International Journal of Primatology

, Volume 38, Issue 4, pp 692–716 | Cite as

The Effects of Biogeography and Biotic Interactions on Lemur Community Assembly

  • James P. Herrera


Geographic patterns of biodiversity result from broad-scale biogeographic and present-day ecological processes. The aim of this study was to investigate the relative importance of biogeographic history and ecology driving patterns of diversity in modern primate communities in Madagascar. I collected data on endemic lemur species co-occurrence from range maps and survey literature for 100 communities in protected areas. I quantified and compared taxonomic, phylogenetic, and functional dimensions of intra- and intersite diversity. I tested environmental and geographic predictors of diversity and endemism. I calculated deforestation rates within protected areas between the years 2000 and 2014, and tested if diversity is related to forest cover and loss. I found the phylogenetic structure of lemur communities could be explained primarily by remotely sensed plant productivity, supporting the hypothesis that there was ecological differentiation among ecoregions, while functional-trait disparity was not strongly related to environment. Taxonomic and phylogenetic diversity also increased with increasing topographic heterogeneity. Beta diversity was explained by both differences in ecology among localities and potential river barriers. Approximately 3000 km2 were deforested in protected areas since the year 2000, threatening the most diverse communities (up to 31%/park). The strong positive association of plant productivity and topographic heterogeneity with lemur diversity indicates that high productivity, rugged landscapes support greater diversity. Both ecology and river barriers influenced lemur community ecology and biogeography. These results underscore the need for focused conservation efforts to slow the loss of irreplaceable evolutionary and ecological diversity.


Beta diversity Deforestation Geographic barriers Macroecology Phylogenetic community ecology Species richness 



I thank the National Science Foundation (Graduate Research Fellowship), Stony Brook University (Turner Fellowship), and the American Museum of Natural History (Gerstner Scholarship) for funding. I thank the following colleagues for helpful comments on this research and earlier drafts of the manuscript: P. C. Wright, E. R. Seiffert, L. M. Dávalos, W. L. Jungers, C. L. Nunn, C. H. Graham, C. Raxworthy, J. J. Flynn, N. B. Simmons, W. Pearse, and S. Desbureaux; members of the AMNH Ecological and Evolutionary Modelling Discussion Group, especially F. Burbrink; and members of the AMNH Center for Biodiversity and Conservation, especially S. Macey. I thank three anonymous reviewers of this manuscript submitted elsewhere, two anonymous reviewers at International Journal of Primatology, and especially J. Setchell for giving helpful feedback on earlier versions of this manuscript and pointing out ways to improve the research.

Supplementary material (4.9 mb)
ESM 1 (ZIP 4.88 mb)


  1. Bannar-Martin, K. H. (2014). Primate and nonprimate mammal community assembly: the influence of biogeographic barriers and spatial scale. International Journal of Primatology, 35(6), 1122–1142.CrossRefGoogle Scholar
  2. Baselga, A. (2010). Partitioning the turnover and nestedness components of beta diversity. Global Ecology and Biogeography, 19(1), 134–143.CrossRefGoogle Scholar
  3. Baselga, A., & Orme, C. D. L. (2012). Betapart: an R package for the study of beta diversity. Methods in Ecology and Evolution, 3(5), 808–812.CrossRefGoogle Scholar
  4. Beaudrot, L. H., & Marshall, A. J. (2011). Primate communities are structured more by dispersal limitation than by niches. Journal of Animal Ecology, 80(2), 332–341.CrossRefPubMedGoogle Scholar
  5. Blair, M., Sterling, E., Dusch, M., Raxworthy, C., & Pearson, R. (2013). Ecological divergence and speciation between lemur (Eulemur) sister species in Madagascar. Journal of Evolutionary Biology, 26(8), 1790–1801.CrossRefPubMedGoogle Scholar
  6. Boubli, J. P., Ribas, C., Alfaro, J. W. L., Alfaro, M. E., da Silva, M. N. F., et al (2015). Spatial and temporal patterns of diversification on the Amazon: a test of the riverine hypothesis for all diurnal primates of Rio Negro and Rio Branco in Brazil. Molecular Phylogenetics and Evolution, 82, 400–412.CrossRefPubMedGoogle Scholar
  7. Brook, G. A., Rafter, M. A., Railsback, L. B., Sheen, S.-W., & Lundberg, J. (1999). A high-resolution proxy record of rainfall and ENSO since AD 1550 from layering in stalagmites from Anjohibe cave, Madagascar. The Holocene, 9(6), 695–705.CrossRefGoogle Scholar
  8. Brown, J. L., Cameron, A., Yoder, A. D., & Vences, M. (2014). A necessarily complex model to explain the biogeography of the amphibians and reptiles of Madagascar. Nature Communications, 5, 5046.CrossRefPubMedGoogle Scholar
