Genetic diversity affects ecosystem functions across trophic levels as much as species diversity, but in an opposite direction

Reviewer #1 (Public review):

Summary:

This work used a comprehensive dataset to compare the effects of species diversity and genetic diversity within each trophic level and across three trophic levels. The results showed that species diversity had negative effects on ecosystem functions, while genetic diversity had positive effects. These effects were observed only within each trophic level and not across the three trophic levels studied. Although the effects of biodiversity, especially genetic diversity across multi-trophic levels, have been shown to be important, there are still very few empirical studies on this topic due to the complex relationships and difficulty in obtaining data. This study collected an excellent dataset to address this question, enhancing our understanding of genetic diversity effects in aquatic ecosystems.

Strengths:

The study collected an extensive dataset that includes species diversity of primary producers (riparian trees), primary consumers (macroinvertebrate shredders), and secondary consumers (fish). It also includes the genetic diversity of the dominant species at each trophic level, biomass production, decomposition rates, and environmental data.

The conclusions of this paper are mostly well supported by the data and the writing is logical and easy to follow.

Weaknesses:

While the dataset is impressive, the authors conducted analyses more akin to a "meta-analysis," leaving out important basic information about the raw data in the manuscript. Given the complexity of the relationships between different trophic levels and ecosystem functions, it would be beneficial for the authors to show the results of each SEM (structural equation model).

The main results presented in the manuscript are derived from a "metadata" analysis of effect sizes. However, the methods used to obtain these effect sizes are not sufficiently clarified. By analyzing the effect sizes of species diversity and genetic diversity on these ecosystem functions, the results showed that species diversity had negative effects, while genetic diversity had positive effects on ecosystem functions. The negative effects of species diversity contradict many studies conducted in biodiversity experiments. The authors argue that their study is more relevant because it is based on a natural system, which is closer to reality, but they also acknowledge that natural systems make it harder to detect underlying mechanisms. Providing more results based on the raw data and offering more explanations of the possible mechanisms in the introduction and discussion might help readers understand why and in what context species diversity could have negative effects.

Environmental variation was included in the analyses to test if the environment would modulate the effects of biodiversity on ecosystem functions. However, the main results and conclusions did not sufficiently address this aspect.

Reviewer #2 (Public review):

Summary:

Fargeot et al. investigated the relative importance of genetic and species diversity on ecosystem function and examined whether this relationship varies within or between trophic-level responses. To do so, they conducted a well-designed field survey measuring species diversity at 3 trophic levels (primary producers [trees], primary consumers [macroinvertebrate shredders], and secondary consumers [fishes]), genetic diversity in a dominant species within each of these 3 trophic levels and 7 ecosystem functions across 52 riverine sites in southern France. They show that the effect of genetic and species diversity on ecosystem functions are similar in magnitude, but when examining within-trophic level responses, operate in different directions: genetic diversity having a positive effect and species diversity a negative one. This data adds to growing evidence from manipulated experiments that both species and genetic diversity can impact ecosystem function and builds upon this by showing these effects can be observed in nature.

Strengths:

The study design has resulted in a robust dataset to ask questions about the relative importance of genetic and species diversity of ecosystem function across and within trophic levels.

Overall, their data supports their conclusions - at least within the system that they are studying - but as mentioned below, it is unclear from this study how general these conclusions would be.

Weaknesses:

(1) While a robust dataset, the authors only show the data output from the SEM (i.e., effect size for each individual diversity type per trophic level (6) on each ecosystem function (7)), instead of showing much of the individual data. Although the summary SEM results are interesting and informative, I find that a weakness of this approach is that it is unclear how environmental factors (which were included but not discussed in the results) nor levels of diversity were correlated across sites. As species and genetic diversity are often correlated but also can have reciprocal feedbacks on each other (e.g., Vellend 2005), there may be constraints that underpin why the authors observed positive effects of one type of diversity (genetic) when negative effects of the other (species). It may have also been informative to run SEM with links between levels of diversity. By focusing only on the summary of SEM data, the authors may be reducing the strength of their field dataset and ability to draw inferences from multiple questions and understand specific study-system responses.

(2) My understanding of SEM is it gives outputs of the strength/significance of each pathway/relationship and if so, it isn't clear why this wasn't used and instead, confidence intervals of Z scores to determine which individual BEFs were significant. In addition, an inclusion of the 7 SEM pathway outputs would have been useful to include in an appendix.

