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Keywords:

  • chigger;
  • exotic species;
  • host-parasite interactions;
  • human health;
  • Orientia tsutsugamushi;
  • Taiwan

Summary

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

1. The role and influence of exotic species in indigenous vector-borne diseases are important but remain understudied. Ascertaining whether disease vectors prefer exotic vs. native hosts has important implications for human health. Moreover, evaluating whether exotic hosts are intrinsically less susceptible to vectors, or whether vector loads can vary with environment, is instructive for possible disease dynamics in the face of range expansion of exotic species. Rattus exulans has recently been recorded for the first time in eastern Taiwan, where scrub typhus is prevalent. We assessed the role of R. exulans as a host for chiggers (larval trombiculid mites), and the degree to which vector loads of R. exulans exhibited spatial variation.

2. We deployed live traps in two villages in Taiwan that differed in human population density and in the incidence of scrub typhus. We recovered and tallied chiggers from small mammals, and identified over one-fifth of chiggers from each host to species. Chiggers were assayed for Orientia tsutsugamushi (OT) infection with nested-PCR.

3.R. exulans was the most common small mammal species captured (31·4% total captures), and supported about one-fifth of total chiggers recovered. Leptotrombidium imphalum dominated the chigger assemblage of most native species (>90%), but Gahrliepia spp. was commonly found in R. exulans (39·1%). We detected OT in the genus Leptotrombidium (39%) but not in the Gahrliepia. Prevalence and loads of chiggers in R. exulans were about 5× and 17× higher, respectively, in the less densely populated village; a similar trend also occurred with native R. losea.

4.Synthesis and applications. Currently, R. exulans appears to play a relatively minor role in supporting chiggers. However, the fact that both prevalence and loads of chiggers in R. exulans vary greatly with environment, along with the abundance of most exotic species and the ecological flexibility of R. exulans, implies a potential health risk as this species expands to areas with more chiggers. Our study suggests that a clearer understanding of interactions among native and exotic hosts and native parasite species can facilitate prediction of the impact of exotic hosts on the dynamics of vector-borne diseases.


Introduction

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

It has been well documented that exotic species can introduce wildlife diseases. For example, the significant decline of the endemic Hawaiian avifauna is partially attributable to the introduction of avian malaria and avian pox by exotic birds and their transmission by introduced mosquitoes (Warner 1969). Similarly, rinderpest virus in imported cattle killed a huge proportion of native artiodactyls in Africa (Plowright 1982). Reduction of native red squirrels Sciurus vulgaris followed by the introduction of eastern gray squirrels S. carolinensis in Britain and Europe likely is related to the more pathogenic effects of parapox virus on red squirrels (Tompkins, White & Boots 2003). Dobson & Foufopoulos (2001) reviewed recent emerging and re-emerging wildlife diseases in North America and reported that the majority of diseases are exotic or likely of exotic origin. Examples include West Nile virus, bovine tuberculosis, and avian pox, but many others exist.

Exotic species may also influence the dynamics of indigenous diseases via their interaction with native hosts, vectors, or pathogens. For instance, the introduction of bank voles Clethrionomys glareolus, a less competent host for the indigenous pathogen Bartonella, reduced disease prevalence in native wood mice Apodemus sylvaticus (Telfer et al. 2005); in contrast, an exotic snail Pomacea canaliculata in China is very susceptible to an indigenous nematode Angiostrongylus cantonensis and has led to outbreaks of a human brain disease caused by the nematode (Wang, Chen & Lun 2007). Although rarely studied, the influence of introduced species on indigenous vector-borne diseases, especially those impacting humans, is critical in the face of ongoing expansion of exotic species, because human diseases may increase if native vectors can exploit exotic hosts.

The further impact of expanding exotic species on disease vectors can be appraised by determining whether exotic hosts are intrinsically less susceptible to vectors, or if vector loads are determined by the environment. Under the former scenario, vectors may not increase with introduction of exotic hosts. Alternatively, if the impact of introduced species is context-dependent, then exotics could be a major concern for human health if they were able to expand into areas with prolific vectors. This is especially risky due to the abundance of most exotic species.

