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 of the Genus 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 and 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 , 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 . 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 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 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 ; 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, , 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.

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DIVERSITY OF FLEAS (SIPHONAPTERA), VECTORS OF PLAGUE PATHOGENS 567 Total 4 (8) 2 (4) 5 (52) 33 (96) 29 (68) 12 (43) 9 (191) 16 (55)

58 (299) 25 (275) 28 (289) 95 (240)

140 (892) 257 (1941) Xiphiopsyllidae

1 (8) 1 (1) 1 (8) 1 (1) Vermipsyllidae

1 (3) 0 (5) 0 (1) 1 (3) 1 (35) 1 (39) Tungidae

0 (2) 0 (1) 0 (2) 0 (1) 1 (2) 1 (1) 1 (3) 2 (4) 2 (18) 3 (21) Stivaliidae

0 (8) 0 (3) 0 (2)

0 (15) 3 (86) 1 (22) 1 (23) 3 (108) Stephanocircidae

3 (7) 3 (9) 3 (43) 3 (51) Rhopalopsyllidae 0 (4) 0 (2)

5 (10) 5 (10)

Flea families 11 (108) 11 (121) 11 Pulicidae 2 (5) 6 (8) 5 (5) 6 (8) 4 (4) 4 (8) 2 (4)

2 (11) 2 (11) 4 (22) 5 (13)

11 (38) 11 13 (86) 19 (22) 37 (152) Leptopsyllidae 1 (3) 1 (9) 1 (3)

9 (26) 3 (17) 3 (97) 1 (10)

12 (30) 46 (205) 49 (234) Hystrichopsyllidae 3 (3) 0 (4) 2 (2)

7 (19) 9 (25) 7 (84) 0 (15) 2 (39)

23 (46) 47 (332) 14 (120) 70 (580) Coptopsyllidae

1 (1) 1 (1) 4 (19) 4 (19) Chimaeropsyllidae

1 (8) 1 (8) 2 (26) 2 (26) Ceratophyllidae 0 (2) 1 (7) 0 (16) 3 (32) 4 (53) 1 (10) 11 (24) 11 12 (24) 26 (44) 31 (202) 35 (131) 73 (396) The number of species (numerator) and genera (denominator) of fl eas recorded as plague microbe vectors The number of species (numerator) and genera (denominator) fl region Zoogeographic Nearctic Afrotropical Indo-Malayan Neotropical Cosmopolitan Total Table 1. Table Palaearctic ea species. The number of species and genera in each zoogeographic region is determined based on the distribution data for 1941 fl

ENTOMOLOGICAL REVIEW Vol. 99 No. 5 2019 568 MEDVEDEV et al. 1 (1) 1 (1) 1 (1) 2 (1) 2 (1) 1 (1) 4 (1) 1 (1) 1 (1) Total 1 (1) 1 (1) Zoogeographic region Order Carnivora Order Scandentia Order Insectivora Order Artiodactyla Order Order Passeriformes Order Didelphimorphia Palaearctic Nearctic Afrotropical Indo-Malayan Neotropical Cosmopolitan The number of species and genera (in parentheses) of birds and mammals recorded as plague microbe carriers in fi ve zoogeographic regions The number of species and genera (in parentheses) birds mammals recorded as plague microbe carriers in fi 5 Didelphidae 1 Alaudidae2 Corvidae3 Muscicapidae4 Turdidae 1 (1) 6 1 (1) 1 (1) Erinaceidae7 Soricidae8 2 (1) Tenrecidae9 Tupaiidae 4 (3) 1 (1) 2 (2) 1 (1) 1 (1) 1 (1) 1 (1) 7 (6) 1 (1) 2 (2) 1 (1) 11 Camelidae 2 (1) 10 Bovidae 2 (2) 1 (1) 3 (3) 12 Suidae13 Canidae14 Felidae15 Mephitidae16 Mustelidae17 Procyonidae18 Viverridae 2 (1) 1 (1) 7 (2) 1 (1) 2 (1) 2 (1) 3 (1) 4 (3) 1 (1) 1 (1) 1 (1) 2 (2) 3 (3) 1 (1) 5 (3) 12 (6) 7 (6) No. Families Table 2. Table

