4 DISCUSSION
By monitoring a total of 44 sample lines, we found that the
scent-marking behavior of giant pandas is indeed consistent with signal
detection theory (Alberts, 1992), and that giant pandas do select and
modify their marking sites to maximize their signaling function at both
micro- and macro-habitat scales. Giant pandas are an energetically
marginal species, their diet is bamboo and their nutritional phase is
low, which affects aspects of movement, communication and reproduction
(Hu et al., 1985; Nie et al., 2012b; Nie et al., 2015). The selection of
marking sites will minimize energy expenditure while increasing the
effectiveness of inter-individual communication.
Our findings show that pandas prefer to scent mark on ridges with animal
trails, and we know by the density of faeces on the sample line that
this is indeed the area with the highest intensity of use by pandas as
well (Table S1). The presence of many animal trails on the ridges also
makes them important paths for the movement of giant pandas (Bai et al.,
2020). However, we likewise noted that slopes without animal trails as
well as ridges had high fecal densities, demonstrating that pandas spend
a significant amount of time in these areas, yet the preference index
for these areas was significantly lower than the corresponding terrain
with animal trails. From this we learn that pandas choose these
locations for scent marking not because they happen to be there, but
because they really need to choose such terrain to maximize signal
propagation efficiency.
The tree species most frequently scent-tagged by giant pandas were
Badung oak (Quercus engleriana ), Yaupon pine (Pinus
tabulaeformis ), and Huashan pine (Pinus armandii ), which are
dominant species with a wide local distribution (Ming et al., 1999). We
speculate that they choose dominant species for marking because they
take less time and energy to be found. In addition to their wide
distribution, their high marking frequency may also be due to the fact
that marked trees are well located for signal transmission and over time
become scent stations (Hu et al., 1985), and they are often located
along animal trails on mountain ridges (Nie et al., 2012a). Marking on
these scent stations commonly used by giant pandas would also increase
the likelihood of their information being detected by signal receivers.
Zhou et al. (2019) have demonstrated that both volatile and non-volatile
compounds in AGS marks were not significantly degraded within two weeks,
suggesting that pandas visit and update marks frequently (Zhou et al.,
2019). Thus depositing marks in better located scent stations would also
reduce the energetic cost of returning and updating markers. Future work
could increase research on scent stations and explore their
microhabitats and conditions such as light that may affect marker
persistence and dispersal to increase conservation of habitats where
potential scent stations exist.
The roughness and SDT of the marked tree of giant pandas differed
significantly from the control tree, similar to the results of previous
study (Nie et al., 2012a), where giant pandas generally do not scent
mark on smooth trunks, which would reduce the persistence of marking;
and the SDT of the marked tree was significantly shorter than that of
the control tree because the closer the distance to the animal trail,
the more likely it is to be detected by the signal recipient, and
because when marking here, giant pandas can travel shorter distances and
save energy.
For both marked and control samples, bamboo density, bamboo cover and
slope were lower and tree density and cover were higher in the marked
sample. Higher bamboo density and cover make it more difficult for giant
pandas to walk among bamboo forests, while relatively low bamboo density
will allow giant pandas to obtain sufficient nutrition while reducing
energy expenditure to traverse bamboo forests (Wei et al., 2015). As for
the lower slope of the marked samples, the reason is that the gentle
slope is a suitable habitat preferred by pandas (Hu et al., 1985), and
the lower slope ensures that pandas complete scent marking in a
relatively stable position (Hou et al., 2021), and walking in a gentle
slope reduces energy expenditure. The higher tree density and tree cover
in the marked sample is mainly due to the fact that the more trees there
are, the greater the chance of trees with larger DBH appearing around
them, and trees with larger DBH are more likely to form tree dens for
giant pandas to breed and nurse their cubs (Wei et al., 2018; Zhang et
al., 2011). In addition, the higher the density of arborvitae, the more
concealed the habitat is, and thus the less likely to be detected by
natural predators (Hu et al., 1985).
