Abstract
Soils support a highly diverse community of plant pathogens, which are highly responsive to global change. Climate and livestock grazing are the main global changes in grasslands, yet, how long-term grazing alone, and in interaction with climate, influence the distribution of soil-borne plant pathogens remain virtually unknown. Here, we present the first long-term regional-scale experimental investigation on the impacts of livestock grazing on soil-borne fungal plant pathogens and their association with plant community across 10 experimental sites spanning a climate gradient in the steppe in Northern China. Our results showed that long-term grazing effects on the diversity and proportion of soil-borne fungal plant pathogens are strongly controlled by temperature, with grazing increasing pathogen richness and proportions largely in cooler grasslands. We further show that long-term grazing supported stronger connections between soil-borne fungal pathogens and plant communities. Our work demonstrates that climate controls the effects of grazing on plant pathogens, which is critical to understand and manage grasslands in a changing world.
Similar content being viewed by others
Introduction
Soil-borne plant pathogens represent an important reservoir of root and leaf pathogens1,2,3 that drive plant disease outbreaks4,5 and affect plant physiology, plant survival, and biomass production6,7,8. In the face of a multitude of global changes, the importance of understanding the community dynamics of soil-borne plant pathogens will grow4,9,10. Long-term grazing by livestock is, in fact, the most important global change in grasslands and poses great potential threats to grassland ecosystem around the globe11,12,13,14. Growing evidence showed that grazing significantly affects soil microbial community15,16 by altering plant community through foraging17 and influencing soil properties via trampling and returning excreta18,19. However, within soil microbes, the effect of grazing on soil-borne fungal plant pathogens and its link with plant community is less well known.
To date, only a few studies examined the grazing impacts on soil-borne fungal plant pathogens community, and found conflicting results20,21,22,23,24. For example, Bai et al.24 found that grazing in a semi‑arid steppe significantly reduced the richness of soil-borne fungal plant pathogens, while Che et al.21 found no effects of grazing on soil-borne fungal plant pathogens in a Tibetan alpine meadow. Different types of grasslands exhibit various climate variables like temperature and precipitation, which were also found to be important driver of soil-borne fungal pathogen community10,25,26. For example, soil-borne fungal plant pathogens are expected to increase in a warmer planet impacting the productivity and health of grasslands10,27. However, how grazing interacts with climatic factors in driving soil-borne fungal plant pathogens remains poorly understood.
Long-term livestock grazing might further influence the associations between pathogen community and plant community. The interactions between plants and pathogens vary depending on functional traits of plant community28,29. Communities dominated by species with fast-growing traits such as higher nitrogen content may have higher pathogen infection than communities dominated by species with slow-growing traits6,30,31. It was found that livestock grazing can alter plant community functional traits32,33, thus likely alter potential pathogen infection34,35. In particular, the long-term effects of livestock grazing can influence the co-evolution of pathogens and plant communities36. For example, grazing can alter plant species richness and lead to a turnover of plant community species, where perennial species with slow-growing traits are replaced by annual fast-growing species37,38,39. Moreover, grazing can regulate the functional trait composition of plant communities through intraspecific trait variation40. Grazing can lead to increased species root nitrogen content33 the main functional trait that affecting potential pathogen infection41, especially for the dominant species with the higher density in plant communities. However, we still lack empirical evidence of long-term grazing impacts on the relationship between soil-borne fungal plant pathogens and the plant community, despite which is of important significance for predicting the potential roles of pathogen in controlling plant community with increasing livestock grazing disturbance worldwide.
The present study aimed to investigate the effects of long-term grazing on soil-borne fungal plant pathogen community and its link with plant community using a long-term standardized livestock exclusion experiment at 10 sites across a climate gradient encompassing several grassland types in northern China (meadow steppe, typical steppe, and desert steppe from east to west) (Supplementary Table 1, Fig. 1a; see ref. 39). This is one of the largest remaining continuous grasslands in the world. We hypothesized that long-term grazing by livestock can interact with climate to drive soil-borne pathogen diversity and proportion, and can further strengthen associations between soil-borne fungal plant pathogen community with the plant community. Temperature is already known to increase soil-borne fungal plant pathogen proportion10 which may dilute the potential effect of grazing on pathogens. Thus, we expect that the influence of grazing may be more noticeable in colder locations where grazing may promote the proportion and diversity of these important soil-borne pathogens and potential risk of plant pathogens infection with consequences for the productivity of grasslands.
a Distribution of sampling sites in northern China (sites are skewed to avoid overlap to clarify where different sites are located), and vegetation contrast inside and outside exclosures in the three grassland types: meadow steppe, typical steppe and desert steppe. b Non-metric multidimensional scaling (NMDS) analysis showed the community composition of soil-borne plant pathogen communities in non-grazed (n = 50) and grazed grasslands (n = 50). Source data are provided as a Source Data file.