The Pacific rat Rattus exulans Peale is widely distributed in Southeast Asia and Pacific islands, and this species was first recorded in Taiwan in 1999 (Motokawa et al. 2001), although only in Ji-an village of Hua-lien County in eastern Taiwan (Chu et al. 2007). The distribution of this exotic species is expanding southward, and by 2005 it had reached Shou-feng village, located across the Mu-gua River (Fig. 1; C.-C. Kuo, unpublished data). Elsewhere, R. exulans is a major threat to seabirds (Jones et al. 2008), and has had devastating effects in introduced regions, especially on islands (Courchamp, Chapuis & Pascal 2003; Towns, Atkinson and Daugherty 2006; Athens 2009). The introduction of R. exulans may also pose human health concerns because they can host plague as well as murine typhus and scrub typhus (Audy & Harrison 1951; Walton et al. 1980; Wodzicki & Taylor 1984). In Taiwan, the seropositivity rates of Hantavirus in R. exulans were higher than other native rodents (Wang 2004).

image

Figure 1.  Location of study plots in Ji-an and Shou-feng villages in eastern Taiwan between 2007 and 2008. Plots where Pacific rats Rattus exulans were absent or present are indicated by circle symbol shading. Also shown are plots beyond the Pacific rat invasion that should be re-sampled once R. exulans expands to this area.

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Scrub typhus, vectored by larval trombiculid mites (i.e. chiggers) harbouring the rickettsia Orientia tsutsugamushi (OT), is an acute, febrile human infectious disease prevalent in the West Pacific, South Asia, and northeast Australia, where about one million cases occur annually, and one billion people are at risk. The symptoms of scrub typhus include fever, headache, and rash and fatality rate can be as high as 50% if not treated appropriately (Kawamura, Tanaka & Takamura 1995; Coleman et al. 2003; Lu et al. 2010). The life cycle of trombiculid mites includes seven stages: egg, deutovum, larva (chigger), protonymph, deutonymph, tritonymph and adult. Only chiggers are parasitic. Nymphs and adults are free living in the soil, feeding mainly on the eggs and larvae of arthropods (Kawamura, Tanaka & Takamura 1995). Leptotrombidium chiggers are the primary vectors, and murine rodents, especially Rattus species, are the predominant hosts of chiggers in regions with endemic scrub typhus (Traub & Wisseman Jr. 1974; Kawamura, Tanaka & Takamura 1995). Humans are accidental hosts, and get infected with scrub typhus when bitten by chiggers infected with OT. Trombiculid mites are the only reservoirs of OT, which can be transmitted transstadially (from larva to nymph to adult) and transovarially (from female to next generations), while vertebrate hosts provide chiggers with food resources but play little roles in transmitting OT (Kawamura, Tanaka & Takamura 1995).

Although one of Taiwan’s least populated counties, Hua-lien County had the country’s highest number of human cases of scrub typhus between 1998 and 2007, except for one offshore islet (Taiwan Centers for Disease Control 2008), and scrub typhus has been endemic there for at least 95 years (Hatori 1919). The introduction of R. exulans to Hua-lien County provides a good opportunity to examine its possible impact on this indigenous human disease. We evaluated the relative role of several small mammal species as hosts of chiggers in Hua-lien, where apart from R. exulans and the rare Rattus argentiventer, and possibly Bandicota indica, all small mammals are native to this region (Lin 1980; Motokawa et al. 2001; Chen 2008). In the study, hosts were defined solely as providers of food resource, without any implication of being reservoirs of disease. We also evaluated whether prevalence and loads of chiggers in R. exulans increased significantly when this exotic species expanded into areas with more abundant chiggers.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Study area

The study was implemented in the lowlands of Ji-an and Shou-feng villages (Fig. 1) in Hua-lien County of eastern Taiwan, where agriculture dominates land use and villages are interspersed among fields. Ji-an is adjacent to the largest city (Hua-lien City) in Hua-lien County, and is much more densely populated (1211 people km−2) than Shou-feng (88 people km−2) (http://web.hl.gov.tw/static/). Between 1998 and 2006, the incidence of scrub typhus in Shou-feng was over twice that in Ji-an (1·45 vs. 0·67 cases/1000 people per year) (Kuo 2010).

