4. Discussion
In our models, the temperature and precipitation contributed the most among all the variables. Temperature and rainfall are determining factors in the activity, abundance, and survival of Culicoides(P. S. Mellor, Boorman, & Baylis, 2000). Previous studies have demonstrated that temperature is positively correlated with theCulicoides activity, and adult vector activity was suppressed at low temperatures (Carpenter et al., 2011; M. Murray, 1987; Searle et al., 2014). At the same time, high temperatures favored larval development leading to faster population growth (Kitaoka, 1982; Vaughan & Turner, 1987). Furthermore, temperature can also influence the AHSV infection rates and the vector Culicoides virogenesis rates (Wellby, Matthew, Peter, & Research, 1996). At high temperatures, the vector virogenesis rates were high (Verhoef, Venter, & Weldon, 2014; Wittmann, Mello, & Baylis, 2002); the incidence of vector-bone diseases were low in cold temperatures (Venter & Meiswinkel, 1994). However, laboratory studies have proved that individual Culicoidessurvived for a relatively short lifespan at very high temperatures (Wellby et al., 1996; Wittmann et al., 2002).
On the other hand, rainfall can also influence the activity ofC.imicola , which will decrease at low moisture levels (Walker, 1977). In Australia, after rainfall, there was an increase in the feed time of many Culicoides midges. The feeding frequency influences the host-biting rates; therefore, the population transformed to one capable of explosive transmission (M. D. Murray, 1986). At a suitable temperature, the abundance of vectors is often more closely related to the rainfall. Diarra found that the largest amount of C.imicolaabundance appeared in the year of the greatest rainfall in Senegal (Diarra et al., 2014). In addition, rainfall influences the spread of AHS by governing the availability of larval habitat and regulating the survival and dispersal of adult Culicoides (Purse, Carpenter, Venter, Bellis, & Mullens, 2015). The water content can determine the suitable semiaquatic habitat for the larva (Meiswinkel, 1997), and more rain may produce more or suitable habitats. However, if the habitats are flooded, C. imicola will drown (Nevill, 1967).
Horse density and land cover were also key factors in the jackknife test, and there was high probability of C.imicola presence in the “Urban and built-up” and “Closed shrublands” areas. The horse density was positively correlated with the AHS occurrence (Riddin, Venter, Labuschagne, & Villet, 2019); other studies (Bakhoum et al., 2016; Fall et al., 2015; Garros et al., 2011) also showed the very complex relationship between the AHS vectors and livestock. Female Culicoides depend mostly on blood meals as a food source (de Beer, Boikanyo, Venter, & Mans, 2020; Slama, Haouas, Mezhoud, Babba, & Chaker, 2015). In dense urban and built-up areas, where the urban population and livestock sector is continually expanding, the transmission probability of AHS may be greatly increased.
Closed shrublands are dominated by shrubs or short statured trees, which results in a moist and shaded microenvironment that is very suitable for livestock breeding; this environment also leads to the development of arbovirus vectors (Diarra et al., 2018; Diarra et al., 2015). In addition, shrublands have highly permeable and organic soils, which are beneficial for the growth and development of larvae. Notably, the maleCulicoides mainly feed on the soft stems of plants; therefore, they need vegetation cover nearby to survive.
