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Ant and Mite Diversity Drives Toxin Variation in the Little Devil Poison Frog

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A Letter to the Editor to this article was published on 01 August 2016

An Erratum to this article was published on 01 August 2016

Abstract

Poison frogs sequester chemical defenses from arthropod prey, although the details of how arthropod diversity contributes to variation in poison frog toxins remains unclear. We characterized skin alkaloid profiles in the Little Devil poison frog, Oophaga sylvatica (Dendrobatidae), across three populations in northwestern Ecuador. Using gas chromatography/mass spectrometry, we identified histrionicotoxins, 3,5- and 5,8-disubstituted indolizidines, decahydroquinolines, and lehmizidines as the primary alkaloid toxins in these O. sylvatica populations. Frog skin alkaloid composition varied along a geographical gradient following population distribution in a principal component analysis. We also characterized diversity in arthropods isolated from frog stomach contents and confirmed that O. sylvatica specialize on ants and mites. To test the hypothesis that poison frog toxin variability reflects species and chemical diversity in arthropod prey, we (1) used sequencing of cytochrome oxidase 1 to identify individual prey specimens, and (2) used liquid chromatography/mass spectrometry to chemically profile consumed ants and mites. We identified 45 ants and 9 mites in frog stomachs, including several undescribed species. We also showed that chemical profiles of consumed ants and mites cluster by frog population, suggesting different frog populations have access to chemically distinct prey. Finally, by comparing chemical profiles of frog skin and isolated prey items, we traced the arthropod source of four poison frog alkaloids, including 3,5- and 5,8-disubstituted indolizidines and a lehmizidine alkaloid. Together, the data show that toxin variability in O. sylvatica reflects chemical diversity in arthropod prey.

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Acknowledgments

We are grateful to Jon Clardy, Andrew Murray, and Adam Stuckert for comments on early versions of the manuscript, and Lola Guarderas at Centro Jambatu for logistical support in Ecuador. This work was funded by the Explorers’ Club 2014 Youth Activity Grant to JRM, the Harvard Museum of Comparative Zoology’s Myvanwy M. and George M. Dick Scholarship Fund for Science Students and the Harvard College Research Program to JRM and SNC, and a Bauer Fellowship from Harvard University, the L’Oreal For Women in Science Fellowship, and the William F. Milton Fund from Harvard Medical School to LAO. EET and LAC acknowledge the support of Wikiri and the Saint Louis Zoo.

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Authors and Affiliations

  1. Center for Systems Biology, Harvard University, Cambridge, MA, 02138, USA

    Jenna R. McGugan, Alexandre B. Roland, Stephanie N. Caty & Lauren A. O’Connell

  2. Small Molecule Mass Spectrometry Facility, Harvard University, Cambridge, MA, 02138, USA

    Gary D. Byrd & Sunia A. Trauger

  3. Cambridge Rindge and Latin High School, Cambridge, MA, 02138, USA

    Nisha Kabir

  4. Centro Jambatu de Investigación y Conservación de Anfibios, Fundación Otonga, Quito, Ecuador

    Elicio E. Tapia & Luis A. Coloma

  5. Ikiam, Universidad Regional Amazónica, Muyuna, Tena, Ecuador

    Luis A. Coloma

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  1. Jenna R. McGugan
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Correspondence to Lauren A. O’Connell.

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Jenna R. McGugan and Gary D. Byrd contributed equally to this work

An erratum to this article can be found at http://dx.doi.org/10.1007/s10886-016-0762-3.

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McGugan, J.R., Byrd, G.D., Roland, A.B. et al. Ant and Mite Diversity Drives Toxin Variation in the Little Devil Poison Frog. J Chem Ecol 42, 537–551 (2016). https://doi.org/10.1007/s10886-016-0715-x

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