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Seed dispersal syndromes in the Madagascan flora: the unusual importance of primates

  • Aurélie Albert-Daviaud (a1), Sarah Perillo (a1) and Wolfgang Stuppy (a1)

Madagascar is one of the most threatened biodiversity hotspots, and protection of its biodiversity is becoming increasingly urgent as deforestation of the island continues. For the long-term success of conservation efforts it is essential that key ecological processes, such as seed dispersal, are protected and restored. Therefore, the identification of ecological gaps is a vital task. For Madagascar, only little is known about plant–animal interactions, and traditional methods of ecological research are too time-consuming to provide crucial information about breakdowns in these interactions. To identify likely dispersal gaps we therefore used a theoretical approach to analyse plant–disperser interactions in Madagascar. We used data science tools to impute missing data on relevant plant traits to subsequently predict the most likely dispersal agents for each of Madagascar's endemic plant species. We found that 38% of the endemic species (N = 8,784) are endozoochorous, and among these 26–41% display a primate syndrome and 17–19% a bird syndrome (depending on the definition of syndromes). This lower percentage of endozoochorous species and higher percentage of species with a primate syndrome in Madagascar compared to other tropical areas reflects the unusual disperser guild on the island. Only five bird species but 20 lemur species are frugivorous, and 16 of those lemur species are currently threatened with extinction. The disappearance of frugivorous lemurs would significantly change the vegetation dynamics of Madagascar's ecosystems, and a high proportion of Madagascar's endemic plants would enter an extinction vortex.

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Akande, O.M. (2015) A comparison of multiple imputation methods for categorical data. MSc thesis. Duke University, Durham, USA.
Ali, J.R. & Krause, D.W. (2011) Late Cretaceous bioconnections between Indo-Madagascar and Antarctica: refutation of the Gunnerus Ridge causeway hypothesis. Journal of Biogeography, 38, 18551872.
Ambler, G., Omar, R.Z. & Royston, P. (2007) A comparison of imputation techniques for handling missing predictor values in a risk model with a binary outcome. Statistical Methods in Medical Research, 16, 277298.
Andriantsaralaza, S., Pedrono, M., Tassin, J., Edmond, R. & Danthu, P. (2010) Baobabs de Madagascar: un anachronisme de la dispersion? Bois et Forêts des Tropiques, 306, 715.
Armesto, J.J. & Rozzi, R. (1989) Seed dispersal syndromes in the rain forest of Chiloe: evidence for the importance of biotic dispersal in a temperate rain forest. Journal of Biogeography, 16, 219226.
Bleher, B. & Böhning-Gaese, K. (2001) Consequences of frugivore diversity for seed dispersal, seedling establishment and the spatial pattern of seedlings and trees. Oecologia, 129, 385394.
Bodner, T.E. (2008) What improves with increased missing data imputations? Structural Equation Modeling, 15, 651675.
Bollen, A. & Elsacker, L.V. (2002) Feeding ecology of Pteropus rufus (Pteropodidae) in the littoral forest of Sainte Luce, SE Madagascar. Acta Chiropterologica, 4, 3347.
Bollen, A., Elsacker, L.V. & Ganzhorn, J.U. (2004) Tree dispersal strategies in the littoral forest of Sainte Luce (SE-Madagascar). Oecologia, 139, 604616.
Bolmgren, K. & Eriksson, O. (2005) Fleshy fruits – origins, niche shifts, and diversification. Oikos, 109, 255272.
Bond, W.J., Silander, J.A. Jr, Ranaivonasy, J. & Ratsirarson, J. (2008) The antiquity of Madagascar's grasslands and the rise of C4 grassy biomes. Journal of Biogeography, 35, 17431758.
Brooks, T.M., Mittermeier, R.A., da Fonseca, G.A.B., Gerlach, J., Hoffmann, M., Lamoreux, J.F. et al. (2006) Global biodiversity conservation priorities. Science, 313, 5861.
Buerki, S., Devey, D.S., Callmander, M.W., Phillipson, P.B. & Forest, F. (2013) Spatio-temporal history of the endemic genera of Madagascar. Botanical Journal of the Linnean Society, 171, 304329.
