4 ǀ DISCUSSION
We
found that as a residential species
that have to share the same space with human, pairs of Himalayan marmots
in Zoige wetland tended to dig more burrows relative to pairs in natural
habitat, resulting in shorter inter burrow distances if they are
suffered persistent but nonfatal disturbance from human activities
(Bryant, 1996; Griffin et al., 2007) due to their high phenotypic
plasticity (Huang et al., 1986;
Poudel et al., 2015a; Poudel et al., 2015b). Besides, most breeding
pairs in the region generally prefer to construct their
reproductive burrows on mounds.
Specifically, relative to pairs in HDH selectively dig their
reproductive burrows on mounds whether the mound volume or the distance
to road, pairs in the LDH did not show the same preference and on
average dug their burrows farther away from roads.
Different
from the fatal threatens like poaching and habitat loss that will
directly kill affected animals (Tilson et al., 2004; Rija et al., 2020),
residents in our study site never kill marmots due to their religious
faith, but their daily activities are a persistent disturbance for the
animals, and the level of disturbance differs between the habitats due
to different road locations and the
number of motorvehicles passing
through. Stray dogs are a deadly threat to marmots
(Poudel et al., 2015a), but although
they are more abundant in the HDH and LDH,
several
garbage dumps in the area are capable of supplying enough food for them
(Figure 1B), dogs around the village do not go out of their way to hunt
marmots within their range (Altmann
& Muruth, 1988). No stray dog
predation on marmots was observed during our fieldwork, the main human
influence on the marmot populations comes from motorvehicles that pass
through the habitat. Seasonal
fluctuation in the intensity of automobiles and dogs in the natural
habitat occurs due to residents driving by with their dogs during the
annual seasonal rotation of pasture, while daily trips between the
village and pastures are done by motorcycles (Table 1).
All
marmot breeding pairs dig a reproductive burrow for regular use to rest,
reproduce and hibernate, but they also dig temporary burrows, which are
occupied less frequently, throughout the home range as a refuge when
threatened (Blumstein et al., 2001;
Zhang et al., 2019). All breeding pairs around the village dig multiple
burrows for shelter, nevertheless, pairs in HDH dug more pair-specific
burrows (19.76 ± 1.4) than pairs in the LDH (13.4±0.96) and NH
(10.8±0.73), probably due to they suffer the heaviest disturbance
(Figure 2). Though nonsignificant, pairs in LDH generally dig two more
burrows than NH pairs, more
available refuges guarantee individuals have more chances of escape, and
consequently, provide a survival advantage when threatened (Blumstein et
al., 2001). Furthermore, shorter
inter all burrow distances resulting from more burrows in the habitats
enable marmots in two disturbed habitats to reach a potential refuge
more quickly when threatened, increasing the likelihood of survival (Li
et al., 2011; Zaman et al., 2019).
Based on observations recorded from
2017 to 2020, no new temporary burrows were dug. It is possible that
more burrows were dug in the HDH during the initial human settlement of
the area, but marmots that had
grown accustomed to humans’ daily activities no longer saw a benefit to
digging new burrows (Mainini et
al., 1992; Schell et al., 2018), which is energetically expensive.
Similarly, though only two more temporary burrows were dug, inter all
burrow distance in LDH is far shorter than in NH, allowing the same
reduction in distance and time required to reach a safe place for
individuals in the habitat as their congeners in HDH. The different
(number of burrows per pair) and same (inter burrow distance) patterns
that emerge between two disturbed habitats may arise because the
disturbances LDP individuals suffer are not intense enough to accustom
them, but drive they selectively
concentrate new burrows near
reproductive burrows like urban woodchucks (Watson, 2009), the mean home
range of LDH pairs (21.98
± 2.86 are) is far smaller than
pairs in NH (39.62 ± 2.55 are) with
there are many unoccupied regions among different pairs in LDP (Figure
S4), consequently, gain shorter inter all burrow distance to meet the
requirements of flee efficiency and spend as little energy as possible
on digging extra burrows simultaneously. Meanwhile, FID of HDP
individuals (65.36 ± 4.45 m) are shorter than NP
individuals (119.40 ± 8.11 m) as
expected, nevertheless, even have the shortest inter all burrow
distance, the FID of LDP individuals (105.00 ± 6.88 m) showed no
coincident trend as HDH, but are as long as FID of marmots in NP (Dill
& Houtman, 1989; Griffin et al., 2007). The differentiation may arise
because the optimal strategy to survival for LDP individuals is to flee
early like NP individuals when threatened however the distance to a
potential refuge (Li et al., 2011). Shorter flee distance and longer FID
guarantees the safety of unaccustomed LDP individuals under the
disturbances of human activities
(Zaman et al., 2019; Feng & Liang,
2020).