  9. Brunsdon, C., & Chen, H. (2014). GISTools: some further GIS capabilities for R: CRAN.
  10. Burney, D. A., Burney, L. P., Godfrey, L. R., Jungers, W. L., Goodman, S. M., et al (2004). A chronology for late prehistoric Madagascar. Journal of Human Evolution, 47(1), 25–63.CrossRefPubMedGoogle Scholar
  11. Burnham, K. P., & Anderson, D. R. (2002). Model selection and multimodel inference: a practical information-theoretic approach. New York: Springer Science+Business Media.Google Scholar
  12. Burns, S. J., Godfrey, L. R., Faina, P., McGee, D., Hardt, B., et al (2016). Rapid human-induced landscape transformation in Madagascar at the end of the first millennium of the common era. Quaternary Science Reviews, 134, 92–99.CrossRefGoogle Scholar
  13. Cavender-Bares, J., Kozak, K. H., Fine, P. V. A., & Kembel, S. W. (2009). The merging of community ecology and phylogenetic biology. Ecology Letters, 12(7), 693–715.CrossRefPubMedGoogle Scholar
  14. Cohen, J., Cohen, P., West, S. G., & Aiken, L. S. (2013). Applied multiple regression/correlation analysis for the behavioral sciences. New York: Routledge.Google Scholar
  15. Craul, M., Radespiel, U., Rasolofoson, D., Rakotondratsimba, G., Rakotonirainy, O., et al (2008). Large rivers do not always act as species barriers for Lepilemur sp. Primates, 49(3), 211–218.CrossRefPubMedGoogle Scholar
  16. Crowley, B. E., Godfrey, L. R., Bankoff, R. J., Perry, G. H., Culleton, B. J., et al (2016). Island-wide aridity did not trigger recent megafaunal extinctions in Madagascar. Ecography. doi: 10.1111/ecog.02376.
  17. Dapporto, L., Ramazzotti, M., Fattorini, S., Talavera, G., Vila, R., & Dennis, R. L. (2013). Recluster: an unbiased clustering procedure for beta-diversity turnover. Ecography, 36(10), 1070–1075.CrossRefGoogle Scholar
  18. Devictor, V., Mouillot, D., Meynard, C., Jiguet, F., Thuiller, W., & Mouquet, N. (2010). Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecology Letters, 13(8), 1030–1040.PubMedGoogle Scholar
  19. Faith, D. P. (1992). Conservation evaluation and phylogenetic diversity. Biological Conservation, 61(1), 1–10.CrossRefGoogle Scholar
  20. Fergnani, P. N., & Ruggiero, A. (2015). Ecological diversity in south American mammals: their geographical distribution shows variable associations with phylogenetic diversity and does not follow the latitudinal richness gradient. PloS One, 10(6), e0128264.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Ferrier, S., Manion, G., Elith, J., & Richardson, K. (2007). Using generalized dissimilarity modelling to analyse and predict patterns of beta diversity in regional biodiversity assessment. Diversity and Distributions, 13(3), 252–264.CrossRefGoogle Scholar
  22. Ganzhorn, J. U. (1988). Food partitioning among Malagasy primates. Oecologia, 75(3), 436–450.CrossRefPubMedGoogle Scholar
  23. Ganzhorn, J. (1997). Test of Fox's assembly rule for functional groups in lemur communities in Madagascar. Journal of Zoology, 241(3), 533–542.CrossRefGoogle Scholar
  24. Ganzhorn, J. U., Malcomber, S., Adrianantoanina, O., & Goodman, S. M. (1997). Habitat characteristics and lemur species richness in Madagascar. Biotropica, 29, 331–343.CrossRefGoogle Scholar
  25. Ganzhorn, J. U., Wright, P. C., & Ratsimbazafy, J. (1999). Primate communities: Madagascar. In J. Fleagle, C. Janson, & K. Reed (Eds.), Primate communities (pp. 75–89). Cambridge: Cambridge University Press.CrossRefGoogle Scholar
