Abstract
Plant pathogens are important for ecosystem functioning and community assembly and respond to a variety of biotic and abiotic factors, which change along elevation gradients. Thus elevational gradients are a valuable model system for exploring how plant community, soil properties, and environmental factors influence pathogens. Yet, how these factors influence pathogens in nature remains poorly understood. We tested patterns and potential mechanisms of plant fungal pathogens along elevational gradients by combining a field survey in the Tibetan Plateau with a global meta-analysis. We found that increasing elevation was associated with a decrease in soil fungal pathogen richness but not foliar fungal disease symptoms. Elevation mainly related to soil fungal pathogen richness through abiotic factors. Whereas no evidence supported association between elevation and foliar fungal disease. The meta-analysis suggests some generality in the results of the field survey: elevation was associated with a decrease in soil fungal pathogen richness, but had no consistent relationship with foliar fungal disease or pathogens. Our study reveals distinct patterns of above- and belowground plant pathogen along elevation gradients and provides new insight into the potential mechanisms in shaping these patterns.
Key-words: Biodiversity-disease Relationship, Community Disease Proneness, Community Pathogen Load, Foliar Fungal Pathogen, Meta-analysis, Soil Fungal Pathogen
Introduction
Pathogens that cause plant diseases can maintain plant diversity by inducing both negative density dependence and life-history trade-offs (Allan et al., 2010; Cappelli et al., 2020), yet the factors that drive pathogen abundance and diversity remain poorly understood. Previous studies in agroecosystems suggest that environmental heterogeneity (shaped by multiple abiotic and biotic factors) can regulate plant pathogens (Stukenbrock and McDonald, 2008). However, whether variation in such factors drive geographic patterns of plant pathogens in natural ecosystem remains an open question.
Abiotic factors such as temperature and precipitation can affect plant pathogens both directly and indirectly through changes in host plant communities and soil properties (Liu et al., 2019). High temperatures often promote both foliar fungal diseases (e.g. Roy et al., 2004; Liu et al., 2019) and soil pathogens (Delgado-Baquerizo et al., 2020). Warming can benefit pathogen fitness by increasing pathogen survival, growth and transmission (Siebold and Tiedemann, 2013), extending the favorable time for pathogen growth (Roy et al., 2004), or narrowing the generation gap of pathogens (Bebber, 2015). Additionally, humidity can increase plant disease by promoting pathogens’ spore germination and growth (Romero et al., 2021).
Abiotic factors are also predicted to influence the diversity, phylogenetic structure, and composition of host plant communities (Zhu et al., 2020), and could thereby indirectly affect plant pathogens (Halliday et al., 2021). In disease ecology, pathogens commonly increase in prevalence and severity with decreasing host diversity and corresponding changes in host density (e.g. via changes in host richness and evenness; Keesing et al., 2010; Halliday and Rohr, 2019). This negative biodiversity-disease relationship is potentially caused by reduced encounter rates, susceptible host regulation, and non-random host species loss (Keesing et al., 2006; Halliday, Rohr, et al., 2020). Accumulated empirical evidence from grasslands and temperate and subtropical forests supports the existence of negative biodiversity-disease relationships in natural communities (e.g. Mitchell et al., 2002; Rottstock et al., 2014; and Liu, Chen, et al., 2020 for a meta-analysis; but see Halliday et al 2017, 2020). Furthermore, changes in diversity are often accompanied by compensatory shifts in the density of component host species in grasslands (Mitchell et al., 2002). The density-dependent transmission of foliar fungal diseases causes communities with higher host density to suffer more seriously from disease at the host population level (Burdon and Chilvers, 1982), and soil pathogens may rely on plant biomass since more biomass will provide more nutrient substance and greater chance for pathogenicity (Liu et al., 2021). Furthermore, disease proneness (i.e. expected community pathogen load based on constituent host plant species) can explain why host diversity loss is strongly associated with increased foliar fungal disease in alpine meadows (Liu et al., 2017). A plant species with high disease proneness (i.e. possess good growth but weak defensive abilities) can harbor more pathogens, and thus a host community with a higher proportion of more disease-prone species is expected to have a higher community pathogen load (Liu et al., 2017).
In addition to plant community characteristics, soil properties can also potentially regulate plant pathogens. Both foliar and soil pathogens are likely to benefit from high soil nutrients in both agro- and natural ecosystems (Huber and Watson, 1974; Liu et al., 2017). Soil nutrients can promote pathogens by increasing tissue nitrogen concentration (Veresoglou et al., 2013), which is one of the most important limiting factors for many pathogens, especially for those that extract nutrients only from living plant tissues (i.e. biotrophic pathogens; Liu, Lu, et al., 2020).
Despite the well-characterized impacts of single abiotic or biotic factors on plant pathogens, how these soil-, plant community-, and environment mediated effects combine to generate patterns of above- and belowground plant pathogens across biogeographic gradients remains poorly understood. For instance, a previous study found that fungal diseases on Phragmites australis increased with latitude in North America, indicating that geographical gradients were associated with the distribution of pathogens (Allen et al., 2020). However, studies along latitude are massive logistical undertakings, and their results are easily affected by the potential confounding factors of geology and biogeographic history (Halbritter et al., 2018). Compared to other biogeographical gradients, elevational change generates highly variable ecological conditions (including soil, plant community, environment) at a relatively small spatial scale (Rowe, 2009), providing an excellent ‘natural laboratory’ to study how biotic and abiotic factors affect plant pathogens (Halliday et al., 2021).
Here, following this framework, we considered soil-, environment-, and plant community-mediated effects to explore patterns and potential mechanisms of plant pathogens along elevation gradients. However, quantifying plant pathogen communities is complicated by the fact that potential plant pathogens do not always cause disease (i.e. the plant disease triangle; Liu and He, 2019). To overcome this challenge, we measured plant pathogen communities in two ways. We measured foliar fungal disease as a quantitative measurement of the disease severity (i.e. relative abundance, rather than absolute abundance) of pathogens that are currently causing disease on plants. Leaves are readily surveyed for disease, allowing for accurate and reliable surveys of pathogen relative abundance in plant communities. However, the disease observed on a leaf is only one small part of the total pathogen potential of an ecological community. In contrast with leaves, soils can serve as a reservoir of plant pathogens capable of causing disease both above-and below ground, even when those pathogens are not currently causing disease on a plant (Delgado-Baquerizo et al., 2020). Surveying the richness and relative abundance of soil fungal pathogen communities using sequencing-based approaches has become a powerful approach to assess the pathogen potential of a community (van Agtmaal et al., 2017).
We combined these two complementary approaches by measuring foliar fungal disease, soil fungal pathogens, plant community characteristics (richness, evenness, biomass and proneness), environmental conditions, and soil properties along an elevational gradient in an alpine meadow in the northeastern Qinghai-Tibetan Plateau to explore patterns of above- and belowground plant pathogens. We sought to answer the following questions: (i ) how do abiotic and biotic factors (soil properties, plant community, environment conditions, above- and belowground plant pathogens) change along elevational gradients?; (ii ) how do soil properties, plant community and environmental conditions affect above- and belowground plant pathogens?; and (iii ) what is the relative importance of the plant community-, environment- and soil-mediated effects for the correlation between elevation and above- and belowground plant pathogens? We additionally performed a systematic meta-analysis to explore the correlation between elevation and above- and belowground plant pathogens and to assess the generality of our main conclusions.
Materials and methods
Field survey along an elevational gradient