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\begin{document}

\title{Effect of plateau pika disturbance on the ecosystem services of alpine
grasslands}



\author[1]{Ying Ying Chen}%
\author[1]{Huan Yang}%
\author[2]{Gen Sheng Bao}%
\author[1]{Xiao Pan Pang}%
\author[3]{Zheng Gang Guo}%
\affil[1]{Lanzhou University}%
\affil[2]{Qinghai University}%
\affil[3]{State Key Laboratory of Grassland Agro-ecosystems}%


\vspace{-1em}



  
  \date{May 04, 2024}


\begingroup
\let\center\flushleft
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\selectlanguage{english}
\begin{abstract}
Herbivore disturbance can affect the grassland ecosystem services though
creating extensive disturbances vegetation and soil. This study focused
on plateau pika (Ochotona curzoniae) disturbance to investigate the
effect of disturbance by small burrowing herbivores on ecosystem
services of alpine grasslands though five sites. In this study, the
palatable plant biomass, plant species richness, soil water storage,
soil organic carbon, total nitrogen, phosphorus and potassium stocks
were used to estimate the forage availability, biodiversity
conservation, water conservation, carbon sequestration and soil nutrient
maintenance. This study showed that plateau pika disturbance was related
to higher plant species richness and soil organic carbon stock,
associated with lower palatable plant biomass and soil water storage,
and had no effect on total potassium stock, whereas the responses of
soil total nitrogen and phosphorus stocks to plateau pika disturbance
were different among sites. The palatable plant biomass, plant species
richness, soil organic carbon, total nitrogen and phosphorus stocks
showed downward parabolas, whereas the soil water storage showed a
decreasing trend with increasing plateau pika disturbance intensity.
These results indicated that the role of plateau pikas is dependent not
only on the management target of alpine grasslands but also on the
plateau pika disturbance intensity.%
\end{abstract}%



\sloppy


\textbf{Title: Effect of plateau pika disturbance onthe ecosystem
services ofalpine grasslands}

\textbf{Running title: plateau pika alters the alpine grassland
ecosystem services}

Ying Ying Chen\textsuperscript{a}, Huan Yang\textsuperscript{a}, Gen
Sheng Bao\textsuperscript{b}, Xiao Pan Pang\textsuperscript{a}, Zheng
Gang Guo\textsuperscript{a*}

\emph{\textsuperscript{a}Key Laboratory of Grassland Livestock Industry
Innovation, Ministry of Agriculture and Rural Affairs; Engineering
Research Center of Grassland Industry, Ministry of Education; College of
Pastoral Agriculture Science and Technology, Lanzhou University,
Lanzhou, 730020, P. R. China}

\emph{\textsuperscript{b}Academy of Animal and Veterinary Sciences,
Qinghai University (Qinghai Academy of Animal and Veterinary Sciences),
Xining, China}

\textsuperscript{*}Correspondence, Zheng Gang Guo,
E-mail:\emph{guozhg@lzu.edu.cn}

\textbf{Acknowledgments}

The authors would like to thank Jing Zhang, Qian Wang, Hai Peng Xu, Wen
Na Zhang, Juan Wang, Ding Yang, Jie Li, Fu Yun Qiao, Di Gang Zhi, Hao
Hao Qi, Gan Lin Feng and Yuan Yuan Duan from Lanzhou University for the
contributions made to this study through their field assistance and
laboratory analysis. This study was funded by the Key Laboratory of
Superior Forage Germplasm in the Qinghai-Tibetan Plateau (2020-ZJ-Y03),
the Changjiang Scholars and Innovative Research Team in University
(IRT17R50), the Major Project of Xizang autonomous region (XZ201901NA03)
and the National Natural Science Foundation of China (31172258), and the
111 Project (B12002).

\textbf{Conflict of Interest Statement}

The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to
influence the work reported in this paper.

\textbf{Author contributions}

Ying Ying Chen and Zheng Gang Guo conceived the ideas and designed the
methodology; Ying Ying Chen, Xiao Pan Pang, Gen Sheng Bao and Huan Yang
collected the data; Ying Ying Chen analysed the data; Ying Ying Chen and
Zheng Gang Guo led the writing of the manuscript. All of the authors
contributed critically to the drafts and gave their final approval for
publication.



\textbf{Abstract}

Herbivore disturbance can affect the grassland ecosystem services though
creating extensive disturbances vegetation and soil. This study focused
on plateau pika (\emph{Ochotona curzoniae} ) disturbance to investigate
the effect of disturbance by small burrowing herbivores on ecosystem
services of alpine grasslands though five sites. In this study, the
palatable plant biomass, plant species richness, soil water storage,
soil organic carbon, total nitrogen, phosphorus and potassium stocks
were used to estimate the forage availability, biodiversity
conservation, water conservation, carbon sequestration and soil nutrient
maintenance. This study showed that plateau pika disturbance was related
to higher plant species richness and soil organic carbon stock,
associated with lower palatable plant biomass and soil water storage,
and had no effect on total potassium stock, whereas the responses of
soil total nitrogen and phosphorus stocks to plateau pika disturbance
were different among sites. The palatable plant biomass, plant species
richness, soil organic carbon, total nitrogen and phosphorus stocks
showed downward parabolas, whereas the soil water storage showed a
decreasing trend with increasing plateau pika disturbance intensity.
These results indicated that the role of plateau pikas is dependent not
only on the management target of alpine grasslands but also on the
plateau pika disturbance intensity.

\textbf{KEYWORDS}

Forage availability; Biodiversity conservation; Water conservation;
Carbon sequestration; Soil nutrient maintenance

\textbf{1 INTRODUCTION}

Grassland covers approximately 40\% of the Earth's land surface (Pang et
al., 2020b), and its multiple ecosystem services can sustain animal
production, ecological functions, flora and fauna, and other human
welfare (Costanza et al., 1997; Dong et al., 2020; Zhang et al., 2018).
However, grassland ecosystem services have been demonstrated to be
affected by herbivore disturbance (Lu et al., 2017; Mart\selectlanguage{ngerman}ínez-Estévez et
al., 2013).

