Invasive plants facilitated by socioeconomic change shelter vectors of scrub typhus and spotted fever

Background Ecological determinants of most emerging vector-borne diseases are little studied, particularly for neglected tropical disease; meanwhile, although socioeconomic change can have significant downstream effect on human risks to vector-borne diseases via a change in land cover, particularly facilitating the invasion of exotic plants, related studies remain very scarce. Scrub typhus and spotted fever are neglected diseases emerging around the globe and are transmitted by chigger mites and ticks, respectively, with small mammals as the primary hosts of both vectors. Methodology/Principal findings We investigated how invasion of Leucaena leucocephala plant after extensive abandonment of farmlands driven by industrialization in Penghu Islands of Taiwan affected abundance of chiggers and ticks by trapping small mammals in three types of habitats (invasion site, agricultural field, human residence) every two months for a year. Invasion sites sheltered more chiggers and ticks than the other two habitats; moreover, both vectors maintained higher abundance in early winter and populations of chiggers were more stable across seasons in invasion sites, suggesting that the invasive sites could be a temporary refuge for both vectors and might help mitigate the negative influence of unfavorable climate. Infective rates of etiologic agents in chiggers and ticks were also higher in invasion sites. Top soil temperature and relative humility were similar across the three habitats, but invasion sites harbored more Rattus losea rat, on which infested chiggers and ticks were more well fed than those from the most commonly trapped species (Suncus murinus shrew), implicating that abundance of superior hosts instead of microclimate, might determine the abundance of both vectors. Conclusions/Significance This study highlights an important but largely neglected issue that socioeconomic change can have unexpected consequence for human health mediated particularly through invasive plants, which could become a hotspot for emerging infectious diseases but usually are very hard to be eradicated. In the future, a more holistic perspective that integrates socioeconomy, land use, exotic species, and human health should be considered to fully understand potential emergence of vector-borne diseases. Author summary Understanding how environmental factors, such as land use change, affect risks to vector-borne diseases helps control and prevent human diseases, but ecological preference of vectors of most neglected diseases remain little investigated. In this study, we found that vectors of scrub typhus (chigger mites) and spotted fever (hard ticks), two emerging neglected diseases, were much more abundant in sites invaded by exotic plants than the other major land cover types in a small island of Taiwan; moreover, populations of chigger mite in invasion sites were more stable across seasons, suggesting that plant invasion sites could be a refuge for disease vectors under unfavorable climate. Higher abundance of chigger mites and ticks was related to higher abundance of a superior rodent host instead of a difference in soil micro-climate. More significantly, these invasive plants are facilitated by extensive abandonment of farmlands driven by industrialization and rural to urban migration, thus demonstrating an important but largely neglected issue that socioeconomic change, when mediated through a change in land cover, can have unexpected downstream effect on emerging neglected tropical diseases.

8 126 eradicating L. leucocephala has been a priority for local government.

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Penghu Islands, at the same time, is the hotspot of scrub typhus, with the highest number of 128 human cases of notifiable scrub typhus among all counties in Taiwan for the past ten years (2008-129 2017, Taiwan Centers for Disease Control, https://nidss.cdc.gov.tw/, accessed October 17, 2018).

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Trapped small mammals, including shrews and rodents, were identified to species, sexed, 168 measured for body weight, body length, and tail length, and examined for ectoparasite infestation.
169 Skins with attached chiggers were removed from host animals with tweezers and placed in vials; 170 100% ethanol were added after 2-3 days when chiggers have released themselves from the skins to 171 preserve intact oral parts for later species identification. Ticks were carefully collected with 172 tweezers and preserved in 100% ethanol. All infested chiggers and ticks were collected and stored 173 in -20°C refrigerator for subsequent molecular determination. Large rodent species, including 174 Rattus losea and Rattus norvegicus, were each implanted with a radio-frequency identification chip 175 (Watron Technology Corporation, Hsinchu, Taiwan) for individual identification before release.
176 Smaller species, including Suncus murinus and Mus musculus, were unable to be permanently 177 marked without difficulty, so were released without being marked.
12 230 as well as whether host species vary in their relative importance among habitats in hosting ticks,  (Fig 4b).

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The sum of chiggers collected from all mammal hosts or uniquely from R. losea both varied 296 among regions, habitats, and months (GEE, all p < 0.001), and there was an interaction between 297 habitat and month (both p < 0.001). There were more chiggers in the eastern region than the other 298 parts of the study area (all p < 0.05) (Figs 6a-b). Invasion sites sheltered more chiggers than the 299 other two habitats in most months, significantly in December (all p < 0.05) (Figs 7a-b). The

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On the other hand, number of chiggers collected solely from S. murinus differed among regions 304 and months (both p < 0.001) but not among habitats (p > 0.05), and there was an interaction 305 between habitat and month (p < 0.001). There were significantly more chiggers in the eastern region 306 than the north and west regions (both p < 0.05) but not the central (p > 0.05) (Fig 6c). There was no 307 significant differences among the three habitats within the same month (all p > 0.05) (Fig 7c), Figure legends