Abstract
The Yunnan red-backed vole (Eothenomys miletus) is an endemic rodent species in China and it often harbors two groups of mites, chigger mites and gamasid mites, on its body surface. A few species of chigger mites and gamasid mites are transmitting vectors of some zoonoses. Based on abundant original data from a long-term field ecological investigation in Yunnan Province of southwest China between 2001 and 2015, the present study made a detailed analysis on the infestation of E. miletus with mites. From 14 to 30 investigated counties, 53,958 mites were collected from 1,900 E. miletus voles with relatively high infestations. Of 232 mite species identified, there were 152 species of chigger mites (44,797 individuals) and 80 species of gamasid mites (9,161 individuals). The overall infestation prevalence (PM) and mean abundance (MA) reached 76.84 % and 28.40 mites/vole, respectively. The chigger mite Leptotrombidium scutellare (the constituent ratio, Cr = 18.60 %), gamasid mite Laelaps chini (Cr = 12.16 %) and chigger mite Leptotrombidium sinicum (Cr = 10.57 %) were three dominant species of mites. The three dominant mite species had an aggregated distribution among the different individuals of E. miletus. Eothenomys miletus in the mountainous landscape harbored much more individuals and species of mites with a higher prevalence (PM = 82.25 %), mean abundance (MA = 38.26 mites/vole) and species richness (Mf = 19.59) than in the flatland landscape (p < 0.05). The infestation of E. miletus with mites in different altitude gradients was uneven and heterogenic, which reflects the infestation fluctuations in different environments. Mites tended to infest male and adult voles with higher PM and MA than female and juvenile ones, which reflects the infestation bias on different sexes and ages of vole hosts. There is no obvious interspecific coexistence, cooperation or competitive exclusion between chigger mites and gamasid mites on E. miletus. Based on iChao1’s formula, the total number of mite species on E. miletus was estimated to be 285.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: margolis revisited. J Parasitol 83(4):575–583. https://doi.org/10.2307/3284227
Cevidanes A, Proboste T, Chirife AD, Millan J (2016) Differences in the ectoparasite fauna between micromammals captured in natural and adjacent residential areas are better explained by sex and season than by type of habitat. Parasitol Res 115(6):2203–2211. https://doi.org/10.1007/s00436-016-4962-0
Chao A, Chiu CH (2016) Nonparametric estimation and comparison of species richness. Wiley, Chichester. https://doi.org/10.1002/9780470015902.a0026329
Chao A, Chazdon RL, Colwell RK, Shen TJ (2010) A new statistical approach for assessing similarity of species composition with incidence and abundance data. Ecol Lett 8(2):148–159. https://doi.org/10.1111/j.1461-0248.2004.00707.x
Chiu CH, Wang YT, Walther BA, Chao A (2014) An improved nonparametric lower bound of species richness via a modified good–Turing frequency formula. Biometrics 70(3):671–682. https://doi.org/10.1111/biom.12200
Dar PA, Reshi ZA (2020) Impact of alien species on species composition, floristic and functional diversity of aquatic and terrestrial ecosystems. Trop Ecol 61(4):1–14. https://doi.org/10.1007/s42965-020-00102-9
Deng GF, Wang DQ, Gu YM, Meng YC (1993) Economic insect fauna of China. Fasc 40, Acari, Dermanyssoidea. Science Press, Beijing (in Chinese)
Ding F, Guo XG, Song WY, Fan R, Zhao CF, Mao KY, Zhang ZW, Peng PY, Lin H, Dong WG, Qian TJ, Yang ZH, Zou YJ (2021a) Infestation and distribution of chigger mites on brown rat (Rattus norvegicus) in Yunnan Province, Southwest China. Trop Biomed 38(1):1–11
Ding F, Liu XH, Guo XG, Fan R, Zhao CF, Zhang ZW, Mao KY, Huang XB (2021b) Analysis of gamasid mites(Acari: Mesostigmata) on Mus pahari in Yunnan Province. Chin J Zool 56(2):240–246. https://doi.org/10.13859/j.cjz.202102009 (in Chinese)
Elliott I, Pearson I, Dahal P, Thomas NV, Roberts T, Newton PN (2019) Scrub typhus ecology: a systematic review of Orientia in vectors and hosts. Parasit Vectors 12(1):513. https://doi.org/10.1186/s13071-019-3751-x
Folstad I, Karter AJ (1992) Parasites, bright males, and the immunocompetence handicap. Am Nat 139(3):603–622. https://doi.org/10.2307/2462500
Guo XG, Qian TJ, Guo LJ, Wang J, Dong WG, Zhang L, Ma ZM, Li W (2003) Spatial distribution pattern of Hoplopleura pacifica (Anoplura:Hoplopleuridae) on its dominant rat host, Rattus flavipectus in Yunnan, China. Insect Sci 10(4):265–269
