ISSN 0013-8738, Entomological Review, 2015, Vol. 95, No. 6, pp. 728–738. © Pleiades Publishing, Inc., 2015. Original Russian Text © B.K. Kotti, 2015, published in Parazitologiya, 2015, Vol. 49, No. 4, pp. 289–303.

Fleas (Siphonaptera) of and Birds in the Great Caucasus B. K. Kotti North-Caucasus Federal University, Stavropol, 355009 Russia e-mail: [email protected] Received November 17, 2014

Abstract—There are 116 species of fleas in the territory of the Great Caucasus, of which 21 species occur on birds and the rest, on mammals. Among the 41 flea genera present in the Caucasian fauna, only Caenopsylla, Phaenop- sylla, and Araeopsylla are absent in the Great Caucasus. There are 11 endemic species. Fleas of 66 species are dis- tributed over the entire mountain system. Parasites of some birds, carnivores, insectivores, and occur from lowlands to highlands. Some species inhabit the forest altitudinal belt while others prefer the foothill and middle mountain areas, being absent in the highlands even though their hosts may occur at all the altitudes. The distribu- tion of other species is limited to lowlands in accordance with that of their main hosts. DOI: 10.1134/S0013873815060068

Earlier we have analyzed the specific traits Special living conditions for mammals, birds, and their of species diversity and host associations of fleas ectoparasites are provided by rocky areas and screes. of the Caucasus, and also established the main pathways of migration of some groups of fleas into The diverse living conditions of mammals and birds this territory (Medvedev and Kotti, 2011, 2012). determine a considerable species diversity of their This communication summarizes the results of fleas. Correspondingly, the flea fauna of the Great many-year research of the flea fauna of the Great Cau- Caucasus is of great interest from the viewpoint of casus. zoogeographic analysis. In addition, studies of the fleas of this territory are of considerable medical im- The mountain system of the Great Caucasus extends portance due to the presence of the East Caucasian and sublatitudinally for almost 1100 km and is subdivided the Central Caucasian alpine natural plague foci as into three main parts. The West Caucasus embraces well as the isolated Kobystan part of the Transcauca- the territories west of Elbrus, the Central Caucasus sian plain-piedmont plague focus (Onishchenko and includes the ranges positioned between Elbrus and Kutyrev, 2004). Kazbek Mountains, and the East Caucasus, the territo- The fleas of the Great Caucasus have been studied ries east of Kazbek. for more than a hundred years. The first publication on Meadow-like steppes constitute the main type of this topic contained a description of a new ectoparasite vegetation in the piedmont areas up to 1000 m above of bats, the flea Ischnopsyllus dolosus (Dampf, 1912). sea level (a.s.l.). Broad-leaved and coniferous forests The fauna of the region was studied by many are typical of the middle mountains at altitudes from researchers, including A.I. Argyropulo, N.F. Darskaya, 1000 to 2000 m a.s.l., whereas subalpine and alpine A.I. Devkin, A.I. Goncharov, I.G. Ioff, E.V. Isaeva, meadows occur in the highlands at altitudes greater N.F. Labunets, M.N. Mirzoeva, V.N. Nefedov, than 2000 m a.s.l. The Great Caucasus provides favor- I.N. Razumova, B.A. Rostigaev, R.F. Savenko, able conditions for existence of a rich fauna of fleas. It Ya.F. Shatas, F. Smit, E.F. Sosnina, N.G. Syrvacheva, includes vast treeless territories inhabited by various A.N. Talybov, and others. An important result of the mammals and birds that make burrows and nest in many years of research was the publication of the Key them, or use the burrows of other homoiotherms. to the Fleas of the Caucasus (Tiflov et al., 1977). Some inhabitants of meadows and steppes build nests The discovery of natural plague foci in the Great on the soil surface. The forest biotopes provide habi- Caucasus in 1971 and 1977 (Onishchenko and tats for nesting in tree hollows or crowns. Kutyrev, 2004) encouraged further studies of

