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\begin{document}

\title{Den characteristics and ecological significance of Marmota himalayana on
the Qinghai-Tibet Plateau}



\author[1]{Shulin Wang}%
\author[1]{Fujiang Hou}%
\affil[1]{Affiliation not available}%


\vspace{-1em}



  
  \date{May 26, 2024}


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\selectlanguage{english}
\begin{abstract}
Dens are places for cavernicolous animals to hibernate, reproduce, and
avoid predators and harsh weather conditions, and thus they have a vital
impact on their survival. M. himalayana is the main large cavernicolous
rodent on the Qinghai-Tibet Plateau. The analysis of den traits and
their ecological functions can reveal mechanisms by which marmots have
adapted to their environment, which is important for further
understanding the ecological significance of this species. From July to
August 2019 (warm season), we used unmanned aerial vehicles to fly at
low altitudes and slow speeds to locate 131 marmot burrows (45 on shaded
slopes, 51 on sunny slopes, and 35 on flat areas) in the northeastern
Qinghai-Tibet Plateau. We then measured the physical characteristics
(den density, entrance size, first tunnel length, volume, orientation
and plant characteristics near the den entrance) of these dens on site.
The physical parameters of the M. himalayana dens showed that they
function to protect the marmots from natural enemies and bad weather,
provide good drainage, and maintain a stable microclimate around the
entrance. This is a result of the marmot's adaptation to the harsh
environment (cold and humidity) of the Qinghai-Tibet Plateau.%
\end{abstract}%



\sloppy


\textbf{INTRODUCTION}

Dens used by cavernicolous animals have a vital impact on their
survival. Dens provide animals with a place to rest, hide, and hibernate
and help them avoid bad weather and predators (Ross et al. 2010; Tsunoda
et al. 2018). The ecological characteristics of a den can accurately
reflect the life, behavior, and social networks of cavernicolous
animals. For example, the yellow-bellied marmot (\emph{Marmota
flaviventris} ) in North America uses dens that resist harsh
environments and predators during hibernation and provide a protective
shelter in summer (Svendsen 1976). Pallas's cat (\emph{Otocolobus manul}
), which inhabits the Mongolian plateau, cannot dig burrows by itself,
so it often uses \emph{Marmota sibirica}dens to give birth, raise
offspring, and avoid natural enemies; the availability of \emph{M.
sibirica} dens thus has a very important impact on the stability of the
\emph{O. manul} population (Ross et al. 2010). The puma (\emph{Puma
concolor} ) living in the American continent uses dens to defend against
predators (e.g., adult \emph{Ursus arctos} ) and to maintain
microclimate stability, therefore increasing the survival rate of its
cubs (Bleich et al. 1996; Benson et al. 2008). American black bears
(\emph{Ursus americanus} ) use various types of dens (excavated, trees,
rock cavities) for hibernation, and their dens provide safe places for
female black bears to give birth and rear their cubs; in addition, some
individuals use tree dens that can resist flooding (White et al. 2001).
Therefore, dens offer an excellent means of studying the ecological
adaptation of cavernicolous animals.

Except for plateau rabbits (\emph{Lepus oiostolus} ), \emph{Marmota
himalayana} (hereafter referred to as the marmot) is the only large
rodent in the alpine meadows of the Qinghai-Tibet Plateau (QTP). Marmots
are herbivores and forage mainly on the leaves and stems of Cyperaceae,
Gramineae, and the flowers of legume species. Marmots are of great
significance to the stability of the alpine meadow ecosystem. First, the
marmot is an important part of the food chain in the grassland
ecosystem. It is important prey for large raptors, foxes, and wolves. In
addition, marmots feed on grasslands that cannot be reached by
livestock, which is equivalent to grazing in these areas and is good for
the health of the grasslands (Oesterheld and McNaughton 1991). The
burrowing and digging behavior of marmots is conducive to the
circulation of organic matter in the grasslands. However, marmots do
also cause obvious harm, as they compete with livestock for fine
pasture, dig grass roots, and destroy turf all year round. In the
pasture, marmot holes are the main hidden danger that causes livestock
leg fractures (Chen 1982). Each of their excavated mounds covers a large
area of grassland (\textasciitilde{}2 m\textsuperscript{2}), causing
ground collapse, soil erosion, and desertification. Marmots are also one
of the main spreaders of the plague in this region (Xu et al. 2020),
which seriously threatens the health of grassland herders and livestock.

