Analysis of gamasid (: ) associated with the Asian house rat, Rattus tanezumi (Rodentia: Muridae) in Yunnan Province, Southwest China Li-Qin Huang, Xian-Guo Guo, John R. Speakman & Wen-Ge Dong

Parasitology Research Founded as Zeitschrift für Parasitenkunde

ISSN 0932-0113 Volume 112 Number 5

Parasitol Res (2013) 112:1967-1972 DOI 10.1007/s00436-013-3354-y

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Parasitol Res (2013) 112:1967–1972 DOI 10.1007/s00436-013-3354-y

ORIGINAL PAPER

Analysis of gamasid mites (Acari: Mesostigmata) associated with the Asian house rat, Rattus tanezumi (Rodentia: Muridae) in Yunnan Province, Southwest China

Li-Qin Huang & Xian-Guo Guo & John R. Speakman & Wen-Ge Dong

Received: 14 June 2012 /Accepted: 14 February 2013 /Published online: 8 March 2013 # Springer-Verlag Berlin Heidelberg 2013

Abstract During a survey lasting from 1990 to 2008, we rats trapped indoors. The parameter K from the negative captured 4,113 Asian house rats, Rattus tanezumi Temminck binomial distribution was used to measure the spatial distri- 1844 (Rodentia: Muridae) from 28 counties of Yunnan bution patterns of the dominant species and revealed Province in Southwestern China. From these rats, a total that all the mites had an aggregated distribution among the of 19,304 gamasid mites (Acari: Mesostigmata) were col- rat hosts. Most mite species showed a predominantly lected and identified as comprising 50 different species. The female-biased population structure with many more females species diversity of gamasid mites from this single rat spe- than males. cies is higher than that reported previously from multiple hosts within a given geographical region. Of the 50 mite species, 31 species belonged to ectoparasites and 19 species belonged to free-living mites. The species diversity of the Introduction mites from rats trapped outdoors was much higher than from Gamasid mites (mesostigmatid mites) belong to the order : : (or suborder) Mesostigmata, subclass Acari in class L.-Q. Huang X.-G. Guo (*) W.-G. Dong Arachnida (Pan and Deng 1980; Deng et al. 1993). Some Vector Laboratory, Institute of Pathogens and Vectors, gamasid mites are ectoparasites while others are predatory Dali University (Branch of Key Laboratory ’ for Preventing and Controlling Plague of mites, nidicolous mites, or edaphic mites found in the hosts Yunnan Province), Dali, Yunnan 671000, China nests, soil, litter, and humus (Pan and Deng 1980; Radovsky e-mail: [email protected] 1985; Walter and Lindquist 1989; Skorupski and Luxton L.-Q. Huang 1998). Small mammals (especially rodents) are the most e-mail: [email protected] common hosts for ectoparasitic gamasid mites (Deng et al. W.-G. Dong 1993; Baker et al. 1956). Besides causing such disorders as e-mail: [email protected] mite dermatitis (Alexander 1984; Chung et al. 1998; Rosen et al. 2002; Heukelbach et al. 2005), some species of ecto- L.-Q. Huang School of Life and Medical Sciences, Xinyu University, Xinyu, parasitic gamasid mites are the transmitting vectors of Jiangxi 338004, China rickettsialpox and hemorrhagic fever with renal syndrome (HFRS) (Deng et al. 1993; Younis et al. 1995;Song1999; J. R. Speakman Huang and Guo 2010). Located in Southwestern China, Institute of Biological and Environmental Sciences, University of Aberdeen, Zoology Building, Tillydrone Avenue, Yunnan Province is an important focus of some zoonoses Aberdeen AB24 2TZ Scotland, UK and vector-borne diseases including HFRS. There have been e-mail: [email protected] several previous scientific papers concerning the species di- versity, host specificity, spatial pattern, and community simi- J. R. Speakman Institute of Genetics and Developmental Biology, Chinese larity of gamasid mites (Guo 1997, 1998,1999a, b;Korneev Academy of Sciences, Beijing, China 2002; Martins-Hatano et al. 2002; Korallo et al. 2007; Luo et Author's personal copy

