Current state of Acarapis Hirst mites (Acariformes, Tarsonemidae) distribution and honeybees infestation in Russia
This paper summarized the distribution of the Acarapis Hirst mites in Russia. Honeybees are parasitized by three mites species of the Acarapis genus: A. woodi Rennie, 1921, A. externus Morgenthaler, 1931 and A. dorsalis Morgenthaler, 1934. The first species, the tracheal mite, parasitizes in the tracheae of the bees and causes acarapidosis. In Russia, the tracheal mite was first found in 1926. During the 20th century, it was detected in several regions of the European part of the country and the Urals. We concluded there had been practically no registered cases in the country before 1991. However, starting from 1991, many newly discovered tracheal mites have been revealed in all geographical regions of Russia: in the European part, in the North Caucasus, in the Urals, in Siberia, and the Far East. Besides the tracheal mite's geographical expansion, a steady increase in this disease is observed in Russia. Two other species of external mites of Acarapis genus, causative agents of exoacarapidosis, are known to be found in far fewer cases in Russia, which is probably connected with little research on this disease's topic and perception as not a serious one.
Keywords: Acarapidosis, tracheal mite, Acarapis woodi, Acarapis externus, Acarapis dorsalis, Russia
Ahn, A.J., Ahn, K.S., Noh, J.N., Kim, Y.H, Yoo, M.S., Kang, S.W., Yu, D.H., Shin, S.S. (2015). Molecular prevalence of Acarapis mite infestations in honey bees in Korea. Korean Journal of Parasitology, 53(3), 315-320.
Bacandritsos, N.K., Saitanis, C.J. (2004). A field study on the long-term incidence of Acarapis woodi in Greece. Journal of Apicultural Research, 43, 21–26.
Bailey, L. (1985) Acarapis woodi: a modern appraisal. Bee World, 66(3), 99–104.
Bakina, S.N. (2016). Ecological and genetic aspects of breeding Central Russian bee colonies to reduce aggressiveness. Abstract of Doctoral Dissertation. Divovo (in Russian).
Belgorod Interregional Veterinary Laboratory (2016). The performance results for the first nine months of 2016. Available from: http://belmvl.ru/obyazatelnaya-informacziya/otchetyi-o-rezultatax-deyatelnosti/rezultatyi-deyatelnosti-za-9-mesyaczev-2016-g.pdf
Belyaeva, N.A. (2016). The disease of adult bees and the efficiency of the beekeeping industry. Znaniye, 2-3(31), 34-37 (in Russian).
Bober, A., Gajda, A. (2019). Akarapidoza – zapomniana choroba. Pasieka, 4, 14-19 (in Polish).
Chantawannakul, P., De Guzman, L., Li J., Williams, G.R. (2016). Parasites, pathogens, and pests of honeybees in Asia. Apidologie, 47(3), 301-324.
Danilin, B.F. (1958). External bee parasitic mites. Pchelovodstvo, 11, 45-46 (in Russian).
De Guzman, L., Rinderer, T.E., Burgett, D.M., Frake, A.M. (2019). Understanding the trends in prevalence and abundance of Acarapis dorsalis and Acarapis externus in Apis mellifera colonies. Trends in Entomology, 15, 85-98.
De Guzman, L., Rinderer, T.E., Delatte, G.T., Stelzer, J.A., Beaman, L., Kuznetsov, V. (2002). Resistance to Acarapis woodi by honey bees from far-eastern Russia. Apidologie, 33, 411–415.
De Jong, D.D., Morse, R.A., Eickwort, G.C. (1982). Mite pests of honey bees. Annual Review of Entomology, 27(1), 229-252.
Decision of the Rosselkhoznadzor on the establishment of statuses of regions of the Russian Federation for infectious animal diseases and conditions for the movement of goods subject to Veterinary surveillance (Control) by the Rosselkhoznadzor (approved on January 20, 2017). Available from: https://fsvps.gov.ru/fsvps/laws/7770.html
Delfinado-Baker, M., Baker, E.W. (1992). Notes on honey bee mites of the genus Acarapis Hirst (Acari: Tarsonemidae). International Journal of Acarology, 8, 211-226.
Dizer, Yu.B. (1953). To the morphology of the Acarapis woodi Rennie mite, an endoparasite of the honey bee. Zoologicheskii Zhurnal, 32(4), 626-630 (in Russian).