Habitat selection is a reflection of the environmental, ecological, and
physiological requirements of a species (Kohji and Kenichi 1998). When
cavernicolous animals excavate dens, they typically show a strong
selectivity with respect to the surrounding environment. For example,
the Japanese red fox (\emph{Vulpes vulpes} ) prefers to dig dens closer
to a water source (Kohji and Kenichi 1998). On the north coast of
Alaska, the arctic fox (\emph{Alopex lagopus} ) prefers to choose dens
on the southern slope in an area with thin permafrost (Garrott et al.
1983), which helps to keep the den warm.

In this study, marmot dens that were present in different terrains
(sunny slopes, shady slopes, and flat areas) were located, and the
physical characteristics of these dens were measured under harsh
environmental conditions (low oxygen, low temperature, and high
precipitation) (Zhang et al. 2019). Here we determined (1) the general
physical characteristics and ecological functions of marmot dens and (2)
whether there are differences in den traits under different terrains.
Our findings highlight the adaptation mechanism of \emph{M.
himalayana}with respect to its environment, which is of great
significance for further understanding the ecological characteristics of
the marmot or other cavernicolous animals all over the world.

\textbf{MATERIAL AND METHODS}

\textbf{Study area}

The present study was undertaken at the Lanzhou University Research
Station in Maqu County, Gansu Province, China (101\selectlanguage{ngerman}°53\selectlanguage{english}'E, 33deg58\selectlanguage{english}'N, 3500 m
a.s.l.). This area is located in the northeast of the QTP. The climate
is cold and humid, with only a warm season (May to September) and cold
season (October to April) (Sun et al. 2015). There is no absolute
frost-free period throughout the year. The annual average temperature is
about 1.2 degC, and the highest temperatures are from June to August, with
an average of \textless{}12 degC; the lowest temperatures (average of \selectlanguage{english}-10
degC) are from December to February. The average annual rainfall is
\textasciitilde{}620 mm, which occurs mainly during the forage growing
season (May to September). These soils are classified as Mat-Cryic
Cambisols based on previous experimental work (Sun et al. 2015), and the
vegetation is characteristic of a typical alpine meadow (Yang et al.
2019). Cyperaceae (\emph{Kobresia graminifolia} , \emph{Kobresia
humilis} , and \emph{Kobresia pygmaea} ) constitute the constructive
species, and Gramineae (\emph{Elymus nutans} and \emph{Poa pratensis} ),
Compositae (\emph{Saussurea hieracioides} , \emph{Aster
diplostephioides} , and \emph{Anaphalis lacteal} ), Ranunculaceae
(\emph{Saussurea hieracioides} , \emph{Anaphalis lacteal} ,
\emph{Anemone rivularis} , \emph{Anemone trullifolia} , and
\emph{Anemone obtusiloba} ), and other associated plants are widely
distributed among them, in addition to scattered \emph{Potentilla
fruticosa} shrubs (Yang et al. 2019). The entire study area has
undulating mountains, with steep and changeable, complex, and fragmented
terrain.

\textbf{Research object}

Marmots are hibernation animals. When the temperature is consistently
\textless{}10 degC, they will hibernate naturally for 3\selectlanguage{english}-6 months and will
then wake up naturally when the temperature warms. Marmots are family
den social animals. Dens are generally classified as hibernation dens,
summer-living dens, and temporary dens according to their functions.
Each family has a den group. The den group is centered on a hibernation
den and is surrounded by several summer lived dens and temporary dens.

The natural enemies of marmots in this study area are mainly stray dogs
(\emph{Canis lupus familiaris} ), Tibetan foxes (\emph{Vulpes ferrilata}
), and large raptors (\emph{Bubo bubo} and \emph{Buteo hemilasius} ).
Marmots are very cautious and often look up to observe the surrounding
environment during foraging. Their area of activity is typically
concentrated within 2\selectlanguage{english}-100 m of their den entrance (Yang and Xie 1983).
When they are disturbed by humans or other predators, they will sound an
alarm, and the surrounding individuals will immediately enter the den
after hearing the alarm (Shi 2007; S.L. Wang, personal observation,
2019). Marmots in this region begin to hibernate during mid-October and
are almost all hibernating by the end of October; they end their
hibernation at the end of March or in early April (Shi 2007). During the
entire warm season, except for periods with severe weather (e.g., heavy
rain and/or hail), they are active outside their dens. Generally, they
leave their dens at sunrise and return at sunset.

