Abstract
Interactions of the plague pathogen with fleas from various natural populations were studied. Large-scale experimental studies carried out mainly in the Siberian natural plague foci demonstrated a significant effect of the population factor on proventricular blocking, the intensity of formation of bacterial clumps in the flea intestine, and the efficiency of pathogen transmission to intact mammals. The results suggest that the ecological plasticity of the plague pathogen is not solely determined by its close contacts with specific flea populations in the past, even though this factor significantly affects the interaction between the pathogen and fleas.
Similar content being viewed by others
REFERENCES
Adyaasuren, Z., Tserennorov, D., Myagmar, Zh., Gankhu-yag, Ts., Otgonbayar, D., Bayar, Ts., Verzhutsky, D.B., Ganbold, D., and Balakhonov, S.V., The current situation in the plague natural foci in Mongolia, Far East. J. Infect. Pathol., 2014, vol. 25, p. 22.
Aparin, G.P. and Golubinsky, E.P., Mikrobiologiya chumy (Microbiology of Plague), Irkutsk: Irkutsk Gos. Univ., 1989.
Balakhonov, S.V., Korzun, V.M., Chipanin, E.V., Afanas’ev, M.V., Mikhailov, E.P., Denisov, A.V., Fomina, L.A., Eshelkin, I.I., Mashkovsky, I.K., Mishchenko, A.I., Rozhdestvensky, E.N., and Yarygina, M.B., Gorno-Altaiskii prirodnyi ochag chumy. Retrospektivnyi analiz, epizootologicheskii monitoring, sovremennoe sostoyanie (The Gorno-Altai Natural Plague Focus: Retrospective Analysis, Epizootological Monitoring, and Current State), Novosibirsk: Nauka-Tsentr, 2014.
Balakhonov, S.V., Verzhutsky, D.B., Kholin, A.V., Bazanova, L.P., Klimov, V.T., Kosilko, S.A., Okunev, L.P., Tokmakova, E.G., Shestopalov, M.Yu., Galatsevich, N.F., Akimova, I.S., and Salchak, L.K., Tuvinskii prirodnyi ochag chumy (The Tuva Natural Plague Focus), Irkutsk: Irkutsk. Gos. Univ., 2019.
Bazanova, L.P., The relationship between the plague microbe (Yersinia pestis) and fleas (Siphonaptera), by the example of Siberian natural plague foci, Extended Abstract of Doctoral Dissertation in Biology, Ulan-Ude, 2009.
Bazanova, L.P. and Maevsky, M.P., Persistence of the plague microbe in the flea Citellophilus tesquorum altaicus, Med. Parazitol. Parazit. Bolezni, 1996, no. 1, p. 45.
Bazanova, L.P. and Verzhutsky, D.B., Evaluation of the epizootic role of the flea Rhadinopsylla li transbaikalica Ioff et Tifl. (1946) in the Tuva natural plague focus, in Aktualnye problemy infektologii i parazitologii: Materialy mezhdunarodnoi nauchnoi konferentsii (Current Problems of Infectology and Parasitology: Proc. of the Int. Conf.), Tomsk, 2001, p. 42.
Bazanova, L.P. and Verzhutsky, D.B., Epizootological significance of fleas (Siphonaptera) in the Tuva natural plague focus: a review, Baikal. Zool. Zh., 2009, no. 3, p. 13.
Bazanova, L.P. and Verzhutsky, D.B., Interpopulation differences of fleas in the transmission of the plague microbe in the Tuva natural focus, Far East. J. Infect. Pathol., 2019, vol. 37, p. 49.
Bazanova, L.P., Verzhutsky, D.B., and Khabarov, A.V., Interpopulation differences in the relationship with the plague pathogen of two common flea species associated with the long-tailed ground squirrel in the Tuva natural focus, in Karantinnye i zoonoznye infektsii v Kazakhstane: Materialy Mezhdunarodnogo simpoziuma (Quarantine and Zoonotic Infections in Kazakhstan: Proc. of the Int. Symp.), Issue 2, Almaty, 2000a, p. 48.
Bazanova, L.P., Voronova, G.A., and Tokmakova, E.G., Differences in proventricular block formation between males and females of Xenopsylla cheopis (Siphonaptera: Pulicidae), Parasitologiya, 2000b, vol. 34, no. 1, p. 56.
Bazanova, L.P., Tokmakova, E.G., and Maevsky, M.P., The role of blocked and unblocked fleas Citellophilus tesquorum altaicus in plague transmission, Probl. Osobo Opasnykh Inf., 2003, no. 86, p. 14.