Herbivore disturbance often has impacts on grassland ecosystem services
(Lu et al., 2017) by altering the plant community (Lu et al., 2017; Niu
et al., 2010; Wu et al., 2009) and soil properties (Lu et al., 2017; Sun
et al., 2011; Wang et al., 2012a). Large herbivore grazing has been
verified to influence grassland ecosystem services (Lu et al., 2017;
McGranahan et al., 2012; Niu et al., 2010; Sun et al., 2011; Woldu and
Saleem, 2000). In addition to large herbivores, tens of thousands of
small burrowing herbivores usually create extensive disturbances on
grassland vegetation and soil (Davidson et al., 2012; Pang et al.,
2020a) by developing burrow systems (Sun et al., 2015), excreting feces
and urine (Zhang et al., 2016), consuming plants (Liu et al., 2017; Sun
et al., 2015), clipping tall plants (Zhang et al., 2020), and producing
bare soil patches (Guo et al., 2012a, 2012b; Yu et al., 2017a, 2017b).
Currently, a few studies have used data from one site to examine the
effect of prairie dog disturbance on grassland ecosystem services in
arid regions (Martínez-Estévez et al., 2013). However, the effect of
disturbance by small burrowing herbivores on vegetation and soil varies
with topography and microclimate (Pang et al., 2020a, 2020b; Wang et
al., 2020a; Yu et al., 2017a). Therefore, it is necessary to use data
from multiple sites to identify a general pattern concerning the effect
of disturbance by small burrowing herbivores on grassland ecosystem
services, which can provide information for grassland management.

Plateau pikas (\emph{Ochotona curzoniae} ) are a common, small burrowing
herbivore in alpine grasslands of the Qinghai-Tibetan Plateau (Smith \&
Foggin, 1999; Zhang et al., 2020). This small animal is considered a
pest in China (Liu et al., 2013; Pang \& Guo, 2017) since it often
exacerbates alpine grassland degradation (Liu et al., 2013; Wilson \&
Smith, 2015; Zhang et al., 2016), and it has been widely eradicated by
poison (Wilson \& Smith, 2015). However, some studies argue that plateau
pikas are key animals in alpine grassland ecosystems (Smith \& Foggin,
1999; Smith et al., 2019). This kind of disagreement has encouraged
professionals to reevaluate the role of plateau pikas in alpine
grassland ecosystems. Thus, plateau pika disturbance in relation to
alpine grassland ecosystem services is possibly a better way to gain
insight into the roles of plateau pikas in alpine grassland ecosystems.
In theory, alpine grasslands encompass a variety of ecosystem services,
as well as grasslands in Europe (Jäger et al., 2020; Obermeier et al.,
2019) and North America (Martínez-Estévez et al., 2013), whereas the
main ecosystem services of alpine grasslands in the Qinghai-Tibetan
Plateau are often given attention for forage availability, biodiversity
conservation (Dong et al., 2010), water conservation (Dong et al., 2020;
Wen et al., 2013), carbon sequestration (Dong et al., 2020; Zhang et
al., 2015) and soil nutrient maintenance (Wen et al., 2013). However,
whether plateau pika disturbance influences alpine grassland ecosystem
services has not yet been well documented.

This study employs plateau pikas as a study animal to investigate the
effect of disturbance by small burrowing herbivores on forage
availability, biodiversity conservation, water conservation, carbon
sequestration and soil nutrient maintenance services across five sites.
Specifically, this study hypothesizes that (1) plateau pika disturbance
is related to lower forage availability services and higher biodiversity
conservation services; (2) plateau pika disturbance is associated with
higher water conservation services; (3) plateau pika disturbance
correlates with higher carbon sequestration services; and (4) plateau
pika disturbance is related to lower soil nutrient maintenance services.

\textbf{2 MATERIALS AND METHODS}

\textbf{2.1 Study sites}

Plateau pikas can live in various habitats with different soil types,
topographies, and microclimates. To identify a general pattern of how
plateau pika disturbance influences the ecosystem services of alpine
grasslands, this study selected five sites with different alpine
grassland types, topographies and microclimates as field survey areas.
These five survey sites have a similar typical plateau continental
climate, with mean annual temperatures of 3.3\selectlanguage{english} in Luqu
(102deg10\selectlanguage{greek}´-\selectlanguage{english}102\selectlanguage{ngerman}°52\selectlanguage{greek}´\selectlanguage{english}E, 34\selectlanguage{ngerman}°16\selectlanguage{greek}´-\selectlanguage{english}34\selectlanguage{ngerman}°37\selectlanguage{greek}´\selectlanguage{english}N), 2.0 in Gangcha (99\selectlanguage{ngerman}°53\selectlanguage{greek}´-\selectlanguage{english}100\selectlanguage{ngerman}°36\selectlanguage{greek}´\selectlanguage{english}E,
37\selectlanguage{ngerman}°17\selectlanguage{greek}´-\selectlanguage{english}37\selectlanguage{ngerman}°29\selectlanguage{greek}´\selectlanguage{english}N), 2.0 in Haiyan (100\selectlanguage{ngerman}°37\selectlanguage{greek}´-\selectlanguage{english}100\selectlanguage{ngerman}°58\selectlanguage{greek}´\selectlanguage{english}E, 36\selectlanguage{ngerman}°51\selectlanguage{greek}´-\selectlanguage{english}37\selectlanguage{ngerman}°14\selectlanguage{greek}´\selectlanguage{english}N), 2.1
in Qilian (99\selectlanguage{ngerman}°28\selectlanguage{greek}´-\selectlanguage{english}100\selectlanguage{ngerman}°54\selectlanguage{greek}´\selectlanguage{english}E, 37\selectlanguage{ngerman}°58\selectlanguage{greek}´-\selectlanguage{english}38\selectlanguage{ngerman}°27\selectlanguage{greek}´\selectlanguage{english}N), and 3.7 in Gonghe
(99\selectlanguage{ngerman}°41\selectlanguage{greek}´-\selectlanguage{english}100\selectlanguage{ngerman}°12\selectlanguage{greek}´\selectlanguage{english}E, 36\selectlanguage{ngerman}°21\selectlanguage{greek}´-\selectlanguage{english}36\selectlanguage{ngerman}°36\selectlanguage{greek}´\selectlanguage{english}N). These survey areas range in elevation
from 3000 m at the Gangcha survey site to 3550 m at the Luqu survey
site, with average annual precipitation varying from 350 mm at the
Gonghe survey site to 630 mm at the Luqu survey site. According to the
Chinese soil classification system (Gong, 2001), the soil type is alpine
meadow soil in the five survey sites, similar to Cambisol in the WRB
soil classification system. Soil nutrients are different among the five
survey site areas (Pang et al., 2020a, 2020b).