  26. Ganzhorn, J. U., Goodman, S. M., Nash, S., & Thalmann, U. (2006). Lemur biogeography. In J. G. Fleagle & S. M. Lehman (Eds.), Primate biogeography: progress and perspectives (pp. 229–254). Developments in Primatology: Progress and Prospects). New York: Springer Science+Business Media.CrossRefGoogle Scholar
  27. Geissler, P., Hartmann, T., Ihlow, F., Rödder, D., Poyarkov, N. A., et al (2015). The lower Mekong: an insurmountable barrier to amphibians in southern Indochina? Biological Journal of the Linnean Society, 114(4), 905–914.CrossRefGoogle Scholar
  28. Godfrey, L. R., Jungers, W. L., & Burney, D. A. (2010). Subfossil lemurs of Madagascar. In L. Werdelin & W. Sanders (Eds.), Cenozoic mammals of Africa (pp. 351–367). Berkeley: University of California Press.CrossRefGoogle Scholar
  29. Goodman, S. M., & Ganzhorn, J. U. (2004a). Biogeography of lemurs in the humid forests of Madagascar: the role of elevational distribution and rivers. Journal of Biogeography, 31(1), 47–55.CrossRefGoogle Scholar
  30. Goodman, S. M., & Ganzhorn, J. U. (2004b). Elevational ranges of lemurs in the humid forests of Madagascar. International Journal of Primatology, 25(2), 331–350.CrossRefGoogle Scholar
  31. Goodman, S. M., & Jungers, W. L. (2014). Extinct Madagascar: picturing the island's past. Chicago: University of Chicago Press.Google Scholar
  32. Goslee, S. C., & Urban, D. L. (2007). The ecodist package for dissimilarity-based analysis of ecological data. Journal of Statistical Software, 22(7), 1–19.CrossRefGoogle Scholar
  33. Gower, S. T., Kucharik, C. J., & Norman, J. M. (1999). Direct and indirect estimation of leaf area index, f APAR, and net primary production of terrestrial ecosystems. Remote Sensing of Environment, 70(1), 29–51.CrossRefGoogle Scholar
  34. Graham, C. H., & Fine, P. V. A. (2008). Phylogenetic beta diversity: linking ecological and evolutionary processes across space in time. Ecology Letters, 11(12), 1265–1277.CrossRefPubMedGoogle Scholar
  35. Graham, C. H., & Hijmans, R. J. (2006). A comparison of methods for mapping species ranges and species richness. Global Ecology and Biogeography, 15(6), 578–587.CrossRefGoogle Scholar
  36. Groeneveld, L., Weisrock, D., Rasoloarison, R., Yoder, A., & Kappeler, P. (2009). Species delimitation in lemurs: multiple genetic loci reveal low levels of species diversity in the genus Cheirogaleus. BMC Evolutionary Biology, 9(1), 30.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Hansen, M. C., Potapov, P. V., Moore, R., Hancher, M., Turubanova, S., et al (2013). High-resolution global maps of 21st-century forest cover change. Science, 342(6160), 850–853.CrossRefPubMedGoogle Scholar
  38. 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(4), 325–333.CrossRefGoogle Scholar
  39. Heinsch, F. A., Reeves, M., Votava, P., Kang, S., Milesi, C., et al. (2003). GPP and NPP (MOD17A2/A3) products NASA MODIS land algorithm. MOD17 User's Guide, 1–57.Google Scholar
  40. Helmus, M. R., Savage, K., Diebel, M. W., Maxted, J. T., & Ives, A. R. (2007). Separating the determinants of phylogenetic community structure. Ecology Letters, 10(10), 917–925.CrossRefPubMedGoogle Scholar
  41. Herrera, J. P., & Dávalos, L. (2016). Phylogeny and divergence times of lemurs inferred with recent and ancient fossils in the tree. Systematic Biology, 65(5), 772–791.CrossRefPubMedGoogle Scholar