Our area of interest is in the tropical and subtropical monsoon climate, and this study shows that they are almost at relatively high risk of AHS infection. The tropical monsoon climate is characterized by high temperatures throughout the year with two seasons: a dry season and a rainy season. The mean temperature of the coldest month is not less than 16 °C, and there is no frost all year round. The subtropical monsoon climate has high temperatures and rain in summer, and the mean temperature of the coldest month ranges from 0 °C–15 °C. Hainan and Fujian are not extremely cold and neither are they too dry; therefore, the weather is suitable for the survival and development ofCulicoides . Leta has suggested high suitability forC.imicola in the tropical and subtropical area (Leta, Fetene, Mulatu, Amenu, Jaleta, Beyene, Negussie, & Revie, 2019)
Eastern Yunnan is adjacent to Guangxi, in the south of the two provinces, there are many wide valleys and basins, which are mainly covered by low vegetation (small bushes and trees). According to the People’s Government of Yunnan Province (http://www.yn.gov.cn/), by 2018, the forest area of Yunnan was approximately 23.11 million hectares, and the forest coverage rate was 60.3%. According to the data from the National Bureau of Statistics of the People’s Republic of China (http://www.stats.gov.cn/), by 2018, Yunnan is the first largest province in terms of mule production in China; the yields of donkeys and horses are also in the top 10 (in 31 provinces). Guangxi is the fifth largest province in terms of horse production. Yunnan and Guangxi are suitable habitats for C.imicola because both these areas are characterized by dense vegetation and high density of livestock. Furthermore, border trade on land is frequent in the Yunnan and Guangxi areas11The 17th China–ASEAN expo will be held in Nanning, Guangxi, China from November 27 to 30, 2020.. Therefore, there may be two pathways for the spread of AHSV: the cross-border movement of infectious hosts and movement of infected Culicoides via livestock trade (Faverjon et al., 2015).
China has a thriving modern horse industry with a lot of attention being paid to horse breeding. The Chinese Equestrian Association joined the International Equestrian Federation in 1982. By 2019, there were approximately 2160 equestrian clubs in China. East China where Fujian is located has the largest number of these clubs (Horsemanship, 2019). Hainan is located at the junction of the Pacific Ocean and the Indian Ocean; it connects Northeast Asia to Southeast Asia. After the establishment of the Hainan Equestrian Association in 2015, the construction of a horse culture characteristic town has been completed. Currently, Hainan clearly encourages the development of horse racing as a sport and supports the creation of the international horse culture, sports, and tourism resorts (Yuanyuan & Yu, 2020). The planning and development of the Hainan Pilot Free Trade Zone will further promote economic and trade cooperation with overseas markets (Meng et al., 2018). Therefore, in addition to the infrastructure, such as racecourses, Hainan and Fujian need to further build an epidemic-free area, especially an AHS-free area.
Fujian and Hainan are coastal provinces of southern China; they have well developed maritime trade, and their sea ports are very important. The horses needed for modern equestrian and horse racing are mostly bred in developed countries such as Europe, North America, and Australia (Power, 2014). A major risk pathway for AHS is the movement of infectious equids, and for example, the AHS outbreak in Europe (1987–1990) was caused by the import of infected zebras from Namibia to Spain (P. S. Mellor & Boorman, 1995; Rodriguez et al., 1992). Previous studies have also shown that the AHSV outbreak in Iran in 1959 was associated with riverine trade (P. G. Howell, 1960). An additional uncontrollable route of AHS introduction into southern China is through infected Culicoides midges carried by the wind from AHS-affected regions. Culicoides midges can be transported from long distances (Reynolds, Chapman, & Harrington, 2006), and they may be blown as far as 700 km when the wind speed is suitable (Pedgley & Tucker, 1977), and there are no orographic obstacles (Bishop, Spohr, & Barchia, 2004). The wind carries the infected Culicoides from the epidemic area to other areas. After landing, these insects bite the local equids who, in turn, spread AHSV.
Although AHS has long been endemic in the sub-Saharan Africa, the transmission of AHSV is heterogeneous spatially and temporally and occurs across a wide area related to the interactions among the vector, host, and environment. AHS is an epidemic with the highest fatality rate in horses; the relevant departments should pay enough attention to prevent AHS from invading China from Southeast Asia.
This research has certain limitations. The mechanism of transmission and infection of AHS is complex; bioclimatic variables, land cover characterization and horse distribution density are only a few of the influential factors. There are other factors, such as horse trade, that should also be considered. Our follow-up study will consider additional factors and provide detailed information.