The five field survey areas were placed in cold-season areas, which were
fenced from mid-April to September, and fences were opened to grazing
yaks with a 3.4 yaks ha\textsuperscript{-1} grazing stock rate from
mid-October to early April (Zhang et al., 2020). The alpine grasslands
in the five survey areas were dominated by \emph{Kobresia humilis}
and\emph{Kobresia pygmaea} . Plateau pikas were the only small burrowing
herbivores in the field survey areas, and their population generally
peaked in August (Pang et al., 2020a, 2020b; Qu et al., 2013), implying
that sampling plants and soil in August may best reflect the effect of
plateau pika disturbance on alpine grassland ecosystem services.

\textbf{2.2 Evaluating ecosystem services of alpine grassland}

Plateau pika disturbance often produces many bare soil patches nested in
alpine grasslands (Wilson \& Smith, 2015; Yu et al., 2017b; Zhao et al.,
2019). The plot scale was suggested to better reflect the effects of
plateau pika disturbance on plant biomass and soil properties (Pang et
al., 2020a, 2020b) because it can simultaneously consider the
heterogeneity of soil properties in the presence of plateau pikas and
the difference in plant biomass and soil properties between areas with
and without plateau pikas (Pang et al., 2020b). Therefore, this study
used a plot scale to examine plateau pika disturbance and its
disturbance intensity in relation to forage availability, water
conservation, carbon sequestration and soil nutrient maintenance
services and used a quadrat scale to examine plateau pika disturbance
and its disturbance intensity in relation to the biodiversity
conservation service. Although there were many kinds of bare soil
patches in the alpine grasslands, this study was restricted to the bare
soil patches induced by plateau pikas. In the presence of plateau pikas,
the soil water storage, soil organic carbon, soil total nitrogen,
phosphorus and potassium stocks were calculated in the bare soil surface
and vegetated surface, respectively.

In this study, the forage availability service was estimated by
palatable plant biomass (Mart\selectlanguage{ngerman}ínez-Estévez et al., 2013). The
biodiversity conservation service was estimated by plant species
richness (Wen et al., 2013). Water conservation services can be assessed
by soil water storage (Ouyang et al., 2011). The carbon sequestration
service can be evaluated by the soil organic carbon stock (Wen et al.,
2013). Soil nutrient maintenance services can be assessed by soil total
nitrogen, phosphorus, and potassium stocks (Wen et al, 2013).

\textbf{2.3 Survey design}

Plateau pikas are social animals that usually live in low and open
habitats, and their young offspring often stay with the family in their
birth year since they are philopatric (Wang et al., 2020; Yu et al.,
2017b). Therefore, plateau pikas are territorial and patchy in a vast
alpine grassland. Because the diffusion of plateau pikas is a gradual
process (Pang et al., 2020b), it is easy to find sites without plateau
pika disturbance, even though these sites might be potentially suitable
habitats for plateau pikas.

A stratified random and paired design was used to select the plots. At
each of the five sites, this study first selected 10 disturbed plots
where plateau pikas were present or active burrow entrances were
observed. These disturbed plots were 3 to 5 km from each other. Second,
a paired adjacent undisturbed plot without the presence of plateau pikas
and active burrow entrances was selected for each disturbed plot. The
distance between each disturbed plot and its paired undisturbed plot
ranged from 500 to 1000 m. If the distance between each disturbed plot
and its paired undisturbed plot was too close, plateau pikas could
possibly move from the disturbed plot to the undisturbed plot. To ensure
that each disturbed plot had a paired undisturbed plot to the greatest
extent, each paired plot was ensured to share the same alpine grassland,
with no obvious differences in soil types, topography or microclimate.
In total, there were 10 pairs of plots at each site and 100 plots across
five sites, including 50 disturbed plots and 50 undisturbed plots. The
size of each plot was 35 m×35 m, similar to the average area of plateau
pika's home range of 1262.5 m\textsuperscript{2} (Fan et al., 1999).
Owing to grazing from mid-October to early April, the litter in each
plot was consumed by livestock, which was better for estimating the
aboveground biomass during the warm season.

\textbf{2.4 Field sampling}

Field surveys were conducted in early August 2020. First, the active
burrow entrance at each plot was estimated by the ``plugging tunnels
method'', in which the burrows were plugged for 3 days, and the number
of plugs that were cleared by the plateau pikas to allow access to the
meadow surface were recorded (Guo et al., 2012a; Yu et al., 2017b). The
average number of burrow entrances with cleared plugs in 3 days was
considered the density of active burrow entrances per plot; second, the
area of each bare soil patch in the disturbed plot was measured by the
segmentation method (Han et al., 2011), and then the sum of all bare
soil patches areas in each disturbed plot was calculated as the bare
soil area for that disturbed plot; third, five vegetated quadrats (1 m×1
m) were placed on the vegetated surface approximately 8 m apart along a
W pattern in all plots (disturbed and undisturbed plots), and they were
moved slightly to avoid bare soil patches in disturbed plots if needed;
fourth, a bare soil patch was selected as a paired bare soil quadrat for
each vegetated quadrat in the disturbed plot, and the distance between
each paired bare soil quadrat and vegetated quadrat was as short as
possible, less than approximately 1 m. Thus, there were five paired
quadrats, consisting of five vegetated quadrats and five bare soil
quadrats in each disturbed plot, and there were five vegetated quadrats
in each undisturbed plot since this study only focused on bare soil
patches induced by plateau pikas.

In each vegetated quadrat of the disturbed or undisturbed plot, all
vascular plant species were identified, and their number was recorded as
the plant species richness of a community. Then, all plants rooted in a
quadrat were harvested into palatable and unpalatable plants (Pang \&
Guo, 2017). Finally, all palatable plant samples were placed into
envelopes and carried back to the laboratory.

