ISSN 0013-8738, Entomological Review, 2013, Vol. 93, No. 5, pp. 595–607. © Pleiades Publishing, Inc., 2013. Original Russian Text © S.G. Medvedev, 2013, published in Entomologicheskoe Obozrenie, 2013, Vol. 92, No. 1, pp. 85–101.
Taxonomic Composition and Zoogeographic Characteristics of the Flea Fauna (Siphonaptera) of Russia S. G. Medvedev Zoological Institute of the Russian Academy of Sciences, Universitetskaya nab. 1, St. Petersburg, 199034 Russia e-mail:
[email protected] Received December 10, 2012
Abstract—255 species and 59 subspecies of fleas from 55 genera of 7 families are known from Russia, which is 30% of the Palaearctic fauna. Additionally, over 187 species of 47 genera from 7 families are known from the neighboring territories of Central and Southern Europe, Transcaucasia, Kazakhstan, Middle Asia, Mongolia, Northeast China, and Japan. 13 species of 12 genera are known only from Russia. Noteworthy is the low percent of endemic species (not more than 4%) and genera (one genus) in the Russian fauna. The principal centers of taxonomic diversity in the Palaearctic, including many endemic species and genera, lie in the Eastern Asian, Central Asian, and Turano-Iranian Subregions, outside Russia and the Euro-Siberian Subregion. The bulk of the Russian fauna is formed by the species and genera of the three largest flea families: Hystrichopsyllidae, Ceratophyllidae, and Leptopsyllidae. The family Ceratophyllidae has the greatest number of genera in the Russian fauna, and Hystrichopsyllidae, the greatest number of species. Western (Western and Western-Central Palaearctic; 84 species from 41 genera of 7 families) and Eastern (Central-Eastern and Eastern Palaearctic; 78 species from 42 genera of 6 families) species are nearly equally represented in the Russian fauna. DOI: 10.1134/S0013873813050084
The aim of the present study is to characterize the volume and taxonomic composition of the flea fauna of Russia and to estimate the distribution of taxonomic diversity over this vast territory. Most of the previous publications have been devoted to the species composition of the flea fauna of the former USSR and Mongolia, i.e., the Eurasian territory comprising not only a significant part of the Euro-Siberian zoogeographic Subregion but also the Turano-Iranian and Central Asian Subregions of the Palaearctic. In view of the geopolitical changes that occurred in the last 20 years, the time is ripe now for inventory of the flea species composition in the territory of Russia, with the purpose of determining the place of the Russian flea fauna in the total Palaearctic fauna and revealing the possible ways of its formation. The importance of this study is determined by high medical significance of fleas as vectors of plague and endemic typhus fever. The plague microbe is transferred by various flea species in more than 24 natural foci in the territories of the Caucasus and Transcaucasia, Kazakhstan, South Siberia, and the Far East, posing a hazard to human health. This publication continues the series of papers devoted to patterns of formation of the flea fauna of Rus-
sia. In earlier communications we have analyzed the taxonomic composition and host associations of fleas in the fauna of the Caucasus as well as the patterns of formation of this fauna (Medvedev and Kotti, 2011, 2012). The ranges of fleas present in the Palaearctic fauna were classified into 7 large groups reflecting its connections with the faunas of other territories. Based on paleogeographic reconstructions, a hypothesis about the possible Western Palaearctic and Eastern Palaearctic sources of the Caucasian flea fauna was put forward. MATERIALS AND METHODS The flea fauna of the Palaearctic has been intensively studied by many experts. The data on the fauna of the former USSR were published in a series of regional keys prepared by I.G. Ioff and a group of his pupils and colleagues (Ioff and Skalon, 1954; Ioff et al., 1965; Skalon, 1970; Tiflov et al., 1977). Extensive material on the distribution of flea species in the Palaearctic fauna was published in the Illustrated Catalogue of the Rothschild Collection of Fleas (Hopkins and Rothschild, 1953, 1956, 1962, 1966, 1971; Traub and Rothschild, 1983). Data on the distribution and host associations of various flea species were presented in the series of papers by R . E . Lewis (1972,
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1973, 1974a, 1974b, 1974c, 1975, 1993; Lewis and Lewis, 1985). There are monographs on the flea faunas of China (Liu et al., 1986), Mongolia (Goncharov et al., 1989), France (Beaucournu and Launay, 1990), and Greece (Beaucournu, 1988). Analysis of data on the flea fauna of Russia was performed using the Information Analytical System (IAS) Parhost1 (Medvedev, 1996, 1997a, 1997b) and Excel spreadsheets. The software of the IAS Parhost1 allows one not only to analyze the associations between certain taxa of fleas and their hosts but also to reveal the specific patterns of these associations in different zoogeographic regions. The Excel spreadsheets were used at the preparatory stage, as a prototype database and an instrument of preliminary unification of the published and collection data. In our previous analysis of the Palaearctic fauna, we followed a scheme according to which this territory was subdivided into 6 subregions; 3 of them, namely the Euro-Siberian, Mediterranean, and Turano-Iranian Subregions, was subdivided into 2 provinces each. The corresponding map of biogeographic subdivision of the Palaearctic had been published earlier (Medvedev, 1996). This scheme shows a good general agreement with the patterns of flea distribution, whereas the individual territorial units are characterized by significant levels of specific and generic endemism.
lia, Northeast China, and Japan. The ranges of these species adjoin the borders of Russia. As noted earlier (Medvedev, 1998a), the faunas of zoogeographic regions are characterized by large fractions of endemic flea species. In particular, the Palaearctic flea fauna includes 94% of endemic species. A few species are known exclusively from the territory of Russia; of these, the following 13 species can be mentioned: Chaetopsylla (Ch.) zibellina of the family Vermipsyllidae; Ceratophyllus (C.) olsufjevi, Margopsylla tolli, Igioffius taiganus and Ceratophyllus (Monopsyllus) paradoxus of the family Ceratophyllidae; Paradoxopsyllus scalonae, Frontopsylla (F.) scalonae and Ophthalmopsylla (Cystipsylla) kasakiensis of the family Leptopsyllidae; Ischnopsyllus (Hexactenopsylla) ussuriensis (Ischnopsyllidae); Rhadinopsylla (Actenophthalmus) acuminata, Eopsylla nuda, Hystrichopsylla (H.) nicolai and Ctenophthalmus (Spalacoctenophthalmus) gigantospalacis of the family Hystrichopsyllidae. Thus, the fraction of “endemic” or, most likely, insufficiently studied species in the fauna of Russia comprises about 4%. The fauna of Russia includes only one monotypic endemic genus: Eopsylla, found in the nest of the Siberian flying squirrel Pteromys volans and on the red-backed vole Clethrionomys rufocanus.