Small mammal trapping and collection of chiggers

We surveyed abandoned agricultural fields from January 2007 to March 2007 (as a preliminary study), and from August 2007 to March 2008 [covering periods with the lowest and the highest number of cases of scrub typhus in humans (Lee et al. 2006)]. In the former period, each field was sampled with two parallel transect lines containing 10 Sherman traps (26·5 × 10 × 8·5 cm) at 10-m intervals, and two hand-made live traps (27 × 16 × 13 cm) at 50-m intervals. Hand-made traps were used to target the larger but less abundant B. indica. Adjacent transect lines were separated by 10 m. After August 2007, we added a third hand-made live trap to each transect line and placed these at 30-m intervals. We used between one and three parallel transect lines in each field in accordance with field size. Because R. exulans remains limited in distribution, some sampling fields were only 50 m apart and some fields were surveyed two to three times to increase R. exulans captures (to avoid concerns over independence, data were pooled across fields for each village; see ‘Data analysis’). Traps were opened and baited in the evening and checked for captures early in the morning. Fields were surveyed for three consecutive nights. Ji-an and Shou-feng were both surveyed in each trapping bout.

Trapped small mammals (rodents and shrews) were transferred to a clean nylon mesh bag which was carefully examined beforehand to ensure that no arthropod vectors remained from earlier captures. Rodents were anesthetized with Zoletil 50 (Fa. Virbac. Carros, France) and examined for gender and reproductive status. We also recorded body weight (g) and length of body, tail, ear and hind-foot (mm). Rodents were thoroughly examined for ectoparasites by carefully combing their fur. Skin with attached chiggers was detached with minimal injury to the animals and preserved in vials; chiggers detached from these skin samples were transferred to 70% ethanol after 2 days, and subsequently tallied. Blood was collected directly by heart puncture for R. exulans and R. argentiventer, whereas for native species we sampled blood either from the submandibular area (small native rodents) or the saphenous vein. Sera was retrieved after centrifugation and stored at −70 °C for later determination. Exotic rodent species were then humanely euthanized. Other rodents were fur clipped and released ≥5 km away from the study areas. Shrews were screened for ectoparasite infestation. Those infested with chiggers were euthanized with an overdose of Zoletil 50, and blood collected from their hearts. Those without ectoparasites were marked with fur clips and released outside the study areas without collecting blood. All procedures were approved by the University of California, Davis Animal Use and Care Administrative Advisory Committee, and met guidelines recommended by the American Society of Mammalogists (Gannon, Sikes and the Animal Care and Use Committee of the American Society of Mammalogists 2007).

Chigger identification

For each individual host, at least one-fifth of parasitized chiggers were randomly selected for species identification. Chiggers were soaked for 2–3 30-min periods in deionized water and then slide-mounted in Berlese fluids (Asco Laboratories, Manchester, UK). Chiggers were examined under a light microscope and identified with published keys (Wang & Yu 1992; Li, Wang & Chen 1997).

Orientia tsutsugamushi detection in chiggers

We detected OT in chiggers of the genera Leptotrombidium and Gahrliepia (see Results) with nested PCR. To retrieve enough DNA, PCR was performed on pools of 30 chiggers each of the same genus. Chiggers were grouped into genera because further classification (i.e. to species) would require the use of Berlese fluids, which destroys DNA material. Chiggers of the same pool were recovered from the same host, except from R. exulans or Apodemus agrarius, where some individuals were infested with <30 chiggers. In those cases, chiggers were pooled from different rodent hosts of the same species. This should not pose any problem because rodents do not play any role in the transmission of OT (Kawamura, Tanaka & Takamura 1995), and our main purpose was to examine whether Gahrliepia, commonly found in R. exulans, was also infective of OT (see below).