1968 Parasitol Res (2013) 112:1967–1972 al. 2007; Vinarski et al. 2007), but few studies have and other instruments were cleaned with disposable paper addressed the gamasid mites associated with a single towels to reduce the chance of cross-contamination. species of rodents. Asian house rats, Rattus tanezumi According to the external morphology, measurements, Temminck 1844 (Muridae), (also called Rattus flavipectus and visible characters of dentition, each rat was identi- Milne-Edwards 1871 in some literature), is widely distrib- fied, and some inconclusive specimens were confirmed uted in Asian countries (Guo et al. 2000; Tobin and Fall by postmortem examination of skull (Huang et al. 1995; 2004; Wilson and Reeder 2005). This species is an agri- Guo 1999a, b). cultural pest that is abundant in Yunnan. Moreover, it is In the laboratory, the collected gamasid mites were an important infectious source and reservoir host of made into glass slide specimens before identification. plague, murine typhus (endemic typhus), scrub typhus Most small and soft mites were rinsed with clean water (tsutsugamushi disease), HFRS, and some other zoonoses to remove the ethanol and mounted on glass slides with (Singleton 2003; Singleton et al. 2004; Plyusnina et al. Hoyer’s medium (Pan and Deng 1980; Deng et al. 1993; 2009; Jonsson et al. 2010). The ectoparasites (including Guo 1997, 1999a, b). Some large and hard mites were ectoparasitic gamasid mites) on the rat are often associated mounted with abienic balsam after digestion, dehydration, with the preservation and transmission of plague, HFRS, and transparency processing (Pan and Deng 1980; Deng and some other zoonoses (He et al. 1997; Guo et al. et al. 1993; Luo et al. 2007). All the mounted mite 2000; Yin et al. 2011). Therefore, it is of importance to specimens were finally identified to species by microsco- study the ectoparasites (including ectoparasitic gamasid py (Pan and Deng 1980;Dengetal.1993). Voucher mites) found on the Asian house rat. Based on former mites and representative rats are deposited in the speci- investigations from Yunnan (Guo 1997, 1998,1999a, b; men repository of the Institute of Pathogens and Vectors, Guo and Qian 2001; Luo et al. 2007; Huang et al. 2010), Dali University, China. the current paper reports the species composition, species Some commonly used indices were calculated for each diversity, and dominant species of gamasid mites on R. mite species, including constituent ratio (Cr), infestation tanezumi in different types of habitat, and includes an prevalence (P), infestation mean abundance (MA), and in- analysis of the spatial distribution pattern and sex structure festation mean intensity (MI) (Margolis et al. 1982; of the dominant mite species. Whitaker 1988; Bush et al. 1997; Guo 1999a; Men et al. 2007). Shannon-Wiener’s diversity index (H) was used to calculate the community diversity of gamasid mite commu- Materials and methods nity (Diker et al. 2004; Magurran 1988;Krebs1985; Shannon and Weaner 1949;ZhaoandGuo1990). The Asian house rats were sampled from 1990 to 2008 in 28 parameter K from the negative binomial distribution locations (counties) across Yunnan Province. The 28 (Waters 1959) was used to determine the spatial distribution counties included were Gongshan, Weixi, Lanping, patterns of the dominant mite species. Xianggelila, Lijiang, Jianchuan, Heqing, Baoshan, Dali, Yangbi, Binchuan, Xiangyun, Weishan, Nanjian, Puer, Ninger, Yuanjiang, Yingjiang, Gengma, Menghai, Fuyuan, Results Qiaojia, Suijiang, Qiubei, Wenshan, Maguan, Mengzi, and Hekou. The rats were randomly trapped with mousetraps in A total of 19,304 gamasid mites collected from 4,113 two types of habitat: indoor habitats (including farmers’ Asian house rats, R. tanezumi, were identified as compris- houses, barns, and stables) and outdoor habitats (including ing 50 species. The majority of rats harbored the mites farmlands, scrublands, and woodlands). The mousetraps with a total infestation rate (P) of 97.84 %, MA of 4.69 were set in the evening and then checked the following mites per examined rat and MI of 4.80 mites per infested morning. Each trapped rat was placed in a pre-marked rat. Of 50 mite species, 31 species were ectoparasites white cloth bag and transferred to the laboratory where it while 19 species were free-living mites (Table 1). The was anesthetized and systematically examined. Gamasid Cr of three dominant mite species reached 91.8 % of mites on the body surface of each rat host, together with the total, and these dominant mites were Laelaps nuttalli those scattered on the white cloth bag, were comprehen- Hirst 1915, Laelaps echidninus Berlese 1887, and sively collected over a large white tray with the help of a Ornithonyssus bacoti Hirst 1913. The P, MA, and MI of magnifier. Mites from each host were preserved in vials of the eight main species were much higher than those of the 70 % ethanol (Pan and Deng 1980;Dengetal.1993; remaining 42 mite species, values of which were so low Durden et al. 1997, 2004). After collection, the white plate they are not presented (Table 2). Author's personal copy