Bunney, K. (2014) Seed dispersal in South African trees, with a focus on the megafaunal fruit and their dispersal agents. MSc thesis. University of Cape Town, South Africa.
Burney, D.A., Burney, L.P., Godfrey, L.R., Jungers, W.L., Goodman, S.M., Wright, H.T. & Jull, A.J.T. (2004) A chronology for late prehistoric Madagascar. Journal of Human Evolution, 47, 2563.
Callmander, M.W., Phillipson, P.B., Schatz, G.E., Andriambololonera, S., Rabarimanarivo, M., Rakotonirina, N. et al. (2011) The endemic and non-endemic vascular flora of Madagascar updated. Plant Ecology and Evolution, 144, 121125.
Caughlin, T.T., Ferguson, J.M., Lichstein, J.W., Zuidema, P.A., Bunyavejchewin, S. & Levey, D.J. (2014) Loss of animal seed dispersal increases extinction risk in a tropical tree species due to pervasive negative density dependence across life stages. Proceedings of the Royal Society of London B, 282, 20142095.
Cornet, A. (1973) Carte bioclimatique de Madagascar. Office de la recherche scientifique et technique outre mer.
Crowley, B.E. (2010) A refined chronology of prehistoric Madagascar and the demise of the megafauna. Quaternary Science Reviews, 29, 25912603.
Crowley, B.E. & Samonds, K.E. (2013) Stable carbon isotope values confirm a recent increase in grasslands in northwestern Madagascar. The Holocene, 23, 10661073.
Deng, Y., Chang, C., Ido, M.S. & Long, Q. (2016) Multiple imputation for general missing data patterns in the presence of high-dimensional data. Scientific Reports, 6, 21689.
Dewar, R.E. & Richard, A.F. (2007) Evolution in the hypervariable environment of Madagascar. Proceedings of the National Academy of Sciences of the United States of America, 104, 1372313727.
Federman, S., Sinnott-Armstrong, M., Baden, A.L., Chapman, C.A., Daly, D.C., Richard, A.R. et al. (2017) The paucity of frugivores in Madagascar may not be due to unpredictable temperatures or fruit resources. PLoS ONE, 12(1), e0168943.
Fleming, T.H., Breitwisch, R. & Whitesides, G.H. (1987) Patterns of tropical vertebrate frugivore diversity. Annual Review of Ecology and Systematics, 18, 91109.
Ganzhorn, J.U., Arrigo-Nelson, S., Boinski, S., Bollen, A., Carrai, V., Derby, A. et al. (2009) Possible fruit protein effects on primate communities in Madagascar and the Neotropics. PLoS ONE, 4(12), e8253.
Gautier-Hion, A., Duplantier, J.-M., Quris, R., Feer, F., Sourd, C., Decoux, J.-P. et al. (1985) Fruit characters as a basis of fruit choice and seed dispersal in a tropical forest vertebrate community. Oecologia, 65, 324337.
Giorgi, R., Belot, A., Gaudart, J., Launoy, G. & the French Network of Cancer Registries FRANCIM (2008) The performance of multiple imputation for missing covariate data within the context of regression relative survival analysis. Statistics in Medicine, 27, 63106331.
Godfrey, L.R., Jungers, W.L., Schwartz, G.T. & Irwin, M.T. (2008) Ghosts and orphans: Madagascar's vanishing ecosystems. In Elwyn Simons: A Search for Origins (eds Fleagle, J.G. & Gilbert, C.C.), pp. 361395. Springer, New York, USA.
Godfrey, L.R., Jungers, W.L., Simons, E.L., Chatrath, P.S. & Rakotosamimanana, B. (1999) Past and present distributions of lemurs in Madagascar. In New Directions in Lemur Studies (eds Rakotosamimanana, B., Rasamimanana, H., Ganzhorn, J.U. & Goodman, S.M.), pp. 1953. Kluwer Academic/Plenum Publishers, New York, USA.
Goodman, S.M. & Benstead, J.P. (2003) The Natural History of Madagascar. The University of Chicago Press, Chicago, USA, and London, UK.
