Abstract
Recent studies have demonstrated that dispersal limitation, which refers to the limited ability of individuals to reach distant geographic areas, is an important influence on the species that are found in primate assemblages. In this study, we investigate the relative influences of dispersal limitation and environmental filtering in 131 African primate assemblages in 9 biogeographic regions throughout sub-Saharan Africa. Specifically, we evaluate the dispersal-ecological specialization hypothesis, which posits that there are trade-offs between dispersal ability and ecological specialization that are influenced by climatic variation along latitudinal gradients. The hypothesis predicts that species in assemblages near the equator, where climatic conditions are more stable, will exhibit stronger dispersal limitation and greater ecological specialization than species within assemblages located further from the equator, where climate is more variable. In contrast, assemblages located at higher latitudes are expected to be influenced more strongly by environmental filtering than dispersal limitation. We used hierarchical cluster analysis to identify regions, conducted partial Mantel tests to evaluate the contributions of dispersal limitation and environmental filtering in each region, and evaluated predictors of those contributions with linear regression. In all regions, dispersal limitation was a stronger predictor of community similarity than was environmental filtering, yet the strength of dispersal limitation varied. Dispersal limitation was greatest at low latitudes and declined with increasing absolute latitude. Thus, primate assemblages exhibited a significant latitudinal gradient in dispersal limitation, but not in environmental filtering. These results support aspects of the dispersal-ecological specialization hypothesis and call for future mechanistic studies to address this broad-scale pattern.
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References
Arita, H. T., & Vazquez-Dominguez, E. (2008). The tropics: Cradle, museum or casino? A dynamic null model for latitudinal gradients of species diversity. Ecology Letters, 11, 653–663.
Arnold, C., Matthews, L. J., & Nunn, C. L. (2010). The 10kTrees website: A new online resource for primate phylogeny. Evolutionary Anthropology, 19, 114–118.
Baselga, A., Jimenez-Valverde, A., & Niccolini, G. (2007). A multiple-site similarity measure independent of richness. Biology Letters, 3(6), 642–645.
Baselga, A., Lobo, J. M., Svenning, J. C., Aragon, P., & Araujo, M. B. (2012). Dispersal ability modulates the strength of the latitudinal richness gradient in European beetles. Global Ecology and Biogeography, 21, 1106–1113.
Beaudrot, L., & Marshall, A. J. (2011). Primate communities are structured more by dispersal limitation than by niches. Journal of Animal Ecology, 80, 332–341.
Beaudrot, L., Rejmánek, M., & Marshall, A. J. (2013). Dispersal modes affect tropical forest assembly across trophic levels. Ecography, 36, 984–993.
Bowman, J., Jaeger, J. A. G., & Fahrig, L. (2002). Dispersal distance of mammals is proportional to home range size. Ecology, 83, 2049–2055.
Carnicer, J., Stefanescu, C., Vila, R., Dinca, V., Font, X., & Penuelas, J. (2013). A unified framework for diversity gradients: The adaptive trait continuum. Global Ecology and Biogeography, 22, 6–18.
Carstensen, D. W., Lessard, J. P., Holt, B. G., Borregaard, M. K., & Rahbek, C. (2013). Introducing the biogeographic species pool. Ecography, 36, 1–9.
Case, T. J., & Taper, M. L. (2000). Interspecific competition, environmental gradients, gene flow, and the coevolution of species' borders. American Naturalist, 155, 583–605.
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, 693–715.
Chase, J. M., Amarasekare, P., Cottenie, K., Gonzalez, A., Holt, R. D., Holyoak, M., et al. (2005). Competing theories for competitive metacommunities. In M. Holyoak, M. A. Leibold, & R. D. Holt (Eds.), Metacommunities: Spatial dynamics and ecological communities (pp. 334–354). Chicago: University of Chicago Press.
Chase, J. M., & Myers, J. A. (2011). Disentangling the importance of ecological niches from stochastic processes across scales. Philosophical Transactions of the Royal Society B: Biological Sciences, 366, 2351–2363.
Cottenie, K. (2005). Integrating environmental and spatial processes in ecological community dynamics. Ecology Letters, 8, 1175–1182.
Cowlishaw, G., & Hacker, J. E. (1997). Distribution, diversity and latitude in African primates. The American Naturalist, 150, 505–512.
Dapporto, L., Ramazzotti, M., Fattorini, S., Talavera, G., Vila, R., & Dennis, R. L. H. (2013a). recluster: An unbiased clustering procedure for beta-diversity turnover. Ecography. doi:10.1111/j.1600-0587.2013.00444.x.
Dapporto, L., Ramazzotti, M., Fattorini, S., Vila, R., Talavera, G., & Dennis, R. L. H. (2013b). recluster: Ordination methods for the analysis of beta-diversity indices. R package version 2.5.
