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Plateau pikas (Ochotona curzoniae) at low densities
have no destructive effect on winter pasture
in alpine meadows
W. R. Wei
A
,
B
,
E
,J. D. He
C
and Q. Y. Zheng
D
A
Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education),
College of Life Sciences, China West Normal University, Nanchong, China.
B
State Key Laboratory of Grassland Agro-Ecosystems, College of Pastoral Agriculture Science and
Technology, Lanzhou University, Lanzhou, China.
C
Key Laboratory of Southwest China Wildlife Resources Conservation (Ministry of Education),
China West Normal University, Nanchong, China.
D
China West Normal University, Nanchong, China.
E
Corresponding author. Email: weiwr18@126.com
Abstract. The plateau pika (Ochotona curzoniae) is a common small mammal species present in the alpine meadow
ecosystem on the Qinghai-Tibetan Plateau (QTP), and is regarded as a pest in alpine meadows when population density
exceeds a certain threshold. However, whether pikas with a low population density have a detrimental effect on alpine
meadows in winter pasture is unknown. Vegetation and soil were sampled in eight individual pika patchy home ranges and
eight control areas, and we found vegetation and soil properties showed different trends in the pika home ranges. Plateau
pika activity significantly increased the below-ground biomass, soil pH and total potassium, but had no significant effect
on the plant species richness or diversity, soil moisture, NH
4
-N, NO
3
-N, total phosphorus, available phosphorus and soil
organic content. However, plateau pika activity reduced some vegetation and soil properties (e.g. vegetation cover,
vegetation height, aboveground biomass, graminoids, soil bulk density and available potassium). These results imply that
pika activity may improve some soil nutrients but have no destructive effect on winter pasture at a low population density.
Additional keywords: alpine meadow, home range, plateau pika, soil nutrients.
Received 25 June 2019, accepted 2 April 2020, published online 14 April 2020
Introduction
Large grazing herbivores can have significant effects on grass-
land ecosystems by influencing plant communities and soil (van
Klink et al. 2015). In addition, foraging and burrowing by small
mammals often causes extensive grassland disturbance. These
disturbances are important bioturbators, and their influence on
grassland ecosystems cannot be ignored (Bagchi and Mishra
2006; Davidson and Lightfoot 2008). Previous studies have
shown that small mammal disturbance can increase plant diver-
sity (Bagchi and Mishra 2006), plant richness (Davidson and
Lightfoot 2008;Svejcaret al. 2019), improve plant productivity
(Martı´nez-Este´vez et al. 2013), and affect soil physical (Galiano
et al. 2014;Svejcaret al. 2019) and chemical properties (Jirout
and Piz
ˇl2014;Galianoet al. 2014) of grassland. However, some
studies have found that small mammal disturbance has no sig-
nificant effects on the plant community (Adams et al. 2010)and
soil properties (Zhang et al. 2016;Yuet al. 2017; Svejcar et al.
2019). Further, other studies have shown that small mammals
with low population densities can increase aboveground biomass
(Pang and Guo 2017;Leiset al. 2008), plant richness (Pang and
Guo 2017)andNO
3–
-N and NH
4þ
-N (Yu et al. 2017), but when
present in high densities, they can decrease plant richness (Pang
and Guo 2017), graminoid biomass (Guo et al. 2012a) and soil
nutrients concentrations (Bagchi and Mishra 2006;Sunet al.
2011;Leiset al. 2008;Guoet al. 2012b;Svejcaret al. 2019).
Therefore, the effects of small mammals on the plant community
and soil appear to vary with population density.