(3) I don't fully agree with the authors calling this a meta-analysis as it is this a single study of multiple sites within a single region and a specific time point, and not a collection of multiple studies or ecosystems conducted by multiple authors. Moreso, the authors are using meta-analysis summary metrics to evaluate their data. The authors tend to focus on these patterns as general trends, but as the data is all from this riverine system this study could have benefited from focusing on what was going on in this system to underpin these patterns. I'd argue more data is needed to know whether across sites and ecosystems, species diversity and genetic diversity have opposite effects on ecosystem function within trophic levels.

Reviewer #3 (Public review):

The manuscript by Fargeot and colleagues assesses the relative effects of species and genetic diversity on ecosystem functioning. This study is very well written and examines the interesting question of whether within-species or among-species diversity correlates with ecosystem functioning, and whether these effects are consistent across trophic levels. The main findings are that genetic diversity appears to have a stronger positive effect on function than species diversity (which appears negative). These results are interesting and have value.

However, I do have some concerns that could influence the interpretation.

(1) Scale: the different measures of diversity and function for the different trophic levels are measured over very different spatial scales, for example, trees along 200 m transects and 15 cm traps. It is not clear whether trees 200 m away are having an effect on small-scale function.

(2) Size of diversity gradients: More information is needed on the actual diversity gradients. One of the issues with surveys of natural systems is that they are of species that have already gone through selection filters from a regional pool, and theoretically, if the environments are similar, you should get similar sets of species, without monocultures. So, if the species diversity gradients range from say, 6 to 8 species, but genetic diversity gradients span an order of magnitude more, you can explain much more variance with genetic diversity. Related to this, species diversity effects on function are often asymptotic at high diversity and so if you are only sampling at the high diversity range, we should expect a strong effect.

(3) Ecosystem functions: The functions are largely biomass estimates (expect decomposition), and I fail to see how the biomass of a single species can be construed as an ecosystem function. Aren't you just estimating a selection effect in this case?

Note that the article claims to be one of the only studies to look at function across trophic levels, but there are several others out there, for example:

Li, F., Altermatt, F., Yang, J., An, S., Li, A., & Zhang, X. (2020). Human activities' fingerprint on multitrophic biodiversity and ecosystem functions across a major river catchment in China. Global change biology, 26(12), 6867-6879.

Luo, Y. H., Cadotte, M. W., Liu, J., Burgess, K. S., Tan, S. L., Ye, L. J., ... & Gao, L. M. (2022). Multitrophic diversity and biotic associations influence subalpine forest ecosystem multifunctionality. Ecology, 103(9), e3745.

Moi, D. A., Romero, G. Q., Antiqueira, P. A., Mormul, R. P., Teixeira de Mello, F., & Bonecker, C. C. (2021). Multitrophic richness enhances ecosystem multifunctionality of tropical shallow lakes. Functional Ecology, 35(4), 942-954.

Wan, B., Liu, T., Gong, X., Zhang, Y., Li, C., Chen, X., ... & Liu, M. (2022). Energy flux across multitrophic levels drives ecosystem multifunctionality: Evidence from nematode food webs. Soil Biology and Biochemistry, 169, 108656.

And the case was made strongly by:

Seibold, S., Cadotte, M. W., MacIvor, J. S., Thorn, S., & Müller, J. (2018). The necessity of multitrophic approaches in community ecology. Trends in ecology & evolution, 33(10), 754-764.

Author response:

Public Reviews:

Reviewer #1 (Public review):

Summary:

This work used a comprehensive dataset to compare the effects of species diversity and genetic diversity within each trophic level and across three trophic levels. The results showed that species diversity had negative effects on ecosystem functions, while genetic diversity had positive effects. These effects were observed only within each trophic level and not across the three trophic levels studied. Although the effects of biodiversity, especially genetic diversity across multi-trophic levels, have been shown to be important, there are still very few empirical studies on this topic due to the complex relationships and difficulty in obtaining data. This study collected an excellent dataset to address this question, enhancing our understanding of genetic diversity effects in aquatic ecosystems.

Strengths:

The study collected an extensive dataset that includes species diversity of primary producers (riparian trees), primary consumers (macroinvertebrate shredders), and secondary consumers (fish). It also includes the genetic diversity of the dominant species at each trophic level, biomass production, decomposition rates, and environmental data.

The conclusions of this paper are mostly well supported by the data and the writing is logical and easy to follow.