According to the preliminary data, more than 255 species and 59 subspecies of fleas representing 55 genera from 7 families have been recorded in the territory of Russia (Table 1). They constitute about 30% of the total fauna of the Palaearctic, which comprises over 900 species.
The Palaearctic fauna includes a total of 96 genera. The ranges of 53 genera can be classified into 10 types. The largest group (18 genera) is characterized by ranges of the Holarctic type; 9 genera have Palaearctic-Indo-Malayan ranges, 8 genera, Palaearctic-Afrotropical-Indo-Malayan ones, and 7 genera, Holarctic-Neotropical ones. Ranges of the PalaearcticAfrotropical type are observed in 3 genera only. Some genera in the Palaearctic fauna also have HolarcticIndo-Malayan (3 genera), Holarctic-Malayan-Neotropical (1), Holarctic-Afrotropical-Neotropical (1), Palaearctic-Afrotropical-Indo-Malayan-Australian (1), and Palaearctic-Afrotropical-Australian (1 genus) ranges (Table 2). The similarity indices (SI) calculated for the flea faunas at the genus level have shown the faunas of the Palaearctic and the Nearctic Regions to be the most similar (22%). The Palaearctic fauna is also close to that of the Indo-Malayan Region (17%).
In addition, at least 187 species of fleas representing 47 genera from 7 families are known from the neighboring territories of Central and South Europe, the Transcaucasia, Kazakhstan and Middle Asia, Mongo-
The largest ranges extending over the territories of 4 zoogeographic regions are known in the genera Ctenophthalmus (family Hystrichopsyllidae) and Xenopsylla (family Pulicidae), which are also the larg-
The Composition of the Flea Faunas of the Palaearctic and Russia The fleas in the fauna of Russia and the Palaearctic as a whole mostly occur on various species of rodents of the families Muridae, Arvicolidae, Gerbillidae, and to a lesser extent, Cricetidae. Among other mammal orders, species of lagomorphs and insectivores have been recorded as hosts of fleas. Some flea species in the fauna of Russia occur on birds, among which passerine birds play the major role as their hosts.
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Table 1. The number of species of different flea families in the faunas of Russia and the entire Palaearctic (numerator: the total number of species and genera; denominator: the number of endemic species and genera) Families of fleas Ancistropsyllidae Coptopsyllidae Vermipsyllidae Pulicidae Tungidae Ceratophyllidae Ischnopsyllidae Leptopsyllidae Hystrichopsyllidae Stivaliidae Total
Number of species
Number of genera
Palaearctic
Russia
Palaearctic
Russia
1 1 19 19 35 34 38 31 2 2 202 176 50 46 205 198 332 324 8 5 892 836
0 0 2 0 14 1 13 0 0 0 70 2 16 1 54 3 86 4 0 0 255 11
1 0 1 1 3 2 10 3 1 0 24 11 8 1 26 17 19 8 3 0 96 43
0 0 1 0 1 0 6 0 0 0 16 0 3 0 12 0 14 1 0 0 55 1
est genera of the order. The former genus is represented in the Russian fauna by 20 species and 17 subspecies. The genus Xenopsylla, mostly associated with semi-desert and desert areas, is represented in the Russian fauna by 10 species and 3 subspecies. The ranges covering 3 zoogeographic regions are characteristic of 18 genera of the families Hystrichopsyllidae (5 genera), Pulicidae (5), Ischnopsyllidae (5), and Ceratophyllidae (3 genera). The flea genera whose species are distributed in 2 zoogeographic regions also constitute a considerable group. There are 10 such genera in the family Ceratophyllidae, 9 in Leptopsyllidae, 5 in Hystrichopsyllidae, and 2 in Ischnopsyllidae. The remaining 43 genera (47% of the total number) are characterized by Palaearctic ranges that belong to 15 types. Among the genera endemic to the Palaearctic, the greatest fraction (40%, or 17 genera) belongs to the family Leptopsyllidae; the family Ceratophyllidae comprises 26% (11 genera), and the family Hystrichopsyllidae, 19% (8 genera). When analyzing the composition of the flea fauna of Russia, we also have to characterize the centers of ENTOMOLOGICAL REVIEW Vol. 93 No. 5 2013
taxonomic diversity of fleas in the Palaearctic. The greatest number of genera and species can be found in two subregions of the Palaearctic. The known fauna of the Eastern Asian Subregion comprises over 320 species of 59 genera; 8 genera are endemic, in particular Megathoracipsylla, Rowleyella, and Spuropsylla of the family Ceratophyllidae; Typhlomyopsyllus and Aconothobius of the family Leptopsyllidae; Liuopsylla (Hystrichopsyllidae) and Mitchella (Ischnopsyllidae). In the Central Asian Subregion there are over 270 species of 54 genera (including 5 endemic ones). The genera Dorcadia of the family Vermipsyllidae, Brevictenidia of the family Ceratophyllidae, Calceopsylla, Chinghaipsylla, and Minyctenopsyllus of the family Leptopsyllidae are distributed only in the Central Asian Subregion. The fauna of the Turano-Iranian Subregion includes 3 endemic genera: Rostropsylla (Ceratophyllidae), Phaenopsylla and Desertopsylla (Leptopsyllidae); that of the Euro-Siberian Subregion includes 2 endemic genera: Ornithopsylla (Pulicidae) and Brachyctenonotus (Leptopsyllidae); that of the Mediterranean Subregion includes 1 endemic genus: Hopkinsipsylla of the family Leptopsyllidae.