We modified the method of Kawamori et al. (1993) in the detection of OT in chiggers. This method targeted a well conserved DNA corresponding to 56-kDa type-specific antigen located on the OT outer membrane. Primers 5′-AGAATCTGCTCGCTTGGATCCA-3′ and 5′-ACCCT ATAGTCAATACCAGCACAA-3′ were applied for the first step PCR, while primers 5′-GAGCAG AGATAGGTGTTATGTA-3′ and 5′-TATTCATTATAGTAGGCTGA-3′ were used in the second stage PCR. The positive PCR products were separated by electrophoresis in 1·5% agarose gels, stained with ethidium bromide, and identified under UV fluorescence. Laboratory Karp and Gilliam strains and deionized water were used as positive and negative controls respectively.

Data analysis

We tested differences in trapping success and prevalence of chiggers for each host species between the two villages using Pearson’s chi-square test with Yates’ correction for continuity. Because some fields could not be considered valid replicates due to their proximity, we pooled data across fields within each village (e.g. analytical sample size was = 2 villages). Data are presented as percentages, but chi-square tests were based on raw data. When comparing chigger loads for each host species between villages, host individuals were treated as independent units. We confirmed normality and homogeneity of variance with Shapiro–Wilk and Levene tests, respectively; data were transformed if necessary. We used a t-test when both assumptions were met and a non-parametric Mann–Whitney U-test otherwise. All procedures were implemented in spss 16.0 (SPSS Inc., Chicago, IL, USA).

Results

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Small mammal trapping

We trapped small mammals in 79 fields (6249 trap-nights): 31 fields were surveyed from January to March 2007 (2232 trap-nights), and 69 fields from August 2007 to March 2008 (4017 trap-nights). Nine fields were sampled in both periods, and 12 fields were surveyed twice within the second period. We captured 1597 individual small mammals (706 in the first time period, 891 in the second) belonging to 10 species (three shrew and seven rodent species). The most commonly captured species was the exotic R. exulans (31·4% of total captures), followed by the natives Suncus murinus (23·9%) and Mus caroli (21·2%). Rattus argentiventer, the other exotic species, constituted only 0·2% of total captures (Table 1).

Table 1.   Prevalence and loads of chiggers (larval trombiculid mites) among small mammal hosts trapped from January to March 2007, and from August 2007 to March 2008 in Hua-lien, eastern Taiwan
Host speciesNo. of captures (% of all)Prevalence (%) of chiggersChigger loadsTotal chiggers recovered (% of all)
Apodemus agrarius149 (9·3)6113·41990 (8·9)
Bandicota indica23 (1·4)4370·51621 (7·2)
Crocidura attenuata1 (0·1)10055 (0·02)
Crocidura suaveolens1 (0·1)1001616 (0·1)
Mus caroli339 (21·2)000 (0)
Mus musculus124 (7·8)30·112 (0·1)
Rattus argentiventer3 (0·2)1002678 (0·4)
Rattus exulans502 (31·4)319·54747 (21·1)
Rattus losea74 (4·6)68189·113 994 (62·2)
Suncus murinus381 (23·9)10·120 (0·1)
Total15972014·122 483

Prevalence and loads of chiggers among small mammal hosts

A total of 22 483 chiggers were recovered. Prevalence was greatest in Rattus losea (68%), followed by A. agrarius (61%) and B. indica (43%). Rattus exulans had moderate prevalence (31%) (Table 1).

Mean chigger loads were much higher in R. losea (189·1) and B. indica (70·5) than other species. Apodemus agrarius (13·4) and R. exulans (9·5) had intermediate chigger loads, whereas the other three common species (M. caroli, Mus musculus and S. murinus) supported very few chiggers (Table 1).