  42. Hijmans, R. J. (2015). Raster: Geographic data analysis and modeling. CRAN.
  43. 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(15), 1965–1978.CrossRefGoogle Scholar
  44. Hurlbert, A. H., & Jetz, W. (2007). Species richness, hotspots, and the scale dependence of range maps in ecology and conservation. Proceedings of the National Academy of Sciences of the USA, 104(33), 13384–13389.CrossRefPubMedPubMedCentralGoogle Scholar
  45. Ives, A. R., & Helmus, M. R. (2010). Phylogenetic metrics of community similarity. The American Naturalist, 176(5), E128–E142.CrossRefPubMedGoogle Scholar
  46. Kamilar, J. M. (2009). Environmental and geographic correlates of the taxonomic structure of primate communities. American Journal of Physical Anthropology, 139(3), 382–393.CrossRefPubMedGoogle Scholar
  47. Kamilar, J. M., & Guidi, L. M. (2010). The phylogenetic structure of primate communities: variation within and across continents. Journal of Biogeography, 37(5), 801–813.CrossRefGoogle Scholar
  48. Kamilar, J. M., & Muldoon, K. M. (2010). The climatic niche diversity of Malagasy primates: a phylogenetic perspective. PloS One, 5(6), e11073.CrossRefPubMedPubMedCentralGoogle Scholar
  49. Karpanty, S. M., & Wright, P. C. (2007). Predation on lemurs in the rainforest of Madagascar by multiple predator species: observations and experiments. In Primate anti-predator strategies (pp. 77–99). Developments in primatology: progress and prospects. New York: Springer Science+Business Media.Google Scholar
  50. Kembel, S. W., & Hubbell, S. P. (2006). The phylogenetic structure of a neotropical forest tree community. Ecology, 87(7), S86–S99.CrossRefPubMedGoogle Scholar
  51. Kembel, S. W., Cowan, P. D., Helmus, M. R., Cornwell, W. K., Morlon, H., et al (2010). Picante: R tools for integrating phylogenies and ecology. Bioinformatics, 26(11), 1463–1464.CrossRefPubMedGoogle Scholar
  52. Kerr, J. T., & Packer, L. (1997). Habitat heterogeneity as a determinant of mammal species richness in high-energy regions. Nature, 385(6613), 252–254.CrossRefGoogle Scholar
  53. Koechlin, J. (1972). Flora and vegetation of Madagascar. In Biogeography and ecology in Madagascar (pp. 145–190). New York: Springer-Verlag.CrossRefGoogle Scholar
  54. Kremen, C., Cameron, A., Moilanen, A., Phillips, S. J., Thomas, C. D., et al (2008). Aligning conservation priorities across taxa in Madagascar with high-resolution planning tools. Science, 320(5873), 222–226.CrossRefPubMedGoogle Scholar
  55. Legendre, P., Fortin, M. J., & Borcard, D. (2015). Should the mantel test be used in spatial analysis? Methods in Ecology and Evolution, 6(11), 1239–1247.CrossRefGoogle Scholar
  56. Lei, R., Engberg, S. E., Andriantompohavana, R., McGuire, S. M., Mittermeier, R. A., et al (2008). Nocturnal lemur diversity at Masoala National Park. Special Publications of Texas Tech University, 53, 1–48.Google Scholar
  57. Louis, E. E. (2006). Molecular and morphological analyses of the sportive lemurs (Family Megaladapidae: Genus Lepilemur) reveals 11 previously unrecognized species. Lubbock: Museum of Texas Tech University.Google Scholar
  58. Louis, E. E., & Lei, R. (2016). Mitogenomics of the family Cheirogaleidae and relationships to taxonomy and biogeography in Madagascar. In S. M. Lehman, U. Radespiel, & E. Zimmermann (Eds.), The dwarf and mouse lemurs of Madagascar: biology, behavior, and conservation biogeography of the Cheirogaleidae. London: Cambridge University Press.Google Scholar
  59. Maechler, M., Rousseeuw, P., Struyf, A., Hubert, M., Hornik, K., Studer, M., & Roudier, P. (2015). Cluster analysis extended Rousseeuw et al. CRAN.
