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Article

The Distribution and Host-Association of the Vector Chigger Species Leptotrombidium imphalum in Southwest China

by
Qiao-Yi Liu
1,
Rong Fan
1,
Wen-Yu Song
1,
Pei-Ying Peng
2,
Ya-Fei Zhao
1,
Dao-Chao Jin
3 and
Xian-Guo Guo
1,*
1
Institute of Pathogens and Vectors, Yunnan Provincial Key Laboratory for Zoonosis Control and Prevention, Dali University, Dali 671000, China
2
Institute of Microbiology, Qujing Medical College, Qujing 655100, China
3
Institute of Entomology, Guizhou University, Guiyang 550025, China
*
Author to whom correspondence should be addressed.
Insects 2024, 15(7), 504; https://doi.org/10.3390/insects15070504
Submission received: 11 April 2024 / Revised: 21 June 2024 / Accepted: 4 July 2024 / Published: 5 July 2024
(This article belongs to the Section Medical and Livestock Entomology)
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Abstract

:

Simple Summary

Leptotrombidium imphalum (a chigger species) can serve as a transmitting vector of scrub typhus. Based on the field investigation in southwest China from 2001 to 2022, this article presents the first report on the distribution and infestation of L. imphalum on small mammals in the region. A total of 2161 L. imphalum were identified from 218 small mammal hosts that crossed three orders, and the majority of the mites were found on the order Rodentia (rodents). Different host species had different susceptibility to the infestation of L. imphalum, and the shrew gymnure (Neotetracus sinensis) was much more susceptible to the infestation than other host species. Leptotrombidium imphalum exhibited an aggregated distribution among different individuals of its hosts. The positive correlation between the infestation indices for L. imphalum on small mammals and the occurrence of scrub typhus, together with the low host specificity of the mite, indicates the potential risk of the mite.

Abstract

Leptotrombidium imphalum is a species of chigger mites, and it can serve as a transmitting vector of scrub typhus. Southwest China is an important focus of scrub typhus. Based on the field investigation in southwest China from 2001 to 2022, this article presents the first report on the distribution and infestation of L. imphalum on rodents and other sympatric small mammals in the region. A total of 2161 L. imphalum were identified from 218 small mammal hosts in 21 of 114 survey sites. The 17 host species of L. imphalum crossed 13 genera and 5 families in 3 orders (Rodentia, Eulipotyphla, and Scandentia), indicating the low host specificity of the mite. The Asian house rat (Rattus tanezumi) was the dominant host species in the 21 sites where L. imphalum were collected, and 49.38% of mites were found on R. tanezumi. Different small mammals had different susceptibility to the infestation of L. imphalum. The prevalence (PM = 27.66%), infestation mean abundance (MA = 6 mites/per examined host), and mean intensity (MI = 21.69 mites/per infested host) for L. imphalum on the shrew gymnure (Neotetracus sinensis) were much higher than those on other host species (p < 0.05), indicating N. sinensis had a high susceptibility to the infestation of L. imphalum. The infestation indices for L. imphalum on small mammal hosts varied along different altitude and latitude gradients (p < 0.05), indicating the environmental heterogeneity of the mite infestation. Leptotrombidium imphalum exhibited an aggregated distribution among different individuals of its hosts. Besides the low host specificity of L. imphalum, the prevalence of the mite was positively correlated with the occurrence of scrub typhus, indicating the potential risk of the mite.