Bazanova, L.P., Verzhutsky, D.B., Nikitin, A.Ya., Tokma-kova, E.G., and Khabarov, A.V., Differences between two populations of Citellophilus tesquorum altaicus from the Tuva natural plague focus in terms of the relationship with the pathogen and morphological characteristics, Med. Parazitol. Parazit. Bolezni, 2004, no. 1, p. 37.
Bazanova, L.P., Verzhutsky, D.B., Nikitin, A.Ya., Tokmakova, E.G., Voronova, G.A., and Khabarov, A.V., Interactions between the plague pathogen and fleas from different parts of the Tuva natural plague focus, Med. Parazitol. Parazit. Bolezni, 2006, no. 3, p. 35.
Bazanova, L.P., Voronova, G.A., and Kosilko, S.A., Relationships between the plague pathogen and its vectors from geographically distant populations, Probl. Osobo Opasnykh Inf., 2010, no. 4, p. 66.
Bazanova, L.P., Voronova, G.A., and Kosilko, S.A., Relationships between the plague pathogen and its vectors from different parasitic systems, Med. Parazitol. Parazit. Bolezni, 2013, no. 1, p. 12.
Bibikova, V.A. and Klassovsky, L.N., Peredacha chumy blokhami (Transmission of Plague by Fleas), Moscow: Meditsina, 1974.
Bolormaa, G., Undraa, B., Baigalmaa, M., and Otgonbaatar, D., Plague in Mongolia, Vector-Borne Zoonotic Dis., 2010, vol. 10, no. 1, p. 69.
Bryukhanova, G.D., Tserennorov, D., Shchedrin, V.I., Chumakova I.V., and Grizhebovsky, G.M., Plague transmission by fleas Citellophilus tesquorum sungaris, Sci. J. Centr. Contr. Res. Nat. Infect. Dis., 1999, vol. 7, p. 205.
Eigelis, Yu.K., Gryzuny Vostochnogo Zakavkaz’ya i problema ozdorovleniya mestnykh ochagov chumy (Rodents of the Eastern Transcaucasia and the Problem of Sanitation of the Local Plague Foci), Saratov: Saratov. Univ., 1980.
Enkhbaatar, L., Jamyansbarav, B., Ariuntuya, O., and Batsaikhan, B., The prevalence and prognosis of plague in Mongolia, Sci. J. Center Inf. Dis. Nat. Foci, 2003, vol. 11, p. 253.
Feoktistov, A.Z., Danilenko, A.F., Yuzvik, L.N., and Shvedko, L.P., Effectiveness of the common flea species as plague vectors in Transbaikalia, in Doklady Irkutskogo protivochumnogo instituta (Reports of Irkutsk Anti-Plague Institute), Issue 10, 1974, p. 206.
Jarrett, C.O., Deak, E., Isherwood, K.E., Oyston, P., Fischer, E., Whitney, A.R., Kobayashi, S.D., DeLeo, F.R., and Hinnebusch, B.J., Transmission of Yersinia pestis from an infectious biofilm in the flea vector, J. Inf. Dis., 2004, vol. 190, p. 783. https://doi.org/10.1086/422695
Knyazeva, T.V., Toporkov, V.P., Berezhnov, A.Z., Velichko, L.N., Balukhin, V.N., Gordienko, T.G., and Podsvirova, V.V., Comparison of the efficiency of plague transmission by fleas of the little ground squirrel from different natural populations, in Prirodnaya ochagovost’, mikrobiologiya i profilaktika zoonozov (Natural Focality, Microbiology, and Prevention of Zoonoses), Saratov, 1989, p. 116.
Korenberg, E.I., Natural focality of infections: current problems and research prospects, Zool. Zh., 2010, vol. 89, no. 1, p. 5.
Kozlov, M.P. and Sultanov, G.V., Chuma (prirodnaya ochagovost’, epizootologiya) (Plague: Natural Foci and Epizootology), Makhachkala: Mavel, 2000.
Kraminsky, V.A., Materials on the military epidemiology of China, Candidate’s Dissertation in Medicine, Voroshilov, 1953.
Kucheruk, V.V., Struktura, tipologiya i raionirovanie prirodnykh ochagov boleznei cheloveka. Itogi razvitiya ucheniya o prirodnoi ochagovosti boleznei cheloveka i dal’neishie zadachi (Structure, Typology and Regionalization of Natural Foci of Human Diseases. The Development of the Theory of Natural Focality of Human Diseases and Further Research Goals), Moscow: Meditsina, 1972, p. 180.
