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Vectors of Plague Pathogens: the Flea Citellophilus Tesquorum (Wagner, 1898), a Parasite of Ground Squirrels of the Genus Spermophilus S

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Vectors of Plague Pathogens: the Flea Citellophilus Tesquorum (Wagner, 1898), a Parasite of Ground Squirrels of the Genus Spermophilus S ISSN 0013-8738, Entomological Review, 2019, Vol. 99, No. 5, pp. 565–579. © Pleiades Publishing, Inc., 2019. Russian Text © The Author(s), 2019, published in Parazitologiya, 2019, Vol. 53, No. 3, pp. 179–197. Diversity of Fleas (Siphonaptera), Vectors of Plague Pathogens: the Flea Citellophilus tesquorum (Wagner, 1898), a Parasite of Ground Squirrels of the Genus Spermophilus S. G. Medvedev a*, B. K. Kotti b**, and D. B. Verzhutsky c*** a Zoological Institute, Russian Academy of Sciences, St. Petersburg, 199034 Russia *e-mail: [email protected], [email protected] b North-Caucasus Federal University, Stavropol, 355009 Russia **e-mail: [email protected] c Irkutsk Anti-Plague Research Institute, Irkutsk, 664047 Russia ***e-mail: [email protected] Received February 17, 2019 Revised March 5, 2019 Accepted March 5, 2019 Abstract—This paper presents the results of analysis of the taxonomic diversity, distribution, and host associations of the fl ea species recorded so far as the plague microbe vectors. The ecological features and epizootic signifi cance of the fl ea Citellophilus tesquorum (Wagner, 1898), a parasite of ground squirrels, are specially considered. DOI: 10.1134/S0013873819050014 This communication opens a series of papers devoted Numerous plague foci of diff erent types occur within to analysis and general assessment of distribution and the steppe and desert natural zones in the plain and host associations of the fl ea species known as active mountain regions of Russia, from the Caucasus to Trans- vectors of the plague pathogen. Here we consider the baikalia, and also in some countries adjoining the taxonomic diversity of the fl ea species and their hosts southern Russian border. The main plague carriers are in which the plague microbe has been detected under various small burrow-dwelling mammals, and its main natural conditions of various regions of the world, and vectors and reservoir hosts are fl eas. When considering also summarize data on distribution and epizootic signi- the role of certain fl ea species as plague vectors, it fi cance of fl eas of the genus Citellophilus Wagner, 1934, should be borne in mind that the plague microbe is well with emphasis on C. tesquorum (Wagner, 1898), a para- adapted only to a small group of species that can retain site of ground squirrels. the pathogen for a long time, including the inter-epi- zootic seasons (Vashchenok, 1988, 1999). For example, Plague has been one of the most dangerous infectious only 19 fl ea species are regarded as the main plague vec- diseases throughout human history, and the plague tors in the territory of Russia and neighboring countries pathogen still poses a high risk of global dissemination. (Natural Plague Foci…, 2004; Goncharov et al., 2013). Natural plague foci occupy vast territories on all the A somewhat greater number of fl ea species have been continents except Australia and Antarctica. Of special recorded as accessory vectors that can participate in concern is the unexpected activation of some natural pathogen transmission after feeding on an infected host. foci recently observed in Central Asia (Balakhonov et al., 2014; Verzhutsky, 2018), on Madagascar, and in This paper is based on analysis of the literature data, a number of other regions (Bertherat, 2016). a considerable part of which was standardized and sum- 565 566 MEDVEDEV et al. marized using Excel spreadsheets. In particular, we Most fl ea species from which the plague microbe has analyzed the extensive material given in Chapter 5 of been isolated under natural conditions in fi ve zoogeo- the recent review Yersinia pestis: Retrospective and graphic regions of the world belong to the three largest Perspective (Dubyanskiy and Yeszhanov, 2016), inclu- families: Leptopsyllidae, Ceratophyllidae, and Hystri- ding Table 5.6 “Species of mammals recognized as chopsyllidae. In particular, the pathogen has been de- plague carriers in diff erent countries” and Table 5.7 tected in 21% of species and 40% of genera of Lepto- “Species and subspecies of fl eas found to be infected in psyllidae, 18% of species and 60% of genera of Cerato- the plague foci in diff erent countries.” All this informa- phyllidae, and 12% of species and 50% of genera of tion was compared with the data on the world fl ea fauna Hystrichopsyllidae. These three families are largely dis- in the PARHOST1 information analysis system, which tributed in the Northern hemisphere (Medvedev, 2000) has been developed at the Zoological Institute of the where most plague foci are located. In the fauna of Russian Academy of Sciences since 2001. Russia these families are represented by 213 species, which comprise 83% of