728 FLEAS (SIPHONAPTERA) OF MAMMALS AND BIRDS 729 its flea fauna. At this stage, research was carried By the degree of host specificity, fleas can be mon- out by L.I. Belyavtseva, A.I. Goncharov, N.P. Gubare- oxenous (ultraspecific) parasites, infesting hosts of va, E.V. Isaeva, K.P. Kadatskaya, Yu.E. Komarov, only one species, or oligoxenous parasites, occurring T.I. Kazakova, P.N. Korzhov, B.K. Kotti, N.F. Labu- on several congeneric host species. Among fleas there nets, A.N. Talybov, Sh.G. Tsikhistavi, Z.G. Shev- are also some pleioxenous parasites whose main hosts chenko, and others. The data on the flea faunas of belong to several genera of one family, and also some parts of the Great Caucasus were summarized in polyxenous parasites that infest hosts from different the monograph Species Diversity of Fleas (Siphonap- families, orders, and even classes (Balashov, 2000). tera) of the Caucasus (Kotti, 2014). The names of the bird species are given below ac- MATERIALS AND METHODS cording to Stepanyan (2003), those of the species, according to Pavlinov and Lisovsky (2012). This work is based on the material collected by the The mammal and bird fauna of the Great Caucasus is author from 1978 to 2014 in different regions of the characterized based on a number of publications (Isa- Great Caucasus. Research was carried out at 20 collec- kov et al., 1966; Tembotov, 1972; Beme et al., 1987; tion sites positioned at altitudes from 300 to 2700 m Tembotov and Kazakov, 1982; Sokolov and Tem- a.s.l. Altogether, about 100 thousand specimens of botov, 1989). fleas collected off 23 thousand mammals and in 410 mammal and bird nests were identified to species. The distribution of six flea species, namely Xeno- From 1978 to 1981, together with researchers from psylla cheopis, Ctenocephalides felis, C. canis, Tar- the Dagestan anti-plague station, we studied the popu- sopsylla octodecimdentata, Nosopsyllus fasciatus, and lations of the common and water voles, the gray ham- Leptopsylla segnis, is determined by the activities of ster, and other small mammals in the subalpine and man. The ranges of the remaining 110 species are clas- alpine belts at 2300–2700 m a.s.l. The sampling sites sified below following the system of Kryzhanovskij were positioned north of the Samur Range near Kok- (2002), which was used in our earlier publications madag Mt., and also in Kulinsky and Agulsky Districts (Kotti, 2005). The flea species are united into groups of Dagestan. In addition, some collections of fleas and and complexes based on the size, outlines, continuity, their hosts were performed in the middle mountain and geographic position of their ranges. belt, in the Samur valley (Akhty and Rutul Districts) and in the foothills, on the north slope of the Gimri The Specificity of Associations between Fleas Range (Buinak District). and Their Hosts From 1976 to 2014, summer expeditions were or- The fleas found in the Great Caucasus and their ganized to the western and central parts of the Great main hosts are listed in Table 1. Although the region Caucasus. Fleas were collected off small mammals in question comprises only one-third of the whole and from their nests in the upper reaches of the rivers territory of the Caucasus, its flea fauna includes Malka, Kuban, Teberda, Malyi Zelenchuk, Bol- 116 species, or 70% of the total number of species shoi Zelenchuk, Bolshaya Laba, and Belaya. In addi- known from the Caucasus. tion, earlier flea collections of S.A. Ashibokova, There are more than 100 mammal species in the N.B. Birulya, G.Ya. Bobyr, A.A. Guseva, N.F. Dar- Great Caucasus (Shidlovsky, 1976; Tembotov skaya, A.I. Devkin, A.N. Dobrolyubov, P.F. Emelja- and Kazakov, 1982; Sokolov and Tembotov, 1989), nov, L.I. Zalutskaya, E.P. Kudzheva, N.F. Labunets, but fleas are known to occur on only about 80 of A.N. Roman, M.A. Tarasov, M.P. Tarasov, K.V. Kha- them. They parasitize various mammals of the orders rin, and K.Yu. Shkarlet were processed. Insectivora, Chiroptera, Carnivora, Artiodactyla, and Some data on the flea fauna of the Great Caucasus Rodentia. There are examples of some flea species were obtained by studying the stock collections and infesting representatives of different orders of mam- archives of Stavropol Anti-Plague Scientific Research mals. For instance, the fleas Hystrichopsylla talpae Institute, the Zoological Institute of the Russian Acad- and H. satunini, widely distributed in the Great Cauca- emy of Sciences (ZIN RAS), and also the Georgian, sus, occur on moles () in the middle mountain Azerbaijan, Dagestan, and Black Sea anti-plague sta- belt, and on voles () in the alpine tions. areas.

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Table 1. Distribution of flea species of the Great Caucasus by the hosts Flea species Hosts Family Pulicidae Billberg, 1820 Pulex irritans L., 1758 wolf, red fox, swine Echidnophaga popovi Ioff et Argyropulo, 1934 badger, red fox Archaeopsylla erinacei (Bouche, 1835) northern white-breasted Ctenocephalides felis (Bouche, 1835) domestic cat C. canis (Curtis, 1826) domestic dog Xenopsylla cheopis (Rothschild, 1903) brown rat X. conformis (Wagner, 1903) Lybian jird Family Vermipsyllidae Wagner, 1889 Chaetopsylla hyaenae (Kolenati, 1846) brown bear C. homoea Rothschild, 1906 least weasel, stoat C. trichosa Kohaut, 1903 badger, red fox C. globiceps (Taschenberg, 1880) red fox, badger C. korobkovae Tiflov et Kolpakova, 1937 red fox C. caucasica Smit, 1953 common and stone martens C. rothschildi Kohaut, 1903 common and stone martens C. mirabilis Ioff et Argyropulo, 1934 common and stone martens Family Coptopsyllidae Wagner, 1928 Coptopsylla caucasica Isayeva-Gurvich, 1950 Lybian jird Family Ceratophyllidae Dampf, 1908 Tarsopsylla octodecimdentata (Kolenati, 1863) red squirrel Myoxopsylla jordani Ioff et Argyropulo, 1934 forest and edible dormice Paraceras melis (Walker, 1856) badger Oropsylla idahoensis (Baker, 1904) Caucasian mountain ground squirrel Nosopsyllus laeviceps Wagner, 1909 Lybian jird N. mokrzeckyi (Wagner, 1916) wood and house mice N. consimilis (Wagner, 1898) common, shrub, and social voles N. fasciatus (Bosc, 1800) brown rat Citellophilus tesquorum (Wagner, 1898) Caucasian mountain ground squirrel Callopsylla caspia (Ioff et Argyropulo, 1934) common vole, Caucasian snow vole C. saxatilis (Ioff et Argyropulo, 1934) Caucasian snow vole C. kazbegiensis Goncharov, 1980 Caucasian snow vole C. waterstoni (Jordan, 1925) common house martin, crag martin C. gemina (Ioff, 1946) rock pigeon, chough C. gypaetina Peus, 1978 bearded vulture Amalaraeus dissimilis (Jordan, 1938) common vole A. arvicolae (Ioff, 1948) water vole A. improvisus (Ioff, 1946) common and shrub voles, Caucasian and Robert’s snow voles Megabothris walkeri (Rothschild, 1902) water vole M. turbidus (Rothschild, 1909) shrub, common, and water voles, Georgian hamster Ceratophyllus borealis Rothschild, 1907 campophilous birds C. spinosus Wagner, 1903 little owl, lesser kestrel

