The first record of an unknown Coccidea Leuckart, 1879 in the midgut of trombiculid larvae Hirsutiella zachvatkini (Acariformes, Trombiculidae)
Journal:
2025. 33 (2)Author:
Shatrov, A. B.About author:
Shatrov, A. B., e-mailZoological Institute, Russian Academy of Sciences, St. Petersburg, Russia
Acknowledgments:
This study was supported by the State Government Research Programs No. 125013001089-0. The confocal laser microscopy was performed in the Core Facilities Centre Taxon at the Zoological Institute of the Russian Academy of Sciences (St. Petersburg, Russia) with the help of Dr. A.A. Petrov.
Annotation:
For the first time, unknown protists were found in the midgut of larvae Hirsutiella zachvatkini (Schluger, 1948) (Trombiculidae), feeding on a bank vole Clethrionomys glareolus in the Pskovskaya Oblast (Russia). The same protozoans were also identified in the tissues of the vole. Generally, these cells were spindle-shaped, around 4 µm in length, exhibiting a violet cytoplasm and a blue centrally located elongated nucleus, as highlighted by staining. Most probably, these cells represent one of the Babesia (Piroplasmida) species in a single-cell stage (e. g., sporozoites), which got into the vole accidentally as a result of a possible tick bite. Alternatively, these cells represent one of the Toxoplasma (Eimeriida) species in the individual cell form (e. g., tachyzoites or sporozoites) that may be encountered in other animals. However, a single instance of the presence of protozoans in trombiculid larvae may suggest that (i) the circulation of protozoans among the population of voles or trombiculids in northwestern Russia is highly restricted and is not of an epidemiological importance and (ii) this path of infection is blind and may cause the subsequent death of both the larva and the protists.
Bibliography:
Alimov, A. F. (Ed.). 2007. Protista: Handbook on Zoology. Nauka, St. Petersburg. Pt. 2. 1144 pp.
Archibald, J. M., Simpson, A. G. B. and Slamovits, C. H. (Eds.). 2017. Handbook of the Protists. 2nd ed. Springer International Publishing AG. 1657 pp. https://doi.org/10.1007/978-3-319-28149-0
Audy, J. R. 1951. Trombiculid mites and scrub itch. Australian Journal of Sciences, 14: 94–96.
Ben-Harari, R. R. 2019. Tick transmission of toxoplasmosis. Expert Review of Anti-infective Therapy, 17: 911–917. https://doi.org/10.1080/14787210.2019.1682550
Boese, J. L. 1972. Tissue reactions at the site of attachment of chiggers. Journal of Medical Entomology, 9: 591.
Dubey, J. P. and Sreekumar, C. 2003. Redescription of Hammondia hammondi and its differentiation from Toxoplasma gondii. International Journal of Parasitology, 33: 1437–1453. https://doi.org/10.1016/S0020-7519(03)00141-3
Elliott, I., Pearson, I., Dahal, P., Thomas, N. V., Roberts, T. and Newton, P. N. 2019. Scrub Typhus Ecology: A Systematic Review of Orientia in Vectors and Hosts. Parasites and Vectors, 12: 513. https://doi.org/10.1186/s13071-019-3751-x
Filippova, N. A. 1997. Iksodovyye Kleshchi Podsemeystva Amblyomminae [Ixodod Ticks of the Subfamily Amblyomminae]. Fauna of Russia and Neighbouring Countries. Arachnoidea. Vol. 4. Iss. 4. Nauka, St. Petersburg, 436 pp. [In Russian]
Hinze-Selch, D. 2015. Toxoplasma gondii infection and neuropsychiatric disease: current insight. Reports in Parasitology, 4: 43–51.
Karbowiak, G. 2004. Zoonotic reservoir of Babesia microti in Poland. Poland Journal of Microbiology, 53, Suppl: 61–65.
Kawamura, A., Tanaka, H. and Tamura, A. 1995. Tsutsugamushi Disease. University of Tokyo Press, Tokyo, 362 pp.
Kudryashova, N. I. 1998. Krasnotelkovyye kleshchi (Acariformes, Trombiculidae) Vostochnoi Palearctiki [Chigger mites (Acariformes, Trombiculidae) of East Palearctics]. KMK Scientific Press, Moscow, 342 pp. [In Russian]
Kuznetsov, Yu. E., Lunina, G. A., Tokarevich, N. K., Kozlov, S. S., Karmokov, I. A., et al. 2024. [Prevalence of Ixodid ticks collected on the territory of some entities of the Northwestern Federal district in relation to Babesia spp.] Medical Parasitology and Parasitic Diseases, 3: 10–15. https://doi.org/10.33092/0025-8326mp2024.3.10-15 [In Russian]
Lillie, R. D. 1969. Patogistologicheskaya Tekhnika i Prakticheskaya Gistokhimiya [Histopathological Technic and Practical Histohemistry]. Mir, Moscow, 639 pp. [In Russian]
Pérez de León, A. A, Vannier, E., Almazán, C., Krause, P. J. 2013. Tick-borne Protozoa. In: D. E. Sonenshine and R. M. Roe (Eds.), Biology of Ticks. Vol. 2. 2nd ed. Oxford University Press, Oxford, pp. 147–179.