  60. Markolf, M., Brameier, M., & Kappeler, P. (2011). On species delimitation: yet another lemur species or just genetic variation? BMC Evolutionary Biology, 11, 216.CrossRefPubMedPubMedCentralGoogle Scholar
  61. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Martin, R. D. (1972). Adaptive radiation and behaviour of the Malagasy lemurs. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 264, 295–352.CrossRefPubMedGoogle Scholar
  63. Matthews, T. J., Cottee-Jones, H. E., & Whittaker, R. J. (2014). Habitat fragmentation and the species–area relationship: a focus on total species richness obscures the impact of habitat loss on habitat specialists. Diversity and Distributions, 20(10), 1136–1146.CrossRefGoogle Scholar
  64. Mayfield, M. M., & Levine, J. M. (2010). Opposing effects of competitive exclusion on the phylogenetic structure of communities. Ecology Letters, 13(9), 1085–1093.CrossRefPubMedGoogle Scholar
  65. Mazerolle, M. (2013). AICcmodavg: model selection and multimodel inference based on (Q)AIC(c). v1.28. CRAN.
  66. Mercier, J.-L., & Wilmé, L. (2013). The eco-geo-Clim model: explaining Madagascar’s endemism. Madagascar Conservation & Development, 8(2), 63–68.Google Scholar
  67. Mittelbach, G. G., & Schemske, D. W. (2015). Ecological and evolutionary perspectives on community assembly. Trends in Ecology & Evolution, 30(5), 241–247.CrossRefGoogle Scholar
  68. Mittermeier, R. A., Louis, E. E., Richardson, M., Schwitzer, C., Langrand, O., et al (2010). Lemurs of Madagascar (3rd ed.). Washington, DC: Conservation International.Google Scholar
  69. Muldoon, K. M., & Goodman, S. M. (2010). Ecological biogeography of Malagasy non volant mammals: community structure is correlated with habitat. Journal of Biogeography, 37(6), 1144–1159.CrossRefGoogle Scholar
  70. Muldoon, K. M., & Goodman, S. M. (2015). Primates as predictors of mammal community diversity in the forest ecosystems of Madagascar. PloS One, 10(9), e0136787.CrossRefPubMedPubMedCentralGoogle Scholar
  71. Newbold, T., Hudson, L. N., Hill, S. L., Contu, S., Lysenko, I., et al (2015). Global effects of land use on local terrestrial biodiversity. Nature, 520(7545), 45–50.CrossRefPubMedGoogle Scholar
  72. Ohba, M., Samonds, K. E., LaFleur, M., Ali, J. R., & Godfrey, L. R. (2016). Madagascar's climate at the K/P boundary and its impact on the island's biotic suite. Palaeogeography, Palaeoclimatology, Palaeoecology, 441, 688–695.CrossRefGoogle Scholar
  73. Oksanen, J., Blanchet, F. G., Kindt, R., Legendre, P., Minchin, P. R., et al. (2013). Package ‘vegan.’ CRAN.
  74. Oliver, T. H., Isaac, N. J., August, T. A., Woodcock, B. A., Roy, D. B., & Bullock, J. M. (2015). Declining resilience of ecosystem functions under biodiversity loss. Nature Communications, 6, 10122.CrossRefPubMedPubMedCentralGoogle Scholar
  75. Ossi, K., & Kamilar, J. M. (2006). Environmental and phylogenetic correlates of Eulemur behavior and ecology (primates: Lemuridae). Behavioral Ecology and Sociobiology, 61(1), 53–64.CrossRefGoogle Scholar
  76. Paradis, E., Claude, J., & Strimmer, K. (2004). APE: analysis of phylogenetics and evolution in R language. Bioinformatics, 20, 289–290.CrossRefPubMedGoogle Scholar
  77. Pastorini, J., Thalmann, U., & Martin, R. D. (2003). A molecular approach to comparative phylogeography of extant Malagasy lemurs. Proceedings of the National Academy of Sciences of the USA, 100(10), 5879–5884.CrossRefPubMedPubMedCentralGoogle Scholar
  78. Pearson, R. G., & Raxworthy, C. J. (2009). The evolution of local endemism in Madagascar: watershed versus climatic gradient hypotheses evaluated by null biogeographic models. Evolution, 63(4), 959–967.CrossRefPubMedGoogle Scholar
  79. Perez, V. R., Godfrey, L. R., Nowak-Kemp, M., Burney, D. A., Ratsimbazafy, J., & Vasey, N. (2005). Evidence of early butchery of giant lemurs in Madagascar. Journal of Human Evolution, 49(6), 722–742.CrossRefPubMedGoogle Scholar
  80. Pinheiro, J., Bates, D., DebRoy, S., & Sarkar, D. (2011). Nlme: linear and nonlinear mixed effects models. R package version 3.1–97. CRAN.
