Long‐term heavy grazing increases community‐level foliar fungal diseases by shifting plant composition

Abstract

In grasslands, the interactions of foliar fungal diseases and their host plants are largely dependent on grazing by large herbivores. However, the relative importance of direct (i.e. pathogen removal) and indirect effects (i.e. via changes in plant community composition) of long‐term grazing on foliar fungal diseases remains largely unexplored, especially under varied grazing intensities. We conducted a 13‐year experiment to explore the effects of grazing intensity on foliar fungal diseases at both plant population and community levels in a semi‐arid grassland. We quantified the contributions of direct and indirect effects of long‐term grazing on community pathogen load. At the population level, the severity of five rusts and five powdery mildews decreased significantly as grazing intensity increased, whereas two leaf spots increased significantly in severity with increasing grazing intensity. Similarly, at the community level, the pathogen load of rusts and powdery mildews was negatively related to the increase in grazing intensity, whereas the pathogen load of leaf spots was positively related to grazing intensity. Overall, heavy grazing (i.e. 8.7 sheep/ha) significantly increased community pathogen load. Our SEM analysis showed that grazing indirectly increased the pathogen load of leaf spots by increasing disease proneness. Grazing decreased the pathogen load of rusts, but this could not be explained by changes in disease proneness. Overall, the indirect effects via changes in community composition of hosts resulting in the increase in community disease proneness outweighed the direct effect of grazing on community pathogen load. Synthesis and applications. Our study provides the first evidence that long‐term heavy grazing can indirectly increase community pathogen load by increasing the abundances of grazing‐tolerant hosts and decreasing the abundances of grazing‐intolerant hosts. These results provide empirical evidence that the pathogen load of foliar fungal diseases in grasslands can depend on the community context of hosts, which can, in turn, be controlled by large herbivores. We recommend that infectious diseases are considered when predicting the responses of grassland ecosystems to anthropogenic activities. Maintaining light to moderate grazing intensity or establishing an appropriate non‐grazing period could be an effective way to control foliar fungal diseases in grasslands.

Contrasting effects of sheep and cattle grazing on foliar fungal diseases by changing plant community characteristics

“…However, although we did find some direct effects of sheep on plant diseases (Liu, Duan, et al, 2021), changes in plant community structure overwhelmed the direct effects of grazing in our system.…”

“…Sheep directly increased biotrophic pathogen load, in line with findings for other mammalian grazers (Zhang et al., 2020) and studies in other systems (Richards et al., 2023) showing, for instance, that coral predators can increase disease through wounding and vectoring pathogens (Renzi et al., 2022). However, sheep grazing only directly facilitated the biotrophs, which might benefit especially from wounding (as shown for snail‐fungal interactions, Silliman & Newell, 2003), as they often consumed the upper parts of grass leaves (Liu, Duan, et al., 2021). The lack of a direct effect of cattle grazing might be due to the relatively low grazing intensity (less than 40% of above‐ground biomass was removed) and the strong changes in plant community composition and litter biomass with cattle grazing.…”

“…Fungal pathogens and their host plants usually co-occur with large vertebrate herbivores in grasslands and the herbivores can play an important role in affecting pathogen abundance (Borer et al, 2009;Liu, Mipam, et al, 2021). However, the impact of herbivores on pathogens remains controversial because different mechanisms may be important in different settings, or for different herbivores, and studies are unable to explain this variation because they typically do not test a range of different mechanisms by which different herbivores affect pathogen abundance (Liu, Duan, et al, 2021;Liu, Mipam, et al, 2021;Zhang et al, 2024). We therefore need to develop and test a mechanistic framework for how herbivores affect pathogens, by directly manipulating the presence of herbivores and simultaneously examining the multiple pathways by which they can impact pathogen infection.…”

Multiple dimensions of biodiversity mediate effects of temperature on invertebrate herbivory in a montane grassland

“…In addition to altering dimensions of plant community diversity, changing environmental conditions can also influence the abundance of particular species groups, which in turn, can alter plant–consumer interactions (Liu et al 2016, 2022, Galmán et al 2018, Moreira et al 2018, Halliday et al 2019, 2020). For example, along this same elevational gradient, low elevation, warmer sites, tended to be dominated by species with fast‐paced life history strategies, while high elevation, cooler sites were dominated by species with slow‐paced life history strategies, with impacts on plant disease severity (Halliday et al 2021).…”

Effects of Different Livestock Grazing on Foliar Fungal Diseases in an Alpine Grassland on the Qinghai–Tibet Plateau

“…Livestock grazing is one of the most intensive human activities in grasslands and is a major driver of the structure and function in these ecosystems [ 10 , 11 , 12 ]. Therefore, the occurrence and severity of foliar fungal diseases in grassland ecosystems largely depend on grazing by livestock [ 13 , 14 , 15 ]. There are two potential mechanisms to explain how grazing could affect foliar fungal diseases.…”