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
  17. Keping Ma
  18. Xiaojuan Liu

  • Curated by eLife

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    Evaluation Summary:

    Using an impressive experimental design, Tang et al. analyzed the effects of intraspecific (genetic) and interspecific (species) diversity in ecosystem processes carried out by forest communities. The results show that both species and genotype diversity influence productivity via changes in overall functional diversity, herbivory, and soil fungal diversity. This study will be important to ecologists and environmentalists interested in ecosystem processes and restoration efforts.

    (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

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 on tree productivity, 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.

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  1. Version published to 10.7554/elife.78703 on eLife
  2. eLife

    Author Response

    Reviewer 1

    Ting Tang et al. present the results of a species x genotype diversity experiment within BEF China. The authors assess the relative impacts of species and genotype diversity on community-level primary productivity of the trees and the potential mediation of this effect via interactions of plants with soil fungi and herbivores. The results show that both species and genotype diversity influence productivity via changes in herbivory, soil fungal diversity, and other unknown mechanisms. Most of the species diversity effects could be directly related to functional diversity, while genotype diversity effects were not well represented by the way functional diversity was measured in this study.

    Thanks for the positive comments on the paper.

    The study is based on an impressive experiment that will certainly allow achieving major insights into the role of genotype and species diversity on ecosystem functioning. However, there are some significant shortcomings in the methods that limit this study. In particular, the incomplete assessment of functional traits, herbivory, and fungal diversity across the subplots used for this study reduces statistical power. Specific measurements of traits, herbivory and fungal diversity in each plot would substantially simplify the design and the analyses and likely also reduce the unexplained variance observed in the study. However, this is nothing that can be changed now and has the likely explanation of feasibility constraints.

    Thank you for the positive comments on the paper and the understanding of the feasibility constraints. In our study, functional traits of all the seed families of the four species across all the species × genetic diversity combinations were sampled, but to reduce circularity, we used the seed-family means across all tree diversity combinations to calculate functional diversity for every subplot instead of only using the functional trait measures obtained in that particular subplot. We have taken up the suggestion to also calculate functional diversity based on trait measurements of individual trees, but also here used data across all plots to reduce circularity. Additionally, we now acknowledge the incomplete assessment of herbivory in the Methods and state that fungal diversity in plant species mixtures was sampled on plot level because of feasibility constraints.

    Lines 334–337: “To reduce circularity, we used the seed-family means across all species × genetic diversity combinations to calculate FDis values per subplot that did not only depend on the functional trait measures obtained in that particular subplot. Using traits measured in a particular subplot to calculate FDis for that subplot bears the risk that the measured traits reflect a response to the local environment, yet we want to use FDis as a predictor variable for the performance of that subplot.”

    Lines 380–382: “The mean value of herbivore damage per species × genetic diversity level was used to fill in missing values in a few subplots with tree individuals lacking herbivory data (Table S3).”

    Lines 385–388: “Soil fungal diversity was used as a proxy of unspecified trophic interactions. To be consistent with the species and genetic diversity treatment design, soil samples were taken on subplot level for the 1.1 and 1.4 diversity treatments, but, due to feasibility constraints, on plot level for the 4.1 and 4.4 diversity treatments in 2017.”

    The writing of the manuscript is generally good. However, given the somewhat diffuse results obtained for genetic diversity effects, they receive a lot of attention in the discussion, while species diversity effects are little mentioned. This could be better balanced and also referred back to the hypotheses. For example, I miss the discussion of the very clear hypothesis that genotype diversity effects are positive in species monocultures but neutral in species mixtures. How do your results fit with this hypothesis? My general impression is that the study is very well framed, but lacks to stick to this frame in the discussion. I am aware that this might be a challenge with the results obtained, but worth trying.

    Thank you for the positive comments on the writing and pointing out the unclear part of the genetic diversity effects. To better connect the discussion to our hypothesis that genotype diversity effects are “more important in species monocultures than in species mixtures” (lines 114–115), we have rewritten the corresponding Discussion section.