Results and discussion
To the best of our knowledge, this study represents the first regional-scale experiment to investigate the effects of decades of continuous grazing on grassland soil-borne pathogen community, and their links with plant communities. Our work provides new experimental evidence that long-term livestock grazing significantly impacted soil-borne fungal plant pathogen richness and proportions, and which were regulated by temperature (Fig. 2; Supplementary Tables 2, 5). We further provide evidence that long-term grazing increased soil-borne plant pathogen richness and proportions in the cooler sites, and rising temperature can mitigate these promoting effects of grazing (Fig. 2; Supplementary Table 5). Furthermore, long-term livestock grazing strengthened the associations between plant community and soil-borne fungal plant pathogen community across the temperature gradient (Fig. 3; Supplementary Tables 3, 6).This knowledge is critical to better manage the future of grasslands in a changing world.
a Relationships between temperature and the effects of grazing on the proportions of soil-borne fungal plant pathogen. b Relationships between temperature and the effects of grazing on soil-borne fungal plant pathogen species richness. Temperature was included as a fixed factor, and plots nested within grassland types were taken as random factors to control for pseudo-replication (n = 50). The fitted line is from the linear mixed-effects models, showed significant relationships; P ≤ 0.05. Log response ratios (LRRs) compare soil-borne fungal plant pathogen proportions and richness outside and inside exclosures. Values > 0 represent positive livestock grazing effects, while values < 0 represent negative livestock grazing effects. For exact statistical values, see Supplementary Table 5. Source data are provided as a Source Data file.
Relationships between plant species richness and soil-borne fungal plant pathogens richness across (a) non-grazed and (b) grazed grasslands. Relationships between plant Simpson’s evenness index and proportions of soil-borne fungal plant pathogens across (c) non-grazed and (d) grazed grasslands. Temperature and precipitation were also fitted as fixed factors to control results by any influence of climate, and plots nested within grassland types were taken as random factors to control for pseudo-replication (n = 50). The fitted line is from the linear mixed-effects models, showed the significant relationships; P ≤ 0.05. For exact statistical values, see Supplementary Table 6. Source data are provided as a Source Data file.
Temperature controls the effects of grazing on plant pathogens
Our study provided evidence that long-term livestock grazing had significant impacts on soil-borne plant pathogen community composition (Stress = 0.16, P < 0.01, Fig. 1b), and temperature determine the magnitude and direction of the effects of long-term grazing on soil-borne fungal plant pathogens proportions and richness (Fig. 2; Supplementary Tables 2, 5). Supporting our hypothesis, long-term grazing increased soil-borne fungal plant pathogen richness and proportions in cooler grasslands, and the positive effects gradually weakened with the temperate increase, even was reversed in warmest grasslands (P = 0.05, Fig. 2a; P = 0.02, Fig. 2b; Supplementary Table 5).
Temperature was found to exhibit strong effect on the proportions of potential fungal plant pathogens in soil in a newest global scale study10. Grazing is known to increase soil temperature by decreasing canopy cover and litter42,43,44. In cooler grasslands, this increase in temperature could lead to positive effects on both richness and proportions of pathogens45. However, in warmer grasslands, the strong effects of high temperature could dilute the potential effect of grazing on pathogens. It is also possible that the rise in soil temperature caused by grazing may surpass the upper threshold limit for pathogen46,47,48. Previous studies also indicated that the way pathogens respond to temperature can differ depending on the range of temperatures being investigated49,50,51,52. Moreover, livestock dung and urine deposition can create nutrient-enriched environments which frequently encourage the thriving of soil-borne fungal pathogens24,31,53,54,55. However, these effects may be mitigated with increasing temperature, which can decrease the water content of feces56, and consequently may not be conducive to the thriving of soil-borne fungal pathogens.
