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.