While shoot herbivores reduce, root herbivores increase nutrient enrichment’s impact on diversity in a grassland model

Abstract

Nutrient enrichment is widespread throughout grassland systems and expected to increase during the Anthropocene. Trophic interactions, like aboveground herbivory, have been shown to mitigate its effect on plant diversity. Belowground herbivory may also impact these habitats' response to nutrient enrichment, but its influence is much less understood, and likely to depend on factors such as the herbivores' preference for dominant species and the symmetry of belowground competition. If preferential toward the dominant, fastest growing species, root herbivores may reduce these species' relative fitness and support diversity during nutrient enrichment. However, as plant competition belowground is commonly considered to be symmetric, root herbivores may be less impactful than shoot herbivores because they do not reduce any competitive asymmetry between the dominant and subordinate plants. To better understand this system, we used an established, two-layer, grassland community model to run a full-factorially designed simulation experiment, crossing the complete removal of aboveground herbivores and belowground herbivores with nutrient enrichment. After 100 yr of simulation, we analyzed communities' diversity, competition on the individual level, as well as their resistance and recovery. The model reproduced both observed general effects of nutrient enrichment in grasslands and the short-term trends of specific experiments. We found that belowground herbivores exacerbate the negative influence of nutrient enrichment on Shannon diversity within our model grasslands, while aboveground herbivores mitigate its effect. Indeed, data on individuals' above-and belowground resource uptake reveals that root herbivory reduces resource limitation belowground. As with nutrient enrichment, this shifts competition aboveground. Since shoot competition is asymmetric, with larger, taller individuals gathering disproportionate resources compared to their smaller, shorter counterparts, this shift promotes the exclusion of the smallest species. While increasing the root herbivores' preferences toward dominant species lessens their negative impact, at best they are only mildly advantageous, and they do very little reduce the negative consequences of nutrient enrichment. Because our model's belowground competition is symmetric, we hypothesize that root herbivores may be beneficial when root competition is asymmetric. Future research into belowground herbivory should account for the nature of competition belowground to better understand the herbivores' true influence.

Small‐scale heterogeneity shapes grassland diversity in low‐to‐intermediate resource environments

“…For grasslands, our findings confirmed that the effects of changes in compositional and configurational heterogeneity of below‐ground resources at fine centimeter‐size scales, as suggested by Schenk (2006), are indeed important. This aligns with recent studies by Crawford et al (2019, 2021), indicating that plant–plant interactions at such scales can be crucial for local plant community dynamics. In addition, plant responses to the spatial distribution patterns of nutrients are species‐specific.…”

“…To investigate the dynamics of the small‐scale heterogeneity–diversity relationship in a grassland community, we used a refined version of the dynamic IBC‐Grass model (an individual‐based model of grassland community) by May et al (2009), which simulates the fate of individual plants over time depending on above‐ and below‐ground resource availability. With this model, different scenarios of plant–plant and plant–environmental interactions have been tested, for example, the effects of varying nutrient content and mowing (May et al, 2009), shoot and root herbivory (Crawford et al, 2021), and habitat isolation on plant communities (Weiss et al, 2014). Other examples include the effects of below‐ground herbivory on the community (Körner et al, 2014; Pfestorf et al, 2016; Crawford et al, 2021), influence of grazing cessation (Weiss & Jeltsch, 2015), and role of intraspecific trait variability in species co‐existence (Crawford et al, 2019).…”

“…individuals (e.g., in grasslands; e.g., Schenk, 2006). Indeed, recent research indicates that plant-plant interactions at such scales can be crucial for understanding local plant community dynamics (e.g., Crawford et al, 2019Crawford et al, , 2021.…”

“…Other examples include the effects of below-ground herbivory on the community (Körner et al, 2014;Pfestorf et al, 2016;Crawford et al, 2021), influence of grazing cessation (Weiss & Jeltsch, 2015), and role of intraspecific trait variability in species co-existence (Crawford et al, 2019). Pfestorf et al (2016) F I G U R E 2 A set of derivative resource maps generated with different levels of patchiness of resource availability derived from empirical soil carbon-to-nitrogen ratio measurements.…”

“…Furthermore, to date, small‐scale variations in soil parameters have not been tested on a scale of centimeters, which is relevant for interactions between small plant individuals (e.g., in grasslands; e.g., Schenk, 2006). Indeed, recent research indicates that plant–plant interactions at such scales can be crucial for understanding local plant community dynamics (e.g., Crawford et al, 2019, 2021).…”