1. Introduction

Chigger mites (or chiggers) are a group of tiny arthropods, and they are the exclusive transmitting vector of scrub typhus (tsutsugamushi disease). Most chigger species are ectoparasites of other animals (vertebrates, invertebrates, and even some arthropods), especially rodents and other sympatric small mammals [1,2,3,4]. As the main hosts of chiggers, rodents and other small mammals are the main infection source and reservoir host of Orientia tsutusgamushi, the pathogen of scrub typhus. Through the biting activity of chiggers, O. tsutusgamushi (Ot) can be transmitted from rodents to humans [5,6]. Besides transmitting Ot, some chigger species (e.g., Leptotrombidium scutellare Nagayo et al., 1921) can serve as the potential vector of Hantavirus (HV), the pathogen of hemorrhagic fever with renal syndrome (HFRS) [7,8]. Southwest China (21°08′–33°41′ N, 97°21′–110°11′ E) is a vast territory, including five provincial regions, Yunnan, Guizhou, Sichuan, Chongqing, and Tibet (Xizang Autonomous Region). Scrub typhus and HFRS are prevalent in southwest China, with some local areas experiencing an outbreak, and it is of medical significance to study chiggers in the region [9,10,11]. In addition, there are Yunnan-Guizhou Plateau, Sichuan Basins, Tibetan Plateau, and Hengduan mountains within the territory of southwest China, with diverse topography, different geographical landscapes, and different types of vegetation and climates, which provide an ideal place to study the distribution and ecological issues of chigger mites on small mammals [12,13].
Although more than 3000 chigger species have been documented in the world, only a few dozens of species (around 50 species) have proved to be the effective vectors of scrub typhus, and 10 of them are the powerful vectors of the disease [6,14,15,16,17,18]. So far, the confirmed vectors of scrub typhus are mainly concentrated in the genus Leptotrombidium, which has the greatest medical significance [6,14,19,20,21,22]. Leptotrombidium imphalum was described and named by Vercammen-Grandjean and Langston in 1975, and it is one of valid species in the genus Leptotrombidium [23,24]. In some foci of scrub typhus, L. imphalum is one of important vectors of scrub typhus, and for example, it has been confirmed as one of the vectors of this disease in Thailand [25,26,27,28,29]. In China, L. imphalum is also considered a significant potential vector of scrub typhus, and O. tsutusgamushi was once isolated from L. imphalum in Yunnan Province of southwest China [30,31].
Previous studies on L. imphalum mainly focused on its efficiency of transmitting the scrub typhus pathogen, O. tsutsugamushi, including the natural and experimental infection of Ot in L. imphalum as well as the transovarial and transstadial transmission of Ot in the mite [25,27,28,32,33,34,35,36,37]. Additionally, some previous studies examined the distribution of Ot in L. imphalum [38], the weight loss of the mouse host (Mus musculus) fed upon by the mite infected with Ot [39], the effective rodent hosts of the mite [25,32], and some other relevant issues [40]. To date, few reports have involved the distribution and infestation of L. imphalum on small mammals in a specific geographical region. From field investigations in southwest China between 2001 and 2022, we collected and identified a lot of L. imphalum, which aroused us to study the distribution and infestation status of this vector species on its small mammal hosts in the region. Being a retrospective study on the basis of previous field investigations, the present study aims to provide more scientific information for further research on this vector species of scrub typhus and to provide a scientific reference for the surveillance and control of the disease and its transmitting vectors in southwest China.

2. Materials and Methods

2.1. Survey Sites

The present study is a retrospective study, and its original data came from previous field investigations in 114 survey sites of southwest China between 2001 and 2022 (see “Table 1” and “Figure 1” in “Section 3”). The field investigations were carried out in different latitudes, longitudes, altitudes, landscapes (mountainous and flatland landscapes), and habitats (indoor and outdoor habitats), and the 114 survey sites are distributed in the five provincial regions of southwest China, Yunnan, Guizhou, Sichuan, Chongqing, and Tibet (Xizang Autonomous Region), covering the most territory of southwest China except western Tibet. In Tibet, only the eastern part was investigated due to the fact that the western part of Tibet is a vast and sparsely populated territory with relatively inconvenient transportation, the existence of hypoxia, and some potential risks in the sparsely populated high-cold areas, and in addition, we did not have enough human resources and financial support to cover the whole territory of Tibet.

2.2. Collection and Identification of Chiggers

According to the “transect line method”, cage traps (18 × 12 × 9 cm; Guixi Mousetrap Apparatus Factory, Guixi, Jiangxi, China) with fresh peanuts, corn, or other baits were placed at each survey site for capturing rodents and other sympatric small mammal hosts (shrews, tree shrews, etc.) [41]. In dry lands, every 25 cage traps (mouse traps) in a group were placed in a straight line, with a spacing of 5 m and a row spacing of 20 m. Considering the complexity and diversity of environmental conditions in the actual investigations, the placement ways of cage traps were flexibly adjusted according to the specific environmental conditions. For example, in the indoors, a cage trap was placed every 15 square meters (15 m2) along the base of the wall. In a paddy field, cage traps were placed along the bank of the field. The same number of cage traps should be placed at each survey site to ensure the “homogeneity” and “comparability” of sampling methods at different survey sites. Each small mammal host captured was separately placed in a cloth bag and transported to the field temporary laboratory [41,42,43,44,45]. In the temporary laboratory, each animal host was separately placed in a big white square plate to collect its ectoparasitic chiggers. Chiggers are very tiny, and they often attach themselves to thin and tender sites of the host skin, including the auricle, outer opening of external auditory canal, groin, perianal area, etc. [46,47]. In order to collect as many chiggers as possible and to ensure that the numbers of chiggers collected from every animal host are comparable, the thin and tender skin sites, especially the auricle and outer opening of external auditory canal where chiggers frequently attach, were chosen as fixed collection sites. Chiggers are very tiny, and it is very difficult to identify them with naked eyes. Under the help of a magnifier, a lancet or curette (ear scraper) was used to scrape the chiggers and chigger-sized objects (suspected chiggers) from the skin of each animal host. The collected chiggers and chigger-sized objects were preserved in 70% ethanol. In the laboratory, the chiggers and chigger-sized objects preserved in 70% ethanol were transferred into distilled water to rinse 2–3 times, and the chiggers were separated from other non-chigger debris under a stereomicroscope (Beijing Electronic Optical Equipment Factory, Beijing, China). The separated chiggers were then mounted on glass slides with Hoyer’s solution [48,49,50]. After dehydration, drying, and transparent process, each glass slide specimen of chigger was carefully observed and measured one by one under a light microscope (Olympus Corporation, Tokyo, Japan) for taxonomic identification [51,52,53,54]. After finishing the identification of all the chigger specimens, L. imphalum was selected as the target of the present study. The use of animals (including animal euthanasia) for our research was officially approved by the Animals’ Ethics Committee of Dali University, and the representative specimens were deposited in the specimen repository of Institute of Pathogens and Vectors, Dali University.

