Abstract
Several factors can influence primate distributions, including evolutionary history, interspecific competition, climate, and anthropogenic impacts. In Madagascar, several small spatial scale studies have shown that anthropogenic habitat modification affects the density and distribution of many lemur species. Ecological niche models can be used to examine broad-scale influences of anthropogenic impacts on primate distributions. In this study, we examine how climate and anthropogenic factors influence the distribution of 11 Eulemur species using ecological niche models. Specifically, we created one set of models only using rainfall and temperature variables. We then created a second set of models that combined these climate variables with three anthropogenic factors: distance to dense settlements, villages, and croplands. We used MaxEnt to generate all the models. We found that the addition of anthropogenic variables improved the climate models. Also, most Eulemur species exhibited reduced predicted geographic distributions once anthropogenic factors were added to the model. Distance to dense settlements was the most important anthropogenic factor in most cases. We suggest that including anthropogenic variables in ecological niche models is important for understanding primate distributions, especially in regions with significant human impacts. In addition, we identify several Eulemur species that were most affected by anthropogenic factors and should be the focus of increased conservation efforts.
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Anderson, R. P., Gomez-Laverde, M., & Peterson, A. T. (2002). Geographical distributions of spiny pocket mice in South America: Insights from predictive models. Global Ecology and Biogeography, 11, 131–141.
Ayres, J. M., & Clutton-Brock, T. H. (1992). River boundaries and species range size in Amazonian primates. American Naturalist, 140(3), 531–537.
Balestri, M., Barresi, M., Campera, M., Serra, V., Ramanamanjato, J., Heistermann, M., & Donati, G. (2014). Habitat degradation and seasonality affect physiological stress levels of Eulemur collaris in littoral forest fragments. PLoS ONE, 9, e107698.
Blair, M. E., Sterling, E. J., Dusch, M., Raxworthy, C. J., & Pearson, R. G. (2013). Ecological divergence and speciation between lemur (Eulemur) sister species in Madagascar. Journal of Evolutionary Biology, 26, 1790–1801.
Boulangeat, I., Gravel, D., & Thuiller, W. (2012). Accounting for dispersal and biotic interactions to disentangle the drivers of species distributions and their abundances. Ecology Letters, 15, 584–593.
Brenneman, R. A., Johnson, S. E., Bailey, C. A., Ingraldi, C., Delmore, K. E., Wyman, T. M., Andriamaharoa, H. E., Ralainasolo, F. B., Ratsimbazafy, J. H., & Louis, E. E. (2012). Population genetics and abundance of the endangered grey-headed lemur Eulemur cinereiceps in south-east Madagascar: Assessing risks for fragmented and continuous populations. Oryx, 46, 298–307.
Brown, J. L., & Yoder, A. D. (2015). Shifting ranges and conservation challenges for lemurs in the face of climate change. Ecology and Evolution. doi:10.1002/ece1003.1418.
Bublitz, D. C., Wright, P. C., Rasambainarivo, F. T., Arrigo‐Nelson, S. J., Bodager, J. R., & Gillespie, T. R. (2015). Pathogenic enterobacteria in lemurs associated with anthropogenic disturbance. American Journal of Primatology, 77(3), 330–337.
Burney, D. A., & Flannery, T. F. (2005). Fifty millennia of catastrophic extinctions after human contact. Trends in Ecology & Evolution, 20, 395–401.
Burney, D. A., & MacPhee, R. D. E. (1988). Mysterious island: What killed Madagascar’s large native animals? Natural History, 97, 46–55.
Crowley, B. E. (2010). A refined chronology of prehistoric Madagascar and the demise of the megafauna. Quaternary Science Reviews, 29, 2591–2603.
Curtis, D. J., & Rasmussen, M. A. (2006). The evolution of cathemerality in primates and other mammals: a comparative and chronoecological approach. Folia Primatologica, 77(1–2), 178–193.
Curtis, D., Zaramody, A., & Martin, R. (1999). Cathemerality in the mongoose lemur, Eulemur mongoz. American Journal of Primatology, 47(4), 279–298.
Dagosto, M., & Yamashita, N. (1998). Effect of habitat structure on positional behavior and support use in three species of lemur. Primates, 39, 459–472.
Dewar, R. E., & Richard, A. F. (2007). Evolution in the hypervariable environment of Madagascar. Proceedings of the National Academy of Sciences of the USA, 104, 13723–13727.
Donati, G., Bollen, A., Borgognini-Tarli, S. M., & Ganzhorn, J. U. (2007). Feeding over the 24-h cycle: Dietary flexibility of cathemeral collared lemurs (Eulemur collaris). Behavioral Ecology and Sociobiology, 61, 1237–1251.