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Table 1. (Contd.) Flea species Hosts C. frigoris Darskaya, 1950 sclerophilous birds C. garei Rothschild, 1902 campophilous birds C. styx Rothschild, 1900 sand martin C. farreni Rothschild, 1905 common house martin, crag martin C. rusticus Wagner, 1903 common house martin, crag martin C. caliotes Jordan, 1937 common house martin, crag martin C. hirundinis (Curtis, 1826) common house martin, crag martin C. enefdeae Ioff, 1950 sclerophilous birds C. gallinae (Schrank, 1803) dendrophilous birds C. fringillae (Walker, 1856) dendrophilous birds C. vagabundus (Boheman, 1866) sclerophilous birds C. tribulis Jordan, 1926 sclerophilous birds C. pullatus Jordan et Rothschild, 1920 dendrophilous birds C. sciurorum (Schrank, 1803) red and Caucasian squirrels, forest and edible dormice Dasypsyllus gallinulae (Dale, 1878) passerine birds Family Leptopsyllidae Rothschild, 1915 Ophthalmopsylla volgensis (Wagner et Ioff, 1926) small and Euphrates five-toed jerboas Frontopsylla semura Wagner et Ioff, 1926 Caucasian mountain ground squirrel F. caucasica Ioff et Argyropulo, 1934 common and shrub voles F. frontalis Rothschild, 1909 wheatears F. laeta Jordan et Rothschild, 1920 common house martin, crag martin Paradoxopsyllus hesperius Ioff, 1946 Caucasian snow vole P. gussevi Mirzoyeva, 1954 Lybian jird, water vole, gray hamster Amphipsylla rossica Wagner, 1912 shrub, common, and water voles, Georgian hamster A. kuznetzovi Wagner, 1912 Caucasian snow vole A. schelkovnikovi Wagner, 1909 gray hamster A. georgica Savenko, 1949 wood mice, gray hamster Mesopsylla apscheronica Wagner et Argyropulo, 1911 small and Euphrates five-toed jerboas Peromyscopsylla bidentata (Kolenati, 1863) common and shrub voles, Caucasian snow vole Leptopsylla taschenbergi (Wagner, 1898) wood, field, and house mice L. algira Jordan et Rothschild, 1911 white-toothed L. nana Argyropulo, 1946 water vole, Caucasian snow vole L. segnis (Schöncherr, 1811) house mouse L. sexdentata (Wagner, 1930) white-toothed shrews Family Ischnopsyllidae Tiraboschi, 1904 Ischnopsyllus obscurus (Wagner, 1898) particolored bat I. elongatus (Curtis, 1832) lesser horseshoe bat I. intermedius (Rothschild, 1898) serotine bat I. octactenus (Kolenati, 1856) common pipistrelle I. variabilis (Wagner, 1898) Nathusius’s pipistrelle I. dolosus Dampf, 1912 mouse-eared bats I. hexactenus (Kolenati, 1856) brown long-eared bat

