The first data on the infestation of the parti-coloured bat, Vespertilio murinus (Chiroptera, Vespertilionidae), with gamasid mites, Steatonyssus spinosus (Mesostigmata, Gamasina, Macronyssidae)

Orlova M.V., Kazakov D.V., Orlov O.L., Mishchenko V.A., Zhigalin A.V.

P. 66-73

This article presents one of the very few records of a macronyssid mite (Mesostigmata, Gamasina, Macronyssidae) infestation of vesper bats (Chiroptera, Vespertilionidae). It is the first report of the influence of host parameters on the infestation of the parti-coloured bat, Vespertilio murinus, by the mite Steatonyssus spinosus. It has been shown that the infestation varies considerably throughout the host’s occupation of summer roosts and the highest infestation was observed in the post-lactation period. Female bats are infested significantly more intensively than male bats due to changes in their immune status during pregnancy and lactation. The infestation decreases in the period when the breeding colony disbands due to both roost switching and the intensification of grooming during this period.DOI: 10.15298/rusjtheriol.16.1.06

• Balashov Y.S. 2009. [Parasitism of ticks and insects on vertebrates]. Saint-Petersburg: Nauka. 358 p. [in Russian].
• Baley J.E. & Schacter B.Z. 1985. Mechanisms of diminished natural killer cell activity in pregnant women and neonates // Journal of Immunology. Vol.134. P.3042–3048.
• Benda P.& Horáček I. 1998. Bats (Mammalia: Chiroptera) of the Eastern Mediterranean. Part 1. Review of distribution and taxonomy of bats in Turkey // Acta Societatis Zoologicae Bohemicae. Vol.62. P.255–313.
• Benda P., Faizolahi K., Andreas M., Obuch J., Reiter A., Ševčík M., Uhrin M., Vallo P. & Ashraf S. 2012. Bats (Mammalia: Chiroptera) of the Eastern Mediterranean and Middle East. Part 10. Bat fauna of Iran // Acta Societatis Zoologicae Bohemicae. Vol.76. P.163–582.
• Borisenko A.V. 1999. [Mobil trap for bat catching] // Plecotus et al. Vol.2. P.10–19 [in Russian with English summary].
• Booth D.T., Clayton D.H. & Block B.A. 1993. Experimental demonstration of the energetic cost of parasitism in free-ranging hosts // Proceedings of the Royal Society of London. Biological Sciences. Vol.253. P.125–129.
• Christe P., Arlettaz R. & Vogel P.2000. Variation in intensity of a parasitic mite (Spinturnix myoti) in relation to the reproductive cycle and immunocompetence of its bat host (Myotis myotis) // Ecology Letters. Vol.3. P.207–212.
• Christe P., Giorgi M.S., Vogel P. & Arlettaz R. 2003. Differential species-specific ectoparasitic mite intensities in two intimately coexisting sibling bat species: resource-mediated host attractiveness or parasite specialisation? // Journal of Animal Ecology. Vol.72. P.866–872.
• Christe P., Glaizot O., Evanno G., Bruyndonckx N., Devevey G., Yannic G., Patthey P., Maeder A., Vogel P. & Arlettaz R. 2007. Host sex and ectoparasites choice: preference for and higher survival on female hosts // Journal of Animal Ecology. Vol.76. P.703–710.
• Clayton D.H. 1991. Coevolution of avian grooming and ectoparasite avoidance // Loye J.E. & Zuk M. (eds.). Bird-parasite interactions, ecology, evolution and behavior. New York: Oxford University Press. P.258–289.
• Dick C.W. & Patterson B.D. 2006. Bat flies: obligate ectoparasites of bats // Morand S., Krasnov B. & Poulin R. (eds.). Micromammals and Macroparasites: From Evolutionary Ecology to Management. Tokyo: Springer-Verlag Publishing. P.179–194.
• Dusbabek F. 1972. The zone of bat acarinia in Central Europe // Folia parasitologica. Vol.19. P.139–154.