Elith, J., Graham, C. H., Anderson, R. P., Dudık, M., Ferrier, S., Guisan, A., et al. (2006). Novel methods improve prediction of species’ distributions from occurrence data. Ecography, 29, 129–151.
Ellis, E. C., Goldewijk, K. K., Siebert, S., Lightman, D., & Ramankutty, N. (2010). Anthropogenic transformation of the biomes, 1700 to 2000. Global Ecology and Biogeography, 19, 589–606.
Ellis, E. C., Goldewijk, K. K., Siebert, S., Lightman, D., & Ramankutty, N. (2013). Anthropogenic biomes of the world, Version 2: 2000. 10.7927/H4D798B9 (Accessed November 12, 2014).
Farris, Z. J., Karpanty, S. M., Ratelolahy, F., & Kelly, M. J. (2014). Predator–primate distribution, activity, and co-occurrence in relation to habitat and human activity across fragmented and contiguous forests in northeastern Madagascar. International Journal of Primatology, 35, 859–880.
Frank, S. A. (2009). The common patterns of nature. Journal of Evolutionary Biology, 22, 1563–1585.
Ganzhorn, J. U. (1997). Test of Fox's assembly rule for functional groups in lemur communities in Madagascar. Journal of Zoology (London), 241, 533–542.
García, G., & Goodman, S. M. (2003). Hunting of protected animals in the Parc National d'Ankarafantsika, north-western Madagascar. Oryx, 37, 115–118.
Golden, C. D. (2009). Bushmeat hunting and use in the Makira Forest, north-eastern Madagascar: A conservation and livelihoods issue. Oryx, 43, 386–392.
Golden, C. D., Fernald, L. C., Brashares, J. S., Rasolofoniaina, B. R., & Kremen, C. (2011). Benefits of wildlife consumption to child nutrition in a biodiversity hotspot. Proceedings of the National Academy of Sciences of the USA, 108, 19653–19656.
Goodman, S. M., & Benstead, J. P. (2005). Updated estimates of biotic diversity and endemism in Madagascar. Oryx, 39, 73–77.
Goodman, S. M., & Ganzhorn, J. U. (2004). Biogeography of lemurs in the humid forests of Madagascar: The role of elevational distribution and rivers. Journal of Biogeography, 31, 47–55.
Gore, M. L., Ratsimbazafy, J., & Lute, M. L. (2013). Rethinking corruption in conservation crime: Insights from Madagascar. Conservation Letters, 6, 430–438.
Grassi, C. (2001). The behavioral ecology of Hapalemur griseus griseus: The influences of microhabitat and population density on this small-bodied prosimian folivore. Dissertation, University of Texas at Austin.
Harcourt, A. H., & Parks, S. A. (2003). Threatened primates experience high human densities: Adding an index of threat to the IUCN Red List criteria. Biological Conservation, 109(1), 137–149.
Harcourt, A. H., & Wood, M. A. (2012). Rivers as barriers to primate distributions in Africa. International Journal of Primatology, 33, 168–183.
Harper, G. J., Steininger, M. K., Tucker, C. J., Juhn, D., & Hawkins, F. (2007). Fifty years of deforestation and forest fragmentation in Madagascar. Environmental Conservation, 34, 325–333.
Harte, J., Zillio, T., Conlisk, E., & Smith, A. B. (2008). Maximum entropy and the state-variable approach to macroecology. Ecology and Evolution, 89, 2700–2711.
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965–1978.
Horning, N. R. (2012). Debunking three myths about Madagascar’s deforestation. Madagascar Conservation & Development, 7, 116–119.
Hosmer, D. W., & Lemeshow, S. (2000). Applied logistic regression (2nd ed.). New York: John Wiley & Sons.
Irwin, M. T. (2006). Ecological impacts of forest fragmentation on diademed sifakas (Propithecus diadema) at Tsinjoarivo, eastern Madagascar: Implications for conservation in fragmented landscape. Dissertation, Stony Brook University.
Irwin, M. T., Wright, P. C., Birkinshaw, C., Fisher, B. L., Gardner, C. J., Glos, J., Goodman, S. M., Loiselle, P., Rabeson, P., Raharison, J.-L., Raherilalao, M. J., Rakotondravony, D., Raselimanana, A., Ratsimbazafy, J., Sparks, J. S., Wilmé, L., & Ganzhorn, J. U. (2010). Patterns of species change in anthropogenically disturbed forests of Madagascar. Biological Conservation, 143, 2351–2362.
