Madagascar has experienced extensive deforestation and overharvesting, and anthropogenic climate change will compound these pressures. Anticipating these threats to endangered species and their ecosystems requires considering both climate change and habitat loss effects. The genus Varecia (ruffed lemurs), which is composed of two Critically Endangered forest-obligate species, can serve as a status indicator of the biodiverse eastern rainforest of Madagascar. Here, we combined decades of research to show that the suitable habitat for ruffed lemurs could be reduced by 29–59% from deforestation, 14–75% from climate change (representative concentration pathway 8.5) or 38–93% from both by 2070. If current protected areas avoid further deforestation, climate change will still reduce the suitable habitat by 62% (range: 38–83%). If ongoing deforestation continues, the suitable habitat will decline by 81% (range: 66–93%). Maintaining and enhancing the integrity of protected areas, where rates of forest loss are lower, will be essential for ensuring persistence of the diversity of the rapidly diminishing Malagasy rainforests.
Subscribe to Journal
Get full journal access for 1 year
only $17.42 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
All code required to reproduce the results is available at https://github.com/adamlilith/varecia.
Barnosky, A. D. et al. Has the Earth’s sixth mass extinction already arrived? Nature 471, 51–57 (2011).
Wilcove, D. S., Rothstein, D., Dubow, J., Phillips, A. & Losos, E. Quantifying threats to imperiled species in the United States. Bioscience 48, 607–615 (1998).
Hernández-Yáñez, H. et al. A systematic assessment of threats affecting the rare plants of the United States. Biol. Conserv. 203, 260–267 (2016).
Gonzalez, P., Wang, F., Notaro, M., Vimont, D. J. & Williams, J. W. Disproportionate magnitude of climate change in United States national parks. Environ. Res. Lett. 13, 104001 (2018).
Pacifici, M. et al. Species’ traits influenced their response to recent climate change. Nat. Clim. Change 7, 205–208 (2017).
Tingley, M. W., Estes, L. D. & Wilcove, D. S. Climate change must not blow conservation off course. Nature 500, 271–272 (2013).
Brown, K. A., Parks, K. E., Bethell, C. A., Johnson, S. E. & Mulligan, M. Predicting plant diversity patterns in Madagascar: understanding the effects of climate and land cover change in a biodiversity hotspot. PLoS ONE 10, e0122721 (2015).
Ganzhorn, J. U., Lowry, P. P., Schatz, G. E. & Sommer, S. The biodiversity of Madagascar: one of the world’s hottest hotspots on its way out. Oryx 35, 346–348 (2001).
Dunham, A. E., Erhart, E. M., Overdorff, D. J. & Wright, P. C. Evaluating effects of deforestation, hunting, and El Niño events on a threatened lemur. Biol. Conserv. 141, 287–297 (2008).
Dunham, A. E., Erhart, E. M. & Wright, P. C. Global climate cycles and cyclones: consequences for rainfall patterns and lemur reproduction in southeastern Madagascar. Glob. Change Biol. 17, 219–227 (2011).
Brown, K. A. & Gurevitch, J. Long-term impacts of logging on forest diversity in Madagascar. Proc. Natl Acad. Sci. USA 101, 6045–6049 (2004).
Park, D. S. & Razafindratsima, O. H. Anthropogenic threats can have cascading homogenizing effects on the phylogenetic and functional diversity of tropical ecosystems. Ecography 42, 148–161 (2019).
O’Brien, S. et al. Decline of the Madagascar radiated tortoise Geochelone radiata due to overexploitation. Oryx 37, 338–343 (2003).
Barrett, M. A. & Ratsimbazafy, J. Luxury bushmeat trade threatens lemur conservation. Nature 461, 470 (2009).
Borgerson, C., McKean, M. A., Sutherland, M. R. & Godfrey, L. R. Who hunts lemurs and why they hunt them. Biol. Conserv. 197, 124–130 (2016).
Brook, C. E. et al. Population viability and harvest sustainability for Madagascar lemurs. Conserv. Biol. 33, 99–111 (2019).
Watson, J. E. M., Whittaker, R. J. & Dawson, T. P. Avifaunal responses to habitat fragmentation in the threatened littoral forests of south-eastern Madagascar. J. Biogeogr. 31, 1791–1807 (2004).
Harper, G. J., Steininger, M. K., Tucker, C. J., Juhn, D. & Hawkins, F. Fifty years of deforestation and forest fragmentation in Madagascar. Environ. Conserv. 34, 325–333 (2007).
