Skip to main content
SpringerLink
Log in

Bat ectoparasites: chigger mites (Trombiculidae), ticks (Ixodidae and Argasidae), and bugs (Cimicidae) in the Eastern Palaearctic

  • Research
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Nine species-level taxa of bat ectoparasites, three chigger mites (Trombiculidae), three hard (Ixodidae), and one soft tick (Argasidae) species, as well as two bug (Cimicidae) species from nine bat species hosts were detected in the Eastern Palaearctic. Trombiculid larvae of Leptotrombidium schlugerae, Leptotrombidium album, and Ascoschoengastia latyshevi were first recorded on bats in the temperate zone of eastern Russia. L. schlugerae was more abundant than A. latyshevi in the same study sites in Eastern Siberia, and the main hosts of both chigger species were Plecotus ognevi and Eptesicus nilssonii. Ixodid ticks Dermacentor marginatus, Ixodes simplex, and Ixodes sp. were sampled from bats in Kazakhstan, the Far East, and Eastern Siberia, respectively. Phylogenetic analysis based on Cox1, 16S rDNA, and ITS2 sequences of I. simplex showed that the specimens from the Far East grouped into a clade distributed in the Eastern Palaearctic and India. In turn, the specimen of Ixodes sp. from Eastern Siberia was most closely related to Ixodes soricis and Ixodes angustus with p-distance of 9.8–10.7% (Cox1), suggesting that this tick probably belongs to a new species. Argas vespertilionis larvae were collected from three widespread bat species in Kazakhstan. Two bug species, Cimex pipistrelli and Cimex aff. lectularius, were recorded in the Far East and Eastern Siberia, respectively. Specimens from Transbaikalia were morphologically identified as Cimex lectularius. However, they differed from the latter by 12.5–12.9% of Cox1 sequences, indicating that C. aff. lectularius may be a new species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Data availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Akhoundi M, Sereno D, Durand R, Mirzaei A, Bruel C, Delaunay P, Marty P, Izri A (2020) Bed bugs (Hemiptera, Cimicidae): overview of classification, evolution and dispersion. Int J Environ Res Public Health 17:4576. https://doi.org/10.3390/ijerph17124576

    Article  PubMed  PubMed Central  Google Scholar 

  • Alkhovsky SV, Lvov DK, Yu SM, Shchetinin AM, Deryabin PG, Samokhvalov EI, Gitelman AK, Botikov AG (2013) The taxonomy of the Issyk-Kul virus (ISKV, Bunyaviridae, Nairovirus), the etiologic agent of the Issyk-Kul fever isolated from bats (Vespertilionidae) and ticks Argas (Carios) vespertilionis (Latreille, 1796). Probl Virol 58:11–15 ([in Russian])

  • Anthony ELP (1988) Age determination in bats. In: Kunz TH (ed) Ecological and behavioral methods for the study of bats. Smithsonian Institution Press, Washington, D.C., pp 47–58

    Google Scholar 

  • Balvín O, Roth S, Talbot B et al (2018) Co-speciation in bedbug Wolbachia parallel the pattern in nematode hosts. Sci Rep 8:8797. https://doi.org/10.1038/s41598-018-25545-y

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Balvín O, Vilímová J, Kratochvíl L (2013) Batbugs (Cimex pipistrelli group, Heteroptera: Cimicidae) are morphologically, but not genetically differentiated among bat hosts. J Zoolog Syst Evol Res 51:287–295. https://doi.org/10.1111/jzs.12031

    Article  Google Scholar 

  • Beron P (2020) Acarorum Catalogus VI. Order Mesostigmata. Gamasina: Dermanyssoidea (Rhinonyssidae, Spinturnicidae). Pensoft & Natn Mus Nat Hist, Sofia. https://doi.org/10.3897/ab.e54206

  • Blake FG, Maxcy KF, Sadusk JF Jr, Kohls GM, Bell EJ (1945) Trombicula fletcheri Womersley and Heaslip, 1943, a vector of tsutsugamushi disease (scrub typhus) in New-Guinea. Science 102:61–64. https://doi.org/10.1126/science.102.2638.61

    Article  CAS  PubMed  ADS  Google Scholar 

  • Bochkov AV (2009) A review of mites of the parvorder Eleutherengona (Acariformes: Prostigmata) — permanent parasites of mammals. Acarina Supplement 1, KMK Scientific Press, Moscow