Logachev, A.I., Features of the plague microbe strains isolated in different parts of the Tuva natural plague focus, Chin. J. Control Endemic Dis., 1999, vol. 14, p. 210.
Lukhnova, L.Yu. and Kazakbaeva, R.A., Survival and competitive ability of the plague pathogen strains in different vectors, in Tezisy dokl. XII Mezhrespublikanskoi nauch.-prakt. konf. protivochumnykh uchrezhdenii Srednei Azii i Kazakhstana po profilaktike chumy (Abstracts of Papers of the 12th Conf. of Anti-Plague Institutions in Central Asia and Kazakhstan on Plague Prevention), Alma-Ata, 1985, p. 69.
Maramovich, A.S., Kosilko, S.A., Innokentieva, T.I., Voronova, G.A., Bazanova, L.P., Nikitin, A.Ya., and Okunev, L.P., Plague in China: The danger of its spreading into Siberia and the Russian Far East, Zh. Mikrobiol. Epidemiol. Immunobiol., 2008, no. 1, p. 95.
Medvedev, S.G., Verzhutsky, D.B., and Kotti, B.K., Diversity of vectors of plague pathogens: polyhostal parasites, fleas of the genus Rhadinopsylla Jordan et Rothschild, 1911 (Siphonaptera, Hystrichopsyllidae), Entomol. Rev., 2020, vol. 100, no. 9, p. 1218. https://doi.org/10.1134/S001387382009002X
Medvedev, S.G., Kotti, B.K., and Verzhutsky, D.B., Diversity of fleas (Siphonaptera), vectors of plague pathogens: the flea Citellophilus tesquorum (Wagner, 1898), a parasite of ground squirrels of the genus Spermophilus, Entomol. Rev., 2019, vol. 99, no. 5, p. 565.
Nikitin, A.Ya. and Bazanova, L.P., Investigation of the possibility of effective xenopair formation between Yersinia pestis and the flea Citellophilus tesquorum, Byull. Vost.-Sibir. Nauch. Tsentra, 2003, no. 3, p. 152.
Nikitin, A.Ya. and Sosunova, I.A., Analiz i prognoz vremennykh ryadov v ekologicheskikh nablyudeniyakh i eksperimentakh (Uchebnoe posobie) (Analysis and Prediction of Time Series in Ecological Observations and Experiments: a Teaching Aid), Irkutsk, 2003.
Popov, V.V. and Verzhutsky, D.B., Characteristics of intrapopulation groups of the long-tailed ground squirrel (Citellus undulatus Pall.) during population depression, Byul. Mosk. Ob-va Ispyt. Prir. Otdel. Biol., 1988, vol. 93, no. 6, p. 47.
Rokitsky, P.F., Biologicheskaya statistika (Biological Statistics), Minsk, Vysheishaya Shkola, 1967.
Rozanova, G.N., Osipova, S.P., and Bagdasarova, T.G., The ability of plague microbe strains with different trophic patterns to induce proventricular blocking in fleas, in Bolezni s prirodnoi ochagovost’yu na Kavkaze: Tezisy dokladov nauchnoi konferentsii (Natural Focal Diseases in the Caucasus: Abstracts of Papers of a Conf.), Stavropol, 1982, p. 122.
Serzhanov, O.S., Khrustselevskaya, N.M., Chumachenko, V.D., Asenov, G.A., and Matakov, M.I., Block formation in fleas Xenopsylla gerbilli caspica from various landscape-ecological areas of the Kyzyl Kum, Probl. Osobo Opasnykh Inf., 1979, no. 4, p. 58.
Sludsky, A.A., Derlyatko, K.I., Golovko, E.N., and Ageev, V.S., Gissarskii prirodnyi ochag chumy (The Hissar Natural Plague Focus), Saratov: Saratov. Univ., 2003.
Sludsky, A.A., Boyko, A.V., Lyapin, M.N., and Tarasov, M.A., A population-based approach to defining the boundaries and number of plague natural foci, Povolzh. Ekol. Zh., 2019, no. 4, p. 493. https://doi.org/10.35885/1684-7318-2019-4-493-502
Suleimenov, B.M., Enzootiya i epizootiya chumy (Enzootics and Epizootics of Plague), Almaty, 2009.
Suntsov, V.V. and Suntsova, N.I., Chuma. Proiskhozhdenie i evolyutsiya epizooticheskoi sistemy (ekologicheskie, geograficheskie i sotsial’nye aspekty) (Plague. Origin and Evolution of the Epizootic System: Ecological, Geographic and Social Aspects), Moscow: KMK Scientific Press, 2006.
