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Species diversity and related ecology of chiggers on small mammals in a unique geographical area of Yunnan Province, southwest China

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Abstract

Chiggers are common ectoparasites and the exclusive vector of scrub typhus. Based on previous investigations from a unique geographical area in Yunnan Province of southwest China, the Three Parallel Rivers Area, we retrospectively studied the species diversity and related ecology of chiggers on rodents and other small mammals. A very high species diversity of 120 chigger species was identified. Five dominant chigger species accounted for 59.4% (5238/8965) of total chiggers, and among them Leptotrombidium scutellare is the second major vector of scrub typhus in China. Species diversity of the chigger community fluctuates greatly in different altitudinal and latitudinal gradients. There are significant differences in species composition, species diversity and dominant species of chiggers among hosts with apparent community heterogeneity. Based on the species abundance distribution, the expected total number of chigger species was estimated to be 170, 50 more than the number of actually collected species; this further indicates a very high chigger species diversity in this area. The bipartite ecological network analysis revealed the intricate relationships between chigger and host species—positive and negative correlations existed among some species of dominant and vector chiggers.

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Data availability

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

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Acknowledgements

We are very grateful to the following people who contributed to the field investigations and laboratory work: Yun-Ji Zou, Qiao-Hua Wang, Wen-Ge Dong, Peng-Biao Yang, Pei-Ying Peng, Yong Zhang, Cong-Hua Gao, Nan Zhao, Jian-Chang He, Guo-Li Li, Yan-Liu Li, Xue-Song He, De-Cai Ouyang, and several colleagues and college students.

Funding

The research leading to these results received funding from the National Natural Science Foundation of China under Grant Agreement No. 82160400 and the Major Science and Technique Programs in Yunnan Province under Grant Agreement No. 202102AA310055-X to Xian-Guo Guo, and the Expert workstation for Dao-Chao Jin in Dali Prefecture.

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Contributions

Conceptualization, funding acquisition, project administration, resources, supervision, validation, and writing—review & editing, X-GG; supervision, D-CJ; data cura-tion, formal analysis, software, visualization, and writing—original draft, YG; investigation, C-FZ, Z-WZ, RF and TC; methodology, J-XZ, YL, P-WY, W-YS. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Xian-Guo Guo.

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The authors declare no competing interests.

Ethical Approval

The capture and use of animal hosts was approved by the local wildlife affairs authority and the Animal Ethics Committee of Dali University, approval code: DLDXLL2020-1104, approval date: 4 November 2020, which followed the international standards of animal euthanasia, 2013 AVMA guidelines (Cima 2013).

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Appendices

Appendix 1: Taxonomic checklist of small mammals captured from nine survey sites in the Three Parallel Rivers Area of northwest Yunnan, China (2001–2015)

Order Rodentia

I Family Muridae

  1. 1.

    Rattus tanezumi Temminck, 1844

  2. 2.

    R. nitidus (Hodgson, 1845)

  3. 3.

    R. norvegicus (Berkenhout, 1769)

  4. 4.

    R. andamanensis Blyth, 1860

  5. 5.

    Niviventer confucianus (Hodgson, 18736)

  6. 6.

    N. fulvescens (Gray, 1847)

  7. 7.

    N. andersoni (Thomas, 1911)

  8. 8.

    N. excelsior (Thomas, 1911)

  9. 9.

    Mus musculus L., 1758

  10. 10.

    M. caroli Bonhote, 1902

  11. 11.

    Apodemus draco (Barrett-Hamiliton, 1900)

  12. 12.

    A. peninsulae (Thomas, 1906)

  13. 13.

    A. chevrieri Milne-Edwards, 1868

  14. 14.

    A. agrarius (Pallas, 1771)

  15. 15.

    A. latronum Thomas, 1911

  16. 16.

    Berylmys bowersi (Anderson, 1879)

  17. 17.

    Micromys minutus (Pallas, 1771)

  18. 18.

    Vernaya fulva (Allen, 1927)

  19. 19.

    Bandicota indica (Bechstein, 1800)

II Family Cricetidae

  1. 20.

    Eothenomys miletus (Thomas, 1914)

  2. 21.

    E. eleusis (Thomas, 1911)

  3. 22.

    E. proditor Hinton, 1923

  4. 23.

    E. custos (Thomas, 1912)

III Family Sciuridae

  1. 24.

    Callosciurus quinquestriatus (Anderson, 1871)

  2. 25.

    Tamiops swinhoei (Milne-Edwards, 1874)

  3. 26.

    Dremomys pernyi (Milne-Edwards, 1867)

  4. 27.

    Rupestes forresti (Thomas, 1922)

IV Family Pteromyidae

  1. 28.

    Petaurista albiventer (Gray, 1834)

  2. 29.

    P. xanthotis (Milne-Edwards, 1872)

  3. 30.

    Trogoterus xanthipes (Milne-Edwards, 1867)

  4. 31.

    Belomys pearsonii (Gray, 1842)

  5. 32.

