Aboveground herbivores drive stronger plant species-specific feedback than belowground fungi to regulate tree community assembly

Abstract

Ectomycorrhizal (EcM) tree species often become more dominant than arbuscular mycorrhizal (AM) tree species in temperate forests, but they generally coexist. Theory predicts that ecological feedback mediated by aboveground herbivory and/or belowground microbes could explain these dominance/coexistence patterns. An experimental test of how aboveground/belowground organisms associated with AM/EcM trees mediate ecological feedbacks has been lacking at the community-level. By establishing AM and EcM tree sapling assemblages in mesocosms and then introducing seedlings of each type in a reciprocal planting experiment, we compared seedling performance under varying sapling species (conspecifics, heterospecifics within the same and different mycorrhizal types), using traits that reflect either aboveground herbivory-mediated feedback or belowground fungal-mediated feedback or both. When examining seedling traits that reflect aboveground herbivory-mediated feedbacks (i.e., foliar damage), AM plants tended to experience less foliar damage and EcM plants more damage under conspecific versus heterospecific saplings within the same mycorrhizal types, and aboveground herbivory-mediated feedback was species-specific rather than mycorrhizal type–specific. Conversely, when examining traits that reflect belowground fungal-mediated feedbacks, both AM and EcM plant species often exhibited mycorrhizal type-specific feedbacks (e.g., greater aboveground biomass under the same versus different mycorrhizal-type saplings) rather than species-specific feedbacks. Furthermore, tree species affected by herbivory-mediated feedback were less affected by belowground feedback, indicating that the relative importance of the feedbacks varied among plant species. Analysis of plant-associated organisms verified that the feedback outcomes corresponded with species accumulation of belowground fungi (but not of aboveground herbivores). Thus, aboveground herbivores drive stronger plant species-specific feedback than belowground fungi to regulate temperate tree diversity.

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Data availability

Arthropod data and its taxonomic information are provided as Online Resource Data 1. Fungal ITS sequences have been deposited under accession numbers BioProject PRJDB5467 and DDBJ DRA005499. The fungal community data is available as Appendix Data 2 of a previous publication (Kadowaki et al. 2018).

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Acknowledgements

This work was supported by Next Generation World-Leading Researchers of Cabinet Office, the Japanese Government (GS014), KAKENHI (26711026), JST PRESTO (JPMJPR16Q6) and Human Frontier Science Program (RGP0029/2019) to HT and JSPS Research Fellowship (13J02732) to KK. We thank Kyoto University Botanical Garden for supporting this work, and Hiroyuki Yoshitomi and Naoki Koike for taxonomic assistance. Tomoko Kadowaki and many students assisted with this experiment, and their help has been invaluable. Corné Pieterse and three anonymous reviewers provided comments that improved the manuscript greatly.

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KK, SY, and HT initiated and managed the project. KK and HT designed experiments. SY and HS performed DNA extraction, PCR and next-generation sequencing. AST performed bioinformatics analysis. KK managed sorting and identification of arthropods. KK analyzed and interpreted all data. KK wrote the first draft with input from all coauthors. All authors contributed to revision of the manuscript.

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Correspondence to Kohmei Kadowaki.

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The authors declare no conflict of interest.

Additional information

Communicated by Corné Pieterse.

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Kadowaki, K., Yamamoto, S., Sato, H. et al. Aboveground herbivores drive stronger plant species-specific feedback than belowground fungi to regulate tree community assembly. Oecologia (2021). https://doi.org/10.1007/s00442-021-04868-0

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Keywords

  • Arthropod
  • Herbivore
  • Mycorrhizal fungi
  • Mycorrhizal type
  • Predator