Generally, most burrows derived from plateau pika activities were less
than 20 cm depth (Yu et al., 2017b), although a few burrows extended to
depths of 60 cm (Fan et al., 1999). In addition, the majority of the
plant roots in the alpine grasslands of the Qinghai-Tibetan Plateau are
in the top 20 cm of the soil. Therefore, this study collected soil
samples at a depth of 20 cm. The soil samples were collected from
vegetated quadrats and bare soil quadrats for each disturbed plot,
whereas they were collected from vegetated quadrats for each undisturbed
plot. Before collecting the soil samples, plants and litter were cleared
from the soil surface. First, a 5-cm diameter soil auger was used to
collect soil samples, with which soil organic carbon and soil nutrient
concentrations (total nitrogen, phosphorus and potassium) were measured;
second, soil profiles in each quadrat were produced by a spade, and a
stainless-steel cutting ring (the volume was 100 cm\textsuperscript{3})
was used to collect soil cores to determine soil bulk density and soil
water content. The soil samples for measuring soil bulk density were
quickly packed into aluminum boxes with recorded weight, and each
aluminum box was numbered. The aluminum boxes with fresh soil were
weighed and recorded on the spot, and these aluminum boxes with soil
samples were stored at 4°C and transported to the laboratory.

\textbf{2.5 Analysis of samples}

In the laboratory, palatable plant samples were dried in an oven at 80°C
for 48 h and weighed. The soil samples used for measuring soil bulk
density and soil water content were dried to a constant weight at
105±2\selectlanguage{english}, and the aluminum boxes with dry soil were weighed and recorded.
The soil samples used for measuring organic carbon, total nitrogen,
total phosphorus and total potassium concentrations were air-dried and
passed through a 2-mm sieve to remove gravel and roots. The soil organic
carbon and total nitrogen concentrations were measured by the
K\textsubscript{2}Cr\textsubscript{2}O\textsubscript{7}-H\textsubscript{2}SO\textsubscript{4}oxidation
method of Walkey and Black (Naelson and Sommers, 1982) and the Kjeldahl
procedure (Foss Kieltec 8400, FOSS, DK). The soil total phosphorus and
total potassium concentrations were measured by Mo-Sb colorimetry
(UV-2102C, UNICO, Shanghai, China, and flame photometry, Model 2655-00
Digital Flame Analyzer, Cole-Parmer Instrument Company, Chicago, IL,
USA) after the soil was digested with perchloric and nitric acid (Nelson
and Sommers, 1982).

The soil bulk density and soil organic carbon and nutrient
concentrations (total nitrogen, phosphorus and potassium) were used to
calculate the soil organic carbon, total nitrogen, phosphorus and
potassium stocks (Pang et al. 2020a, 2020b). The soil bulk density and
soil water content were used to calculate the soil water storage (Jia et
al., 2020). The soil water content was estimated by\(\text{SWC}=\frac{(\text{Ws}\text{Ds})}{(\text{Ws}\text{Am}})\times 100\%\),
where \emph{SWC} is the soil water content (\%); \emph{Ws} and
\emph{Ds}are the weight of the aluminum box with a fresh soil sample (g)
and the weight of the aluminum box with a dry soil sample (g), and
\emph{Am} is the weight of the aluminum box (g).

\textbf{2.6 Calculations}

The bare soil area consisted of all bare soil patches, and the vegetated
surface area was estimated by the plot areas minus the bare soil areas.
The bare soil area in the disturbed plot was estimated by adding all
bare soil patch areas. In each undisturbed plot, bare soil areas were
considered zero, and the vegetated surface area was considered 100\%.

The palatable plant biomass was calculated by the following
equation:\emph{GB} =\emph{B\textsubscript{q}}
\selectlanguage{english}?\selectlanguage{greek}\emph{δ\textsubscript{va}}\selectlanguage{english} , where\emph{GB} , \emph{B\textsubscript{q}}
and \selectlanguage{greek}\emph{δ\textsubscript{va}}\selectlanguage{english} were the palatable plant biomass at the
plot, palatable plant biomass at the quadrat scale (g
m\textsuperscript{-2}) and vegetated surface area, respectively. The
plant species richness in a quadrat (1 m\selectlanguage{ngerman}×1 m) was measured by the
species number of each quadrat. Soil water storage was performed using
the method recommended by Jia et al. (2020). The soil organic carbon
stock per plot was estimated by using the methods described by Pang et
al. (2020a). The soil total nitrogen, phosphorus and potassium stocks
per plot were quantified according to the method of Pang et al. (2020b).

\textbf{2.7 Data analysis}

To develop a general pattern of ecosystem services in relation to
plateau pika disturbance across the five sites, two-way analysis of
variance (ANOVA) with a general linear model (GLM) was used to analyze
the effects of plateau pika disturbance, the sites and their
interactions on palatable plant biomass, plant species richness, soil
water storage, soil organic carbon, soil total nitrogen, soil total
phosphorus and soil total potassium stocks. In the model, the
abovementioned parameters acted as response variables, and plateau pika
disturbance, site and their interactions were introduced as fixed
effects.

In addition, the paired-samples T test was used to examine the
differences in palatable plant biomass, plant species richness, soil
water storage, soil organic carbon stock, soil total nitrogen stock,
soil total phosphorus stock and soil total potassium stock between the
disturbed and undisturbed plots at each site. Here, the ``disturbed
plots'' and ``undisturbed plots'' were regarded as one-to-one
corresponding samples, the paired plots were considered random factors,
and the disturbed/undisturbed plots were considered to be fixed effects,
which were used to verify the results from five sites and to support the
general pattern.

To clarify the responses of palatable plant biomass, plant species
richness, soil water storage, soil organic carbon stock, soil total
nitrogen stock, soil total phosphorus stock and soil total potassium
stock to the plateau pikas disturbance intensity, a linear model (LM)
was used to examine the relationships between palatable plant biomass,
plant species richness, soil water storage, soil organic carbon stock,
soil total nitrogen stock, soil total phosphorus stock and soil total
potassium stock and active burrow entrance densities in all disturbed
plots and in an individual site. The active burrow entrance densities
were considered to be a fixed factor, and they were used to construct
regression curves between palatable plant biomass, plant species
richness, soil water storage, soil organic carbon stock, soil total
nitrogen stock, soil total phosphorus stock and soil total potassium
stock and active burrow entrance densities.

Significant differences were assessed at \emph{P} \textless{}0.05. All
statistical analyses were performed with the SPSS 17.0 software package
from SPSS Inc., Chicago, IL, USA.