Grazing resulted in stronger connections between soil-borne fungal pathogen community and plant community
Our results showed that while pathogen richness was positively linked with plant richness (P = 0.03, Fig. 3b; Supplementary Table 6) and pathogen proportions were negatively linked with plant Simpson’s evenness index (P < 0.01, Fig. 3d; P = 0.01, Supplementary Fig. 2b; Supplementary Table 6) in grazed grasslands, these relationships were absent in non-grazed grasslands (Fig. 3a; Fig. 3c; Supplementary Fig. 2a; Supplementary Table 6). The increased plant species richness found in our grazed grasslands (P = 0.03, Supplementary Fig 1a) resulted in a greater number of potential host species. This, in turn, could support a diverse community of specialized pathogens57. Consequently, there might be a stronger association between plant species richness and the richness of soil-borne fungal plant pathogens in grazed grasslands (Fig. 3b; Supplementary Table 6). Moreover, our previous study show that long-term grazing led to an increase in the relative abundance of annual species with fast-growing traits39. These species typically have higher nitrogen content, resulting in lower defense capabilities58,59 and making them more susceptible to infection by pathogens. In addition, grazing can increase soil nitrogen concentration by returning readily accessible nitrogen in urine and dung19,60, thereby changing plant root nitrogen concentration, as our results showed the increased community-level root nitrogen concentration in grazed grasslands (P < 0.01, Fig. 4a; Supplementary Table 7). The strengthened associations between the plant community and pathogen community may also be attributed to the improved root nitrogen concentration (Fig. 4a; Supplementary Table 7), which acts as a crucial survival resources for pathogens61.
The effect of grazing on (a) community-level root nitrogen concentration and (b) dominant species root nitrogen concentration. Temperature and precipitation were also fitted as fixed factors to control results by any influence of climate, and plots nested within grassland types were taken as random factors to control for pseudo-replication (n = 50). The line in the middle of the box represents the median, while the upper and lower hinges indicate the first and third quartiles, marking the central 50% of the data distribution. The two-tailed statistical tests indicate significant effects by ***P ≤ 0.001. For exact statistical values, see Supplementary Table 7. Source data are provided as a Source Data file.
On the other hand, grazing can alter trait values within species62,63. For example, in response to the detrimental effects of defoliation, plants may increase nitrogen uptake to support regrowth and recovery64. Such change may increase the susceptibility of plants to pathogens34,35, especially for dominant species with the higher density in plant communities, which could lead to more efficient density-dependent transmission for pathogens6,65. Our result also revealed a significant negative correlation between relative abundance of soil-borne fungal plant pathogens and plant Simpson’s evenness index (with lower values signifying increased predominance by a single species) in grazed grasslands (Fig. 3d; Supplementary Fig. 2b; Supplementary Table 6), even though grazing itself did not have a significant effect on the plant Simpson’s evenness index (Supplementary Fig. 1b). It is possible that the negative correlation results from the increased sensitivity of dominant plants species to pathogens. Our results also showed that long-term grazing increased the root nitrogen concentration of dominant plant species (P < 0.01, Fig. 4b; Supplementary Table 7), which can increase their susceptibility to pathogens34,35, thus facilitating more effective density-dependent spread of pathogens6.
Conclusions
In summary, our results from a replicated experiment across broad climate gradients highlight that temperature is a key moderator of the long-term impacts of managed grazing on soil-borne potential fungal plant pathogens. Long-term livestock grazing poses greater potential threats to plant pathogen infections in cooler grasslands, and rising temperatures can mitigate the promoting effects of grazing on plant pathogens. Our results may have implications for the management and conservation of grasslands, particularly with projected future global change and its potential influence on plant pathogens. Given the enhancement of pathogen reservoirs (both the diversity and proportions) under grazing conditions in cooler regions, as well as the closer relationship between plants and pathogens, we suggest that the risk of plant pathogen outbreaks should be given more concern in cooler and experiencing long-term grazing grasslands.
Materials and methods
Sampling sites
The study area was located in grasslands of Eurasian steppe in Northern China (111.23 E to 123.51 E, 41.25N to 49.52N), where the climate is predominantly arid and semi-arid continental, the mean annual precipitation ranged from 232 mm to 435 mm. To generate enough variability to test the interactive effects of climate and grazing on soil-borne fungal plant pathogens community, we selected experimental sites across a climate gradient spanning three major types of grasslands including meadow steppe, typical steppe and desert steppe along 1100 km east to west transect39 (See Fig. 1a and Supplementary Table 1 for details of the study sites). All of these sites have experienced over half a century of continuous grazing, primarily by sheep and goats, followed by cattle and horses. At each experimental site, a grazing exclosure spanning over ten years was established by erecting a fence to prevent livestock grazing in the area. A full description of our study area and experimental setups can be found in ref. 39. We estimated key climate variables, mean annual temperature (hereafter temperature) and mean annual precipitation (hereafter precipitation) using datafrom the WorldClim global database66 (https://www.worldclim.org/).
