Discussion
In our study, we further confirmed that sarcoptic mange is the reason
that caused the mass death events in gorals and serows in the past years
and is still being transmitted in the gorals and serows in the Qinling
Mountains based on expand surveys and sampling. Our results showed that
mites from samples of all the dead gorals and serows were S.
scabiei according to both morphological and PCR analyses of thecox 1 and ITS2 genes(Fraser et al., 2018; Pence & Ueckermann,
2002). According to previous reports, scabies can cause serious
cutaneous lesions, characterized by alopecia, marked lichenification and
thick crusting on the legs, head and trunk of blue sheep, ibex, chamois
and hare (Cardells et al., 2021; Dagleish et al., 2007; Oleaga et al.,
2019; Sarasa et al., 2011). These lesion characteristics have also been
observed in foxes and wombats with sarcoptic mange in pictures from
infrared cameras or online(Arenas et al., 2002; Borchard et al., 2012;
Scott D. M. et al., 2020); therefore, we can confirm that sarcoptic
mange has been spreading among gorals and serows since at least 2012, as
the same cutaneous lesions were recorded in photos and described by
people. In these photos, severe cutaneous lichenification on the joints
and lips obviously impacts the activity of animals, and infected animals
may have difficulty walking on hillsides(S4). This may be an important
factor, as the majority of the dead gorals and serows were found at low
altitudes and on mild slopes in our previous study(Zhu et al., 2021).
We could not accurately map the accurate path of transmission of scabies
without the GPS coordinates of all the dead gorals and serows in each
year. In the Alpine chamois population, the spatial spread of sarcoptic
mange presented an “oil spot”-like pattern, with an average annual
spread of approximately 4.64±3.12 km/year(Rossi et al., 2007; Turchetto
et al., 2014). In our study, gross observation indicated that sarcoptic
mange was spreading in the Qinling Mountains from west to east.
Moreover, the distance between mean center of dead animal’s GPS
coordinates in Ningshan in 2012 and the main place of dead animals in
Zhashui was about 70 km in 2019-2020, consistent with this spreading
speed. Additionally, these results refute our previous hypothesis that
climate change or excessive population densities caused sarcoptic mange
outbreaks in goral and serow populations throughout the Qinling
Mountains. On larger spatial and temporal scales, we noted that
sarcoptic mange in goral and serow populations in the Minshan Mountains
has persisted since 1996(Cheng et al., 2018; Yang et al., 1997). The
Micang Mountains are situated between the Qinling Mountains and Minshan
Mountains, and there are no reports of sarcoptic mange in wildlife in
the Micang Mountains. Additionally, the survey by our institute
conducted in the western Qinling Mountains in Gansu Province showed
similar patterns of goral and serow deaths, and pictures were captured
by an infrared camera(S2C). Therefore, we need additional evidences to
reveal the relationship of sarcoptic mange in wildlife located between
the Minshan Mountains and Qinling Mountains.
In all records, the dead animals were mainly found in the winter and
early spring. Sarcoptic mange in red deer and ibex showed similar
seasonal patterns, with peaks in early spring(Iacopelli F et al., 2020).
According to researches, S. scabiei mites are transmitted by
direct or indirect contact(Arlian & Morgan, 2017). Off their hosts,S. scabiei mites are able to survive for 24-36 h at 21°C and
40-80% relative humidity, allowing transmission to a new host, and
lower temperatures and higher humidity values can prolong their
survival(Heukelbach & Feldmeier, 2006; Niedringhaus,Brown, & Ternent
et al., 2019). Additionally, the average survival time of an infected
ibex is 121±71 days(Alasaad et al., 2013). Therefore, we hypothesize
that dead and weak wild animals infected with scabies are important
sources of infection for healthy animals in winter and early spring, and
subsequently, the newly infected animals maintain the transmission cycle
of sarcoptic mange. In this way, sarcoptic mange is continually spread,
and the distribution expands among gorals and serows in the Qinling
Mountains.