  • Corbet GB (1978) The mammals of the Palaearctic region: a taxonomic review. Cornell University Press, London

    Google Scholar 

  • Coroiu I (2016a) Eptesicus nilssonii. The IUCN Red List of Threatened Species 2016: e.T7910A22116204. https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T7910A22116204.en

  • Coroiu I (2016b) Vespertilio murinus. The IUCN Red List of Threatened Species 2016: e.T22947A22071456. https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T22947A22071456.en

  • Csorba G, Hutson AM (2016) Nyctalus noctula. The IUCN Red List of Threatened Species 2016: e.T14920A22015682. https://doi.org/10.2305/IUCN.UK.2016-2.RLTS.T14920A22015682.en

  • Dzhanokmen KA (1969) Materials on chigger mites (Family Trombiculidae) of Kazakhstan [Materialy po kleshcham-krasnotelkam (sem. Trombiculidae) Kazahstana]. Prirodnoochagovye Bolezni i Voprosy Parazitologii v Srednej Azii i Kazahstane 5:219–221 ([in Russian])

  • 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 12:1–36. https://doi.org/10.1186/s13071-019-3751-x

  • Emel'yanova ND, Vysokovskiy NN (1962) On the issue of bat wintering and their ectoparasites in the vicinity of Krasnoyarsk [K voprosu o zimovkah letuchih myshej i ih ektoparazitah v okrestnostyah Krasnoyarska]. Doklady Irkutskogo Protivochumnogo Instituta 3:146–148 ([in Russian])

  • Filippova NA (1977) Ixodid ticks of the subfamily Ixodinae Fauna of USSR Arachnida Iksodovye [kleshchi podsemejstva Ixodinae Fauna SSSR. Paukoobraznye] 4:4 (Nauka, Leningrad. [in Russian])

  • Filippova NA (1997) Ixodid ticks of subfamily Amblyomminae. Fauna of Russia and neighbouring countries. Arachnoidea [Iksodovye kleshchi podsem. Amblyomminae. Fauna Rossii i sopredel'nyh stran. Paukoobraznye], Vol. IV, issue 5. “Nauka” Publishing House, St. Petersburg. [in Russian]

  • Filippova NA, Neronov VM, Farang-Azad A (1976) Materials on the fauna of ixodids (Acarina, Ixodidae) of small mammals in Iran. Entomol Rev 55:467–479 ([in Russian])

  • Folmer O, Hoesh WR, Black MB, Vrijenhoek RC (1994) Conserved primers for PCR amplification of mitochondrial DNA from different invertebrate phyla. Mol Mar Biol Biotech 3:294–299

    CAS  Google Scholar 

  • Frances SP, Watcharapichat P, Phulsuksombati D, Tanskul P (2000) Transmission of Orientia tsutsugamushi, the etiological agent for scrub typhus, to co-feeding mites. Parasitology 120:601–607. https://doi.org/10.1017/s0031182099005909

    Article  PubMed  Google Scholar 

  • Fukui D (2015) Vespertilio sinensis. In: Ohdachi SD, Ishibashi Y, Iwasa MA, Fukui D, Saitoh T (eds) The wild mammals of Japan, 2nd edn. Shoukadon Book Sellers, Kyoto, pp 96–98

  • Fukui D, Sano A (2020) Myotis petax. The IUCN Red List of Threatened Species 2020: e.T85342726A85342734. https://doi.org/10.2305/IUCN.UK.2020-2.RLTS.T85342726A85342734.en

  • Fukui D, Sun K, Kruskop, SV (2019) Myotis macrodactylus. The IUCN Red List of Threatened Species 2019: e.T14177A22065868. https://doi.org/10.2305/IUCN.UK.2019-3.RLTS.T14177A22065868.en

  • Fukunaga M, Yabuki M, Hamase A, Oliver JH Jr, Nakao M (2000) Molecular phylogenetic analysis of ixodid ticks based on the ribosomal DNA spacer, internal transcribed spacer 2, sequences. J Parasitol 86:38–43. https://doi.org/10.1645/0022-3395(2000)086[0038:MPAOIT]2.0.CO;2

    Article  CAS  PubMed  Google Scholar 

  • Godlevska L, Bücs S, Kruskop SV, Gazaryan S, Benda P, Paunović M (2020) Pipistrellus pipistrellus (errata version published in 2021). The IUCN Red List of Threatened Species 2020: e.T85333513A196581936. https://doi.org/10.2305/IUCN.UK.2020-2.RLTS.T85333513A196581936.en