It is also worth noting that the
inter reproductive burrow distance in
HDH (118.31 ± 36.82 m) is shorter than that of the other two habitats
(Figure 4A), a pattern may arise because the regions surrounding the HDH
are uninhabitable due to improper soil and vegetation characteristics
(Guo et al., 2020; Figure S1), HDP is actually an isolated population
cannot freely communicate with other populations. The same as a
reintroduced Alpine marmot population in Dolomiti Bellunesi National
Park, Italy (Borgo et al., 2009), the HDH has been fully exploited by
the growing breeding pairs since the village began to settle in the
region. 72 pairs per km2 may be the maximum
environmental carrying capacity for the species in such a ecosystem.
In
contrast, no similar variation emerged between LDP and NP, may because
LDH is an open area conducive to free dispersal as the NH (Figure S2 to
S5). This might explain why the inter burrow distance for reproductive
burrows in the LDH was no different than that observed in the NH.
LDH is an open space, marmots in
the region have the freedom to actively avoid human influences in
emigration, a strategy that is superior to the passive adaptation to
human influence. The average inter reproductive burrow distances
observed in LDH (143.73 ± 48.25 m) and NH (145.57 ± 38.66 m) may reflect
more typical distancing between marmot pairs: reducing resource
competition while maintaining regular contact between pairs.
Together
with the diversification on FID and two inter burrow distances, we
concluded that compared with HDP,
the reactions of LDP individuals may be the normal outcomes (dig more
extra and concentrated temporary burrows and flee earlier to avoid
potential dangers but also appropriate inter “family” distance) when
Himalayan marmot affected by persistent, but nonfatal disturbances from
humans.
The
characteristics of reproductive den site selection also differed among
the habitats. Most NH pairs constructed their
reproductive burrows on mounds, and
pairs in HDH also selectively dig their reproductive burrows on mounds
(Figure 5A), even when those mounds were relatively close to a road and
smaller than the mounds used by pairs in NH
(Figure 5B, 5C). Marmots use their
reproductive burrows giving birth to their offspring, and spending a lot
of time resting/basking at the entrance to the burrow. This special
preference to mound may because pairs build their reproductive burrows
on mounds ensure better drainage relative to burrows dug on flat ground
(Szor et al., 2008). Besides, similar to alpine marmots preferentially
remaining near large stones that they climb to engage in
surveillance to watch for predators
more effectively (Borgo, 2003),
Himalayan marmots in alpine meadow
with less mound also selectively use site with many big stone to gain
better vigilance and bask efficiency (Figure S6). However, in our site
in Zoige wetland, due to the lack of large stone, rest or
vigilance on mound higher than flat
ground may also able to gain a better vision of the surrounding areas,
improving their chances of detecting
predators.
Most animals choose to locate reproductive dens at sites where they can
conceal themselves to better protect themselves and their offspring
(Ross et al., 2010; May et al.,
2012; Sazatornil et al., 2016; Lai et al., 2020). Consequently, we
predicted that pairs of Himalayan marmot would stay as far from the
roads as possible, but breeding pairs in HDH still preferentially built
their reproductive burrows on the mounds near roads despite the
increased frequency of disturbance from the motorvehicles, which can be
harmful (Whittington et al., 2019). This surprising result suggests that
the availability of mounds is the primary determinants of site selection
for reproductive burrows in Himalayan marmots.