• Encarnaзгo J.A., Baulechner D. & Becker N.I. 2012. Seasonal Variations of Wing Mite Infestations in Male Daubenton’S Bats (Myotis daubentonii) in Comparison to Female and Juvenile Bats // Acta Chiropterologica. Vol.14. No.1. P.153–159.
• Faraway J.J. 2006. Extending the linear model with R: Generalized linear, mixed effects and nonparametric regression models. Boca Raton-London-New York: Chapman & Hall/CRC. P.331.
• Furukawa K., Itoh K., Okamura K., Kumagai K. & Suzuki M. 1984. Changes in NK cell activity during the estrous cycle and pregnancy in mice // Journal of Reproductive Immunology. No.6. P.353–363.
• Giorgi M.S., Arlettaz R., Christe P. & Vogel P. 2001. The energetic grooming costs imposed by a parasitic mite (Spinturnix myoti) upon its bat host (Myotis myotis) // Proceedings of the Royal Society of London. Biological Sciences. Vol.268. P.2071–2075.
• Grossman C.J. 1985. Interactions between the gonadalsteroids and the immune system // Science. Vol.227. P.257–261.
• Haitlinger R. 1978. Pasozyty zewnetrzne nietoperzy Dolnego Śląska. III. Spinturnicidae, Argasidae, Ixodidae (Acarina) // Wiadomosci parazitologiezne. Vol.24. P.475–490.
• Hart B.L. 1997. Behavioural defence // Clayton D.H. & Moore J. (eds.) Host-parasite evolution. General principles and avian models. NewYork: Oxford University Press. P.59–77.
• Hosken D.J. & O’Shea J.E. 2001. Sperm production and immune function in two Australian bats, Chalinolobus morio and Nyctophilus geoffroyi // Ethology Ecology & Evolution. Vol.13. P.173–180.
• Khabilov T.K. 1992. [Mammals. Bats]. Dushanbe: Donish, 351 p. [In Russian, with English summary].
• Klein S.L. 2000. The effects of hormones on sex differences in infection: from genes to behavior // Neuroscience & Biobehavioral Reviews. Vol.24. P.627–638.
• Klein S.L. 2004. Hormonal and immunological mechanisms mediating sex differences in parasite infection. Parasite Immunology. Vol.26. No.6–7. P.247–264.
• Kurta A., Bell G.P., Nagy K.A. & Kunz T.H. 1989. Energetics of pregnancy and lactation in free-ranging little brown bats (Myotis lucifugus) // Physiological Zoology. Vol.62. P.804–818.
• Kurta A., Kunz T.H. & Nagy K.A. 1990. Energetics and water flux of free-ranging big brown bats (Eptesicus fuscus) during pregnancy and lactation // Journal of Mammalogy. Vol.71. P.59–65.
• Lourenзo S. & Palmeirim J.M. 2008. Which factors regulate the reproduction of ectoparasites of temperate-zone cave-dwelling bats? // Parasitology Research. Vol.104. No.1. P.127–134.
• Lučan R.K. 2006. Relationships between the parasitic mite Spinturnix andegavinus (Acari: Spinturnicidae) and its bat host, Myotis daubentonii (Chiroptera: Vespertilionidae): seasonal, sex- and age-related variation in infestation and possible impact of the parasite on the host condition and roosting behaviour // Folia Parasitologica. Vol.53. P.147–152.
• Mastitskiy S.E. & Shitikov V.K. 2015. [Statistical analysis and data visualisation using R]. Moscow: DMK-Press. 496 p. [in Russian].
• McKay L.I. & Cidlowski J.A. 1999. Molecular control of immune/inflammatory responses: interactions between nuclear factor kappa B and steroid receptor-signaling pathways // Endocrine Reviews. Vol.20. P.435–459.
• McLean J.A. & Speakman J.R. 1997. Non-nutritional maternal support in the brown long-eared bat // Animal Behaviour. Vol.54. P.1193–1204.
• Marshall A.G. 1981. The ecology of ectoparasitic insects. London: Academic Press. 459 p.
• Miller L. & Hunt J.S. 1996. Sex steroid hormones and macrophage function // Life Sciences. Vol.59. P.1–14.
