Plant community-, environment- and soil-mediated relationships between elevation and above- and belowground plant pathogens
Together, our results provide broad evidence that above- and belowground pathogens had distinct geographical vertical pattern which were shaped by different mechanisms. For foliar fungal pathogens, we found empirical evidence that plant community characteristics (i.e. community proneness index and evenness), rather than soil properties, were the main drivers of community pathogen load in our field survey. However, results did not support any direct or indirect relationship between elevation and foliar fungal disease.
These results highlight the importance of host identity to determine community-level diseases. In the field survey, shifts in plant community proneness to diseases ultimately led to difference in community pathogen load, a finding that is consistent with other studies from both plant diseases (Mitchell et al., 2002; Liu et al., 2017) and alsoRibeiroia ondatrae caused amphibian diseases (Johnson et al., 2013). However, although only a small part of the 73 plant species’ distributions overlaps with each other and generates considerable variance in the composition of host communities for pathogens along the elevation gradient, the degree of communities prone to disease did not synchronously change. Therefore, plant community mediated effect was not found in our study.
In general, our results indicated that abiotic factors mediated the association between elevation and soil fungal pathogen richness, while elevation showed no significant direct or indirect association with foliar fungal diseases and soil fungal pathogen relative abundance. Indeed, different measurements for pathogens (i.e. OTU richness versus relative abundance) may explain the inconsistent responses of pathogens to abiotic and biotic factors. For instance, positive plant richness- pathogen diversity relationship and negative diversity- disease relationship can be observed in natural plant communities, given that increasing plant species diversity provides more diverse hosts while simultaneously inducing dilution effects (Rottstock et al., 2014). However, there is insufficient evidence to determine the relative strength of which pathogen richness responds to the abiotic and biotic environment. In addition, the different patterns of above- and belowground plant pathogens along elevational gradients can be partly explained by their differences in life history characteristics. Rusts (e.g. Phragmidium , Puccinia and Uromyces ) are the dominant foliar fungal pathogens in our study site (Liu et al., 2019); these fungi belong to a group of obligate biotrophic pathogens that can only extract nutrients from living plant cells (Duplessis et al., 2021) and have relatively narrow host ranges (one or just a few phylogenetically close plant species; Zhang, 2009). In contrast, soil plant pathogens are commonly necrotrophic with a relatively broad host range (Delgado-Baquerizo et al., 2020). Therefore, we expect that negative biodiversity-disease relationships might occur more commonly for foliar pathogens; foliar diseases are strongly dependent on their hosts, so they can be easily captured by host composition rather than environmental factors (e.g. temperature). For soil biota, we found empirical evidence that increasing elevation was associated with reductions in soil fungal pathogen richness via changes in soil properties (Soil PCA1 ). Our meta-analysis providing further evidence of a general negative association between soil fungal pathogen richness and elevation among studies. However, elevation had no significant association with soil fungal pathogen relative abundance. Unlike the severity of foliar fungal disease or fungal pathogen relative abundance, soil fungal pathogen richness depends on the relative rate of fungal colonization and extinction of fungal taxa. On the one hand, temperature may promote soil fungal pathogen richness through the following three mechanisms: First, temperature is a key limiting factor for plant biomass and richness (Chu et al., 2019). Broad evidence from plants suggests that the species richness of lower trophic levels can determine the diversity of higher trophic levels, including fungal pathogens (Kamiya et al., 2014; Rottstock et al., 2014; Liu et al., 2016). Moreover, increased plant biomass provides greater host availability and more diverse habitats for pathogens. These plant-mediated paths can shape a potential negative relationship between elevation and soil fungal pathogen richness. Second, temperature can promote coevolution between hosts and pathogens, given the stronger inter-trophic interactions in warm areas (Roslin et al., 2017; Liu, Chen, et al., 2020); this is thought to be a main factor shaping pathogen richness. Third, temperature can determine the distribution of soil pathogens via environment filtering (Tedersoo et al., 2014); the fitness of pathogens is largely affected by temperature and humidity through impacts on survival, growth, dispersal and reproduction, both at local and global scales (Tedersoo et al., 2014; Liu et al., 2019; Delgado-Baquerizo et al., 2020).
On the other hand, soil properties may be a regulator of plant pathogens. Firstly, soil nutrients may benefit pathogens in both agro- and natural ecosystems by increasing tissue nitrogen concentration (Huber and Watson, 1974; Veresoglou et al., 2013; Liu et al., 2017). Secondly, soil properties can alter the competition dynamics and shape plant community composition (e.g. inducing the light asymmetry under nitrogen addition; Xiao et al., 2021), which possibly indirectly influence soil plant pathogens by preferring species with better growth ability (Cappelli et al., 2020). The soil fungal pathogen relative abundance showed no significant variation along the elevation gradient, despite considerable changes in temperature and soil properties. We attribute this to the small proportion of soil fungal pathogens relative to total soil fungi (i.e. percentage of soil fungal pathogens copy number; on average of 7.72% in our study), which may potentially limit the ability of soil pathogens to respond to biotic and abiotic variables.