\textbf{Den location and field measurement}

The entrance of a marmot den is oval in shape, with excavated
soil/gravel piled up near the entrance (Fig. 1), which results in a
truncated cone-shaped pile that is obviously different from the
surrounding grassland (Appendix Fig. A1). In addition, marmots often
traverse a fixed route around the den entrance, trampling on the grass
and forming a path that is easy identified (Appendix Fig. A2). Tibetan
foxes occasionally are seen in the study area, and they may use dens
that have been abandoned by marmots. However, it is easy to distinguish
between the den entrance of a fox and a marmot (Appendix Fig. A1).

Marmot dens were investigated during the summer (July to September) of
2019 by searching the study area from unmanned aerial vehicles (UAVs)
flying 40\selectlanguage{english}-50 m above the ground at speeds of 30\selectlanguage{english}-50 km/h. Dens located
during aerial surveys were ground checked to verify their identity based
on the presence of a large amount of marmot scat (Appendix Fig. A3),
footprints, trails, and the presence of an adult or cubs (Garrott et al.
1983).

During the entire study period, we investigated 32 sites and 131 dens
(51 on sunny slopes (facing south or west), 45 on shady slopes (facing
north or east), and 35 in flat areas). We did not carefully distinguish
between temporary dens, summer lived dens, and hibernation dens. We
measured the following indicators of these dens and the surrounding
environment.

(1) Den density: We calculated the den density for each terrain based on
the area of the surveyed sites as scanned by UAVs (Qin et al. 2019) and
the number of dens recorded.

(2) Den entrance size: As the den entrance of\emph{M. himalayana} is
oval in shape, it thus has two parameters, the long axis (\emph{a} ) and
the short axis (\emph{b} ). The entrance area (S) was calculated using
the following formula:

\(\mathrm{S}\mathrm{\ }\mathrm{=}\mathrm{\ }\mathrm{\pi}\mathrm{\ }\mathrm{\times}\mathrm{\ }\frac{a}{2}\mathrm{\ }\mathrm{\times}\mathrm{\ }\frac{b}{2}\)(1)

(3) First tunnel length: We used a measuring tape to measure the length
from the entrance to the first corner of the tunnel.

(4) Den volume: We used the equal volume method to measure the tunnel
volume based on the pile of dirt beside each den. The volume of the
truncated cone-shaped pile is approximately equal to the tunnel volume:

\(\mathrm{V}\mathrm{\ }\mathrm{\approx}\mathrm{\ }\frac{\mathrm{1}}{\mathrm{3}}\mathrm{\ }\mathrm{\times}\mathrm{\ }\mathrm{H}\mathrm{\ }\mathrm{\times}\mathrm{\ }\mathrm{\pi}\mathrm{\ }\mathrm{\times}\mathrm{\ }\left(\mathrm{R}^{\mathrm{2}}\mathrm{\ }\mathrm{+}\mathrm{\ }\mathrm{R}\mathrm{\ }\mathrm{\times}\mathrm{\ }\mathrm{r}\mathrm{\ }\mathrm{+}\mathrm{\ }\mathrm{r}^{\mathrm{2}}\right)\)(2)

Where V is the tunnel volume; H is the height of the mound; and R and r
represent the upper and lower radius of the mound, respectively.

(5) Den orientation and angle of den entrance: We used a rangefinder
(Aicevoos Z5, China) to measure the orientation and angle of the
entrance. Here we divided the den orientation into eight directions: N
(0deg, at the top (12 o'clock) position), NE (1deg\selectlanguage{english}-89deg), E (90deg), SE
(91deg\selectlanguage{english}-179deg), S (180deg), SW (181deg\selectlanguage{english}-269deg), W (270deg), and NW (271deg\selectlanguage{english}-360deg).

(6) Path density near the den entrance: We determined the path density
according to the trampling situation of the vegetation around the den
entrance.