• Micherdzinski W. 1980. Eine Taxonomische Analyse der Familie Macronyssidae Oudemans, 1936. I: Subfamilie Ornithonyssinae Lange, 1958 (Acarina: Mesostigmata). Warszawa: Polska Akademia Nauk. 254 p.
• Mшller A.P., De Lope F., Moreno J., Gonzales G. & Perez J.J. 1994. Ectoparasites and host energetics: house martin bugs and house martin nestlings // Oecologia. Vol.98. P.263–268.
• Mooring M.S. & Hart B.L. 1995. Differential grooming rate and tick load of territorial-male and female impala, Aepyceros melampus // Behavioural Ecology. Vol.6. P.94–101.
• Morales-Montor J., Mohamed F. & Damian R.T. 2004. Schistosoma mansoni: the effect of adrenalectomy on the murine model // Microbes and Infection. Vol.6. No.5. P.475–480.
• Ogajanyan A.M. & Arutyunyan E.S. 1974. [Mites of fam. Macronyssidae Oudemans, 1936 (Parasitiformes, Gamasoidea) parasitizing bats of Armenia] // Biological Journal of Armenia. Vol.27. No.10. P.75–82. [In Russian with Armenian summary].
• Orlova M.V., Orlov O.L. & Kshnyasev I.A. 2012. Changes in the abundance of parasitic gamasid mite Macronyssus corethroproctus (Oudemans, 1902) during the overwintering period of its host, the Pond bat Myotis dasycneme (Boie, 1825) // Russian Journal of Ecology. Vol.43. No.4. P.328–332.
• Orlova M.V. 2013. Ectoparasites of the parti-coloured bat (Vespertilio murinus Linnaeus, 1758, Chiroptera, Mammalia) in the Urals and adjacent regions // Entomological Review. Vol.93. No.9. P.1236–1242.
• Orlova M.V., Kshnyasev I.A., Orlov O.L. & Zhigalin A.V. 2015a. Some factors behind density dynamics of bat flies (Diptera, Nycteribiidae) — ectoparasites of the boreal chiropterans: omitted predictors and hurdle model identification // Vestnik zoologii. Vol.49. No.4. P.333–340.
• Orlova M., Orlov O., Zhigalin A. & Mishchenko V. 2015b. Comparative analysis of vespertilionid bats’ (Chiroptera: Vespertilionidae) infestation with gamasid mites of the genus Macronyssus Kolenati, 1858 during hibernation in the Urals and Western Siberia // Zoology and Ecology. Vol.25. No.4. P.314–318.
• Orlova M.V., Stanyukovich M.K. & Orlov O.L. 2016. Gamasid mites (Mesostigmata: Gamasina) parasitizing bats (Chiroptera: Rhinolophidae, Vespertilionidae, Molossidae) of Palaearctic boreal zone (Russia and adjacent countries). Tomsk: TSU Publishing House. 150 p.
• Pinchuk L.M. 1971. [Mites of the genus Steatonyssus (Parasitiformes: Macronyssidae) from bats of Moldova] // Animal and plant parasites. Kishinev. Vol.7. P.110–115 [in Russian].
• Racey P.A. 2009. Reproductive assessment of bats // Kunz T.H. & Parsons S. (eds.) Ecological and behavioural methods for the study of bats. Baltimore: Johns Hopkins University Press. P.249–264.
• Reckardt K. & Kerth G. 2009. Does the mode of transmission between hosts affect the host choice strategies of parasites? Implications from a field study on bat fly and wing mite infestation of Bechstein’s bats // Oikos. Vol.118. P.183–190.
• Roulin A., Brinkhof M.W.G., Bize P., Richner H., Jungi T.W., Bavoux C., Boileau N. & Burneleau G. 2003. Which chick is tasty to parasites? The importance of host immunology vs. parasite life history // Journal of Animal Ecology. Vol.72. P.75–81.
• Rupp D., Zahn A. & Ludwig P. 2004. Actual records of bat ectoparasites in Bavaria (Germany) // Spixiana. Vol.27. No.2. P.185–190.