    Hylopetes alboniger (Hodgson, 1836)

  6. 33.

    Pteromys volans (L., 1758)

Order Eulipotyphla

V Family Talpidae

  1. 34.

    Scaptonyx fusicaudus Milne-Edwrds, 1872

VI Family Soricidae

  1. 35.

    Sorex excelsus Allen, 1923

  2. 36.

    S. cylindricauda Milne-Edwards, 1871

  3. 37.

    Episoriculus leucops (Hosfield, 1855)

  4. 38.

    Suncus murinus (L., 1766)

  5. 39.

    Crocidura attenuata Milne-Edwards, 1872

  6. 40.

    Anourosorex squamipes Milne-Edwards, 1872

Order Scandetia

VII Family Tupaiidae

  1. 41.

    Tupaia belangeri (Wagner, 1841)

Order Lagomorpha

VIII Family Ochotonidae

  1. 42.

    Ochotona thibetana (Milne-Edwards, 1871)

  2. 43.

    O. roylii (Ogilby, 1839)

Order Carnivora

IX Family Mustelidea

  1. 44.

    Mustela kathiah Hodgson, 1835

Appendix 2: Taxonomic checklist of chiggers identified from nine survey sites in the Three Parallel Rivers Area of northwest Yunnan, China (2001–2015). Species marked with ‘**’ are proven effective vectors of scrub typhus, tsutsugamushi disease, and those with ‘*’ are potential vectors of scrub typhus

I Family Trombiculidae

Subfamily Trombiculinae

  1. 1.

    Leptotrombidium scutellare** (Nagayo et al., 1921)

  2. 2.

    L. sinicum Yu et al., 1981

  3. 3.

    L. eothenomydis Yu and Yang, 1986

  4. 4.

    L. hiemalis Yu et al., 1982

  5. 5.

    L. rusticum Yu et al., 1986

  6. 6.

    L. shuqui Wen et Xiang, 1984

  7. 7.

    L. wangi Yu et al., 1986

  8. 8.

    L. densipunctatum Yu et al., 1982

  9. 9.

    L. yongshengense Yu and Yang, 1986

  10. 10.

    L. yui* (Chen and Hsu, 1955)

  11. 11.

    L. xiaguanense Yu et al., 1981

  12. 12.

    L. imphalum** Vercammen-Grandjean and Langston, 1976

  13. 13.

    L. gongshanense Yu et al., 1981

  14. 14.

    L. spicanisetum Yu et al., 1986

  15. 15.

    L. cuonae Wang et al., 1996

  16. 16.

    L. deplanoscutum Yu et al., 1981

  17. 17.

    L. lianghense Yu et al., 1983

  18. 18.

    L. wenense (L. kaohuense)** Yang et al., 1959

  19. 19.

    L. qujingense Yu et al., 1981

  20. 20.

    L. dianchi Wen et Xiang, 1984

  21. 21.

    L. jinmai Wen et Xiang, 1984

  22. 22.

    L. longimedium Wen et Xiang, 1984

  23. 23.

    L. akamushi** Barumpt, 1910

  24. 24.

    L. alpinum Yu et Yang, 1986

  25. 25.

    L. trapezoidum Wang et al., 1981

  26. 26.

    L. allosetum Wang et al., 1981

  27. 27.

    L. sinotupaium Wen et Xiang, 1984

  28. 28.

    L. hsui Yu et al., 1986

  29. 29.

    L. robustisetum Yu et al., 1983

  30. 30.

    L. biluoxueshanense Yu et al., 1982

  31. 31.

    L. cangjiangense Yu et al., 1981

  32. 32.

    L. hupeicum Ma et Hsu, 1965

  33. 33.

    L. apodemi* Wen et Sun, 1984

  34. 34.

    L. intermedium* Nagayo et al., 1920

  35. 35.

    L. biji Wen et Xiang, 1984

  36. 36.

    L. apodevrieri Wen et Xiang, 1984

  37. 37.

    L. suense Wen, 1984

  38. 38.

    L. huangdi Wen et Yang, 1984

  39. 39.

    L. zhongdianense Yu et Yang, 1981

  40. 40.

    L. bishanense Yu et al., 1986

  41. 41.

    L. yunlingense Yu et Zhang, 1981

  42. 42.

    L. ejingshanense Yu et al., 1982

  43. 43.

    L. baoshui Wen et Xiang, 1984

  44. 44.

    L. laojunshanense Yu et al., 1986

  45. 45.

    L. caudatum Wen et al., 1984

  46. 46.

    L. xinjiangense Shao et Wen, 1984

  47. 47.

    L. jianshanense Yu et al., 1982

  48. 48.

    L. saltuosum Yu et al., 1982

  49. 49.

    L. sexsetum Yu et Hu, 1981

  50. 50.

    L. rupestre* Traub et Nadchatram, 1967

  51. 51.

    L. bambicola Wen et Xiang, 1984

  52. 52.

    L. liaoji Wen et Sun, 1984

  53. 53.

    L. rattistae Wen et al., 1984

  54. 54.

