Tropical land use alters functional diversity of soil food webs and leads to monopolization of the detrital energy channel
Abstract
Agricultural expansion is among the main threats to biodiversity and functions of tropical ecosystems. It has been shown that conversion of rainforest into plantations erodes biodiversity, but further consequences for food-web structure and energetics of belowground communities remains little explored. We used a unique combination of stable isotope analysis and food web energetics to analyze in a comprehensive way consequences of the conversion of rainforest into oil palm and rubber plantations on the structure of and channeling of energy through soil animal food webs in Sumatra, Indonesia. Across the 23 animal groups studied, most of the taxa switched to freshly-fixed plant carbon (low Δ13C values) indicating 'fast' energy channeling in plantations as opposed to 'slow' energy channeling through the detrital pathway in rainforests (high Δ13C values). These shifts led to changes in isotopic divergence, dispersion, evenness and uniqueness. However, earthworms as major detritivores stayed unchanged in their trophic niche and monopolized the detrital pathway in plantations, resulting in similar energetic metrics across land-use systems. Functional diversity metrics of soil food webs were associated with reduced amount of litter, tree density and species richness in plantations, providing guidelines how to improve the complexity of the structure of and channeling of energy through soil food webs. Our results highlight the strong restructuring of soil food webs with the conversion of rainforest into plantations threatening soil functioning and ecosystem stability in the long term.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting file
Article and author information
Author details
Funding
Deutsche Forschungsgemeinschaft (192626868-SFB 990)
- Zheng Zhou
Deutsche Forschungsgemeinschaft (192626868-SFB 990)
- Valentyna Krashevska
Deutsche Forschungsgemeinschaft (192626868-SFB 990)
- Rahayu Widyastuti
Deutsche Forschungsgemeinschaft (192626868-SFB 990)
- Stefan Scheu
Deutsche Forschungsgemeinschaft (192626868-SFB 990)
- Anton Potapov
China Scholarship Council (202004910314)
- Zheng Zhou
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- David A. Donoso, Escuela Politécnica Nacional, Ecuador
Publication history
- Received: November 9, 2021
- Preprint posted: February 11, 2022 (view preprint)
- Accepted: March 29, 2022
- Accepted Manuscript published: March 31, 2022 (version 1)
- Version of Record published: April 22, 2022 (version 2)
- Version of Record updated: April 28, 2022 (version 3)
Copyright
© 2022, Zhou 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
-
- 826
- Page views
-
- 181
- Downloads
-
- 3
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
Download links
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)
Further reading
-
- Ecology
- Epidemiology and Global Health
The global spread of antibiotic resistance could be due to a number of factors, and not just the overuse of antibiotics in agriculture and medicine as previously thought.
-
- Ecology
- Evolutionary Biology
How the ecological process of community assembly interacts with intra-species diversity and evolutionary change is a longstanding question. Two contrasting hypotheses have been proposed: Diversity Begets Diversity (DBD), in which taxa tend to become more diverse in already diverse communities, and Ecological Controls (EC), in which higher community diversity impedes diversification. Previously, using 16S rRNA gene amplicon data across a range of microbiomes, we showed a generally positive relationship between taxa diversity and community diversity at higher taxonomic levels, consistent with the predictions of DBD (Madi et al., 2020). However, this positive 'diversity slope' plateaus at high levels of community diversity. Here we show that this general pattern holds at much finer genetic resolution, by analyzing intra-species strain and nucleotide variation in static and temporally sampled metagenomes from the human gut microbiome. Consistent with DBD, both intra-species polymorphism and strain number were positively correlated with community Shannon diversity. Shannon diversity is also predictive of increases in polymorphism over time scales up to ~4-6 months, after which the diversity slope flattens and becomes negative – consistent with DBD eventually giving way to EC. Finally, we show that higher community diversity predicts gene loss at a future time point. This observation is broadly consistent with the Black Queen Hypothesis, which posits that genes with functions provided by the community are less likely to be retained in a focal species' genome. Together, our results show that a mixture of DBD, EC, and Black Queen may operate simultaneously in the human gut microbiome, adding to a growing body of evidence that these eco-evolutionary processes are key drivers of biodiversity and ecosystem function.