Seo, M.-G. and Kwak, D. 2025. Molecular detection of Toxoplasma gondii in ticks and their respective host dogs. Parasites, Hosts and Diseases, 63: 66–74. https://doi.org/10.3347/PHD.24091
Shatrov, A. B. 2000. Krasnotelkovyye kleshchi (Acariformes, Trombiculidae) i ich parasitism na pozvonochnich zhivotnich [Trombiculid mites and their parasitism on vertebrate hosts]. St. Petersburg University Publishers, St. Petersburg, 276 pp. [In Russian with English summary]
Shatrov, A. B. 2009. Stylostome formation in trombiculid mites (Acariformes: Trombiculidae). Experimental and Applied Acaroljgy, 49: 261–280. 10.1007/s10493-009-9264-0
Shatrov, A. B. and Antonovskaia, A. A. 2021. Stylostome of the trombiculid mite larvae Neotrombicula talmiensis (Schluger, 1955) (Acariformes, Trombiculidae) feeding on two host species in the Russian Far East. Acarologia, 61: 412–431. https://doi.org/10.24349/acarologia/20214442
Shatrov, A. B., and Mirolubov, A. A. 2015. Stylostome and feeding of the trombiculid larva Neotrombicula tianshana Shao et Wen, 1984 (Acariformes: Parasitengona) from the Baikal region. International Journal of Acarology, 41: 537–550. https://doi.org/10.1080/01647954.2015.1079238
Shatrov, A. B. and Stekolnikov, A. A. 2011. Redescription of a human-infesting European trombiculid mite Kepkatrombicula desaleri (Acari: Trombiculidae) with data on its mouthparts and stylostome. International Journal of Acarology, 37: 176–193. https://doi.org/10.1080/01647954.2010.548342
Shatrov, A. B., Kazakov, D. V., Antonovskaia, A. A. and Gorobeyko, U. V. 2022. Morphological characterization of stylostome and skin reaction produced by Leptotrombidium album (Acariformes, Trombiculidae) on the bat Barbastella pacifica from Kunashir Island. Systematic and Applied Acarology, 27: 1970–1990. https://doi.org/10.11158/saa.27.10.9
Shatrov, A. B., Takahashi, M., Noda, S. and Misumi, H. 2014. Stylostome organization in feeding Leptotrombidium larvae (Acariformes: Trombiculidae). Experimental and Applied Acarology, 64: 33–47. https://doi.org/10.1007/s10493-014-9809-8
Skotarczak, B. I. 2016. The role of ticks in transmission cycle of Toxoplasma gondii. Annals of Parasitology. 62: 185–191. https://doi.org/10.17420/ap6203.52
Takahashi, M., Misumi, H., Urakami, H., Nakajima, S., Furui, S., Yamamoto, S., Furuya, Y., Misumi, M. and Matsumoto, I. 2004. Mite vector (Acari: Trombiculidae) of scrub typhus in a new endemic area in Northern Kyoto, Japan. Journal of Medical Entomology, 41: 107–114.
Telford, S. R., Mather, T. N., Adler G. H. and Spielman A. 1990. Short-tailed shrews as reservoirs of the agent of Lyme disease and human babesiosis. Journal of Parasitology, 76: 681–683.
Tołkacz, K., Bednarska, M., Alsarraf, M., Dwużnik, D., Grzybek, M., Welc-Falęciak, R., Behnke, J. M. and Bajer, A. 2017. Prevalence, genetic identity and vertical transmission of Babesia microti in three naturally infected species of vole, Microtus spp. (Cricetidae). Parasites and Vectors, 10: 66. https://doi.org/10.1186/s13071-017-2007-x
Traub, R. and Wisseman, C. L. 1974. The ecology of chigger-borne rickettsiosis (scrub-typhus). Journal of Medical Entomology, 11: 237–303.
Traub, R., Wisseman, C. L., Jones, M. R. and O’Keefe, J. J. 1975. The acquisition of Rickettsia tsutsugamushi by chiggers (trombiculid mites) during the feeding process. Annals of the New York Academy of Sciences, 266: 91–114.
Truong, A. T., Yoo, M. S., Min, S. et al. 2022. Toxoplasma gondii and Rickettsia spp. in ticks collected from migratory birds in the Republic of Korea. Scientific Reports, 12: 12672. https://doi.org/10.1038/s41598-022-16785-0
Vannier, E., Peter, J. and Krause, P. J. 2012. Human babesiosis. New England Journal of Medicine, 366: 2397–2407.
Westblade, L. F., Simon, M. S., Mathison, B. A. and Kirkman L. A. 2017. Babesia microti: from mice to ticks to an increasing number of highly susceptible humans. Journal of Clinical Microbiology, 55: 2903–2912. https://doi.org/10.1128/JCM.00504-17
Wrenn, W. J. 1996. Immune responses to mange mites and chiggers. In: S. Wikel (Ed.), The Immunology of Host-Ectoparasitic Arthropod Relationships. CAB International, Wallingford, UK, pp. 259–289.
Wright, S. M., Wikel, S. K. and Wrenn W. J. 1988. Host immune responsiveness to the chigger, Eutrombicula cinnabaris. Annals of Tropical Medicine and Parasitology, 82: 283–293.