ENTOMOLOGICAL REVIEW Vol. 99 No. 5 2019 DIVERSITY OF FLEAS (SIPHONAPTERA), VECTORS OF PLAGUE PATHOGENS 569 1 (1) 2 (1) 8 (4) 1 (1) 2 (1) 1 (1) 4 (1) 1 (1) 2 (1) 3 (2) 2 (2) Total 10 (7) 13 (4) 52 (16) 115 (36) 115 2 (1) 76 (31) 3 (2) 346 (144) 1 (1) 2 (1) 8 (4) 1 (1) 4 (1) 1 (1) 1 (1) 43 (11) 1 (1) 5 (4) 3 (1) 3 (2) Zoogeographic region 2 (1) 1 (1) 3 (2) 9 (1) 2 (1) 40 (18) 27 (8) Order Primates Order Rodentia Order Hyracoidea Order Lagomorpha 2 (1) 1 (1) 4 (1) 1 (1) 28 (5) 6 (4) 3 (1) 3 (1) 1 (1) 10 (7) 15 (4) 41 (18) 19 (5) 105 (51) 67 (22) 64 (31) 45 (22) 62 (22) Palaearctic Nearctic Afrotropical Indo-Malayan Neotropical Cosmopolitan (Contd.) Total 26 Dasyproctidae 28 Echimyidae 27 Dipodidae 29 Geomyidae 20 Procaviidae 19 Cercopithecidae 21 Leporidae 23 Caviidae 22 Ochotonidae 24 Chinchillidae 25 Cricetidae 30 Gliridae 31 Eleteromyidae 32 Muridae 33 Pedetidae 34 Sciuridae No. Families Table 2. Table

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Cricetidae, and in the Afrotropical and Indo-Malayan of this polytypic species (comprising two subspecies) regions, to Muridae. The number of genera to which covers the steppe and semi-desert zones from East these species belong also refl ects the higher taxonomic Europe to West, Middle, and Central Asia and to South diversity of plague carriers among Cricetidae in the Siberia (Kotti, 2018). At the same time, this fl ea species Palaearctic and Neotropical regions and among Muridae has not been recorded as plague vector in the eastern, in the Afrotropical and Indo-Malayan regions. Siberian part of its range. On the whole, the plague foci and the main pathogen The South Siberian fl ea species Rhadinopsylla (Rali- carriers have the following distribution in Russia and psylla) li transbaikalica Ioff et Tifl ov, 1947 currently adjacent countries (Table 3). Plain and mountain foci serves as an accessory plague vector in the Tuva focus supported by ground squirrels cover vast territories in (Galatsevich, 2018). No accessory vectors have been the North Caucasus, Northwest and North Caspian Sea revealed in the more eastern, Transbaikalian focus; regions, and also the Lower Volga basin. The main however, another member of the genus Neopsylla pathogen carriers in these foci are the little ground squir- Wagner, 1903, the South Siberian fl ea N. abagaitui Ioff , rel Spermophilus pygmaeus (Pallas, 1778) and the Cau- 1946, and also some other fl ea species were recorded as casian mountain ground S. musicus (Menetries, occasional vectors. 1832). In the Siberian part of Russia lie the Tuva and Transbaikalian foci where the carriers are the long-tailed Fleas of the Genus Citellophilus S. undulatus (Pallas, 1778) and the Dau- The 46 genera of the family Ceratophyllidae vary in rian ground squirrel S. dauricus (Brandt, 1844), respec- their species composition, and only 14 of them include tively. The main vector and also reservoir of the plague more than 10 species each. For instance, the genus Cera- pathogen in all these foci is the polytypic fl ea species tophyllus Curtis, 1831 counts 66 species, and the genus Citellophilus tesquorum (Wagner, 1898) represented by Nosopsyllus Jordan, 1933 comprises 54 species. Accor- four subspecies. ding to diff erent authors, the genus Citellophilus com- The fl ea C. tesquorum was recorded as the main vec- prises 11 species and 8 subspecies (Traub et al., 1983) or tor in the gerbil-based Caspian polyhostal plague focus 13 species and 7 subspecies (Lewis, 2003). (Goncharov et al., 2013), where the main carriers are not The ground-living Sciuridae in Eurasia reached pros- only gerbils but also the little ground squirrel. perity in the Late Pliocene, 2.5–3.5 million years ago Another fl ea species, C. trispinus, serves as an acces- (Gromov and Baranova, 1981; Pavlinov et al., 1995), sory vector in the gerbil-based Muyunkum desert plague and it was probably at that time that most fl ea species of focus, where the main pathogen carrier is the great the genus Citellophilus originated. gerbil and the main vector is C. tesquorum, while the In morphological features, fl eas of the genus Citello- yellow ground squirrel Spermophilus fulvus (Lichten- philus most closely resemble members of another Palae- stein, 1823) is an accessory carrier. arctic genus, Callopsylla Wagner, 1934. The latter com- Expansion of the main (highly virulent) subspecies of prises 4 subgenera with 28 species that parasitize a wide the plague pathogen from to the Altai Moun- range of hosts including not only rodents, lagomorphs, tains and its further spread in the populations of the and insectivores but also birds. Fleas of the genus Citel- gray and the fl ea Oropsylla silantiewi (Wagner, lophilus are associated with burrow-dwelling rodents 1898) was recorded in 2012 (Balakhonov et al., 2014). of the family Sciuridae, and among them, mostly with Currently this territory is occupied by two overlapping ground squirrels of the genus Spermophilus Cuvier, plague foci, one supported by the Mongolian pika and 1825 (= Citellus). Several Citellophilus species are per- the fl eas associated with this host, the other, by the gray manent parasites of marmots of the genus Marmota Blu- marmot and O. silantiewi. menbach, 1779 (Traub et al., 1983). Correspondingly, fl eas of the genus Citellophilus have been recorded The fl ea Neopsylla setosa (Wagner, 1898) is believed as the main vectors in the marmot- and ground squirrel- to be the second main vector in some plague foci within based plague foci in Russia and adjacent countries (Nat- European Russia. The vast Euro-Siberian-Asian range ural Plague Foci…, 2004).

