Ticks (Acari: Ixodoidea) in China: Geographical distribution, host diversity, and specificity

Abstract Ticks are obligate blood‐sucking ectoparasites, which not only directly damage through bites but also transmit many pathogens. China has a high diversity of tick species, 125 species have been reported, including 111 hard tick and 14 soft tick species. Many of the ticks are important vectors of pathogens, resulting in zoonoses. The dynamics of ticks are affected by both the host and habitat environment. However, systematic studies on the geographical distribution, host diversity, and specificity of ticks are limited in China. To achieve this goal, the relevant available data were summarized and analyzed in this study. Ticks are distributed in all parts of China and Xinjiang has the most records of ticks. The distribution of ticks in adjacent areas is similar, indicating that the habitat environment affects their distribution. Most ticks are widely distributed, whereas some species are endemic to their distributed regions. Ticks are parasitic on mammals, birds, and reptiles, of which mammals are the main host species. Overall, most ticks parasitize different hosts, only a few ticks have strict host specificity, such as ticks that are specifically parasitic on reptiles and bats. In addition, environmental changes and control efforts also influence the dynamics of ticks. These results can better reveal tick biological traits and are valuable for tick control.


| INTRODUCTION
Ticks are obligate blood-sucking arthropods found throughout most regions of the world. Ticks infest every class of terrestrial vertebrates, including mammals, birds, reptiles, and even amphibians (Sonenshine & Roe, 2013). Ticks are important to humans through the direct effects of their feeding and as vectors for various agents of disease in both man and livestock (de la Fuente, Estrada-Pena, Venzal, Kocan, & Sonenshine, 2008).
More than 16 specific tick-borne (or tick-caused) diseases of humans and more than 19 tick-borne diseases of livestock and companion animals have been described to date (Nicholson, Sonenshine, Lane, & Uilenberg, 2009). The frequencies of several tick-borne diseases and their geographical distribution are increasing, owing in part to climatic changes (Estrada-Peña, Ayllón, & De La Fuente, 2012;Gray, Dautel, Estrada-Peña, Kahl, & Lindgren, 2009). For example, the incidence of Lyme disease (LD), a well-known tick-borne disease, dramatically increased and spread to all parts of the United States in recent years (https://www.cdc.gov/ lyme/index.html). In addition, tick infestation causes economic losses due to body weight or milk production loss or treatment cost used for its prevention and control. For example, at least 80% of the world's cattle population are at risk from tick-borne diseases (Ghosh, Azhahianambi, & Yadav, 2007). Ticks cause a huge loss to cattle milk production conjugated with nutritional status and a poor management pattern in Ethiopia (Duguma, Kechero, & Janssens, 2012). Over 900 tick species have been identified to date globally, and they mostly belong to two families, the Ixodidae or hard ticks, and the Argasidae or soft ticks (Barker & Murrell, 2004;Guglielmone et al., 2010). Furthermore, hard ticks are divided into Prostriata (genus Ixodes) and Metastriata (remaining genera). In nature, most hard ticks are non-nidicolous, shelter in leaf litter, duff, rotting vegetation, or are buried in sand and under gravel and stones. Almost all of the non-nidicolous ones are species of the Metastriata subgroup of the Ixodidae. Most Argasidae and many Prostriata ticks are nidicolous, living in nests, burrows, caves, or other shelters used by their hosts or hiding close by. There are four stages, namely egg, larva, nymph, and adult in the life cycle of ticks. Ticks spend most of their life cycle off the host, exposed to these environmental conditions, and they