Field sampling and measurements
In late July–August of 2020, during the period of peak annual standing biomass, we sampled plant communities and soils for plant pathogens. The sampling was conducted using regional paired comparison and replicated site methods. At each site, we randomly selected a 50 m × 50 m plot from the exclosure and another 50 m × 50 m plot from the adjacent grazed grasslands. We sampled plants in five 1 m2 quadrats placed at the four corners and the center of each plot. In each quadrat, we recorded the presence of each plant species in the quadrat, and calculated species richness as the total number of species in a quadrat. We also calculated the Simpson’s evenness index as the inverse Simpson index divided by the number of species observed, which expresses how evenly the individuals in the community are distributed over the different species. The community becomes more and more dominated by one species when it approaches 0. The inverse Simpson index was calculated using diversity function within the R package vegan. Subsequently, we measured root nitrogen concentration (the main plant functional trait affecting pathogen infection41) on several species of plants that were among the more common species at each site (those comprising at least 90% of the total plant abundance in each site; Supplementary Table 4). We randomly selected at least 5 mature plants from each species in each quadrat, ensuring a comprehensive sample for our analysis. For each sampled plant, we carefully excavated the root system and cleared away all soil attached to the roots. The samples were then vacuum-sealed and frozen at −18 °C in preparation for chemical analysis. Then, we washed the fine roots of each samples (root diameter <2 mm) in deionized water, oven-dried them at 65 °C for 48 h. The dried roots were ground to powder to measure root nitrogen concentration with a Discrete Auto Analyzer (Smartchem 600, AMS Alliance, Italy). We calculated the community-weighted means of root nitrogen concentration for each quadrat in the non-grazed and grazed plots at each site33, as well as the root nitrogen concentration of the most dominant species at each site.
We collected soil samples by taking five soil cores (2.5-cm diameter) at 10 cm depth in each of the five 1 m2 quadrats at each site. We combined the five soil cores from each quadrat to form one composite sample, removed coarse material (rocks and roots), and kept the sample in a freezer (MOBICOOL CoolFreeze CF-50) at −20 °C prior to soil microbial community analysis.
Microbial community analyses
To characterize the soil-borne pathogens, we extracted microbial DNA using the PowerSoil DNA Isolation Kit (Mo Bio Laboratories, Carlsbad, CA, USA) according to the manufacturer’s protocols. We determined the final DNA concentration and purification using a NanoDrop 2000 UV-vis spectrophotometer (Thermo Scientific, Wilmington, USA). Fungal communities were assessed using the forward primer ITS-1F (5′-CTTGGTCATTTAGAGGAAGTAA-3′) and the reverse primer ITS-2R (5′-GCTGCGTTCTTCATCGATGC-3′). The PCR reactions were conducted as described in ref. 39. The MiSeq sequences were demultiplexed and quality-filtered using Trimmomatic, requiring an average quality score above 20 over a 50 bp sliding window. Sequences with an overlap greater than 10 bp were merged based on their overlapping sequences. Reads containing ambiguous bases were removed, and paired-end reads were joined with a minimum 10 bp overlap using FLASH version 1.2.7, allowing up to two mismatched nucleotides. Operational taxonomic units (OTUs) were defined using UPARSE version 7.167 with a 97% similarity threshold for clustering. Singleton OTUs and chimeric sequences, identified by the UCHIME algorithm, were also removed. For ITS, we assigned taxonomy using the UNITE reference database68. We obtained the proportions of potential fungal plant pathogens from the amplicon sequencing analyses as inferred by parsing the soil phylotypes using FungalTraits69. Finally, we calculated the proportions of potential fungal plant pathogens as the percentage of OTUs belonging to the group out of the total fungal OTUs for the sample. Fungal pathogen richness (OTU richness) was calculated as the sum of the fungal pathogen OTUs present in each sample. To minimize the effects of sequencing depth on community composition index measure, the number of gene sequences from each sample was rarefied to compare all samples at equivalent sequencing depths corresponding to the lowest sequencing coverage.