\textbf{3 RESULTS}

\textbf{3.1 Effects of plateau pika disturbance on the ecosystem
services of alpine grasslands}

\textbf{3.1.1 Effect of plateau pika disturbance on palatable plant
biomass}

Plateau pika disturbance (disturbance) significantly affected the
palatable plant biomass (Table 1), whereas the five sites (site) did not
affect the palatable plant biomass. The interactions between site and
disturbance also significantly affected palatable plant biomass. When
data from five sites or an individual site were analyzed, the palatable
plant biomass was lower in the disturbed plot than in the undisturbed
plot (Figure. 1A; Figure. 1B).

\textbf{3.1.2 Effect of plateau pika disturbance on plant species
richness}

Site and disturbance had significant effects on plant species richness
(Table 1), whereas their interaction had no significant effect on plant
species richness. On the overall scale or on the individual site scale,
the plant species richness in the disturbed plot was higher than that in
the undisturbed plot (Figure. 2A; Figure. 2B).

\textbf{3.1.3 Effect of plateau pika disturbance on soil water storage}

Site and disturbance were found to have significant effects on soil
water storage (Table 1), whereas their interaction was not found to have
a significant effect on soil water storage. In contrast to the
undisturbed plot, the soil water storage was lower in the disturbed plot
when five sites or one site were considered (Figure. 3A; Figure. 3B).

\textbf{3.1.4 Effect of plateau pika disturbance on the soil organic
carbon stock}

The soil organic carbon stock was significantly affected by site,
disturbance and their interactions (Table 1). When all the sites or the
individual site were considered, the soil organic carbon stock in the
disturbed plot was higher than that in the undisturbed plot (Figure. 4A;
Figure. 4B).

\textbf{3.1.5 Effects of plateau pika disturbance on the soil total
nitrogen, phosphorus and potassium stocks}

The soil total nitrogen and total phosphorus stocks were significantly
affected by site and disturbance, whereas they were not affected by the
interactions between site and disturbance. The soil total potassium
stock was found to be affected only by the site (Table 1).

Accounting for an overall scale effect, the soil total nitrogen and the
total phosphorus stocks in the disturbed plot were higher than those in
the undisturbed plot (Figure. 5A; Figure. 5C), whereas the soil total
potassium stock was not different between the disturbed and undisturbed
plots (Figure. 5E). Accounting for a site-scale effect, plateau pika
disturbance increased the soil total nitrogen stock at Gangcha, Haiyan
and Qilian (Figure. 5B) and the soil total phosphorus stock at Luqu and
Gonghe (Figure. 5D), whereas it had no impact on the soil total nitrogen
stock at Luqu and Gonghe or the soil total phosphorus stock at Gangcha,
Haiyan and Qilian; plateau pika disturbance had a similar effect on the
soil total potassium stock at each site (Figure. 5F).

\textbf{3.2 Effects of plateau pika disturbance intensity on the
ecosystem services of alpine grasslands}

\textbf{3.2.1 Effect of plateau pika disturbance intensity on palatable
plant biomass}

The simulation result of the linear model (LM) indicated that the
palatable plant biomass showed a significant downward parabola as the
disturbance intensity increased when data from five sites (Figure. 6A)
or data from individual site (Figure. 6B) were considered.

\textbf{3.2.2 Effect of plateau pika disturbance intensity on plant
species richness}

Accounting for the five-site scale effect, the plant species richness
increased and then decreased as the plateau pika disturbance intensity
increased (Figure. 7A). Accounting for one site effect, the plant
species richness showed hump-shaped trends at Gangcha, Haiyan and Qilian
and increased linearly at Luqu and Gonghe with increasing disturbance
intensity (Figure. 7B).

\textbf{3.2.3 Effect of plateau pika disturbance intensity on soil water
storage}

When five sites were considered, the soil water storage decreased
linearly as the plateau pika disturbance intensity increased (Figure.
8A). When individual site was considered, the soil water storage showed
downward parabolas at Luqu, Haiyan and Qilian and showed a linearly
decreasing curve at Gangcha and Gonghe with increasing disturbance
intensity (Figure. 8B).

\textbf{3.2.4 Effect of plateau pika disturbance intensity on soil
organic carbon stock}

Accounting for an overall scale effect, the soil organic carbon stock
showed a significant unimodal curvilinearity as the disturbance
intensity increased (Figure. 9A). Considering site-scale effects, the
soil organic carbon stock also showed significant unimodal
curvilinearity at each site with increasing disturbance intensity
(Figure. 9B).

\textbf{3.2.5 Effects of plateau pika disturbance intensity on soil
total nitrogen, phosphorus andpotassium stocks}

When data from the five sites were analyzed together, the soil total
nitrogen (Figure 10A), phosphorus (Figure. 11A) and potassium (Figure.
12A) stocks increased and then decreased as the disturbance intensity
increased.

When data from each site were analyzed separately, the relationship
between the disturbance intensity and soil total nitrogen (Figure. 10B)
and phosphorus (Figure. 11B) stocks was similar at each site, in
agreement with the overall scale effect, whereas the relationship
between the disturbance intensity and soil total potassium stock was
different among five sites, in which the response of soil total
potassium stock to the disturbance intensity was similar to the overall
scale effect at Luqu and Gonghe (Figure. 12B), whereas it showed no
obvious trends at Gangcha, Haiyan and Qilian as the disturbance
intensity increased.

