Discussion
Contrastingly to the common paradigm that the role of ecosystem
engineers is most pronounced in harsh abiotic conditions (Crain and
Bertness 2006), our results generally show alimited impact of
long-tailed marmots on N and P content in plant biomass and no impact on
vegetation cover in an extremely arid, cold ecosystem.
A decrease in vegetation cover due to burrowing animal activity is
mostly caused by the presence of mounds close to the burrow entrance,
which have not been colonised by plants. (Dotter, 2009; Louw et al.,
2019). Our results showed no possibility of plant regrowth on mounds in
the present conditions in the studied area. Therefore, we excluded
mounds from the analysis of vegetation cover and tried to answer the
question, of whether marmots modify plant recruitment on actually
inhabitable soil. We found high variability in the parameters we
measured using aerial images, which is the reason why we decided to
perform the analysis on a small scale and numerous repetitions,
analysing each 20 m buffer around a burrow separately. Based on our
results, the response of vegetation cover to the proximity of burrows
could be positive, negative, binomial (with higher cover at highest and
lowest distances from the burrow entrance) or non-existing (Fig. 2).
This could suggest that those types occur depending on the balance
between herbivory and nutrient supplementing through excretion. However,
the relationship is probably best analysed by visual inspection of the
distribution of burrows relative to vegetation cover (Fig. 1): patches
of high cover occur along the slope of the river terrace, and probably
reflect past paths of water flow. Marmot burrows were located both on
and off these patches, and there are large areas with high vegetation
cover and no burrows. The type of relationship between the distance from
the nearest burrow and vegetation cover we found using the linear model
depends probably on the location of the burrow relative to a vegetation
patch. If it is located outside the patch, but the patch falls within
the 20 buffer, then the trend is negative. When the burrow is in the
patch, but the buffer reaches an area of bare soil, the trend is
positive (see Fig. 1D). The edges of the vegetation patches are sharp
and seem unaltered by burrow presence. The distribution of burrows is
clearly not random across the searched part of the valley (Fig 1A) and
can be an effect of selectivity towards physical soil properties, which
we cannot account for. Marmots seem to avoid alluvial fans, especially
active areas, a large part of the second river terrace and the middle
part of the third terrace. Based on this, we assumed that there is no
clear relationship between burrow presence and vegetation cover.
Given the limited effect of the additional nutrients on plants (see
below), the slow growth of plants and the fact that marmots graze almost
exclusively in the burrow area (Blumstein, 1998), it is puzzling that
vegetation cover does not seem impacted by burrow proximity. Some
burrow-dwelling mammals are known to create large patches of bare soil
due to herbivory and trampling (Davidson et al., 2012; Harris et al.,
2015; J. Zhao et al., 2021). We cannot explain this result, as we do not
know the primary production of plants, the population size of marmots
and their feeding requirements, as well as the time spent in different
burrows. The only study on the impact of long-tailed marmot (or any
other burrow-dwelling species) activity on plants conducted in a
comparable environment in Eastern Pamir, found a small impact of the
presence of marmot burrows on plant species composition, and the results
varied among study sites. Generally, dwarf shrubs occurred more often in
disturbed areas than in undisturbed areas, as opposed to herbs (Dotter,
2009), which suggest that browsing does impact the plant community, as
shrubs are more resistant to herbivory.
Our results on the relationship between the distance from the burrow and
N and P content in plant biomass are ambiguous. Only one out of six
species, E.altaicum , showed an increase in biomass N and P
content with increasing proximity of the burrow entrance. However, the
effect size in this species is enormous, with N content increasing by
80% and P content by 250% with decreasing distance from the burrow
(Fig. 4). This implies that there is a nutrient input caused by marmots,
and so do the result of analyses of soil sampled within the high cluster
(Fig. 1A). It had almost 100 times higher P (0.31 mg/kg) 10 times higher
and N (0.169%) content than from other parts of the valley (0.47 –
0.125 mg/kg and 0.01 – 0.06%, respectively), which the authors of this
study attribute to marmot activity (Kabala et al., 2021), as the sample
was collected within the high cluster, close to several burrows (Fig.