2.3. Statistics for Chigger Infestation

The constituent ratio (Cr, %) was conventionally used to calculate the percentage of L. imphalum in the chigger community. The constituent ratio (the composition ratio, Cr) is a commonly used index in statistics and reflects the proportion of an internal component in the whole, and it is usually expressed as a percentage. The total sum of the constituent ratios must be 100% [55,56,57]. The prevalence (PM, %) was used to calculate the infestation frequency of small mammal hosts with L. imphalum, the percentage of infested hosts. The mean abundance (MA) was used to calculate the average infestation intensity of L. imphalum on the examined hosts (chiggers/per examined host), and mean intensity (MI) was used to calculate the average infestation intensity of L. imphalum on the infested hosts (chiggers/per infested host). The formulae for Cr, PM, MA and MI were as follows [55,56,57,58,59].
C r = N i N × 100 %
P M = H i H × 100 %
M A = N i H
M I = N i H i
In the above formulas, Ni represents the number of L. imphalum, N represents the total number of all chiggers, Hi represents the number of hosts infected with L. imphalum, and H represents the total number of hosts.

2.4. Measurement of Spatial Distribution Pattern of L. imphalum

The Iwao’s regression model and Taylor’s power law were used to measure the spatial distribution pattern of L. imphalum among different individuals of its hosts [60,61,62,63]. The statistical analyses were conducted with SPSS 26.0 and R software (Version 4.3.3). The formulae of Iwao’s regression model and Taylor’s power law were as follows [64,65,66]. The spatial distribution pattern is used to determine the distributing style of a certain population among the sampling units, which is an important issue in ecology. The spatial distribution patterns are usually divided into three types: uniform distribution, random distribution, and aggregated distribution [61,66,67,68].
Iwao ’ s regression model :   M ∗ = α + β M
M i ∗ = M i + σ i 2 M i − 1
M i = ∑ j = 1 N i M i j N i
Taylor ’ s power law :   l g σ 2 = l g a + b l g m
In above formulae, Mij represents the number of L. imphalum on host individual j in sampling unit i, Ni represents the number of host individuals in sampling unit i, and Mi and σi2 represent the mean and variance of L. imphalum on all host individuals in sample unit i. M* represents the Lloyd mean crowding, and M represents the mean of L. imphalum in all sample units; α stands for the intercept and β the slope in establishing Iwao’s regression model. In Iwao’s regression model, when α = 0 and β = 1, the spatial distribution pattern was determined to be the random distribution, and when α > 0 and β > 1, it was the aggregated distribution. In Taylor’s power law, σ and m (m = M) express the same in above formula, lga = intercept (the intercept on the Y-axis, where Y = l g σ 2 ) and b = slope (regression coefficient). When lga > 0, b = 1, the spatial distribution pattern was determined to be the random distribution, and when lga > 0, b > 1, it was the aggregated distribution.

2.5. Relationship of Zoonotic Diseases to Prevalence of L. imphalum

Based on the documented human cases of two zoonotic diseases, scrub typhus and hemorrhagic fever with renal syndrome (HFRS), in Yunnan Province of southwest China between 2007 and 2015 [69,70,71], the linear regression model was used to analyze the relationship between the infestation prevalence (PM) of L. imphalum on small mammal hosts and the human cases of two zoonotic diseases. The human cases of scrub typhus and HFRS in other four provincial regions (Guizhou, Sichuan, Chongqing, and Tibet) of southwest China, however, were unavailable, and the linear regression analysis did not cover these four provincial regions. In the linear regression analysis, the prevalence (PM) of L. imphalum was used as an explanatory variable (independent variable), and the number of human cases infected with the diseases (scrub typhus or HFRS) was used as a response variable (dependent variable). Since the data did not conform to normal distribution, the “MASS” package in R software (Version 4.3.3) was used for normal transformation [72]. The linear regression analysis was performed with the package “ggpubr” of R software (Version 4.3.3) [73].

