Ecological and microbiological diversity of chigger mites, including vectors of scrub typhus, on small mammals across stratified habitats in Thailand

Abstract

Background: Scrub typhus, caused by a bacterial pathogen (Orientia spp.), is a potentially life-threatening febrile illness widely distributed in the Asia-Pacific region and is emerging elsewhere. The infection is transmitted by the larval stage of trombiculid mites ("chiggers") that often exhibit low host specificity. Here, we present an analysis of chigger ecology for 38 species sampled from 11 provinces of Thailand and microbiomes for eight widespread species. Results: In total, > 16,000 individual chiggers were collected from 1574 small mammal specimens belonging to 18 species across four horizontally-stratified habitat types. Chigger species richness was positively associated with higher latitudes, dry seasonal conditions, and host maturity; but negatively associated with increased human land use. Human scrub typhus incidence was found to be positively correlated with chigger species richness. The bacterial microbiome of chiggers was highly diverse, with Sphingobium, Mycobacterium, Neisseriaceae and various Bacillales representing the most abundant taxa. Only Leptotrombidium deliense was found to be infected with Orientia and another potential pathogen, Borrelia spp., was frequently detected in pools of this species. β-diversity, but not α-diversity, was significantly different between chigger species and geographic regions, although not between habitat types. Conclusion: Our study identified several key environmental and host-derived correlates of chigger species richness across Thailand, which in turn impacted on human scrub typhus incidence. Moreover, this first extensive field survey of the chigger microbiome revealed species-and province-level variation in microbial β-diversity across the country, providing a framework for future studies on interactions between pathogens and other symbionts in these understudied vectors. Background The Trombiculoidea is a superfamily of mites (Acari: Acariformes) with a unique mode of parasitism among medically-relevant arthropod vectors. The larval stage, colloquially known as chiggers or berry bugs, is ectoparasitic on vertebrates (or occasionally invertebrates). In contrast, the deutonymph and adult stages have an edaphic lifestyle and are free-living predators of arthropods or their eggs [1]. Chiggers are the exclusive biological vectors of scrub typhus, a potentially life-threatening febrile illness of humans that historically has been associated only with the Asia-Pacific region [2]. However, recently endemic scrub typhus has been reported from the Middle East [3] and South America [4], and local transmission is suspected in sub-Saharan Africa [5]. The main aetiological agent of the disease, Orientia tsutsugamushi (Rickettsiales: Rickettsiaceae), is a vertically-transmitted chigger symbiont that has been reported to induce reproductive manipulations in its arthropod host [6]. The epidemiology of scrub typhus remains poorly understood, largely because chiggers are minute (typically < 250 μm in length) and very challenging to identify and utilise for molecular chara...

Infestation and seasonal fluctuation of chigger mites on the Southeast Asian house rat (Rattus brunneusculus) in southern Yunnan Province, China

“…The average temperature was positively correlated with all the infestation parameters ( P M , MA and MI ) of W. ( W. ) turmalis ( P < 0.05). The positive correlation suggests that warm temperature may be beneficial to the survival, development and reproduction of W. ( W. ) turmalis , and this is in accordance with the situation of most chigger mites ( Chaisiri et al, 2019 ; Clopton and Gold, 1993 ; Li et al, 1997 ; Santibáñez et al, 2015 ).…”

“…Leptotrombidium ( L. ) deliense and L. ( L. ) scutellare often invade and sting humans and it is very easy for them to transmit the diseases from rats to humans ( Li et al, 2005 ; Santibáñez et al, 2015 ; Wu, 2005 ). Ascoschoengastia indica is a potential vector of scrub typhus and it can carry O. tsutsugamushi ( Chaisiri et al, 2019 ; Tilak and Kunte, 2019 ; Wu et al, 2013 ). The abundant L .…”

“…Chigger mites are a large group of arthropods with a unique mode of parasitism among medically-relevant arthropods and their larvae (often known as chiggers) are the exclusive ectoparasitic stage in their complex lifec cycle ( Zhang et al, 2011 ; Walter et al, 2009 ; Santibáñez et al, 2015 ; Chaisiri et al, 2019 ). Most stages of chigger mites are edaphic creatures and some of them (deutonymphs and adults) are predators of some other arthropods (especially arthropod eggs) in the soil ( Chaisiri et al, 2019 ; Shatrov and Kudryashova, 2006 ; Li et al, 1997 ). Chiggers are common ectoparasites on vertebrates (occasionally some invertebrates), and rodents and some other small mammals are their common hosts ( Elliott et al, 2019 ; Daniel and Stekolnikov, 2009 ; Lv et al, 2019 ).…”

“…Scrub typhus is a zoonotic disease potentially threatening human health and it is widely prevalent in Asian Pacific regions where more than one billion people are at risk of being infected and around one million new cases are reported annually ( Bonell et al, 2017 ). In recent years, the prevalence of the disease in many places has shown a rapid increase, and the epidemic foci have been continuously expanding ( Chaisiri et al, 2019 ; Elliott et al, 2019 ; Tilak and Kunte, 2019 ). Scrub typhus was previously believed to be only associated with Asian Pacific regions ( Bonell et al, 2017 ), but it has probably spread to some other places of the world in recent years.…”

High prevalence and low diversity of chigger infestation in small mammals found inBangkok Metropolitanparks

“…It can be hypothesized that lack of biodiversity-rich areas such as natural habitat or preserve forest (particularly on the mountainous landscape) in Bangkok may limit the abundance and diversity of chiggers and probably affect Orientia bacteria's ecological niche and transmission (particular horizontally). This hypothesis has been postulated by Chaisiri et al (2019), with the evidence that (1) chigger diversity in murid rodents from Thailand gradually decreased towards urbanization and (2) scrub typhus incidence was found to be positively correlated with chigger species richness. This finding is in line with the low disease incidence in Bangkok; only 20 and 31 cases of scrub typhus were documented during 2018 and 2019, respectively (Report 506: Bureau of Epidemiology, Ministry of Public Health, Thailand).…”