will complete many important biological processes during the nonparasitic phase, such as moulting of engorged larvae and nymphs, oviposition of engorged females, incubation of eggs and host seeking. For larvae, nymphs, and adults, they need to feed or mate on the host at certain periods. The engorged ones detach from the host to seek shelter in a suitable microenvironment, where they can digest its meal and molt to the next stage. Depending on whether larvae and nymphs molt to the nymph or adult stage, respectively, off or on the host, hard ticks are classified as 3-, 2-, or 1-host ticks, and most of them have a 3-host life cycle, taking at least a year to complete their life cycle. However, life cycles of the soft ticks are more variable than those of hard ticks. For instance, soft ticks have multiple nymph stages that require a blood meal, and soft ticks tend to feed rapidly, whereas hard ticks tend to complete feeding processes that last days (Sonenshine & Roe, 2013).
Ticks have evolved several different strategies to facilitate their survival, while waiting for vertebrate hosts. In non-nidicolous species, the ticks crawl up emergent vegetation, where they wait for a passing host (the ambush strategy), and the questing periods might last many weeks or even months. Many tick species are able to survive for long periods because they can minimize evaporative water loss. Some ticks use the hunter strategy in host seeking, and they are attracted by CO 2, ammonia, and other odorants, emerge from their shelters and walk or run toward their hosts. Nidicolous ticks exhibit very different behavioral patterns than those of non-nidicolous species. They shelter in the nests or burrows of their preferred hosts (or close by).
There they are exposed to greater humidity and less extreme environmental conditions than their nonnidicolous relatives. These ticks rarely, if ever, are found questing outside of the host's dwelling. All stages of most of the nidicolous ticks feed on the same type of host. The nidicolous lifestyle often leads to host specificity, as it does to some degree in many species of Ixodidae ticks (J. Z. Liu & Yang, 2013;Sonenshine & Roe, 2013). Obviously, the life cycle and population dynamics of ticks are influenced by two factors, host seeking efficiency and host availability. The former factor is often associated with the population density, distribution pattern and activity periods of the host and the environmental conditions in tick seeking regions.
Host availability refers to whether the host can be used or preferred by ticks. Previous studies have conformed two contrasting hypotheses concerning tick-host associations: Ticks select certain hosts in a given environment, and ticks select certain environments and feed on any available host within these (Cumming, 1998;Hoogstraal & Aeschlimann, 1982;Klompen, Black, Keirans, & Oliver, 1996;Nava & Guglielmone, 2013).
In a broad sense, the host specificity of ticks is quantified as the number of host species, or host range.
However, meta-surveys found a significant correlation between host range and sampling effort and suggested that ticks are habitat rather than host specialists, thus simply counting the number of hosts used by ticks cannot fully reflect the host specificity degree (Cumming, 1998;Nava & Guglielmone, 2013). At the scale of the global geographic distribution of a species, ticks tend to be host generalists, and the ecological similarity of the host environment may be more important than host phylogenetic similarities in determining the ticks' host range. At a more local scale, host specialization seems to be the norm in ticks. In addition, the host range of ticks is often related to tick-borne pathogen circulation and disease risk (Mccoy, Léger, & Dietrich, 2013).
Taken together, evaluating the host range of a particular tick species is more informative in understanding tick ecology and evolution.