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Table 2. The number of species and subspecies of fleas in the fauna of Russia and adjacent territories Flea taxa
Pulex Echidnophaga Ctenocephalides Pariodontis Synosternus Xenopsylla Euchoplopsyllus Archaeopsylla Spilopsyllus Chaetopsylla Dorcadia Vermipsylla Coptopsylla
Range type
Russia species
Adjacent territories
subspecies
Family Pulicidae Neotropical-Nearctic 1 Palaearctic-Afrotropical-Australian 2 Palaearctic-Afrotropical-Indo2 Malayan Palaearctic-Afrotropical-IndoMalayan Palaearctic-Afrotropical-IndoMalayan Palaearctic-Afrotropical-Indo4 Malayan-Australian Holarctic-Neotropical Trans-Palaearctic 2 Euro-Mediterranean 1 Family Vermipsyllidae Holarctic 13 Central Asian 1 Central-Eastern Asian Family Coptopsyllidae Trans-Palaearctic 2 Family Ceratophyllidae
species
subspecies
1 5 4
3 2 1
1
3
1
2 3
10
3
17
1
1
3 2 1
3
1
17 1 2
3
12
2 1
Total
6
Dasypsyllus
Holarctic-Indo-Malayan-Neotropical
2
2
Ceratophyllus
Holarctic-Neotropical
29
5
4
3
41
Nosopsyllus
Palaearctic-Afrotropical-IndoMalayan
5
3
10
7
25
Paraceras
Palaearctic-Indo-Malayan
1
1
Amalaraeus
Holarctic
5
4
Amphalius
Holarctic
1
Margopsylla
Holarctic
1
Megabothris
Holarctic
7
Mioctenopsylla
Holarctic
2
2
Oropsylla
Holarctic
5
1
Tarsopsylla
Holarctic
1
Callopsylla
Trans-Palaearctic
6
1
6
2
15
Citellophilus
Trans-Palaearctic
4
2
8
4
18
Igioffius
Euro-Asian (extra-Mediterranean)
1
1
Myoxopsylla
Euro-Mediterranean-Iranian
1
1
Brevictenidia
Central Asian
Paramonopsyllus
Eastern Asian
1
Aenigmopsylla
Eastern Asian
1
Rostropsylla
Turanian
2 1
5
14
1
3 1
2
1
10 4
1
7 1
1
1
1
2 1
1
1
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Table 2 (Contd.) Flea taxa
Amphipsylla Ctenophyllus Peromyscopsylla Ornithophaga Leptopsylla Mesopsylla Ophthalmopsylla Paradoxopsyllus Pectinoctenus Frontopsylla Ochotonobius Brachyctenonotus Caenopsylla Phaenopsylla Desertopsylla Myodopsylla Nycteridopsylla Araeopsylla Ischnopsyllus Rhinolophopsylla Ctenophthalmus Atyphloceras Corrodopsylla Hystrichopsylla Neopsylla Doratopsylla Catallagia Rhadinopsylla Stenoponia Nearctopsylla Palaeopsylla Eopsylla Typhloceras Paraneopsylla Wagnerina Total
Range type
Russia species
Family Leptopsyllidae Holarctic 12 Holarctic 2 Holarctic 6 Holarctic 1 Palaearctic-Afrotropical 5 Trans-Palaearctic 3 Trans-Palaearctic 5 Euro-Siberian-Turano-Iranian5 Central-Eastern Asian Euro-Siberian-Turano-Central Asian 2 Euro-Siberian-Turano-Iranian11 Central-Eastern Asian Euro-Asian (extra-Mediterranean) 1 European 1 Sahara-Mediterranean-Turano-Iranian Turano-Iranian Turanian Family Ischnopsyllidae Holarctic-Neotropical 1 Holarctic-Indo-Malayan 3 Palaearctic-Afrotropical-IndoMalayan Palaearctic-Afrotropical-Indo12 Malayan Palaearctic-Afrotropical Family Hystrichopsyllidae Holarctic-Afrotropical-Neotropical 28 Holarctic-Neotropical 1 Holarctic-Neotropical 1 Holarctic-Neotropical 5 Holarctic-Indo-Malayan 9 Holarctic-Indo-Malayan 2 Holarctic 4 Holarctic 15 Holarctic 5 Holarctic 1 Palaearctic-Indo-Malayan 9 Central Asian 1 Euro-Mediterranean Euro-Asian (extra-Mediterranean) 2 Euro-Asian (extra-Mediterranean) 2 256
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Adjacent territories
subspecies 6 1 1 4 2
10
species
subspecies
13 2 2
6
2 2 3 9 4 11
4 5
8
2
Total
37 4 9 1 8 13 15 14 6 40 3 1 1 4 1
1 4 1
9 1
1
1 13 1
2
1
15
1
1
2
7 1
20 1
17
3
6 1
4 1
2 1
5
1
8 5 1 5
60
1 1 3 187
72 3 1 5 22 4 4 30 11 2 16 1 1 3 7 591
1
2 88
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The Eastern Asian Subregion can be distinguished both by the total number of species and by the highest fraction of endemic species among them (68%, or 215 out of 320 species). Endemic species comprise 46% in the fauna of the Central Asian Subregion and from 30 to 40% in the faunas of the Turano-Iranian and Mediterranean Subregions and the European Province. The dendrograms of faunistic similarity at the genus level based on the Jaccard and Czekanowski-Sørensen indices reveal a similar picture. In particular, the faunas of the Central Asian and Euro-Siberian Subregions are the most similar, whereas the fauna of the TuranoIranian Subregion is close to them. These three subregions are clustered together with the Eastern Asian Subregion. In turn, the faunas of the Sahara-Arabian and Mediterranean Subregions are grouped together. Most of the territory of Russia belongs to the EuroSiberian Subregion whose fauna includes over 280 species of 51 genera. It resembles the Central Asian Subregion in the number of genera and species but is distinguished by the smallest fractions of endemic species (less than 37%) and genera (less than 4%). The vast majority of flea species in the fauna of Russia (213, or 83% of the total number) belongs to 3 families: Hystrichopsyllidae 1 , Ceratophyllidae, and Leptopsyllidae. In the fauna of the entire Palaearctic, species of these 3 families also comprise 83%. The common trait in their geographic distribution is concentration of most taxa in the northern hemisphere where a rich and diverse fauna of these 3 families has been formed. Such distribution is also characteristic of the bat parasites of the family Ischnopsyllidae which is essentially cosmopolitan (with exception of the Antarctic Region). The greatest number of endemic genera and species in the families Hystrichopsyllidae (the infraorder Hystrichopsyllomorpha), Ceratophyllidae, Leptopsyllidae, and Ischnopsyllidae (the infraorder Ceratophyllomorpha) 2 is observed in the Central and Eastern Asian Subregions of the Palaearctic (Medvedev, 1998a). For example, endemic Palaearctic genera constitute over 50% in the family Hystrichopsyllidae, 46% in Ceratophyllidae, and 65% in Leptopsyllidae. _____________ 1
As in our previous publications (Medvedev, 2009b), the family Hystrichopsyllidae is considered here in the broad sense. 2 The subdivision of the order of fleas into 4 infraorders was proposed earlier (Medvedev, 1994, 1998b, 2009b).