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Table 1. (Contd.) Flea species Hosts Nycteridopsylla eusarca Dampf, 1908 common pipistrelle N. pentactena (Kolenati, 1856) brown long-eared bat, barbastelle N. dictena (Kolenati, 1856) particolored bat Rhinolophopsylla unipectinata (Taschenberg, 1880) Mehely’s horseshoe bat Family Hystrichopsyllidae Tiraboschi, 1904 Ctenophthalmus inornatus Wagner, 1916 long-clawed mole vole C. acuminatus Ioff et Argyropulo, 1954 Ciscaucasian hamster C. rettigi Rothschild, 1908 Georgian hamster C. proximus (Wagner, 1903) wood mice C. kirschenblatti Argyropulo, 1936 shrub vole, Robert’s snow vole C. golovi Ioff et Tiflov, 1930 common and shrub voles, Caucasian mountain ground squirrel C. chionomydis Ioff et Rostigayev, 1950 Caucasian snow vole C. bifurcus Ioff, 1940 Caucasian snow vole C. secundus Wagner, 1916 social vole C. intermedius Argyropulo, 1935 common and shrub voles C. parvus Argyropulo, 1935 shrub vole C. shovi Rostigayev, 1948 shrub and common voles, Robert’s snow vole C. bogatschevi Wagner et Argyropulo, 1934 common vole C. wagneri Tiflov, 1928 common and shrub voles C. schuriscus Ioff, 1940 common and shrub voles C. orientalis (Wagner, 1898) common and social voles, Caucasian mountain ground squirrel C. dagestanicus Rostigayev, 1967 common vole C. kazbek Tiflov, 1953 shrub vole Palaeopsylla gromovi Argyropulo, 1934 long-tailed shrews, Transcaucasian water P. caucasica Argyropulo, 1946 Levantine and Caucasian moles P. alpestris Argyropulo, 1946 Levantine and Caucasian moles P. osetica Ioff, 1953 Levantine and Caucasian moles Doratopsylla dampfi Argyropulo, 1935 long-tailed shrews, Transcaucasian water shrew Rhadinopsylla ucrainica Wagner et Argyropulo, 1934 social vole, Lybyan jird R. li Argyropulo, 1941 Caucasian mountain ground squirrel R. caucasica Argyropulo, 1946 common and shrub voles Neopsylla pleskei Ioff, 1928 common vole N. setosa (Wagner, 1898) Caucasian mountain ground squirrel Paraneopsylla dampfi Ioff, 1946 Caucasian snow vole Stenoponia tripectinata (Tiraboschi, 1902) Lybian jird S. ivanovi Ioff et Tiflov, 1934 common and shrub voles Hystrichopsylla talpae Curtis, 1826 common and shrub voles, Levantine and Caucasian moles H. satunini Wagner, 1916 shrub and common voles, Levantine and Caucasian moles Atyphloceras nuperum (Jordan, 1931) shrub vole

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The Fleas of Insectivores rotine bat Eptesicus serotinus (Schreber) while I. obscurus and Nycteridopsylla dictena occur on the The insectivores present in the Great Caucasus are particolored bat Vespertilio murinus L. The 12 flea the main hosts of 10 species of fleas. The flea Palae- species of the family Ischnopsyllidae are probably opsylla alpestris of the family Hystrichopsyllidae oc- distributed in the foothill and middle mountain belts curs ubiquitously on the Levantine mole levan- tis Thomas and the Caucasian mole T. caucasica over the entire Great Caucasus, similar to their hosts Satunin. The range of one more mole parasite, (Labunets and Degtyareva, 1985). P. caucasica, is restricted to the West Caucasus. The Fleas of Carnivores Moles appear to be the main hosts of P. osetica. The flea Archaeopsylla erinacei of the family Pulicidae Carnivores serve as the main hosts of 14 flea spe- parasitizes the northern white-breasted hedgehog Eri- cies in the Great Caucasus. The flea Pulex irritans naceus roumanicus in the foothills of the Great Cauca- infests mammals of the families Canidae, Mustelidae, sus. and Felidae. The parasites of the wolf Canis lupus L., The fleas Doratopsyla dampfi and Palaeopsylla the red fox Vulpes vulpes (L.), and the badger Meles gromovi are also distributed in all the areas of the meles (L.) are three species of fleas: Chaetopsylla Great Caucasus inhabited by their hosts, three species globiceps and C. trichosa of the family Vermipsylli- of long-tailed shrews of the genus L. and the dae, and also Echidnophaga popovi of the family Puli- Transcaucasian water shrew teres Miller. cidae. The flea Paraceras melis, also of the family White-toothed shrews of the genus Wagler Pulicidae, is a specific parasite of the badger. The are widely distributed over a considerable part of the common marten Martes martes (L.) and the stone mar- Great Caucasus. Their parasites, Leptopsylla algira ten M. foina (Erxleben) are infested with Chaetopsylla and L. sexdentata of the family Leptopsyllidae, were mirabilis, C. caucasica, and C. rothschildi. One more recorded on these shrews only in the eastern part of species of the genus Chaetopsylla, C. homoea, was the region. recorded on the least weasel Mustela nivalis L. and the stoat M. erminea L., whereas the flea C. hyaenae was The Fleas of Bats found on the brown bear Ursus arctos L. The data on the host associations of the specific bat In the Great Caucasus, the flea Ctenocephalides fe- ectoparasites of the family Ischnopsyllidae in the lis was mostly recorded on the domestic cat Felis ca- Great Caucasus are still largely incomplete. The flea tus L., and another species of this genus, C. canis, on Rhinolophopsylla unipectinata was found on Mehely’s the domestic dog Canis familiaris L. horseshoe bat Rhinolophus mehelyi Matschie and may Most species of carnivores and their parasites are infest other horseshoe bats present in the region. distributed over the whole territory of the Great Cau- Mouse-eared bats of the genus Myotis Kaup are hosts casus. The only exception is the flea Echidnophaga of the fleas Ischnopsyllus intermedius and I. dolosus. popovi whose distribution is restricted to the eastern The brown long-eared bat Plecotus auritus L. is in- Great Caucasus, where the species occurs at the west- fested with the fleas Ischnopsyllus hexactenus and ern boundary of its range. Nycteridopsylla pentactena. The latter species repre- sents a peculiar genus of fleas whose adults parasitize The Fleas of Rodents bats only in winter. The flea N. pentactena was also found on the barbastelle Barbastella barbastellus Rodentia is the largest order of mammals. In the Great Caucasus rodents serve as main hosts of 56 flea (Schreber) and the common pipistrelle Pipistrellus species, or more than half of all the mammal fleas in pipistrellus (Schreber). Two other members of the the local fauna. Many of these fleas have wide ranges genus Nycteridopsylla, N. eusarca and N. pentactena, of hosts including representatives of different families were also found on the latter host. of rodents which, however, all belong to the same Nathusius’s pipistrelle Pipistrellus nathusii ecological group. For example, the social vole Micro- (Keyserling et Blasius) is the main host of the flea tus socialis (Pallas) () and the Lybian jird Ischnopsyllus variabilis, whereas the various noctule Meriones erythrourus Gray (Muridae) co-occur in bats of the genus Nyctalus Bowdich are the main hosts some xerophytic biotopes. Their common parasite is of I. elongatus. The flea I. intermedius infests the se- the flea Rhadinopsylla ucrainica. Such fleas as