Razafindratsima, O. H. et al. Edge effects on components of diversity and above-ground biomass in a tropical rainforest. J. Appl. Ecol. 55, 977–985 (2018).
Vieilledent, G. et al. Combining global tree cover loss data with historical national forest cover maps to look at six decades of deforestation and forest fragmentation in Madagascar. Biol. Conserv. 222, 189–197 (2018).
Kremen, C. et al. Aligning conservation priorities across taxa in Madagascar with high-resolution planning tools. Science 320, 222–226 (2008).
Hannah, L. Protected areas and climate change. Ann. NY Acad. Sci. 1134, 201–212 (2008).
Fisher, B. L. & Girman, D. J. in Diversite et Endemism a Madagascar (eds Lourenco, W. R. & Goodman, S. M.) 331–344 (Société de Biogéographie, 2000).
Greene, B. T., Lowe, W. H. & Likens, G. E. Forest succession and prey availability influence the strength and scale of terrestrial–aquatic linkages in a headwater salamander system. Freshw. Biol. 53, 2234–2243 (2008).
Vieites, D. R. et al. Vast underestimation of Madagascar’s biodiversity evidenced by an integrative amphibian inventory. Proc. Natl Acad. Sci. USA 106, 8267–8272 (2009).
The IUCN Red List of Threatened Species (IUCN, 2018).
Jenkins, R. K. B. et al. Analysis of patterns of bushmeat consumption reveals extensive exploitation of protected species in eastern Madagascar. PLoS ONE 6, e27570 (2011).
Balko, E. A. & Underwood, H. B. Effects of forest structure and composition on food availability for Varecia variegata at Ranomafana National Park, Madagascar. Am. J. Primatol. 66, 45–70 (2005).
Borgerson, C. The effects of illegal hunting and habitat on two sympatric endangered primates. Int. J. Primatol. 36, 74–93 (2015).
White, F. J., Overdorff, D. J., Balko, E. A. & Wright, P. C. Distribution of ruffed lemurs (Varecia variegata) in Ranomafana National Park, Madagascar. Folia Primatol. 64, 124–131 (1995).
Baden, A. L. et al. Anthropogenic pressures explain population genetic structure in a critically endangered moist forest specialist, Varecia variegata. Sci. Rep. 9, 16276 (2019).
Baden, A. L. et al. Species-level view of population structure and gene flow for a critically endangered primate (Varecia variegata). Ecol. Evol. 4, 2675–2692 (2014).
Lehtinen, R. M., Ramanamanjato, J.-B. & Raveloarison, J. G. Edge effects and extinction proneness in a herpetofauna from Madagascar. Biodivers. Conserv. 12, 1357–1370 (2003).
Farris, Z. J. et al. Threats to a rainforest carnivore community: a multi-year assessment of occupancy and co-occurrence in Madagascar. Biol. Conserv. 210, 116–124 (2017).
Federman, S. et al. The paucity of frugivores in Madagascar may not be due to unpredictable temperatures or fruit resources. PLoS ONE 12, e0168943 (2017).
Dunham, A. E., Razafindratsima, A. E., Rakotonirina, O. H. & Wright, P. C. Fruiting phenology is linked to rainfall variability in a tropical rain forest. Biotropica 50, 396–404 (2018).
Dew, J. L. & Wright, P. Frugivory and seed dispersal by four species of primates in Madagascar’s eastern rain forest. Biotropica 30, 425–437 (1998).
Moses, K. L. & Semple, S. Primary seed dispersal by the black-and-white ruffed lemur (Varecia variegata) in the Manombo forest, south-east Madagascar. J. Trop. Ecol. 27, 529–538 (2011).
Razafindratsima, O. H. & Martinez, B. T. Seed dispersal by red-ruffed lemurs: seed size, viability and beneficial effect on seedling growth. Ecotropica 18, 15–26 (2012).
Martinez, B. T. & Razafindratsima, O. H. Frugivory and seed dispersal patterns of the red-ruffed lemur, Varecia rubra, at a forest restoration site in Masoala National Park, Madagascar. Folia Primatol. 85, 228–243 (2014).
Razafindratsima, O. H., Jones, T. A. & Dunham, A. E. Patterns of movement and seed dispersal by three lemur species. Am. J. Primatol. 76, 84–96 (2014).
Razafindratsima, O. H. & Dunham, A. E. Frugivores bias seed–adult tree associations through nonrandom seed dispersal: a phylogenetic approach. Ecology 97, 2094–2102 (2016).