Dolgieva, Z.M., Bazgiev, M.A., Badurgova, K.Sh., Dolgiev, M-G.M., Yandiev, A.M., Katsiev, A.-A.S. (2018). New knowledge on the productivity of planned bee breeds in the Republic of Ingushetia. Gornoye Selskoye Khozyaystvo, 3, 140-144 (in Russian).
Domatskaya, T.F., Domatsky, A.N., Zinatullina, Z.Ya. (2019a). Invasions and infections of Apis mellifera honey bees in apiaries of the Tyumen region and other regions of Russia. Biomics, 11(2), 125-130 (in Russian).
Domatskaya, T.F., Domatsky, A.N., Zinatullina, Z.Ya. (2019b). Mixed infestations - infections of honey bees in apiaries of the Tyumen region. Actual problems of agriculture in mountainous areas. Materials of the VII International Scientific and Practical Conference. Gorno-Altaysk: GAGU, 260-264 (in Russian).
Domatskaya, T.F., Domatsky, A.N., Zinatullina, Z.Ya. (2020). Distribution of diseases of honey bees in apiaries of the Tyumen region. Bulletin of KrasSAU, 7, 87-92 (in Russian).
Domatskaya, T.F., Stolbov, N.M. (2009). 35 years of the Laboratory of Bee Diseases of the All–Union Scientific Research Institute of Veterinary Entomology and Arachnology. Pchelovodstvo, 9, 6-8 (in Russian).
Downey, D.L., Winston, M.L. (2001). Honey bee colony mortality and productivity with single and dual infestations of parasitic mite species. Apidologie, 32, 567-575.
Eishen, F. (1987). Overwintering performance of honey bee colonies heavily infested with Acarapis woodi (Rennie). Apidologie, 18(4), 293-304.
Fakhimzadeh, K., Hokkanen, H., Sikkilä, J., Pirhonen, K., Lintula, E. (1993). The First Survey of Acarapis woodi in Finland. Bee World, 74(3), 129-132.
Fedorenko, L.N., Lysenko, A.A. (2012). Epizootological monitoring transmissible diseases of bees in Krasnodar region. Topical problems in veterinary medicine. Proceed. XI Siberian Veterinary Conference. Novosibirsk: NSAU, 173-174 (in Russian).
FGBI Federal Centre for Animal Health (ARRIAH). Available from: http://www.arriah.ru/en
Gaponova, V.S., Grobov, O.F. (1978). Mite-borne bee disease. Moscow: Rosselkhozizdat, 91pp. (in Russian).
Garrido-Bailón, E., Bartolomé, C., Prieto, L. (2012). The prevalence of Acarapis woodi in Spanish honey bee (Apis mellifera) colonies. Experimental Parasitology, 132(4), 530-536.
Giordani, G. (1965). Recherches au laboratoire sur Acarapis woodi (Rennie), agent de l'acariose des abeilles (Apis mellifera L.). Bulletin apicole, 8, 76-159.
Grobov, O.F. (1978). Nest mites of the honey bee (Apis mellifera L.): their meaning and basic principles of fighting mite-borne lesions. Doctor's degree dissertation. Moscow,. (in Russian).
Grobov, O.F. (1991). Mites: parasites of bees and pests of their products. Moscow: Rosagropromizdat. (in Russian).
Grobov, O.F., Smirnov, A.M., Popov, E.T. (1987). Diseases and pests of honey bees. Moscow: Agropromizdat (in Russian).
Ibay, L.A. (1989). Biology of the two external Acarapis species of honeybees, Acarapis dorsalis and Acarapis externus (Acari: Tarsonemidae). M. S. Oregon State University, USA.
Ilyina, E.K., Aladina, O.N. (2014). Epizootology of diseases of the honeybee on the territory of the Orenburg region. Bulletin of the Orenburg State Agrarian University, 4, 183-185 (in Russian).
Kashina, G.V. (2009). Ecological and toxicological foundations of the system of protection of honey bees from diseases and pests. Abstract of Doctoral Dissertation. Krasnoyarsk (in Russian).
Khanbekova, E.M., Rubtsova, L.E., Babin, Yu.Yu., Elatkin, N.P., Lavrukhin, D.K., Tret'yakov, A.V., Sprygin, A.V. (2013). Viruses and parasites of Apis melifera caucasica Gorb. as related to losses of honeybee colonies in Big Kaukas mountings in Azerbaijan under different ebvironmental conditions and location. Sel'skokhozyaistvennaya biologiya, 6, 43-54 (in Russian).
Khezril, M., Moharami, M. (2017). The Incidence of Acarapis woodi and Varroa destructor in Kurdistan Apiaries, Iran. Animal and Veterinary Sciences, 5(6), 97-101.
