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