1D). This allows us to treat the mound area as a natural fertilization
experiment and interpret it as such, with necessary caution. The limited
impact of nutrient addition on vegetation cover and biomass N and P
content suggests, that plants are not limited by nutrient availability,
but probably by abiotic factors, mainly water scarcity, as they simply
lack the necessary moisture to utilize the additional nutrients (He &
Dijkstra, 2014), and the effect of nitrogen addition was proven to be
correlated with precipitation (Yahdjian et al., 2011). Burrowing animals
are known to increase water availability for plants, as their
constructions promote water infiltration and prevent water runoff and
evaporation (Laundre, 1993; Whitford & Kay, 1999). However, this
probably does not occur in our study area. Most of the precipitation is
presumably instantly lost to evaporation, irrespective of the presence
or absence of marmots. In turn, plants are adapted to these conditions
and have deep roots, up to 50 cm (Kabala et al., 2021), to utilize any
soil moisture. Even if there was an increase in water infiltration in
the surface layer of the soil, it could probably not be used by plants.
The response of E.altaicum to the marmot-derived nutrient input
implies that this species, apart from being capable to utilize the
additional N and P, is more efficient at water uptake and/or preventing
water loss than other species. However, we lack information about the
functional traits of plant species from our study, so we are not able to
confirm this hypothesis.
The results of N:P stoichiometry in the distance gradient from the
burrow entrance show a shift from P limitation at higher distances to N
limitation close to the burrow. The use of the N:P ratio to identify the
limiting nutrient, where N:P < 14 indicates N limitation, N:P
< 16 P limitation and values in between indicate co-limitation
has been prosed for wetlands (Koerselman & Meuleman, 1996) and proven
useful in grasslands (Craine & Jackson, 2010; G. Zhao et al., 2017). We
are using this tool with caution, because the high N concertation in
plants inhabiting alpine habitats, and the resulting high N:P ratios
(such as those we found in most species) are mainly caused by slow
growth and adaptations to low temperatures, not by P limitation (Körner,
2003). Those adaptations are species-specific and most probably
site-specific, therefore we are only looking at values within E.
altaicum , and they indicate, that faeces are a more important source of
P than N. Faeces have similar N content as plant biomass, whereas the P
content is almost three times higher, indicating that they are a better
source of P than plant litter. Soil P content can be also increased by
the presence of marmot bones, which we have observed on several mounds.
Up to 30% of marmots fail to survive the hibernation period (Blumstein
& Arnold, 1998), their remains are probably ejected on the surface
after hibernation or during burrow maintenance. Plants growing on
initial soils are usually not P-limited, as it is abundant from
weathering minerals, as opposed to N (Walker & Syers, 1976). However,
in high mountain continental areas, the low temperature and
precipitation can hamper weathering to the point that plans are limited
by P shortage (Darcy et al., 2018).
Increased N and P content in plant biomass close to burrows are mostly
caused by the input of organic matter by the burrowing animal, but it
can be also an indirect effect of animal activity: (1) Disturbed soil
has higher temperatures and is more susceptible to N mineralization,
increasing the amount of plant-available soil N (Whicker & Detling,
1988) (2) Defoliation (including grazing) may increase N uptake by
plants (Jaramillo & Detling, 1988; Yan & Lu, 2020). Therefore, we
decided to use stable isotope composition as a marker of animal-derived
N use by plants. Faeces of rodents are enriched in 15N
compared to diet by 1.4 – 2.5‰ (Hwang et al., 2007; Sare et al., 2005)
due to its discrimination in metabolic pathways. Given that long-tailed
marmots mainly stay close to the burrow while foraging (Blumstein,
1998), we hypothesised, that the elevated δ15N values
in faeces and the enhanced N cycling in burrow proximity would result in
higher δ15N in plants growing closer to the burrow
entrance. The lack of difference between δ15N values
of plants and faeces in most cases (Fig. 5) implies little isotopic
enrichment of the latter. Results on isotopic enrichment (trophic
discrimination) in faeces are based on feeding experiments, where food
is usually provided ad libitum. Fasting and nutritional stress,
which is frequent in the natural environment, is known to affect
δ15N values of animal tissues (Doi et al., 2017; Hertz
et al., 2015) and could also alter the metabolic pathways leading to
faeces enrichment in 15N. Previous studies found no
clear pattern of stable isotope ratios in diet and faeces of burrowing
animals. Plains vizcacha (Lagostomus maximus ) faeces had lower
δ15N values by approx. 4‰ than soils and shrubs at
burrow systems, with no interpretation by authors (Villarreal et al.,
2008). Grasses close to arctic fox (Vulpes lagopus ) dens had
similar δ15N values to grasses from control sites,
despite the significant impact of fox burrows on the available N pool in
soils (Gharajehdaghipour et al., 2016). Authors attributed the loss of
animal-derived 15N to discrimination during
mineralization and plant uptake (where high N availability could further
increase discrimination). Other studies showed an increase in
δ15N in plants at burrows, proving the fertilizing
effect of animal faeces (Ben-David et al., 1998; García et al., 2002).