\textbf{4 DISCUSSION}

This study shows that plateau pika disturbance is related to lower
palatable plant biomass and higher plant species richness across five
sites or at an individual site, demonstrating that plateau pika
disturbance decreases the forage availability service and increases the
biodiversity conservation service, in agreement with the first
hypothesis. Plateau pika disturbance in relation to lower palatable
plant biomass has also been reported in a previous study (Liu et al.,
2017), while prairie dog disturbance has been reported to be related to
higher palatable plant biomass (Martínez-Estévez et al., 2013). Prairie
dog disturbance encourages the arid grassland in North America to shift
from annual plants to perennial plants, in which blue gramma
(\emph{Bouteluoa gracilis} ) and vine mesquite (\emph{Panicum obtusum} )
are usually perennial plants that are palatable for livestock
(Sierra-Corona et al., 2015), whereas plateau pika disturbance enables
alpine grassland composition to change from sedge to unpalatable
broad-leaved plants in the Qinghai-Tibetan Plateau (Pang \& Guo, 2018).
In this case, plateau pikas preferentially consume dicotyledons, and
most dicotyledons are unpalatable plants (Pang \& Guo, 2017; Zhao et
al., 2013). Thus, plateau pika consumption can benefit palatable plant
growth (Pang \& Guo, 2017) since it can alleviate the competitive
pressure of monocotyledons, and these monocotyledons are palatable
plants (Li et al., 2015; Zhao et al., 2013). However, plateau pikas
often bury many plants in the process of producing bare soil patches,
thereby reducing aboveground plants at the plot scale. The decrease in
palatable plant biomass, which is derived from bare soil patches and
sedge replacement by unpalatable broad-leaved plants, is greater than
the increase in palatable plant biomass derived from the alleviation
effect of plateau pika consumption. Therefore, plateau pika disturbance
contributes to a negative effect on palatable plant biomass, resulting
in a decrease in forage availability services. In addition, plateau pika
disturbance in relation to higher plant species richness is similar to
that of other small burrowing herbivore disturbances, such as that of
the plains pocket gopher (Rogers et al., 2001), the coexisting kangaroo
rat and mole rat (Davidson \& Lightfoot, 2008), and the prairie dog
(Hagenah \& Bennett, 2013). Higher plant species richness caused by
plateau pikas can be explained by several mechanisms: first, plateau
pika activities are likely to enhance the environmental heterogeneity
(Guo et al., 2012b; Pang et al., 2020a; Yu et al., 2017a), which creates
gaps for opportunistic plant species (Hagenah \& Bennett, 2013; Pang \&
Guo, 2017); second, bare soil patches caused by plateau pikas provide
additional good habitat for plant seeds to germinate and settle (Pang \&
Guo, 2017) because it is difficult for plant seedlings to survive on
vegetated surfaces with 7 to 8 cm root mats with less soil and water
supplies (Li et al., 2015); third, the burrow of plateau pikas is the
only habitat home for snow finch (\emph{Montifringilla ruficollis} )
(Liu et al., 2013), and this bird can recruit more plant seeds in areas
with plateau pikas. These three processes encourage plateau pika
disturbance to increase the biodiversity conservation service.

Plateau pika disturbance is associated with lower soil water storage
across all five sites or at each individual site, in contrast to the
second hypothesis. This result has also been found in a previous study
(Liu et al., 2013), whereas it is different from prairie dog disturbance
(Martínez-Estévez et al., 2013). The different responses of soil water
storage to disturbance by small burrowing herbivores are ascribed to the
soil porosity and compaction of grassland. Prairie dog disturbance
increases soil water storage by reducing the compaction and increasing
the pore spaces of arid grassland (Martínez-Estévez et al., 2013), while
plateau pika disturbance has no impact on the soil bulk density of
alpine grassland (Pang et al., 2020b) and encourages more topsoil water
to infiltrate into deep soil though bare soil patches and burrow
entrances in root mats (Li et al., 2015), contributing to a decrease in
soil water storage in the topsoil layer. In addition, bare soil patches
caused by plateau pikas can increase water evaporation in topsoil
because of the lack of vegetation insulation. Thus, the plateau pika
disturbance results in low soil water storage in the topsoil layer,
contributing to a reduction in the water conservation service.

Plateau pika disturbance correlates with higher soil organic carbon
stock and does not relate to soil total potassium stock across the five
sites or individual site, whereas plateau pika disturbance has different
impacts on soil total nitrogen stock and soil total phosphorus stock
among five sites, demonstrating that there is a general pattern for
plateau pika disturbance in relation to carbon sequestration and soil
potassium maintenance services, and no general pattern concerns the
effects of plateau pika disturbance on the soil total nitrogen and total
phosphorus maintenance services. These results support the third
hypothesis but do not support the fourth hypothesis. In this case,
plateau pika disturbance can increase the soil organic carbon stock in
two possible ways: first, plateau pika disturbance can input extra
organic matter through the deposition of uneaten food (Liu et al., 2009;
Liu et al., 2013; Yu, et al., 2017a; Zhang et al., 2016) and the
excretion of urine and feces (James et al., 2009; Yu et al., 2017b);
second, the burrowing behavior of plateau pikas can protect the soil
organic matter pools from ultraviolet light and cannot be blown away by
wind (Pang et al., 2020a), which reduces the decomposition,
mineralization and removal of soil organic matter (Clark et al., 2016;
Yurkewycz et al., 2014). Since the responses of soil total nitrogen and
total phosphorus maintenance to plateau pika disturbance are
site-dependent, which is similar to previous studies (Pang et al.
2020b), soil total nitrogen and phosphorus maintenance is not suitable
for estimating the effect of disturbance by small burrowing herbivores
on the ecosystem services of alpine grasslands.

Additionally, this study found that plateau pika disturbance intensity
was also related to palatable plant biomass, plant species richness,
soil water storage, soil organic carbon stock, and soil total nitrogen
and phosphorus stocks. As the disturbance intensity increases, the
palatable plant biomass, plant species richness, soil organic carbon
stock, soil total nitrogen and phosphorus stocks show downward
parabolas, demonstrating that there is a threshold of plateau pika
disturbance intensity for maximizing the forage availability,
biodiversity conservation, carbon sequestration, and soil nitrogen and
phosphorus maintenance services. When the disturbance intensity is
within the threshold of disturbance intensity, plateau pika disturbance
can enhance soil total nitrogen (Li et al., 2014) and organic carbon
accumulation (Yu et al., 2017b), increase palatable plant biomass (Pang
\& Guo, 2018) by improving the growth potential of grass plants (Wang et
al., 2012b), and encourage more hygrophytes and mesophytes, annual and
perennial, common and rare plants to coexist (Guo et al., 2012b),
contributing to higher forage available, biodiversity conservation,
carbon sequestration, soil total nitrogen and phosphorus maintenance
services. When the disturbance intensity is below the threshold of
disturbance intensity, the dominant sedge plants place great competitive
pressure on grass plants, which leads grass plants to maintain a low
percentage (Pang \& Guo, 2018; Wang et al., 2012b) and makes it
difficult for rare plants to coexist. Once the disturbance intensity
surpasses its threshold, low soil water content in alpine grassland (Liu
et al., 2013) only sustains the xerophytes and mesophytes, most of which
are unpalatable (Pang \& Guo, 2018), resulting in reductions in
palatable plant biomass and plant species richness. Notably, the
responses of plant species richness to plateau pika disturbance
intensity showed linear increases at Luqu and Gonghe, which were
ascribed to the disturbance intensity. The disturbance intensities at
these two sites were lower than the threshold of disturbance intensity
(Table 2), which validates the general patterns of plateau pika
disturbance intensity in relation to plant species richness. Plateau
pika disturbance can increase the input of soil organic matter (Pang \&
Guo, 2017; Pang et al., 2020a), and this increase in soil organic matter
is lower when the disturbance intensity is below the threshold. Low
vegetation biomass at high disturbance intensities (Pang \& Guo, 2017;
Pang et al., 2020a; Sun et al., 2015) also decreases the input of soil
organic matter. Thus, soil organic carbon sequestration and soil
nitrogen and phosphorus maintenance services are low when the
disturbance intensity is below or over the thresholds.

