Environmental DNA from archived leaves reveals widespread temporal turnover and biotic homogenization in forest arthropod communities

  1. Henrik Krehenwinkel  Is a corresponding author
  2. Sven Weber
  3. Rieke Broekmann
  4. Anja Melcher
  5. Julian Hans
  6. Rüdiger Wolf
  7. Axel Hochkirch
  8. Susan Rachel Kennedy
  9. Jan Koschorrek
  10. Sven Künzel
  11. Christoph Müller
  12. Rebecca Reztlaff
  13. Diana Teubner
  14. Sonja Schanzer
  15. Roland Klein
  16. Martin Paulus
  17. Thomas Udelhoven
  18. Michael Veith
  1. University of Trier, Germany
  2. German Federal Environment Agency, Germany
  3. Max Planck Institute for Evolutionary Biology, Germany
  4. Ludwig Maximilians University, Germany

Abstract

A major limitation of current reports on insect declines is the lack of standardized, long-term, and taxonomically broad time series. Here, we demonstrate the utility of environmental DNA from archived leaf material to characterize plant-associated arthropod communities. We base our work on several multi-decadal leaf time series from tree canopies in four land use types, which were sampled as part of a long-term environmental monitoring program across Germany. Using these highly standardized and well-preserved samples, we analyze temporal changes in communities of several thousand arthropod species belonging to 23 orders using metabarcoding and quantitative PCR. Our data do not support widespread declines of α-diversity or genetic variation within sites. Instead, we find a gradual community turnover, which results in temporal and spatial biotic homogenization, across all land use types and all arthropod orders. Our results suggest that insect decline is more complex than mere α-diversity loss, but can be driven by β-diversity decay across space and time.

Data availability

All raw reads are available in the Dryad Digital Repository (https://doi.org/10.5061/dryad.x0k6djhmp).The OTU table with metadata and qPCR resullts has been uploaded as Supplementary Material

The following data sets were generated

Article and author information

Author details

  1. Henrik Krehenwinkel

    University of Trier, Trier, Germany
    For correspondence
    krehenwinkel@uni-trier.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5069-8601
  2. Sven Weber

    University of Trier, Trier, Germany
    Competing interests
    The authors declare that no competing interests exist.
  3. Rieke Broekmann

    University of Trier, Trier, Germany
    Competing interests
    The authors declare that no competing interests exist.
  4. Anja Melcher

    University of Trier, Trier, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Julian Hans

    University of Trier, Trier, Germany
    Competing interests
    The authors declare that no competing interests exist.
  6. Rüdiger Wolf

    University of Trier, Trier, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-8144-5954
  7. Axel Hochkirch

    University of Trier, Trier, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Susan Rachel Kennedy

    University of Trier, Trier, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Jan Koschorrek

    German Federal Environment Agency, Berlin, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Sven Künzel

    Department Evolutionary Genetics, Max Planck Institute for Evolutionary Biology, Plön, Germany
    Competing interests
    The authors declare that no competing interests exist.
  11. Christoph Müller

    Ludwig Maximilians University, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  12. Rebecca Reztlaff

    University of Trier, Trier, Germany
    Competing interests
    The authors declare that no competing interests exist.
  13. Diana Teubner

    University of Trier, Trier, Germany
    Competing interests
    The authors declare that no competing interests exist.
  14. Sonja Schanzer

    Ludwig Maximilians University, Munich, Germany
    Competing interests
    The authors declare that no competing interests exist.
  15. Roland Klein

    University of Trier, Trier, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-8735-0393
  16. Martin Paulus

    University of Trier, Trier, Germany
    Competing interests
    The authors declare that no competing interests exist.
  17. Thomas Udelhoven

    University of Trier, Trier, Germany
    Competing interests
    The authors declare that no competing interests exist.
  18. Michael Veith

    University of Trier, Trier, Germany
    Competing interests
    The authors declare that no competing interests exist.

Funding

No external funding was received for this work.

Copyright

© 2022, Krehenwinkel et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 2,330
    views
  • 366
    downloads
  • 14
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Henrik Krehenwinkel
  2. Sven Weber
  3. Rieke Broekmann
  4. Anja Melcher
  5. Julian Hans
  6. Rüdiger Wolf
  7. Axel Hochkirch
  8. Susan Rachel Kennedy
  9. Jan Koschorrek
  10. Sven Künzel
  11. Christoph Müller
  12. Rebecca Reztlaff
  13. Diana Teubner
  14. Sonja Schanzer
  15. Roland Klein
  16. Martin Paulus
  17. Thomas Udelhoven
  18. Michael Veith
(2022)
Environmental DNA from archived leaves reveals widespread temporal turnover and biotic homogenization in forest arthropod communities
eLife 11:e78521.
https://doi.org/10.7554/eLife.78521

Share this article

https://doi.org/10.7554/eLife.78521

Further reading

    1. Ecology
    Ming-Qiang Wang, Shi-Kun Guo ... Chao-Dong Zhu
    Research Article

    Environmental factors can influence ecological networks, but these effects are poorly understood in the realm of the phylogeny of host-parasitoid interactions. Especially, we lack a comprehensive understanding of the ways that biotic factors, including plant species richness, overall community phylogenetic and functional composition of consumers, and abiotic factors such as microclimate, determine host-parasitoid network structure and host-parasitoid community dynamics. To address this, we leveraged a 5-year dataset of trap-nesting bees and wasps and their parasitoids collected in a highly controlled, large-scale subtropical tree biodiversity experiment. We tested for effects of tree species richness, tree phylogenetic, and functional diversity, and species and phylogenetic composition on species and phylogenetic diversity of both host and parasitoid communities and the composition of their interaction networks. We show that multiple components of tree diversity and canopy cover impacted both, species and phylogenetic composition of hosts and parasitoids. Generally, phylogenetic associations between hosts and parasitoids reflected nonrandomly structured interactions between phylogenetic trees of hosts and parasitoids. Further, host-parasitoid network structure was influenced by tree species richness, tree phylogenetic diversity, and canopy cover. Our study indicates that the composition of higher trophic levels and corresponding interaction networks are determined by plant diversity and canopy cover, especially via trophic links in species-rich ecosystems.

    1. Ecology
    Itai Bloch, David Troupin ... Nir Sapir
    Research Article

    Optimal foraging theory posits that foragers adjust their movements based on prey abundance to optimize food intake. While extensively studied in terrestrial and marine environments, aerial foraging has remained relatively unexplored due to technological limitations. This study, uniquely combining BirdScan-MR1 radar and the Advanced Tracking and Localization of Animals in Real-Life Systems biotelemetry system, investigates the foraging dynamics of Little Swifts (Apus affinis) in response to insect movements over Israel’s Hula Valley. Insect movement traffic rate (MoTR) substantially varied across days, strongly influencing swift movement. On days with high MoTR, swifts exhibited reduced flight distance, increased colony visit rate, and earlier arrivals at the breeding colony, reflecting a dynamic response to prey availability. However, no significant effects were observed in total foraging duration, flight speed, or daily route length. Notably, as insect abundance increased, inter-individual distances decreased. These findings suggest that Little Swifts optimize their foraging behavior in relation to aerial insect abundance, likely influencing reproductive success and population dynamics. The integration of radar technology and biotelemetry systems provides a unique perspective on the interactions between aerial insectivores and their prey, contributing to a comprehensive understanding of optimal foraging strategies in diverse environments.