Tree species and genetic diversity increase productivity via functional diversity and trophic feedbacks

  1. Ting Tang
  2. Naili Zhang
  3. Franca J Bongers
  4. Michael Staab
  5. Andreas Schuldt
  6. Felix Fornoff
  7. Hong Lin
  8. Jeannine Cavender-Bares
  9. Andrew L Hipp
  10. Shan Li
  11. Yu Liang
  12. Baocai Han
  13. Alexandra-Maria Klein
  14. Helge Bruelheide
  15. Walter Durka
  16. Bernhard Schmid  Is a corresponding author
  17. Keping Ma  Is a corresponding author
  18. Xiaojuan Liu  Is a corresponding author
  1. Chinese Academy of Sciences, China
  2. Beijing Forestry University, China
  3. Technical University Darmstadt, Germany
  4. Georg-August-University Göttingen, Germany
  5. University of Freiburg, Germany
  6. Nanjing Xiaozhuang University, China
  7. University of Minnesota, United States
  8. Morton Arboretum, United States
  9. Martin Luther University Halle-Wittenberg, Germany
  10. Helmholtz Centre for Environmental Research, Germany
  11. University of Zurich, Switzerland

Abstract

Addressing global biodiversity loss requires an expanded focus on multiple dimensions of biodiversity. While most studies have focused on the consequences of plant interspecific diversity, our mechanistic understanding of how genetic diversity within plant species affects plant productivity remains limited. Here, we use a tree species × genetic diversity experiment to disentangle the effects of species diversity and genetic diversity, and how they are related to tree functional diversity and trophic feedbacks. We found that tree species diversity increased tree productivity via increased tree functional diversity, reduced soil fungal diversity and marginally reduced herbivory. The effects of tree genetic diversity on productivity via functional diversity and soil fungal diversity were negative in monocultures but positive in the mixture of the four tree species tested. Given the complexity of interactions between species and genetic diversity, tree functional diversity and trophic feedbacks on productivity, we suggest that both tree species and genetic diversity should be considered in afforestation.

Data availability

All numerical data were used to generate the figures that have been deposited in Dryad.

The following data sets were generated

Article and author information

Author details

  1. Ting Tang

    Institute of Botany, Chinese Academy of Sciences, Beijing, China
    Competing interests
    No competing interests declared.
  2. Naili Zhang

    College of Forestry, Beijing Forestry University, Beijing, China
    Competing interests
    No competing interests declared.
  3. Franca J Bongers

    Institute of Botany, Chinese Academy of Sciences, Beijing, China
    Competing interests
    No competing interests declared.
  4. Michael Staab

    Ecological Networks, Technical University Darmstadt, Darmstadt, Germany
    Competing interests
    No competing interests declared.
  5. Andreas Schuldt

    Forest Nature Conservation, Georg-August-University Göttingen, Göttingen, Germany
    Competing interests
    No competing interests declared.
  6. Felix Fornoff

    Nature Conservation and Landscape Ecology, University of Freiburg, Freiburg, Germany
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0446-7153
  7. Hong Lin

    Institute of Applied Ecology, Nanjing Xiaozhuang University, Nanjing, China
    Competing interests
    No competing interests declared.
  8. Jeannine Cavender-Bares

    Department of Ecology, Evolution, and Behavior, University of Minnesota, St. Paul, United States
    Competing interests
    No competing interests declared.
  9. Andrew L Hipp

    Morton Arboretum, Lisle, United States
    Competing interests
    No competing interests declared.
  10. Shan Li

    Institute of Botany, Chinese Academy of Sciences, Beijing, China
    Competing interests
    No competing interests declared.
  11. Yu Liang

    Institute of Botany, Chinese Academy of Sciences, Beijing, China
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4259-6028
  12. Baocai Han

    Institute of Botany, Chinese Academy of Sciences, Beijing, China
    Competing interests
    No competing interests declared.
  13. Alexandra-Maria Klein

    Faculty of Environment and Natural Resources, University of Freiburg, Freiburg, Germany
    Competing interests
    No competing interests declared.
  14. Helge Bruelheide

    Institute of Biology, Martin Luther University Halle-Wittenberg, Halle, Germany
    Competing interests
    No competing interests declared.
  15. Walter Durka

    Department of Community Ecology, Helmholtz Centre for Environmental Research, Halle, Germany
    Competing interests
    No competing interests declared.
  16. Bernhard Schmid

    Department of Geography, University of Zurich, Zurich, Switzerland
    For correspondence
    bernhard.schmid@geo.uzh.ch
    Competing interests
    Bernhard Schmid, Reviewing editor, eLife.
  17. Keping Ma