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It should be noted that according to the IAS PAR- Citellophilus lebedewi princeps (Ioff , 1946) has HOST1 data on the world fl ea fauna, fl eas of the genus a Central-Palaearctic, Turanian range: West and East Citellophilus as a whole have been recorded on 66 spe- Tien Shan, Pamiro-Alai, and Hindu Kush. The main cies from 6 families; in particular, on 22 species host is the red marmot. from 4 genera of the family Sciuridae, 31 species from 15 genera of Cricetidae, 8 species from 5 genera of Di- 4. Citellophilus martinoi (Wagner et Ioff , 1926) has podidae, 4 species from 2 genera of Muridae, 1 species a West-Palaearctic, European range: Central and South- of Gliridae, and 1 species of Zapodidae. east Europe. The main host is the European ground squirrel Spermophilus citellus (L., 1766). Citellophilus is one of the six fl ea genera character- ized by trans-Palaearctic distribution. Ranges of this Citellophilus martinoi martinoi has a West-Palae- type are also observed in fl eas of the genera Ophthalmo- arctic, European range: Central and Southeast Europe. psylla Wagner et Ioff , 1926, Mesopsylla Dampf, 1910 The main host is the European ground squirrel. (Leptopsyllidae), and Coptopsylla Jordan and Roth- Citellophilus martinoi rotundus Rosicky, 1956 has schild, 1908 (Coptopsyllidae) parasitizing ground squir- a West-Palaearctic, European range: Central Europe. rels, gerbils, and jerboas, and also in members of the The main host is the European ground squirrel. genus Callopsylla (Ceratophyllidae) associated with pikas, marmots, and arvicoline and cricetine rodents. 5. Citellophilus menzbieri (Ioff , 1950) has a Central- Broad trans-Palaearctic distribution is also typical of Palaearctic, Turanian range: West Tien Shan. The main the hedgehog parasites from the genus Archaeopsylla host is Menzbier’s marmot Marmota menzbieri Kash- Dampf, 1908 (Pulicidae). karov, 1925. Fleas of the genus Citellophilus occur in the steppe 6. Citellophilus relicticola (Fedina, 1946) has a Cen- and mountain areas of Central and Southern Europe, tral-Palaearctic, Turanian range: Central and West Tien , Western, Middle, and Central Asia, South Shan, Xinjiang. The main hosts are the Tien Shan ground Siberia, and the Amur region. However, the number squirrel Spermophilus relictus (Kashkarov, 1923) and of species of this genus is the greatest in Kazakhstan, the russet ground squirrel S. major (Pallas, 1779). Middle and Central Asia. 7. Citellophilus simplex (Wagner, 1902) has a West- The summarized data for 11 species and 12 subspe- Palaearctic, European-East Mediterranean range: East- cies of the genus Citellophilus are given below. ern Europe and Asia Minor. The main hosts are the 1. Citellophilus gracilis (Mikulin, 1957) has an East- European ground squirrel and the speckled ground Palaearctic, Siberian-Central Asian range: Dzungarian squirrel Spermophilus suslicus (Guldenstaedt, 1770). Alatau. The main host is the red-cheeked ground squir- Citellophilus simplex simplex has a West-Palaearctic, rel Spermophilus erythrogenys (Brandt, 1841). European-East Mediterranean range: Eastern Europe 2. Citellophilus jenissejensis (Wagner, 1902) has and Asia Minor. a Central-East-Palaearctic, Siberian range: the moun- Citellophilus simplex rosickyi Cyprich, 1989 has tains of Central Asia and the south of Middle Siberia. a West-Palaearctic, European range: Central Europe. The main host is the long-tailed ground squirrel Spermo- philus undulatus (Pallas, 1778). 8. Citellophilus sungaris (Jordan, 1929) is a distinct species according to Lewis (1990) and a subspecies of 3. Citellophilus lebedewi (Wagner, 1933) has a Cen- Citellophilus tesquorum in the opinion of some other tral-Palaearctic, Central Asian-Turanian range: Tien authors. It has a Central-East-Palaearctic, Siberian-East Shan, Pamiro-Alai, and Hindu Kush. Its main hosts are Asian-Central Asian range: Cisbaikalia, Transbaikalia, the red marmot Marmota caudata (Geoff rey, 1842) and Yakutia, Amur region, Northeast , Southeast Altai, the gray marmot M. baibacina (Kastschenko, 1899). eastern part of the Uvs Lake Basin and Mongolian Altai, Citellophilus lebedewi lebedewi has an East-Palae- the Gobi area (except the eastern part), and plains of arctic, Central Asian range: Central Tien Shan. The main East Mongolia. The main hosts are the Daurian and hosts are the red and gray marmots. long-tailed ground squirrels.