Jenkins, R. K., Keane, A., Rakotoarivelo, A. R., Rakotomboavonjy, V., Randrianandrianina, F. H., Razafimanahaka, H. J., Ralaiarimalala, S. R., & Jones, J. P. (2011). Analysis of patterns of bushmeat consumption reveals extensive exploitation of protected species in eastern Madagascar. PLoS One, 6, e27570.
Jiménez-Valverde, A., & Lobo, J. M. (2007). Threshold criteria for conversion of probability of species presence to either–or presence–absence. Acta Oecologica, 31, 361–369.
Johns, A. D., & Skorupa, J. P. (1987). Responses of rain-forest primates to habitat disturbance—a review. International Journal of Primatology, 8(2), 157–191.
Johnson, S. E., & Overdorff, D. J. (1999). A census of brown lemurs (Eulemur fulvus sspp.) in Southeastern Madagascar: Methods-testing and conservation implications. American Journal of Primatology, 47, 51–60.
Johnson, S. E., Delmore, K. E, Brown, K. A., Wyman, T. M., Louis, E. E., Jr. (2015) Niche divergence in a brown lemur (Eulemur spp.) hybrid zone: Using ecological niche models to test models of stability. International Journal of Primatology. doi:10.1007/s10764-015-9872-y.
Junker, J., Blake, S., Boesch, C., Campbell, G., Toit, L. D., Duvall, C., et al. (2012). Recent decline in suitable environmental conditions for African great apes. Diversity and Distributions, 18, 1077–1091.
Kappeler, P. M., & Fichtel, C. (2015). The evolution of eulemur social organization. International Journal of Primatology. doi:10.1007/s10764-015-9873-x.
Kamilar, J. M. (2009). Environmental and geographic correlates of the taxonomic structure of primate communities. American Journal of Physical Anthropology, 139, 382–393.
Kamilar, J. M., & Beaudrot, L. (2013). Understanding primate communities: Recent developments and future directions. Evolutionary Anthropology, 22, 174–185.
Kamilar, J. M., & Beaudrot, L. (2015) Quantitative methods for primate biogeography and macroecology In C. A. Shaffer, F. Dolins, J. R. Hickey, N. P. Nibbelink, & L. M. Porter (eds.), GPS and GIS for primatologists: A practical guide to spatial analysis. New York: Cambridge University Press.
Kamilar, J. M., & Guidi, L. M. (2010). The phylogenetic structure of primate communities: Variation within and across continents. Journal of Biogeography, 37, 801–813.
Kamilar, J. M., & Ledogar, J. A. (2011). Species co-occurrence patterns and dietary resource competition in primates. American Journal of Physical Anthropology, 144, 131–139.
Kamilar, J. M., & Muldoon, K. M. (2010). The climatic niche diversity of Malagasy primates: A phylogenetic approach. PLoS ONE, 5, e11073. doi:10.1371/journal.pone.0011073.
Kamilar, J. M., & Paciulli, L. M. (2008). Examining the extinction risk of specialized folivores: A comparative study of colobine monkeys. American Journal of Primatology, 70(9), 1–12.
Kamilar, J. M., Muldoon, K. M., Lehman, S. M., & Herrera, J. P. (2012). Testing Bergmann’s rule and the resource seasonality hypothesis in Malagasy primates using GIS-based climate data. American Journal of Physical Anthropology, 147, 401–408.
Kamilar, J. M., Blanco, M., & Muldoon, K. M. (2015) Ecological niche modeling of mouse lemurs (Microcebus spp.) and its implications for their species diversity and biogeography. In S. M. Lehman, U. Radespiel, & E. Zimmermann (eds.), Dwarf and mouse lemurs of Madagascar: Biology, behavior and conservation biogeography of the Cheirogaleidae. Cambridge, U.K.: Cambridge University Press.
Kissling, W. D., Dormann, C. F., Groeneveld, J., Hickler, T., Kühn, I., McInerny, G. J., Montoya, J. M., Romermann, C., Schiffers, K., Schurr, F. M., Singer, A., Svenning, J.-C., Zimmermann, N. E., & O’Hara, R. B. (2012). Towards novel approaches to modelling biotic interactions in multispecies assemblages at large spatial extents. Journal of Biogeography, 39, 2163–2178.
Kistler, L., Ratan, A., Godfrey, L. R., Crowley, B. E., Hughes, C. E., Lei, R., Cui, Y., Wood, M. L., Muldoon, K. M., Andriamialison, H., McGraw, J. J., Tomsho, L. P., Schuster, S. C., Miller, W., Louis, E. E., Yoder, A. D., Malhi, R. S., & Perry, G. H. (2015). Comparative and population mitogenomic anfalyses of Madagascar's extinct, giant ‘subfossil’ lemurs. Journal of Human Evolution, 79, 45–54.