• R Development Core Team. 2011. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. Available from: http://www.R-project.org
• Rybin S.N. 1983. [Gamasid mites of bats and their shelters in South Kyrgyzstan] // Parasitologiya. Vol.17. No.5. P.355–360 [in Russian with English summary].
• Rydell J. & Baagшe H.J. 1994. Vespertilio murinus // Mammalian Species. Vol.467. P.1–6.
• Savita X.X., Rai U. 1998. Sex steroid hormones modulate the activation of murine peritoneal macrophages: receptor mediated modulation // Comparative Biochemistry and Physiology. Part C: Pharmacology, Toxicology and Endocrinology. Vol.119. P.199–204.
• Sharifi M., Mozafari F., Taghinezhad N. & Javanbakht H. 2008. Variation in ectoparasite load reflects life history traits in the lesser mouse-eared bat Myotis blythii (Chiroptera: Vespertilionidae) in western Iran // Journal of Parasitology. Vol.94. No.3. P.622–625.
• Shitikov V.K., Rosenberg G.S. 2014. [Randomization and bootstrap: a statistical analysis in biology and ecology using R]. Togliatti: Cassandra. 314 p. [In Russian with English summary].
• Stanyukovich M.K. 1990. [Gamasid mites and argasid ticks of bats from Pribaltica and Leningrad district] // Parasitologiya. Vol.24. No.3. P.193–199 [in Russian with English summary].
• Stanyukovich M.K. 1993. [Gamasid mites of bats from Russia and adjunct countries (Gamasina: Spinturnicidae, Macronyssidae)]: thes. diss.… PhD. St. Petersburg. 16 p. [In Russian].
• Stanyukovich M.K. 1997. Keys to the gamasid mites (Acari: Parasitiformes, Mesostigmata, Macronyssoidea et Laelaptoidea) parasiting bats (Mammalia, Chiroptera) from Russia and adjacent countries // Rudolstдdter naturhistorische Schriften. Vol.7. P.13–46.
• Sundary A.A., Bogdanowicz W., Varman D.R., Marimuthu G. & Rajan K.E. 2012. Ectoparasite Raymondia lobulata infestation in relation to the reproductive cycle of its host — the greater false vampire bat Megaderma lyra // Journal of Parasitology. Vol.98. P.60–62.
• Teng K.F. 1980. Notes on the genus Steatonyssus in China (Acarina: Macronyssidae) // Acta Zootaxonomica Sinica. Vol.5. No.1. P.59–62.
• Till W.M. & Evans G.O. 1964. The genus Steatonyssus Kolenati (Acari: Mesostigmata) // Bulletin of the British Museum (Natural History). Vol.11. P.511–582.
• Toder V., Nebel L., Elrad H., Blank M., Durdana A. & Gleicher N. 1984. Studies of natural killer cells in pregnancy. II. The immunoregulatory effect of pregnancy substances // Journal of Clinical Immunology. Vol.14. P.129–133.
• Vasen’kov D. A. & Potapov M. A. 2007. [Using body condition index in a study of bat ecology] // Plecotus et al. Vol.10. P.21–31 [in Russian with English summary].
• Wikel S.K. 1996. The immunology of host-ectoparasitic arthropod relationships. Wallingford: CAB International. 331 p.
• Whitaker J.O., Jr. 1988. Collecting and preserving ectoparasites for ecological study // Kunz T.H. (ed.) Ecological and Behavioral Methods for the Study of Bats. Washington: Smithsonian Inst. Press. P.459–474.
• Zahn A. & Rupp D. 2004. Ectoparasite load in European vespertilionid bats // Journal of Zoology. London. Vol.262. No.4. P.1–9.
• Zhang L., Parsons S., Daszak P., Wei L., Zhu G. & Zhang S. 2010. Variation in the abundance of ectoparasitic mites of flat-headed bats // Journal of Mammalogy. Vol.91. No.1. P.136–143.
• Zemskaya A.A. 1973. [Parasitic gamasid mites and their medical importance]. Moscow: Meditsina. 167 p. [In Russian].