Fig. 7. (a) Structure equation modeling exploring direct and
indirect effects of fraction(grazing and grazing exculsion), grassland
type, plant index(coverage and patrick index), and soil chemical
properties in fungal diversity and (b) standardized effects of fraction,
grassland type, plant index, and soil chemical properties in fungal
diversity. Line thickness indicates the correlation strength: the
thicker the line, the stronger is the correlation. The red and blue
arrows indicate negative and positive relationships, respectively. The
width of the arrow is proportional to the strength of the relationship.
The numbers adjacent to the arrows represent standardized path
coefficients. The proportion of variance explained
(R2) appeared alongside each response variable in the
model.
Discussion
4.1. Effect of grazing exclusion on soil physicochemical properties in
different grassland types
Whether grazing exclusion can change the diversity and composition of
soil fungal communities, soil chemistry is the dominant factor (Li et
al., 2019; Qin et al., 2021). There is growing evidence that fungal
communities are more sensitive to carbon and nitrogen sources than
bacterial communities (Zhang et al., 2018). Our study found that C:N did
not differ significantly among the three grassland types in either 0-5
cm or 5-10 cm soils before grazing exclusion, probably because grazing
can promote root secretions and fallen leaves decomposition through
trampling, which can increase the amount of C and N entering the soil
and keep soil C and N in dynamic equilibrium (Bi et al., 2018). Whereas
C:N was significantly higher in temperate deserts than in temperate
steppes and mountain meadows after grazing exclusion, the interaction of
exclusion and grassland type significantly altered C:N, indicating that
grazing exclusion reduces soil C and N pools (Sun et al., 2020), and is
prominent in steppes and meadows. In addition, we found that grazing
exclusion significantly increased SOC in all three grassland types and
SWC in both temperate steppes and mountain meadow, due to higher soil
fertility associated with good plant cover and greater apoplastic
accumulation (Marzaioli et al., 2010; Jing et al., 2014). Above-ground
biomass has a direct effect on apoplastic accumulation, which increases
soil moisture. It explains the increase in SWC in both temperate
steppesand mountain meadow. At the same time, apoplastic decomposes more
rapidly in moist soils, and large amounts of decomposing apoplastic can
increase soil nutrients (Jing et al., 2014).
Secondly, soil TP showed a close correlation with temperate desert, and
grazing exclusion significantly increased the content of temperate
desert TP, which is inconsistent with previous studies (Yang et al.,
2018), it may be due to the fact that soil nutrients still had not
returned to their original levels after 9 years of grazing exclusion,
but were in an unstable and fluctuating state, this may be related to
the change in the main vegetation types on the surface, the rate of
decomposition and the amount of nutrient uptake and return by plant
roots. The effects of grazing exclusion on pH, C:N, C:P and N:P in the
three grasslands were not significant regardless of the soil stratum.
The reasons for this phenomenon may be: (1) the removal of grazing
pressure after grazing exclusion in degraded grasslands, the
disappearance of conditions that maintain the spatial pattern of soil
nutrients or vegetation, the increase in spatial heterogeneity of soil
nutrients, and the increase in the proportion of stochastic factors,
making the research results more stochastic and the study results
appearing differences (David, 1988); (2) the grazing areas have a higher
soil nutrient content due to the trampling of livestock, which leads to
the crushing of apoplastic and its entry into the soil, thus
accelerating the circulation of organic matter, as well as the excrement
of grazing livestock; and (3) the regional differences in the soil
itself may also be responsible for this difference.
4.2. Effects of grazing exclusion on the composition and diversity of
soil fungi
Our results go further than the commonly reported differences in fungal
composition between grassland types (Zhang et al., 2010; Yang et al.,
2022; Wang et al., 2021). Consistent with previous results (Maestre et
al., 2015; Ren et al., 2017), we found that at the phylum level, the
pre-grazing exclusion Ascomycota and Basidiomycota were
the dominant fungi in all three grassland types. After the grazing
exclusion Ascomycota decreased by 14.72% and 9.74% in temperate
deserts and mountain meadows, respectively, while it increased by 4.82%
in temperate steppes. In contrast to the Ascomycota , theBasidiomycota increased by 238.8% and 47.68% in temperate
deserts and mountain meadows, respectively, while it decreased by
23.12% in temperate steppes. This may be due to the higher soil pH in
temperate desert and the soils of temperate steppes and mountain meadows
is acidic, and the positive response of Ascomycota andBasidiomycota fungi to changes in soil pH, the higher abundance
of Ascomycota in soils with higher pH (Tedersoo et al., 2014),
which also explains the higher relative abundance of Ascomycotain temperate deserts. Additionally, studies of soil fungi have found
that the highest diversity in soils is found in Ascomycota andBasidiomycota fungi in recent years, while later studies
analysing the occurrence patterns of globally dominant soil fungal taxa
have found a strong spatial structure of soil fungal communities along
ecological gradients, but also signs of mass dispersal and the ability
of some fungi to dominate many environments, with wind-dispersedAscomycota taxa dominating the soil fungal communities, followed
by Basidiomycota and other fungi (Bucbe et al., 2009; Egidi et
al., 2019). Next, significant differences were found between the three
grassland types for the Glomeromycota and Mucoromycota ,
and it was found that the Mortierellomycota was not influenced by
either grazing exclusion or grassland type, but the interaction between
the two had a significant effect on the Mortierellomycota . It has
been shown that the activity of Glomeromycota is reduced in high
acidity environments and is not efficient at taking up nitrogen or
phosphorus from organic matter and converting it to inorganic components
for plant use, eventually plants gradually form new symbiotic
relationships with other organic matter mycorrhizal fungi and replace
the Glomeromycota (Smith et al., 2008). In this study, the low
organic matter content of the temperate desert soil and the lower
relative abundance of Glomeromycota compared to the other two
types of grassland. Validating the findings of most studies on the
relationship between Glomeromycota and soil physicochemical
properties, and support previous studies suggesting a suppressive effect
of soil organic matter content on Glomeromycota (Pellissier et
al., 2015; Smith et al., 2008). Furthermore, at the phyla level, it was
found that grazing exclusion, grassland type and the interaction between
the two significantly altered Sordariomycetes andPezizomycetes , with grassland type having a highly significant
effect on Ustilaginomycetes and a significant effect onEurotiomycetes and Orbiliomycetes . This represents the
different responses of various fungal phylas to environmental change,
reflecting the role of environmental niche separation in selecting
fungal communities (Pellissier et al., 2014).