Köndgen, S., Kühl, H., N'Goran, P. K., Walsh, P. D., Schenk, S., Ernst, N., Biek, R., Formenty, P., Mätz-Rensing, K., Schweiger, B., Junglen, S., Ellerbrok, H., Nitsche, A., Briese, T., Lipkin, W. I., Pauli, G., Boesch, C., & Leendertz, F. H. (2008). Pandemic human viruses cause decline of endangered great apes. Current Biology, 18, 260–264.
Lehman, S. M. (2006). Nested distribution patterns and the historical biogeography of the primates of Guyana. In S. M. Lehman & J. G. Fleagle (Eds.), Primate biogeography (pp. 63–80). New York: Springer Science+Business Media.
Liu, C., Berry, P. M., Dawson, T. P., & Pearson, R. G. (2005). Selecting thresholds of occurrence in the prediction of species distributions. Ecography, 28, 385–393.
Markolf, M., & Kappeler, P. M. (2013). Phylogeographic analysis of the true lemurs (genus Eulemur) underlines the role of river catchments for the evolution of micro-endemism in Madagascar. Frontiers in Zoology, 10, 70.
Markolf, M., Rakotonirina, H., Fichtel, C., von Grumbkow, P., Brameier, M., & Kappeler, P. M. (2013). True lemurs… true species-species delimitation using multiple data sources in the brown lemur complex. BMC evolutionary biology, 13(1), 233.
Miller, L. E. (Ed.). (2002). Eat or be eaten: Predator sensitive foraging in primates. Cambridge, U.K.: Cambridge University Press.
Muldoon, K., & Goodman, S. (2010). Ecological biogeography of Malagasy non-volant mammals: Community structure is correlated with habitat. Journal of Biogeography, 37, 1144–1159.
Myers, N., Mittermeier, R. A., Mittermeier, C. G., da Fonseca, G. A. B., & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403, 853–858.
Nunn, C. L. (2012). Primate disease ecology in comparative and theoretical perspective. American Journal of Primatology, 74, 490–509.
Oates, J. F., Whitesides, G. H., Davies, A. G., Waterman, P. G., Green, S. M., Dasilva, G. L., & Mole, S. (1990). Determinants of variation in tropical forest primate biomass: New evidence from west Africa. Ecology, 71(1), 328–343.
Ossi, K. M., & Kamilar, J. M. (2006). Environmental and phylogenetic correlates of Eulemur behavior and ecology (Primates: Lemuridae). Behavioral Ecology and Sociobiology, 61, 53–64.
Overdorff, D. J. (1991). Ecological correlates to social structure in two prosimian primates: Eulemur fulvus rufous and Eulemur rubriventer in Madagascar. Ph.D. dissertation, Duke University, Durham, NC.
Overdorff, D. J. (1993). Ecological and reproductive correlates to range use in red-bellied lemurs (Eulemur rubriventer) and rufous lemurs (Eulemur fulvus rufus). In J. Ganzhorn & P. M. Kappeler (Eds.), Lemur social systems and their ecological basis (pp. 167–178). New York: Plenum Press.
Peterson, A. T., Soberon, J., Pearson, R. G., Anderson, R. P., Martinez-Meyer, E., Nakamura, M., & Araújo, M. B. (2011). Ecological niches and geographic distributions. Princeton, NJ: Princeton University Press.
Phillips, S. J., & Dudık, M. (2008). Modeling of species distributions with Maxent: New extensions and a comprehensive evaluation. Ecography, 31, 161–175.
Phillips, S. J., Anderson, R. P., & Schapire, R. E. (2006). Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190, 231–259.
Radosavljevic, A., & Anderson, R. P. (2014). Making better Maxent models of species distributions: Complexity, overfitting and evaluation. Journal of Biogeography, 41(4), 629–643.
Rasambainarivo, F. T., Gillespie, T. R., Wright, P. C., Arsenault, J., Villeneuve, A., & Lair, S. (2013). Survey of Giardia and Cryptosporidium in lemurs from the Ranomafana National Park, Madagascar. Journal of Wildlife Diseases, 49, 741–743.
Raxworthy, C. J., Ingram, C. M., Rabibisoa, N., & Pearson, R. G. (2007). Applications of ecological niche modeling for species delimitation: A review and empirical evaluation using day geckos (Phelsuma) from Madagascar. Systematic Biology, 56(6), 907–923.