(7) Vegetation characteristics near the den entrance: For each den, to
avoid any influence of the mound, we selected a quadrat (0.5 m x 0.5 m)
in the opposite direction of the mound and 30 cm away from the den
entrance (referred to as the near entrance quadrat). At the same time,
we analyzed a control quadrat (CK) at a distance of 30 m (referred to as
activity area) away from the den entrance. Individual plant species
(referring to species richness) and the height of each species
(referring to an average height per species) were recorded in each
quadrat, and aboveground vegetation was collected and dried to a
constant weight at 65 degC.

\textbf{Statistical analyses}

Data were analyzed using Statistical Package for the Social Sciences
(SPSS) (version 26.0; SPSS, Inc., Chicago, IL, USA). Data were checked
for normal distribution using the Shapiro-Wilk test. Data for marmot den
characteristics that were not indicated as being normally distributed
were log\textsubscript{10}-transformed to pursue normality and
homogeneity of variances. We set terrains as fixed effects and
replicates as a random effect. Factorial ANOVA (One-way ANOVA) analysis
of variance with a least significant difference (LSD) test for multiple
comparisons was used to compare various indicators of marmot den
characteristics among different terrains. Figures were constructed using
Origin 9.1.

Principal component analysis (PCA) was performed to study the
relationship between the environmental variables (terrain and plant
traits) and the den characteristics. PCA was performed using CANOCO
version 5.0 (\selectlanguage{polish}Š\selectlanguage{english}milauer and Lep\selectlanguage{polish}š \selectlanguage{english}2014).

\textbf{RESULTS}

\textbf{Den density}

According to the area searched by UAVs, the den density on shady slopes,
on sunny slopes, and in flat areas was 0.83, 0.97, and 0.60/ha,
respectively. The den density on sunny slopes was significantly higher
than that on shady slopes and in flat areas (F\textsubscript{2, 128} =
3.47, \emph{P} \textless{} 0.05) (Fig. 2), which means that marmots
prefer to dig burrows on sunny slopes.

\textbf{Den entrance size}

The long axis (28.59 \selectlanguage{ngerman}± 4.32 cm) of the oval-shaped entrances was
significantly longer than the short axis (22.95 ± 3.57 cm)
(F\textsubscript{1, 129} = 3.24, \emph{P} \textless{} 0.05). The average
length of the long axis among entrances in flat areas (31.00 ± 4.27 cm)
was significantly longer than that on sloped terrain (27.21 ± 3.71 cm)
(F\textsubscript{1, 129} = 3.37, \emph{P} \textless{} 0.05). There was
no significant difference in the length of the short axis of the
entrance among different terrains (F\textsubscript{2, 128} =
4.32,\emph{P} = 0.082). In addition, there was no significant difference
in the entrance area among the shady slopes (0.19 ± 0.03
m\textsuperscript{2}), the sunny slopes (0.19 ± 0.04
m\textsuperscript{2}), and the flat areas (0.22 ± 0.06
m\textsuperscript{2}) (F\textsubscript{2, 128} = 2.34, \emph{P} = 0.073)
(Fig. 3).

\textbf{First tunnel length}

Across all dens, the average length of the first tunnel was 248.64 ±
23.67 cm. The first tunnel length of the dens on the shady slopes and
sunny slopes and in flat areas was 257.50 ± 101.33, 226.67 ± 93.93, and
256.25 ± 76.15 cm, respectively, and the differences among them were
significant (F\textsubscript{2, 128} = 4.37, \emph{P}\textless{} 0.05)
(Fig. 4).

\textbf{Tunnel volume}

Tunnel volume was not significantly different among dens on shady slopes
(0.26 ± 0.08) and sunny slopes (0.32 ± 0.15) and in flat areas (0.29 ±
0.17) (F\textsubscript{2, 128} = 3.25, \emph{P} = 0.077) (Fig. 5).

\textbf{Den orientation}

Among the 45 dens on shady slopes, 37.50\% had an east-facing exposure,
25.00\% had a northeast-facing aspect, and 37.50\% were oriented to the
southeast. Among the 51 dens on sunny slopes, 20.00\% had south-facing
exposures, 30.00\% had a southwest-facing aspect, and 50\% were oriented
to the west. Among the 35 dens in flat areas, 37.50\% had east-facing
exposures, 25.00\% had a south-facing aspect, and 37.50\% were oriented
to the southwest (Fig. 6).