Statistical analysis
We employed pairwise Adonis tests and non-metric multidimensional scaling (NMDS) to visually compare the species compositional differences in the soil-borne fungal plant pathogen communities in non-grazed and grazed grasslands. We then used linear mixed-effects models (LMMs) to analyze the interactive effects of grazing and climate on soil-borne fungal plant pathogen richness and proportions. In these models, grazing, climate factors (temperature and precipitation), and their interaction were included as fixed factors, and plots nested within grassland types were treated as random factors to control for pseudo-replication. Soil-borne fungal plant pathogen richness was log-transformed to linearize the data before analysis, which was applied throughout all relevant analyses. Next, we fitted LMMs to explore the relationship between temperature and the effects of grazing on soil-borne fungal plant pathogen richness and proportions across the 10 sites. The effects of grazing on soil-borne fungal plant pathogen richness and proportions were estimated as the log ratio of these factors in non-grazed grassland divided by that in grazed grassland, log (grazed/non-grazed).
Further, partial Mantel test was utilized to test the correlations between plant community and soil-borne fungal plant pathogen community excluding the effects of climate factors (temperature and precipitation) in non-grazed and grazed grasslands, respectively. Then, we used LMMs to analyze the relationship between plant species richness and soil-borne fungal plant pathogen richness, and relationship between plant Simpson’s evenness index and soil-borne fungal plant pathogen proportions in non-grazed and grazed grasslands, respectively. In these LLMs, climate factors (temperature and precipitation) were also fitted as fixed factors to control our results by any influence of climate, and plots nested within grassland types were taken as random factors to control for pseudo-replication. These analyses were performed on standardized fixed variables using Z-Score standardization (deviation from mean/SD). For all the significant relationships in the LLMs, the regression lines were fitted with the slope and intercept extracted from the LLMs. In addition, we further run LMMs including grazing as predictor variable to analyze the effects of grazing on plant species richness, plant Simpson’s evenness index, community-level root nitrogen concentration and dominant species root nitrogen concentration with climate factors (temperature and precipitation) also fitted as fixed factors and plots nested within grassland types as random factors. Plant species richness was log-transformed to linearize the data. Linear mixed-effects modeling was performed using the lme function within the nlme package. Pairwise Adonis tests with Bonferroni correction were performed using the pairwise.adonis function from the pairwiseAdonis package. Partial Mantel test was performed using the mantel.partial function within the vegan package. All statistical tests were performed using an alpha level of 0.05. All statistical analyses were performed using R (version 4.3.1, R Core Team, 2023).
Statistics and reproducibility
All the statistical analyses described above can be reproduced by following the procedures outlined. The data and R scripts necessary to perform these analyses are available in the Data Availability and Code Availability sections.
Reporting summary
Further information on research design is available in Nature Portfolio Reporting Summary linked to this article.
Data availability
All data that support the findings of this study are available in the Figshare database (https://doi.org/10.6084/m9.figshare.27636804)70. The mean annual temperature and mean annual precipitation of each site were obtained from the WorldClim global database66 (https://www.worldclim.org/). Source values underlying the figures can be found in supplementary data.
Code availability
R scripts used for data analysis have been deposited in the Figshare database (https://doi.org/10.6084/m9.figshare.27636804)70.
References
Gilbert, G. S. Evolutionary ecology of plant diseases in natural ecosystems. Annu. Rev. Phytopathol. 40, 13–43 (2002).
Tkacz, A., Bestion, E., Bo, Z., Hortala, M. & Poole, P. S. Influence of plant fraction, soil, and plant species on microbiota: a multikingdom comparison. mBio 11, e02785-19 (2020).
Gong, T. & Xin, X.-F. Phyllosphere microbiota: community dynamics and its interaction with plant hosts. J. Integr. Plant Biol. 63, 297–304 (2021).
Chakraborty, S. & Newton, A. C. Climate change, plant diseases and food security: an overview. Plant Pathol. 60, 2–14 (2011).
Fisher, M. C. et al. Emerging fungal threats to animal, plant and ecosystem health. Nature 484, 186–194 (2012).
Bever, J. D., Mangan, S. A. & Alexander, H. M. Maintenance of plant species diversity by pathogens. Annu. Rev. Ecol. Evol. Syst. 46, 305–325 (2015).
Jeger, M. J., Salama, N. K. G., Shaw, M. W., van den Berg, F. & van den Bosch, F. Effects of plant pathogens on population dynamics and community composition in grassland ecosystems: two case studies. Eur. J. Plant Pathol. 138, 513–527 (2014).
Rottstock, T., Joshi, J., Kummer, V. & Fischer, M. Higher plant diversity promotes higher diversity of fungal pathogens, while it decreases pathogen infection per plant. Ecology 95, 1907–1917 (2014).