    L. linhuaikongense* (Wen et Hsu, 1961)

  55. 55.

    L. miyajimai (Fukuzumi et Obata, 1951)

  56. 56.

    L. fujianense Liao et Wang, 1983

  57. 57.

    L. burnsi (Sasa et al., 1953)

  58. 58.

    L. insulare** Wei et al., 1989

  59. 59.

    L. gemiticulum (Traub et al., 1958)

  60. 60.

    L. yunnanense Yu et al., 1980

  61. 61.

    L. huangchuanense Yang, 1994

  62. 62.

    L. bayanense Yang, 1994

  63. 63.

    Trombiculindus alpinus Yu et Yang, 1979

  64. 64.

    T. yunnanus Wang et Yu, 1965

  65. 65.

    T. cuneatus Traub et Evans, 1951

  66. 66.

    T. bambusoides Wang et Yu, 1965

  67. 67.

    T. nujiange Wen et Xiang, 1984

  68. 68.

    Neotrombicula longmenis Wen et Xiang, 1984

  69. 69.

    N. deqinensis Yu et Wang, 1981

  70. 70.

    N. japonica (Tanaka et al., 1930)

  71. 71.

    N. tongtianhensis Yang et al., 1995

  72. 72.

    N. aeretes Hsu et Yang, 1985

  73. 73.

    N. microtomici Wen et al., 1984

  74. 74.

    N. microti (Ewing, 1928)

  75. 75.

    Microtrombicula nadchatrami Vercammen-Grandjean, 1965

  76. 76.

    Helenicula hsui Zhao, 1990

  77. 77.

    H. lanius (Radford, 1946)

  78. 78.

    Doloisia brachypus (Audy et Nadchatram, 1957)

  79. 79.

    D. taishanensis Teng, 1982

  80. 80.

    D. furcipelta Yu et al., 1983

  81. 81.

    Ascoschoengastia indica* (Hirst, 1915)

  82. 82.

    A. yunnanensis Yu et al., 1980

  83. 83.

    A. leechi (Domrow, 1962)

  84. 84.

    A. menghaiensis Yu et al., 1986

  85. 85.

    A. rattinorvegici Wen, 1984

  86. 86.

    Herpetacarus spinosetosus Wang et al., 1980

  87. 87.

    H. tenuiclavus Yu et al., 1979

  88. 88.

    H. hastoclavus Yu et al., 1979

  89. 89.

    Euschoengastia weifangensis Teng et Zhang, 1989

Subfamily Gahrliepiinae Womersley, 1952

  1. 90.

    Walchia pacifica* (Chen et Hsu, 1955)

  2. 91.

    W. parapacifica (Chen et al., 1955)

  3. 92.

    W. micropelta (Traub et Evans, 1957)

  4. 93.

    W. chinensis* (Chen et Hsu, 1955)

  5. 94.

    W. kor (Chen et Hsu, 1957)

  6. 95.

    W. enode Gater, 1932

  7. 96.

    W. sheensis Wen, 1984

  8. 97.

    W. xishaensis Zhao et al., 1986

  9. 98.

    W. ewingi (Fuller, 1949)

  10. 99.

    Schoengastiella ligula Radford, 1946

  11. 100.

    Gahrliepia zhongwoi Wen et Xiang, 1984

  12. 101.

    G. longipedalis Yu et Yang, 1986

  13. 102.

    G. radiopunctata Hsu et al., 1965

  14. 103.

    G. octosetosa Chen et al., 1956

  15. 104.

    G. latiscutata Chen et Fan, 1981

  16. 105.

    G. lengshui Wen et Xiang, 1984

  17. 106.

    G. yangchenensis Chen et Hsu, 1957

  18. 107.

    G. deqinensis Yu et Yang, 1982

  19. 108.

    G. tenuiclava Yu et al., 1983

  20. 109.

    G. tenella Traub et Morrow, 1955

  21. 110.

    G. chekiangensis Chu, 1964

  22. 111.

    G. yunnanensis Hsu et al., 1965

  23. 112.

    G. chungkingensis Jeu et al., 1963

  24. 113.

    G. megascuta Hsu et al., 1965

  25. 114.

    G. madun Wen et Xiang, 1984

  26. 115.

    G. linguipelta Jeu et al., 1983

  27. 116.

    G. fimbriata Traub et Morrow, 1955

  28. 117.

    Intermedialia hegu (Yu, Yang et Wu, 1979)

II Family Leeuwenhoekiidae

Subfamily Leeuwenhoekiinae

  1. 118.

    Chatia maoyi Wen et Xiang, 1984

  2. 119.

    C. alpine Shao et Wen, 1984

  3. 120.

    Shunsennia scabrisetosa Huang, 1986

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Guo, Y., Zhou, JX., Guo, XG. et al. Species diversity and related ecology of chiggers on small mammals in a unique geographical area of Yunnan Province, southwest China. Exp Appl Acarol 91, 439–461 (2023). https://doi.org/10.1007/s10493-023-00841-z

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