\textbf{Angle of den entrance}

Based on our on-site measurements, we found that the angle of the den
entrance on shady slopes was 32.87 ± 3.98°, which was significantly
lower than that on sunny slopes (38.67 ± 4.23°) and in flat areas (38.13
± 3.92°) (F\textsubscript{2, 128} = 1.39, \emph{P} \textless{} 0.05).
However, the angle of the den entrance was not significantly different
between those on sunny slopes and in flat areas (F\textsubscript{1, 129}
= 2.37,\emph{P} = 0.083) (Fig. 7).

\textbf{Path density around the den entrance}

Path density around the den entrance reflects the activity intensity
of\emph{M. himalayana} . There was an average of 2.68 ± 0.82 paths per
den. The path density for dens on shady slopes and sunny slopes and in
flat areas was 2.75 ± 0.97, 2.33 ± 0.75, and 2.88 ± 0.59, respectively;
there were no significant differences in path densities
(F\textsubscript{2, 128} = 3.28, \emph{P} = 0.065) (Fig. 8).

\textbf{Plant characteristics near the den entrance and active area}

Species richness near the den entrance (16.76 ± 3.59 species) was
significantly lower than that in the active area (31.92 ± 3.43 species)
across all dens (F\textsubscript{1, 129} = 2.73, \emph{P} \textless{}
0.05). Species richness in active areas near dens in flat areas was
significantly higher than that on sloping terrain (F\textsubscript{1,
129} = 0.85, \emph{P} \textless{} 0.05). There was no significant
difference in species richness near the entrance of the dens among the
three terrains (F\textsubscript{2, 128} = 4.41, \emph{P} = 0.061) (Fig.
9).

Species height in the quadrat near the den entrance (20.28 ± 4.19 cm)
was significantly lower than that in the active area quadrat (28.30 ±
3.52 cm) (F\textsubscript{1, 129} = 2.92, \emph{P} \textless{} 0.05).
Species height near the entrance on shady slopes (26.96 ± 4.67 cm) was
significantly higher than that near the entrance on sunny slopes (11.00
± 2.12 cm) and in flat areas (19.71 ± 3.74 cm) (F\textsubscript{2, 129}=
3.83, \emph{P} \textless{} 0.05) (Fig. 9).

Across all dens, aboveground biomass in the activity area (222.72 ±
39.51 g) was significantly higher than that near the den entrance
(150.77 ± 30.62 g) (F\textsubscript{1, 129} = 2.78, \emph{P} \textless{}
0.05). The aboveground biomass near the den entrance on sunny slopes
(113.03 ± 24.17 g) was significantly lower than that on shady slopes
(162.81 ± 17.96 g) and in flat areas (166.91 ± 16.70 g)
(F\textsubscript{2, 129} = 3.23, \emph{P} \textless{} 0.05) (Fig. 9).

\textbf{Relationship between environmental factors and den
characteristics}

In a PCA of these data, principal component (PC) 1 and PC 2 explained
89.11\% of the total variation in the environmental characteristics
(axis 1 = 76.73\%, axis 2 = 12.38\%). Terrain had a substantial
influence on den density, orientation, and entrance size and on the
angle of the den entrance. In addition, species richness had a
substantial impact on path density and tunnel volume (Fig. 10).

\textbf{DISCUSSION}

\textbf{Den site selection by marmots}

The underground structure of marmot dens is very complex, and digging a
complete burrow requires a lot of work. Animals tend to use the smallest
investment of energy to get the greatest return (Mcfarland 1993).
Marmots decide where to dig their dens only after careful consideration,
and, therefore, environmental factors (i.e., the terrain and plant
traits) have an important influence on their site selection behavior.