Eeley, H. A. C., & Foley, R. A. (1999). Species richness, species range size and ecological specialisation among African primates: Geographical patterns and conservation implications. Biodiversity and Conservation, 8, 1033–1056.
Eeley, H. A. C., & Lawes, M. J. (1999). Large-scale patterns of species richness and species range size in anthropoid primates. In J. G. Fleagle, C. Janson, & K. Reed (Eds.), Primate communities (pp. 191–219). New York: Cambridge University Press.
Fielding, A. H. (2007). Cluster and classification techniques for the biosciences. New York: Cambridge University Press.
Fleagle, J. G., Janson, C. H., & Reed, K. E. (Eds.). (1999). Primate communities. New York: Cambridge University Press.
Gandon, S., & Michalakis, Y. (2001). Multiple causes of the evolution of dispersal. Oxford: Oxford University Press.
Gavilanez, M. M., & Stevens, R. D. (2013). Role of environmental, historical and spatial processes in the structure of Neotropical primate communities: Contrasting taxonomic and phlogenetic perspectives. Global Ecology and Biogeography, 22, 607–619.
Gompper, M. E., & Gittleman, J. L. (1991). Home range scaling: Intraspecific and comparative trends. Oecologia, 87, 343–348.
Grubb, P. (1982). Refuges and dispersal in the speciation of African forest mammals. In G. T. Prance (Ed.), Biological diversification in the tropics (pp. 537–553). New York: Columbia University Press.
Guillot, G., & Rousset, F. (2013). Dismantling the Mantel tests. Methods in Ecology and Evolution, 4, 336–344.
Harcourt, A. H. (1998). Ecological indicators of risk for Primates, as judged by species’ susceptibility to logging. In T. Caro (Ed.), Behavioral ecology and conservation (pp. 56–79). New York: Oxford University Press.
Harcourt, A. H. (2000). Latitude and latitudinal extent: A global analysis of the Rapoport effect in a tropical mammalian taxon: primates. Journal of Biogeography, 27, 1169–1182.
Harcourt, A. H. (2012). Human biogeography. Berkeley: University of California Press.
Harcourt, A. H., & Wood, M. A. (2012). Rivers as barriers to primate distributions in Africa. International Journal of Primatology, 33, 168–183.
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.
Holt, B. G., Lessard, J. P., Borregaard, M. K., Fritz, S. A., Araujo, M. B., Dimitrov, D., et al. (2013). An update of Wallace’s zoogeographic regions of the world. Science, 339, 74–78.
Hubbell, S. P. (2001). The unified neutral theory of biodiversity and biogeography. Princeton, NJ: Princeton University Press.
Hubbell, S. P. (2005). Neutral theory in community ecology and the hypothesis of functional equivalence. Functional Ecology, 19, 166–172.
Janzen, D. H. (1967). Why mountain passes are higher in the tropics. The American Naturalist, 101, 233–249.
Jocque, M., Field, R., Brendonck, L., & De Meester, L. (2010). Climatic control of dispersal-ecological specialization trade-offs: A metacommunity process at the heart of the latitudinal diversity gradient? Global Ecology and Biogeography, 19, 244–252.
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., & Cooper, N. (2013). Phylogenetic signal in primate behavior, ecology and life history. Philosophical Transactions of the Royal Society B: Biological Sciences, 368, 20123041.
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.
Kamilar, J. M., Martin, S. K., & Tosi, A. J. (2009). Combining biogeographic and phylogenetic data to examine primate speciation: An example using Cercopithecin monkeys. Biotropica, 41, 514–519.
Kamilar, J. M., & Muldoon, K. M. (2010). The climatic niche diversity of Malagasy primates: A phylogenetic perspective. Plos One, 5, e11073.
Kreft, H., & Jetz, W. (2010). A framework for delineating biogeographical regions based on species distributions. Journal of Biogeography, 37, 2029–2053.
Laurance, W. F. (1990). Comparative responses of five arboreal marsupials to tropical forest fragmentation. Journal of Mammalogy, 71, 641–653.
Leithead, M., Anand, M., Duarte, L. D., & Pillar, V. D. (2012). Causal effects of latitude, disturbance and dispersal limitation on richness in a recovering temperate, subtropical and tropical forest. Journal of Vegetation Science, 23, 339–351.
Linder, H. P., de Klerk, H. M., Born, J., Burgess, N. D., Fjeldsa, J., & Rahbek, C. (2012). The partitioning of Africa: Statistically defined biogeographical regions in sub-Saharan Africa. Journal of Biogeography, 39, 1189–1205.
Lindstedt, S. L., Miller, B. J., & Buskirk, S. W. (1986). Home range, time, and body size in mammals. Ecology, 67, 413–418.