    Lines 248–164: “In contrast of our second hypothesis, we found that the effects of genetic diversity via functional diversity and multi-trophic feedbacks were negative in species monocultures but positive in the species mixture (Fig. 5 and Fig. S3). We found genetic diversity had positive effects on tree functional diversity and soil fungal diversity, which supports the trade-offs between genetic and species diversity discussed in the previous section. However, the hypothesized positive effects of tree functional diversity on productivity turned negative in species monoculture. This result indicates that functional diversity may not have positive effects on the ecosystem functioning under low environmental heterogeneity, i.e. species monocultures in our study (Hillebrand and Matthiessen 2009). Therefore, our findings show that the different effects of genetic diversity on tree productivity between species monocultures and mixtures, not only depend on the different effects of genetic diversity on functional diversity and trophic interaction but also on the varied tree productivity consequences from functional diversity and trophic interaction on tree productivity between species monocultures and mixtures. Moreover, other aspects of tree genetic diversity seem to play an important role not only for productivity in tree species mixtures (see previous section) but also for productivity in tree species monocultures. These may include unmeasured functional traits such as root traits (Bardgett et al., 2014) or unknown mechanisms underpinning effects of tree genetic diversity.”

    Given the complex results obtained, I also feel that the title and main message received in the abstract do not fully reflect the results. Genetic diversity effects on productivity, but also on herbivory and fungal diversity, are not general (e.g. Fig. 2) nor are all genetic diversity effects on productivity mediated by functional diversity and trophic feedback. I think the title and main message of the study should be articulated more precisely.

    In this study we did not find direct effects of genetic diversity on tree productivity in the binary analyses (Fig. 2), but we did find indirect effects of genetic diversity on tree productivity via functional diversity and trophic feedbacks in the path analysis (Fig. 4). Now we have pointed this out in the Discussion.

    Lines 201–204: “Although only species diversity but not genetic diversity was found to affect tree productivity in binary analyses, both kinds of diversity positively affected tree community productivity and trophic interactions via functional diversity according to our structural equation models (SEMs) depicted in the corresponding path-analysis diagrams (see Fig. 4).”

    We agree that not all genetic diversity effects on productivity were mediated by functional diversity and trophic feedbacks. This may have been because we did not include all relevant functional traits and trophic interactions in this study. Nevertheless, our findings support the hypothesis that genetic diversity can affect productivity via functional diversity and trophic feedbacks and suggest more possibilities for further research. We have explained this in the Discussion.

    Lines 230–238: “Even after accounting for tree functional diversity and trophic feedbacks, we still detected a direct negative effect of tree genetic diversity on tree productivity, while the direct effect of tree species diversity was fully explained by functional diversity and trophic feedbacks. This suggests that aspects of genetic diversity that do not contribute to functional diversity or trophic interactions as measured in this study may reduce ecosystem functioning, e.g. due to trade-offs between genetic diversity and species diversity. For example, it has been shown that in species-diverse grassland ecosystems, niche-complementarity between species can increase at the expense of reduced variation within species (van Moorsel et al., 2018; van Moorsel et al., 2019; Zuppinger-Dingley et al., 2014; Zvereva et al., 2012).”

    Lines 260–264: “Moreover, other aspects of tree genetic diversity seem to play an important role not only for productivity in tree species mixtures (see previous section) but also for productivity in tree species monocultures. These may include unmeasured functional traits such as root traits (Bardgett et al., 2014) or unknown mechanisms underpinning effects of tree genetic diversity.”

    Reviewer 2

    This study aims to disentangle the contributions of genetic and species diversity to tree community fitness. It confirms the role of genetic diversity in functional and ecological traits but shows how these effects change when plant species diversity is increased, which can potentially add to our understanding of the interplay between plant diversity at various levels and community and ecosystem functions. It would be desirable to make emphasis whether differences between the effects of genetic and species diversity are comparable since they can act at complementary but different levels. It is hard to establish whether the effects of species diversity override the effects of genetic diversity by shared mechanisms; or whether a high species diversity reduces plant intraspecific interactions and the consequent effects of genetic diversity by density-dependent effects. However, this point has to be emphasized in the discussion.

    Thank you for your positive comments on this paper. In the binary analyses in this paper, we used general linear mixed-model analysis to detect the effects of genetic diversity within species. Now we have clarified this in the Methods and the Results section. However, in Fig. 2 we also indicate the significance of the main effect of genetic diversity. We do not focus on this because of the interaction between species and genetic diversity. In statistical terms, fitting genetic diversity effects separately for species monocultures and mixture (2 degrees of freedom) is equivalent (i.e. has the same sum of squares) as fitting the main effect of genetic diversity (1 degree of freedom) and the interactions species x genetic diversity (1 degree of freedom).