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Ctenophthalmus orientalis and C. golovi are common Voles are hosts of various flea species. For exam- to the steppe-dwelling voles and hamsters (Cricetidae) ple, the main hosts of the flea C. schuriscus are the and the Caucasian mountain ground squirrel Spermo- common and shrub voles while those of the flea philus musicus Menetries (Sciuridae). The flea Cera- C. shovi are the same two species and also the Cauca- tophyllus sciurorum infests the Caucasian squirrel sian snow vole. The flea Amalaraeus improvisus is Sciurus anomalus Gmelin and the red squirrel associated with the same hosts and also with Robert’s S. vulgaris L. as well as dormice (Gliridae) which also snow vole. The typical parasite of the water vole in the live on trees. western and central parts of the Great Caucasus is Members of the family Sciuridae are the main hosts Amalaraeus arvicolae, whereas in the central and of nine species of fleas. In particular, Oropsylla ida- eastern parts it is Megabothris walkeri. The long- hoensis, Citellophilus tesquorum, Frontopsylla se- clawed mole vole Prometheomys schaposchnikovi mura, and C. golovi occur on the Caucasian mountain Satunin was recorded as the main host of ground squirrel in the whole of Elbrus region. The flea Ctenophthalmus inornatus in the West and Central Rhadinopsylla li was found on this host only in the Caucasus. alpine belt, whereas Neopsylla setosa and Cteno- There are several species of ground voles of the ge- phthalmus orientalis were recorded only in the eastern nus Fatio in the Great Caucasus. The shrub part of the host range. The flea Tarsopsylla octo- voles T. majori Thomas and T. daghestanicus Shid- decimdentata was brought to the Caucasus during the lovsky can be distinguished only by karyotypic charac- first half of the last century, in the process of introduc- ters (Akhverdyan et al., 1992); therefore, the parasite tion of the red squirrel from Altai. faunas of these two species are difficult to character- One of the rare flea species is Myoxopsylla jordani, ize. a parasite of the forest and edible dormice (Gliridae). On the whole, ground voles in the territory of the Of the family Allactagidae, the small five-toed jer- Great Caucasus serve as hosts to the following 15 boa Allactaga elater (Lichtenstein) and the Euphrates species from three families of fleas: Amalaraeus im- jerboa A. euphratica Thomas are the main hosts of the provisus, Megabothris turbidus, and Nosopsyllus con- fleas Ophthalmopsylla volgensis and Mesopsylla ap- similis of the family Ceratophyllidae; Amphipsylla scheronica of the family Leptopsyllidae in the Great rossica and Frontopsylla caucasica of the family Lep- Caucasus. topsyllidae; Ctenophthalmus parvus, C. schuriscus, More than 40 species of fleas have been recorded C. wagneri, C. dagestanicus, C. kirschenblatti, C. go- on various rodents of the family Cricetidae. Some lovi, Rhadinopsylla caucasica, Stenoponia ivanovi, representatives of the subfamilies Cricetinae and Arvi- and Hystrichopsylla satunini of the family Hystricho- colinae are infested with the same flea species. For psyllidae. However, of all these species, only example, such fleas as Callopsylla caspia, Megaboth- Ctenophthalmus parvus and C. dagestanicus are spe- ris turbidus, Frontopsylla caucasica, Ctenophthalmus cific parasites of ground voles of the genus Terricola. golovi, and C. intermedius occur in the mixed colonies The remaining flea species are non-specific parasites, of the common vole arvalis (Pallas) and the their diversity being determined by the broad distribu- water vole terrestris L., and also of the tion of ground voles over the Great Caucasus. Georgian hamster Mesocricetus raddei (Nehring) and It should be noted that in the foothill forests on the the gray hamster Cricetulus migratorius (Pallas) in the north slopes of the western Great Caucasus, the shrub alpine areas of the East Caucasus. These host-parasite communities facilitate the transfer of the plague vole serves as the main host only to three of the above pathogen between the different and flea species species. In contrast, seven flea species occur on the in the East Caucasian natural alpine plague focus. shrub vole in the alpine belt of the West Caucasus (Belyavtseva and Teknedzhan, 1983; Kotti and Ko- Among the fleas associated with Cricetinae there tova, 2014). are some examples of ultraspecific parasites. For in- stance, the flea Amphipsylla schelkovnikovi occurs The common vole Microtus arvalis (Pallas) is only on the gray hamster, whereas Ctenophthalmus a widespread inhabitant of steppes and meadows. In rettigi and C. acuminatus infest only the Ciscaucasian the Great Caucasus this rodent is the main host of hamster. 18 flea species, none of which is monoxenous. Only