2.6. Analysis of Influencing Factors on L. imphalum

Six environmental factors (temperature, humidity, elevation, precipitation, landscape, and habitat) were used as the independent variables, and the annual infestation prevalence (PM) of L. imphalum on small mammal hosts was taken as the dependent variable. The analysis of geographical detector (GD) was used to calculate the determination powers of the independent variables (environmental factors) to the dependent variable (PM of L. imphalum). The higher the value of determination power, the more prominent the influence of corresponding factors on the mite (L. imphalum). The analysis was conducted with package “GD” in R software (Version 4.3.3) [74,75,76]. The climate factors such as temperature, humidity, and precipitation were obtained from the National Earth System Science Data Center of China (https://www.geodata.cn/main/, accessed on 15 September 2023).

3. Results

3.1. Collection Sites of L. imphalum

The field investigations were carried out at 114 survey sites in the five provincial regions of southwest China between 2001 and 2022. The names of 114 survey sites and their abbreviations were listed in “Table 1”. A total of 2161 L. imphalum were collected from 21 of 114 survey sites (Figure 1). Of 21 sites where L. imphalum was collected, 15 sites were distributed in Yunnan Province, 5 sites in the south of Sichuan Province, and 1 site in the southeast of Guizhou Province. There were no L. imphalum collected in the other two provincial regions, Chongqing and Tibet (Table 1, Figure 1).
Table 1. The 114 survey sites and their abbreviations in southwest China (2001–2022).
Table 1. The 114 survey sites and their abbreviations in southwest China (2001–2022).
No.Names of Survey Sites and Their AbbreviationsNo.Names of Survey Sites and Their AbbreviationsNo.Names of Survey Sites and Their Abbreviations
NamesAbbrsNamesAbbrsNamesAbbrs
1An YueAY39Jin ShaJS77Se NiSN1
2Ba YiBY40Jin TangJT78Shan NanSN3
3Bin ChuanBC41Jiu LongJL79Shong ZhongSZ1
4Bo MiBM42Ka RuoKR80Shi ZhuSZ2
5Cang YuanCY1 *43Lang ZhongLZ281Si MaoSM *
6Chang ShouCS44Lan PingLP182Si NanSN2
7Cha YuCY245Le ZhiLZ183Song PanSP
8Da FangDF46Liang HeLH184Sui JiangSJ
9Da LiDL *47Li PingLP285Teng ChongTC
10Dao ChengDC248Long ChuanLC *86Tong NanTN
11Da YingDY149Long LiLL287Tong ZiTZ
12De ChangDC1 *50Lu HuoLH288Wan ZhouWZ
13De QinDQ151Lu LiangLL189Wei NingWN
14Dian JiangDJ52Lu ShuiLS90Wei XiWX *
15Ding QingDQ253Lu XiangLX91Wei YuanWY
16Du YunDY254Ma Er KangMEK92Wen ShanWS2
17Fu ChengFC55Ma GuanMG93Wu ShengWS3
18Fu GongFG56Mang KangMK94Xiang ChengXC
19Fu LingFL57Mei TanMT95Xiang Ge Li LaXGLL
20Fu YuanFY *58Meng HaiMH *96Xi XiuXX
21Gan ZiGZ59Meng LaML3 *97Xuan HanXH
22Geng MaGM *60Meng ZiMZ98Xu ZhouXZ
23Gong Bu Jiang DaGBJD61Mian NingMN99Ya JiangYJ3
24Gong ShanGS62Mi LinML1100Yan BianYB2
25Guan LingGL63Mu YiMY101Yan YuanYY1 *
26Gui DingGD64Mu LiML2 *102Ying JiangYJ2
27He KouHK65Ning ErNE *103Yong DeYD
28Hong YaHY166Ping ChangPC104You YangYY3
29Hong YuanHY267Ping ShanPS105Yuan JiangYJ1 *
30Hua XiHX68Pu AnPA106Yu LongYL *
31Hui DongHD *69Jian WeiJW107Yun YangYY2
32Hui ShuiHS70Qiao JiaQJ108Zhao JueZJ1 *
33Jian ChuanJC *71Qiu BeiQB109Zhen FengZF
34Jiang JinJJ72Ren ShouRS110Zheng AnZA
35Jiang KouJK73Rong JiangRJ *111Zhi JinZJ2
36Jiang YangJY74Rui LiRL *112Zhong ShanZS
37Jing HongJH *75Ruo Er GaiREG113Zhong XianZX
38Jin PingJP76San SuiSS114Zi ZhongZZ
Annotation: The survey sites marked with “*” were the sites where Leptotrombidium imphalum was collected.
Insects 15 00504 g001
Figure 1. The distribution of 114 survey sites and the sites where Leptotrombidium imphalum was collected in southwest China (2001–2022). Annotation: The survey sites marked with blue dots were the sites where Leptotrombidium imphalum was collected.
Figure 1. The distribution of 114 survey sites and the sites where Leptotrombidium imphalum was collected in southwest China (2001–2022). Annotation: The survey sites marked with blue dots were the sites where Leptotrombidium imphalum was collected.
Insects 15 00504 g001