    Lines 415–424: “To determine how species and genetic diversity and their interaction affected tree functional diversity and trophic interactions, linear mixed-effects models (LMMs) were fitted with two types of contrast coding. In the first, we used the ordinary 2-way analysis of variance with interaction and in the second we replaced the genetic diversity main effect and the interaction with separate genetic diversity effects for species monocultures and the species mixture (Table S6). Note that as our design was orthogonal, fitting sequence did not matter in either of the codings. However, we focused our major analysis on the second type of coding to make it consistent with our hypotheses. Main effects of genetic diversity are presented in inset panels in Fig. 2. Our second contrast coding ensured that we tested the effects of genetic diversity separately in species monocultures and species mixture, but within the same analysis.”

    Lines 120–121: “Using linear mixed-model analyses, we tested the effects of species diversity and genetic diversity within species on trophic interactions and community productivity.”

    Meanwhile, to emphasize that species diversity and genetic diversity could affect each other, we discussed that the trade-offs between species and genetic diversity could contribute to the effects of tree diversity on tree community productivity. We also discussed that the different effects of genetic diversity between species monocultures and mixtures may occur because different biotic environments resulted from different species diversity.

    Lines 232–238: “This suggests that aspects of genetic diversity that do not contribute to functional diversity or trophic interactions as measured in this study may reduce ecosystem functioning, e.g. due to trade-offs between genetic diversity and species diversity. For example, it has been shown that in species-diverse grassland ecosystems niche-complementarity between species can increase at the expense of reduced variation within species (van Moorsel et al., 2018; van Moorsel et al., 2019; Zuppinger-Dingley et al., 2014; Zvereva et al., 2012).”

    Lines 250–260: “We found genetic diversity had positive effects on tree functional diversity and soil fungal diversity, which supports the trade-offs between genetic and species diversity discussed in the previous section. However, the hypothesized positive effects of tree functional diversity on productivity turned negative in species monoculture. This result indicates that functional diversity may not have positive effects on the ecosystem functioning under low environmental heterogeneity, i.e. species monocultures in our study (Hillebrand and Matthiessen 2009). Therefore, our findings show that the different effects of genetic diversity on tree productivity between species monocultures and mixtures, not only depend on the different effects of genetic diversity on functional diversity and trophic interaction but also on the varied tree productivity consequences from functional diversity and trophic interaction on tree productivity between species monocultures and mixtures.”

    The experimental design has to be explained in more detail, in particular how plants were planted in the species monocultures. It is not stated whether the same or different species were used in the plots or in subplots. The design lacks proper replication for the treatment with high genetic diversity in species monocultures (n=2) which could lead to a biased result, especially if those plots were located in the same area.

    Thank you for the valuable comments on the experiment design. In total, we used four species and eight seed families per species for the whole experiment, and now we have added a diagram of the experimental design to the supplementary material (Fig. S5) to show the species and seed-family information for every subplot. Furthermore, we have added a table to the supplementary material to indicate the occurrence time of each species and each seed family across all the tree diversity-treatment combinations (Table S2). The high genetic diversity in species monoculture (1.4 treatment) was replicated 2 times per species and thus had 8 replications (Fig. S5). However, because we did not have enough seedlings, we could only establish these treatments at subplot level and thus put the different species for the 1.4 treatment into only two plots. Now we have added more explanation of the plot design in the Methods part. The plot distribution was completely randomized across the experimental site and plots of the same treatments were mostly located at least 50 m from each other (see Fig. 1 from Bongers et al., 2020, pasted here further below). The reason that there are more plots for the 1.1 treatment is that typically in biodiversity experiments more plots are needed at the lowest diversity treatment because of the desire to have all seed families occurring in any mixture also present as monoculture. Regarding the point that the four diversity treatments varied between rather than within plots, we ensured that diversity effects were tested at the plot level by including plot as random-effects term in the mixed models.