Suntsov, V.V., Hostal effect of territorial expansion of the plague microbe Yersinia pestis from the populations of the Mongolian tarbagan (Marmota sibirica), Zool. Zh., 2020, vol. 99, no. 11, p. 1307. https://doi.org/10.31857/S0044513420090160
The Atlas of Plague and Its Environment in the People’s Republic of China, Beijing: Science Press, 2000.
Tokmakova, E.G., Bazanova, L.P., and Vershinin, E.A., The ability of the fleas Citellophilus tesquorum and Frontopsylla luculenta luculenta (Siphonaptera, Ceratophyllidae) to survive below-zero temperatures during winter, Entomol. Rev., 2019, vol. 99, no. 4, p. 525. https://doi.org/10.1134/S0013873819040134
Tserennorov, D., Epizootological significance of fleas Citellophilus tesquorum sungaris (Jordan, 1929) and Frontopsylla luculenta luculenta (Jordan et Rothschild, 1923) in natural plague foci in Mongolia, Extended Abstract of Candidate’s Dissertation in Biology, Stavropol, 1999.
Vashchenok, V.S., The role of fleas (Siphonaptera) in plague epizootology, Parazitologiya, 1999, vol. 33, no. 3, p. 198.
Vershinin, E.A., Ecological features of fleas associated with the Daurian ground squirrel in the Transbaikalian natural plague focus, Candidate’s Dissertation in Biology, Irkutsk, 1993.
Verzhutsky, D.B., Epizootological role of the population organization of fleas parasitizing the long-tailed ground squirrel in the Tuva natural plague focus, Parazitologiya, 1999, vol. 33, no. 3, p. 242.
Verzhutsky, D.B., Spatial organization of the populations of a host and its ectoparasites: theoretical and applied aspects, by the example of the long-tailed ground squirrel and its fleas, Extended Abstract of Doctoral Dissertation in Biology, Irkutsk, 2005.
Verzhutsky, D.B., Interpopulation relationships in the long-tailed ground squirrel in Southwest Tuva, Byul. Mosk. Ob-va Ispyt. Prir. Otdel. Biol., 2006, vol. 111, no. 5, p. 52.
Verzhutsky, D.B., The marker role of ectoparasites in population studies of their hosts, Baikal. Zool. Zh., 2012, vol. 10, no. 2, p. 94.
Verzhutsky, D.B., Activation of natural plague foci in Central Asia: groundless fears or a real threat? Prir. Vnutr. Azii, 2018, vol. 6, no. 1, p. 7.
Verzhutsky, D.B., Zonov, G.B., and Popov, V.V., Epizootological significance of flea accumulation in aggregations of long-tailed ground squirrel females in the Tuva natural plague focus, Parazitologiya, 1990, vol. 24, no. 3, p. 186.
Verzhutsky, D.B., Chumakova, N.A., Galatsevich, N.F., and Kovaleva, N.I., On the ecology of the flea Citellophilus tesquorum Wagn., 1898 in Southwest Tuva, Baikal. Zool. Zh., 2009, no. 1, p. 17.
Verzhutsky, D.B., Tkachenko, S.V., Galatsevich, N.F., Chumakova, N.A., Nemkova, N.K., Akimova, I.S., Kholin, A.V., and Balakhonov, S.V., Discovery of new epizootic sites in the Tuva natural plague focus, Nats. Prior. Ross., 2016, vol. 22, no. 4, p. 17.
Voronova, G.A., Ceratophilus tesquorum altaicus Ioff, 1936 as the main vector and reservoir host of the plague microbe in the Tuva natural focus, in Epidemiologiya i profilaktika osobo opasnykh infektsii v MNR i SSSR (Epidemiology and Prevention of Particularly Dangerous Infections in the Mongolian People’s Republic and the USSR), Ulaanbaatar: Gosizdat, 1978, p. 152.
Voronova, G.A. and Bazanova, L.P., On the possibility of local epizootics in Siberia as the result of plague pathogen introduction from Mongolia, J. Infect. Pathol., 2009, vol. 16, no. 3, p. 88.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest. The authors declare that they have no conflict of interest.
Statement on the welfare of animals. All the applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All the procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.
Rights and permissions
About this article
Cite this article
Bazanova, L.P., Verzhutsky, D.B. Interpopulation Differences of Fleas (Siphonaptera) in the Transmission of Plague Pathogen. Entmol. Rev. 102, 207–221 (2022). https://doi.org/10.1134/S0013873822020051
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0013873822020051