3.2. Hosts of L. imphalum

The 2161 individuals of L. imphalum were identified from 218 small mammal hosts, which belong to 17 species, 13 genera, and 5 families in 3 orders, Rodentia, Eulipotyphla, and Scandentia, in which the dominant host species was the Asian house rat or Oriental house rat, Rattus tanezumi (the constituent ratio Cr = 40.83%, 89/218) in the genus Rattus, family Muridae, and order Rodentia (Table 2). At the order level of hosts, the majority of L. imphalum (Cr = 84.87%, 1834/2161) came from the order Rodentia (rodents), which were the most important hosts of L. imphalum. The number of L. imphalum from the order Eulipotyphla (insectivores) came next with Cr = 14.90% (322/2161), and only five mites (Cr = 0.23%, 5/2161) were identified from the order Scandentia (tree shrews). At the species level of hosts, 49.38% of L. imphalum (Cr = 49.38%, 1067/2161) were identified from R. tanezumi, and “Figure 2” visualized in detail the constituent ratios (Cr) of the identified 2161 L. imphalum among different orders, families, genera, and species of the hosts, 218 small mammals. The infestation indices of L. imphalum varied among different host species, with the highest prevalence (PM = 27.66%), mean abundance (MA = 6 mites/per examined host), and mean intensity (MI = 21.69 mites/per infested host) on the shrew gymnure, Neotetracus sinensis (Table 2) (p < 0.05).

3.3. Infestation Variations of Leptotrombidium imphalum in Different Environments

To analyze infestation variations of L. imphalum on its small mammal hosts in different environments, the survey sites with L. imphalum collected were categorized as different landscapes (mountainous and flatland landscapes), different habitats (indoor and outdoor habitats), and different altitude gradients (500–1000 m, 1001–1500 m, 1501–2000 m, 2001–2500 m, and 2501–3000 m). The results showed that the infestation indices for L. imphalum on small mammal hosts varied in different environments. The differences of the infestation indices along different altitude and latitude gradients were statistically significant (p < 0.05) (Table 3 and Table 4), but those in different landscapes (mountainous and flatland landscapes) and different habitats (indoor and outdoor habitats) were not statistically significant (p > 0.05) (Table 5 and Table 6).

3.4. Spatial Distribution Pattern of L. imphalum

Iwao’s regression model and Taylor’s power law were used to analyze the spatial distribution pattern of L. imphalum among different individuals of its small mammal hosts. The calculated Iwao’s regression formula was M* = 10.44 + 2.88M (R2 = 0.86, p < 0.05), with both α and β (α = 10.44, β = 2.88) exceeding boundary values (0 and 1) for determining the aggregated distribution. The calculated Taylor’s power formula was l g σ 2 = 0.65 + 1.7 l g m (R2 = 0.91, p < 0.05), with both lga and b (lga = 0.65, b = 1.7) also exceeding the boundary values (0 and 1) for determining the aggregated distribution.