ENTOMOLOGICAL REVIEW Vol. 99 No. 5 2019 572 MEDVEDEV et al. 5 4 1 3 3 1 1 6 1 6 16 Total 2 8 1* 1 1* 1 Far East Siberia and 1 3 1* 1* Asia Central 1 3 1 5 3* 4 2* 4* Kazakhstan 5 2 5 1* 2* 1* region NW and N NW Caspian Sea 4 4 1 7 Caucasus and Transcaucasia Type of focus Type (main carriers) PikasVoles Marmots Gerbils Ground squirrelsGerbils 1 Voles 1* 1 Gerbils Marmots Gerbils Voles Ground squirrels Gerbils Gerbils Ground squirrelsPikas 1* (Wagner, 1898); Holarctic (Wagner, J. et R., 1923; Middle-Central (Wagner, 1895); Caucasian– (Wagner, ; Central-Middle Asian ilus ; Central-Middle Wagner et Argyropulo, 1934; Argyropulo, et Wagner ) iranus Family Coptopsyllidae Family Ceratophyllidae (Wagner, 1909); Caucasian–Middle (Wagner, (Wagner, 1898); European–Middle (Wagner, Flea species and its range Family Hystrichopsyllidae (Ioff et Argyropulo, 1934); Argyropulo, et ( C .) caspia (Ioff Flea species that are main and accessory plague vectors, the number of plague foci in Russia and adjacent countries where these species occur Amphalius runatus (J. et R., 1923); Holarctic Callopsylla Table 3. Table Asian European–Middle Citellophilus lebedewi Asian 1898); European–Middle C. tesquorum (Wagner, Western-Central , 1926); et Ioff C. trispinus (Wagner Asian 1898); European– Nosopsyllus ( N .) consimilis (Wagner, Asian Middle N . ( Gerbillophilus Transcaucasian N . ( G .) laeviceps Asian ( O .) silantiewi Oropsylla Coptopsylla lamellifer Middle Asian Middle Asian Rhadinopsylla dahurica Asian Neopsylla setosa

ENTOMOLOGICAL REVIEW Vol. 99 No. 5 2019 DIVERSITY OF FLEAS (SIPHONAPTERA), VECTORS OF PLAGUE PATHOGENS 573 3 1 1 1 6 3 1 10 10 Total 1 1 1* 1 1* 1 1* 1 Far East Siberia and 3 1 1 1* Asia Central 12 1 4 1 2 2 8 Kazakhstan 1 15 14 38 10 103 region NW and N NW Caspian Sea 1 7 26 Caucasus and Transcaucasia Type of focus Type (main carriers) Marmots Ground squirrels Pikas Gerbils Voles Pikas Pikas Voles Gerbils Gerbils Gerbils Gerbils Gerbils Ioff et Argyropulo, Argyropulo, et Ioff (Tifl ov, 1937); Middle-Central ov, (Tifl (J. et R., 1923); South Siberian– (Wagner, 1903); Mediterranean (Wagner, Family Pulicidae Ioff et Tifl ov, 1947; South Siberian ov, Tifl et Ioff Family Leptopsyllidae Jord., 1926; Middle-Central Asian Jord., 1926; Middle-Central Flea species and its range Ioff et Tifl ov, 1946; Middle Asian 1946; Middle ov, Tifl et Ioff (F.) elata caucasica (F.) Ioff , 1930; Middle-Central Asian , 1930; Middle-Central Ioff Roths., 1913; Middle-Central Asian Roths., 1913; Middle-Central (Wagner, 1903); Western-Central Asian Western-Central 1903); (Wagner, Ioff , 1930; Western-Middle Asian Western-Middle , 1930; Ioff Wagner, 1933; South Siberian–Central Asian 1933; South Siberian–Central Wagner, (Contd.) Table 3. Table * an accessory vector. Ctenophyllus hirticrus Asian Central R. li ventricosa R. li transbaikalica Frontopsylla Xenopsylla conformis Asian 1934; Eucaucasian hetera F. Scalon, 1935; South Paradoxopsyllus scorodumovi Siberian Pectinoctenus nemerosa X. gerbilli X. gerbilli minax X. hirtipes X. nuttalli X. skrjabini Total

