Tropical land use alters functional diversity of soil food webs and leads to monopolization of the detrital energy channel
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Evaluation Summary:
Zhou et al. provide a robust study on isotopic and metabolic changes of a soil community across a gradient of different land-use types in Sumatra, Indonesia. By mixing community-based analyses of stable isotopes and size-based metabolic measures, they are able to elucidate, for the first time, important links among plants and the soil food web in tropical ecosystems. This study is of importance to tropical biologists, ecosystem ecologists and biodiversity conservationists aiming to understand the impacts of humans on tropical forests.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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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 animal groups studied, most of the taxa had lower litter-calibrated Δ 13 C values in plantations than in rainforests, suggesting that they switched to freshly-fixed plant carbon ('fast' energy channeling) in plantations from the detrital C pathway ('slow' energy channeling) in rainforests. 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 on 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.
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Author Response:
Reviewer #2:
This study examined the effect of land-use change on soil animal food webs in Sumatra, Indonesia using datasets of stable isotopes and metabolisms of 23 animal groups. They found that the calibrated 13C values of soil animals are generally higher in the rainforests compared to those in the plantations, and multidimensional metrics of the soil animal community (e.g., isotopic dispersion) differed across the land-use types. They also showed that the community food web metrics are influenced by environmental variables (e.g., soil pH and tree density and species richness. These results demonstrate that the conversion of rainforest to plantations could affect not only the above- but also the below-ground components of the ecosystems and likely the ecosystem functions.
Strength:
This is the first attempt …
Author Response:
Reviewer #2:
This study examined the effect of land-use change on soil animal food webs in Sumatra, Indonesia using datasets of stable isotopes and metabolisms of 23 animal groups. They found that the calibrated 13C values of soil animals are generally higher in the rainforests compared to those in the plantations, and multidimensional metrics of the soil animal community (e.g., isotopic dispersion) differed across the land-use types. They also showed that the community food web metrics are influenced by environmental variables (e.g., soil pH and tree density and species richness. These results demonstrate that the conversion of rainforest to plantations could affect not only the above- but also the below-ground components of the ecosystems and likely the ecosystem functions.
Strength:
This is the first attempt to investigate the effect of land-use changes in soil food web structure with stable isotope and metabolism datasets. This study is based on a great amount of data of high quality (biomass and metabolism rates, high taxonomic resolution for some taxa) and collected from four land-uses, which were achieved through a well-organized project. It is also noteworthy that the measurement of stable isotopes of tiny soil invertebrates required the improvement of the continuous flow isotope ratio mass spectrometer. The collaborations among international groups and across different disciplines shows a direction to be followed in studies on global environmental issues.
Weakness:
The only weakness of this study is that the isotopic measurements were conducted on the high-rank taxonomic group level (order or family) based on an assumption that "the high-rank animal taxa in soil are generally consistent in their isotopic niches and reflect the trophic niches of species in most taxa" (L164-165). Although I am not sure if I understand this assumption correctly, the authors consider that different species in some taxa should have similar isotopic (trophic) niches. If so, it is difficult to accept this assumption because previous studies have already reported large variations in C and N isotope ratios (~ 6 permil) within the order or family (e.g., oribatids, collembola, ants, and earthworms). The isotopic variation exceeds those observed across the land-use types. Because of the considerable variation within the high-rank taxa, which species were included in the mixed samples (only 3 to 15 individuals for each taxonomic group, Line 176) should have affected the present results and thus the key claims in this paper. Therefore, it would be necessary to scrutinize whether the samples used for the isotopic analyses could represent the high-rank taxa and whether the isotopic values presented in this study are understandable in light of the previous knowledge of their biology. I suppose that this could be a main focus of this study. Based on the compiled isotopic datasets, previous work (Potapov et al. 2019, Funct. Ecol.) successfully shows that the high-rank taxa can be treated as trophic nodes in food web studies. However, the work does not demonstrate that the isotopic values of relatively few individuals of a high-rank taxon could be used as the representative values of the taxon.
For the justification of using stable isotopes of high-ranks taxonomic groups please see our response to this point in ‘Essential Revisions’ above. For Oribatids and Collembola we had 15 individuals, and we include 829 samples to represent Oribatida, and 202 samples to represent Collembola. Soil ants and earthworms were typically represented by a single (few) dominant species per site in our study, which were represented with our measurements (see https://link.springer.com/10.1007/s10530-021-02539-y for earthworms and https://iopscience.iop.org/article/10.1088/1755-1315/771/1/012031 for ants).