  • Godlevska L, Kruskop SV, Gazaryan S (2021) Eptesicus serotinus (amended version of 2020 assessment). The IUCN Red List of Threatened Species 2021: e.T85199559A195834153. https://doi.org/10.2305/IUCN.UK.2021-1.RLTS.T85199559A195834153.en

  • Goff ML, Loomis RB, Welbourn WC, Wrenn WJ (1982) A glossary of chigger terminology (Acari: Trombiculidae). J Med Entomol 19:221–238

    Article  CAS  PubMed  Google Scholar 

  • Gromov IM, Gureev AA, Novikov GA, Sokolov II, Strelkov PP, Chapsky KK (1963) Mammals of the fauna of the USSR, part 1 (Key guides to the fauna of Russia, published by the Zoological Institute of the USSR Academy of Sciences, 83). Publishing House of the USSR Academy of Sciences, Moscow, Leningrad ([in Russian])

  • Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci USA 101(41):14812–14817. https://doi.org/10.1073/pnas.0406166101

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Hornok S (2017) Dermacentor marginatus (Sulzer, 1776) (Figs. 111–113). In: Estrada-Peña A, Mihalca A, Petney T (eds) Ticks of Europe and North Africa. A guide to species identification. Springer, Cham, pp 281–285. https://doi.org/10.1007/978-3-319-63760-0_54

  • Hornok S, Estrada-Peña A, Kontschán J, Plantard O, Kunz B, Mihalca AD, Thabah A, Tomanović S, Burazerović J, Takács N, Görföl T, Estók P, Tu VT, Szőke K, Fernández de Mera IG, de la Fuente J, Takahashi M, Yamauchi T, Takano A (2015) High degree of mitochondrial gene heterogeneity in the bat tick species Ixodes vespertilionis, I. ariadnae and I. simplex from Eurasia. Parasit Vectors 8:457. https://doi.org/10.1186/s13071-015-1056-2

  • Hornok S, Kontschán J, Kováts D, Kovács R, Angyal D, Görföl T et al (2014) Bat ticks revisited: Ixodes ariadnae sp nov. and allopatric genotypes of I. vespertilionis in caves of Hungary. Parasit Vectors 7:202. https://doi.org/10.1186/1756-3305-7-202

  • Hornok S, Szoke K, Görföl T, Földvári G, Tu VT, Takács N et al (2017a) Molecular investigations of the bat tick Argas vespertilionis (Ixodida: Argasidae) and Babesia vesperuginis (Apicomplexa: Piroplasmida) reflect “bat connection” between Central Europe and Central Asia. Exp Appl Acarol 72:69–77. https://doi.org/10.1007/s10493-017-0140-z

    Article  PubMed  Google Scholar 

  • Hornok S, Szőke K, Tu VT, Kontschán J, Takács N, Sándor AD, Halajian A, Földvári G, Estók P, Plantard O, Epis S, Görföl T (2017b) Mitochondrial gene heterogeneity of the bat soft tick Argas vespertilionis (Ixodida: Argasidae) in the Palaearctic. Parasit Vectors 10:109. https://doi.org/10.1186/s13071-017-2037-4

  • Hornok S, Szoke K, Meli ML, Sándor AD, Görföl T, Estók P et al (2019) Molecular detection of vector-borne bacteria in bat ticks (Acari: Ixodidae, Argasidae) from eight countries of the Old and New Worlds. Parasit Vectors 12:50. https://doi.org/10.1186/s13071-019-3303-4

    Article  PubMed  PubMed Central  Google Scholar 

  • Johnson CG (1939) Taxonomic characters, variability and relative growth in Cimex lectularius L. and C. columbarius Jenyns (Heteropt. Cimicidae). Trans R Entomol Soc Lond 89:543–568. https://doi.org/10.1111/j.1365-2311.1939.tb00736

    Article  Google Scholar 

  • Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589. https://doi.org/10.1038/nmeth.4285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kamo H, Kawashima K, Nishimura K (1957) Notes on the trombiculid mites infesting bats in Kyushu, Japan, including descriptions of two new species (Acarina: Trombiculidae). Kyushu J Med Sci 8:209–216