ENTOMOLOGICAL REVIEW Vol. 95 No. 6 2015 FLEAS (SIPHONAPTERA) OF MAMMALS AND BIRDS 735 one flea, Nosopsyllus consimilis, occurs on the com- formes) and the little owl Athene noctua (Scopoli) mon vole ubiquitously (except the alpine areas). (Strigiformes); both bird species tend to nest in build- ings. The flea Callopsylla gemina was recorded on the The Caucasian snow vole gud Satunin and Robert’s snow vole C. roberti Thomas are the rock pigeon Columba livia Gmelin (Columbiformes) main hosts of the fleas Callopsylla saxatilis, Amphi- and the chough Pyrrhocorax pyrrhocorax (L.) (Pas- psylla kuznetzovi, Paradoxopsyllus hesperius, Cteno- seriformes). The flea Frontopsylla frontalis is a para- phthalmus chionomydis, C. bifurcus, and Paraneo- site of the isabelline wheatear Oenanthe isabellina psylla dampfi in the Great Caucasus. (Temminck) (Passeriformes) but it was also recorded on the Caucasian snowcock Tetraogallus caucasicus The fauna of the Great Caucasus includes six spe- (Pallas) (Galliformes). cies of the family Muridae. Of the 15 species of fleas Among the birds of prey, only one species is a host recorded on murid rodents, three species are associ- of a monoxenous flea. In particular, the flea Callo- ated with wood mice of the genera Sylvaemus Ognev psylla gypaetina parasitizes the bearded vulture and Apodemus. The fleas Leptopsylla taschenbergi Gypaetus barbatus (L.) that nests in rock cavities. and Nosopsyllus mokrzeckyi also parasitize the house mouse Mus musculus L. The latter is the main host of Passerines comprise the great majority in the bird the monoxenous flea Leptopsylla segnis. The flea fauna of the Great Caucasus. They are infested with fauna of the brown rat Rattus norvegicus (Berkenhout) 16 species of fleas, of which seven occur in well- in the Great Caucasus includes two species from dif- protected perennial nests of swallows and martins ferent families, namely Nosopsyllus fasciatus and (Hirundinidae). Only one of them, Ceratophyllus styx, Xenopsylla cheopis. is a monoxenous parasite of the sand martin Riparia riparia (L). Such fleas as Callopsylla waterstoni, The subfamily Gerbillinae is represented in the re- Ceratophyllus farreni, C. rusticus, C. caliotes, C. hi- gion only by the Lybian jird that inhabits the south- rundinis, and Frontopsylla laeta infest the common eastern foothills of the Great Caucasus. Fleas of four house martin Delichon urbica L. and the crag martin different families have been recorded there on this Ptyonoprogne rupestris (Scopoli), building mud nests. host: Xenopsylla conformis of the family Pulicidae, Nosopsyllus laeviceps of the family Ceratophyllidae, Fleas have been also recorded on 41 passerine bird Stenoponia tripectinata of the family Hystrichopsylli- species from the following 13 families: Alaudidae, dae, and Coptopsylla caucasica of the family Coptop- Motacillidae, Sturnidae, Corvidae, Trogloditidae, syllidae (Kadatskaya, 1969). Prunellidae, Sylviidae, Muscicapidae, Paridae, Sitidae, Passeridae, Fringillidae, and Emberizidae. However, Thus, about half of the 95 flea species associated no flea species shows clear preference for hosts from with mammals in the Great Caucasus are monoxenous any particular bird family, due to the fact that these parasites. The fleas infesting hosts from one or several birds build a new nest for each laying. For example, families make up a considerable fraction (31%), the hosts of the flea Dasypsyllus gallinulae build vari- whereas the fraction of oligoxenous parasites is much ously designed nests in such humid biotopes as forests smaller (17%). or river banks.