Weaknesses:

While the dataset is impressive, the authors conducted analyses more akin to a "meta-analysis," leaving out important basic information about the raw data in the manuscript. Given the complexity of the relationships between different trophic levels and ecosystem functions, it would be beneficial for the authors to show the results of each SEM (structural equation model).

We understand the point raised by the reviewer. Our objective was to focus the Results section on the main hypotheses, and for this we let away the raw statistics. We can definitively show the seven individual SEM, highlighting the major links, which may help understand some processes. This will be done in the next version of the manuscript.

The main results presented in the manuscript are derived from a "metadata" analysis of effect sizes. However, the methods used to obtain these effect sizes are not sufficiently clarified. By analyzing the effect sizes of species diversity and genetic diversity on these ecosystem functions, the results showed that species diversity had negative effects, while genetic diversity had positive effects on ecosystem functions. The negative effects of species diversity contradict many studies conducted in biodiversity experiments. The authors argue that their study is more relevant because it is based on a natural system, which is closer to reality, but they also acknowledge that natural systems make it harder to detect underlying mechanisms. Providing more results based on the raw data and offering more explanations of the possible mechanisms in the introduction and discussion might help readers understand why and in what context species diversity could have negative effects.

We hope you will be right. As said above, we will explore this possibility.

Environmental variation was included in the analyses to test if the environment would modulate the effects of biodiversity on ecosystem functions. However, the main results and conclusions did not sufficiently address this aspect.

This will be addressed by the more in-depth analysis of individual SEM, and we will discuss this further.

Reviewer #2 (Public review):

Summary:

Fargeot et al. investigated the relative importance of genetic and species diversity on ecosystem function and examined whether this relationship varies within or between trophic-level responses. To do so, they conducted a well-designed field survey measuring species diversity at 3 trophic levels (primary producers [trees], primary consumers [macroinvertebrate shredders], and secondary consumers [fishes]), genetic diversity in a dominant species within each of these 3 trophic levels and 7 ecosystem functions across 52 riverine sites in southern France. They show that the effect of genetic and species diversity on ecosystem functions are similar in magnitude, but when examining within-trophic level responses, operate in different directions: genetic diversity having a positive effect and species diversity a negative one. This data adds to growing evidence from manipulated experiments that both species and genetic diversity can impact ecosystem function and builds upon this by showing these effects can be observed in nature.

Strengths:

The study design has resulted in a robust dataset to ask questions about the relative importance of genetic and species diversity of ecosystem function across and within trophic levels.

Overall, their data supports their conclusions - at least within the system that they are studying - but as mentioned below, it is unclear from this study how general these conclusions would be.

Weaknesses:

(1) While a robust dataset, the authors only show the data output from the SEM (i.e., effect size for each individual diversity type per trophic level (6) on each ecosystem function (7)), instead of showing much of the individual data. Although the summary SEM results are interesting and informative, I find that a weakness of this approach is that it is unclear how environmental factors (which were included but not discussed in the results) nor levels of diversity were correlated across sites. As species and genetic diversity are often correlated but also can have reciprocal feedbacks on each other (e.g., Vellend 2005), there may be constraints that underpin why the authors observed positive effects of one type of diversity (genetic) when negative effects of the other (species). It may have also been informative to run SEM with links between levels of diversity. By focusing only on the summary of SEM data, the authors may be reducing the strength of their field dataset and ability to draw inferences from multiple questions and understand specific study-system responses.

We will address this issue by performing a more in-depth analysis of each individual SEMs, and provide directly these raw data. Regarding the comment on species-genomic diversity correlations (SGDCs), we would like to point out that this has already been addressed in a previous paper (Fargeot et al. Oikos, 2023). There is actually no correlations between genomic and species diversity in these dataset, which is merely explain by the selection of the sampling sites. The relationships between species diversity, genomic diversity and environmental factors are also detailed in Fargeot et al. (2023). We precisely published this paper first to focus here “only” on BEFs. But we realize we need to provide further information and discuss further these issues. This will be done in the next version of the manuscript.

(2) My understanding of SEM is it gives outputs of the strength/significance of each pathway/relationship and if so, it isn't clear why this wasn't used and instead, confidence intervals of Z scores to determine which individual BEFs were significant. In addition, an inclusion of the 7 SEM pathway outputs would have been useful to include in an appendix.

Yes, we can provide p-values. Results from p-values will provide the same information than 95%Cis, both yield very similar (if not exactly the same) results/conclusions. We wil provide the 7 SEMs in Appendices.