| TICK SPECIES RECORDED IN CHINA
The data on tick species distributed in China are mainly obtained from published literature (Z. Deng & Jiang, 1991;Duan, 2013;T. Guo et al., 2017;Y. Guo et al., 2016;Wen & Chen, 2016;X. Yu et al., 1997). Wen and Chen (2016) also examined and revised the valid species names of the Argasidae ticks of the world. A total of 125 tick species have been recorded and described in the area of study. Based on these data, the detailed information on the valid species names and distributions are presented in Table 1. As shown, the Ixodidae family comprises 111 species from seven genera, Amblyomma (eight species), Anomalohimalaya (two species), Dermacentor (14 species), Haemaphysalis (43 species), Hyalomma (seven species), Ixodes (29 species), and Rhipicephalus (eight species), and the Argasidae family comprises 14 species from two genera, Argas (10 species), and Ornithodoros (four species). Considering that some new tick species and new recorded tick species were recently reported (T. Guo et al., 2017;Y. Guo et al., 2016;Wen & Chen, 2016), and China has a vast territory and various landscape types, the number of tick species in China will most likely increase in future study efforts.

| GEOGRAPHICAL DISTRIBUTION OF TICKS IN CHINA
In China, Deng and Jiang (1991)  In addition, there are many studies that focused on the geographical distribution of ticks at the province level (G. P. Liu et al., 2008;Y. Z. Wang et al., 2015;Y. S. Yang et al., 2008;Yu et al., 1997). Here, these data are reviewed and summarized, detailed information is present in Table 1 Without consider the sampling bias, as shown in Figure 1, Xinjiang has the most tick species records (49 species), followed by Qinghai, Gansu, Yunnan, Fujian, and Taiwan, more than 30 species are found in these provinces. The provinces that have more than 20 species comprise Tibet, Sichuan, Shaanxi, and Hubei. Most of the remaining provinces have more than 10 species. It is worth noting that tick species records in Henan, Jiangxi, Hunan, Zhejiang, and Chongqing are relatively less, and tick species records in Beijing and Tianjin are lacking.
Ecological differences among these regions mainly result in differences in tick species records. For example, Xinjiang has different ecological types from inland areas and its livestock and wildlife are rich, so that many endemic tick species can survive in this region. Similarly, some endemic tick species are found in Tibet that is located in the Qinghai-Tibetan Plateau. Obviously, tick species records are strongly correlated with sampling and investigation efforts, ticks with great medical and agricultural importance receive more attention. In such cases, the tick species diversity of each province cannot be simply evaluated based on these records and more investigations of tick distribution are required, especially in areas where low numbers of tick species have been reported.

| HOST DIVERSITY OF TICKS IN CHINA
There are differences in host distribution and diversity across tick distributed areas. In China, ticks can infest many vertebrates, including mammals, birds and reptiles, although their performances on these hosts remain largely unknown. X. J. Yang, Chen, Yang, and Liu (2008) have counted that about 130 animal species of 20 orders can be hosted by ticks in China. Of the 125 tick species examined in this study, nine species are from reptiles, 31 from birds, and 112 from mammals (Table 1). Furthermore, reptiles comprise lizards, snakes, and tortoises. Birds infested by ticks are mostly poultry, pigeons and wild birds. Like other studies, mammals are the main hosts of ticks, including Artiodactyla, Carnivora, Chiroptera, Insectivora, Lagomorpha, Perissodactyla, Pholidota, Primates, and Rodentia. Among the mammal hosts, most tick species are found on Artiodactyla and Rodentia, with 80 and 42 species of ticks respectively. In addition, many ticks are found on domestic animals, including cattle, buffaloes, sheep, goats, rabbits, pigs, dogs, horses, and donkeys, which are marked as livestock in this study. These ticks will cause host body weight or milk production loss and act as reservoirs of diseases, thus they receive much attention (Yin & Luo, 2007; Z. Yu et al., 2015). Some tick species can infest different classes of animals. For example, larvae F I G U R E 1 Tick species recorded in each province in China and nymph ticks of Ixodes persulcatus are found on birds and small mammals. Cattle, pangolins and lizards are hosts of Amblyomma crassipes. These ticks that have wide host range may have adapted to different host types, including host habitats, host immunity, and so on. A series of experimental studies on the life cycle or reproductive barriers of ticks have also reinforced the hypothesis. In detail, under laboratory conditions, many ticks exhibited physiological plasticity as they can feed successfully using novel hosts not related to the natural hosts (Z. Chen et al., 2009;Faccini, Cardoso, Onofrio, Labruna, & Barros-Battesti, 2010;Labruna, Soares, Martins, Soares, & Cabrera, 2011;J. Liu et al., 2005;Ma et al., 2013;Olegário, Gerardi, Tsuruta, & Szabó, 2011;Pinter, Dias, Gennari, & Labruna, 2004). Meanwhile, these findings raise the possibility that the host diversity of ticks is undervalued, and various hosts can be used by ticks. Assessment of the host diversity of ticks is strongly affected by sampling bias and data record anomalies. In such cases, the influences of the two factors should be paid more attention to in investigating the host diversity of ticks.  (Hoogstraal & Aeschlimann, 1982). However, Klompen et al. (1996) concluded that adaptation to a particular habitat is more relevant for tick distributions than adaptation to a particular host. In a later study, Cumming (1998) suggested that both host specificity and ecological specificity could be important in determining tick distributional ranges and their evolution and that it depends on each particular tick species. A meta-analysis of host specificity in Neotropical hard ticks revealed that strict host specificity is not common among these ticks and suggested that the influence of tick ecology and evolution of habitat specificity, tick generation time, phenology, time spent off the host, and the type of life cycle could be more important than host species (Nava & Guglielmone, 2013). Although strict host specificity is not common in ticks in these studies, many ticks exhibited host specificity to varying degrees. Analyzing tick-host specificity at different taxonomic levels of both ticks and their hosts, Cumming (1998) revealed that most of the well-collected genera of African ticks are found mainly on mammals,