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Evaluation Summary:
Zhou et al. provide a robust study on isotopic and metabolic changes of a soil community across a gradient of different land-use types in Sumatra, Indonesia. By mixing community-based analyses of stable isotopes and size-based metabolic measures, they are able to elucidate, for the first time, important links among plants and the soil food web in tropical ecosystems. This study is of importance to tropical biologists, ecosystem ecologists and biodiversity conservationists aiming to understand the impacts of humans on tropical forests.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)
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Reviewer #1 (Public Review):
Tropical ecosystems comprise species-rich assemblages of myriad invertebrate groups that are difficult to work with. These invertebrates form complex, multitrophic food webs that recycle energy locked in dead wood. For a long time, progress in soil ecology has been hampered by the taxonomic impediment, but also by shortcomings in our understanding of basic natural history. Zhou et al. leapfrogged these obstacles by using stable isotopes (techniques that elucidate the position of a species in the food web and [old vs. -human- young] energy pathways) and metabolic rates (that together with abundance, provide a measure of how much energy a species recycles in a community).
The strengths of this ms thus lie in the usage of comprehensive datasets (stable isotopes of δ13C and δ15N, and metabolic rates of 23 soil …
Reviewer #1 (Public Review):
Tropical ecosystems comprise species-rich assemblages of myriad invertebrate groups that are difficult to work with. These invertebrates form complex, multitrophic food webs that recycle energy locked in dead wood. For a long time, progress in soil ecology has been hampered by the taxonomic impediment, but also by shortcomings in our understanding of basic natural history. Zhou et al. leapfrogged these obstacles by using stable isotopes (techniques that elucidate the position of a species in the food web and [old vs. -human- young] energy pathways) and metabolic rates (that together with abundance, provide a measure of how much energy a species recycles in a community).
The strengths of this ms thus lie in the usage of comprehensive datasets (stable isotopes of δ13C and δ15N, and metabolic rates of 23 soil taxa) on a series of equally-comprehensive and well-defined metrics, used together for the first time in tropical ecosystems. This approach allows the authors to explore simultaneously changes in community, trophic and energy-pathway metrics, something rarely seen in the published literature.
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Reviewer #2 (Public Review):
This study examined the effect of land-use change on soil animal food webs in Sumatra, Indonesia using datasets of stable isotopes and metabolisms of 23 animal groups. They found that the calibrated 13C values of soil animals are generally higher in the rainforests compared to those in the plantations, and multidimensional metrics of the soil animal community (e.g., isotopic dispersion) differed across the land-use types. They also showed that the community food web metrics are influenced by environmental variables (e.g., soil pH and tree density and species richness. These results demonstrate that the conversion of rainforest to plantations could affect not only the above- but also the below-ground components of the ecosystems and likely the ecosystem functions.
Strength:
This is the first attempt to …
Reviewer #2 (Public Review):
This study examined the effect of land-use change on soil animal food webs in Sumatra, Indonesia using datasets of stable isotopes and metabolisms of 23 animal groups. They found that the calibrated 13C values of soil animals are generally higher in the rainforests compared to those in the plantations, and multidimensional metrics of the soil animal community (e.g., isotopic dispersion) differed across the land-use types. They also showed that the community food web metrics are influenced by environmental variables (e.g., soil pH and tree density and species richness. These results demonstrate that the conversion of rainforest to plantations could affect not only the above- but also the below-ground components of the ecosystems and likely the ecosystem functions.
Strength:
This is the first attempt to investigate the effect of land-use changes in soil food web structure with stable isotope and metabolism datasets. This study is based on a great amount of data of high quality (biomass and metabolism rates, high taxonomic resolution for some taxa) and collected from four land-uses, which were achieved through a well-organized project. It is also noteworthy that the measurement of stable isotopes of tiny soil invertebrates required the improvement of the continuous flow isotope ratio mass spectrometer. The collaborations among international groups and across different disciplines shows a direction to be followed in studies on global environmental issues.
Weakness:
The only weakness of this study is that the isotopic measurements were conducted on the high-rank taxonomic group level (order or family) based on an assumption that "the high-rank animal taxa in soil are generally consistent in their isotopic niches and reflect the trophic niches of species in most taxa" (L164-165). Although I am not sure if I understand this assumption correctly, the authors consider that different species in some taxa should have similar isotopic (trophic) niches. If so, it is difficult to accept this assumption because previous studies have already reported large variations in C and N isotope ratios (~ 6 permil) within the order or family (e.g., oribatids, collembola, ants, and earthworms). The isotopic variation exceeds those observed across the land-use types. Because of the considerable variation within the high-rank taxa, which species were included in the mixed samples (only 3 to 15 individuals for each taxonomic group, Line 176) should have affected the present results and thus the key claims in this paper. Therefore, it would be necessary to scrutinize whether the samples used for the isotopic analyses could represent the high-rank taxa and whether the isotopic values presented in this study are understandable in light of the previous knowledge of their biology. I suppose that this could be a main focus of this study. Based on the compiled isotopic datasets, previous work (Potapov et al. 2019, Funct. Ecol.) successfully shows that the high-rank taxa can be treated as trophic nodes in food web studies. However, the work does not demonstrate that the isotopic values of relatively few individuals of a high-rank taxon could be used as the representative values of the taxon.
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