Delavaux, C. S. et al. Root pathogen diversity and composition varies with climate in undisturbed grasslands, but less so in anthropogenically disturbed grasslands. ISME J. 15, 304–317 (2021).
Delgado-Baquerizo, M. et al. The proportion of soil-borne pathogens increases with warming at the global scale. Nat. Clim. Chang. 10, 550 (2020).
Allan, E. et al. Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition. Ecol. Lett. 18, 834–843 (2015).
Eldridge, D. J. et al. Competition drives the response of soil microbial diversity to increased grazing by vertebrate herbivores. Ecology 98, 1922–1931 (2017).
Wang, L. et al. Diversifying livestock promotes multidiversity and multifunctionality in managed grasslands. Proc. Natl. Acad. Sci. USA 116, 6187–6192 (2019).
Wang, L. et al. Livestock overgrazing disrupts the positive associations between soil biodiversity and nitrogen availability. Funct. Ecol. 34, 1713–1720 (2020).
Wang, Z. et al. Impact of long-term grazing exclusion on soil microbial community composition and nutrient availability. Biol. Fertil. Soils 55, 121–134 (2019).
Wang, C. et al. Grazing and nitrogen addition restructure the spatial heterogeneity of soil microbial community structure and enzymatic activities. Funct. Ecol. 35, 2763–2777 (2021).
Yang, H. et al. Diversity-dependent stability under mowing and nutrient addition: evidence from a 7-year grassland experiment. Ecol. Lett. 15, 619–626 (2012).
Sorensen, L. I., Mikola, J., Kytoviita, M.-M. & Olofsson, J. Trampling and spatial heterogeneity explain decomposer abundances in a sub-arctic grassland subjected to simulated reindeer grazing. Ecosystems 12, 830–842 (2009).
Liu, C. et al. Towards a mechanistic understanding of the effect that different species of large grazers have on grassland soil N availability. J. Ecol. 106, 357–366 (2018).
Eldridge, D. J. & Delgado-Baquerizo, M. Functional groups of soil fungi decline under grazing. Plant Soil 426, 51–60 (2018).
Che, R. et al. Total and active soil fungal community profiles were significantly altered by six years of warming but not by grazing. Soil Biol. Biochem. 139, 107611 (2019).
Wang, J., Liu, G., Zhang, C. & Wang, G. Effect of long-term destocking on soil fungal functional groups and interactions with plants. Plant Soil 448, 495–508 (2020).
Wang, J., Wang, X., Liu, G., Wang, G. & Zhang, C. Grazing-to-fencing conversion affects soil microbial composition, functional profiles by altering plant functional groups in a Tibetan alpine meadow. Appl. Soil Ecol.166, 104008 (2021).
Bai, H. et al. Soil fungi regulate the response of plant production-community composition relationship to grazing and mowing in a semi-arid steppe. Plant Soil 473, 573–589 (2022).
Tedersoo, L. et al. Global diversity and geography of soil fungi. Science 346, 1078 (2014).
Ochoa-Hueso, R. et al. Drought consistently alters the composition of soil fungal and bacterial communities in grasslands from two continents. Glob. Change Biol. 24, 2818–2827 (2018).
Singh, B. K. et al. Climate change impacts on plant pathogens, food security and paths forward. Nat. Rev. Microbiol. 21, 640–656 (2023).
Albornoz, F. E., Burgess, T. I., Lambers, H., Etchells, H. & Laliberte, E. Native soilborne pathogens equalize differences in competitive ability between plants of contrasting nutrient-acquisition strategies. J. Ecol. 105, 549–557 (2017).
Laliberte, E., Lambers, H., Burgess, T. I. & Joseph Wright, S. Phosphorus limitation, soil-borne pathogens and the coexistence of plant species in hyperdiverse forests and shrublands. N. Phytol. 206, 507–521 (2015).
Gianoli, E. & Salgado-Luarte, C. Tolerance to herbivory and the resource availability hypothesis. Biol. Lett. 13, 20170120 (2017).
Cappelli, S. L., Pichon, N. A., Kempel, A. & Allan, E. Sick plants in grassland communities: a growth-defense trade-off is the main driver of fungal pathogen abundance. Ecol. Lett. 23, 1349–1359 (2020).
Wang, C., Li, X., Lu, X., Wang, Y. & Bai, Y. Intraspecific trait variation governs grazing-induced shifts in plant community above- and below-ground functional trait composition. Agric. Ecosyst. Environ. 346, 20170120 (2023).
