1. Introduction
Chigger mites belong to the families Trombiculidae and Leeuwenhoekiidae in the subclass Acari [
1,
2]. It is estimated that about 3013 species of chigger mites have been recorded worldwide [
3,
4], and over 510 species have been reported in China [
3,
4,
5]. The life cycle of chigger mites is complex, with seven basic stages: the egg, deutovum (prelarva), larva, nymphochrysalis, nymph, imagochrysalis and adult (male and female). The larva (chiggers) is the only ectoparasitic stage in rodents and other animal hosts [
1,
6,
7]. In addition to directly biting humans to cause chigger dermatitis, chiggers are the exclusive vector of scrub typhus (tsutsugamushi disease), which is the most important medical significance of the mites. In addition, some chigger species, e.g.,
Leptotrombidium scutellare (Nagayo, Miyagawa, Mitamura, Tamiya and Tenjin, 1921), can be potential vectors of hemorrhagic fever with renal syndrome, HFRS [
4,
8,
9]. With the spread of scrub typhus worldwide in recent years, the prevalence of the disease in China is also on the rise [
10,
11].
Rodents account for more than 40% of all mammals in the world, and they are widely distributed in different environments [
12,
13]. In addition to being harmful to agriculture and forestry, rodents can also carry a variety of pathogens of some zoonotic diseases such as scrub typhus, leptospirosis, tularemia, HFRS and plague [
3,
12,
13]. South China field mouse (
Apodemus draco Barrett-Hamilton, 1900) and Lantsang field mouse (
A. ilex Thomas, 1922) belong to the genus
Apodemus of the family Muridae in the order Rodentia, and they are two sibling species of mice with similar morphology [
14,
15,
16]. These two sibling rodent species were once regarded as the same species, and
A. ilex was once considered a subspecies of
A. draco [
16,
17,
18]. A series of previous studies on these two mouse species have involved their taxonomic status and morphological characteristics [
14,
15,
19,
20], relative fatness and seasonal changes in digestive tract length [
21,
22], eco-physiology [
23], karyotype [
24,
25] and molecular differentiation [
16,
26], but there is little research literature on their ectoparasites including chiggers [
18,
20]. To date, there have been no specific reports on chiggers of these two sibling mouse species in southwest China.
The southwest China involved in the present paper covers five provincial regions, Yunnan, Guizhou, Sichuan, Chongqing and Tibet (Xizang Autonomous Region), with a vast territory, accounting for 24.5% of China’s land area [
27]. Recent studies have shown that there are obvious differences in the geographical distribution of
A. draco and
A. ilex in southwest China. The former is mainly distributed east of the Jinsha River (roughly equivalent to the east of 101°50′ E), while the latter is mainly distributed west of the Lantsang River (roughly equivalent to the west of 100°45′ E) [
16,
17,
28]. Based on previous field investigations in southwest China from 2001 to 2015, this paper retrospectively studied the species composition, infestation status and some ecological characteristics (community structure and species abundance distribution) of chiggers on these two sibling species of
Apodemus mice for the first time. As an exploration of some unknown scientific issues, this study aims to compare the difference in chigger infestation on these two sibling mouse species, enrich the knowledge of these two mouse species and their ectoparasites, and provide more scientific information for subsequent related research.
4. Discussion
Previously
A. draco and
A. ilex were regarded as the same species, and
A. ilex was once considered a subspecies of
A. draco [
18,
44,
45]. Recent studies have proved that
A. draco and
A. ilex are two independent species of rodents, and they are two sibling species. Although
A. draco and
A. ilex are quite similar in morphology, they still have some differences in morphology, molecular characteristics and geographical distribution areas [
16,
17,
28].
Apodemus draco is mainly distributed in countries and regions such as China, north Myanmar and northeast India. In China,
A. draco is mainly distributed in Yunnan, Tibet and Fujian provincial regions. The distribution range of
A. ilex is narrow and mainly distributed south of the Yangtze River in south China and west of the Lantsang River in southwest China [
16,
17,
28]. The present study revealed that
A. draco and
A. ilex were distributed in southwest China, but they were not the dominant rodent species in this area (only 567
A. draco and 154
A. ilex were captured). The distribution range of two mouse species in southwest China was obviously different.
Apodemus draco was mainly captured east of the Jinsha River, and
A. ilex was mainly captured west of the Lantsang River (
Figure 1). This result is consistent with some previous research reports [
16,
28].