Magurran, A. E. (1988). Ecological diversity and its measurements. Princeton, NJ: Princeton University Press.
Munguia, M., Peterson, A. T., & Sanchez-Cordero, V. (2008). Dispersal limitation and geographical distributions of mammal species. Journal of Biogeography, 35, 1879–1887.
Oksanen, J., Blanchet, F., Kindt, R., Legendre, P., Minchin, P. R., O’Hara, R. B., et al. (2013). vegan: Community Ecology Package. R. p. v. 2.0-7. Available at http://CRAN.R-project.org/package=vegan
R Development Core Team. (2013). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.
Rapoport, E. H. (1982). Areography: Geographical strategies of species. New York: Pergamon Press.
Reed, K. E., & Bidner, L. R. (2004). Primate communities: Past, present and possible future. Yearbook of Physical Anthropology, 47, 2–39.
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, 7874–7876.
Rovero, F., Marshall, A. R., Jones, T., & Perkin, A. (2009). The primates of the Udzungwa Mountains: Diversity, ecology and conservation. Journal of Anthropological Science, 87, 93–126.
Salisbury, C. L., Seddon, N., Cooney, C. R., & Tobias, J. A. (2012). The latitudinal gradient in dispersal constraints: Ecological specialisation drives diversification in tropical birds. Ecology Letters, 15, 847–855.
Schwarzkopf, L., & Rylands, A. (1989). Primate species richness in relation to habitat structure in Amazonian rainforest fragments. Biological Conservation, 48, 1–12.
Seber, G. A. F. (1984). Multivariate observations. New York: John Wiley & Sons.
Smouse, P. E., Long, J. C., & Sokal, R. R. (1986). Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Systematic Zoology, 35, 627–632.
Soininen, J., McDonald, R., & Hillebrand, H. (2007). The distance decay of similarity in ecological communities. Ecography, 30, 3–12.
Steinbauer, M. J., Dolos, K., Reineking, B., & Beierkuhnlein, C. (2012). Current measures for distance decay in similarity of species composition are influenced by study extent and grain size. Global Ecology and Biogeography, 21, 1203–1212. doi:10.1111/j.1466-8238.2012.00772.x.
Stevens, G. C. (1989). The latitudinal gradient in geographical range: How so many species coexist in the tropics. American Naturalist, 133, 240–256.
Tosi, A. J., Detwiler, K. M., & Disotell, T. R. (2005). X-chromosomal window into the evolutionary history of the guenons (Primates : Cercopithecini). Molecular Phylogenetics and Evolution, 36, 58–66.
Tuomisto, H., Ruokolainen, L., & Ruokolainen, K. (2012). Modelling niche and neutral dynamics: On the ecological interpretation of variation partitioning results. Ecography, 35, 961–971.
Vavrek, M. J. (2011). Fossil: palaeoecological and palaeogeographical analysis tools. Palaeontologia Electronica, 14:1T. http://palaeo-electronica.org/2011_1/238/index.html. Accessed 1 Oct 2013.
Weir, J. T., & Schluter, D. (2007). The latitudinal gradient in recent speciation and extinction rates of birds and mammals. Science, 315, 1574–1576.
Whitmee, S., & Orme, C. D. L. (2013). Predicting dispersal distance in mammals: a traitbased approach. Journal of Animal Ecology, 82(1), 211–221.
Wiens, J. J., & Donoghue, M. J. (2004). Historical biogeography, ecology and species richness. Trends in Ecology & Evolution, 19, 639–644.
Acknowledgments
We thank Joanna Setchell for the invitation to contribute to this International Journal of Primatology special issue following the 2013 American Association of Physical Anthropologists (AAPA) symposium on primate communities and for editing this paper; Jillian DeBenny and Joshua Kohn for African primate data compilation; Catherine Graham, Sandy Harcourt, Marcel Rejmánek, Kelly Stewart, Katie Feilen, Nicole Sharp, Julie Linden, Dena Clink, and Jay Read for discussion; and two anonymous reviewers for comments that improved this manuscript. This work was supported by University of California Davis fellowships to L. Beaudrot from the Graduate Group in Ecology and the Office of Graduate Studies.
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Species data references (Appendix S1), locations of sites included and excluded from the study (Appendix S2), the cluster analysis dendrogram (Appendix S3), and partial Mantel test results with an alternative similarity index (βsim index; Appendix S4) are available online. (DOCX 214 kb)
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Beaudrot, L., Kamilar, J.M., Marshall, A.J. et al. African Primate Assemblages Exhibit a Latitudinal Gradient in Dispersal Limitation. Int J Primatol 35, 1088–1104 (2014). https://doi.org/10.1007/s10764-014-9773-5
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DOI: https://doi.org/10.1007/s10764-014-9773-5