The pathogenic characteristics of sarcoptic mange are mainly related to
the invasion and lifecycle of the mites. Once a mite has identified a
suitable location on the skin, it rapidly penetrates into the epidermis
and burrows approximately parallel to the corneal layer at a rate of
0.5-5 mm per day; the saliva, feces and eggs produced by the mite cause
acute pruritus in the host(Hengge et al., 2006; Heukelbach & Feldmeier,
2006). Accordingly, hyperplasia of the epidermis, hyperkeratosis,
hyperplasia of the sebaceous glands and inflammatory infiltrates have
frequently been observed in the red deer, chamois, roe deer
(Capreolus capreolus ), red fox, vicuña, lynx and so on(Oleaga et
al., 2012; Oleaga et al., 2019). In our samples, most of the
pathological changes were similar; however, there was no hyperplasia of
the sebaceous glands, and only moderate inflammatory infiltrates were
observed. Whether the absence of hyperplasia of the sebaceous glands and
only a moderate inflammatory infiltrates indicates milder lesions is
unclear. The results of the gross and histopathology examinations showed
that the whole skin area of the dead animals was severely damaged. This
suggests that the skin of the animal lost the ability to maintain body
temperature. This is also an important factor in the death of infected
animals that died in winter and early spring. Additionally, breaks in
the epidermis allow the development of pathogenic bacterial
infection(Abdel-Saeed, 2020; Romani et al., 2015). In humans, crusting
is a rare manifestation of scabies, caused by the uncontrolled
proliferation of mites in the skin as a result of an insufficient immune
response by the host(Karthikeyan, 2009). However, crusting has often
been observed in wildlife in our research and in other reports. This
suggests that the dead animals experienced a long period of infection
and that the immune response failed at the end of life. Therefore,
improving animal immunity and administering anti-infection therapies are
important measures during the treatment of wild animals with severe
scabies.
Although the genus Sarcoptes has only one species, genetic
diversity among S. scabiei from different hosts and areas has
been proven(Gomez-Puerta et al., 2022; Soglia et al., 2007). The ITS2
region and cox 1 gene are widely used in the molecular diagnosis
of sarcoptic mange, and ITS2 sequencing is more suitable for
phylogenetic studies of astigmatid mites than the characterization of
different species based on geographical distribution(Alasaad et al.,
2009; Oleaga et al., 2012). However, the cox 1 gene is also
suitable for the phylogenetic analysis of S. scabiei(Gomez-Puerta et al., 2022; Lastuti et al., 2019; Peltier et al.,
2017b). S. scabiei is distributed among three genetically
distinct clades; human-origin S. scabiei from Panama and
Australia comprise 2 distinct clades, respectively, and rabbit-originS. scabiei from China comprise 1 distinct clade, all of which
have been reported in previous reports(Andriantsoanirina et al., 2015;
Peltier et al., 2017b). In contrast to results from black bears and
other wildlife in Japan, the 11 mite sequences in the current study
belonged to the rabbit-origin clade based on phylogenetic analysis and
are evolutionarily similar to mites from rabbits in China(Patrice et
al., 2015; Peltier et al., 2017a). Members of the rabbit-origin clade
have the largest number of hosts and widest distribution among mites in
the three clades(Andriantsoanirina et al., 2015). This indicates that
these mites have the capacity to infect multiple hosts and that the
primary infection source among wildlife may be domestic rabbits. More
in-depth research is needed to prove this hypothesis.
Sarcoptic mange can cause decreases in wildlife populations and is a
substantial threat to global biodiversity(Rossi et al., 2007). Since the
outbreaks of sarcoptic mange in the study regions, local residents have
noticed a decrease in the number of gorals. However, the effects of
sarcoptic mange on gorals have not been assessed. Thus, we analyzed data
from an infrared camera installed in a channel where gorals were
relatively abundant before and after the outbreak of sarcoptic mange.
The results clearly showed that the number of photos of gorals
significantly decreased during the outbreak. This area is also a takin
reserve, and the takin population remained relatively stable. Because
the numbers of photos of serows were small in 2018 and 2019, changes in
the serow population were difficult to assess. Nevertheless, similar to
previous reports on other wildlife species, the goral’s population
suffered a substantial decline owing to sarcoptic mange. The takin
population has not yet been affected.