  81. Price, T. D., Hooper, D. M., Buchanan, C. D., Johansson, U. S., Tietze, D. T., et al (2014). Niche filling slows the diversification of Himalayan songbirds. Nature, 509(7499), 222–225.CrossRefPubMedGoogle Scholar
  82. Purvis, A., & Hector, A. (2000). Getting the measure of biodiversity. Nature, 405(6783), 212–219.CrossRefPubMedGoogle Scholar
  83. Quantum GIS Development Team. (2015). Quantum GIS geographic information system. Open Source Geospatial Foundation Project.
  84. R Core Team. (2014). R: a language and environment for statistical computing.
  85. Radespiel, U., Ratsimbazafy, J., Rasoloharijaona, S., Raveloson, H., Andriaholinirina, N., Rakotondravony, R., Randrianarison, R., & Randrianambinina, B. (2011). First indications of a highland specialist among mouse lemurs (Microcebus spp.) and evidence for a new mouse lemur species from eastern Madagascar. Primates, 53(2), 157–170.Google Scholar
  86. Rangel, T. F., Colwell, R. K., Graves, G. R., Fučíková, K., Rahbek, C., & Diniz-Filho, J. A. F. (2015). Phylogenetic uncertainty revisited: Implications for ecological analyses. Evolution. doi: 10.1111/evo.12644.
  87. Rasoloarison, R. M., Weisrock, D. W., Yoder, A. D., Rakotondravony, D., & Kappeler, P. M. (2013). Two new species of mouse lemurs (Cheirogaleidae: Microcebus) from eastern Madagascar. International Journal of Primatology, 34(3), 455–469.CrossRefGoogle Scholar
  88. Razafindratsima, O. H., Mehtani, S., & Dunham, A. E. (2013). Extinctions, traits and phylogenetic community structure: insights from primate assemblages in Madagascar. Ecography, 36(1), 47–56.CrossRefGoogle Scholar
  89. Razafindratsima, O. H., Jones, T. A., & Dunham, A. E. (2014). Patterns of movement and seed dispersal by three lemur species. American Journal of Primatology, 76(1), 84–96.CrossRefPubMedGoogle Scholar
  90. Rosauer, D., Laffan, S. W., Crisp, M. D., Donnellan, S. C., & Cook, L. G. (2009). Phylogenetic endemism: a new approach for identifying geographical concentrations of evolutionary history. Molecular Ecology, 18(19), 4061–4072.CrossRefPubMedGoogle Scholar
  91. Samonds, K. E., Godfrey, L. R., Ali, J. R., Goodman, S. M., Vences, M., et al (2013). Imperfect isolation: factors and filters shaping Madagascar’s extant vertebrate fauna. PloS One, 8(4), e62086.CrossRefPubMedPubMedCentralGoogle Scholar
  92. Scales, I. R. (2014). The drivers of deforestation and the complexity of land use in Madagascar. In I. Scales (Ed.), Conservation and environmental management in Madagascar (pp. 105–125). New York: Routledge.Google Scholar
  93. Schwitzer, C., Mittermeier, R., Johnson, S. E., Donati, G., Irwin, M. T., et al (2014). Averting lemur extinctions amid Madagascar's political crisis. Science, 343, 842–843.CrossRefPubMedGoogle Scholar
  94. Smith, R. J., & Jungers, W. L. (1997). Body mass in comparative primatology. Journal of Human Evolution, 32(6), 523–559.CrossRefPubMedGoogle Scholar
  95. Smith, B. T., McCormack, J. E., Cuervo, A. M., Hickerson, M. J., Aleixo, A., et al (2014). The drivers of tropical speciation. Nature, 515(7527), 406–409.CrossRefPubMedGoogle Scholar
  96. Sreekar, R., Huang, G., Zhao, J. B., Pasion, B. O., Yasuda, M., et al (2015). The use of species–area relationships to partition the effects of hunting and deforestation on bird extirpations in a fragmented landscape. Diversity and Distributions, 21(4), 441–450.CrossRefGoogle Scholar
  97. Swenson, N. G., Enquist, B. J., Pither, J., Thompson, J., & Zimmerman, J. K. (2006). The problem and promise of scale dependency in community phylogenetics. Ecology, 87(10), 2418–2424.CrossRefPubMedGoogle Scholar
  98. Tattersall, I. (2007). Madagascar's lemurs: cryptic diversity or taxonomic inflation? Evolutionary Anthropology, 16, 12–23.CrossRefGoogle Scholar
  99. van Etten, J. (2012). Gdistance: distances and routes on geographical grids. CRAN.