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Citellophilus sungaris lobatschevi (Cyprich, Kiefer et Citellophilus tesquorum transcaucasicus (Ioff et Ar- Krumpál, 1985) has an East-Palaearctic, Central Asian gyropulo, 1934) has a West Palaearctic, European range: range: Mongolia. The hosts are the long-tailed ground Lesser Caucasus (Northwest Armenia and Northeast squirrel and the red-cheeked ground squirrel S. erythro- Turkey). The main host is the Anatolian ground squirrel genys (Brandt, 1843). Spermophilus xanthoprymnus (Bennett, 1835). 9. Citellophilus tesquorum (Wagner, 1898) has a trans- 10. Citellophilus trispinus (Wagner et Ioff , 1926) has Palaearctic, European-Siberian-Central-East Asian range: a Central Palaearctic, Turano-Iranian range: plains of Southern Europe, Caucasus, Kazakhstan, Middle and Kazakhstan, Middle, Central, and Western Asia. The Central Asia, South Siberia. The species parasitizes main host is the yellow ground squirrel. various ground squirrels of the genus Spermophilus. Citellophilus trispinus trispinus (Wagner et Ioff , Citellophilus tesquorum tesquorum has a West Palae- 1926) has a Central Palaearctic, Turano-Iranian range: arctic, European range: southeastern parts of Kazakhstan (except the eastern part), Middle, Central, and Rostov Province of Russia as far as the lower course and Western Asia. The main host is the yellow ground of the Donets and the Don. The main host is the little squirrel. ground squirrel. Citellophilus trispinus balkhaschensis (Mikulin, 1958) Citellophilus tesquorum altaicus (Ioff , 1936) was has a Central Palaearctic, Turanian range: Kazakhstan considered a separate species by Lewis (1990). It has (eastern part), Xinjiang. The main host is the yellow an East Palaearctic, Siberian-East Asian range: Zaisan ground squirrel. Hollow, Dzungaria, southern slopes of Dzungarian Ala- tau, Altai, West Sayan, Khakassia, Tuva, western part of 11. Citellophilus ullus (Mikulin, 1957) has a Central the Uvs Lake Basin, North Hangai, Mongolian and Gobi Palaearctic, Turanian range: Kazakhstan, Middle and Altai. The main hosts are the long-tailed and red-cheeked Central Asia. The main host is the red-cheeked ground ground squirrels. squirrel.

Citellophilus tesquorum ciscaucasicus (Ioff , 1936) The Flea Citellophilus tesquorum has a West Palaearctic, European range: area between the Donets and the Volga rivers, East Ciscaucasia. The As noted above, the polytypic species Citellophilus main host is the little ground squirrel. tesquorum is the main vector and reservoir of the plague pathogen in a number of plague foci in Russia. This fl ea Citellophilus tesquorum dzetysuensis (Mikulin, 1951) has a range of the trans-Palaearctic type, which can be has an East Palaearctic, Central Asian range: northern generally described as European-Siberian-Central Asian. (in the east also southern) slopes of Dzungarian Alatau. The species belongs to the group of oligoxenous para- The main host is the long-tailed ground squirrel. sites associated with several taxonomically close host species; such parasites are common among fl eas. Oligo- Citellophilus tesquorum elbrusensis Goncharov, 2011 xenous parasites form essential associations with hosts has a West Palaearctic, European range: central part from a specifi c taxon, even though they may sometimes of the Greater Caucasus. The main host is the Cauca- occur on hosts from other taxa. The fl eas Xenopsylla sian mountain ground squirrel S. musicus (Menetries, conformis (Wagner, 1903) and Nosopsyllus laeviceps 1832). (Wagner, 1909), parasitizing gerbils of the genus Citellophilus tesquorum mongolicus (J. et R., 1911) Meriones Illiger, 1811, also belong to the group of oligo- has an East Palaearctic, Central Asian range: North xenous parasites. The main hosts of Citellophilus China, Manchuria. The main host is the Daurian ground tesquorum are ground squirrels of the genus Spermo- squirrel S. dauricus (Brandt, 1844). philus (Medvedev, 2002). Citellophilus tesquorum transvolgensis (Ioff , 1936) The Old World fauna includes 14 species of ground has a trans-Palaearctic, Euro-Siberian range: the trans- squirrels, of which 13 belong to the genus Spermophilus Volga area, Kazakhstan, and south of West Siberia. The (the Alashan, Arctic, russet, Caucasian, Daurian, long- main host is the little ground squirrel. tailed, European, yellow, speckled, red-cheeked, Anato-