We found that the number of marked trees that were reused was much
higher than those that were used only once, but did not detect
significant differences between the variables of either. We hypothesize
that the location of the repeated marked trees may be more prominent and
have a wider field of view, where pandas often pass by, which may also
increase the chance of other similar species finding the signal. The
most used mark type in giant pandas is the AGS marks, which often remain
in the natural environment for more than 3 months because of their low
volatility (Hagey & Macdonald, 2003; Swaisgood et al., 2004), in order
to better convey individual information. In contrast, urine markers
contain more volatile substances than AGS marks and have a shorter
retention time in the environment, and are often used to convey the
estrus status of individuals (Zhou et al., 2019) and the competitive
ability of males (White et al., 2002), among others.
The appearance of scratch mark is always accompanied by AGS mark, so we
believe that scratch mark itself does not convey information, but is a
by-product left behind when AGS marking is performed. An interesting
finding is that some marked trees have only bite mark and are more
numerous than those with only urinary mark, which was not found in
previous studies, and we predict that its role is also correlated with
mark height, and if the mark is higher, it indicates that the individual
is larger and more competitive, similar to AGS mark and urinary mark
(White et al., 2002), but specific role needs to be further
investigated. McGuire et al. found that body size affects the frequency
of marking in a study of domestic dogs (Canis lupus familiaris )
(Mcguire & Bemis, 2017). However, in the study of giant pandas, we only
know that body size reflects their competitive ability (Nie et al.,
2012b), but whether it affects the frequency of marking deserves further
investigation.
Statistics on mark orientation revealed that the most marks were toward
the animal path, which is because facing the animal trail also increases
the chance of the mark being detected by its own species; for those
marks that were backward toward the trail, we predicted possible scent
counter-marking behavior, which is one of the main responses taken by
animals when they encounter the scent of other competitors of the same
species (Johnson, 1973). But before counter-marking they evaluate
individuals that are already marked, probably because they are not as
competitive as the former and want to mark in a superior position on the
marker tree, so they mark on the back (Müller & Manser, 2008). However,
the exact reason needs to be confirmed by a large number of future
studies.
Footpad scent communication has been found in fellow bear species brown
bear (Ursus arctos ) (Sergiel et al., 2017) and polar bear
(Ursus maritimus ) (Owen et al., 2015), and most bear species have
large home ranges and are non-dominant, and releasing scent while
walking is a very effective form of intraspecific communication. An
interesting question is whether giant pandas use footpad scent similarly
for communication? We monitored some sites in this study where giant
panda tracks were pitted (Figure S4). Unfortunately, we did not find
other pandas observing and sniffing the tracks in our follow-up
observations. This may be due to our small sample size or the fact that
we did not specifically focus on this direction, and we hope to continue
this study in the future to confirm our suspicions.
It has been shown that the frequency of marking in giant pandas (Nie et
al., 2012a) and the compound content of AGS marks (Zhou et al., 2019)
differ significantly between the sexes. Zhou et al. detected large
differences in the composition and content of compounds in AGS marks
between captive and wild giant pandas (Zhou et al., 2019), which may
also be one of the reasons for the low reproductive ability of captive
giant pandas, and future research on scent marks of giant pandas in the
field environment should be strengthened to clarify which compounds
affect the estrus and reproduction of giant pandas, and applied to
captive giant pandas to improve their reproductive success. This is a
tremendous step forward for the survival and reproduction of the panda
populations.
However, current research on chemical communication has still not kept
up with acoustic communication (Wiley, 2006). Due to the construction of
Giant Panda National Park, some human facilities will inevitably be
built in the living environment of giant pandas in the future. It has
been shown that human facilities can affect the scent marking behaviors
of domesticated felines (Krofel et al., 2017), and scent marking of
pandas should be continuously studied to detect whether the marking
behaviors of pandas will be changed due to the influence of human
facilities, so that more precise conservation of panda habitats can be
carried out. For example, assessing the impact range size of human
facilities prior to their construction and then locating them as far
away from core giant panda habitat as possible.