We calculated total chiggers, the product of mean chigger loads and total captures for a given host species, to represent the number of chiggers supported by each host species. Rattus losea sustained the most chiggers (62·2% of all chiggers recovered). In spite of its moderate chigger loads, the abundance of R. exulans resulted in moderately high chigger populations (21·1%), followed by A. agrarius (8·9%) and B. indica (7·2%). Other species altogether sustained <1% of total chiggers (Table 1).

Composition of chiggers among small mammal hosts

We identified approximately one-third of the chiggers recovered in this study (7111 chiggers = 31·6%). Of these, 839 (11·8% of identified) were excluded because they could not be keyed to species (but were identified to be Leptotrombidium spp.) due to unsuitable position for keying when mounted on the slides. Of the remaining 6272 chiggers, Leptotrombidium imphalum dominated the assemblage (83·9%), followed by Gahrliepia spp. (10·8%). The remaining 5·3% comprised small proportions of L. deliense, Walchia spp. and other species of Leptotrombidium (Table 2).

Table 2.   Species composition of chiggers (%) among small mammal hosts trapped from January to March 2007, and from August 2007 to March 2008 in Hua-lien, eastern Taiwan
Host speciesChigger species composition (%) within each host speciesNo. chiggers identified
Leptotrombidium imphalumLeptotrombidium delienseLeptotrombidium othersWalchia sp.Gahrliepia sp.
Apodemus agrarius94·63·61·600799
Bandicota indica96·61·70·90·90351
Crocidura attenuata33·366·70003
Crocidura suaveolens10000009
Mus musculus001000010
Rattus argentiventer97·22·800036
Rattus exulans52·31·31·36·039·11573
Rattus losea94·51·91·00·91·83479
Suncus murinus91·78·300012
Total83·92·01·32·010·86272

Most host species were infested mainly by L. imphalum (>90·0%), except R. exulans, M. musculus and Crocidura attenuata (Table 2). The latter two species, as well as Crocidura suaveolens and S. murinus warrant further study as we were unable to obtain sufficient chiggers from these species for further assessment. Chiggers recovered from R. exulans comprised mostly L. imphalum (52·3%), followed by Gahrliepia spp. (39·1%) (Table 2).

Prevalence of OT among chiggers

Due to the low chigger loads in the most commonly found host species (Table 1), only 80 pools of chiggers were examined for OT infection. We detected OT in the Leptotrombidium spp. (39%, = 65) recovered from B. indica (80%, = 5), A. agrarius (61%, = 18), R. losea (28%, = 25) and R. exulans (18%, = 17). OT was not found in the genus Gahrliepia (0%, = 15) recovered from R. exulans.

A comparison of prevalence and loads of chiggers among small mammal hosts in JI-an vs. Shou-feng

We surveyed 23 plots (1932 trap-nights) in Ji-an, and 56 plots (4317 trap-nights) in Shou-feng. R. exulans was the most common species in Ji-an (41·8%), followed by S. murinus (24·4%) and M. musculus (22·2%) (Table 3). R. exulans was also the most abundant species in Shou-feng (28·5%), followed by M. caroli (24·9%) and S. murinus (23·7%) (Table 3). Trapping success (captures/trap-nights) was approximately 50% greater in Shou-feng (28·8%) than in Ji-an (18·2%)(chi-square test with Yates’ correction, χ2 = 78·56, < 0·001), but trapping success of R. exulans was similar in both villages (Ji-an: 7·6%; Shou-feng: 8·2%; χ2 = 0·60, = 0·44).