Guo XG, Qian TJ, Meng XY, Dong WG, Shi WX, Wu D (2006) Preliminary analysis of chigger communities associated with house rats (Rattus flavipectus) from six counties in Yunnan, China. Syst Appl Acarol 11(1):13–21. https://doi.org/10.11158/saa.11.1.2
Guo XG, Speakman JR, Dong WG, Men XY, Qian TJ, Wu D, Qin F, Song WY (2013) Ectoparasitic insects and mites on Yunnan red-backed voles (Eothenomys miletus) from a localized area in southwest China. Parasitol Res 112(10):3543–3549. https://doi.org/10.1007/s00436-013-3537-6
Hoogenboom MO, Frank GE, Blowes SA, Chase TJ, Zawada KJA, Dornelas M (2015) Disparity between projected geographic rangesof rare species: a case study of Echinomorpha nishihirai (Scleractinia). Mar Biodivers Rec 8:e147. https://doi.org/10.1017/S175526721500114
Huang LQ, Guo XG, Speakman JR, Dong WG (2013) Analysis of gamasid mites (Acari: Mesostigmata) associated with the Asian house rat, Rattus tanezumi (Rodentia: Muridae) in Yunnan Province, Southwest China. Parasitol Res 112(5):1967–1972. https://doi.org/10.1007/s00436-013-3354-y
Jiang ZG, Ma Y, Wu Y, Wang YX, Zhou KY, Liu SY, Feng ZJ (2015) China’s mammal diversity and geographic distribution. Science Press, Beijing. [In Chinese]
Kataranovski M, Mirkov I, Belij S, Popov A, Petrovic Z, Kataranovski D (2011) Intestinal helminths infection of rats (Ratus norvegicus) in the Belgrade area (Serbia): the effect of sex, age and habitat. Parasite 18(2):189–196. https://doi.org/10.1051/parasite/2011182189
Krasnov B, Stanko M, Khokhlova IS, Mosanský L (2010) Aggregation and species coexistence in fleas parasitic on small mammals. Ecography 29(2):159–168. https://doi.org/10.1111/j.2005.0906-7590.04353.x
Liu Z, Guo XG, Fan R, Zhao CF, Mao KY, Huang ZW, Zhao Y (2020) Ecological analysis of gamasid mites on the body surface of Norway rats (Rattus norvegicus) in Yunnan Province, southwest China. Biologia 75:1325–1336. https://doi.org/10.2478/s11756-019-00383-z
Manu M (2013) Diversity of soil mites (Acari: Mesostigmata: Gamasina) in various deciduous forest ecosystems of Muntenia region (southern Romania). Biol Lett 50(1):3–16. https://doi.org/10.2478/biolet-2013-0001
Marchenko II, Bogomolova IN (2015) Spatial-typologic organization of populations of soil gamasid mites (Acari, Mesostigmata) in northern Altai Mountains. Contemp Probl Ecol 8(2):202–210. https://doi.org/10.1134/S1995425515020122
Matthee S, Stekolnikov AA, van der Mescht L, Froeschke G, Morand S (2020) The diversity and distribution of chigger mites associated with rodents in the South African savanna. Parasitology 147(9):1038–1047. https://doi.org/10.1017/S0031182020000748
Morand S, De Bellocq JG, Stanko M, Miklisová D (2004) Is sex-biased ectoparasitism related to sexual size dimorphism in small mammals of Central Europe? Parasitology 129(Pt 4):505–510. https://doi.org/10.1017/s0031182004005840
Nagayo M, Miyagawa Y, Mitamura T, Tamiya T, Tenjin S (1921) Five species of tsutsugamushi (the carries of Japanese river fever) and their relation to the tsutsugamushi disease. Am J Epidemiol 1(5):569–591. https://doi.org/10.1093/oxfordjournals.aje.a118053
Peng PY, Guo XG, Song WY, Hou P, Zou YJ, Fan R, He XS (2015) Analysis of ectoparasites (chigger mites, gamasid mites, fleas and sucking lice) of the Yunnan red-backed vole (Eothenomys miletus) sampled throughout its range in southwest China. Med Vet Entomol 29(4):403–415. https://doi.org/10.1111/mve.12134
Peng PY, Guo XG, Song WY, Hou P, Zou YJ, Fan R (2016) Ectoparasitic chigger mites on large oriental vole (Eothenomys miletus) across southwest, China. Parasitol Res 115(2):623–632. https://doi.org/10.1007/s00436-015-4780-9
Peng PY, Guo XG, Jin DC, Dong WG, Qian TJ, Qin F, Yang ZH, Fan R (2018) Landscapes with different biodiversity influence distribution of small mammals and their ectoparasitic chigger mites: A comparative study from southwest China. PLoS One 13(1):e0189987. https://doi.org/10.1371/journal.pone.0189987
Pongsiri M, Roman J, Ezenwa V, Goldberg T, Koren H, Newbold S, Ostfeld R, Pattanayak S, Salkeld D (2009) Biodiversity loss affects global disease ecology. Bio Science 59(11):945–954. https://doi.org/10.1525/bio.2009.59.11.6
Poulin R (1997) Species richness of parasite assemblages: evolution and patterns. Annu Rev Ecol Evol Syst 28(1):341–358. https://doi.org/10.1146/annurev.ecolsys.28.1.341
Robinson SA, Forbes MR, Hebert CE, Mclaughlin JD (2008) Male-biased parasitism by common helminths is not explained by sex differences in body size or spleen mass of breeding cormorants Phalacrocorax auritus. J Avian Biol 39(3):272–276. https://doi.org/10.1111/j.0908-8857.2008.04340.x