Goodman, S.M. & Benstead, J.P. (2005) Updated estimates of biotic diversity and endemism for Madagascar. Oryx, 39, 7377.
Goodman, S.M. & Ganzhorn, J.U. (1997) Rarity of figs (Ficus) on Madagascar and its relationship to a depauperate frugivore community. Revue d'Ecologie (Terre et Vie), 52, 321329.
Graham, J.W., Olchowski, A.E. & Gilreath, T.D. (2007) How many imputations are really needed? Some practical clarifications of multiple imputation theory. Prevention Science, 8, 206213.
Guimarães, P.R. Jr, Galetti, M. & Jordano, P. (2008) Seed dispersal anachronisms: rethinking the fruits extinct megafauna ate. PLoS ONE, 3(3), e1745.
Hardt, J., Herke, M., Brian, T. & Laubach, W. (2013) Multiple imputation of missing data: a simulation study on a binary response. Open Journal of Statistics, 3, 370378.
Herrera, C.M. (2002) Seed dispersal by vertebrates. In Plant−Animal Interactions: An Evolutionary Approach (eds Herrera, C.M. & Pellmyr, O.), pp. 185208. Blackwell Science, Oxford, UK.
Hinchliff, C.E., Smith, S.A., Allman, J.F., Burleigh, J.G., Chaudhary, R., Coghill, L.M. et al. (2015) Synthesis of phylogeny and taxonomy into a comprehensive tree of life. Proceedings of the National Academy of Sciences of the United States of America, 112, 1276412769.
Howe, H.F. (2016) Making dispersal syndromes and networks useful in tropical conservation and restoration. Global Ecology and Conservation, 6, 152178.
Howe, H.F. & Smallwood, J. (1982) Ecology of seed dispersal. Annual Review of Ecology and Systematics, 13, 201228.
Hughes, L., Dunlop, M., French, K., Leishman, M.R., Rice, B., Rodgerson, L. & Westoby, M. (1994) Predicting dispersal spectra: a minimal set of hypotheses based on plant attributes. Journal of Ecology, 82, 933950.
Hutcheon, J.M. (2003) Frugivory by Malagasy bats. In The Natural History of Madagascar (eds Goodman, S.M. & Benstead, J.P.), pp. 12051207. The University of Chicago Press, Chicago, USA, and London, UK.
IUCN (2015) The IUCN Red List of Threatened Species v. 2015-4. Http:// [accessed 19 November 2015].
Janson, C.H. (1983) Adaptation of fruit morphology to dispersal agents in a Neotropical forest. Science, 219, 187189.
Janzen, D.H. & Martin, P.S. (1982) Neotropical anachronisms: the fruits the gomphotheres ate. Science, 215, 1927.
Jordano, P. (2000) Fruits and frugivory. In Seeds: The Ecology of Regeneration in Plant Communities (ed. Fenner, M.), pp. 125166. CABI, Wallingford, UK.
Jordano, P., Forget, P.-M., Lambert, J.E., Böhning-Gaese, K., Traveset, A. & Wright, S.J. (2011) Frugivores and seed dispersal: mechanisms and consequences for biodiversity of a key ecological interaction. Biology Letters, 7, 321323.
Kuhlmann, M. & Ribeiro, J.F. (2016) Fruits and frugivores of the Brazilian Cerrado: ecological and phylogenetic considerations. Acta Botanica Brasilica, 30, 495507.
Lomáscolo, S.B. & Schaefer, H.M. (2010) Signal convergence in fruits: a result of selection by frugivores? Journal of Evolutionary Biology, 23, 614624.
Lorts, C.M., Briggeman, T. & Sang, T. (2008) Evolution of fruit types and seed dispersal: a phylogenetic and ecological snapshot. Journal of Systematics and Evolution, 46, 396404.
Madagascar Catalogue (2013) Catalogue of the Vascular Plants of Madagascar. Missouri Botanical Garden, St. Louis, USA, & Antananarivo, Madagascar.
Mangiafico, S. (2016) rcompanion: Functions to support extension education program evaluation. R package version 1.2.0. Https://
Mercier, J.-L. & Wilmé, L. (2013) The Eco-Geo-Clim model: explaining Madagascar's endemism. Madagascar Conservation & Development, 8, 6368.