Razafindratsima, O. H. & Dunham, A. E. Assessing the impacts of nonrandom seed dispersal by multiple frugivore partners on plant recruitment. Ecology 96, 24–30 (2015).
Frey, J. K. Variation in phenology of hibernation and reproduction in the endangered New Mexico meadow jumping mouse (Zapus hudsonius luteus). PeerJ 3, e1138 (2015).
IPCC Climate Change 2014: Synthesis Report (eds Core Writing Team, Pachauri, R. K. & Meyer, L. A.) (IPCC, 2014).
Dawe, K. L. & Boutin, S. Climate change is the primary driver of white-tailed deer (Odocoileus virginianus) range expansion at the northern extent of its range; land use is secondary. Ecol. Evol. 6, 6435–6451 (2016).
Wright, P. C. et al. Frugivory in four sympatric lemurs: implications for the future of Madagascar’s forests. Am. J. Primatol. 73, 585–602 (2011).
Federman, S. et al. Implications of lemuriform extinctions for the Malagasy flora. Proc. Natl Acad. Sci. USA 113, 5041–5046 (2016).
Vieilledent, G., Grinand, C. & Vaudry, R. Forecasting deforestation and carbon emissions in tropical developing countries facing demographic expansion: a case study in Madagascar. Ecol. Evol. 3, 1702–1716 (2013).
Kull, C. A. et al. The introduced flora of Madagascar. Biol. Invasions 14, 875–888 (2012).
Marsh, L. K. & Chapman, C. Primates in Fragments: Complexity and Resilience (Springer, 2013).
Costanza, J. K. & Terando, A. J. Landscape connectivity planning for adaptation to future climate and land-use change. Curr. Landsc. Ecol. Rep. 4, 1–13 (2019).
Harvey, C. A. et al. Extreme vulnerability of smallholder farmers to agricultural risks and climate change in Madagascar. Phil. Trans. R. Soc. Lond. B 369, 20130089 (2014).
Golden, C. D., Gupta, A. C., Vaitla, B. & Myers, S. S. Ecosystem services and food security: assessing inequality at community, household and individual scales. Environ. Conserv. 43, 381–388 (2016).
Molotoks, A. et al. Global hotspots of conflict risk between food security and biodiversity conservation. Land 6, 67 (2017).
Jones, J. Madagascar: fear and violence making rainforest conservation more challenging than ever. The Conversation http://theconversation.com/madagascar-fear-and-violence-making-rainforest-conservation-more-challenging-than-ever-108142 (2018).
Borgerson, C. et al. The use of natural resources to improve household income, health, and nutrition within the forests of Kianjavato, Madagascar. Madagascar Conserv. Dev. 13, 45–52 (2018).
Golden, C. D. et al. Economic valuation of subsistence harvest of wildlife in Madagascar. Conserv. Biol. 28, 234–243 (2014).
Borgerson, C. Optimizing conservation policy: the importance of seasonal variation in hunting and meat consumption on the Masoala Peninsula of Madagascar. Oryx 50, 405–418 (2016).
Farris, Z. J. et al. Hunting, exotic carnivores, and habitat loss: anthropogenic effects on a native carnivore community, Madagascar. PLoS ONE 10, e0136456 (2015).
Poulsen, J. R., Clark, C. J. & Bolker, B. M. Decoupling the effects of logging and hunting on an Afrotropical animal community. Ecol. Appl. 21, 1819–1836 (2011).
Qiao, H., Escobar, L. E. & Peterson, A. T. Accessible areas in ecological niche comparisons of invasive species: recognized but still overlooked. Sci. Rep. 7, 1213 (2017).
Lehikoinen, A. et al. Declining population trends of European mountain birds. Glob. Change Biol. 25, 577–588 (2019).
Thorne, J. H. et al. Alternative biological assumptions strongly influence models of climate change effects on mountain gorillas. Ecosphere 4, 108 (2013).
Smith, A. B., Godsoe, W., Rodríguez-Sánchez, F., Wang, H.-H. & Warren, D. Niche estimation above and below the species level. Trends Ecol. Evol. 34, 260–273 (2019).
Brown, J. L. et al. Spatial biodiversity patterns of Madagascar’s amphibians and reptiles. PLoS ONE 11, e0144076 (2016).
Goodman, S. M. & Benstead, J. P. Updated estimates of biotic diversity and endemism for Madagascar. Oryx 39, 73–77 (2005).