The plateau pika (Ochotona curzoniae) is an endemic small
mammal that inhabits the Qinghai-Tibetan Plateau, China. It is
generally believed that at high densities, pikas are either a
driving factor, or a contributor, to grassland degradation
(Smith and Foggin 1999; Sun et al. 2011), and that they could
become a pest in alpine meadows because they compete with
livestock for food (Fan 1999; Guo et al. 2012a,2012b), and
create bare-ground patches which can enhance moisture evapo-
ration and soil erosion (Pech et al. 2007; Liu et al. 2010; Guo
et al. 2012b). Consequently, to preserve alpine meadows, the
Chinese government has implemented policies to control pika
CSIRO PUBLISHING
The Rangeland Journal, 2020, 42, 55–61
https://doi.org/10.1071/RJ19042
Journal compilation ÓAustralian Rangeland Society 2020 www.publish.csiro.au/journals/trj
densities over the past several decades. However, these control
efforts are unsatisfactory because pika population densities
often recover quickly, often as short as one breeding season
(Liu et al. 2012). Moreover, these control efforts are controver-
sial, and several studies have argued that the plateau pika should
be considered as a keystone species in maintaining alpine
meadow biodiversity (Smith and Foggin 1999; Lai and Smith
2003; Wen et al. 2013). Abandoned pika burrows provide shelter
for many native birds and lizards (Lai and Smith 2003), and
pikas are also an important prey for nearly all plateau carnivores
(Fan 1999; Lai and Smith 2003; Delibes-Mateos et al. 2011). In
addition, pika burrowing activities influence the hydrological
functioning of grassland ecosystems, and reduce the chance of
flooding by increasing water infiltration (Cai and Zhou 2009;
Guo et al. 2012b; Wilson and Smith 2015).
The alpine meadows are mainly used for grazing by livestock
(Tibetan sheep and yak), and are often classified into summer
pasture and winter pasture according to the different grazing
management during warm and cold periods (Sun et al. 2015).
Pikas occur in both summer and winter pastures (Wei et al.
2019). Since livestock strongly affect vegetation and soil in the
meadow growing season, the soil and vegetation condition of
summer pastures cannot be determined solely by studying the
effects of pikas (Shen et al. 2004). However, winter pasture is a
useful pasture to study the effects of pikas on vegetation and soil
because the vegetation in winter pasture is unaffected by
livestock during the growing season (Shen et al. 2004).
Plateau pika populations are widespread and fairly continu-
ous in degraded pasture (Pech et al. 2007; Jia et al. 2014), and
numerous studies have investigated the effects of pikas on plants
and soil characteristics. However, pika home ranges are patchily
distributed in non-degraded pasture, and this is particularly
obvious in winter pasture (Sun et al. 2016; Wei et al. 2019).
The impact of pika on alpine vegetation and soils in winter
pasture has yet to be studied, therefore the objective of the
present study was to investigate how pikas influence grassland
vegetation and soil in winter pasture where pikas have a patchy
distribution, to provide useful information for the management
of the plateau pika in the Qinghai-Tibetan Plateau.
Methods
Study site
The study area is located at the Hequ racecourse, Maqu
County, eastern Qinghai-Tibet Plateau in Gansu Province
(33.67758,34.69508N, 100.88888,101.88958E), China.
Alpine meadows account for 89.5% of the total land area in
Maqu county (Wei et al. 2014). The elevation of the study site is
3430 m (a.s.l.). The climatic conditions consist of a short warm
season (June to September) and a long cool season (October to
May), with a mean annual temperature is 1.28C (ranging from
–10.08C in January to 11.78C in July). Mean annual precipitation
is 564 mm, 80% of which occurs from May to September, and
potential annual evaporation is 1352 mm. The soil type is an
alpine meadow soil. The vegetation in this alpine meadow
is dominated by Elymus nutans griseb (Poaceae), Kobresia
pygmaea (Cyperaceae), Anemone rivularis (Ranunculaceae),
Potentilla anserine (Rosaceae), Cremanthodium lineare
(Compositae) and other common plants (Wei et al. 2019).
Field investigation
The study site was an area of 800 800 m of alpine meadow
previously used as summer pasture, and has been fenced since
2011. The study area is utilised as a winter pasture, only grazed
during the cool season (October to mid-April) by Tibetan sheep
(Ovis aries), with an annual stocking rate of ,20 head of sheep
ha
1
. Within the study area, there were 14 patchy home ranges
(the pika family groups are distributed patchily in their habitat),
with a radius exceeding 15 m that have been continuously
occupied by pikas for the last five years (Wei et al. 2019). Con-
sistent with many studies (Fan 1999;Sunet al. 2011;Guoet al.
2012a), these patchy home ranges are often surrounded by short
and sparse vegetation. Conversely, vegetation is tall and dense in
the areas without pika activity. In July 2015 we investigated eight
of these patchy home ranges which had similar vegetation.