all the species recorded in Rus- In addition, we analyzed the data on the species com- sia (Medvedev, 1998, 2013a, 2013b). The family Hystri- position of fl eas infected with the plague microbe in chopsyllidae comprises about 37% of all the fl ea species 45 foci in Russia and adjacent countries, cointained in in the Palaearctic fauna, while Leptopsyllidae and Cera- Supplement 3 to the reference edition List of Species tophyllidae comprise 23% each. In the family Pulicidae, and Subspecies of Fleas Recorded as Plague Carriers under Natural Conditions (Goncharov et al., 2013). The the plague pathogen has been detected in 24% of the summarized data on the signifi cance of the fl ea Citello- species from 86% of the genera. philus tesquorum in the natural Eurasian plague foci are The presently known carriers of the plague microbe given in Table 4 below. belong to 9 orders of mammals and 1 order of birds (Table 2). The pathogen carrier state has been recorded Fleas and Their Hosts as Vectors and Carriers for 346 of 5937 species (about 6%)1, 144 of 1258 genera of the Plague Pathogen (about 10%), 33 of 156 families (about 20%), and 9 of Most homoiothermic and poikilothermic animals are 28 orders (about 30%) of mammals. The greatest num- only occasionally involved in the epizootic process and ber of carrier species (34%) is found in the family play no signifi cant role in maintaining the enzootic Cricetidae. Other rodents also play a considerable role plague foci. The carriers and vectors that really support as plague carriers, which comprise 22% of species in the the plague pathogen and ensure its survival belong to family Muridae and 15% in Sciuridae. Other orders and much fewer species, usually only several species in each families of mammals, namely lagomorphs (Leporidae), particular natural focus. In some cases, other species carnivores (Mustelidae and Viverridae), and insecti- may be additionally included in the pathogen circulation vores (Soricidae), have much smaller shares of plague during specifi c phenological seasons or specifi c phases carrier species, from 2 to 4%. of the epizootic cycle (Rall, 1965). Among the plague carriers, the greatest number of Natural plague infection was detected in 233 species species (30%) and genera (34%) occur in the Palae- of mammals (Karimova et al., 2010) and at least in arctic; they belong to 15 families of mammals and 244 species and subspecies of fl eas in the world fauna 5 families of birds. The main carriers of the plague (Goncharov and Plotnikova, 2010). Our analysis of the pathogen in the Eurasian foci are believed to be ground more recently published data (Dubyanskiy and Yeszha- squirrels, marmots, gerbils, rats, voles, and pikas (Kari- nov, 2016) has shown that the fl ea species revealing mova and Neronov, 2007). According to our analysis, plague infection in the nature belong to 95 out of the greatest number of plague carrier species in the 240 genera, i.e., to 40% of the total number of fl ea gen- Palaearctic has been recorded not only in the families era in the world fauna, and to 12 out of 18 families Cricetidae and Sciuridae but also in Dipodidae. The (Table 1). At present, plague infection has been detected plague carriers in the Nearctic Region mostly belong to in 257 species of fl eas, which constitute 12% of all the Sciuridae and Cricetidae, in the Neotropical Region, to 2162 known species. It should be noted that the world fl ea fauna also includes 846 described subspecies. 1 See https://en.wikipedia.org/wiki/List_of_mammal_genera. ENTOMOLOGICAL REVIEW Vol. 99 No. 5 2019 ENTOMOLOGICAL REVIEW Vol. 99No.5 2019 Vol. REVIEW ENTOMOLOGICAL Table 1. The number of species (numerator) and genera (denominator) of fl eas recorded as plague microbe vectors PATHOGENS PLAGUE OF VECTORS (SIPHONAPTERA), FLEAS OF DIVERSITY Flea families Zoogeographic region Ceratophyllidae Chimaeropsyllidae Coptopsyllidae Hystrichopsyllidae Leptopsyllidae Pulicidae Rhopalopsyllidae Stephanocircidae Stivaliidae Tungidae Vermipsyllidae Xiphiopsyllidae Total 31 (202) 4 (19) 47 (332) 46 (205) 11 (38) 0 (8) 0 (2) 1 (35) 140 (892) Palaearctic 11 (24) 1 (1) 7 (19) 9 (26) 4 (22) 0 (3) 0 (1) 1 (3) 33 (96) 35 (131) 14 (120) 3 (17) 6 (8) 0 (4) 0 (2) 0 (5) 58 (299) Nearctic 12 (24) 9 (25) 3 (97) 5 (5) 0 (2) 0 (1) 0 (1) 29 (68) 0 (16) 2 (26) 7 (84) 1 (10) 13 (86) 0 (15) 1 (2) 1 (8) 25 (275) Afrotropical 0 (2) 1 (8) 3 (3) 1 (3) 5 (13) 0 (2) 1 (1) 1 (1) 12 (43) 3 (32) 0 (15) 1 (9) 2 (11) 3 (86) 9 (191) Indo-Malayan 1 (7) 0 (4) 1 (3) 2 (5) 1 (22) 5 (52) 4 (53) 2 (39) 6 (8) 11 (108) 3 (43) 2 (18) 28 (289) Neotropical 1 (10) 2 (2) 4 (4) 5 (10) 3 (7) 1 (3) 16 (55) 4 (8) 4 (8) Cosmopolitan 2 (4) 2 (4) 73 (396) 2 (26) 4 (19) 70 (580) 49 (234) 37 (152) 11 (121) 3 (51) 3 (108) 3 (21) 1 (39) 1 (8) 257 (1941) Total 26 (44) 1 (8) 1 (1) 23 (46) 12 (30) 19 (22) 5 (10) 3 (9) 1 (23) 2 (4) 1 (3) 1 (1) 95 (240) The number of species and genera in each zoogeographic region is determined based on the distribution data for 1941 fl ea species.
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