The Fleas of Birds The hosts of the fleas Ceratophyllus gallinae and C. pullatus nest in tree hollows and similar sheltered There are 270 species of birds nesting in the Great places. These are, for example, the great tit Parus ma- Caucasus and adjoining territories (Khokhlov and jor L. and the coal tit P. ater L. Such forest birds as Ilyukh, 1998; Belik et al., 2003, 2013). Various birds the common chiffchaff Phylloscopus collybita (Vieil- of the orders Anseriformes, Falconiformes, Columbi- lot), the chaffinch Fringilla coelebs L., and the Eura- formes, Strigiformes, and Passeriformes are hosts of sian wren Troglodytes troglodytes (L.) build nests with 21 species from four genera of fleas. grass walls. They are infested with two species of Some flea species are associated with birds belong- fleas, Ceratophyllus gallinae and C. pullatus. ing to different orders but occupying similar habitats. The fleas Ceratophyllus tribulis and C. fringillae For instance, the flea Ceratophyllus spinosus infests occur on birds that nest in burrows and buildings or the lesser kestrel Falco naumanni Fleischer (Falconi- make their nests of twigs. Such hosts include the

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Table 2. Distribution of fleas in the territory of the Great Caucasus Number of flea species Flea families Great Caucasus West Caucasus Central Caucasus East Caucasus total as a whole Pulicidae 4 4 7 4 7 Vermipsyllidae 7 (1) 7 (1) 4 4 8 (1) Coptopsyllidae 0 0 1 0 1 Ceratophyllidae 29 (1) 33 (1) 32 (1) 26 37 (2) Leptopsyllidae 8 12 17 (2) 8 18 (2) Ischnopsyllidae 1 11 11 11 11 Hystrichopsyllidae 18 (2) 25 (2) 22 (2) 13 34 (6) Total 77 (4) 92 (4) 94 (5) 66 116 (11) The number of endemic species is given in parentheses.

Eurasian tree sparrow Passer montanus (L.), the house psylla georgica, Ctenophthalmus intermedius, and sparrow P. domesticus (L.), the common starling Stur- C. dagestanicus, in the eastern part of the Great Cau- nus vulgaris L., the jackdaw Corvus monedula L., and casus. All these fleas, except for Chaetopsylla cau- the Eurasian magpie Pica pica (L.). One more group casica associated with carnivores, are parasites of unites the fleas of birds nesting on the ground, in rock rodents living in shallow burrows with specific hydro- fissures, and among stones. In particular, the fleas thermal conditions. Ceratophyllus enefdeae, C. vagabundus, C. garei, C. frigoris, and C. borealis parasitize the black red- There are 66 flea species distributed over the entire start Phoenicurus ochruros (S.G. Gmelin), the grey territory of the Great Caucasus. As can be seen from wagtail Motacilla cinerea Tunstall, and the white wag- Table 2, the flea fauna of the Central and East Cauca- tail Motacilla alba L. sus includes more species than that of the West Cauca- sus. Thus, the host-parasite associations between fleas Some fleas infesting birds and carnivores are dis- and birds depend on such factors as the duration of tributed from the foothills to the subalpine belt. Be- nest use by the host and the nest position (Darskaya, sides, such parasites of small mammals as Megaboth- 1964; Jurik, 1974). The latter factor determines the ris turbidus, Amphipsylla rossica, Leptopsylla ta- temperature and humidity inside the nest, which are schenbergi, Ctenophthalmus proximus, C. golovi, important conditions for the nidicolous parasites. C. wagneri, Palaeopsylla gromovi, Hystrichopsylla talpae, and H. satunini also occupy a wide range of The Distribution of Fleas over the Great Caucasus altitudes. Among the 41 flea genera known from the Cauca- Such bird and rodent parasites as Callopsylla cas- sus, only the genera Caenopsylla, Phaenopsylla, and pia, C. waterstoni, C. gemina, C. gypaetina, Cerato- Araeopsylla are present in the southern Transcaucasia phyllus caliotes, C. rusticus, C. enefdeae, Amalaraeus but absent in the Great Caucasus. improvisus, A. dissimilis, Paradoxopsyllus hesperius, There are 11 flea species endemic to the Great Cau- Frontopsylla caucasica, F. laeta, Amphipsylla kuznet- casus, which comprise 10% of the total number of zovi, Ctenophthalmus chionomydis, C. churiscus, Rha- fleas in this territory. The ranges of Ctenophthalmus dinopsylla caucasica, R. li, and Paraneopsylla dampfi parvus and C. kirschenblatti are restricted to the west mostly occur in the subalpine belt and the alpine of the Great Caucasus, and those of Chaetopsylla cau- meadows. casica and Amalaraeus improvisus, to the west and Among the inhabitants of the foothill and middle center of the region. Ctenophthalmus bifurcus and mountain belts there are fleas associated with bats as C. kazbek were recorded in the central, and Callo- well as some rodents and birds, in particular, Xeno- psylla kazbegiensis, Paradoxopsyllus gussevi, Amphi- psylla conformis, Coptopsylla caucasica, Myoxopsylla