3.5. Relationship of Zoonotic Diseases to Prevalence of L. imphalum

Table 7 listed the documented human cases of two zoonotic diseases (scrub typhus and hemorrhagic fever with renal syndrome, HFRS) from Yunnan Province of southwest China between 2007 and 2015 [69,70,71]. The results of the linear regression analysis showed that the infestation prevalence (PM) of L. imphalum on small mammals had high explanatory power for the incidence of scrub typhus (R = 0.93, p < 0.05) but not for the incidence of HFRS (R = 0.8, p > 0.05) (Figure 3).
Table 7. The human cases of scrub typhus and hemorrhagic fever with renal syndrome (HFRS) and the infestation prevalence of L. imphalum on small mammals in Yunnan Province of southwest China (2007–2015).
Table 7. The human cases of scrub typhus and hemorrhagic fever with renal syndrome (HFRS) and the infestation prevalence of L. imphalum on small mammals in Yunnan Province of southwest China (2007–2015).
YearScrub Typhus CasesHFRS CasesPrevalence (PM, %) of L. imphalum
2007365140.06
2008526200.14
20101155150.15
20121884491.48
201531762641.74
Insects 15 00504 g003
Figure 3. Linear correlations between the prevalence of Leptotrombidium imphalum on small mammals and the documented human cases of two zoonotic diseases, scrub typhus (A) and HFRS (B), in Yunnan Province of southwest China (2007–2015). The grey zone is the 95% confidence interval, and the dark line is the linear regression line. (Annotation: (B) in the above figure were those after normal transformation due to the fact that the data did not conform to normal distribution).
Figure 3. Linear correlations between the prevalence of Leptotrombidium imphalum on small mammals and the documented human cases of two zoonotic diseases, scrub typhus (A) and HFRS (B), in Yunnan Province of southwest China (2007–2015). The grey zone is the 95% confidence interval, and the dark line is the linear regression line. (Annotation: (B) in the above figure were those after normal transformation due to the fact that the data did not conform to normal distribution).
Insects 15 00504 g003

3.6. Analysis of Influencing Factors on L. imphalum

Of six environmental factors (temperature, humidity, elevation, precipitation, landscape, and habitat), the determination powers of humidity and temperature (independent variables) to the PM of L. imphalum (dependent variable) reached 69.77% (p < 0.01) and 67.02% (p < 0.01), respectively. The determination power of the mutual interaction of these two factors (humidity and temperature) went up to 96.26% (p < 0.05).

4. Discussion

As mentioned in “Section 1”, the most confirmed vectors of scrub typhus are concentrated in the genus Leptotrombidium, and from this point of view, most chigger species of Leptotrombidium have the potential to transmit the disease, though there has been no direct evidence for many Leptotrombidium species to date [14,20,21,22]. In China, six chigger species in the genus Leptotrombidium are the main vectors of scrub typhus, and they are L. deliense (Walch, 1922); L. scutellare Nagayo et al., 1921; L. rubellum Wang et Liao, 1984; L. wenense Wu et al., 1982; L. insulare Wei et al., 1989; and L. sialkotense Vercammen-Grandjean and Langston, 1976 [8,77,78]. Additionally, L. scutellare has also been identified as a potential vector of hemorrhagic fever with renal syndrome (HFRS) in China [7,8]. Besides the six main vectors of scrub typhus, L. imphalum and some other chigger species (more than ten species) are also important potential vectors of the disease in China [36,79,80,81,82]. Numerous pieces of evidence have demonstrated that L. imphalum can be an effective vector of scrub typhus [27,28,29,30]. For example, the pathogen of scrub typhus (O. tsutusgamushi, Ot) has been isolated from L. imphalum in Yunnan Province of southwest China [30,31]. The transstadial and transovarial transmission of O. tsutusgamushi in L. imphalum have been achieved in the laboratory, and the temporal changes in prevalence of O. tsutsugamushi infecting the eggs of L. imphalum also support the disease transmission efficiency of the mite [27,29,33,34,35,83]. Although L. imphalum is medically important, few studies have involved the distribution, infestation, and related ecology of this vector species on rodents and other small mammal hosts in a vast geographical territory like southwest China. For the first time, this paper reported the distribution and infestation status of L. imphalum on its small mammal hosts in southwest China, an important focus of scrub typhus and HFRS [9,10,11,79,84].
The results of the present study showed that 2161 L. imphalum were identified from 17 species of small mammal hosts in 21 of 114 survey sites in southwest China, and the 17 host species crossed 13 genera and 5 families in 3 orders (Rodentia, Eulipotyphla, and Scandentia), indicating the low host specificity of the mite. Previous studies have demonstrated that most chigger species have low host specificity, which is beneficial to their transmission of scrub typhus among different animal hosts [54,85,86]. The low host specificity of L. imphalum may increase the potential risk of the mite. Although the host specificity of L. imphalum is low, the mite still has a preference for some specific hosts. In the present study, the majority of L. imphalum were identified from rodents (the order Rodentia), indicating that rodents are the main hosts of L. imphalum in southwest China. The infestation indices for L. imphalum varied among different species of small mammal hosts, with the highest PM, MA, and MI on the shrew gymnure, N. sinensis (p < 0.05), indicating that N. sinensis is more susceptible to the infestation of L. imphalum. In the present study, the infestation indices for L. imphalum on small mammal hosts varied along different altitude and latitude gradients (p < 0.05), and this result reveals the environmental heterogeneity of chigger infestations [86,87]. The result of the geographical detector (GD) analysis showed that the determination power of the mutual interaction of temperature and humidity to the infestation prevalence (PM) of L. imphalum on small mammals was as high as 96.26% (p < 0.05). This result suggested that temperature and humidity can significantly influence the infestation of L. imphalum. The results of the present study are consistent with previous studies [51,86,88].
The spatial distribution pattern in the present study refers to the distribution of L. imphalum among different individuals of its small mammal hosts. In ecology, the spatial distribution patterns are usually divided into three types: uniform distribution, random distribution, and aggregated distribution [66,67,68]. The results of the present study revealed that the values of α and β (α = 10.44, β = 2.88) in Iwao’s regression analysis and the values of lga and b (lga = 0.65, b = 1.7) in Taylor’s power law all exceeded the boundary values (0 and 1) for determining the aggregated distribution. Therefore, the spatial distribution pattern of L. imphalum among different individuals of small mammal hosts were determined to be of an aggregated distribution. This aggregated distribution means that chiggers (L. imphalum) are not evenly distributed among different host individuals. Some hosts have few or no chiggers on their body surface, while other hosts have many chiggers, forming a mite colony [89,90,91]. The aggregated distribution of L. imphalum is consistent with previous reports on some other species of chigger mites, and this aggregated distribution pattern may be beneficial to the growth, development, and reproduction of chigger mites and other parasites [53,92,93,94]. The results of the linear regression analysis in the present study showed that the prevalence (PM) of L. imphalum had high explanatory power for the incidence of scrub typhus, with a high positive correlation between the PM of L. imphalum and the human cases of scrub typhus (R = 0.93, p < 0.05), but not for the incidence of HFRS (Figure 3). The results further suggest that L. imphalum is closely related to the prevalence of scrub typhus but not related to that of HFRS. Although L. imphalum has been identified as an important vector of scrub typhus, there has been no evidence showing that it can serve as a vector of HFRS and other zoonotic diseases [26,33,95]. The investigated region (southwest China) of the present study is one of main foci of scrub typhus in China [11,84,96], the positive correlation between the PM of L. imphalum and the human cases of scrub typhus, together with the low host specificity of the mite, may increase the potential risk of the mite’s transmission of scrub typhus in southwest China.