The relative diversity of species and genera of these 3 families in Russia somewhat differs from that in the entire Palaearctic. In the fauna of the Palaearctic, genera of the families Leptopsyllidae, Ceratophyllidae, and Hystrichopsyllidae comprise 27, 25, and 20% of the total number of genera, respectively. In the fauna of Russia, the family Ceratophyllidae is represented by the greatest number of genera (31%), whereas genera of the families Hystrichopsyllidae and Leptopsyllidae comprise 25 and 22%, respectively. The fraction of species of the family Hystrichopsyllidae in the Palaearctic fauna is about 37%, whereas those of the families Leptopsyllidae and Ceratophyllidae are equal (23% each). In the Russian fauna, the fraction of species of the family Hystrichopsyllidae is also the greatest (about 33%). A considerable part of species (28) of the family Hystrichopsyllidae belongs to the polytypic genus Ctenophthalmus. Species of the families Ceratophyllidae and Leptopsyllidae comprise 28 and 21% of the Russian fauna, respectively. Species of the family Ceratophyllidae present in Russia constitute the greatest fraction: 36% of the total number of species of this family known in the Palaearctic. This family is represented in the Russian fauna by the greatest number of genera: 17, among which the genus Ceratophyllus, mostly uniting bird parasites, is distinguished by its species diversity (29 out of 73). It should be noted that species of the family Ischnopsyllidae present in the Russian fauna also constitute a large fraction (32%) of the total number of species of this family known in the Palaearctic. This family of fleas is unique in that all of its species are ectoparasites of bats. The family Ceratophyllidae is characterized by cosmopolitan (Holarctic-Indo-Malayan-AfrotropicalNeotropical-Antarctic) distribution. Its species have been found in all the continents except Australia (they are also absent in New Zealand). Within the Palaearctic, the family is characterized by a gradual decrease in the number of endemic species from the Central Asian to Turano-Iranian to Mediterranean to Sahara-Arabian Subregion. Species of the genus Megabothris are widely distributed in the Euro-Siberian Subregion. Some of them, associated with forest rodents, have transPalaearctic ranges. The genera Callopsylla, Citellophilus, Nosopsyllus, and Oropsylla are represented in the fauna of Russia by 4–6 species each. They mostly occur on rodents in the steppe and desert zones. The ENTOMOLOGICAL REVIEW Vol. 93 No. 5 2013
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remaining genera of the family Ceratophyllidae have 1 or 2 species each in the Russian fauna. Species of the family Leptopsyllidae present in the Russian fauna comprise 26% of their number in the Palaearctic; they belong to 12 genera. The family is characterized by a Holarctic-Afrotropical-Indo-Malayan range, with most of the species (87%) of its 26 genera being concentrated in the Palaearctic. The fauna of the Central Asian Subregion includes the maximum number of species of this family, whereas the fraction of endemics among them (46%) is much smaller than in the Eastern Asian Subregion (72%) and somewhat smaller than in the Turano-Iranian Subregion (48%). Such largest genera of the family Leptopsyllidae as Leptopsylla, Peromyscopsylla, Pectinoctenus of the tribe Leptopsyllini, and also Ctenophyllus, Frontopsylla, Ophthalmopsylla, and Paradoxopsyllus of the tribe Paradoxopsyllini are mostly distributed in the Palaearctic. Species of the monotypic tribe Amphipsyllini and the tribe Paradoxopsyllini occur in the central and eastern parts of the Palaearctic, whereas those of the tribe Leptopsyllini are distributed in the forest zone of its western and central parts. The genera Amphipsylla and Leptopsylla can be distinguished by the number of species in the fauna of Russia (12 and 11 species, respectively). The genera Peromyscopsylla, Leptopsylla, Ophthalmopsylla, and Paradoxopsyllus are represented in Russia by 5 or 6 species each. Two species of the genus Peromyscopsylla, infesting rodents of the genera Mus and Rattus and characterized by trans-Palaearctic ranges, are broadly distributed in the Euro-Siberian Subregion. The remaining genera are represented by 1 to 3 species each; some of them occur in steppes and semi-deserts (fleas of the genus Mesopsylla, on jerboas) or in the mountains (fleas of the genera Ctenophyllus and Ochotonobius, on pikas), whereas some representatives of the monotypic genera parasitize birds (Ornithophaga) or the Siberian zokor (Brachyctenonotus). Fleas of the family Ischnopsyllidae, which are specific ectoparasites of bats, are represented in the Russian fauna by 16 species of 3 genera, which constitutes 32% of the species composition of the Palaearctic fauna of this family. The largest genus is Ischnopsyllus, represented in Russia by 12 species with different types of ranges. Besides, the Russian fauna includes 3 species of the Holarctic genus Nycteridopsylla, characterized by reproduction on the wintering bats. The ENTOMOLOGICAL REVIEW Vol. 93 No. 5 2013
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only Palaearctic species of the genus Myodopsylla has a trans-Palaearctic range and is broadly distributed in the Euro-Siberian Subregion. This genus is otherwise well represented in North and South America. The Palaearctic fauna of the family Ischnopsyllidae is the largest in terms of species diversity: it includes over 50 species of 8 genera, 1 genus being endemic. The greatest number of endemic species in the Palaearctic can be found in the Central Asian Subregion; the number of endemics is smaller in the Eastern Asian and Euro-Siberian Subregions, and is still smaller in the Turano-Iranian and Sahara-Arabian Subregions. The family Hystrichopsyllidae is the largest in the order of fleas. It is represented in the Russian fauna by 86 species and 14 subspecies from 14 genera. Two genera of the subfamily Ctenophthalminae are best represented in the Russian fauna: Ctenopthalmus with 29 species and 6 subspecies, and Palaeopsylla with 9 species. The fauna of Russia also includes 15 species of the genus Rhadinopsylla (Rhadinopsyllinae) and 15 species from 3 genera of the subfamily Neopsyllinae: Neopsylla, Catallagia, and Paraneopsylla. As mentioned above, both the absolute and relative number of endemic species in the family Hystrichopsyllidae is the greatest in the Eastern Asian Subregion; the fraction of endemic species is smaller in the Central Asian Subregion but greater in the TuranoIranian Subregion. Another characteristic trait of the family Hystrichopsyllidae is the presence of a considerable number of endemic species in the Mediterranean Subregion, whereas the Sahara-Arabian fauna of the family is extremely poor. A different type of distribution is characteristic of the other 3 families represented in the Palaearctic and Russian faunas: Pulicidae, Coptopsyllidae, and Vermipsyllidae (the infraorder Pulicomorpha). The family Pulicidae is mostly distributed in the tropical and subtropical zones and is characterized by the absence of endemic species in the Eastern Asian Subregion and a small number of such species in the Euro-Siberian and Central Asian Subregions. At the same time, the greatest fraction of endemics in the family Pulicidae can be observed in the Turano-Iranian Subregion, followed by the Mediterranean and Sahara-Arabian Subregions. In the fauna of Russia the family Pulicidae is represented by only 12 species of 10 genera, 6 species having cosmopolitan ranges. Among the remaining species, broad trans-Palaearctic distribution is typical of the flea Paraceras melis which occurs on