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Table 1 Gamasid mites and their living types collected from Asian house rats, Rattus tanezumi in Yunnan, Southwest China

Living types Collected gamasid mites from Asian house rats

Number Species names and collected individuals of the mites of species

Ectoparasites 31 Laelaps nuttalli (10,938); L. echidninus (5,373); L. turkestanicus (235); L. traubi (94); L. guizhouensis (8); L. chini (4); L. algericus (2); L. taingueni (1); L. xingyiensis (1); Ornithonyssus bacoti (1,408); Liponyssoides muris (223); Echinonyssus sunci or Hirstionyssus sunci (222); Tricholaelaps myonyssognathus (219); Androlaelaps singularis (31); Androlaelaps fahrenholzi or Haemolaelaps glasgowi (13); A. hsui (9); Haemolaelaps casalis (9); H. cordatus (2); H. semidesertus (2); H. traubi (1); Haemogamasus pontiger (31); H. monticola (18); H. oliviformis (8); H. sexsetosus (2); H. dorsalis (1); H. nidiformis (1); Eulaelaps stabularis (4); E. substabularis (4); E. shanghaiensis (2); Dipolaelaps anourosorecis (1); Deutonymphs sp. (1). Free-living 19 Proctolaelaps pygmaeus (178); Hypoaspis lubrica (83); H. miles (54); H. pavlovskii (35); H. chianensis (11); Parasitus consanguineous (18); P. baoshanensis (1); Lasioseius medius (10); L. praevius (3); L. paucispathus (1); L. trifurcipilus (1); Lasioseius sp. (16); Parasitidae sp. (11); Macrochelidae sp. (8); Gymnolaelaps sinensis (2); Asca idiobasis (1); Parholaspidae sp. (1); Macrocheles sp. (1); Phytoseiidae sp. (1).

The numbers in the brackets are the collected individuals of gamasid mites. sp gamasid mites which have not been identified to species

The total number of mite species (species richness) found Discussion on rats living outdoors (46 species) was much higher than on rats living indoors (26 species). Shannon-Wiener’s di- The results suggest that the infestation of gamasid mites on Asian versity indices of the gamasid mite community on the in- house rats (R. tanezumi) is very common. However, not all the door rats (H=0.3605) was slightly lower than in the outdoor identified mites were ectoparasites. Of 50 mite species, a few rats (H=0.4539) (Table 3). The Cr of O. bacoti, one of the potential transmission vectors of HFRS and other zoonotic dis- dominant mite species, was significantly lower on rats living eases were collected. These potential vectors included O. bacoti outdoors (1.68 %) compared to rats living indoors (21.92 %) (a dominant mite species), Echinonyssus sunci (Hirstionyssus (χ2=984.78; df=1; P<0.001). sunci), Eulaepas stabularis, Eulaepas shanghaiensis, and The parameter K was used to determine the spatial dis- Androlaelaps fahrenholzi (Haemolaelaps glasgowi)(Denget tribution patterns of three dominant mite species, L. nuttalli, al. 1993; Wang et al. 1996; Chung et al. 1998;Wuetal. L. echidninus, and O. bacoti. The mean (m), variance (σ2), 1998a, b; Zhang et al. 2000, 2001; Rosen et al. 2002; and K value of the mites are shown in Table 4. All the Heukelbach et al. 2005). At present, however, the transmission dominant mite species showed an aggregated distribution efficiency of these potential vectors can’tbedeterminedinthe pattern (Table 4). Most mite species showed a predominant- prevalence of local zoonotic diseases, and more research work ly female-biased structure with many more females than need to be made in the future. males. However, the sex ratio (♀/♂) was highly variable In comparison with other related reports on ectoparasites, (from 3.70 to 56.33) between species (Table 5). the species diversity of gamasid mites from a single rodent

Table 2 The constituent ratios (Cr), infestation prevalence (P), Species name Individuals Individuals Cr (%) P (%) MA±S.E. MI±S.E. mean abundance (MA), and of gamasid mites of gamasid mites of infested rats mean intensity (MI ) of eight main species of gamasid mites L. nuttalli 10,938 930 56.66 22.61 2.66±0.71 11.76±1.13 on Asian house rats, Rattus L. echidninus 5,373 1,073 27.84 26.09 1.31±0.21 5.01±0.40 tanezumi O. bacoti 1,408 305 7.29 7.42 0.34±0.31 4.62±1.18 L. turkestanicus 235 21 1.22 0.51 0.06±0.20 11.19±0.62 L. muris 223 46 1.16 1.12 0.05±0.03 4.85±0.32 E. sunci 222 77 1.15 1.87 0.05±0.02 2.88±0.28 T. myonyssognathus 219 87 1.13 2.12 0.05±0.01 2.52±0.20 P. pygmaeus 178 51 0.92 1.24 0.04±0.01 3.49±0.40 Author's personal copy