    Google Scholar 

  • Kejíková R, McKee C, Straková P, Šikutová S, Mendel J, Rudolf I (2022) First detection of Bartonella spp. in bat bugs Cimex pipistrelli (Hemiptera: Cimicidae). Central Eur Parasitol Res 121:3341–3345. https://doi.org/10.1007/s00436-022-07668-4

    Article  Google Scholar 

  • Khabilov TK, Tadzhibaeva DE (2021) On the current status of members of the order Chiroptera on the territory of Tajikistan. Plecotus 24:35–49 ([in Russian])

  • Kruskop SV, Fukui D (2019) Plecotus ognevi. The IUCN Red List of Threatened Species 2019:e.T136598A21996784. https://doi.org/10.2305/IUCN.UK.2019-3.RLTS.T136598A21996784.en

  • Kudryashova NI (1998) Chigger mites (Acariformes, Trombiculidae) of East Palearctics. KMK Scientific Press, Moscow ([in Russian])

  • Kudryashova NI, Lushchekina AA (2011) Chigger mites (Trombiculidae) of small mammals in Mongolia. Moscow University Publishing, Moscow ([in Russian])

  • Lv J, Wu S, Zhang Y, Chen Y, Feng C, Yuan X et al (2014) Assessment of four DNA fragments (COI, 16S rDNA, ITS2, 12S rDNA) for species identification of the Ixodida (Acari: Ixodida). Parasit Vectors 7:93. https://doi.org/10.1186/1756-3305-7-93

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lv J, Fernández de Marco MdM, Goharriz H, Phipps LP, McElhinney LM, Hernández-Triana LM et al (2018) Detection of tick-borne bacteria and babesia with zoonotic potential in Argas (Carios) vespertilionis (Latreille, 1802) ticks from British bats. Sci Rep 8:1865. https://doi.org/10.1038/s41598-018-20138-1

    Article  CAS  PubMed  PubMed Central  ADS  Google Scholar 

  • Mans BJ, Featherston J, Kvas M, Pillay KA, de Klerk DG, Pienaar R, de Castro MH, Schwan TG, Lopez JE, Teel P, Pérez de León AA, Sonenshine DE, Egekwu NI, Bakkes DK, Heyne H, Kanduma EG, Nyangiwe N, Bouattour A, Latif AA (2019) Argasid and ixodid systematics: Implications for soft tick evolution and systematics, with a new argasid species list. Ticks and Tick-borne Diseases 10(1):219–240. https://doi.org/10.1016/j.ttbdis.2018.09.010

  • Matthews AE, Klimov PB, Proctor HC, Dowling APG, Diener L, Hager SB, Larkin JL, Raybuck DW, Fiss CJ, McNeil DJ, Boves TJ (2018) Cophylogenetic assessment of New World warblers (Parulidae) and their symbiotic feather mites (Proctophyllodidae). J Avian Biol 49:e01580. https://doi.org/10.1111/jav.01580

    Article  Google Scholar 

  • McKee CD, Krawczyk AI, Sándor AD, Görföl T, Földvári M, Földvári G, Dekeukeleire D, Haarsma A-J, Kosoy MY, Webb CT, Sprong H (2019) Host Phylogeny, Geographic Overlap, and Roost Sharing Shape Parasite Communities in European Bats. Front Ecol Evol 7:69. https://doi.org/10.3389/fevo.2019.00069

    Article  Google Scholar 

  • Medvedev SG, Stanjukovich MK, Tiunov MP, Farafonova GV (1991) Ectoparasites of bats from the Far East of the USSR. Parazitologiya 25:27–38 ([in Russian])

  • Moniuszko H, Wojnarowski K, Cholewińska P (2022) Not only Leptotrombidium spp an annotated checklist of chigger mites (Actinotrichida: Trombiculidae) associated with bacterial pathogens. Pathogens 11:1084. https://doi.org/10.3390/pathogens11101084

    Article  PubMed  PubMed Central  Google Scholar 

  • Nguyen LT, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300

    Article  CAS  PubMed  Google Scholar 

  • Oba M, Omatsu T, Takano A, Fujita H, Sato K, Nakamoto A et al (2016) A novel Bunyavirus from the soft tick, Argas vespertilionis, in Japan. J Vet Med Sci 78:443–445. https://doi.org/10.1292/jvms.15-0536