Mittermeier, C.G., Louis, E.E., Richardson, M., Schwitzer, C., Langrand, O., Rylands, A.B. et al. (2010) Lemurs of Madagascar. Conservation International, Arlington, USA.
Muscarella, R. & Fleming, T.H. (2007) The role of frugivorous bats in tropical forest succession. Biological Reviews, 82, 573590.
Osuri, A.M., Ratnam, J., Varma, V., Alvarez-Loayza, P., Astaiza, J.H., Bradford, M. et al. (2016) Contrasting effects of defaunation on aboveground carbon storage across the global tropics. Nature Communications, 7, 11351.
Penone, C., Davidson, A.D., Shoemaker, K.T., DiMarco, M., Rondinini, C., Brooks, T.M. et al. (2014) Imputation of missing data in life-history trait datasets: which approach performs the best? Methods in Ecology and Evolution, 5, 961970.
Picot, M., Jenkins, R.K.B., Ramilijaona, O., Racey, P.A. & Carrière, S.M. (2007) The feeding ecology of Eidolon dupreanum (Pteropodidae) in eastern Madagascar. African Journal of Ecology, 45, 645650.
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team (2016) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-128,
Razafindratsima, O.H.F.E. (2015) Nonrandom seed dispersal by lemur frugivores: mechanism, patterns and impacts. PhD thesis. Rice University, Houston, USA.
R Development Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Rubin, D.B. (1987) Multiple Imputation for Nonresponse in Surveys. John Wiley & Sons, New York, USA.
Spjut, R.W. (1994) A Systematic Treatment of Fruit Types. The New York Botanical Garden Press, New York, USA.
Terborgh, J., Nuñez-Iturri, G., Pitman, N.C.A., Cornejo Valverde, F.H., Alvarez, P., Swamy, V. et al. (2008) Tree recruitment in an empty forest. Ecology, 89, 17571768.
Turner, I.M. (2001) The Ecology of Trees in the Tropical Rain Forest. Cambridge University Press, Cambridge, UK.
van Buuren, S. & Groothuis-Oudshoorn, K. (2011) mice: Multivariate Imputation by Chained Equations in R. Journal of Statistical Software, 45, 167.
van der Pijl, L. (1982) Principles of Dispersal in Higher Plants. Springer-Verlag, Berlin, Germany.
Voigt, F.A., Bleher, B., Fietz, J., Ganzhorn, J.U., Schwab, D. & Böhning-Gaese, K. (2004) A comparison of morphological and chemical fruit traits between two sites with different frugivore assemblages. Oecologia, 141, 94104.
Vorontsova, M.S., Besnard, G., Forest, F., Malakasi, P., Moat, J., Clayton, W.D. et al. (2016) Madagascar's grasses and grasslands: anthropogenic or natural? Proceedings of the Royal Society B, 20152262.
White, I.R., Royston, P. & Wood, A.M. (2011) Multiple imputation using chained equations: issues and guidance for practice. Statistics in Medicine, 30, 377399.
Willson, M. & Traveset, A. (2000) The ecology of seed dispersal. In Seeds: The Ecology of Regeneration in Plant Communities (ed. Fenner, M.), pp. 85110. CABI, Wallingford, UK.
Willson, M.F., Irvine, A.K. & Walsh, N.G. (1989) Vertebrate dispersal syndromes in some Australian and New Zealand plant communities, with geographic comparisons. Biotropica, 21, 133147.
Willson, M.F., Rice, B.L. & Westoby, M. (1990) Seed dispersal spectra: a comparison of temperate plant communities. Journal of Vegetation Science, 1, 547562.
Wright, P. (1999) Lemur traits and Madagascar ecology: coping with an island environment. Yearbook of Physical Anthropology, 42, 3172.
Yoder, A.D. & Nowak, M.D. (2006) Has vicariance or dispersal been the predominant biogeographic force in Madagascar? Only time will tell. Annual Review of Ecology, Evolution, and Systematics, 37, 405431.
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