Twelve 50 50 cm quadrants of vegetation and soil in each of the
pika patchy home ranges were sampled, together with three
randomly selected quadrats outside each pika family home range
that were located at least 10 m away, and without any pika bur-
rows, runways and tracks, and which were used as controls. The
active burrow density of the study site was determined in July of
2015 using the active burrow abundance survey method. The
active burrow entrances were recorded by closing all burrow
entrances with cow-dung at 1500 hours, and the open burrow
entrances after 24 h were considered the active burrow abundance
of this winter pasture. The recorded density of active burrows was
32.51 burrows per ha which falls in the range of low burrow
density according to Guo et al. (2012a,2012b).
Vegetation community composition and biomass
Vegetation cover, community height, species richness, species
frequency and aboveground and below-ground biomass were
determined in July 2015. Plant species cover was calculated with
the acupuncture method (Guo et al. 2012a). Plant community
height was measured by averaging the heights of 10 randomly
selected plants. Species richness was determined by the number
of species recorded in a 0.25-m
2
quadrat. Species frequency was
calculated based on occurrence in 10 quadrats. Aboveground
community biomass was assessed by clipping all plants at
ground level in a 0.25-m
2
quadrat, drying them at 808C for 24 h
and weighing. The below-ground biomass (0–15 cm) obtained
from a soil core (radius of 3 cm, height of 15 cm) was collected,
washed, dried at 808C for 24 h and weighed.
Soil sampling and laboratory analysis
The ring knife measure was used to determine soil bulk density
(SBD) at 15 cm depth. Adjacent soil columns 15 15 cm in size
were dug to the same depth to determine soil moisture (SM), soil
pH, ammonium nitrogen (NH
4
-N), nitrate nitrogen (NO
3
-N),
total phosphorus (TP), available phosphorus (AP), total potas-
sium (TK), available potassium (AK) and organic matter content
(SOC) (Wei et al. 2019). Soil water content of 100-g soil sam-
ples was measured by drying at 1058C. Soil pH was measured
using a glass electrode (Spectrum Technology Inc., Shanghai,
China) in a 1:5 soil/water suspension. The organic matter con-
tent was determined by the Walkley-Black wet combustion
method. NH
4
-N and NO
3
-N (extracted by 1 mol/L KCl) were
determined with the AutoAnalyzer 3 (BranþLuebbe GmbH,
56 The Rangeland Journal W. R. Wei et al.
Hamburg, Germany). The soil concentrations of TP, AP
(extracted by 0.5 mol/L NaHCO
3
), TK, and AK (extracted by
1 mol/L CH
3
COONH
4
) were measured with an ULTIMA
Inductively Coupled Plasma Spectrometer (Jobin Yvon Co.,
Paris, France) (Yu et al. 2017).
Calculation methods
Plant biomass was divided into four different taxonomic
groups: Gramineae (grasses), Cyperaceae (sedges),Leguminosae
(legumes) and forbs. Cyperacea and Gramineae are the preferred
food of livestock, hence the % graminoids was calculated as:
Graminoids %ðÞ¼ Cypereaceae þGramineaeÞðð =
total plant biomassðÞÞ100:
The diversity index used the Shannon–Wiener’s diversity
index, calculated as:
H¼Xn
i¼1Pi log Pi
where Pi is the proportion of plants made of that the ith species.
Data analysis
All data were analysed using SPSS 17.0 for Windows. The non-
parametric Mann–Whitney test was used to test for the differ-
ences of vegetation cover, plant height, species richness,
aboveground biomass, below-ground biomass, graminoids,
plant diversity, soil pH, SBD, SM, NH
4
-N, NO
3
-N, TP, AP, TK,
AK and SOC, because ‘pika home ranges’ and ‘controls’ were
regarded as two independent samples in our study. The statis-
tical significance was defined at the 95% confidence level
(a¼0.05). All mean values are presented with s.e.