    Article  CAS  PubMed  Google Scholar 

  • Olson DM, Dinerstein E, Wikramanayake ED, Burgess ND, Powell GVN, Underwood EC, D'Amico JA, Itoua I, Strand HE, Morrison JC, Loucks CJ, Allnutt TF, Ricketts TH, Kura Y, Lamoreux JF, Wettengel WW, Hedao P, Kassem KR (2001) Terrestrial ecoregions of the world: a new map of life on Earth. Bioscience 51:933–938. https://doi.org/10.1641/0006-3568(2001)051[0933:TEOTWA]2.0.CO;2

    Article  Google Scholar 

  • Ossa G, Johnson JS, Puisto AIE, Rinne V, Sääksjärvi IE, Waag A, Vesterinen EJ, Lilley TM (2019) The Klingon batbugs: Morphological adaptations in the primitive bat bugs, Bucimex chilensis and Primicimex cavernis, including updated phylogeny of Cimicidae. Ecol Evol 9:1736–1749. https://doi.org/10.1002/ece3.4846

  • Péricart J (1972) Hémiptères Anthocoridae, Cimicidae et Microphysidae de l’Ouest-Paléarctique. In: Balachowsky AS (ed) Faune de l’Europe et du Bassin Méditerranéen, vol 7. Masson et Cie éditeurs, Paris, pp 1–402

  • Racey PA (1974) Ageing and assessment of reproductive status of pipistrelle bats, Pipistrellus pipistrellus. J Zool (lond) 173:264–271

    Article  CAS  Google Scholar 

  • Robbins RG, Bangs MJ (2004) First report of Ixodes kopsteini Oudemans (Acari: Ixodida: Ixodidae) from the Kingdom of Cambodia, with a summary of known hosts of this tick in continental southeastern Asia. Proc Entomol Soc Wash 106:472–474

    Google Scholar 

  • Sándor AD, Mihalca AD, Domşa C, Péter Á, Hornok S (2021) Argasid ticks of Palearctic bats: distribution, host selection, and zoonotic importance. Front Vet Sci 8:684737. https://doi.org/10.3389/fvets.2021.684737

    Article  PubMed  PubMed Central  Google Scholar 

  • Scheffler I, Dolch D, Ariunbold J, Stubbe A, Stubbe M, Abraham A, Thiele K (2010) Ectoparasites of bats in Mongolia (Ischnopsyllidae, Nycteribiidae, Cimicidae and Spinturnicidae). Explor Biol Resour Mong 11:367–381

    Google Scholar 

  • Scheffler I, Dolch D, Ariunbold J, Stubbe A, Stubbe M, Abraham A, Thiele K (2012) Ectoparasites of bats in Mongolia, Part 2 (Ischnopsyllidae, Nycteribiidae, Cimicidae and Acari). Explor Biol Resour Mong 12:135–151

    Google Scholar 

  • Scheffler I, Jargalsaikhan A, Bolorchimeg I, Stubbe A, Stubbe M, Abraham A, Thiele KD (2016) Bat ectoparasites of Mongolia, Part 3. Explor Biol Resour Mong 13:395–408

    Google Scholar 

  • Sheng J, Jiang M, Yang M, Bo X, Zhao S, Zhang Y, Wureli H, Wang B, Tu C, Wang Y (2019) Tick distribution in border regions of Northwestern China. Ticks Tick-Borne Dis 10:665–669. https://doi.org/10.1016/j.ttbdis.2019.02.011

    Article  PubMed  Google Scholar 

  • Shluger EG (1948) New chiggers of the fauna of the USSR [Novye krasnotelki (Acari, Trombidiidae) fauny SSSR]. Entomol Rev 30:157–164 ([in Russian])

  • Sievers F, Wilm A, Dineen DG, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539. https://doi.org/10.1038/msb.2011.75

    Article  PubMed  PubMed Central  Google Scholar 

  • Socolovschi C, Kernif T, Raoult D, Parola P (2012) Borrelia, Rickettsia, and Ehrlichia species in bat ticks, France, 2010. Emerg Infect Dis 18:1966–1975. https://doi.org/10.3201/eid1812.111237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Starikov VP, Mayorova AD, Sarapultseva ES, Bernikov KA, Nakonechny NV, Morozkina AV, Borodin AV, Petukhov VA (2017) Materials on Ixodes tick (Ixodidae) of the Khanty-Mansi Autonomous Okrug-Yugra. Samara J Sci 6:88–91 ([in Russian])

  • Stekolnikov AA (2013) Leptotrombidium (Acari: Trombiculidae) of the world. Zootaxa 3728:1–173. https://doi.org/10.11646/zootaxa.3728.1.1