Klochko, R.T., Lugansky, S.N., Blinov, A.V. (2015). Acarapidosis of bees. Pchelovodstvo, 3, 32-35 (in Russian).
Kolbina, L.M., Nepeyvoda, S.N., Maslennikov, I.V., Vorobieva, S.L., Sannikova, N.A., Kozlovskaya, N.V., Pankov, E.V. (2015). The most common diseases of bees in the Udmurt Republic. Issues of Legal Regulation in Veterinary Medicine, 1, 29-32 (in Russian).
Kulikov, N.S. (1966). Mite infestations. Pchelovodstvo, 11, 30-32 (in Russian).
Lajtha, K. (2016). The occurrence of Acarapis dorsalis, Acarapis externus and Acarapis woodi mites in honey bee populations surrounding poitiers, France. Available from: http://www.researchgate.net/publication/48140508
Lozhkina, M.V. (2020). Parasitosis of bees on private apiaries of Kostroma region. Scientific research young scientists. Proceed. V Int. Sc. Conf. Penza: ICNS "Science and Education", 271-273 (in Russian).
Maeda, T., Sakamoto, Y. (2016). Tracheal mites, Acarapis woodi, greatly increase overwinter mortality in colonies of the Japanese honeybee, Apis cerana japonica. Apidologie, 47, 762–770.
Maeda, T., Sakamoto, Y. (2020). Range expansion of the tracheal mite Acarapis woodi (Acari: Tarsonemidae) among Japanese honey bee, Apis cerana japonica, in Japan. Experimental and Applied Acarology, 80(4), 477-490.
McMullan, J.B., Brown, M.J. (2009). A qualitative model of mortality in honey bee (Apis mellifera) colonies infested with tracheal mites (Acarapis woodi). Experimental and Applied Acarology, 47, 225-234.
Melnik, N.V., Muravskaya, A.I. (2007). Acarapidosis is an actual problem. Pchelovodstvo, 5, 26-27 (in Russian).
Melnik, V.N., Muravskaya, A.I., Melnik, N.V. (2005). New means in the control of acarapidosis. Collection of scientific research works on beekeeping. Rybnoe, 190-194 (in Russian).
Moore, P.A., Wilson, M.E., Skinner, J.A. (2015). Honey bee tracheal mites: gone? But not for good. Available from: https://bee-health.extension.org/honey-bee-tracheal-mites-gone-but-not-for-good/
Moreva, L.Ya., Tsurkan, M.S., Abramchuk, A.V. (2008). Diseases of honey bees in apiaries of the Krasnodar krai. Veterinaria Kubani, 4, 28-30 (in Russian).
Muzysheva, A.Sh., Gadaev, H.H. (2018). Monitoring illness of bees in pasces of the Chechen republic. Science and Youth. Proceed. All-Russian Sc. Conf. Grozny: ChSU, 238-242 (in Russian).
Neira, M., Dussaubat, C., Manquián, N., Bahamonde, P., Vera, M. (2007) Sanidad apícola en Chile, situación de las Principales enfermedades. Agro Sur, 35(1), 47-48 (in Spanish).
On the detection of pathogens of bee diseases by specialists of the Rosselkhoznadzor laboratory on Sakhalin (2017). Rosselkhoznadzor. Available from: https://fsvps.gov.ru/fsvps/news/23000.html
Orantes, F.J., García-Fernández, P. (1997). A scientific note on the current low levels of honey bee tracheal mite in southern Spain. Apidologie, 28, 149-150.
Order of December 19, 2011 No. 476 «On approval of the list of contagious, including especially dangerous, animal diseases for which restrictive measures (quarantine) may be imposed» (2016). Vestnik veterinarii, 3(78), 41-42 (in Russian).
Otis, G.W., Scott-Dupree, C.D. (1992). The efficacy of four miticides for the control of Acarapis woodi (Rennie) in a fall treatment program. Apidologie, 23(2), 97-106.
Perepelova, L.I. (1940). Acarosis bees and control it. Oryol (in Russian).
Perepelova, L.I., Samyshkina, V.S. (1969). Control of acarapidosis in honey bees. Moscow: Rosselkhozizdat. (in Russian).
Piyunkina, V.V. (2014). Ecological and epizootic indicators of animal husbandry in the central right-bank zone of the Nizhny Novgorod region. Abstract of Ph. Thesis. Nizhniy Novgorod. (in Russian).