Global Assessment Report on Biodiversity and Ecosystem Services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES Secretariat, 2019).
Hoegh-Guldberg, O. et al. in Special Report on Global Warming of 1.5 °C (eds Masson-Delmotte, V. et al.) Ch. 3 (IPCC, WMO, 2018).
Muldoon, K. M. & Goodman, S. M. Primates as predictors of mammal community diversity in the forest ecosystems of Madagascar. PLoS ONE 10, e0136787 (2015).
Bruner, A. G., Gullison, R. E., Rice, R. E. & da Fonseca, G. A. B. Effectiveness of parks in protecting tropical biodiversity. Science 291, 125–128 (2001).
Morelli, T. L. et al. Managing climate change refugia for climate adaptation. PLoS ONE 11, e0159909 (2016).
Tollefson, J. Fate of Madagascar’s forests in the hands of incoming president. Nature 565, 407 (2019).
Raftery, A. E., Chunn, J. L., Gerland, P. & Sevčíková, H. Bayesian probabilistic projections of life expectancy for all countries. Demography 50, 777–801 (2013).
World Population Prospects 2017 (United Nations, 2017).
Riitters, K., Wickham, J., O’Neill, R., Jones, B. & Smith, E. Global-scale patterns of forest fragmentation. Conserv. Ecol. 4, 3 (2000).
Baden, A. L., Brenneman, R. A. & Louis, E. E. Jr Morphometrics of wild black-and-white ruffed lemurs (Varecia variegata; Kerr, 1792). Am. J. Primatol. 70, 913–926 (2008).
Balko, E. A. A Behaviorally Plastic Response to Forest Composition and Logging Disturbance by Varecia variegata variegata in Ranomafana National Park, Madagascar (State Univ. New York, 1998).
Vasey, N. & Tattersal, I. Do ruffed lemurs form a hybrid zone? Distribution and discovery of Varecia, with systematic and conservation implications. Am. Museum Novit. 26, 1–26 (2002).
Irwin, M. T., Johnson, S. E. & Wright, P. C. The state of lemur conservation in south-eastern Madagascar: population and habitat assessments for diurnal and cathemeral lemurs using surveys, satellite imagery and GIS. Oryx 39, 204–218 (2005).
Mittermeier, R. A. et al. Lemurs of Madagascar (Conservation International, 2010).
Fick, S. E. & Hijmans, R. J. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37, 4302–4315 (2017).
Buckland, S. T. et al. Advanced Distance Sampling Vol. 2 (Oxford Univ. Press, 2004).
Buckland, S. T. et al. Introduction to Distance Sampling: Estimating Abundance of Biological Populations (Oxford Univ. Press, 2001).
Sterling, E. & Ramaroson, M. G. Rapid assessment of the primate fauna of the eastern slopes of the Réserve Naturelle Intégrale d’Andringitra, Madagascar. Field. Zool. 85, 293–305 (1996).
Williams, B., Nichols, J. D. & Conroy, M. J. Analysis and Management of Animal Populations (Academic, 2002).
Borchers, D. L. & Marques, T. A. From distance sampling to spatial capture–recapture. Adv. Stat. Anal. 101, 475–494 (2017).
Altmann, J. Observational study of behavior: sampling methods. Behaviour 49, 227–267 (1974).
Karger, D. N. et al. Climatologies at high resolution for the Earth’s land surface areas. Sci. Data 4, 170122 (2017).
Anderson, R. P. & Raza, A. The effect of the extent of the study region on GIS models of species geographic distributions and estimates of niche evolution: preliminary tests with montane rodents (genus Nephelomys) in Venezuela. J. Biogeogr. 37, 1378–1393 (2010).
Guevara, L., Gerstner, B. E., Kass, J. M. & Anderson, R. P. Toward ecologically realistic predictions of species distributions: a cross-time example from tropical montane cloud forests. Glob. Change Biol. 24, 1511–1522 (2018).
Stolar, J. & Nielsen, S. E. Accounting for spatially biased sampling effort in presence-only species distribution modelling. Divers. Distrib. 21, 595–608 (2015).
Boria, R. A., Olson, L. E., Goodman, S. M. & Anderson, R. P. Spatial filtering to reduce sampling bias can improve the performance of ecological niche models. Ecol. Model. 275, 73–77 (2014).
Hirzel, A. H., Le Lay, G., Helfer, V., Randin, C. & Guisan, A. Evaluating the ability of habitat suitability models to predict species presences. Ecol. Model. 199, 142–152 (2006).