    Article  PubMed  Google Scholar 

  • Stekolnikov AA, Quetglas J, Ibáñez C, Sánchez-Navarro S (2022) Contribution to the fauna of chiggers (Acariformes: Trombiculidae) parasitizing bats in Spain. Acarologia 62:1201–1209. https://doi.org/10.24349/qojp-y0ow

    Article  Google Scholar 

  • Tamura K, Stecher G, Kumar S (2021) MEGA11: molecular evolutionary genetics analysis version 11. Mol Biol Evol 38:3022–3027. https://doi.org/10.1093/molbev/msab120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Titschack E (1949) Die bettwanze und die taubenwanze. Verh Dt Ges Angew Entomol 11:71–77

    Google Scholar 

  • Tiunov MP (1997) Bats of the Russian far East. Dal’nauka, Vladivostok [in Russian]

  • Tzortzakaki O, Papadatou E, Kati V, Giokas S (2019) Winners and losers in an urban bat community: a case study from southeastern Europe. Hystrix 30:134–140. https://doi.org/10.4404/hystrix-00204-2019

    Article  Google Scholar 

  • Ullah H, Kontschán J, Takács N et al (2019) A new Rickettsia honei-related genotype, two novel soft tick haplotypes and first records of three mite species associated with bats in Pakistan. Systematic Appl Acarol 24(11):2106–2118. https://doi.org/10.11158/saa.24.11.6

  • Urakami H, Tamura A, Tarasevich IV, Kadosaka T, Shubin FN (1999) Decreased prevalence of Orientia tsutsugamushi in trombiculid mites and wild rodents in the Primorye region, Far East Russia. Microbiol Immunol 43:975–978. https://doi.org/10.1111/j.1348-0421.1999.tb03358.x

    Article  CAS  PubMed  Google Scholar 

  • Usinger RL (1966) Monograph of Cimicidae. Entomological Society of America, Baltimore

    Google Scholar 

  • Varma MGR, Converse JD (1976) Keterah virus infections in four species of Argas ticks (Ixodoidea: Argasidae). J Med Entomol 13:65–70. https://doi.org/10.1093/jmedent/13.1.65

    Article  CAS  PubMed  Google Scholar 

  • Vercammen-Grandjean PH, Langston RL (1976) The chigger mites of the world (Acarina: Trombiculidae et Leeuwenhoekiidae). George Williams Hooper Foundation, University of California, San Francisco, III. Leptotrombidium complex

    Google Scholar 

  • Wen TH (ed) (1984) Sand mites of China (Acariformes: Trombiculidae et Leeuwenhoekiidae). Xue Lin Publ. House, Shanghai. [in Chinese]

  • Yamauchi T, Funakoshi K (2000) Ticks (Acari: Ixodoidea) from Chiroptera (Mammalia) of the Kyushu mainland, Japan. J Acarological Soc Japan 9:51–54

    Article  Google Scholar 

  • Yamauchi T, Abe Y, Mogi M (2021) New host and locality records of bat ticks (Acari: Ixodiadae) in Japan. Int J Acarology 47:461

    Article  Google Scholar 

  • Young MR, Proctor HC, deWaard JR, Hebert PDN (2019) DNA barcodes expose unexpected diversity in Canadian mites. Mol Ecol 28:5347–5359. https://doi.org/10.1111/mec.15292

    Article  CAS  PubMed  Google Scholar 

  • Zajkowska P, Moniuszko H, Mąkol J (2018) Host-parasite associations between bats (Mammalia: Chiroptera) and Chiggers (Trombidiformes: Trombiculidae) – a review and checklist. Ann Zool 68:97–178. https://doi.org/10.3161/00034541ANZ2018.68.1.006

    Article  Google Scholar 

  • Zhovty IF, Zarubina VN, Prokop'ev VN, Shvedko LP (1962) On bat ectoparasites in southeastern Transbaikalia and adjacent areas of the Mongolian People's Republic [Ob ektoparazitah rukokrylyh yugo-vostochnogo Zabajkal'ya i prilezhashchih rajonov Mongol'skoj Narodnoj Respubliki]. Izvestiya Nauchno-Issledovatel'skogo Protivochumnogo Instituta Sibiri i Dal'nego Vostoka 24:338–343 ([in Russian])