    Institute of Botany, Chinese Academy of Sciences, Beijing, China
    For correspondence
    kpma@ibcas.ac.cn
    Competing interests
    No competing interests declared.
  18. Xiaojuan Liu

    Institute of Botany, Chinese Academy of Sciences, Beijing, China
    For correspondence
    liuxiaojuan06@ibcas.ac.cn
    Competing interests
    No competing interests declared.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9292-4432

Funding

National Natural Science Foundation of China (31870409)

  • Ting Tang
  • Franca J Bongers
  • Xiaojuan Liu

Strategic Priority Research Program of the Chinese Academy of Sciences (XDB31000000)

  • Naili Zhang
  • Xiaojuan Liu

National Natural Science Foundation of China (32161123003)

  • Naili Zhang
  • Yu Liang
  • Keping Ma
  • Xiaojuan Liu

Younth Innovation Promotion Association CAS (2019082)

  • Xiaojuan Liu

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. David A. Donoso, Escuela Politécnica Nacional, Ecuador

Version history

  1. Received: March 17, 2022
  2. Preprint posted: March 28, 2022 (view preprint)
  3. Accepted: November 14, 2022
  4. Accepted Manuscript published: November 29, 2022 (version 1)
  5. Version of Record published: December 15, 2022 (version 2)

Copyright

© 2022, Tang 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

  • 1,721
    views
  • 407
    downloads
  • 10
    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. Ting Tang
  2. Naili Zhang
  3. Franca J Bongers
  4. Michael Staab
  5. Andreas Schuldt
  6. Felix Fornoff
  7. Hong Lin
  8. Jeannine Cavender-Bares
  9. Andrew L Hipp
  10. Shan Li
  11. Yu Liang
  12. Baocai Han
  13. Alexandra-Maria Klein
  14. Helge Bruelheide
  15. Walter Durka
  16. Bernhard Schmid
  17. Keping Ma
  18. Xiaojuan Liu
(2022)
Tree species and genetic diversity increase productivity via functional diversity and trophic feedbacks
eLife 11:e78703.
https://doi.org/10.7554/eLife.78703

Share this article

https://doi.org/10.7554/eLife.78703

Further reading

    1. Ecology
    2. Evolutionary Biology
    Chunxiao Li, Tao Deng ... Shiqi Wang
    Research Article

    The long-trunked elephantids underwent a significant evolutionary stage characterized by an exceptionally elongated mandible. The initial elongation and subsequent regression of the long mandible, along with its co-evolution with the trunk, present an intriguing issue that remains incompletely understood. Through comparative functional and eco-morphological investigations, as well as feeding preference analysis, we reconstructed the feeding behavior of major groups of longirostrine elephantiforms. In the Platybelodon clade, the rapid evolutionary changes observed in the narial region, strongly correlated with mandible and tusk characteristics, suggest a crucial evolutionary transition where feeding function shifted from the mandible to the trunk, allowing proboscideans to expand their niches to more open regions. This functional shift further resulted in elephantids relying solely on their trunks for feeding. Our research provides insights into how unique environmental pressures shape the extreme evolution of organs, particularly in large mammals that developed various peculiar adaptations during the late Cenozoic global cooling trends.

    1. Ecology
    Shuai-Shuai Zhang, Pei-Chao Wang ... Chen-Zhu Wang
    Research Article

    Almost all herbivorous insects feed on plants and use sucrose as a feeding stimulant, but the molecular basis of their sucrose reception remains unclear. Helicoverpa armigera as a notorious crop pest worldwide mainly feeds on reproductive organs of many plant species in the larval stage, and its adult draws nectar. In this study, we determined that the sucrose sensory neurons located in the contact chemosensilla on larval maxillary galea were 100–1000 times more sensitive to sucrose than those on adult antennae, tarsi, and proboscis. Using the Xenopus expression system, we discovered that Gr10 highly expressed in the larval sensilla was specifically tuned to sucrose, while Gr6 highly expressed in the adult sensilla responded to fucose, sucrose and fructose. Moreover, using CRISPR/Cas9, we revealed that Gr10 was mainly used by larvae to detect lower sucrose, while Gr6 was primarily used by adults to detect higher sucrose and other saccharides, which results in differences in selectivity and sensitivity between larval and adult sugar sensory neurons. Our results demonstrate the sugar receptors in this moth are evolved to adapt toward the larval and adult foods with different types and amounts of sugar, and fill in a gap in sweet taste of animals.