  100. Vavrek, M. J. (2011). Fossil: palaeoecological and palaeogeographical analysis tools. Palaeontologia Electronica, 14(1), 16.Google Scholar
  101. Vences, M., Wollenberg, K. C., Vieites, D. R., & Lees, D. C. (2009). Madagascar as a model region of species diversification. Trends in Ecology & Evolution, 24(8), 456–465.CrossRefGoogle Scholar
  102. Virah-Sawmy, M., Willis, K. J., & Gillson, L. (2010). Evidence for drought and forest declines during the recent megafaunal extinctions in Madagascar. Journal of Biogeography, 37(3), 506–519.CrossRefGoogle Scholar
  103. Voarintsoa, N. R. G., Wang, L., Railsback, L. B., Brook, G. A., Liang, F., et al. (2017). Multiple proxy analyses of a U/Th-dated stalagmite to reconstruct paleoenvironmental changes in northwestern Madagascar between 370CE and 1300CE. Palaeogeography, Palaeoclimatology, Palaeoecology, 469, 138–155.Google Scholar
  104. Voelker, G., Marks, B., Kahindo, C., A'genonga, U., Bapeamoni, F., et al (2013). River barriers and cryptic biodiversity in an evolutionary museum. Ecology and Evolution, 3(3), 536–545.CrossRefPubMedPubMedCentralGoogle Scholar
  105. Webb, C. O. (2000). Exploring the phylogenetic structure of ecological communities: an example for rain forest trees. The American Naturalist, 156, 145–155.CrossRefPubMedGoogle Scholar
  106. Wilmé, L., Goodman, S. M., & Ganzhorn, J. U. (2006). Biogeographic evolution of Madagascar's microendemic biota. Science, 312(5776), 1063–1065.CrossRefPubMedGoogle Scholar
  107. Wollenberg, K. C., Vieites, D. R., Van Der Meijden, A., Glaw, F., Cannatella, D. C., & Vences, M. (2008). Patterns of endemism and species richness in Malagasy cophyline frogs support a key role of mountainous areas for speciation. Evolution, 62(8), 1890–1907.CrossRefPubMedGoogle Scholar
  108. Wright, P. C., & Martin, L. B. (1995). Predation, pollination, and torpor in two nocturnal prosimians: Cheirogaleus major and Microcebus rufus in the rainforest of Madagascar. In L. Alterman, G. Doyle, & K. Izard (Eds.), Creatures of the dark: the nocturnal prosimians (pp. 45–60). New York: Springer-Verlag.CrossRefGoogle Scholar
  109. Yoder, A. D., Olson, L. E., Hanley, C., Heckman, K. L., Rasoloarison, R., et al (2005). A multidimensional approach for detecting species patterns in Malagasy vertebrates. Proceedings of the National Academy of Sciences of the USA, 102(supplement 1), 6587–6594.CrossRefPubMedPubMedCentralGoogle Scholar
  110. Yoder, A. D., Campbell, C. R., Blanco, M. B., dos Reis, M., Ganzhorn, J. U., et al. (2016). Geogenetic patterns in mouse lemurs (genus Microcebus) reveal the ghosts of Madagascar's forests past. Proceedings of the National Academy of Sciences of the USA, 201601081.Google Scholar
  111. Zhao, F., Xu, B., Yang, X., Jin, Y., Li, J., et al (2014). Remote sensing estimates of grassland aboveground biomass based on MODIS net primary productivity (NPP): a case study in the Xilingol grassland of northern China. Remote Sensing, 6(6), 5368–5386.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  1. 1.Department of Mammalogy, Division of Vertebrate Zoology, American Museum of Natural HistoryNew YorkUSA
  2. 2.Division of Vertebrate Paleontology, American Museum of Natural HistoryNew YorkUSA
  3. 3.Richard Gilder Graduate School, American Museum of Natural HistoryNew YorkUSA

Personalised recommendations