Results
Plant community
Vegetation cover, height, aboveground biomass, graminoids
and the relative abundance of Grass functional group biomass
were significantly lower in patchy home ranges compared with
the controls (Fig. 1a–c,f,h). In contrast, the below-ground
biomass, the relative abundance of sedge, legume and forb
functional group biomass were significantly higher in patchy
home ranges compared with the controls (Fig. 1d,h). However,
plant richness and plant diversity in patchy home ranges did not
significantly differ from the controls (Fig. 1e,g).
Soil properties in pika patchy home ranges and in the
controls
Soil physical properties
SM was similar but SBD was higher in controls compared
with the patchy home ranges (Fig. 2a,b). Soil pH was the reverse
(Fig. 2c).
Nutrient availability
The NH
4
-N, NO
3
-N, TP, AP and SOC in patchy home ranges
did not differ from the controls (Fig. 2d,e,f,hand k). TK was
higher in patchy home ranges compared with controls (Fig. 2i),
but AK exhibited the opposite pattern (Fig. 2j).
0
20
40
60
Vegetation cover (%)
Above-ground biomass (g m–2)
Species richnessPlant diversity
Vegetation height (cm)
Below-ground biomass (g dm–3)
Graminoids (%)
0
20
10
40
30
a
50
0
20
10
40
30
50
60
80
100
0
60
90
30
0
20
25
10
5
15
0
Controls
2.0
3.0
2.5
1.0
0.5
1.5
120
150
b
b
a
0
60
80
20
40
120
100
b
a
a
a
aa
b
a
b
a
b
b
b
b
a
a
aa
0
20
10
5
15
The relative cover of the four
functional groups biomass (%)
Grass Sedge Legume Forbs
Home ranges
Controls
Home ranges
(a)(b)
(c)(d)
(e)(f)
(g)(h)
Sam
p
le areas
Fig. 1. Vegetation cover (a), community height (b), aboveground bio-
mass m
2
(c), below-ground biomass (0– 15 cm) g m
2
(d), species richness/
0.25 m
2
(e), graminoids (f), plant diversity (Shannon–Wiener index)/
0.25 m
2
(g) and the relative cover of the four functional group’s biomass
(%) (h) in pika home ranges and controls. Data are represented as the
mean s.e. Different lower-c ase letters within a measurement type indicate
differences at P,0.05.
Pikas do not affect winter meadow pasture The Rangeland Journal 57
Discussion
Plateau pikas can influence vegetation communities directly by
their foraging behaviour and indirectly through their burrowing
behaviour. Results here demonstrate that pika activity decreased
vegetation cover, height and aboveground biomass in alpine
meadows. However, these changes do not imply the grassland
productivity has been reduced or that the pasture has degraded.
Pika digging activities will bury some plants and reduce vege-
tation cover (Guo et al. 2012a). Pikas foraging activities and the
clipping of tall plants will inevitably decrease the vegetation
height and aboveground biomass (Sun et al. 2011). In addition to
these changes in plant characteristics in relation to pika activity,
vegetation changes among the major functional plant groups
were recorded. Graminoids decreased, largely driven by grass
rather than sedge abundance (Fig. 1h). Two explanations are
suggested. First, grasses are preferred by pikas (Sun et al. 2010),
although the pika diet has been reported to be generalised, and
closely related to the composition of the habitat plant commu-
nity (Lai and Smith 2003). Second, pikas prefer habitats with
sparse and low vegetation (Wangdwei et al. 2013), so they clip
tall grasses (mainly Elymus nutans,Poa annua and Koeleria
glauca) to make predator detection easier, and so reduce pre-
dation risk. Corresponding with the decline in grasses, there was
a relative increase in forbs and to a lesser extent in legumes,
since grass decline provides a survival space for forbs and
legumes (Sun et al. 2010; Guo et al. 2012a).
Our results also show that below-ground biomass, species
diversity and richness in pika home ranges are not significantly
different compared with the controls. Such patterns of below-
ground biomass in response to herbivory are uncommon (Pech
et al. 2007; Delibes-Mateos et al. 2011; Sun et al. 2011), and
there are two possible explanations for the patterns of below-
ground biomass recorded. First, this result may be associated
with pika disturbance increasing soil permeability, which in turn
leads to an increase in root biomass (Wei et al. 2019). Second,
pika activity increases legumes and forbs, and these species
allocate more biomass to belowground (Peng et al. 2020). A
previous study found that significant differences in species
diversity and richness were related to areas of pika family home
range that differ in pika activity, which is often highly variable
in peripheral areas and more uniform in central areas (Wei et al.
