Quaternary biogeography of Madagascar. In: Lourenco WR (ed) Biogéographie de Madagascar. ORSTOM, Paris, pp 49–58
Cornet A (1974). Essai de cartographie bioclimatique à Madagascar. Notice Explicative No. 55, ORSTOM, Paris.
Crowley BE, Blanco MB, Arrigo-Nelson SJ, Irwin MT (2013) Stable isotopes document resource partitioning and effects of forest disturbance on sympatric cheirogaleid lemurs. Naturwissenschaften 100:943–956. https://doi.org/10.1007/s00114-013-1094-6
Ganzhorn JU (1987) A possible role of plantations for primate conservation in Madagascar. Am J Primatol 12:205–215
Ganzhorn JU, Schmid J (1998) Different population dynamics of Microcebus murinus in primary and secondary deciduous dry forests of Madagascar. Int J Primatol 19:785–796
Ganzhorn JU, Kappeler PM (1996) Lemurs of the Kirindy Forest. Primate Report 46:257–274
Génin F, Rambeloarivony H (2018) Mouse lemurs (Primates: Cheirogaleidae) cultivate green fruit gardens. Biol J Linn Soc 124:607–620
Godfrey LR, Jungers WL, Schwartz GT, Irwin MT (2008) Ghosts and Orphans. Madagascar’s vanishing ecosystems. In: Fleagle JG, Gilbert CC (eds) Elwyn Simons: A search for origins Development in Primatology Progress and Prospects Series. Springer, New York, pp 361–395
Goodman SM, Jungers WL (2014) Extinct Madagascar: Picturing the Island’s Past. The University of Chicago Press, Chicago
Harcourt AH, Doherty DA (2005) Species-area relationships of primates in tropical forest fragments: a global analysis. J Appl Ecol 42:630–637
Harper G, Steininger MK, Tucker CJ, Juhn D, Hawkins F (2007) Fifty years of deforestation and forest fragmentation in Madagascar. Environ 34:325–333
Hending D, McCabe G, Holderied M (2017) Sleeping and ranging behavior of the Sambirano mouse lemur, Microcebus sambiranensis. Int J Primatol 38:1072–1089
Henke-von der Malsburg J, Fichtel C (2018) Are generalists more innovative than specialists? A comparison of innovative abilities in two wild sympatric mouse lemur species. R Soc Open Sci. https://doi.org/10.1098/rsos.180480
Humbert H (1927) La destruction d’une flore insulaire par le feu. Principaux aspects de la végétation à Madagascar. Mémoires Academie Malgache 5:1–78
Irwin MT (2008) Feeding ecology of Propithecus diadema in forest fragments and continuous forest. Int J Primatol 29:95–115
Jones JPG, Ratsimbazafy J, Ratsifandrihamanana AN, Watson JEM, Andrianandrasana HT, Cabeza M, Cinner JE, Goodman SM, Hawkins F, Mittermeier RA et al (2019) Last chance for Madagascar’s biodiversity. Nat Sustain 2:350–352
Karanewsky CJ, Wright PC (2015) A preliminary investigation of sleeping site selection and sharing by the brown mouse lemur Microcebus rufus during the dry season. J Mammal 96:1344–1351
Knoop S, Chikhi L, Salmona J (2018) Mouse lemurs’ use of degraded habitat: a review of the literature. Lemur News 21:21–31
Lowry PP, Schatz GE, Phillipson PP (1997) The classification of natural and anthropogenic vegetation in Madagascar. In: Goodman SM, Patterson BD (eds) Natural change and human impact in Madagascar. Smithsonian Institution Press, Washington DC
Marsh LK, Chapman CA (2013) Primates in Fragments Developments in Primatology: Progress and Prospects Series. Springer, New York
Marsh C, Link A, King-Bailey G, Donati G (2016) Effects of fragment and vegetation structure on the population abundance of Ateles hybridus, Alouatta seniculus and Cebus albifrons in Magdalena Valley, Colombia. Folia Primatol 87:17–30. https://doi.org/10.1159/000443929
Miandrimanana C, Reid JL, Rivoharison T, Birkinshaw C (2018) Planting position and shade enhance native seedling performance in forest restoration for an endangered Malagasy plant. Plant Divers 41:118–123
Morelli TL, Smith AB, Mancini AN, Balko EA, Borgerson C, Dolch R, Farris Z, Federman S, Golden CD et al (2020) The fate of Madagascar’s rainforest habitat. Nat Clim Change 10:89–96. https://doi.org/10.1038/s41558-019-0647-x
Mullin KE, Rakotomanga MG, Razafiarimanana MLC, Barata IM, Dawson J, Hailer F, Orozco-terWengel P (2021) First amphibian inventory of one of Madagascar’s smallest protected areas, Ankafobe, extends the range of the Critically Endangered Anilany helenae (Vallan, 2000) and the Endangered Boophis andrangoloaka (Ahl, 1928). Herpetol Notes 14:521–531
Nowak K, Lee PC (2013) “Specialist” primates can be flexible in response to habitat alteration. In: Marsh LK, Chapman CA (eds) Primates in Fragments: Complexity and Resilience. Springer, New York, pp 199–212
Perrier de la Bâthie H (1936) Biogéographie de plantes de Madagascar. Société d’Edition Géographiques, Maritimes et Coloniales, Paris
Poelstra J, Salmona J, Tiley G et al (2020) Cryptic patterns of speciation in cryptic primates: microendemic mouse lemurs and the multispecies coalescent. Syst Biol 70:203–218. https://doi.org/10.1093/sysbio/syaa053
Radespiel U (2006) Ecological Diversity and Seasonal Adaptations of Mouse Lemurs (Microcebus spp.). In: Gould L, Sauther ML (eds) Lemurs Developments in Primatology: Progress and Prospect. Springer, Boston