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badgers. Representatives of the genus Archaeopsylla are associated with hedgehogs; the flea A. erinacei has a Western Palaearctic range, and A. sinensis, an Eastern Palaearctic one. The distribution of the families Vermipsyllidae and Coptopsyllidae is limited by the northern hemisphere. In particular, the family Coptopsyllidae is characterized by a Southern Palaearctic or a European-West Mediterranean-Sahara-Arabian-Turano-Iranian range. All the species of this family present in the Mediterranean and Sahara-Arabian Subregions are endemic to these territories, a significant number of endemics being also typical of the Turano-Iranian Subregion. One non-endemic species is present in the Central Asian Subregion. In the fauna of Russia the family Coptopsyllidae is represented by a single species Coptopsylla bairamaliensis distributed in the northwestern Caspian region. This species has a range of the Western Palaearctic type and is a winter parasite of gerbils. The family Vermipsyllidae (39 species of 3 genera) has a Holarctic range. It includes some stationary and semi-stationary parasites associated with carnivores and ungulates. In the fauna of Russia this family is represented by 14 species, among which Chaetopsylla (Arctopsylla) tuberculaticeps, a parasite of bears, has a Holarctic range, and Chaetopsylla (Ch.) homoea, a parasite of mustelid carnivores, has a transPalaearctic range; the ranges of the remaining 11 species of the genus Chaetopsylla belong to 4 types. The flea Dorcadia dorcadia infesting wild and domestic artiodactyls is distributed in the south of West Siberia. The Ranges of Flea Species in the Russian Fauna For preliminary analysis of the distribution of flea species and genera in the territory of Russia, the species ranges were classified into larger groups according to their association with the western, central, and eastern parts of the Palaearctic. This simplified scheme provides a preliminary estimation of the distribution of taxonomic diversity in the fauna of Russia. The Western Palaearctic conditionally includes the western part of the European Province, including Europe, and territories of the Mediterranean and Sahara-Arabian Subregions. The Central Palaearctic includes the eastern part of the European Province, i.e., the territory of West Siberia from the Ural Mountains to the Yenisei, and also the Turano-Iranian and Central Asian Subregions. The Eastern Palaearctic
includes the Siberian Province and the Eastern Asian Subregion. The ranges of flea species in the fauna of Russia can be classified into (1) Holarctic, (2) transPalaearctic, (3) Western Palaearctic and WesternCentral Palaearctic, (4) Central Palaearctic, (5) Central-Eastern Palaearctic and Eastern Palaearctic (for brevity, the word “Palaearctic” is omitted in the names of these range types in the text below) (Table 3). Each of the 7 families represented in the Russian fauna has a specific ratio of the number of species with different types of ranges. In particular, the family Ceratophyllidae reveals the highest diversity of range types (13 out of the 15 distinguished types). About 40% of the species from 8 genera of this family have vast Holarctic (11 species) or trans-Palaearctic (17 species) ranges. Of these, 9 species are associated with birds, 3 species, with carnivores (badgers and sables), and others, with sciurid and murid rodents. A high diversity of ranges is characteristic of species of the families Leptopsyllidae (10 types) and Hystrichopsyllidae (9 types). Holarctic ranges are observed only in 5 out of 54 species of Leptopsyllidae and in 3 out of 86 species of Hystrichopsyllidae. The fractions of species with trans-Palaearctic ranges in these two families are also relatively small. More than half of the species of the family Leptopsyllidae are represented in the fauna of the Central part of the Palaearctic. The ranges of 2 species of this family (Amphipsylla marikovskii and Peromyscopsylla ostsibirica), parasites of small forest rodents, cover the Eastern Palaearctic and the Canadian Subregion of the Nearctic. A group of 30 species from 8 genera with Western ranges can be distinguished in the family Hystrichopsyllidae; 15 of these species belong to the large genus Ctenophthalmus. Another large group includes species of 10 genera of the family Hystrichopsyllidae which are represented in the CentralEastern (14 species) and Eastern (12 species) parts of the Palaearctic. The greatest number of such species belongs to the genera Rhadinopsylla (6) and Neopsylla (5). Of the 16 species of the family Ischnopsyllidae, 7 are restricted to the Western, and 3, to the Eastern Palaearctic; 5 species of this family have transPalaearctic distribution. The ranges of 12 species of the family Pulicidae known in the Palaearctic belong to 6 types; the broad distribution of 6 species of this family is determined by anthropogenic factors. The ENTOMOLOGICAL REVIEW Vol. 93 No. 5 2013
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603
Archaeopsylla Spilopsyllus Echidnophaga Paraceras Xenopsylla Ctenocephalides Pulex Chaetopsylla Dorcadia
Cosmopolitan
Eastern Palaearctic
Central Palaearctic
Central-Eastern Palaearctic
Western-Central Palaearctic
Family Pulicidae 1 1 1
1 1
1 1
1
1
Coptopsylla Ceratophyllus Amalaraeus Nosopsyllus Myoxopsylla Oropsylla Callopsylla Megabothris Citellophilus Tarsopsylla Mioctenopsylla Aenigmopsylla Igioffius Margopsylla Paramonopsyllus
Western Palaearctic
Holarctic
Genera
Trans-Palaearctic
Table 3. Distribution of flea species in the fauna of Russia by the principal range types
7 1 1
7 1
1 1 4 1
2
Family Vermipsyllidae 3 3 Family Coptopsyllidae 1 Family Ceratophyllidae 3 3 1 1 1 1 3
1
1
2 2 1 4 1
2
1
1
2 1 2 1 4 2 1 13 1
1 2
Total
2 2 1
1
26 4 5 1 5 6 7 4 1 1 1 1 1 1
1
1
5
2
1
1
1 2 1 2
2 1
1 1 1 1 1 Family Leptopsyllidae
Paradoxopsyllus
3
Frontopsylla
2
1
1
Peromyscopsylla
2
1
1
Leptopsylla
1
Amphipsylla
2
Mesopsylla
2 1
1
1
3
4
1
2
Ophthalmopsylla
1
Ctenophyllus
1
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2
11
1
5 1
1
1 2
1
5 11 3
1
5
1
2
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Ochotonobius Pectinoctenus Ornithophaga Brachyctenonotus Ischnopsyllus Nycteridopsylla Myodopsylla
Cosmopolitan
Eastern Palaearctic
Central Palaearctic
Central-Eastern Palaearctic
Western-Central Palaearctic
Western Palaearctic
Holarctic
Genera
Trans-Palaearctic
Table 3 (Contd.)