In contrast to forage availability, biodiversity conservation, carbon
sequestration, soil nitrogen and phosphorus maintenance services, the
water conservation service shows a decreasing trend as the plateau pika
disturbance intensity increases, which is ascribed to evaporation and
water infiltration on bare soil patches. Previous studies have shown
that evaporation and water infiltration from topsoil to deep soil are
higher in bare soil patches than in vegetated surfaces (Liu et al.,
2013; Yu et al., 2017b). As the soil bare area increases, the amount of
water evaporation and infiltration shows an increasing trend (Liu et
al., 2013), which encourages the soil water storage to decrease,
contributing to a gradual decrease in the water conservation services of
alpine grasslands.

Data from one site show that prairie dog disturbance has a positive
impact on grassland ecosystem services in arid regions of North America
(Martínez-Estévez et al., 2013), whereas data from five sites show that
plateau pika disturbance and its disturbance intensity have a positive
or negative impact on different ecosystem services of alpine grasslands
in the Qinghai-Tibetan Plateau. Thus, a general pattern can be
identified for the effect of plateau pika disturbance on forage
availability, biodiversity conservation, water conservation and carbon
sequestration services, whereas the soil nutrient maintenance service in
relation to plateau pika disturbance varies by site. These results
indicated that plateau pika control should consider the management
target of ecosystem services for alpine grasslands and its disturbance
intensity threshold in the Qinghai-Tibetan Plateau. The findings of this
study present a possible pattern of how disturbance by small burrowing
herbivores influences grassland ecosystem services and open a broader
vision for insight into small burrowing herbivore in relation to
grassland ecosystem services.

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\textbf{Table legends}

\textbf{Table 1} Palatable plant biomass, plant species richness, soil
water storage, soil organic carbon stock, soil total nitrogen stock,
soil total phosphorus stock and soil total potassium stock in relation
to plateau pika disturbance (disturbance), site (site) and their
interaction.

\textbf{Table 2} Percentage of bare soil area of the total plot area (35
m \selectlanguage{english}? 35 m) in the presence of plateau pikas. Significance was evaluated
using one-way ANOVA with the Tukey post hoc test. Different letters
denote significant differences at \emph{P} \textless{}0.05. Presented
are the means +-1 standard deviation for the five sites; each site had 10
replicates (n=50).

\textbf{Table 1}\selectlanguage{english}
\begin{longtable}[]{@{}llllllllll@{}}
\toprule
Response variable & Site & Site & Disturbance & Disturbance &
Disturbance & Disturbance & Disturbance & Site\selectlanguage{ngerman}×Disturbance &
Site\selectlanguage{ngerman}×Disturbance\tabularnewline
\midrule
\endhead
& F & \emph{P} & \emph{P} & & F & \emph{P} & & F &
\emph{P}\tabularnewline
Palatable plant biomass & 5.857 & 0.058 & 0.058 & & 17.331 &
\textbf{0.014} & & 3.392 & \textbf{0.012}\tabularnewline
Plant species richness & 59.074 & \textbf{0.001} & \textbf{0.001} & &
28.058 & \textbf{0.006} & & 1.746 & 0.147\tabularnewline
Soil water storage & 111.215 & \textbf{0.000} & \textbf{0.000} & &
76.053 & \textbf{0.001} & & 0.758 & 0.470\tabularnewline
Soil organic carbon stock & 12.544 & \textbf{0.016} & \textbf{0.016} & &
21.033 & \textbf{0.010} & & 3.900 & \textbf{0.006}\tabularnewline
Soil total nitrogen stock & 46.779 & \textbf{0.001} & \textbf{0.001} & &
90.628 & \textbf{0.001} & & 0.224 & 0.924\tabularnewline
Soil total phosphorus stock & 6.557 & \textbf{0.048} & \textbf{0.048} &
& 11.204 & \textbf{0.029} & & 0.949 & 0.439\tabularnewline
Soil total potassium stock & 10.317 & \textbf{0.022} & \textbf{0.022} &
& 0.004 & 0.955 & & 0.581 & 0.677\tabularnewline
\bottomrule
\end{longtable}

\textbf{Table 2}\selectlanguage{english}
\begin{longtable}[]{@{}ll@{}}
\toprule
Location & Bare soil area (\%)\tabularnewline
\midrule
\endhead
Luqu & 6.67\selectlanguage{ngerman}±1.00b\tabularnewline
Gangcha & 12.82\selectlanguage{ngerman}±1.58a\tabularnewline
Haiyan & 12.80\selectlanguage{ngerman}±2.34a\tabularnewline
Qilian & 11.56\selectlanguage{ngerman}±1.89a\tabularnewline
Gonghe & 6.48\selectlanguage{ngerman}±1.04b\tabularnewline
\bottomrule
\end{longtable}\selectlanguage{ngerman}



\textbf{Figure legends}

\textbf{FIGURE 1} Palatable plant biomass of undisturbed and disturbed
plots across five sites (A) and each site (B) (mean ± standard error).

\textbf{FIGURE 2} Plant species richness of the undisturbed and
disturbed plots across five sites (A) and each site (B) (mean ± standard
error).

\textbf{FIGURE 3} Soil water storage of the undisturbed and disturbed
plots across five sites (A) and each site (B) (mean ± standard error)

\textbf{FIGURE 4} Soil organic carbon stock of undisturbed and disturbed
plots across five sites (A) and each site (B) (mean ± standard error).

\textbf{FIGURE 5} Soil total nitrogen stock of undisturbed and disturbed
plots across five sites (A) and each site (B) (mean ± standard error),
soil total phosphorus stock of undisturbed and disturbed plots across
five sites (C) and each site (D) (mean ± standard error), soil total
potassium stock of undisturbed and disturbed plots across five sites (E)
and each site (F) (mean ± standard error).