Cai, J. et al. Below-ground root nutrient-acquisition strategies are more sensitive to long-term grazing than above-ground leaf traits across a soil nutrient gradient. Funct. Ecol. 38, 1475–1485 (2024).
Paap, T., Burgess, T. I., Rolo, V., Steel, E. & Hardy, G. E. S. J. Anthropogenic disturbance impacts stand structure and susceptibility of an iconic tree species to an endemic canker pathogen. Ecol. Manag. 425, 145–153 (2018).
Ebeling, A. et al. Nutrient enrichment increases invertebrate herbivory and pathogen damage in grasslands. J. Ecol. 110, 327–339 (2022).
Zhao, X. et al. Effects of livestock overgrazing on the relationships between plant and microbial diversity across the temperate steppes in northern China. Land Degrad. Dev. 34, 1197–1207 (2023).
Lajoie, G. & Vellend, M. Understanding context dependence in the contribution of intraspecific variation to community trait-environment matching. Ecology 96, 2912–2922 (2015).
Hanke, W. et al. The impact of livestock grazing on plant diversity: an analysis across dryland ecosystems and scales in southern Africa. Ecol. Appl. 24, 1188–1203 (2014).
Zhang, M. et al. Experimental impacts of grazing on grassland biodiversity and function are explained by aridity. Nat. Commun. 14, 5040 (2023).
Niu, K., He, J.-S. & Lechowicz, M. J. Grazing-induced shifts in community functional composition and soil nutrient availability in Tibetan alpine meadows. J. Appl. Ecol. 53, 1554–1564 (2016).
Lozano, Y. M., Aguilar-Trigueros, C. A., Roy, J. & Rillig, M. C. Drought induces shifts in soil fungal communities that can be linked to root traits across 24 plant species. N. Phytol. 232, 1917–1929 (2021).
Shen, X., Liu, B., Li, G., Yu, P. & Zhou, D. Impacts of grassland types and vegetation cover changes on surface air temperature in the regions of temperate grassland of China. Theor. Appl. Climatol. 126, 141–150 (2016).
Yan, Y. et al. Grazing modulates soil temperature and moisture in a Eurasian steppe. Agric. Meteorol. 262, 157–165 (2018).
Zhang, H., Fan, J., Gao, D., Liu, Y. & Du, H. Effect of decreasing the interception of solar illuminance by vegetation on ground temperature in degraded grasslands. Sustainability 14, 4488(2022).
Pfender, W. F. & Vollmer, S. S. Freezing temperature effect on survival of Puccinia graminis subsp graminicola in Festuca arundinacea and Lolium perenne. Plant Dis. 83, 1058–1062 (1999).
Thompson, S., Alvarez-Loayza, P., Terborgh, J. & Katul, G. The effects of plant pathogens on tree recruitment in the Western Amazon under a projected future climate: a dynamical systems analysis. J. Ecol. 98, 1434–1446 (2010).
Bachelot, B. et al. Altered climate leads to positive density-dependent feedbacks in a tropical wet forest. Glob. Chang. Biol. 26, 3417–3428 (2020).
Liu, Y. & He, F. Warming shifts soil microbial communities and tropical tree seedling mortality. Ecology 103, e3810 (2022).
Manici, L. M., Bregaglio, S., Fumagalli, D. & Donatelli, M. Modelling soil borne fungal pathogens of arable crops under climate change. Int. J. Biometeorol. 58, 2071–2083 (2014).
Thompson, S. E., Levin, S. & Rodriguez-Iturbe, I. Rainfall and temperatures changes have confounding impacts on Phytophthora cinnamomi occurrence risk in the southwestern USA under climate change scenarios. Glob. Chang. Biol. 20, 1299–1312 (2014).
Yang, L.-N. et al. Trade-offs and evolution of thermal adaptation in the Irish potato famine pathogen Phytophthora infestans. Mol. Ecol. 25, 4047–4058 (2016).
Zhan, J., Ericson, L. & Burdon, J. J. Climate change accelerates local disease extinction rates in a long-term wild host-pathogen association. Glob. Chang. Biol. 24, 3526–3536 (2018).
Burdon, J. J., Thrall, P. H. & Ericson, L. The current and future dynamics of disease in plant communities. Annu. Rev. Phytopathol. 44, 19–39 (2006).
Lekberg, Y. et al. Nitrogen and phosphorus fertilization consistently favor pathogenic over mutualistic fungi in grassland soils. Nat. Commun. 12, 3484 (2021).