    Lines 305–323: “For each of the four species, we collected seeds from eight mother trees to allow for two replications of four-family mixtures per species. Furthermore, to avoid the effects of unequal representation of particular seed families and correlations between seed family presence and diversity treatments, we made sure that every seed family occurred the same number of times at each diversity level (see Table S2, small deviations from the rule were required where not enough seeds from a seed family could be obtained). Due to budget limitations and the number of replicates required per single seed family, the 1.1 and 1.4 diversity treatments were applied at subplot level (0.25 mu) and replicated 32 and 8 times, respectively. The 4.1 and 4.4 diversity treatments were applied at plot level (1 mu) and were replicated 8 and 6 times, respectively (Fig. S5; see also Fig. 1 in Bongers et al., 2020). To allow for simpler analysis, we obtained most community measures at subplot level also for the 4.1 and 4.4 diversity treatments and thereafter used the subplots for all tests of diversity effects on these community measures, including plots as error (i.e. random-effects) term for testing the diversity effects in the corresponding mixed models. In total, because one 1-mu plot could not be established due to logistic constraints, the number of subplots used was 92 (32 subplots of 1.1, 8 subplots of 1.4, 28 subplots of 4.1 and 24 subplots of 4.4 diversity treatment). Note that in biodiversity experiments lower richness levels represent more different communities and thus require more plots. For the highest richness level, where there is typically only one species composition, this same community is typically replicated multiple times, as we did here for the 4.4. diversity treatment.”

  3. eLife

    Evaluation Summary:

    Using an impressive experimental design, Tang et al. analyzed the effects of intraspecific (genetic) and interspecific (species) diversity in ecosystem processes carried out by forest communities. The results show that both species and genotype diversity influence productivity via changes in overall functional diversity, herbivory, and soil fungal diversity. This study will be important to ecologists and environmentalists interested in ecosystem processes and restoration efforts.

    (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.)

  4. eLife

    Reviewer #1 (Public Review):

    Ting Tang et al. present the results of a species x genotype diversity experiment within BEF China. The authors assess the relative impacts of species and genotype diversity on community-level primary productivity of the trees and the potential mediation of this effect via interactions of plants with soil fungi and herbivores. The results show that both species and genotype diversity influence productivity via changes in herbivory, soil fungal diversity, and other unknown mechanisms. Most of the species diversity effects could be directly related to functional diversity, while genotype diversity effects were not well represented by the way functional diversity was measured in this study.

    The study is based on an impressive experiment that will certainly allow achieving major insights into the role of genotype and species diversity on ecosystem functioning. However, there are some significant shortcomings in the methods that limit this study. In particular, the incomplete assessment of functional traits, herbivory, and fungal diversity across the subplots used for this study reduces statistical power. Specific measurements of traits, herbivory and fungal diversity in each plot would substantially simplify the design and the analyses and likely also reduce the unexplained variance observed in the study. However, this is nothing that can be changed now and has the likely explanation of feasibility constraints.

    The writing of the manuscript is generally good. However, given the somewhat diffuse results obtained for genetic diversity effects, they receive a lot of attention in the discussion, while species diversity effects are little mentioned. This could be better balanced and also referred back to the hypotheses. For example, I miss the discussion of the very clear hypothesis that genotype diversity effects are positive in species monocultures but neutral in species mixtures. How do your results fit with this hypothesis? My general impression is that the study is very well framed, but lacks to stick to this frame in the discussion. I am aware that this might be a challenge with the results obtained, but worth trying.

    Given the complex results obtained, I also feel that the title and main message received in the abstract do not fully reflect the results. Genetic diversity effects on productivity, but also on herbivory and fungal diversity, are not general (e.g. Fig. 2) nor are all genetic diversity effects on productivity mediated by functional diversity and trophic feedback. I think the title and main message of the study should be articulated more precisely.

  5. eLife

    Reviewer #2 (Public Review):

    This study aims to disentangle the contributions of genetic and species diversity to tree community fitness. It confirms the role of genetic diversity in functional and ecological traits but shows how these effects change when plant species diversity is increased, which can potentially add to our understanding of the interplay between plant diversity at various levels and community and ecosystem functions. It would be desirable to make emphasis whether differences between the effects of genetic and species diversity are comparable since they can act at complementary but different levels. It is hard to establish whether the effects of species diversity override the effects of genetic diversity by shared mechanisms; or whether a high species diversity reduces plant intraspecific interactions and the consequent effects of genetic diversity by density-dependent effects. However, this point has to be emphasized in the discussion.

    The experimental design has to be explained in more detail, in particular how plants were planted in the species monocultures. It is not stated whether the same or different species were used in the plots or in subplots. The design lacks proper replication for the treatment with high genetic diversity in species monocultures (n=2) which could lead to a biased result, especially if those plots were located in the same area.

  7. Version published to 10.1101/2022.03.25.485785v1 on bioRxiv