Interannual variation in land-use intensity enhances grassland multidiversity

Abstract

Although temporal heterogeneity is a well-accepted driver of biodiversity, effects of interannual variation in land-use intensity (LUI) have not been addressed yet. Additionally, responses to land use can differ greatly among different organisms; therefore, overall effects of land-use on total local biodiversity are hardly known. To test for effects of LUI (quantified as the combined intensity of fertilization, grazing, and mowing) and interannual variation in LUI (SD in LUI across time), we introduce a unique measure of whole-ecosystem biodiversity, multidiversity. This synthesizes individual diversity measures across up to 49 taxonomic groups of plants, animals, fungi, and bacteria from 150 grasslands. Multidiversity declined with increasing LUI among grasslands, particularly for rarer species and aboveground organisms, whereas common species and belowground groups were less sensitive. However, a high level of interannual variation in LUI increased overall multidiversity at low LUI and was even more beneficial for rarer species because it slowed the rate at which the multidiversity of rare species declined with increasing LUI. In more intensively managed grasslands, the diversity of rarer species was, on average, 18% of the maximum diversity across all grasslands when LUI was static over time but increased to 31% of the maximum when LUI changed maximally over time. In addition to decreasing overall LUI, we suggest varying LUI across years as a complementary strategy to promote biodiversity conservation.

Keywords: Biodiversity Exploratories; agricultural grasslands; biodiversity loss.

Fig. 1.

Organism groups used to calculate multidiversity. Of 49 taxonomic groups surveyed on 27 grasslands, 45 are shown on the tree. Eighteen groups were measured on all 150 grasslands, and 16 of them are shown in green on the tree. The groups WS3 and TM7 are candidate bacterial phyla. In addition to the groups shown on the tree, our analyses included lichens (150 plots), Homoptera (now considered paraphyletic but used as a group for convenience, 150 plots), viruses (27 plots), and a fungal subphylum incertae sedis (27 plots), which could not be placed on the tree. The tree was created based on National Center for Biotechnology Information taxonomy (www.ncbi.nlm.nih.gov/), and therefore shows relationships among groups but without true branch lengths.

Fig. 2.

Effect of LUI on multidiversity of 18 taxonomic groups of all species (A), relatively rare species (i.e., the 90% of species with the lowest total abundance) (B), and relatively common species (i.e., the 10% of species with the highest total abundance across plots) (C). Lines show model fits for different values of LUI_sd, from LUI_sd = 0 to the maximum interannual land-use change observed in any plot, LUI_sd = 1. In all cases, model predictions were calculated using multimodel averaging across all models in the 95% confidence set and were averaged across regions (more details are provided in Methods). In C, not all models in the 95% confidence set could be used for multimodel averaging because it would not be possible to average across different types of models (e.g., those with the compound LUI and those with individual components). AICc weights of models that could be used for multimodel averaging summed to 78%.

Fig. 3.

Response to LUI of scaled species richness for the 18 taxonomic groups measured on 150 plots. For each group, the predictions from the best-fit model are shown (Methods and Table S2). Where temporal variation in LUI (LUI_sd) appeared in the model, model fits are shown for different values of LUI_sd. (A–R) The groups are sorted in order of their response to LUI, from the group showing the strongest decline (A) to the strongest increase (R). For each group, changes in species richness with increasing LUI are shown beside the name of the group on the graph and were calculated as the difference between the relative species richness predicted by the model at minimum LUI (LUI = 0.5) and the predicted species richness at maximum LUI (LUI = 3.5). Model predictions were evaluated at the mean LUI_sd and were averaged across regions. AMF, arbuscular mycorrhizal fungi.

Fig. 4.

Response of the multidiversity of all 49 groups across 27 grasslands differed between the aboveground (A, 17 taxonomic groups) and belowground (B, 32 taxonomic groups) compartments. (A) Model predictions were calculated using multimodel averaging across all models in the 95% confidence set and were averaged across regions. (B) Best-fit model contained only mowing intensity.