2019). Such significant spatial differences in species diversity
and richness were not recorded here, since data from the central
and peripheral activity areas were averaged. This suggests
vegetation characteristics are related to the sampling areas in
pika home ranges which are directly influenced by pika activity
(Wei et al. 2019). In addition, species richness was not signifi-
cantly different in pika home ranges and control areas, which
may be related to the quadrant size used. In this study, quadrant
size was 0.25 m
2
, smaller than quadrants used in other studies
(Sun et al. 2016; Pang and Guo 2017).
In alpine meadows, a large amount of dead roots and litter
are stored in the form of organic matter due to the extremely
cool climate, and this organic matter decomposes slowly,
resulting in a relatively low quantity of nutrients. Pikas play
an important role in soil nutrient cycling and their digging
activities can change the process of nutrient cycling by
burying vegetation in soil, fragmenting plants and excretion
1.0
1.5
SM (%)Soil pH
0
20
10
40
30
aaa
50
b
(a)(b)
0
1.0
0.5
1.5
SBD (g cm–3)
NH4-N (mg/kg)
NO3-N (mg/kg)
AP (mg/kg)AK (mg/kg)
TP (g/kg)TK (g/kg)SOC (g/kg)
(c)
(e)
(d)
00
2
4
6
8
20
10
40
30
a
a
50
ab
0
7
14
21
28
0
2.0
2.5
0.5
1.5
1.0
(f)
(h)(i)
(j)(k)
aa
a
a
0
20
25
10
5
0
4
3
2
1
15
0
20
25
30
35
10
5
15
0
200
250
300
100
50
150
aaa
b
a
ba
a
Controls
Home ranges
Controls
Home ranges
Sam
p
le areas
Fig. 2. Soil moisture (a), soil bulk density (b), soil pH (c), NH
4
-N (d),
NO
3
-N (e), total phosphorus (f), available phosphorus (h), total potassium (i),
available potassium (j) and organic matter content (k) at the 15 cm depth in
pika home ranges and controls. Data are represented as the mean s.e.
Different lower-case letters within a measurement type indicate differences
at P,0.05.
58 The Rangeland Journal W. R. Wei et al.
activities (Sun et al. 2011). In addition, the soil nutrient content
is related to the intensities of pikas disturbance (Pang and Guo
2017;Yuet al. 2017). However, previous studies show
inconsistent results. Some studies have shown pika activity
increased SM (Sun et al. 2010), SBD (Zhou et al. 2018), total
nitrogen and SOC (Pang and Guo 2017;Yuet al. 2017), and TP
and AP, NH
4
-N and NO
3
-N (Yu et al. 2017). Conversely, other
studies recorded that pika activity decreased SM (Pang and
Guo 2017;Zhouet al. 2018), SOC and NH
4
-N (Zhou et al.
2018), and had no significant influence on soil pH (Zhang et al.
2016), AK (Yu et al. 2017),andTPandTK(PangandGuo
2017). Our results indicate that SM, NH
4
-N, NO
3
-N, TP, AP
and SOC were similar between control areas and pika home
ranges, soil pH and TK were higher in pika home ranges, and
SBD and AK were lower in pika home ranges compared with
the controls. The SM was lower in the pika home ranges than in
the controls, but not significantly so. This may be the result of a
combination of increased soil evaporation caused by the
decline of vegetation cover, and increased soil permeability
due to a decrease in SBD (Fig. 2b). The changes in alkaline pH
is related to the inorganic carbon (Wei et al. 2019). However,
we do not have any data on inorganic carbon. No significant
difference in NH
4
-N, NO
3
-N, TP, AP and SOC were found in
pika home ranges and controls. This may be attributed to the
fact that the low intensity of pika disturbances was less
effective on reinforcing the soil mineralisation rate than was
its ability to promote plant absorption and the utilisation of soil
nutrients because of the phosphorusaswellasnitrogen
deficiency in alpine meadow (Guo et al. 2012b;Yuet al.