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Table 3 The species richness (number of species), Shannon-Wiener’s diversity (H) and dominant species of gamasid mite community on Rattus tanezumi in the indoor and outdoor habitats

Habitats Rat individuals Gamasid mites Constituent ratios of dominant mite species

Species richness HL. nuttall L. echidninus O. bacoti Other mite species

Indoors 2,084 26 0.3,605 46.17 25.18 21.92 6.74 Outdoors 2,029 46 0.4,539 60.99 28.53 1.68 8.80

species reported here are even higher than previously reported on rats living indoors than outdoors. This reflects the fact from multiple species in similar-sized geographical areas that O. bacoti prefers indoor habitats which are usually drier (Ritzi and Whitaker 2003; Storm and Ritzi 2008;Ogugeet and warmer than outdoors (Deng et al. 1993; Radovsky et al. 2009; Paramasvaran et al. 2009; Changbunjong et al. 2010) al. 1975). . The results imply that Asian house rats may have a great Similar to other reports, most of the gamasid mites we potential to harbor a variety of gamasid mites. In comparison found had a prominently female-biased structure (Radovsky with other ectoparasites (for example, sucking lice), most 1994;GuoandQian2001;Oliver1977; Weeks and gamasid mites may have lower host specificity (Pan and Hoffmann 1999). This might be related to their partheno- Deng 1980; Walter and Lindquist 1989;Dengetal.1993; genesis, which commonly occurs in mites and some other Simberloff and Moore 1997; Skorupski and Luxton 1998), (Oliver 1977; Weeks and Hoffmann 1999). some mite species for other small mammals may “cross- We used the parameter K to study the spatial distribution infest” Asian house rats, and some free-living mites in soil, patterns of the dominant mite species. The results revealed litter, or humus may accidentally lose their way to crawl onto that all dominant mite species had an aggregated distribution the rats. among their host rats, a pattern common for many parasites Yunnan Province is a well-known geographical region (Crofton 1971; Anderson and May 1978;Whiteand with complex topography and diversified habitats. More Bennetts 1996). This means that some hosts have very few than 55 % of China’s species and over 50 % of or no parasites, but others with a high-infestation intensity China’s plant species have been found there (Young and that form “parasite clumps.” This aggregated distribution Wang 1989; Yang et al. 2004). The assemblages of gamasid may increase the probability of mating and survival of the mites on rodents seem to be influenced by a series of factors, parasites (Rohde 1993; Kennedy 1976). including host factors, geographical locations, seasons, tem- perature, light, humidity, and plants. The off-host environ- Acknowledgments We thank the following people for their contri- ment may play a very important role in influencing the butions and help in the field investigation and laboratory work: Ti-jun species diversity, abundance, and distribution of the mites Qian, Wei Li, Xing-yuan Men, Sheng-yong Zhang, Yan-fen Meng, (Proctor 2003; Vinarski et al. 2007; Luo et al. 2007). In this Tian-guang Ren, Yong-guang Jing, Yi Yan, Qiao-Hua Wang, and some paper, the species diversity of gamasid mites in the outdoor college students in Dali University. The project was supported by the Natural Science Foundation of China to Xian-guo Guo (no. 30760226, habitats (46 mite species) was much higher than in the 81060139, and 81160208). indoor habitats (26 mite species), suggesting a key role for the habitat on infestation patterns. When living outdoors, Asian house rats seem more likely to get “cross-infesta- Table 5 The sex ratios of eight main species of gamasid mites ” tions when they contact with other rat species, and more- Species of gamasid mites Sex ratios over, they seem to have more chances to harbor some free- living mites (Simberloff and Moore 1997). One of the Females Males (♀/♂) dominant mite species, O. bacoti, was much more abundant L. nuttalli 7,767 1,446 5.37 L. echidninus 4,896 181 27.05 Table 4 The mean (m), variance (σ2), and K value of three dominant O. bacoti 355 43 8.26 species of gamasid mites L. turkestanicus 215 7 30.71 L. muris 73 13 5.62 Species of gamasid mites m σ2 K E. sunci 210 7 30.00 L. nuttalli 2.66 20.97 0.39>0 T. myonyssognathus 148 40 3.70 L. echidninus 1.31 1.84 3.24>0 P. pygmaeus 169 3 56.33 O. bacoti 0.34 3.87 0.03>0 Other 42 species 436 20 21.8 Author's personal copy

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