Author Contributions

Conceptualization, resources, validation, writing—review and editing, project administration, funding acquisition and supervision X.-G.G.; supervision and funding acquisition, D.-C.J.; software, data curation, formal analysis, visualization and writing—original draft preparation, Q.-Y.L.; investigation and data curation, R.F. and Y.-F.Z.; methodology, W.-Y.S. and P.-Y.P. All authors have read and agreed to the published version of the manuscript.

Funding

This study was funded by the National Natural Science Foundation of China (No. 82160400) and the Major Science and Technique Programs in Yunnan Province (No. 202102AA310055-X).

Institutional Review Board Statement

The use of animals (including animal euthanasia) for our research was officially approved by the Animals’ Ethics Committee of Dali University, approval code: DLDXLL2020-1104, approval date: 4 November 2020.

Data Availability Statement

The experimental data used to support the findings of this study are available from the corresponding author request.

Acknowledgments

We would like to express our sincere thanks to the following people who contributed to the field investigations and laboratory work: Yun-Ji Zou, Qiao-Hua Wang, Ti-Jun Qian, Wen-Ge Dong, Yu Guo, Peng-Biao Yang, Yong Zhang, Cong-Hua Gao, Nan Zhao, Jian-Chang He, Guo-Li Li, Yan-Liu Li, De-Cai Ouyang, some colleagues and college students. The present study was supported by the National Natural Science Foundation of China (No. 82160400) and the Major Science and Technique Programs in Yunnan Province (No. 202102AA310055-X) to Xian-Guo Guo and the expert workstation for Dao-Chao Jin in Dali Prefecture. We thank them for the above financial support.

Conflicts of Interest

The authors declare no conflicts of interest.