However, those studies were done on burrows of predators, which have
higher δ15N values in tissues and faeces due to longer
trophic chains (Fry, 2006). In such a case, when groups involved in the
relationship are separated by several trophic steps, each with its
specific isotopic enrichment (Vander Zanden & Rasmussen, 2001), the
isotopic difference and the resulting method resolution is high enough.
A mechanism typical for the interaction between burrow-dwelling animals
and plants which does not occur under the circumstances we studied is
the role of burrow mounds. They consist of subsurface soil and are
initially bare, creating a new microhabitat for plants. They differ in
physicochemical properties from the surrounding soil, promoting pioneer
(Semenov et al., 2001; Swihart, 1991; Van Staalduinen & Werger, 2007)
and nitrophile plants (Ballová et al., 2019; La et al., 2003). Mounds on
our study sites consisted mainly of stones larger than 2 cm, which make
up most of the subsurface soil layers (Kabala et al., 2021). Fine soil
particles, as well as soil moisture ejected by marmots from deeper
layers are probably removed by wind, like it has been found in desert
environments (Sharma & Birla, 1975) long before it can be utilized by
plants. Also, there is no evidence for the presence of deep organic
matter in our study area (Kabala et al., 2021). Those are probably the
reasons for the lack of plant succession on mounds we found, similarly
to another study in Eastern Pamir (Dotter, 2009). Furthermore, marmot
activity causes a loss of inhabitable sites for plants, probably for
decades.
Researchers studying ecosystem engineering by burrowing animals have
identified the crucial role of water availability in the interaction
between those animals and plants. In arid regions, burrows and their
inhabitants have a larger impact on plant species richness (Romero et
al., 2015), soil nutrients (Decker, Eldridge, et al., 2019;
Mallen-Cooper et al., 2019), decomposition rate (Decker, Leonard, et
al., 2019) as compared to more arid environments. However, these
comparisons may be biased, as there is simply more burrowing animals and
more studies on ecosystem engineers in arid regions (Coggan et al.,
2018). Other authors refused to identify any factor which could drive
the effect size of burrow-dwelling ecosystem engineers, as it is solely
site- and species-specific (Louw et al., 2019; Root-Bernstein &
Ebensperger, 2013), and our results seem to fit this description. In
humid, productive ecosystems where plants are mainly limited by biotic
factors, such as herbivory and competition, the effect of ecosystem
engineering is small (Crain & Bertness, 2006). In arid ecosystems,
burrowing animals enhance nutrient cycling, which is hampered by water
shortage, thus locally increasing productivity (Gharajehdaghipour et
al., 2016; Yu et al., 2017). However, below a certain level of water
availability, as drought directly limits plant growth, this effect
decreases as it probably occurred in this study. Our results do not
undermine the paradigm on the relationship between abiotic factors and
the effect size of ecosystem engineers, but they lengthen the abiotic
gradient by extreme habitats which are strongly understudied.
Eastern Pamir, similarly to other mountain regions, is particularly at
risk due to climate change (Kohler et al., 2010). As temperatures are
increasing, melting glaciers will continue to reveal patches of bare
soil (Mętrak et al., 2015). But as precipitation in Eastern Pamir is
expected to decrease even further (Lioubimtseva & Henebry, 2009;
Normatov & Normatov, 2020), the succession of these areas will probably
remain extremely slow and the impact of marmots on plants minimal.
Rising temperatures may increase the rate of mineral weathering
(Gislason et al., 2009), further diminishing the role of animal-derived
nutrients for plants.
Despite the relatively small impact on plant nutritional status and
vegetation cover, long-tailed marmots inhabiting extremely dry mountain
habitats, most probably have a crucial impact on the ecosystem. Given
the burrow density, marmots are probably the most abundant animal
species in terms of biomass. This can make them an important food source
for predators inhabiting our study area: wolves (Canis lupus ) red
foxes (Vulpes vulpes ), and snow leopards (Uncia uncia ),
which are known to prey on marmots, especially the two latter species
(Blumstein & Robertson, 1995; Jumabay-Uulu et al., 2014; Khatoon et
al., 2017). Marmot burrows can provide unique refuges of stable
temperature and high humidity, crucial for the development of insects,
especially in arid environments (Pike & Mitchell, 2013; Whitford &
Kay, 1999). Marmot burrows can be used by other animals as the only
shelter from strong winds and predators. Due to the unique character of
the studied environment, the mechanisms described in this paragraph,
similarly to our results on animal-plant interactions, can happen
differently than in grasslands, steppes and mountain meadows. We think,
that a lot of questions in this area are open to further research.