ENTOMOLOGICAL REVIEW Vol. 99 No. 5 2019 DIVERSITY OF FLEAS (SIPHONAPTERA), VECTORS OF PLAGUE PATHOGENS 575 lian, little, and Tien Shan ground squirrels) and 1, the in Kazakhstan. The plague microbe has not been iso- long-clawed ground squirrel, to the genus Spermophi- lated since 1971 in the Transbaikalian steppe focus, lopsis (Gromov and Erbaeva, 1995; Wilson and Reeder, since 1991 in the Northwest Caspian steppe focus, since 2005). Citellophilus tesquorum is either a dominant or 1996 in the South Manchurian focus, since 2001 in the one of 2–3 codominants in the fl ea assemblages of all Terek-Sunzha focus, since 2002 in the Volga-Ural steppe the above ground squirrel species, with few exceptions. focus, since 2004 in the Dagestan plain-foothill focus, Some subspecies distributed in isolated territories or and since 2008 in the Central Caucasian high-mountain associated with certain hosts are presently regarded as focus. It should be noted that in most foci where the distinct species, for instance, C. jenissejensis (the form pathogen can no longer be isolated, antibodies to the occurring on the long-tailed ground squirrel in the south plague microbe in blood or its DNA in living of Krasnoyarsk Territory and in Khakassia) or C. relicti- objects are periodically detected, indicating that the cola (the species associated with the Tien Shan ground pathogen is still preserved in the local biocenoses. squirrel in Tien Shan). Based on analysis of the earlier experimental data, Within the distribution range of Eurasian ground Bibikova and Klassovsky (1974) concluded that the squirrels there are 11 plague foci with a total area of fl eas C. tesquorum had low ability to form the proven- slightly less than 500 thousand km2, in which these tricular block. In the opinion of Vashchenok (1988), the rodents serve as the main pathogen carriers (Table 4). subspecies C. t. ciscaucasicus had high activity as the The little ground squirrel is involved in the functioning plague vector while C. t. altaicus had low activity. In of fi ve foci: the Northwest Caspian steppe, Terek-Sun- a later work, the same author noted that in the plague zha low-mountain, Dagestan plain-foothill, Volga-Ural foci involving the little and Caucasian mountain ground steppe, and trans-Ural steppe one. The fi rst three foci lie squirrels, “infection is transmitted by the highly active entirely within the Russian territory, the fourth extends vector Neopsylla setosa and by the somewhat less active into Kazakhstan by a signifi cant portion, and the fi fth vector Citellophilus tesquorum” (Vashchenok, 1999, focus is located in Kazakhstan. The main carrier in two p. 199). It should be noted that in the Central Caucasian foci is the Daurian ground squirrel: the Transbaikalian plague focus, the only one with the Caucasian mountain steppe (positioned in the territories of Russia, Mongolia, ground squirrel as the main carrier, N. setosa plays and China) and the South Manchurian one (in the north- a considerable role as the plague vector only in the east- east of China). The long-tailed ground squirrel is the ern part of the focus where this fl ea is distributed. Only main carrier in the Tuva mountain (Russia) and the East 2.4% of the plague microbe strains isolated from fl eas Tien Shan (China) plague foci; the Caucasian mountain was obtained from N. setosa, whereas 83.3% of the ground squirrel is the main carrier in the Central Cauca- strains were isolated from C. tesquorum (Natural Plague sian high-mountain focus (Russia), and the Alashan Foci…, 2004). ground squirrel, in the Huangtu Plateau focus (on the boundary of Gansu and Ningxia provinces of China). It should be borne in mind that proventricular block In the remaining Eurasian plague foci, ground squirrels formation and pathogen transmission effi ciency depend are only sporadically included in the epizootic process, on many factors: ambient temperature and humidity, usually during its high activity (The Atlas of Plague…, the duration of feeding and frequency of feeding acts in 2000; Natural Plague Foci…, 2004; Karimova and Ner- infected fl eas, the phenological period when the experi- onov, 2007, Distribution…, 2012; Dubyanskiy and Yes- ment was carried out, and specifi city of the laboratory zhanov, 2016). animals. Experiments in the Siberian plague foci showed that C. tesquorum fl eas feeding on ground squirrels Among the above plague foci involving ground squir- could easily get infected and effi ciently transmit the rels as the main carriers and C. tesquorum as the only plague pathogen to other hosts (Voronova, 1984; Baza- vector or one of the main vectors, two are presently characterized by high epizootic activity: the Tuva focus nova and Maevsky, 1996). The frequency of block for- in Russia and the Gansu-Ningxia focus in China. mation was found to vary considerably over the season (Voronova, 1978; Bazanova, 2009). In July and early Epizooties of low or medium activity have been re- August, during high activity of the epizootic process, corded in the recent years in the trans-Ural steppe focus the rate of proventricular block formation in C. tesquo-

