Assessing the roles of nitrogen, biomass, and niche dimensionality as drivers of species loss in grassland communities

Abstract

Eutrophication is a major driver of species loss in plant communities worldwide. However, the underlying mechanisms of this phenomenon are controversial. Previous studies have raised three main explanations: 1) High levels of soil resources increase standing biomass, thereby intensifying competitive interactions (the “biomass-driven competition hypothesis”). 2) High levels of soil resources reduce the potential for resource-based niche partitioning (the “niche dimension hypothesis”). 3) Increasing soil nitrogen causes stress by changing the abiotic or biotic conditions (the “nitrogen detriment hypothesis”). Despite several syntheses of resource addition experiments, so far, no study has tested all of the hypotheses together. This is a major shortcoming, since the mechanisms underlying the three hypotheses are not independent. Here, we conduct a simultaneous test of the three hypotheses by integrating data from 630 resource addition experiments located in 99 sites worldwide. Our results provide strong support for the nitrogen detriment hypothesis, weaker support for the biomass-driven competition hypothesis, and negligible support for the niche dimension hypothesis. The results further show that the indirect effect of nitrogen through its effect on biomass is minor compared to its direct effect and is much larger than that of all other resources (phosphorus, potassium, and water). Thus, we conclude that nitrogen-specific mechanisms are more important than biomass or niche dimensionality as drivers of species loss under high levels of soil resources. This conclusion is highly relevant for future attempts to reduce biodiversity loss caused by global eutrophication.

Keywords: fertilization; meta-analysis; nutrient enrichment; productivity; species diversity.

Fig. 1.

General characteristics of the data included in our meta-analysis. (A) Geographical distribution of the sites included in the meta-analysis [red, sites of the nutrient network included in Harpole et al.’s study (8); green, other sites]. (B) The experimental treatments included in the meta-analysis and their prevalence in the dataset.

Fig. 2.

Predicted species richness (mean ± 95% CI) as a function of (A) standing biomass, (B) the number of added resources, and (C) the presence of nitrogen. (A) Prediction is based on a mixed-effects linear model with the linear and quadratic terms of biomass as fixed effects (conditional R² = 0.888, marginal R² = 0.073). (B) Blue, prediction of a mixed-effects linear model with the number of resources treated as a continuous variable (conditional R² = 0.879, marginal R² = 0.024); red, predictions of a mixed-effects model with the number of resources treated as dummy variables (conditional R² = 0.880, marginal R² = 0.025). Data for four added resources are not shown due to small sample size. (C) Predictions are based on a mixed-effects model with three levels of resource addition treatments: control (red, no addition), treatments that do not include nitrogen (blue, N = 0), and treatments that include nitrogen (blue, N = 1, conditional R² = 0.889, marginal R² = 0.031). Biomass and richness are in logarithmic scale. See SI Appendix, Table S3 for statistical details.

Fig. 3.

Results of a structural equation model testing the three hypotheses together (the biomass-driven competition hypothesis, the niche dimension hypothesis, and the nitrogen detriment hypothesis). The model includes two equations; one with composite biomass as the response variable (conditional R² = 0.83, marginal R² = 0.07); another with species richness as the response variable (conditional R² = 0.9, marginal R² = 0.05). The observed variables are represented in rectangles. The hexagon indicates a composite variable (biomass-predicted species richness, including the linear and quadratic terms of biomass). Arrows show structural relationships (solid arrows indicate a positive effect, while dashed arrows indicate a negative effect). Black arrows represent significant (P < 0.05) relationships, and the gray arrow represents the nonsignificant relationship. Numbers near arrows are standardized coefficients obtained by local estimation. ***P < 0.001. The model was tested against nested unsaturated models and was found to be the best according to the AICc. See SI Appendix, Table S5 for details. Note that interpretation of arrows related to the composite variable within SEM differs from other types of variables (see details in Methods).

Fig. 4.

Effects of the four resources examined in our analysis (N, P, K, and water) on (A) standing biomass and (B) species richness. Data shown are estimates of the predicted effects on (A) biomass and (B) richness, as estimated by mixed-effects models including all resources and their combinations (NP, NK, PK, NPK, and NPK with water) as fixed effects, without (blue) and with (red) biomass as a predictor in the model. Interactions are not shown, since they were statistically insignificant. For ease of interpretation, the estimated effects (mean ± 95% CI) of each resource were transformed into percentage gain/loss of (A) biomass and (B) richness relative to the control (the dashed lines). See SI Appendix, Table S6 for details of the biomass model, and see SI Appendix, Table S7 for the richness model.