Unlike the effect of grazing exclusion on soil fungal composition,
grazing exclusion, grassland type and the interaction between the two
did not significantly alter soil fungal α-diversity in either 0-5 cm or
5-10 cm soils, similar to previous findings (Hao et al., 2020; Yang et
al., 2019; Ding et al., 2020). The insignificant response of fungal
alpha diversity to grazing exclusion and grassland type may be due to
that fungi are less sensitive than bacteria (Cheng et al., 2016; Zhang
et al., 2018). These results are consistent with previous findings that
soil fungi are more stable than bacteria (Hamonts et al., 2017; Wang et
al., 2019). Although there was no effect on fungal α-diversity, we found
that the interaction of grazing exclusion and grassland type
significantly altered fungal β-diversity. This may be the ability of
many soil microorganisms to colonise the inter-rhizosphere, where root
biomass and plant C:N ratios may influence the utilisation of
inter-rhizosphere resources by altering root turnover or root
secretions, which may in turn strongly alter the composition of the
microbial community (Chase, 2010; Philippot et al., 2013). Moreover,
other studies have detected significant effects of grazing exclusion on
soil fungal β-diversity (Chen et al., 2020). In the current study, the
strong link between soil microbial diversity and grazing exclusion and
grassland type can be explained by the fact that microbial communities
are often directly influenced by above-ground plant biomass and
community structure (de Vries et al., 2012). For example, grazing
exclusion increases above-ground plant biomass and apoplastic content,
thus increased fungal diversity (Hamonts et al., 2017). The increase in
species richness induced by grazing exclusion suggests that high plant
diversity results in a greater variety of organic matter ultimately
flowing into the subsurface, thereby generating more ecological niches
for use by different species of microorganisms and altering the
diversity of microbial communities (Lodge, 1997; Brodie et al., 2003).
The results indicated that there was no significant change in soil
fungal alpha diversity but significant differences in fungal beta
diversity under the influence of both grazing exclusion and grassland
type.
4.3. Potential drivers of soil fungal community diversity
SEM analysis showed that grazing exclusion had a significant effect on
fungal community diversity by directly affecting total soil phosphorus,
and that grassland type had a significant effect on fungal community
diversity by directly affecting soil organic carbon, which in turn
affected total nitrogen and phosphorus. In line with our findings, other
studies have also shown that soil total phosphorus and nitrogen are
closely related to soil fungal diversity (Lindahl et al., 2015; Lauber
et al., 2008). In contrast, a recent experiment showed that soil fungal
abundance and diversity differed between grassland habitats, but that
this difference did not correlate with geographical distance, and that
certain environmental factors, including climate, soil pH, nitrogen and
phosphorus, were the main influences on the distribution, abundance and
diversity of soil fungal communities (Pellissier et al., 2014). In our
study, combining direct and indirect effects reveals that soil total
nitrogen is the most important predictor of changes in fungal community
diversity, the strong association between soil total nitrogen and fungal
diversity is justified because total nitrogen is the main source of
energy for soil microorganisms (Lindahl et al., 2015). For example,
nitrogen provides an adequate source of nitrogen for fungal symbioses,
and plants no longer import too much carbon into the subsurface for
nitrogen acquisition, which can have an impact on fungal composition and
biomass (Norris et al., 2013). However, it has been shown that fungal
diversity does not correlate with total soil nitrogen and phosphorus,
suggesting that environmental factors may not be a limiting factor in
the structural diversity of soil fungal communities at the larger scale
studied (Li., 2015). In the present study, soil organic carbon had an
indirect effect on fungal community diversity, similar to the results of
previous studies (Li., 2015). Soil organic carbon provides nutrients and
energy for plant growth and soil microbial life (Li et al., 2006), and
its content reflects the effectiveness of limiting resources in the soil
and is the ‘source’ of nutrients for soil fungal community growth, the
level of which affects soil fungal community structure and diversity. In
addition, the natural environment in different regions can also affect
soil fungal diversity, harsh environments such as drought can reduce
fungal diversity and abundance (Maestre et al., 2015). In summary, soil
nutrient content is the main factor influencing fungal diversity,
especially total soil nitrogen, total phosphorus and organic carbon.
Conclusions
As revealed by the data from our study, the composition of soil fungal
communities differed between grassland types. Under the influence of
both grazing exclusion and grassland type, there was no significant
change in soil fungal alpha diversity, but significant differences in
fungal beta diversity. The changes in soil total nitrogen and phosphorus
caused by grazing exclusion were closely related to soil fungal
diversity. These results suggest that soil nutrient content is the main
factor influencing fungal diversity, especially soil total nitrogen,
total phosphorus and organic carbon.