| HOST SPECIFICITY OF TICKS IN CHINA
with Aponomma specializing on squamate reptiles, Carios on bats and Argas on birds. Furthermore, host preference is more obvious at a specific level, and at least 39 tick species exhibit specialization to a taxonomic level below class. Field observations suggest that even broad host generalists tend to feed on only a few main hosts locally, with these hosts changing across different areas of the distribution (Balashov, 2010). Significant patterns of local hostassociated genetic structure have been observed in several tick species (McCoy et al., 2013). In these cases, ticks have adapted to different environmental conditions and thus preferred different hosts depending on availability in a particular area.
Studies of host specificity of ticks in China are relatively limited (Deng & Jiang, 1991). In this study, general patterns of tick-host specificity are described based on available data, although sometimes recorded data are incomplete. Some tick species were only found on a single host species, in such case, whether or not they have strict host specificity is not determined. Additionally, three tick species, Ixodes frontalis, Haemaphysalis primitive, and Argas robertsi, had no host records.
In general, hosts that can be used by ticks comprise reptiles, birds, and mammals. Among these tick species, nine species feed on reptiles, and five are specific for reptiles. Seven of the nine reptile-feeding ticks belong to Amblyomma genus (  (Cumming, 1998;Hoogstraal & Aeschlimann, 1982). Mammals serve as hosts for more tick species than do birds and reptiles, and at least one species of each tick genus utilizes mammals as hosts (Table 1). Artiodactyla are hosts for 80 tick species, including almost all tick genera found in China. Adult or immatures of these ticks utilize Artiodactyla as their main source of blood, and many of them also parasitize other mammals, birds, and reptiles. In contrast, only two species, Haemaphysalis kitaokai and Hyalomma isaaci feed on Perissodactyla, the former is also found on Artiodactyla, and the host range of another one also comprises Artiodactyla Overall, only a few ticks in China have strict host specificity, and most ticks can live on different hosts. These observations are consistent with previous results that analyze host specificity of ticks (Cumming, 1998;Hoogstraal & Aeschlimann, 1982;Klompen et al., 1996;Nava & Guglielmone, 2013 Another possibility is that adult and immature ticks occupy different habitats, where they can utilize different hosts (Hoogstraal & Aeschlimann, 1982).

| TICK DYNAMICS UNDER ENVIRONMENTAL CHANGES AND CONTROL
As mentioned above, ticks spend most of their life cycle off hosts, exposed to environmental conditions that are largely altered by human activity and climate change. In a dynamic environment, the tick distribution and abundance and tick-borne disease risk will be strongly influenced. For example, Gray et al. (2009) reviewed the effects of climate change on several tick species in Europe. Robinson et al. (2015) revealed that both forested habitat and temperature were important drivers of LD spread in Minnesota, USA. In recent years, China's urbanization process is accelerating (M. Chen, Lu, & Zha, 2010), and industrial structures of agriculture and animal husbandry have been largely adjusted. These will cause changes in the suitable environment and preferred hosts of ticks, and influences of these changes on tick dynamics can be expected, although there is no systematic study on this issue. In contrast, many ticks are of medical and economic importance, and the prevention and control of ticks has always been received attention. In China, there are many effective control strategies for ticks, including rotational grazing (Dong et al., 2007), chemical control (Nong et al., 2013;Rajput, Hu, Chen, Arijo, & Xiao, 2006), biological control (Ren et al., 2012;Sun et al., 2013), and vaccine development (T. T. Zhang et al., 2017). In such cases, the dynamic changes in ticks also deserve further study.

| CONCLUSION AND PERSPECTIVE
Geographical distribution, host diversity, and specificity of 125 tick species in China are reviewed in this study. The tick distributions varied across different regions, Xinjiang has the most tick species records, while few species are present in some provinces. Endemic and universal species are also observed. The distribution pattern is partly due to the different ecological environments in the distributed area. Ticks feed on mammals, birds, and reptiles, most species choose mammals as their hosts. Host diversity of soft ticks is lower than that of hard ticks. Furthermore, only a few ticks have strict host specificity, and most ticks can live on different hosts. These observations are helpful for research on tick ecology and biology. However, more efforts are needed to effectively control ticks and tick-borne diseases, including investigation of tick performance on different hosts, tick population dynamics and outbreak risk, mechanisms of tick biology and tick-pathogen interactions, and tick control strategies.

ACKNOWLEDGMENTS
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