Table 3.   Total captures and relative abundance of each small mammal host species in Ji-an and Shou-feng villages from January to March 2007, and from August 2007 to March 2008 in Hua-lien, eastern Taiwan
Host speciesJi-anShou-feng
No. of capturesRelative abundance (%)No. of capturesRelative abundance (%)
Apodemus agrarius0014912·0
Bandicota indica30·9201·6
Crocidura attenuata0010·1
Crocidura suaveolens0010·1
Mus caroli298·231024·9
Mus musculus7822·2463·7
Rattus argentiventer0030·2
Rattus exulans14741·835528·5
Rattus losea92·6655·2
Suncus murinus8624·429523·7
Total3521245
Total trap-nights19324317

Six small mammal species occurred in both villages. Chigger prevalence was greater in Shou-feng for all host species except M. musculus (Ji-an: 4%; Shou-feng: 2%) and M. caroli (0% for both villages) (Fig. 2a). Prevalence of chiggers on R. exulans in Shou-feng was nearly 5× that in Ji-an (χ2 = 50·15, < 0·001), and that on R. losea was >2× greater in Shou-feng (χ2 = 3·85, = 0·05). The other four species did not differ in prevalence between these villages (Fig. 2a).

image

Figure 2.  Comparison of prevalence (a) and loads (b) of chiggers in small mammal host species between Ji-an and Shou-feng villages. Statistical results are from Chi-square contingency tests (a) and Mann–Whitney U-test (b). Notice that the y-axis in (b) is a logarithmic scale.

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Chigger loads also were higher in Shou-feng, with the exception of M. caroli (0 for both villages). Chigger loads in R. exulans were >17× higher in Shou-feng than Ji-an (Mann–Whitney U-test, U = 17303, Z = −7·23, < 0·001), and those in R. losea were 11× higher in Shou-feng (U = 132·5, Z = −2·69, = 0·007). Chigger loads in the other four species did not differ between the two villages (Fig. 2b). Total chiggers recovered from all small mammals were much higher in Shou-feng (22 191) than in Ji-an (292); after correcting for differential trapping effort, total chiggers recovered in Shou-feng were nearly 34 times those in Ji-an.

Discussion

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The exotic R. exulans was the most abundant small mammal in our study sites, but it played a relatively minor role in supporting chigger populations, contributing to about one-fifth of total chiggers recovered. Moreover, about 40% of chiggers recovered from this species belonged to Gahrliepia spp. in which OT was not detected, indicating that R. exulans may support a lower proportion of chiggers that could potentially transmit OT to humans. Rattus argentiventer, the other recently introduced species, sustained very few chiggers (0·35% of total chiggers) due to its rare occurrence. In contrast, the native R. losea was not common (<5% of total captures), but was by far the dominant host for chiggers (62·24% total chiggers). It is still not clear whether the introduction of R. exulans has replaced or even facilitated other native species which also host chiggers. These data suggest that, currently, the presence of R. exulans is not likely to increase greatly the susceptibility of local residents to scrub typhus.

Some rodent species in our study appear intrinsically less susceptible to chiggers (M. caroli and M. musculus), exhibiting similarly low prevalence and loads in both study regions. This may be due to their smaller body size (both <15 g) and less amount of energy reserve, thus less tolerant of vector infestation (Hart et al. 1992; Olubayo et al. 1993). In contrast, the prevalence and loads of chiggers in R. exulans (mean body weight >30 g) were very different in Shou-Feng and Ji-an (5× and 17× higher, respectively, in the former), supporting the hypothesis that prevalence and loads can greatly increase in response to local conditions. Such significant variation despite similar population density (trapping success) of R. exulans at both villages suggests that the degree of chigger infestation could be determined by the environment (or other native mammals, or both), although the inefficiency of sampling free-living chiggers in Taiwan (Wang et al. 2005) precluded us from comparing populations of host-seeking chiggers at these two areas. However, even after correcting for differential trapping effort, the total number of chiggers recovered from small mammals in Shou-feng was nearly 34× than in Ji-an. Rodents in abandoned fields harboured many more chiggers than those in frequently disturbed fields (Kuo 2010), so one explanation for the difference in chigger abundance between Shou-feng and Ji-an could be the much lower human density and associated disturbance at the former, although this is confounded by the higher small mammal abundances there. Because both prevalence and loads of chiggers in R. exulans can vary with local conditions, monitoring the expansion of R. exulans and its subsequent influence on chigger abundance and human incidence of scrub typhus is imperative.