In Zoige wetland, mounds on the dry
flat ground could be the limiting resource (Guo et al., 2020), as
marmots always built burrows in the mounds that were present regardless
of their size or distance from the road. For example, one occupied mound
(HDH11) in HDH was only 2.2 meters from a road (Figure S3), and the
average size of the occupied mounds in the HDH is smaller (2.14 ± 2.65
m3) than the occupied mounds in the NH (6.23
± 5.13m3)
(Figures 6A, 6B), indicating that marmots will use all the mounds they
can find in an area, even smaller ones. There were no unoccupied mounds
left in the HDH, and some breeding pairs that could not find a natural
mound will built their own very small mounds around the entrance of
their burrows (Figures 6C, 6D). There are no natural hiding places for
marmots in the Zoige wetland (Zhang, 2019), and unlike predators,
disturbances from daily human activities are nonfatal, consequently,
sites that allowed for vigilance
while resting were the only suitable choices for reproductive burrows,
even if they were frequently disturbed by motorvehicles. Den site
selection of American black bears (Ursus americanus ) and American
badger (Taxidea taxus ), and the habitat utilization of Barbary
macaques (Macaca sylvanus ) were also found to be unaffected by
the distance to roads (Waller et al., 2013; Sunga et al., 2017; Waterman
et al., 2019), suggesting that many species will tolerate persistent but
non-life-threatening human disturbance to retain access to otherwise
favorable habitat. The importance to the marmots of the vigilance and
good drainage of mound-built burrows (Szor et al., 2008) outweighed
disadvantages to digging reproductive burrows close to a road.
Furthermore, dig their reproductive burrows near road may also arise
because relative to other species sensitive to human disturbance (i.e.
snowy plover Charadrius nivosus and Yunnan lake newt) (Webber et
al., 2013; Amphibiaweb, 2021), marmots species are more able to endure
nonfatal human disturbances (Neuhaus & Mainini, 1998; Griffin et al.,
2007). Himalayan marmots disturbed in HDH for generations are highly
accustomed to human activities are no longer selective pressures on the
den site selection of the marmots in the habitat (Schell et al., 2018).
Site selection for reproductive burrows in the LDH showed a different
profile relative to the other two populations, with burrows almost
equally likely to be located on mounds or on flat ground. Moreover, the
average volume of the mounds selected for reproductive burrows in the
LDH is significantly larger (75.47 ± 78.69 m3) than
the mounds in HDH and NH. This discrepancy might result from the
radically different topography of the area. Aside from having many large
mounds, the LDH is sloped, with some areas of the flat ground allowing
for surveillance equal to the tops of mounds in the other two habitats
(Figures 6E, 6F). Consequently, pairs in LDH are no longer limited by
the availability of mounds. This is consistent with the greater average
distances from reproductive burrows to the road in the LDH (98.06 ±
48.06 m) as opposed to the HDH
(28.88
± 12.29 m). Unlike the marmots of
HDP, who are forced to prioritize vigilance and drainage, marmots in LDH
have greater flexibility in sites where they can build reproductive
burrows and so tend to avoid the roads.
Unlike reproductive burrows,
temporary burrows were common on flat ground in all three habitats
because they were used only to evade immediate threats. Good vision and
drainage are not important for temporary burrows (Borgo, 2003; Szor et
al., 2008). Consequently, Himalayan marmots dig temporary burrows in any
location as needed and reserve their reproductive burrows for mounds
when possible. This demonstrates the use of
multiple habitat utilization
strategies at once to cope with human disturbance and natural dangers.
Generally, relative to animals
sensitive to human activities like Yunnan lake newt or some certain
populations suffer extensive human disturbance like Asiatic lions,
Himalayan marmot have a high plasticity, variation in habitat
utilization in response to the varied intensity of nonfatal human
disturbance of the species emerged,
and heavier suffered population even gain a higher population density
(Guo Cheng personal observation). Furthermore, it is also possible that
other aspects of this species’ ecology, such as if the feeding range
size of LDP individuals shows the same trend with their home ranges and
if their time budget, body condition, may also change in response to
human activity to improve survival, as has been observed in other
animals require further study (Wright et al., 2009; Poudel et al.,
2015b;
Santini
et al., 2019; Yang et al., 2019).