Our primary concern is the cross-species transmission of S.
scabiei in this study. As mentioned above, this scabies species belongs
to the genetic rabbit-origin clade and impose a potential risk of
multi-host infection(Andriantsoanirina et al., 2015; Fraser et al.,
2016). This is concerning because many rare and endangered wildlife
species live in the Qinling Mountains. However, there is still debate
concerning host specificity in S. scabiei (De et al., 2020; Old et
al., 2018; Samuel et al., 2001).Whether scabies can cause mass deaths
among giant panda, takin, leopard, and gold monkey populations is an
important issue. In the Alps, sarcoptic mange has caused mass death
events among chamois, and mass death events have been sporadically
reported in other sympatric wild ruminants(Rossi et al., 2007).
Efficient transmission of scabies from Capra pyrenaica to the
sympatric Sardinian moufflon (Ovis musimon ), a red deer, has been
observed in northern Spain since the appearance of scabies inRupicapra r. pyrenaica (Fernández-Morán et al.,
1997). Interestingly, prey-to-predator scabies transmission among
wild animals has been proven(Francis et al., 2011). According to these
reports, host susceptibility, host traits and adaptation strategies of
scabies play key roles in cross-species transmission(Browne et al.,
2022; Niedringhaus,Brown, & Sweeley et al., 2019).
In our study, although there was no evidence of sarcoptic mange in wild
animals other than gorals and serows, the risk of sarcoptic mange
spillover from gorals and serows into other animal populations remains
in the Qinling Mountains. This risk is due to the following: 1.Other wild animals are susceptible to scabies. Reports of scabies in
other animals in the same order are common(Escobar et al., 2022).
Although there are no reports of sarcoptic mange in the giant panda,
psoroptic acariasis is common in the captive giant panda(Wang et al.,
2018). 2. These animals share similar environments with gorals
and serows (S5). In our collected samples, the location of G9 was near
to that of M2. Notably, giant pandas eating dead takin and other animals
have been reported in the news. This means that giant pandas and
leopards may contract scabies by eating dead gorals. 3. The high
population density of takins and golden monkeys may promote the spread
of scabies(Devenish-Nelson et al., 2014). Therefore, we think that the
main wild mammal populations in the Qinling Mountains are at high risk
of sarcoptic mange outbreaks.
Based on our results, we propose the following protective measures.1. Carry out specific monitoring . Especially in winter and early
spring, locating and burying carcasses with scabies are very important
measures for interrupting the transmission of sarcoptic mange in
wildlife in a timely manner. 2. Actively treat infected
animals. The application of sarcoptic mange therapies is easier in
animals with mild infections, and fluralaner and ivermectin are very
effective for the treatment of this disease in wildlife(Rowe et al.,
2019; Wilkinson et al., 2021). Consequently, recovered animals will be
resistant to scabies recurrence(Alasaad et al., 2013). Therefore,
locating and treating infected animals as soon as possible is
beneficial. These cured animals may play an important role in the
recovery of populations. Regarding treatment of free-range wildlife, the
greatest challenge is locating and capturing sick animals. Herein, we
propose a feasible noncontact therapeutic regimen according to the
characteristics of sarcoptic mange and routine activities of sick
animals. A bionic injection device containing drugs can be installed on
a tree on the sides of rivers. When sick animals scratch the infected
area on the tree to relieve itching, the drugs are injected into the
subcutaneous tissue. 3. Strengthen monitoring of the giant
panda, takin, golden monkey and other animals. Locating dead animals
and collecting samples as soon as possible could help identify sarcoptic
mange spillover, which needs further study, and this could guide the
establishment of more effective protection strategies to prevent
outbreaks in time. 4. Eliminate the risk of transmission of
scabies among wild animals, domestic animals and humans. Mange is an
ideal disease for One Health research because it can infect domestic and
wild animals as well as humans, and the environment can play a role in
transmission(Astorga et al., 2018). In our survey, farmed swine and
goats were frequently in close proximity to free-ranging animals in the
Qinling Mountains. This is an important route of transmission for
zoonotic diseases. Therefore, this contact should be limited to a
specific area; this could also prevent other diseases from being
transmitted among the domestic and wild animals and humans.
In conclusion, this report is the first to reveal the prevalence and
pathogenic characteristics of sarcoptic mange in wild animal populations
in the Qinling Mountains, analyze the risk factors for transmission and
propose protection strategies. This information can guide the design of
future management and control strategies and contribute to the
preservation of biodiversity in the Qinling Mountains.