1 1
1 2 1 1
1 1 1 Family Ischnopsyllidae 4 1 3
4
Total
3
12 3 1
1
29
1 Family Hystrichopsyllidae
Ctenophthalmus
3
15
2
2
6
2
3
3
1
Hystrichopsylla
2
1
1
Doratopsylla
2
Atyphloceras
1
Paraneopsylla
1
Palaeopsylla Rhadinopsylla
7 3
Stenoponia
1
8
3
15
1
5 2 1
1 2
1
1
5
1
4
2
1
9
Catallagia
1
2
Corrodopsylla
1
Neopsylla
1
2
1
1
4 1
Eopsylla
1
1
Nearctopsylla
1
1
Wagnerina Total
37
20
55
27
37
1
1
27
35
2 8
246
Notes: The Eastern-Palaearctic-Indo-Malayan, Eastern-Palaearctic-Nearctic, Eastern-Palaearctic-Nearctic-Neotropical, Western-Palaearctic-Nearctic, trans-Palaearctic-Indo-Malayan-Nearctic-Neotropical, and Central-Eastern-Palaearctic-Nearctic ranges are not shown. For explanation, see text.
fauna of the Eastern Palaearctic includes 5 out of the 14 species of the family Vermipsyllidae, whereas the faunas of the Western and Western-Central parts include 3 species each. The group of fleas with broad trans-Palaearctic and Holarctic ranges includes 59 species from 25 genera of 5 families. Half of them (29 species) belongs to 10 genera of the family Ceratophyllidae, mostly to the genus Ceratophyllus in which 7 species have Holarctic ranges and 7 other species have trans-Palaearctic ranges. Trans-Palaearctic and Holarctic ranges are also
known in some species of the genera Oropsylla, Tarsopsylla, and Amalaraeus. In addition, broad transPalaearctic ranges are characteristic of 4 species of the genus Megabothris and of one species in each of the genera Citellophilus, Nosopsyllus, Callopsylla, and Paraceras. Species of the genus Dasypsyllus have vast ranges extending over several zoogeographic regions. In the family Hystrichopsyllidae, some species of the genera Rhadinopsylla and Ctenophthalmus have trans-Palaearctic ranges, and some species of the genus Neopsylla have Holarctic and trans-Palaearctic ENTOMOLOGICAL REVIEW Vol. 93 No. 5 2013
TAXONOMIC COMPOSITION AND ZOOGEOGRAPHIC CHARACTERISTICS
ones. For example, N. pleskei has a broad EuroSiberian-Turano-Iranian-Central-Eastern Asian range, and N. setosa has a Euro-Siberian-Turano-CentralEastern Asian range. Holarctic ranges are also typical of some species of the genera Catallagia and Corrodopsylla. A similar ratio of the species with trans-Palaearctic and Holarctic ranges can be observed in the family Leptopsyllidae. Ranges of both types are known in some species of the genera Frontopsylla and Peromyscopsylla; trans-Palaearctic ranges are to be found in the genera Ophthalmopsylla, Ctenophyllus and Ochotonobius, and Holarctic ones, in the genera Amphipsylla and Pectinoctenus. One species in the genus Chaetopsylla of the family Vermipsyllidae has a Holarctic range. All the broad ranges observed in species of the family Ischnopsyllidae belong to the transPalaearctic types. The group of fleas with ranges of the Western and Western-Central types includes 84 species from 28 genera of 7 families; of these, 55 species of 21 genera are present in the Western Palaearctic, and 27 species of 14 genera occur in its Western and Central parts. Ranges of 15 species of the genus Ctenophthalmus cover the Western Palaearctic, and those of 2 more species extend over both the Western and the Central parts. Western and Western-Central ranges are characteristic of some (1 to 3) species of the genera Ceratophyllus (Ceratophyllidae), Rhadinopsylla and Hystrichopsylla (Hystrichopsyllidae), Ischnopsyllus (Ischnopsyllidae), Leptopsylla and Frontopsylla (Leptopsyllidae), and also Chaetopsylla and Vermipsylla (Vermipsyllidae). The genera Amalaraeus, Nosopsyllus and Myoxopsylla (Ceratophyllidae), Coptopsylla (Coptopsyllidae), Doratopsylla, Atyphloceras and Paraneopsylla (Hystrichopsyllidae), Nycteridopsylla (Ischnopsyllidae), Paradoxopsyllus and Peromyscopsylla (Leptopsyllidae), and also Archaeopsylla and Spilopsyllus (Pulicidae) are represented by a few species (1 or 2 each) in the Western Palaearctic. The genus Palaeopsylla is best represented in this part of the Palaearctic (7 species). Some genera of fleas present in the Russian fauna do not include any species with ranges limited by the Western Palaearctic. In particular, the genera Oropsylla and Callopsylla (Ceratophyllidae), Stenoponia (Hystrichopsyllidae), Amphipsylla and Mesopsylla ENTOMOLOGICAL REVIEW Vol. 93 No. 5 2013
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(Leptopsyllidae), and Echidnophaga (Pulicidae) include from 1 to 3 species with broader, WesternCentral ranges. Central Palaearctic ranges are characteristic of 27 species in the fauna of Russia. Such ranges can be observed in 1 or 2 species in each of the 19 genera of 5 families. Five species of the genus Ctenophthalmus have Turanian ranges; within the territory of Russia they occur in the northwestern Caspian region and in Dagestan. Species with Central Palaearctic ranges are also present in such large genera as Ceratophyllus, Nosopsyllus, Callopsylla and Paramonopsyllus of the family Ceratophyllidae; Coptopsylla of the family Coptopsyllidae; Ctenophthalmus, Rhadinopsylla, Paraneopsylla, Neopsylla, Stenoponia and Wagnerina of the family Hystrichopsyllidae; Paradoxopsyllus, Frontopsylla, Leptopsylla, Amphipsylla, Mesopsylla, Ophthalmopsylla and Brachyctenonotus of the family Leptopsyllidae, and also Xenopsylla of the family Pulicidae. The ranges of 78 species of fleas in the Russian fauna cover both the Central and the Eastern Palaearctic and reveal considerable diversity. The fleas Peromyscopsylla ostsibirica