(3) I don't fully agree with the authors calling this a meta-analysis as it is this a single study of multiple sites within a single region and a specific time point, and not a collection of multiple studies or ecosystems conducted by multiple authors. Moreso, the authors are using meta-analysis summary metrics to evaluate their data. The authors tend to focus on these patterns as general trends, but as the data is all from this riverine system this study could have benefited from focusing on what was going on in this system to underpin these patterns. I'd argue more data is needed to know whether across sites and ecosystems, species diversity and genetic diversity have opposite effects on ecosystem function within trophic levels.

We agree. “Meta-regression” would perhaps be more adequate than “meta-analyses”. As said above, more details will be provided on the next version of the manuscript.

Reviewer #3 (Public review):

The manuscript by Fargeot and colleagues assesses the relative effects of species and genetic diversity on ecosystem functioning. This study is very well written and examines the interesting question of whether within-species or among-species diversity correlates with ecosystem functioning, and whether these effects are consistent across trophic levels. The main findings are that genetic diversity appears to have a stronger positive effect on function than species diversity (which appears negative). These results are interesting and have value.

However, I do have some concerns that could influence the interpretation.

(1) Scale: the different measures of diversity and function for the different trophic levels are measured over very different spatial scales, for example, trees along 200 m transects and 15 cm traps. It is not clear whether trees 200 m away are having an effect on small-scale function.

Trees identification and invertebrate (and fish) sampling are done on the same scale. Trees are spread along the river so that their leaves fall directly in the river. Traps have been installed all along the same transect in various micro-habitats. Diversity have been measured at the exact same scale for all organisms. We will try to be more precise.

(2) Size of diversity gradients: More information is needed on the actual diversity gradients. One of the issues with surveys of natural systems is that they are of species that have already gone through selection filters from a regional pool, and theoretically, if the environments are similar, you should get similar sets of species, without monocultures. So, if the species diversity gradients range from say, 6 to 8 species, but genetic diversity gradients span an order of magnitude more, you can explain much more variance with genetic diversity. Related to this, species diversity effects on function are often asymptotic at high diversity and so if you are only sampling at the high diversity range, we should expect a strong effect.

We will provide more information. The range of diversity also vary according to the trophic level; there are more invertebrate species than fish species. But overall the rage of species number is large.

(3) Ecosystem functions: The functions are largely biomass estimates (expect decomposition), and I fail to see how the biomass of a single species can be construed as an ecosystem function. Aren't you just estimating a selection effect in this case?

The biomass estimated for a certain area represent an estimate of productivity, whatever the number of species being considered. Obviously, productivity of a species can be due to environmental constraints; the biomass is expected to be lower at the niche margin (selection effect). But is these environmental effects are taken into account (which is the case in the SEMs), then the residual variation can be explained by biodiversity effects. We will try to make it more clear.

Note that the article claims to be one of the only studies to look at function across trophic levels, but there are several others out there, for example:

Thanks, we will cite some of these studies (and make our claim less strong)

Li, F., Altermatt, F., Yang, J., An, S., Li, A., & Zhang, X. (2020). Human activities' fingerprint on multitrophic biodiversity and ecosystem functions across a major river catchment in China. Global change biology, 26(12), 6867-6879.

Luo, Y. H., Cadotte, M. W., Liu, J., Burgess, K. S., Tan, S. L., Ye, L. J., ... & Gao, L. M. (2022). Multitrophic diversity and biotic associations influence subalpine forest ecosystem multifunctionality. Ecology, 103(9), e3745.

Moi, D. A., Romero, G. Q., Antiqueira, P. A., Mormul, R. P., Teixeira de Mello, F., & Bonecker, C. C. (2021). Multitrophic richness enhances ecosystem multifunctionality of tropical shallow lakes. Functional Ecology, 35(4), 942-954.

Wan, B., Liu, T., Gong, X., Zhang, Y., Li, C., Chen, X., ... & Liu, M. (2022). Energy flux across multitrophic levels drives ecosystem multifunctionality: Evidence from nematode food webs. Soil Biology and Biochemistry, 169, 108656.

And the case was made strongly by:

Seibold, S., Cadotte, M. W., MacIvor, J. S., Thorn, S., & Müller, J. (2018). The necessity of multitrophic approaches in community ecology. Trends in ecology & evolution, 33(10), 754-764.