Razafindratsima, O. H., & Dunham, A. E. (2015). Assessing the impacts of nonrandom seed dispersal by multiple frugivore partners on plant recruitment. Ecology, 96, 24–30.
Reed, K. E., & Fleagle, J. G. (1995). Geographic and climatic control of primate diversity. Proceedings of the National Academy of Sciences of the USA, 92(17), 7874–7876.
Schwitzer, C., Mittermeier, R. A., Davies, N., Johnson, S. E., Ratsimbazafy, J., Razafindramanana, J., Louis, E. E., & Rajaobelina, S. (2013). Lemurs of Madagascar: A strategy for their conservation 2013–2016. IUCN SSC Primate Specialist Group Report. Bristol Conservation and Science Foundation, and Conservation International, Bristol, U.K.
Schwitzer, C., Mittermeier, R. A., Johnson, S. E., Donati, G., Irwin, M., Peacock, H., Ratsimbazafy, J., Razafindramanana, J., Louis, E. E., Jr., Chikhi, L., Colquhoun, I. C., Tinsman, J., Dolch, R., LaFleur, M., Nash, S., Patel, E., Randrianambinina, B., Rasolofoharivelo, T., & Wright, P. C. (2014). Averting lemur extinctions amid Madagascar's political crisis. Science, 343, 842–843.
Tattersall, I. (1987). Cathemeral activity in primates: a definition. Folia primatologica, 49(3-4), 200–202.
Tattersall, I., & Sussman, R. W. (1998). ‘Little brown lemurs’ of northern Madagascar. Folia Primatologica, 69(Suppl. 1), 379–388.
Tecot, S. R. (2008). Seasonality and predictability: The hormonal and behavioral responses of the red-bellied lemur, Eulemur rubriventer, in southeastern Madagascar. University of Texas at Austin.
Tecot, S. (2010). It’s all in the timing: Out of season births and infant survival in Eulemur rubriventer. International Journal of Primatology, 31, 715–735.
Tecot, S. (2013). Variable energetic strategies in disturbed and undisturbed rain forest habitats: Fecal cortisol levels in southeastern Madagascar. In J. Masters, M. Gamba, F. Génin, & R. Tuttle (eds.), Leaping ahead: Advances in prosimian biology (pp. 185–195). Developments in Primatology: Progress and Prospects. New York: Springer Science+Business Media.
Thorne, J. H., Seo, C., Basabose, A., Gray, M., Belfiore, N. M., & Hijmans, R. J. (2013). Alternative biological assumptions strongly influence models of climate change effects on mountain gorillas. Ecosphere, 4, Article108.
Wilmé, L., Goodman, S. M., & Ganzhorn, J. U. (2006). Biogeographic evolution of Madagascar's microendemic biota. Science, 312(5776), 1063–1065.
Wright, P. C. (1999). Lemur traits and Madagascar ecology: Coping with an island environment. Yearbook of Physical Anthropology, 42, 31–72.
Wright, P. C., Arrigo‐Nelson, S. J., Hogg, K. L., Bannon, B., Morelli, T. L., Wyatt, J., Harivelo, A. L., & Ratelolahy, F. (2009). Habitat distrubance and seasonal fluctuations of lemur parasites in the rain forest of Ranomafana National Park, Madagascar. In M. A. Huffman & C. A. Chapman (Eds.), Primate parasite ecology: The dynamics of host‐parasite relationships (pp. 311–330). Cambridge, U.K.: Cambridge University Press.
Wright, P. C., Tecot, S. R., Erhart, E. M., Baden, A. L., King, S. J., & Grassi, C. (2011). Frugivory in four sympatric lemurs: Implications for the future of Madagascar's forests. American Journal of Primatology, 73, 585–602.
Yackulic, C. B., Chandler, R., Zipkin, E. F., Royle, J. A., Nichols, J. D., Campbell Grant, E. H., & Veran, S. (2013). Presence‐only modelling using MAXENT: When can we trust the inferences? Methods in Ecology and Evolution, 4, 236–243.
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We thank Steig Johnson and Guiseppe Donati for inviting us to contribute to this special issue. Our article was improved by helpful comments provided by four anonymous reviewers and Steig Johnson.
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Kamilar, J.M., Tecot, S.R. Anthropogenic and Climatic Effects on the Distribution of Eulemur Species: An Ecological Niche Modeling Approach. Int J Primatol 37, 47–68 (2016). https://doi.org/10.1007/s10764-015-9875-8
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DOI: https://doi.org/10.1007/s10764-015-9875-8