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Insects 15 00504 g002
Figure 2. The visualization of the constituent ratios (Cr) of 2161 chiggers (L. imphalum) among different orders, families, genera, and species of hosts (218 small mammal hosts) in southwest China (2001–2022). Annotation: The shade width indicates the constituent ratio of the chigger L. imphalum on a certain order, family, genus, or species of the host.
Figure 2. The visualization of the constituent ratios (Cr) of 2161 chiggers (L. imphalum) among different orders, families, genera, and species of hosts (218 small mammal hosts) in southwest China (2001–2022). Annotation: The shade width indicates the constituent ratio of the chigger L. imphalum on a certain order, family, genus, or species of the host.
Insects 15 00504 g002
Table 2. The constituent ratios and infestation indices of Leptotrombidium imphalum on different small mammal hosts in southwest China (2001–2022).
Table 2. The constituent ratios and infestation indices of Leptotrombidium imphalum on different small mammal hosts in southwest China (2001–2022).
Host SpeciesNo. of HostsNo. of L. imphalum and Its Constituent Ratio (Cr, %)Infestation Indices of L. imphalum
NumberCr, %Prevalence (PM, %)Mean Abundance (MA)Mean Intensity (MI)
Rattus tanezumi89106749.383.88 *0.46 *11.99 *
Apodemus chevrieri2930814.252.36 *0.25 *10.62 *
Neotetracus sinensis1328213.0527.66 *6 *21.69 *
Other species8750423.321.57 *0.09 *5.79 *
Total2182161100
Annotation: The symbol “*” represents p < 0.05.
Table 3. Infestation variations of Leptotrombidium imphalum on small mammal hosts along different altitude gradients in southwest China (2001–2022).
Table 3. Infestation variations of Leptotrombidium imphalum on small mammal hosts along different altitude gradients in southwest China (2001–2022).
Altitudes Gradients (m)No. of HostsNo. and Constituent Ratios of L. imphalumInfestation Indices of L. imphalum
No.Cr, %PM, %MAMI
500–10007669432.114.68 *0.43 *9.13 *
1001–15004142319.583.92 *0.40 *10.32 *
1501–20005675935.123.06 *0.41 *13.55 *
2001–25004228213.051.20 *0.07 *6.71 *
2501–3000330.140.43 *0.00 *1 *
Total2182161100
Annotation: The confidence intervals are 99.9–100% for the prevalence (PM), 98.8–99.8% for the mean abundance (MA), and 94.1–99.0% for the mean intensity (MI), respectively. The symbol “*” represents p < 0.05.
Table 4. Infestation indices of Leptotrombidium imphalum in different latitude gradients.
Table 4. Infestation indices of Leptotrombidium imphalum in different latitude gradients.
Latitude
(°N)		No. of HostsNo. and Constituent Ratios of Leptotrombidium imphalumInfestation Indices of Leptotrombidium imphalum
NumberCr, %PM, %MAMI
21–22101102347.3410.69 *1.08 *10.13 *
23–2419532.451.04 *0.03 *2.79 *
25–267181437.671.30 *0.15 *11.46 *
27–282727112.541.24 *0.12 *10.04 *
Total2182161100
Annotation: The confidence intervals are 99.9–100% for PM, 98.5–99.7% for MA, and 98.3–100% for MI, respectively. The symbol “*” represents p < 0.05.
Table 5. Infestation indices of Leptotrombidium imphalum in different habitats.
Table 5. Infestation indices of Leptotrombidium imphalum in different habitats.
HabitatsNo. of HostsNo. and Constituent Ratios of Leptotrombidium imphalumInfestation Indices of Leptotrombidium imphalum
NumberCr, %PM, %MAMI
Indoor4100.460.690.022.5
Outdoor214215199.542.150.2210.05
Total2182161100
Annotation: The confidence intervals are 99.0–100% for PM, 97.0–99.5% for MA, and 98.3–100% for MI, respectively.
Table 6. Infestation indices of Leptotrombidium imphalum in different landscapes.
Table 6. Infestation indices of Leptotrombidium imphalum in different landscapes.
LandscapesNo. of HostsNo. and Constituent Ratios of Leptotrombidium imphalumInfestation Indices of Leptotrombidium imphalum
NumberCr, %PM, %MAMI
Mountainous151144566.872.030.199.57
Flatland6771633.132.180.2310.69
Total2182161100
Annotation: The confidence intervals are 99.9–100% for PM, 99.5–99.9% for MA, and 98.3–100% for MI, respectively.
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Liu, Q.-Y.; Fan, R.; Song, W.-Y.; Peng, P.-Y.; Zhao, Y.-F.; Jin, D.-C.; Guo, X.-G. The Distribution and Host-Association of the Vector Chigger Species Leptotrombidium imphalum in Southwest China. Insects 2024, 15, 504. https://doi.org/10.3390/insects15070504

AMA Style

Liu Q-Y, Fan R, Song W-Y, Peng P-Y, Zhao Y-F, Jin D-C, Guo X-G. The Distribution and Host-Association of the Vector Chigger Species Leptotrombidium imphalum in Southwest China. Insects. 2024; 15(7):504. https://doi.org/10.3390/insects15070504

Chicago/Turabian Style

Liu, Qiao-Yi, Rong Fan, Wen-Yu Song, Pei-Ying Peng, Ya-Fei Zhao, Dao-Chao Jin, and Xian-Guo Guo. 2024. "The Distribution and Host-Association of the Vector Chigger Species Leptotrombidium imphalum in Southwest China" Insects 15, no. 7: 504. https://doi.org/10.3390/insects15070504

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