Boyce, M. S., Vernier, P. R., Nielsen, S. E. & Schmiegelow, F. K. A. Evaluating resource selection functions. Ecol. Model. 157, 281–300 (2002).
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).
Warren, D. L., Glor, R. E. & Turelli, M. Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62, 2868–2883 (2008).
Broennimann, O. et al. Measuring ecological niche overlap from occurrence and spatial environmental data. Glob. Ecol. Biogeogr. 21, 481–497 (2012).
Nunes, L. A. & Pearson, R. G. A null biogeographical test for assessing ecological niche evolution. J. Biogeogr. 44, 1331–1343 (2017).
Smith, A. B. enmSdm: tools for modeling niches and distributions of species. R package version 0.3.1.0. (2018).
Hijmans, R. J., Phillips, S., Leathwick, J. & Elith, J. dismo: species distribution modeling. R package version 1.1-4. (2017).
Hijmans, R. J. raster: geographic data analysis and modeling. R package version 3.0-7. (2017).
Hijmans, R. J. geosphere: spherical trigonometry. R package version 1.5-10. (2017).
Bivand, R. & Rundel, C. rgeos: interface to geometry engine - open source (‘GEOS’). R package version 0.5-1. (2017).
R Core Team R: A Language and Environment for Statistical Computing (R Foundation, 2013).
Smith, A. B. fasterRaster: faster raster processing in R using GRASS GIS. R package version 0.4.1. (2018).
Neteler, M., Bowman, M. H., Landa, M. & Metz, M. GRASS GIS: a multi-purpose open source GIS 2012. Environ. Model. Softw. 31, 124–130 (2012).
We thank the Ministry of the Environment and Sustainable Development of the Government of Madagascar for issuing the numerous research permits to undertake the field surveys underpinning this study and for sharing protected area data. We also thank the University of Antananarivo, MICET/CVB/ICTE and GERP for facilitating the application process for several of these permits and for logistical support. We thank the many conservationists, researchers and research assistants from around Madagascar, without whom data collection would have been impossible, and we are grateful to the following for funding: Alan Graham Fund in Global Change; Animal Behavior Society; American Society of Primatology; The Aspinall Foundation; Beauval Nature; CERZA Conservation; Cleveland Metroparks Zoo; Douroucouli Foundation; Edna Bailey Susan Fund; European Association for Zoos and Aquariums; The Explorers Club; Hunter College of the City University of New York; Idea Wild; International Foundation for Science; IUCN ‘SOS - Save Our Species’; J. William Fulbright Foundation; Mohamed bin Zayed Species Conservation Fund; National Geographic Society Conservation Trust (C280–14, C021–17), Waitts grant (no. W96-10); National Science Foundation DDIG (BSC-0725975), SBE-IBSS PRF (1513638); The Natural Sciences and Engineering Research Council of Canada; Peoples Trust for Endangered Species; Primate Action Fund; Primate Conservation, Inc.; Primate Society of Great Britain; PSC-CUNY; The Rufford Foundation; Saint Louis Zoo’s WildCare Institute; Schlumberger Foundation; Sophie Danforth Conservation Fund; Stony Brook University; Wilford A. Dence Memorial Fellowship for Wildlife Science. The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of the U.S. Fish and Wildlife Service.
The authors declare no competing interests.
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary methods, results, Tables 1, 2 and 4 and Figs. 1–7.
Change in suitability by protected area.
Mean predicted suitability by scenario and elevational band.
Sampling for Varecia.
Animation illustrating forest loss between 2015 and 2080 under relaxed (left) and strict (right) forest protection scenarios.
About this article
Cite this article
Morelli, T.L., Smith, A.B., Mancini, A.N. et al. The fate of Madagascar’s rainforest habitat. Nat. Clim. Chang. 10, 89–96 (2020). https://doi.org/10.1038/s41558-019-0647-x
Assessment of the threatened carnivore community in the recently expanded rainforest protected area Anjanaharibe-Sud Special Reserve, Madagascar
Endangered Species Research (2020)
Genetic population structure of endangered ring‐tailed lemurs ( Lemur catta ) from nine sites in southern Madagascar
Ecology and Evolution (2020)
Restoration Ecology (2020)
Climatic Change (2020)
Study Protocol: A Cross-Sectional Examination of Socio-Demographic and Ecological Determinants of Nutrition and Disease Across Madagascar
Frontiers in Public Health (2020)