For comparative purposes, we trapped small mammals and collected chiggers in regions ahead of the R. exulans invasion front (Fig. 1), using identical sampling and during the same time period as this study (Kuo 2010). In areas where R. exulans had not yet invaded, A. agrarius was the dominant host of chiggers (47·8% of total chiggers recovered), followed by R. losea (40·8%). Prevalence and loads of chiggers in A. agrarius were much lower in Shou-feng than in the area beyond the invasion front (prevalence: 61% vs. 97%; loads: 13·4 vs. 105·3). Similar trends were observed for R. losea (prevalence: 72% vs. 100%; loads: 212·6 vs. 544·1) and B. indica (prevalence: 50% vs. 90%; loads: 81·1 vs. 288·1) (Kuo 2010). Together with the variable susceptibility of R. exulans to chiggers, we expect that if this rodent can expand into and maintain high population density in this region, its presence may significantly increase the total number of chiggers. In southeast Asia and Pacific islands, R. exulans occurs in houses, plantations, grasslands, and forest, but rarely in virgin rainforest (Audy & Harrison 1951; Williams 1973; Roberts & Craig 1990). Almost all of lowland Hua-lien has been converted for human use. It is thus likely that R. exulans will expand further within this region. However, the outcome of expansion of R. exulans on chigger populations will also depend on the responses of native species, especially the main hosts of chiggers (A. agrarius and R. losea). Our study provides valuable baseline data for investigating the response of chiggers and native small mammal species to the ongoing expansion of R. exulans.

The prevalence and loads of chiggers were lower in R. exulans than in some native small mammal species (R. losea, B. indica and A. agrarius), but higher than others (M. caroli, M. musculus and S. murinus). Given these observations, it seems that inferences about the susceptibility of exotic hosts that have been extrapolated from species-poor systems (normally 1–2 species; e.g. Malmstrom et al. 2005; Telfer et al. 2005; Georgiev et al. 2007) may yield an overly simplistic view of the role of exotics within more diverse assemblages. This further suggests that the influence of exotic species on indigenous disease dynamics is context-dependent. When exotics invade areas with highly susceptible native host species, their impact on disease dynamics may be negligible, or even negative if they suppress native host populations. On the contrary, vectors and diseases may be amplified if the invasive species is a viable host for the vectors and the indigenous community is mostly less susceptible. Consequently, predicting whether a vector-borne disease will emerge after the introduction of a new species requires an understanding of host–parasite interactions in the native communities, as well as of the extent to which native parasites can exploit exotic hosts.

Many studies have documented the health risks that exotic species can pose to humans. Introduced Norway rats Rattus norvegicus and black rats (Rattus rattus) are reservoirs of plague in Madagascar (Chanteau et al. 1998). Hantavirus has been isolated from introduced R. norvegicus in Korea and Brazil (Lee, Baek & Johnson 1982; LeDuc et al. 1985). Rickettsia felis, which is pathogenic to humans, has been retrieved from fleas on exotic house mice Mus musculus in Hawaii (Eremeeva et al. 2008). Our study adds R. exulans to the list of exotic species potentially impacting human health. More importantly, similar studies have been implemented primarily from the perspectives of public health, leaving underlying ecological processes poorly evaluated and possible disease dynamics underappreciated. Our study demonstrates that the impact of exotic species on human diseases may be contingent on local conditions. A better understanding of the interactions between exotic species and disease vectors will help to predict the emergence of vector-borne disease. Given the pace of species introductions globally, this knowledge will be crucial for successful management and control.

Acknowledgements

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

We thank HY Wu and her students for logistical support during the field work. DA Kelt, JE Foley, and DH Van Vuren provided constructive comments on this manuscript. This study would not have been possible without the financial support by Taiwan Centers for Disease Control (DOH96-DC-2019). C.-C. Kuo was also financially supported by the University of California, Davis, the Pacific Rim Research Program and the American Society of Mammalogists.

References

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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