Poltev, V.I., Diseases of bees, Moscow-Leningrad: Kolos, 304 pp. (in Russian). Report of Administration of the Primorsky krai for 2017 (2017). Available from http://monitoring.zspk.gov.ru/%D1%84%D0%B0%D0%B9%D0%BB/1827068/%D0%9E%D1%82%D1%87%D0%B5%D1%82_%D0%93%D0%9F%D0%9A-pdf
Results of the work of the veterinary service of the Kirov region for 2017 (2017). Available from http://www.vetuprkirov.ru/assets/mgr/docs/doklady-o-rezultatach/doklad-2017.pdf
Rosselkhoznadzor (2021). The Federal Service for Veterinary and Phytosanitary Surveillance, Russian Federation Ministry of Agriculture. Available from https://fsvps.gov.ru/fsvps/iac/rf/operative-messages.html
Sakamoto, Y., Maeda, T., Yoshiyama, M., Pettis, J.S. (2017). Differential susceptibility to the tracheal mite Acarapis woodi between Apis cerana and Apis mellifera. Apidologie, 48, 150-58.
Sammataro, D., De Guzman, L., George, S., Ochoa, R., Otis, G. (2013). Standard methods for tracheal mite research. Journal of Apicultural Research, 52(4), 1-20.
Sammataro, D., Gerson, U., Needham, G. (2000). Parasitic mites of honey bees: Life History, Implications, and Impact. Annual Review of Entomology, 45, 519-548.
Shakib, V., Mehdi, E.S. (2016). Unprecedented first record of infestation level Acarapis woodi (Rennie) and overwintering ability in Savojbolagh regions of Alborz province in Iran. Journal of Entomology and Zoology Studies, 4(3), 1-13.
Smirnov, A.M. (1972). Control of acarapidosis. Pchelovodstvo, 4, 19-22 (in Russian).
Stachurska-Hagen, T., Al-Touama, Z., Dahle, B., Robertson, L.J. (2018). Molecular methods indicate lack of spread of Acarapis woodi introduced to honey bees in western Norway. Veterinary Parasitology, 11, 49–54.
Stepanenko, A.V., Samiuddin, R., Ikram, A.M., Markov, A.N., Lysenko, A.A. (2019). Characteristics of associative diseases of bees registered in the Krasnodar Kray. Technological innovation in the modern world. Materials of the International scientific conference. Ufa, 54-59 (in Russian).
The Federal Service for Veterinary and Phytosanitary Supervision in the Republic of Karelia, Arkhangelsk Region and Nenets Autonomous Okrug (2015). Available from: https://www.ursn10.ru/assets/files/Imported_02/Akt-proverki-Upr.-veterinarii-1-1259.pdf
Turaev, O.S., Safarov, M.M. (2016). Tracheal mite - Acarapis woodi - a parasite of honey bees in Uzbekistan. Modern environmental state of the natural and Scientific and practical aspects of rational nature use. Proceed. I Int. Sc. Conf. Solyonoye Zaymishche: CSRIAA, 3266-3270 (in Russian).
Vasilevsky, N.M., Domolazov, S.M. (2011). Epizootic state of beekeeping for infectious and invasive diseases of bees in the Republic of Tatarstan. Kazan State Academy of Veterinary Medicine named after N.E. Bauman, 205, 36-40 (in Russian).
Vorobyova, S.L. (2015). Characteristics of environmental factors affecting the life of bee colonies in the climatic conditions of the middle Urals. Thesis of Doctoral Dissertation. Izhevsk (in Russian).
Woodward, S.L., Quinn, J.A. (2011). Encyclopedia of Invasive Species., California, USA: ABC-CLIO, LLC.
World Organisation for Animal Health (OIE) (2021). Detailed country (ies) disease incidence. Available from: https://www.oie.int/wahis_2/public/wahid.php/Diseaseinformation/statusdetail
Yamov, V.Z., Domatsky, V.N. (2013). Results of scientific activity of GNU VNIIVEA of the Russian Agricultural Academy. Agro-food policy in Russia, 1, 4-6 (in Russian).
Zinatullina, Z.Ya, Dolnikova, T.Y., Domatskaya, T.F., Domatsky A.N. (2018). Monitoring diseases of honey bees (Apis mellifera) in Russia. Ukranian Journal of Ecology, 8(3):106-112.
Zinatullina, Z.Ya., Domatskaya, T.F., Domatsky, A.N. (2017). Infection diseases of bees on apiaries of the Tyumen region. Pchelovodstvo, 8, 20-22 (in Russian).