and Amphipsylla marikovskii have Eastern-Palaearctic-Nearctic ranges, whereas Amalaraeus dissimilis, a parasite of forest voles, and the flea Amphalius runatus have Central-EasternPalaearctic-Nearctic ranges. The poorly known species Palaeopsylla (P.) incurva, associated with shrews of the genus Sorex, probably has an Eastern-PalaearcticIndo-Malayan range. A broad Eastern-PalaearcticNearctic-Neotropical range is characteristic of the bird parasite Dasypsyllus (Neornipsyllus) stejnegeri. Central-Eastern-Palaearctic ranges are observed in 36 species of 21 genera, and Eastern-Palaearctic ones, in 35 species of 25 genera. None of these genera includes many species with ranges of these types. For example, Eastern-Palaearctic ranges are characteristic of 1 species in each of the following 11 genera: Amalaraeus and Aenigmopsylla (Ceratophyllidae), Palaeopsylla, Eopsylla, Nearctopsylla and Wagnerina (Hystrichopsyllidae), Peromyscopsylla, Ctenophyllus, Pectinoctenus (Leptopsyllidae), Archaeopsylla (Pulicidae), and Dorcadia (Vermipsyllidae). Central-EasternPalaearctic ranges are also known in single representatives of 9 genera: Nosopsyllus, Oropsylla, Mioctenopsylla, Igioffius, Margopsylla (Ceratophyllidae), Paradoxopsyllus, Leptopsylla, Ornithophaga (Leptopsyllidae), and Xenopsylla (Pulicidae).
606
MEDVEDEV
In the fauna of the eastern part of Russia, the genus Rhadinopsylla is represented by 3 species with Central-Eastern ranges and 3 more species with EasternPalaearctic ones. In addition, 4 species of the genus Amphipsylla with Eastern ranges and 4 species of Neopsylla with Central-Eastern-Palaearctic ranges are also distributed there. DISCUSSION Thus, the species composition of fleas in the fauna of Russia, whose territory occupies most of the vast Euro-Siberian Subregion, comprises about 30% of the total Palaearctic fauna. The Russian fauna is characterized by small fractions of endemic species (no more than 4%) and genera (only 1 genus). It includes 255 species belonging to 55 genera, which constitutes 58% of the number of genera in the Palaearctic. These genera belong to 7 out of the 10 Palaearctic families. All the principal centers of taxonomic diversity, including many endemic species and genera, lie in the Eastern Asian, Central Asian, and Turano-Iranian Subregions, i.e., outside the Euro-Siberian Subregion. A considerable part of the Euro-Siberian Subregion was relatively recently affected by the glaciations; the vast territories of northwestern and northeastern European Russia and Siberia are still characterized by severe conditions that limit the faunistic diversity of the flea hosts. The core of the flea fauna of Russia is formed by species and genera of the three largest families: Hystrichopsyllidae, Ceratophyllidae, and Leptopsyllidae. The family Ceratophyllidae holds the first place in the number of genera in the Russian fauna, while the family Hystrichopsyllidae is represented by the greatest number of species. In the former family, the best represented genus is Ceratophyllus which includes 29 species in the Russian fauna. In the family Hystrichopsyllidae, the genus Ctenophthalmus has the broadest distribution and is represented in Russia by 28 species associated with various murid and cricetid rodents, ground squirrels, and insectivores. In the family Leptopsyllidae, the greatest number of species is observed in the genera Amphipsylla (12 species associated with hamsters, mice, and voles) and Leptopsylla (11 species infesting murid rodents). The groups of flea species in the Russian fauna with ranges of the Western and Western-Central types and those with Central-Eastern and Eastern types are approximately equal in size (84 and 78 species, respec-
tively). The species present in the western part of Russia belong to 41 genera of 7 families, while those distributed in the eastern part belong to 42 genera of 6 families (the family Coptopsyllidae being represented by a single species only in the European Province and the Turano-Iranian Subregion). The genera Aenigmopsylla, Amphalius, Igioffius and Margopsylla of the family Ceratophyllidae; Eopsylla and Nearctopsylla of the family Hystrichopsyllidae; Ornithophaga of the family Leptopsyllidae; Xenopsylla of the family Pulicidae, and Dorcadia of the family Vermipsyllidae are not represented in the western part of Russia. On the other hand, species of the genera Doratopsylla, Atyphloceras and Paraneopsylla of the family Hystrichopsyllidae, Mesopsylla of the family Leptopsyllidae, Echidnophaga and Spilopsyllus of the family Pulicidae are absent in the eastern part of Russia. The next stage of our research will be devoted to characterizing the pattern of formation of the flea fauna of Russia, in particular, the role of the European, Caucasian, Central Asian, and Far Eastern centers of taxonomic diversity of fleas in this process. The significance of the Beringian bridge in the exchange of flea species between the Palaearctic and Nearctic will also be estimated. ACKNOWLEDGMENTS This work was based on the collection of the Zoological Institute of the Russian Academy of Sciences (UFK ZIN No. 2-2.20) and financially supported by the Russian Foundation for Basic Research (grant no. 08-04-00216-a). REFERENCES 1. Beaucournu, J.-C., “Catalogue des Siphonapteres de la Grece,” in Fauna Graeciae, 3. Siphonaptera (Soc. Zool. Hellénique, Athenes, 1988), pp. 1–104. 2. Beaucournu, J.-C. and Launay, H., “Les Puces (Siphonaptera),” in Faune de France. Vol. 76 (1990), pp. 1–550. 3. Goncharov, A.I., Romasheva, T.P., Kotti, B.K., et al., A Key to Fleas of the People’s Republic of Mongolia (Ulaanbaatar, 1989) [in Russian]. 4. Hopkins, G.H.E. and Rothschild, M., An Illustrated Catalogue of the Rothschild Collection of Fleas (Siphonaptera) in the British Museum, 1 (University Press, Cambridge, London, 1953). 5. Hopkins, G.H.E. and Rothschild, M., An Illustrated Catalogue of the Rothschild Collection of Fleas (Siphonaptera) in the British Museum, 2 (University Press, Cambridge, London, 1956). ENTOMOLOGICAL REVIEW Vol. 93 No. 5 2013