We found that den density on shady and sunny slopes was higher than that
in flat areas (Fig. 2; Fig. 10). Topographic characteristics directly
affect the moisture and thickness of the soil. Dens located on slopes
may allow a more extensive system of burrows to be excavated (Garrott et
al. 1983). A den must be dry and have clean underground shelters in
which marmots can live (Shi 2007). Although flat areas are conducive to
digging burrows, alpine meadow have frequent precipitation during the
warm season and rainwater can easy flow into the den. Therefore, the den
density is lower in flat areas. The soil layer on the shady slopes in
this region is thick (\textasciitilde{}1 m) relative to that on the
other two regions (He and Li 2016) and is therefore convenient for
marmots to build their underground den systems. In areas where the soil
is shallow and the lower layer is rocky, it is difficult for marmots to
excavate burrows. A study that looked at den site preference indicated
that Arctic foxes like to dig dens on slopes with thin permafrost (30
cm) (Garrott et al. 1983). Marmots like to excavate their burrows on
sunny slopes, in addition to their need for a dry and comfortable
habitat, they also benefit from basking in the sun and staying warm,
which is vital for avoiding cold temperatures and to avoid freezing in
winter after they hibernate (Shi 2007).

\textbf{Den characteristics and functions}

The shape of the den entrance is typically determined by the
morphological structure of the inhabitant. Marmots have a flattened body
shape. This body shape is conducive to remaining close to the ground to
avoid being discovered by predators when the marmots are active outside
the den. Field measurements were used to determine that the long axis of
the oval-shape entrance to these dens was significantly longer than the
short axis (Fig. 3). These dimensions are larger than the den entrance
diameter (27 and 19 cm for the long and short axis, respectively) of the
steppe marmot (\emph{Marmota bobak} Müll.) that inhabits the Ukraine
(Nikol'Skii and Savchenko 2002). The shape and size of the den entrance
facilitate the rapid entry of the marmot while preventing predators from
entering (Rodrick and Mathews 1999). There was no significant difference
in the area of the den entrance among different terrains, which suggests
that the size of the den entrance helps to maintain a stable temperature
inside the den (Nikol'Skii and Savchenko 2002), which is an adaptive
strategy used by marmots to protect themselves and to reduce the
possible impact of the external environment (Jia et al. 1991). We also
found that dens in flat areas had a longer long axis relative to the
long axis of dens on slopes. This may be due to the wider field of
vision that marmots have access to on slopes; thus, a larger den
entrance makes it easier for a marmot hiding inside the den to observe
potential predators.

We found that the average first tunnel length was 248.64 cm (Fig. 4),
which is longer than that (127.3 cm) of dens in other parts of the QTP
(Zhang et al. 2019); this difference is most likely due to the different
geographical and climatic conditions across different regions. The first
tunnel is deep and long, which can increase the infiltration distance of
rainwater after entering the tunnel, thereby minimizing the accumulation
of water deeper within the den. This is especially important in rainy
areas (i.e., the QTP). In addition, the shortest length of the first
tunnel in this study was 100 cm, which is greater than the average body
length of \emph{M. himalayana} (55 cm) and thus ensures that they can
enter the den quickly to avoid predators (Zhang et al. 2019).

Tunnel volume reflects the internal structural traits of the marmot den.
We found that on average the den volume was 0.29 m\textsuperscript{3},
slightly larger than that (0.23 m\textsuperscript{3}) in other parts of
the QTP (Wang 1992), but there was no significant difference in the den
volume among the different terrains analyzed here (Fig. 5). The
underground den system has a complex internal structure and multiple
nests, which are places for marmots to breed, hibernate, and store food
(hay). The truncated cone-shape mound near the den entrance represents
an observatory for the resident marmot(s). They often stand on the mound
to observe the environment around the den entrance (sometimes for
\textgreater{}1 h), and they become active around the entrance only
after confirming that there is no potential danger (Yang and Xie 1983).
These mounds do, however, form a large number of naked spots on the
grassland and represent one of the main reasons for grassland
degradation in this region (Chen 1982).

Whereas the aspect of a den may confer certain advantages, the direction
of the den opening may be related to site-specific conditions such as
vegetation, drainage, or climate (Rodrick and Mathews 1999). Among the
131 dens surveyed in this study, there were no dens oriented toward the
north, and only a few (9.09\%) dens located on shady slopes displayed a
northeast aspect (Fig. 6). Danilov (1961) suggested that dens oriented
southward have a more favorable microclimate because of the protection
from the prevailing northeasterly winds. For example, den orientation
for the red fox on Assateague Island, Maryland, is often associated with
local prevailing wind directions (Krim et al. 1990). Chesemore (1969)
found that most entrances of arctic fox dens had a southerly, easterly,
or westerly orientation, possibly indicating a preference for a warmer
exposure. We did not, however, assess any microclimatic variables of the
dens in this study.

