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Coprolites reveal ecological interactions lost with the extinction of New Zealand birds

Alexander P. Boast, Laura S. Weyrich, Jamie R. Wood, Jessica L. Metcalf, Rob Knight and Alan Cooper
PNAS February 13, 2018. 115 (7) 1546-1551; published ahead of print February 13, 2018. https://doi.org/10.1073/pnas.1712337115
Alexander P. Boast
aAustralian Centre for Ancient DNA, University of Adelaide, Adelaide, SA 5005, Australia;bSchool of Environment, The University of Auckland, Auckland 1142, New Zealand;cLandcare Research, Lincoln 7608, New Zealand;
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  • ORCID record for Alexander P. Boast
  • For correspondence: apboast@gmail.comalan.cooper@adelaide.edu.au
Laura S. Weyrich
aAustralian Centre for Ancient DNA, University of Adelaide, Adelaide, SA 5005, Australia;
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Jamie R. Wood
cLandcare Research, Lincoln 7608, New Zealand;
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Jessica L. Metcalf
dDepartment of Animal Sciences, Colorado State University, Fort Collins, CO 80526;
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Rob Knight
eDepartment of Pediatrics, University of California, San Diego, La Jolla, CA 92093;fDepartment of Computer Science and Engineering, University of California, San Diego, La Jolla, CA 92093;gCenter for Microbiome Innovation, University of California, San Diego, La Jolla, CA 92093
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Alan Cooper
aAustralian Centre for Ancient DNA, University of Adelaide, Adelaide, SA 5005, Australia;
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  • For correspondence: apboast@gmail.comalan.cooper@adelaide.edu.au
  1. Edited by James A. Estes, University of California, Santa Cruz, CA, and approved December 27, 2017 (received for review August 4, 2017)

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Significance

Ancient DNA metabarcoding of coprolites (ancient dung) has greatly improved our ability to investigate the behavior and ecology of extinct species. We use coprolites from extinct New Zealand birds to show how this approach can reveal aspects of dietary behavior, such as the consumption of ectomycorrhizal fungi, and both the distribution and coextinction of parasites. We show how this approach can identify lost ecological interactions, which have key implications for understanding, conserving, and restoring currently threatened ecosystems.

Abstract

Over the past 50,000 y, biotic extinctions and declines have left a legacy of vacant niches and broken ecological interactions across global terrestrial ecosystems. Reconstructing the natural, unmodified ecosystems that preceded these events relies on high-resolution analyses of paleoecological deposits. Coprolites are a source of uniquely detailed information about trophic interactions and the behaviors, gut parasite communities, and microbiotas of prehistoric animal species. Such insights are critical for understanding the legacy effects of extinctions on ecosystems, and can help guide contemporary conservation and ecosystem restoration efforts. Here we use high-throughput sequencing (HTS) of ancient eukaryotic DNA from coprolites to reconstruct aspects of the biology and ecology of four species of extinct moa and the critically endangered kakapo parrot from New Zealand (NZ). Importantly, we provide evidence that moa and prehistoric kakapo consumed ectomycorrhizal fungi, suggesting these birds played a role in dispersing fungi that are key to NZ’s natural forest ecosystems. We also provide the first DNA-based evidence that moa frequently supplemented their broad diets with ferns and mosses. Finally, we also find parasite taxa that provide insight into moa behavior, and present data supporting the hypothesis of coextinction between moa and several parasite species. Our study demonstrates that HTS sequencing of coprolites provides a powerful tool for resolving key aspects of ancient ecosystems and may rapidly provide information not obtainable by conventional paleoecological techniques, such as fossil analyses.

  • ancient DNA
  • metabarcoding
  • coprolites
  • moa
  • New Zealand

Footnotes

  • ↵1To whom correspondence may be addressed. Email: apboast{at}gmail.com or alan.cooper{at}adelaide.edu.au.
  • Author contributions: A.P.B., L.S.W., J.R.W., J.L.M., R.K., and A.C. designed research; A.P.B., L.S.W., J.R.W., and J.L.M. performed research; A.P.B., L.S.W., J.R.W., and J.L.M. analyzed data; and A.P.B., L.S.W., J.R.W., J.L.M., R.K., and A.C. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Data deposition: Raw data and supporting metadata from this study are available on both Qiita, https://qiita.ucsd.edu (study ID 11507) and EBI, https://www.ebi.ac.uk (accession no. ERP106282).

  • See Commentary on page 1411.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1712337115/-/DCSupplemental.

Published under the PNAS license.

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Metabarcoding of coprolites of NZ’s extinct birds
Alexander P. Boast, Laura S. Weyrich, Jamie R. Wood, Jessica L. Metcalf, Rob Knight, Alan Cooper
Proceedings of the National Academy of Sciences Feb 2018, 115 (7) 1546-1551; DOI: 10.1073/pnas.1712337115

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Metabarcoding of coprolites of NZ’s extinct birds
Alexander P. Boast, Laura S. Weyrich, Jamie R. Wood, Jessica L. Metcalf, Rob Knight, Alan Cooper
Proceedings of the National Academy of Sciences Feb 2018, 115 (7) 1546-1551; DOI: 10.1073/pnas.1712337115
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