Du, S. et al. The proportion of soil-borne fungal pathogens increases with elevated organic carbon in agricultural soils. mSystems 7, e01337–21 (2022).
Zhang, M. et al. Effects of herbivore assemblage on the spatial heterogeneity of soil nitrogen in eastern Eurasian steppe. J. Appl. Ecol. 57, 1551–1560 (2020).
Eck, J. L., Stump, S. M., Delavaux, C. S., Mangan, S. A. & Comita, L. S. Evidence of within-species specialization by soil microbes and the implications for plant community diversity. Proc. Natl. Acad. Sci. USA 116, 7371–7376 (2019).
Joseph, M. B., Mihaljevic, J. R., Orlofske, S. A. & Paull, S. H. Does life history mediate changing disease risk when communities disassemble? Ecol. Lett. 16, 1405–1412 (2013).
Wilschut, R. A., Hume, B. C. C., Mamonova, E. & van Kleunen, M. Plant-soil feedback effects on conspecific and heterospecific successors of annual and perennial Central European grassland plants are correlated. Nat. Plants 9, 1057 (2023).
Bakker, E. S., Olff, H., Boekhoff, M., Gleichman, J. M. & Berendse, F. Impact of herbivores on nitrogen cycling: contrasting effects of small and large species. Oecologia 138, 91–101 (2004).
Dordas, C. Role of nutrients in controlling plant diseases in sustainable agriculture. A review. Agron. Sustain. Dev. 28, 33–46 (2008).
Firn, J., Huong, N., Schuetz, M. & Risch, A. C. Leaf trait variability between and within subalpine grassland species differs depending on site conditions and herbivory. Proc. R. Soc. B 286, 20190429 (2019).
Jessen, M.-T., Kaarlejarvi, E., Olofsson, J. & Eskelinen, A. Mammalian herbivory shapes intraspecific trait responses to warmer climate and nutrient enrichment. Glob. Chang. Biol. 26, 6742–6752 (2020).
Jaramillo, V. J. & Detling, J. K. Grazing history, defoliation, and competition - effects on shortgrass production and nitrogen accumulation. Ecology 69, 1599–1608 (1988).
Bagchi, R. et al. Pathogens and insect herbivores drive rainforest plant diversity and composition. Nature 506, 85 (2014).
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. & Jarvis, A. Very high resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965–1978 (2005).
Edgar, R. C. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat. Methods 10, 996 (2013).
Abarenkov, K. et al. The UNITE database for molecular identification of fungi—recent updates and future perspectives. N. Phytol. 186, 281–285 (2010).
Polme, S. et al. FungalTraits: a user-friendly traits database of fungi and fungus-like stramenopiles. Fungal Divers. 105, 1–16 (2020).
Wang, Y. et al. Data for ‘Long-term grazing effects on soil-borne pathogens are driven by temperature.’ Figshare repository. https://doi.org/10.6084/m9.figshare.27636804 (2024).
Acknowledgements
This work was supported by National Natural Science Foundation of China (No. 32371622, 32271642), the National Key Research and Development Program of China (2022YFF1300604), the Young Elite Scientists Sponsorship Program by CAST (2023QNRC001), the Youth Talent Support Project of Jilin Province (QT202315), and the Program for Introducing Talents to Universities (B16011). Ministry of Education Innovation Team Development Plan, Grant/Award Number: 2013‐373. M.D-B. acknowledges support from TED2021-130908B-C41/AEI/10.13039/501100011033/Unión Europea NextGenerationEU/PRTR and from the Spanish Ministry of Science and Innovation for the I + D + i project PID2020-115813RA-I00 funded by MCIN/AEI/10.13039/501100011033.
Author information
Authors and Affiliations
Contributions
Y.W. M.Z., and L.W. conceived and designed the experiments and led in data analysis and writing efforts; M.D.-B. contributed to revise the manuscript critically; G.L., J.C., X.P., Y.W., and Y.X. performed experiments. All the authors contributed critically to the drafts and gave final approval for publication.
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing interests.
Peer review
Peer review information
Communications Biology thanks Shihong Jia and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Primary Handling Editors: Shouli Li and Tobias Goris. A peer review file is available.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
About this article
Cite this article
Wang, Y., Zhang, M., Delgado-Baquerizo, M. et al. Long-term grazing effects on soil-borne pathogens are driven by temperature. Commun Biol 7, 1568 (2024). https://doi.org/10.1038/s42003-024-07280-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/s42003-024-07280-5