2017). A previous study found that the TK of vegetated land
and bare land was significantly different in pika activity areas
(Guo et al. 2012b). The increase in soil TK may be due to the
random setting of quadrats that did not distinguish between
vegetated and bare land. The changes in soil AK may be the
result of accelerated absorption and utilisation of AT in plants
because pika foraging activities stimulate plant growth in
growingseason(Sunet al. 2010).
Indeed, our results show that the presence of pika activity has
effects on vegetation characteristics. The changes in vegetation
are caused by the pika foraging activities and attempts to reduce
predation risks (Wei et al. 2019). The reduction in vegetation
cover, height, aboveground biomass and graminoids is merely a
cosmetic phenomenon. The grasses regrow during the next
growing season or when pikas are removed. Therefore, the pikas
have an effect on the vegetation, but it is not damaging. There are
several caveats related to our study. Summer pasture is grazed
from June to September, and winter pasture from October to
May. Compared with winter grazing, summer grazing has a
greater impact on vegetation as this is the growing season. The
vegetation condition in the growing season will directly affect
the predation risk of pikas (Wei et al. 2019), and indirectly affect
pika reproduction and mortality rates (Choying 2016). Vegeta-
tion in the summer pasture is strongly affected by grazing,
especially overgrazing, which favours the expansion of pika
populations (Shi 1983). Grazing winter pasture does not directly
affect plant growth, but has indirect effects during the growing
season. Although sampling was completed in summer while
livestock were in summer pasture, pika herbivory and livestock
grazing can interact, and grazing intensity can vary greatly over
very small distances (Harris et al. 2015,2016; Yeh et al. 2017).
However, we did not examine summer grazed pasture, and the
influence of pikas on summer pasture may be different from
their influence on winter pasture. In addition, pikas do not
occupy a habitat for an extended time period (Wei et al.
2014). A possible factor is that our study period spans only
one year, and a long-term study may be more useful in deter-
mining whether yearly variations in winter climatic conditions
affect how pikas interact with winter pasture grassland.
Pika colonies can be continuous over very large areas (Han
et al. 2008), especially in heavily grazed areas. Such over-
grazing leads to habitat degeneration which is more suitable for
pika survival and reproduction (Fan 1999;Maet al. 2007). In
contrast, our study area was grazed only in winter, with less
vegetation and soil disturbance by livestock, and the pika
population density was relatively low and more stable. Within
our study area, plateau pika showed a conspicuous patchy
distribution and only affected some vegetation and soil proper-
ties, which did not cause extensive grassland damage.
The findings in the present study should be interpreted in the
light of the study conditions: it was conducted in the winter
season when pasture growth is minimal and the pika density was
low. Consequently, conclusions drawn from these findings
should be restricted to similar situations. Further research is
needed in situations where the pika density is moderate or high
in winter pasture. This could help explain the relationship
between pika population density and grassland, and whether
pikas will exacerbate alpine meadow degradation when popula-
tion densities exceed a certain threshold.
Conclusions
Plateau pikas affect some vegetation and soil characteristics of
winter pasture in alpine meadows. Specifically, pikas decreased
vegetation cover, height, aboveground biomass, graminoids,
SBD and AK and increased the below-ground biomass and TK.
There was an effect, and this effect was significant. However,
these changes do not mean that pikas activities reduced the
grassland productivity. Instead, these results imply that low
density pika activity does not cause extensive damage to winter
pasture grassland. The plateau pika fulfils the definition of an
‘ecosystem engineer’, as an organism that directly or indirectly
modulates the availability of resources for other species, by
causing physical state changes in biotic or abiotic material
(Smith and Foggin 1999; Lai and Smith 2003). Our results
suggest that control and management of pikas when their density
is low is unnecessary, since they act as ecosystem engineers and
have no destructive effect on the winter pasture.
Conflicts of interest
The authors declare no conflicts of interest.
Acknowledgements
We thank Paul Novelly and Maria K Oosthuizen for critically reading and
commenting on the manuscript. This research was financially supported by
the Fundamental Research Funds of China West Normal University
(18Q046), the Special Fund for Agro-Scientific Research in the Public
Interest (201203041) and the Gansu Provincial Science and Technology
Program (1054nkcp159).
Pikas do not affect winter meadow pasture The Rangeland Journal 59
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