\textbf{FIGURE 6} Relationship between palatable plant biomass and
plateau pika disturbance intensity across five sites (A) and each site
(B) based on linear models (LMs). An adjusted local smoothed regression
line (A) and five adjusted local smoothed regression lines (B) were used
to determine the relationship between the disturbance intensity and each
palatable plant biomass with data from five sites and individual site
data, respectively.

\textbf{FIGURE 7} Relationship between plant species richness and
plateau pika disturbance intensity across five sites (A) and each site
(B) based on linear models (LMs).

\textbf{FIGURE 8} Relationship between soil water storage and plateau
pika disturbance intensity across five sites (A) and each site (B) based
on linear models (LMs).

\textbf{FIGURE 9} Relationship between soil organic carbon stock and
plateau pika disturbance intensity across five sites (A) and each site
(B) based on linear models (LMs).

\textbf{FIGURE 10} Relationship between soil total nitrogen stock and
plateau pika disturbance intensity across five sites (A) and each site
(B) based on linear models (LMs).

\textbf{FIGURE 11} Relationship between soil total phosphorus stock and
plateau pika disturbance intensity across five sites (A) and each site
(B) based on linear models (LMs).

\textbf{FIGURE 12} Relationship between soil total potassium stock and
plateau pika disturbance intensity across five sites (A) and each site
(B) based on linear models (LMs).

\textbf{Hosted file}

\verb`image1.emf`  available at \url{https://authorea.com/users/389176/articles/503789-effect-of-plateau-pika-disturbance-on-the-ecosystem-services-of-alpine-grasslands}

\textbf{FIGURE 1} Palatable plant biomass of undisturbed and disturbed
plots across five sites (A) and each site (B) (mean ± standard error).

\textbf{Hosted file}

\verb`image2.emf`  available at \url{https://authorea.com/users/389176/articles/503789-effect-of-plateau-pika-disturbance-on-the-ecosystem-services-of-alpine-grasslands}

\textbf{FIGURE 2} Plant species richness of the undisturbed and
disturbed plots across five sites (A) and each site (B) (mean ± standard
error).

\textbf{Hosted file}

\verb`image3.emf`  available at \url{https://authorea.com/users/389176/articles/503789-effect-of-plateau-pika-disturbance-on-the-ecosystem-services-of-alpine-grasslands}

\textbf{FIGURE 3} Soil water storage of the undisturbed and disturbed
plots across five sites (A) and each site (B) (mean ± standard error).

\textbf{Hosted file}

\verb`image4.emf`  available at \url{https://authorea.com/users/389176/articles/503789-effect-of-plateau-pika-disturbance-on-the-ecosystem-services-of-alpine-grasslands}

\textbf{FIGURE 4} Soil organic carbon stock of undisturbed and disturbed
plots across five sites (A) and each site (B) (mean ± standard error).

\textbf{Hosted file}

\verb`image5.emf`  available at \url{https://authorea.com/users/389176/articles/503789-effect-of-plateau-pika-disturbance-on-the-ecosystem-services-of-alpine-grasslands}

\textbf{FIGURE 5} Soil total nitrogen stock of undisturbed and disturbed
plots across five sites (A) and each site (B) (mean ± standard error),
soil total phosphorus stock of undisturbed and disturbed plots across
five sites (C) and each site (D) (mean ± standard error), soil total
potassium stock of undisturbed and disturbed plots across five sites (E)
and each site (F) (mean ± standard error).

\textbf{Hosted file}

\verb`image6.emf`  available at \url{https://authorea.com/users/389176/articles/503789-effect-of-plateau-pika-disturbance-on-the-ecosystem-services-of-alpine-grasslands}

\textbf{FIGURE 6} Relationship between palatable plant biomass and
plateau pika disturbance intensity across five sites (A) and each site
(B) based on linear models (LMs). An adjusted local smoothed regression
line (A) and five adjusted local smoothed regression lines (B) were used
to determine the relationship between the disturbance intensity and each
palatable plant biomass with data from five sites and individual site
data, respectively.

\textbf{Hosted file}

\verb`image7.emf`  available at \url{https://authorea.com/users/389176/articles/503789-effect-of-plateau-pika-disturbance-on-the-ecosystem-services-of-alpine-grasslands}

\textbf{FIGURE 7} Relationship between plant species richness and
plateau pika disturbance intensity across five sites (A) and each site
(B) based on linear models (LMs).

\textbf{Hosted file}

\verb`image8.emf`  available at \url{https://authorea.com/users/389176/articles/503789-effect-of-plateau-pika-disturbance-on-the-ecosystem-services-of-alpine-grasslands}

\textbf{FIGURE 8} Relationship between soil water storage and plateau
pika disturbance intensity across five sites (A) and each site (B) based
on linear models (LMs).

\textbf{Hosted file}

\verb`image9.emf`  available at \url{https://authorea.com/users/389176/articles/503789-effect-of-plateau-pika-disturbance-on-the-ecosystem-services-of-alpine-grasslands}

\textbf{FIGURE 9} Relationship between soil organic carbon stock and
plateau pika disturbance intensity across five sites (A) and each site
(B) based on linear models (LMs).

\textbf{Hosted file}

\verb`image10.emf`  available at \url{https://authorea.com/users/389176/articles/503789-effect-of-plateau-pika-disturbance-on-the-ecosystem-services-of-alpine-grasslands}

\textbf{FIGURE 10} Relationship between soil total nitrogen stock and
plateau pika disturbance intensity across five sites (A) and each site
(B) based on linear models (LMs).

\textbf{Hosted file}

\verb`image11.emf`  available at \url{https://authorea.com/users/389176/articles/503789-effect-of-plateau-pika-disturbance-on-the-ecosystem-services-of-alpine-grasslands}

\textbf{FIGURE 11} Relationship between soil total phosphorus stock and
plateau pika disturbance intensity across five sites (A) and each site
(B) based on linear models (LMs).

\textbf{Hosted file}

\verb`image12.emf`  available at \url{https://authorea.com/users/389176/articles/503789-effect-of-plateau-pika-disturbance-on-the-ecosystem-services-of-alpine-grasslands}

\textbf{FIGURE 12} Relationship between soil total potassium stock and
plateau pika disturbance intensity across five sites (A) and each site
(B) based on linear models (LMs).

\selectlanguage{english}
\FloatBarrier
\end{document}