Download references

Acknowledgements

We would like to thank Oleg N. Morozov (Center of Children’s Complementary Education and Evenkis’ Folk Crafts, Bagdarin, Russia), Alexandra P. Shumkina and Elena Yu. Shumkina (“Mechta”, Irkutsk, Russia), Vadim V. Bobrovsky and Polina S. Van (Petrenko) (Komsomolsk-on-Amur, Russia), Ekaterina Krival’ (Kyren, Russia), Evgeny E. Kozlovsky (Yuzhno-Kurilsk, Russia), Vasily V. Gorobeyko (Vladivostok, Russia), and “Altyn-Emel” State National Nature Park (Almaty, Kazakhstan) for their help in mounting the expeditions, and Dr. Dimitry A. Gapon (Zoological Institute of the Russian Academy of Sciences, St. Petersburg, Russia) for his help in the identification of bugs. Molecular genetic studies were held in the Institute of Environmental and Agricultural Biology (X-BIO), University of Tyumen, and Collective Research Center “Center for the development of progressive personalized technologies for health” (SC FHHRP, Irkutsk, Russia). Authors would like to thank PhD Viacheslav V. Sinkov (SC FHHRP, Irkutsk, Russia) for technical assistance in sequencing.

Funding

The study was carried out by D.V.K. with the support of the Priority 2030 program of the Ministry of Science and Higher Education of Russian Federation. Authors D.V.K., M.A.Kh., A.A.A., and U.V.G. have received research support and receives a salary from University of Tyumen, Scientific Centre for Family Health and Human Reproduction Problems, Lomonosov Moscow State University, and Federal Scientific Center of the East Asia Terrestrial Biodiversity (SB RAS), respectively.

Author information

Authors and Affiliations

  1. Institute of Environmental and Agricultural Biology (X-BIO), University of Tyumen, Volodarskogo, 6, 625003, Tyumen, Russia

    Denis V. Kazakov

  2. Federal State Public Science Institution “Scientific Centre for Family Health and Human Reproduction Problems”, Timiryazeva, 16, Irkutsk, 664003, Russia

    Maxim A. Khasnatinov

  3. Department of Entomology, Faculty of Biology, Lomonosov Moscow State University, Leninskie Gory, 1-12, Moscow, 119234, Russia

    Anastasia A. Antonovskaia

  4. Federal Scientific Center of the East Asia Terrestrial Biodiversity, Far Eastern Branch of the Russian Academy of Sciences, 100-Letiya Vladivostoka, Vladivostok, 159, 690022, Russia

    Uliana V. Gorobeyko

Authors
  1. Denis V. Kazakov
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maxim A. Khasnatinov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anastasia A. Antonovskaia
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Uliana V. Gorobeyko
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

D.V.K. conceived and designed the study. D.V.K., M.A.Kh., and U.V.G. collected the bat ectoparasites in the field. A.A.A. identified trombiculid mites. M.A.Kh. identified ixodid and argasid ticks. D.V.K. and M.A.Kh. performed molecular and data analyses. D.V.K., M.A.Kh., A.A.A., and U.V.G. prepared the manuscript.

Corresponding author

Correspondence to Denis V. Kazakov.

Ethics declarations

Competing interests

The authors declare no competing interests.

Ethics approval

All procedures involving animals were in compliance with the European Convention for the Protection of Vertebrate Animals used for Experimental and Other Scientific Purposes (Strasbourg, 18 March 1986), and ethical approval was granted by the University of Tyumen Biomedical Ethic Committee (No. 8, July 2023, Tyumen, Russia). All bat species in this study are listed in The IUCN Red List of Threatened Species (Coroiu 2016a, b; Csorba and Hutson 2016; Fukui et al. 2019; Kruskop and Fukui 2019; Fukui and Sano 2020; Godlevska et al. 2020, 2021) as Least Concern.

Consent to participate

This is not applicable to the present manuscript.

Consent for publication

All authors reviewed and approved the final version of the manuscript.

Conflict of interest

The authors declare no competing interests.

Additional information

Section Editor: Otranto Domenico

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 265 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kazakov, D.V., Khasnatinov, M.A., Antonovskaia, A.A. et al. Bat ectoparasites: chigger mites (Trombiculidae), ticks (Ixodidae and Argasidae), and bugs (Cimicidae) in the Eastern Palaearctic. Parasitol Res 123, 83 (2024). https://doi.org/10.1007/s00436-023-08093-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00436-023-08093-x

Keywords

Search

Navigation