TAXONOMIC COMPOSITION AND ZOOGEOGRAPHIC CHARACTERISTICS 6. Hopkins, G.H.E. and Rothschild, M., An Illustrated Catalogue of the Rothschild Collection of Fleas (Siphonaptera) in the British Museum, 3 (University Press, Cambridge, London, 1962). 7. Hopkins, G.H.E. and Rothschild, M., An Illustrated Catalogue of the Rothschild Collection of Fleas (Siphonaptera) in the British Museum, 4 (University Press, Cambridge, London, 1966). 8. Hopkins, G.H.E. and Rothschild, M., An Illustrated Catalogue of the Rothschild Collection of Fleas (Siphonaptera) in the British Museum, 5 (University Press, Cambridge, London, 1971). 9. Ioff, I.G., Mikulin, M.A., and Skalon, O.N., A Key to Fleas of Central Asia and Kazakhstan (Meditsina, Moscow, 1965) [in Russian]. 10. Ioff, I.G. and Skalon, O.N., A Key to Fleas of Eastern Siberia, the Far East, and Adjacent Regions (Meditsina, Moscow, 1954) [in Russian]. 11. Lewis, R.E., “The Thoracic Musculature of the Indian Rat Flea, Xenopsylla cheopis (Siphonaptera),” Ann. Entomol. Soc. Am. 54, 387–397 (1961). 12. Lewis, R.E., “Notes on the Geographical Distribution and Host Preferences in the Order Siphonaptera. Pt. 1. Pulicidae,” J. Med. Entomol. 9, 511–520 (1972). 13. Lewis, R.E., “Notes on the Geographical Distribution and Host Preferences in the Order Siphonaptera. Pt. 2. Rhopalopsyllidae, Malacopsyllidae and Vermipsyllidae,” J. Med. Entomol. 10, 255–260 (1973). 14. Lewis, R.E., “Notes on the Geographical Distribution and Host Preferences in the Order Siphonaptera. Pt. 3. Hystrichopsyllidae,” J. Med. Entomol. 11, 147–167 (1974a). 15. Lewis, R.E., “Notes on the Geographical Distribution and Host Preferences in the Order Siphonaptera. Pt. 4. Coptopsyllidae, Pygiopsyllidae, Stephanocircidae and Xiphiopsyllidae,” J. Med. Entomol. 11, 403–413 (1974b). 16. Lewis, R.E., “Notes on the Geographical Distribution and Host Preferences in the Order Siphonaptera. Pt. 5. Ancistropsyllidae, Chimaeropsyllidae, Ischnopsyllidae, Leptopsyllidae and Macropsyllidae,” J. Med. Entomol. 11, 525–540 (1974c). 17. Lewis, R.E., “Notes on the Geographical Distribution and Host Preferences in the Order Siphonaptera. Pt. 6. Ceratophyllidae,” J. Med. Entomol. 11, 658–676 (1975). 18. Lewis, R.E., “Notes on the Geographical Distribution and Host Preferences in the Order Siphonaptera. Pt. 8. New Taxa Described between 1984 and 1990, with a Current Classification of the Order,” J. Med. Entomol. 30, 239–256 (1993).
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19. Lewis, R.E. and Lewis, J.H., “Notes on the Geographical Distribution and Host Preferences in the Order Siphonaptera. Pt. 7. New Taxa Described between 1972 and 1983, with a Supraspecific Classification of the Order,” J. Med. Entomol. 22, 134–152 (1985). 20. Liu Zhiying et al., “Siphonaptera (Insecta),” in Fauna Sinica (Science Press, Beijing, 1986), pp. 1–1334. 21. Medvedev, S.G., “Geographical Distribution of Families of Fleas (Siphonaptera),” Entomol. Obozr. 75 (4), 815–833 (1996) [Entomol. Rev. 76 (8), 978–992 (1996)]. 22. Medvedev, S.G., “Host-Parasite Relations in Fleas (Siphonaptera). I,” Entomol. Obozr. 76 (2), 318–336 (1997a) [Entomol. Rev. 77 (2), 200–215 (1997)]. 23. Medvedev, S.G., “Host-Parasite Relations of Fleas (Siphonaptera): II,” Entomol. Obozr. 76 (4), 765–769 (1997b) [Entomol. Rev. 77 (4), 511–521 (1997)]. 24. Medvedev, S.G., “Fauna and Host-Parasite Relations of Fleas (Siphonaptera) in the Palaearctic,” Entomol. Obozr. 77 (2), 295–314 (1998a) [Entomol. Rev. 78 (3), 292–308 (1998)]. 25. Medvedev, S.G., “Classification of Fleas (Order Siphonaptera) and Its Theoretical Foundations,” Entomol. Obozr. 77 (4), 916–934 (1998b) [Entomol. Rev. 78 (9), 1080–1093 (1998)]. 26. Medvedev, S.G., “Classification of the Flea Families (Siphonaptera): I. Family Hystrichopsyllidae (Part 5),” Entomol. Obozr. 88 (3), 693–711 (2009b) [Entomol. Rev. 90 (2), 203–217 (2009)]. 27. Medvedev, S.G. and Kotti, B.K., “Patterns of Formation of the Flea (Siphonaptera) Fauna in the Caucasus,” Parazitologiya 45 (6), 470–487 (2011) [Entomol. Rev. 92 (4), 409–421 (2012)]. 28. Medvedev, S.G. and Kotti, B.K., “Host Associations and Origin in the Formation of the Caucasian Fauna of Fleas (Siphonaptera),” Entomol. Obozr. 91 (4), 714–734 (2012) [Entomol. Rev. 93 (3), 293–308 (2013)]. 29. Skalon, O.N., “Order Siphonaptera (Aphaniptera, Suctoria), or Fleas,” in Keys to Insects of the European Part of the USSR. Vol. 5, Issue 2 (Nauka, Leningrad, 1970), pp. 841–844 [in Russian]. 30. Tiflov, V.E., Skalon, O.N., and Rostigaev, B.A., A Key to Fleas of the Caucasus (Stavropol. Knizhnoe Izdat., Stavropol, 1977) [in Russian]. 31. Traub, R.E., Rothschild, M., and Haddow, J.F., The Ceratophyllidae: Key to the Genera and Host Relationships, with Notes on Their Evolution, Zoogeography and Medical Importance (Univ. Press, Cambridge, 1983).