Smith AT, Johnston CH (2016)Eothenomys miletus (errata version published in 2017). The IUCN Red List of Threatened Species 2016: e.T136275A115205387.https://doi.org/10.2305/IUCN.UK.2016-3.RLTS.T136275A22376031.en
Vinarski MV, Korallo-Vinarskaya NP (2017) An annotated catalogue of the gamasid mites associated with small mammals in Asiatic Russia. The family Haemogamasidae (Acari: Mesostigmata: Gamasina). Zootaxa 4273(1):1–18. https://doi.org/10.11646/zootaxa.4273.1.1
Xiang R, Guo XG (2021) Research advances of Leptotrombidium scutellare in China. Korean J Parasitol 59(1):1–8. https://doi.org/10.3347/kjp.2021.59.1.1
Xiang R, Guo XG, Zhao CF, Fan R, Mao KY, Zhang ZW, Huang XB (2021) Infestation and distribution of gamasid mites on Himalayan field rat (Rattus nitidus) in Yunnan Province of Southwest China. Biologia 76:1763–1773. https://doi.org/10.2478/s11756-021-00679-z
Yang YM, Tian K, Hao JM, Pei SJ, Yang YX (2004) Biodiversity and biodiversity conservation in Yunnan. China Biol Conserv 13(4):813–826. https://doi.org/10.1023/B:BIOC.0000011728.46362.3c
Yin PW, Guo XG, Jin DC, Fan R, Zhao CF, Zhang ZW, Huang XB, Mao KY (2021) Distribution and host selection of tropical rat mite, Ornithonyssus bacoti, in Yunnan Province of Southwest China. Animals (Basel)11(1):110. https://doi.org/10.3390/ani11010110
Zhang Y, Yuan J, Yang X, Zhou J, Yang W, Peng C, Zhang HL, Shi Z (2011) A novel hantavirus detected in Yunnan red-backed vole (Eothenomys miletus) in China. J Gen Virol 92(Pt 6):1454–1457. https://doi.org/10.1099/vir.0.030122-0
Zhang B, Zhang H, Jing Q, Wu YX, Ma SQ (2020) Differences in species diversity, biomass, and soil properties of five types of alpine grass-lands in the northern Tibetan plateau. PLoS One 15(2):e0228277. https://doi.org/10.1371/journal.pone.0228277
Zheng ZM, Jiang ZK, Chen AG (2012) Rodent zoology. Shanghai Jiao Tong University Press, Shanghai. [in Chinese]
Zhu WL, Cai JH, Lian X, Wang ZK (2010) Adaptive character of metabolism in Eothenomys miletus in Hengduan Mountains region during cold acclimation. J Therm Biol 35(8):417–421. https://doi.org/10.1016/j.jtherbio.2010.09.002
Zhu WL, Jia T, Lian X, Wang ZK (2010) Effects of cold acclimation on body mass, serum leptin level, energy metabolism and thermogenesis in Eothenomys miletus in Hengduan Mountains region. J Therm Biol 35(1):41–46. https://doi.org/10.1016/j.jtherbio.2009.10.006
Zomer RJ, Xu JC, Wang MC, Trabucco A, Li ZQ (2015) Projected impact of climate change on the effectiveness of the existing protected area network for biodiversity conservation within Yunnan Province, China. Biol Conserv 184:335–345. https://doi.org/10.1016/j.biocon.2015.01.031
Acknowledgements
More than 60 people have joined this study, including field investigation, collection of mites (chigger mites and gamasid mites) and other ectoparasites, preparation of specimens and identification of the mites. Here we would like to express our sincere thanks to the following people who have made special contributions to the field investigation and laboratory work: Qiao-Hua Wang, Yong Zhang, Cong-Hua Gao, Nan Zhao, Jian-Chang He, Guo-Li Li, Xue-Song He, Yun-Ji Zou, De-Cai Ouyang, Shuang-Lin Wang, some colleagues and college students. The project was supported by the National Natural Science Foundation of China (No. 81960380, 81672055) to Xian-Guo Guo, and the Innovation Team of Vector Biology, Dali University (No. ZKLX2019104). We would like to express our thanks for the fund support.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The sampling of the Yunnan red-backed voles (Eothenomys miletus) was officially permitted by the local authority of wildlife service in Dali Prefecture of Yunnan Province, China. The use of animals (Yunnan red-backed voles) for research was also officially approved by the Animal Ethics Committee of Dali University.
Conflict of interest
No conflict of interest exists in the submission of this manuscript, and the manuscript is approved by all authors for publication.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
ESM 1
(PDF 428 KB)
Rights and permissions
About this article
Cite this article
Xiang, R., Guo, XG., Ren, TG. et al. Infestation and distribution of mites on the Yunnan red-backed vole (Eothenomys miletus) in Yunnan Province of southwest China between 2001 and 2015. Biologia 77, 61–68 (2022). https://doi.org/10.1007/s11756-021-00884-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11756-021-00884-w