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.