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Research Article

Implications of lemuriform extinctions for the Malagasy flora

Sarah Federman, Alex Dornburg, Douglas C. Daly, Alexander Downie, George H. Perry, Anne D. Yoder, Eric J. Sargis, Alison F. Richard, Michael J. Donoghue, and Andrea L. Baden
PNAS first published April 11, 2016; https://doi.org/10.1073/pnas.1523825113
Sarah Federman
aDepartment of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520;
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  • For correspondence: sarah.federman@yale.edu
Alex Dornburg
bNorth Carolina Museum of Natural Sciences, Raleigh, NC 27601;
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Douglas C. Daly
cInstitute of Systematic Botany, New York Botanical Garden, Bronx, NY 10458;
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Alexander Downie
aDepartment of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520;
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George H. Perry
dDepartment of Anthropology, Pennsylvania State University, University Park, PA 16802;
eDepartment of Biology, Pennsylvania State University, University Park, PA 16802;
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Anne D. Yoder
fDepartment of Biology, Duke University, Durham, NC 27708;
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Eric J. Sargis
gDepartment of Anthropology, Yale University, New Haven, CT 06520;
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Alison F. Richard
gDepartment of Anthropology, Yale University, New Haven, CT 06520;
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Michael J. Donoghue
aDepartment of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520;
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Andrea L. Baden
hDepartment of Anthropology, Hunter College, New York, NY 10065;
iDepartment of Anthropology, The Graduate Center, City University of New York, New York, NY 10065;
jThe New York Consortium in Evolutionary Primatology, New York, NY 10065
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  1. Edited by Rodolfo Dirzo, Stanford University, Stanford, CA, and approved March 10, 2016 (received for review December 4, 2015)

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Significance

Madagascar is a conservation priority because of its unique and threatened biodiversity. Lemurs, by acting as seed dispersers, are essential to maintaining healthy and diverse forests on the island. However, in the past few thousand years, at least 17 lemur species, many of which were inferred seed dispersers, have gone extinct. We outline the substantial impact that these extinctions have likely had on Malagasy forests by comparing the gape sizes and diets of living and extinct lemurs to identify large-seeded Malagasy plants that appear to be without extant animal dispersers. Additionally, we identify living lemurs that are endangered yet occupy unique and essential dispersal niches. This information can inform conservation initiatives targeting the protection and restoration of these vulnerable ecosystems.

Abstract

Madagascar’s lemurs display a diverse array of feeding strategies with complex relationships to seed dispersal mechanisms in Malagasy plants. Although these relationships have been explored previously on a case-by-case basis, we present here the first comprehensive analysis of lemuriform feeding, to our knowledge, and its hypothesized effects on seed dispersal and the long-term survival of Malagasy plant lineages. We used a molecular phylogenetic framework to examine the mode and tempo of diet evolution, and to quantify the associated morphological space occupied by Madagascar’s lemurs, both extinct and extant. Using statistical models and morphometric analyses, we demonstrate that the extinction of large-bodied lemurs resulted in a significant reduction in functional morphological space associated with seed dispersal ability. These reductions carry potentially far-reaching consequences for Malagasy ecosystems, and we highlight large-seeded Malagasy plants that appear to be without extant animal dispersers. We also identify living lemurs that are endangered yet occupy unique and essential dispersal niches defined by our morphometric analyses.

  • anachronism
  • extinction
  • lemurs
  • Madagascar
  • seed dispersal

Footnotes

  • ↵1To whom correspondence should be addressed. Email: sarah.federman{at}yale.edu.
  • Author contributions: S.F. and A.L.B. designed research; S.F., A. Dornburg, D.C.D., A. Downie, G.H.P., and A.L.B. performed research; S.F. and A. Dornburg analyzed data; and S.F., A. Dornburg, D.C.D., A. Downie, G.H.P., A.D.Y., E.J.S., A.F.R., M.J.D., and A.L.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: Phylogenetic and morphological datasets used in this study, along with any associated R scripts, are available in the Zenodo repository, https://zenodo.org/ (DOI 10.5281/zenodo.45471).

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1523825113/-/DCSupplemental.

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Lemuriform extinctions and the Malagasy flora
Sarah Federman, Alex Dornburg, Douglas C. Daly, Alexander Downie, George H. Perry, Anne D. Yoder, Eric J. Sargis, Alison F. Richard, Michael J. Donoghue, Andrea L. Baden
Proceedings of the National Academy of Sciences Apr 2016, 201523825; DOI: 10.1073/pnas.1523825113

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Lemuriform extinctions and the Malagasy flora
Sarah Federman, Alex Dornburg, Douglas C. Daly, Alexander Downie, George H. Perry, Anne D. Yoder, Eric J. Sargis, Alison F. Richard, Michael J. Donoghue, Andrea L. Baden
Proceedings of the National Academy of Sciences Apr 2016, 201523825; DOI: 10.1073/pnas.1523825113
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Proceedings of the National Academy of Sciences: 118 (8)
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