Radespiel U, Ehresmann P, Zimmermann E (2003) Species-specific usage of sleeping sites in two sympatric mouse lemur species (Microcebus murinus and M. ravelobensis) in northwestern Madagascar. Am J Primatol 59:139–151. https://doi.org/10.1002/ajp.10071 (PMID: 12682922)
Radespiel U, Ratsimbazafy JH, Rasoloharijaona S, Raveloson H, Andriaholinirina N, Rakotondranvony R, Randrianarison RM, Randrianambinina B (2012) First indications of a highland specialist among mouse lemurs (Microcebus spp.) and evidence for a new mouse lemur species from eastern Madagascar. Primates 53:57–170
Ramananjato V, Rakotomalala Z, Park DS, DeSisto CM, Raoelinjanakolona NN, Guthrie NK, Fenosoa ZE, Jonhson SE, Razafindratsima O (2020) The role of nocturnal omnivorous lemurs as seed dispersers in Malagasy rain forests. Biotropica 52:758–765
Razafindratsima OH, Brown KA, Carvalho F, Johnson SE, Wright PC, Dunham AE (2018) Edge effects on components of diversity and above-ground biomass in a tropical rainforest. J Appl Ecol 55:977–985. https://doi.org/10.1111/1365-2664.12985
Schülke O, Ostner J (2007) Physiological ecology of cheirogaleid primates: a variation in hibernation and torpor. Acta Ethol 10:13–21
Schüßler D, Blanco MB, Salmona J, Poelstra J, Andriambeloson J-B, Miller A, Randrianambinina B, Rasolofoson DW, Mantilla-Contreras J, Chikhi L, Louis EE, Yoder AD, Radespiel U (2020) Ecology and morphology of mouse lemurs (Microcebus spp.) in a hotspot of microendemism in northeastern Madagascar with the description of a new species. Am J Primatol 82:e23180. https://doi.org/10.1002/ajp.23180
Setash CM, Zohdy S, Gerber BD, Karanewsky CJ (2017) A biogeographical perspective on the variation in mouse lemur density throughout Madagascar. Mammal Rev 47:212–229. https://doi.org/10.1111/mam.12093
Shaw DC, Watson DM, Mathiasen RL (2004) Comparison of dwarf mistletoes (Arceuthobium spp., Viscaceae) in the western United States with mistletoes (Amyema spp., Loranthaceae) in Australia ecological analogs and reciprocal models for ecosystem management. Aust J Bot 52:381–498. https://doi.org/10.1071/BT03074
Steffens TS, Lehman SM (2018) Lemur species-specific metapopulation responses to habitat loss and fragmentation. PLoS One. https://doi.org/10.1371/journal.pone.0195791
Tiley G, Blanco MB, Ralison J, Rasoloarison R, Stahlke A, Hohenlohe P, Yoder AD (2020) Population genomic structure in Goodman’s mouse lemur reveals long-standing separation of Madagascar’s Central Highlands and eastern rainforests. bioRxiv. https://doi.org/10.1101/2020.01.30.923300
Vitali A, Sasal Y, Vázquez D, Rodriguez-Cabal M (2020) The disruption of a keystone interaction erodes pollination and seed dispersal networks. Authorea. https://doi.org/10.22541/au.159493097.78173255
Vorontsova MS, Besnard G, Forest F, Malakasi P, Morat K, Clayton WD, Ficinski P, Savva GM, Nanjarisoa OP, Razanatsoa J, Randriatsara FO, Kimeu JM, Luke WRK, Kayombo C, Linder HP (2016) Madagascar’s grasses and grasslands: anthropogenic or natural? Proc R Soc Lond B 283:20152226
Watson D, Herring M (2012) Mistletoe as a keystone resource: an experimental test. Proc R Soc Lond B 279:3853–3860. https://doi.org/10.1098/rspb.2012.0856
Yoder AD, Campbell CR, Blanco MB, dos Reis M, Ganzhorn JU, Goodman SM, Hunnicutt KE, Larsen PA, Kappeler PM, Rasoloarison RM, Ralison JM, Swofford D, Weisrock DW (2016) Geogenetic patterns in mouse lemurs (genus Microcebus) reveal the ghosts of Madagascar’s forest past. Proc Natl Acad Sci USA 113:8049–8056
We thank the Government of Madagascar for authorizing us to conduct research at Ankafobe. We are indebted to Madame Beatrice, P. Rafanomezantsoa, A. Bendrainy, L. H. Ramerina, and T. Ralainaorina for their assistance in the field. Financial support was partly provided by the Duke Tropical Conservation Initiative Seed Grant to J.J. Swenson and A.D. Yoder, and Primate Action Fund to M.B. Blanco. This is Duke Lemur Center publication # 1490.
Conflict of interest
The authors declare no conflict of interest.
Our research adhered to the legal requirements of the Government of Madagascar, under Research Permit N°225/15/MEEF/SG/DGF/DAPT/SCBT, reissued by the Ministry of Environment, Ecology and Forests (current MEDD), and our research protocols complied with the Duke Institutional Animal Care and Use Committee (IACUC) under protocol A263-17–12. In addition, prior to beginning research, we informed local state representatives (Ankazobe) of the proposed work and asked them to validate our research permit, and also informed local communities through VOI-Sohisika so as to avoid misunderstandings concerning our work at this site.
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Andriambeloson, JB., Blanco, M.B., Andriantsalohimisantatra, A. et al. Living in tiny fragments: a glimpse at the ecology of Goodman’s mouse lemurs (Microcebus lehilahytsara) in the relic forest of Ankafobe, Central Highlands, Madagascar. Primates (2021). https://doi.org/10.1007/s10329-021-00947-1
- Ecological flexibility
- Radio collar