ENTOMOLOGICAL REVIEW Vol. 99 No. 5 2019 576 MEDVEDEV et al. 78.1 71.8 78.0 69.4 83.3 78.9 57.9 82.5 39.3 > 64 83.3*** obtained from ( N. setosa : 58.9) C. tesquorum , %* Share of plague isolates Spermophilus and marmots , Distribution …, 2012; Dubyanskiy and Main vectors C. tesquorum , O. silantievi C. tesquorum , O. silantievi C. tesquorum C. tesquorum Neopsylla setosa Citellophilus tesquorum , 2004; Karimova and Neronov, 2007, , 2004; Karimova and Neronov, Main carriers S. alashanicusS. undulatus , M. baibacina C. tesquorum , N. abagaitui S. pygmaeusS. pygmaeusS. dauricus , Marmota sibirica C. tesquorum , N. setosa S. undulatus C. tesquorum , N. setosa S. musicus S. dauricus C. tesquorum , R. li S. pygmaeusS. pygmaeus C. tesquorum N. setosa , C. tesquorum Spermophilus pygmaeus 2 Natural Plague Foci… km 2160 2480 4600 11150 10826 67400 65500 ~ 15000 ~ 150000 Focus area, in natural Eurasian plague foci involving ground squirrels of the genus …, 2000; The Atlas of Palgue The Citellophilus tesquorum ea of the plague microbe cance of the fl Marmota as carriers Signifi Focus, country, and year of the fi rst isolation and year of the fi Focus, country, Volga-Ural steppe, Russia and Kazakhstan, 1912Volga-Ural steppe, Kazakhstan, 1913 Trans-Ural steppe, Russia, Mongolia, China, 1911Transbaikalian 99100 34000** mountain, Russia, 1964 Tuva Central Caucasian high-mountain, Russia, 1971 South Manchurian, China, 1928 Gansu-Ningxia, China, 1956 Shan North, China, 1955 Tien East Terek-Sunzha low-mountain, Russia, 1970 Terek-Sunzha Dagestan plain-foothill, Russia, 1951 Northwest Caspian steppe, Russia, 1913 Table 4. Table The table is based on literature sources ( Yeszhanov, 2016). Yeszhanov, eas. * as related to all the isolates obtained from fl ** including the Mongolian and Chinese parts of focus. eas parasitizing the long-tailed ground squirrel. *** as related to the isolates obtained from fl of the genus