The angle between the tunnel and the ground has an important influence
on the structural stability of the den. We found that on average the
angle of the den entrance was 36 ± 4.82° (Fig. 7), which is smaller than
that of a previous study (45°) (Zhang et al. 2019). A smaller angle of
the den entrance results in structural instability, and makes it easy
for the den to collapse, especially in pastures, where this hidden
danger leads to leg fractures among large livestock. In contrast, a
larger angle makes it difficult to dig the burrow and the excavated soil
can easily backfill the tunnel; in addition, rainwater easily collects
in the den. Thus, the moderate angle noted here is the result of a
trade-off between structural stability and better drainage (Wang and
Wang 2006).

Marmots are timid by nature. When they are active outside their dens,
they walk along a fixed route, trampling the grass and forming a path.
The number of paths reflects the activity intensity of a marmot near its
den entrance. We found that these paths are arranged radially around the
entrance, with an average of 2.68 ± 0.82 paths near each entrance (Fig.
8). Marmots are one of the main spreaders of bubonic plague in this
region (Xu et al. 2020), and thus one method to control the spread of
this disease is the use of annular mousetraps to trap and kill marmots.
If mousetraps are laid out on the path near the den entrance, the
capture rate can be increased (Zhou et al. 2019).

\textbf{Plant characteristics near the den entrance}

Vegetation characteristics (richness, height, and biomass) have an
important influence on the den-selecting behavior of marmots (Li et al.
2017). We found that species richness in marmot activity areas was
significantly higher than that near the den entrance (Fig. 9). The
active area for these marmots was mainly concentrated within 2\selectlanguage{english}-100 m
near the den entrance. Plants in the active area provide food and water
for the marmots, as well as bedding for their nests in winter. Marmots
like to feed on succulent and highly nutritious forage and can get
enough water from their forage without additional water. Generally,
marmots like to excavate burrows on sloped terrain, but we found that
there were also some dens in flat areas (0.60/ha), and the species
richness in those areas was significantly higher than that on sloped
terrain. High species richness may be the reason why marmots are
attracted to these places to dig dens (Shi 2007).

Plant height also has a significant influence on the activities of
marmots (Li et al. 2017). We found that plant height within the activity
area was significantly higher than that near the den entrance (Fig. 9).
The low plants near the den entrance allow marmots to hide in their
tunnels while observing the outside environment (Shi 2007), thus
ensuring that there is no danger before they leave their dens. In
addition, marmots often stand and observe their surroundings when
feeding, and the exposed den entrance serves as a marker, which helps
them return to their den quickly when danger is detected (Zhang et al.
2019).

Because marmots are active only near the entrance to their dens, the
availability of food in those areas directly affects their den-selecting
behavior and quality of life. We found that the aboveground biomass in
the active area was significantly higher than that near the den entrance
(Fig. 9). Abundant food sources ensure that marmots can reserve enough
energy before hibernation to prepare for the 6-month hibernation period
(October to April).

\textbf{CONCLUSIONS}

Den characteristics of \emph{M. himalayana} are the result of adaptation
to the harsh environment of the QTP. Their physical parameters indicate
that dens function in the avoidance of natural enemies and bad weather,
in providing good drainage, and in maintaining a stabile microclimate.
In addition, this study also provides a theoretical basis for the
mechanism by which \emph{M. himalayana} adapted to its environment.

\textbf{ACKNOWLEDGMENTS}

The authors wish to thank Gericaidan (head of Maqu research station) for
field assistance.

\textbf{CONFLICT OF INTEREST}

None.

\textbf{AUTHOR CONTRIBUTIONS}

Shulin Wang collected and analyzed the data and wrote the paper. Fujiang
Hou designed the research and assisted with paper revision.

\textbf{DATA ACCESSIBILITY}

Data are available through the Figshare
(\emph{https://doi.org/10.6084/m9.figshare.13365329} )

\textbf{ORCID}

Shu-lin Wang https://orcid.org/0000\selectlanguage{english}-0003\selectlanguage{english}-0776\selectlanguage{english}-8912

Fu-jiang Hou https://orcid.org/0000-0002-5368-7147

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