ENTOMOLOGICAL REVIEW Vol. 95 No. 6 2015 FLEAS (SIPHONAPTERA) OF MAMMALS AND BIRDS 737 jordani, Ceratophyllus sciurorum, C. gallinae, 6. Darskaya, N.F., “On Comparative Ecology of Bird Fleas C. fringillae, C. pullatus, C. tribulis, Tarsopsylla oc- of the Genus Ceratophyllus Curt., 1832,” in Bek- todecimdentata, Nosopsyllus. consimils, N. laeviceps, lemishev, V.N. and Tiflov, V.E., Ectoparasites (Mos- Ctenophthalmus secundus, Rhadinopsylla ucrainica, cow State Univ., Moscow, 1964), pp. 31–180 [in Rus- and Stenoponia tripectinata. These fleas are absent in sian]. the alpine belt even though some of their hosts occur 7. Isaeva, E.V., “A Review of the Fauna of Fleas (Sipho- at those altitudes. naptera) of Azerbaijan,” Probl. Osobo Opasn. Inf. 1 (17), 177–195 (1971). CONCLUSION 8. Isakov, Yu.A., Zimina, R.P., and Panfilov, D.V., “The Fauna,” in The Caucasus, Ed. by A.P. Gerasi- The parasites of rodents prevail among the fleas in mov (Nauka, Moscow, 1966), pp. 256–304 [in Rus- the Caucasian fauna, whereas the number of species sian]. infesting carnivores, bats, and insectivores is several 9. Jurik, M., “Bionomics of Fleas in Bird Nests in the times smaller. Only one flea species occurs on even- Territory of Czechoslovakia,” Acta Sci. Natur. Brno 8 toed ungulates. (10), 1–54 (1974). 10. Kadatskaya, K.P., Candidate’s Dissertation in Biology More than half the flea species are broadly distrib- (Saratov, 1969). uted over the Great Caucasus. The fleas having narrow 11. Kotti, B.K., “On Zoogeography of the Caucasus,” in regional ranges may occur on hosts with narrow or Modern Biogeography, Ed. by A.A. Likhovid and wide ranges. The distribution of flea species over the V.K. Rakhilin (Stavropol State Univ., Stavropol, 2005), altitudinal belts of the Great Caucasus has some spe- pp. 216–223 [in Russian]. cific traits. There are examples of the same flea spe- 12. Kotti, B.K., Species Diversity of Fleas (Siphonaptera) cies occurring on different hosts at different altitudes; of the Caucasus (North-Caucasus Fed. Univ., Stavropol, on the contrary, there are cases of the species composi- 2014) [in Russian]. tion of fleas on a particular host changing with alti- 13. Kotti, B.K. and Kotova, E.G., “The Fauna of Mammal tude. The general diversity of hosts and natural condi- Fleas (Siphonaptera) of the Malaya Laba—Belaya Inter- tions and the presence of local barriers typical of fluve,” Med. Parazitol. Parazitar. Bolezni, No. 1, 35–37 mountain landscapes have facilitated the formation of (2014). a diverse flea fauna in the Great Caucasus. 14. Kryzhanovskij, O.L., The Composition and Distribution of the Insect Faunas of the World (KMK Sci. Press, ACKNOWLEDGMENTS Moscow, 2002) [in Russian]. The work was financially supported by the Russian 15. Labunets, N.F. and Degtyareva, L.V., “On the Fleas of Foundation for Basic Research (grants 11-04-00917-a Bats in the North Caucasus,” Parazitologiya 19 (3), and 14-04-01139). 177–180 (1988). 16. Matyushkin, E.N., “The Mixed Nature of the Mammal REFERENCES Fauna of the Ussuri Basin: Its Common Features, History, and Recent Manifestations in the Middle 1. Akhverdyan, M.R., Lyapunova, E.A., and Voron- Sikhote-Alin Communities,” in Collected Papers of the tsov, N.N., “Karyology and Systematics of the Shrub Zoological Museum of Moscow State University, Voles of the Caucasus and Transcaucasia (Terricola, Issue 13, Ed. by O.L. Rossolimo and V.A. Dolgov Arvicolinae, Rodentia),” Zool. Zh. 71 (3), 96–100 (Moscow, 1972), pp. 86–144 [in Russian]. (1992). 17. Medvedev, S.G. and Kotti, B.K., “Patterns of Formation 2. Balashov, Yu.S., “Terms and Concepts Used in Study- of the Flea (Siphonaptera) Fauna in the Caucasus,” Pa- ing Populations and Communities of Ectoparasites,” razitologiya 45 (6), 470–487 (2011) [Entomol. Rev. 92 Parazitologiya 34 (5), 361–370 (2000). (4), 409–422 (2012)]. 3. Belik, V.P., “Ornithogeographic Connections and Re- 18. Medvedev, S.G. and Kotti, B.K., “Host Associations gionalization of the Great Caucasus,” Strepet 11 (1), 5– 88 (2013). and Origin of the Caucasian Fauna of Fleas (Siphona- 4. Beme, R.L., Zhordaniya, R.G., and Kuznetsov, A.A., ptera),” Entomol. Obozr. 91 (4), 714–734 (2012) [En- The Birds of (Sabchota Sakartvelo, Tbilisi, tomol. Rev. 93 (3), 293–309 (2013)]. 1987) [in Russian]. 19. Onishchenko, G.G. and Kutyrev, V.V., Natural Plague 5. Dampf, A., “Eine neue Aphanipteren—Art (Ischnopsyl- Foci in the Caucasus, Caspian Sea Region, Central lus dolosus sp. n.) aus dem Kaukasus,” Rev. Russe Asia, and Siberia (Meditsina, Moscow, 2004) [in Rus- d’Entomol. 12, 41–59 (1912). sian].

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