ENTOMOLOGICAL REVIEW Vol. 99 No. 5 2019 DIVERSITY OF FLEAS (SIPHONAPTERA), VECTORS OF PLAGUE PATHOGENS 577 rum reached the maximum value of 10.6%, while the generations per year (Galatsevich, 2018), apparently as time interval from infection to development of the fi rst the result of improved living conditions of the preimagi- plug was reduced to 3 days. nal stages due to climate changes in Central Asia. The plague microbe is preserved for a long time in the Most species of ground squirrels hibernate during organism of C. tesquorum. In an early experiment, fl eas more or less extended periods of adverse conditions. in an artifi cial burrow retained the pathogen for up to The long-tailed ground squirrels and the fl eas C. tesquo- 102 days (Evseeva and Firsov, 1932). rum overwinter separately; therefore, the plague patho- gen persists in the fl ea organisms, without contact with During excavation of long-tailed ground squirrel the main carrier, for about 8 months a year (Vernitsky burrows in the Tuva natural focus in winter, the plague et al., 2003). microbe was isolated from two samples of fl eas col- lected in the nest substrates. The infected fl eas were Females of most ground-living Sciuridae species identifi ed as C. tesquorum in both cases (Verzhutsky form peculiar temporary aggregations during pregnancy et al., 2003). The cited authors also noted that of the and weaning (Michener, 1983; King, 1989). In the long- plague microbe strains isolated in spring, the great ma- tailed ground squirrel, such aggregations result in con- jority was also obtained from C. tesquorum. centration of brood nests within small areas, where the density of C. tesquorum adults increases about 20-fold. Experiments carried out under quasi-natural condi- The areas where ground squirrel females aggregate in tions in the Tuva plague focus showed that fl eas infected May–June are characterized by abnormally high densi- with the plague pathogen could survive winter without ties of adult fl eas (up to several thousand individuals per a host and transmit infection to other hosts in the follow- hectare) and provide optimal stations for preservation, ing year. More than a half (50.0–64.3%) of the tested accumulation, and dissemination of the plague microbe fl eas retained the plague pathogen for 10–11 months, (Verzhutsky, 1999). and about 30% of them, for 13–15 months. Some indi- viduals, mostly females, retained the plague microbe for CONCLUSIONS up to 22 months and could subsequently infect healthy ground squirrels (Bazanova, 2009). Proventricular block Within the Nearctic Region, plague foci are mostly formation in C. tesquorum was recorded long after the located in the West American Subregion; within the moment of infection, even on the 282–411th days (Baza- Neotropical Region, in the Brazilian and Andean sub- nova and Maevsky, 1996; Voronova and Bazanova, regions; within the Afrotropical Region, in the Mada- 2004). Fleas from diff erent populations varied signifi - gascar Subregion, in the west of the East African Sub- cantly in the effi ciency of pathogen transfer (Bazanova region, and in the south of the Cape Subregion; within et al., 2000; Bazanova, 2009). Analysis of long-term the Palaearctic Region, in the Turanian Province of the data revealed an abrupt increase in the proventricular Turano-Iranian Subregion, the Central Asian Subregion, block formation rates in C. tesquorum during the recent and the southeast of the East Asian Subregion; within decades in all the three natural Siberian plague foci the Indo-Malayan Region the plague foci are restricted (Verzhutsky et al., 2018). to the west of the Indian Subregion and the west and east of the Indochinese Subregion. The life cycle of C. tesquorum is largely determined by the biological traits of its main hosts. The species The above analysis demonstrates considerable taxo- develops in one annual generation over the greatest part nomic diversity of the plague carriers and vectors. The of its range. The adults reactivated from and fl ea species from which the plague microbe has been newly eclosed ones start reproducing in spring; the isolated under natural conditions belong to 40% of the generations change and the population is supplemented genera and more than a half of the families known in the with new adults during summer. In mid-August the great world fauna. These numbers indicate a wide distribution majority of C. tesquorum fl eas cease feeding and remain of the plague pathogen along biocenotic chains, which in the vacant summer nests of their hosts (Verzhutsky may lead to formation of new plague foci, for example, et al., 2009). According to the recent data, in the Tuva in response to climate changes. However, stable circula- natural plague focus this species currently produces two tion of the plague pathogen both during epizooties and

ENTOMOLOGICAL REVIEW Vol. 99 No. 5 2019 578 MEDVEDEV et al. in the inter-epizootic periods is supported only by 11. Goncharov, A.I. and Plotnikova, E.P., “Zoogeographic a small number of fl ea species and their hosts. Citello- Distribution of Genera and Species of Fleas of the Fam- philus tesquorum is one of the most important plague ily Pulicidae (Insecta, Siphonaptera) Known to be Natu- vectors among fl eas. It should be noted that the factors ral Carriers of the Plague Microbe,” Mezhdunarodnyi determining some biological traits of this species are Zhurnal Prikladnykh i Fundamentalnykh Issledovanii 11, 25−26 (2010). still poorly understood. Some important aspects may be 12. Goncharov, A.I., Tokhov, Yu.M., Plotnikova, E.P., and clarifi ed in the future by using molecular methods. Artyushina, Yu.S., List of Species and Subspecies of Fleas Recorded as Plague Carriers under Natural Con- FUNDING ditions (Stavropol, 2013) [in Russian]. 13. 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