The results of this study showed that
A. draco and
A. ilex were not only obviously different in distribution areas but also different in chigger infestations, including species composition, community structure, infestation status and dominant chigger species. The Jaccard similarity index (
J) used in this study is an index reflecting the similarity of species composition of any two communities. When 0.00 <
J < 0.25, the species composition of two communities is extremely dissimilar, 0.25 ≤
J < 0.50 means moderately dissimilar, 0.50 ≤
J < 0.75 means moderately similar, and 0.75 ≤
J < 1.00 means extremely similar [
46]. The results reveal that the species composition of the chigger community on two sibling species of
Apodemus are very different with
J = 0.12 (
J < 0.25), and the community parameters (
S,
H,
E and
D) are also different. The overall infestation prevalence (
PM), mean abundance (
MA) and mean intensity (
MI) of chiggers on
A. draco are higher than those on
A. ilex. The dominant chigger species on
A. draco are
T. yunnanus,
L. scutellare and
L. sinicum, which are obviously different from the dominant mite species on
A. ilex (
L. rusticum,
L. densipunctatum and
L. gongshanense) (
Table 3). Previous studies have shown that different small mammal species have different susceptibilities to the infestation of ectoparasites, including chiggers, which leads to differences in species composition, infestation status and dominant parasite species on different species of animal hosts [
1,
47]. Chevrier’s field mouse (
A. chevrieri Miline-Edwards, 1868) is a mouse species in the same genus (
Apodemus) as
A. draco and
A. ilex, and it is one of the dominant rodent species in southwest China [
30]. A special study on chiggers of
A. chevrieri in southwest China showed that its overall infestation prevalence (
PM = 31.95%), mean abundance (
MA = 6.32 mites/mouse) and mean intensity (
MI = 19.77 mites/mouse) with chiggers were significantly higher than the corresponding infestation indexes on the two mouse species of
Apodemus in this study. The dominant chigger species on
A. chevrieri are
L. scutellare,
L. densipunctatum and
L. cricethrionis Wen, Sun and Sun, 1984, which are also obviously different from
A. draco and
A. ilex in this study [
30]. The above differences reflect the different susceptibility of different mouse host species to chigger infestation. In this study, there are a series of differences in species composition, infestation status and dominant species composition of chiggers between two mouse species of
Apodemus, which further verify the different susceptibility of different hosts to chiggers and the different preference of chiggers to different hosts. From the aspect of ectoparasites, the differences in species composition, infestation status and dominant species composition of chiggers between two sibling mouse species also support that
A. draco and
A. ilex belong to two independent species [
16,
28]. As one of the dominant chigger species of
A. draco,
L. scutellare is not only the second major vector of scrub typhus in China but also a potential vector of hemorrhagic fever with renal syndrome [
9,
48]. The occurrence of
L. scutellare on the body surface of
A. draco may increase the potential risk of spreading the pathogen of scrub typhus,
Orientia tsutsugamushi, from rodents to humans.
The calculation results of the Jaccard similarity index (
J) showed that the species composition of chiggers on different sexes of two mouse species,
A. draco and
A. ilex, were quite different (
J < 0.5, moderately dissimilar). Besides, the infestation indexes (
PM,
MA,
MI) of chigger on different sexes of two mouse species were also different (
Table 5). These results indicate that there is sex bias in chigger infestation between male and female hosts [
29,
36]. Sex bias is prevalent in parasite infections (including ectoparasite infestations), and many parasites are more likely to choose to parasitize in male hosts [
4,
49,
50], but the preference of chiggers to male hosts is not obvious in this paper (
Table 5), which may need further studies.
In this study, the interspecific relationship between the dominant chigger species on two mouse species was measured by association coefficient (
V). The results showed that the association coefficient (
V) between
L. sinicum and
L. scutellare on
A. draco was close to 0 (
V = 0.09,
V ≈ 0). The
V between
L. rusticum and
L. densipunctatum on
A. ilex was close to 0.5 (
V = 0.49,
V ≈ 0.5). The association coefficient (
V) used in this paper is one of the simple and practicable methods to judge the interspecific relationship between any two species in a certain community. The range of
V is from 0 to positive and negative 1, that is, [1, ±1]. When
V approaches 0, the distribution of the two species is independent of each other. When
V is positive and close to 1, it means that two species have a tendency to coexist in a certain environment or on a certain species of host for parasites. When the
V is negative and close to -1, it means that there is a mutually exclusive relationship between the two species [
5,
40]. This study implies that the distribution of
L. sinicum and
L. scutellare on
A. draco seems independent of each other without obvious interspecific dependency. A low degree of interdependence, however, exists between
L. rusticum and
L. densipunctatum on
A. ilex, and these two chigger species tend to choose the same individuals of
A. ilex at the same time, but the degree of interdependence is still relatively low (
V < 0.5).
The results showed that all the distribution indexes calculated were larger than the critical value (
C > 1,
m* >
m,
I > 1) of determining the aggregated distribution (
Table 1,
Table 8), and this indicates that the dominant chigger species are of aggregated distribution among different individuals of their corresponding mouse host,
A. draco and
A. ilex. This aggregated distribution further indicates that the distribution of dominant chigger species among different individuals of their hosts is very uneven. Some host individuals may harbor a large number of chiggers on their body surface, while some other hosts may have no or only a few chiggers. The aggregated distribution of ectoparasites, including chiggers, suggests that there is an intraspecific relationship of mutual attraction and interdependence between different individuals of the same parasite species. This mutual attraction and interdependence within a certain species are conducive to the survival, mating and reproduction of the population [
5,
51].
The species abundance distribution aims to reveal the relationship between the number of species and the number of individuals in a community, which reflects the proportion structure of common and rare species in the community [
33,
42,
43]. In the present study, the species abundance distribution of the chigger community on
A. draco was successfully fitted by Preston’s lognormal model, which shows that most chigger species are rare species with few individuals, while few mite species are dominant species with abundant individuals. With the increase of chigger individuals, the number of chigger species gradually decreased (
Table 9,
Figure 6). The result is consistent with some previous reports on the species abundance of chiggers [
36,
43]. Due to the small number of individuals and species of chiggers and mice collected, however, Preston’s lognormal model is not applicable to the chigger community on
A. ilex. In ecological practice, if the species abundance distribution of a specific community is successfully fitted by Preston’s log-normal distribution model, the number of expected total species in the community can be roughly estimated, but this estimation must be based on a large number of samples [
52]. Due to the small number of host samples (only 567
A. draco and 154
A. ilex captured) and a small number of chiggers (total 290), the total number of chigger species was not estimated in this paper, which remains to be conducted in further studies.
It must be pointed out that the present study is just a preliminary comparison of chiggers on two sibling mouse species due to the small number of host samples, especially A. ilex, and some results may still be unstable. With the expansion of survey areas and the increase of host samples in future research, some results may fluctuate and change to some extent.