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Culicoides biting midges (Diptera, Ceratopogonidae) in various climatic zones of Russia and adjacent lands A.V. Sprygin1*, O.A. Fiodorova2, Yu.Yu Babin1, N.P. Elatkin1, B. Mathieu3, M.E. England4, and A.V. Kononov1 Federal Center for Animal Health, Vladimir, Russia, [email protected] Russian Research Institute for Veterinary Entomology and Arachnology Rosselhozakademii, Tyumen, Russia 3 Institut de Parasitologie et de Pathologie Tropicale Faculté de Médecine de Strasbourg, Strasbourg, France 4 Vector-borne Viral Diseases Programme, The Pirbright Institute, Ash Road, Woking, Surrey, United Kingdom 1

2

Received 1 April 2014; Accepted 3 June 2014 ABSTRACT: Culicoides biting midges play an important role in the epidemiology of many vector-borne infections, including bluetongue virus, an internationally important virus of ruminants. The territory of the Russian Federation includes regions with diverse climatic conditions and a wide range of habitats suitable for Culicoides. This review summarizes available data on Culicoides studied in the Russian Federation covering geographically different regions, as well as findings from adjacent countries. Previous literature on species composition, ranges of dominant species, breeding sites, and host preferences is reviewed and suggestions made for future studies to elucidate vector-virus relationships. Journal of Vector Ecology 39 (2): 306315. 2014. Keyword Index: Culicoides, Russia, arbovirus, biodiversity, Ceratopogonidae.

INTRODUCTION Biting midges of the genus Culicoides (Diptera, Ceratopogonidae), are small blood-sucking insects found in nearly every part of the world. These insects are 1 to 3 mm long and most species are identified by workers using wing pigmentation patterns. The recent circulation of bluetongue virus (BTV) and Schmallenberg virus (SBV) in Europe have highlighted the role of Culicoides midges as biological vectors within this region (Carpenter et al. 2009). Since there is no barrier for flying insects to cross borders with adjacent countries, it is of high importance to have a complete understanding of which Culicoides species could potentially expand the range of an associated pathogen into adjacent lands. It has been shown that Russia supports a diverse range of Culicoides species, but the results of most studies conducted have been in the Russian language and are often inaccessible for international readership due to linguistic barriers. Therefore, in this review we examine available Russian literature on biological and ecological characteristics of Culicoides species with particular reference to potential arboviral vectors. In contrast to the paper by Glukhova (2005) that provides keys for morphological identification, this review examines ecological characteristics of Culicoides of interest. Morphological classifications of Culicoides species and synonymy status have varied throughout the years and so here we attempt to update findings according to the current species names referenced in the world catalogue (Borkent 2014). The dominance of single species in the ecosystems of Russia and neighboring countries, as described in this review, varies not only among regions but also across smaller zones with similar habitats within the study region. This is likely to be related to

the variation in climate conditions, landscape, and the biotic community within a region. It appears that hydrological and hydrochemical conditions of breeding sites play an important role in the peak time of abundance from year to year, as well as influencing within-season activity fluctuations. Therefore, this review is designed to proceed from region to region providing a basic concept of the species biodiversity and abundance recorded in the relevant literature. In some of the literature reviewed, the species Culicoides schultzei Enderlein is sometimes referred to as “affiliated” (“C. aff. schultzei”), a term previously used by Glukhova (2005). C. schultzei is now considered to be a group of several cryptic species (Cornet and Brunhes 1994) and Boorman (1989) suggested that most records from the North Sahara referred to Culicoides oxystoma Kieffer. Recently, Morag et al. (2012) used a phylogenetic approach to study this species complex in Israel and showed the presence of C.oxystoma and other species of the Schultzei group. The species Culicoides okumensis Arnaud described from Okinawa in 1956 has since become a synonym of Culicoides actoni Smith by Kitaoka (1977). In a later article, Kitaoka (1985) suggested that the records from Gutsevich (1975) of C. okumensis in the Soviet Union were actually Culicoides dobyi Callot and Kremer. However, for the purpose of this review it is important to refer to Gutsevich (1975), who distinguished specimens using the morphology of hairs on eyes. From these studies, it is probable that records of C. okumensis refer to C. actoni and those of C. dobyi refer to Culicoides chiopterus Meigen. Culicoides biting midges in Russia Studies carried out by one of the most prolific entomologists in Russia, Valentina Glukhova, indicate that there are over 80 species found in Russia (Glukhova 1989)

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with 38 species in Siberia and the Far East (Mirzaeva 1989). In the 1960s, Culicoides were studied by Ostroushko in the wooded tundra and taiga zone of the Komi Republic using direct collections from animals and humans. A total of 19 Culicoides species were identified throughout the Republic: Сulicoides pulicaris Linnaeus, Сulicoides grisescens Edwards, Сulicoides fagineus Edwards, Culicoides impunctatus Goetghebuer, Сulicoides obsoletus Meigen, С. chiopterus, Culicoides stigma Meigen, Culicoides helveticus Callot, Kremer and Deduit, Culicoides fascipennis Staeger, Culicoides subfascipennis Kieffer, Culicoides pallidicornis Kieffer, Culicoides kibunensis Tokunaga, Culicoides cunctans Winnertz, Culicoides sphagnumensis Williams, Culicoides circumscriptus Kieffer, Culicoides salinarius Kieffer, Culicoides manchuriensis Tokunaga, Culicoides simulator Edwards, and Culicoides festivipennis Kieffer (Ostrouschko 1969). The most abundant species were members of the Pulicaris group (in particular С. pulicaris s.s.), С. grisescens and members of the subgenera Avaritia and Silvaticulicoides (Ostrouschko 1969). In the late 1960s and 1970s, Ostroushko also recorded that in the taiga zone, Culicoides flight activity starts in early June and continues until the first snow (the beginning or end of October) with two generational peaks. The first activity peak in late June involves С. obsoletus, С. chiopterus, С. stigma, and С. fascipennis. The second peak is quantitatively much larger and predominantly consists of C. pulicaris. In autumn, С. pulicaris and С. grisescens are dominant in collections, with sporadic occurrences of Obsoletus group species. In contrast to the taiga zone, Ostroushko (1980) found that in wooded tundra the first peak activity of Culicoides was in late July. Moreover, in wooded tundra, Culicoides were only active during daylight hours with no flight activity recorded during the night. The author also discovered that Culicoides are capable of being active during high light intensities, in contrast with the findings by Glukhova (1956) in Karelia and Amosova (1956) in Primorskii Krai. This could be a specific adaptation to northern conditions characterized by short summers and extended daylight. The authors conclude that in wooded tundra, Culicoides exhibit a wider ecological flexibility compared to that found in the taiga zone. The larval habitats of Culicoides are also investigated in wooded tundra and found in various water pools and swampy areas (Ostroushko 1969). С. pulicaris is the dominant species in the Komi region with wide ecological flexibility (about 90% in wooded tundra and up to 67% in the taiga zone). The next most abundant species in wooded tundra are С. fascipennis and С. chiopterus, comprising 1.5% and 1.8% of collections, respectively (Ostroushko 1980). It is likely that С. obsoletus and С. grisescens are typical of forest areas (dominated by coniferous trees), which is consistent with findings by other entomologists (Glukhova 1956, Gutsevitch 1973). In the southern European part of Russia, in Voronezh Oblast, entomological studies were performed from 1954 to 1963, where a total of 20 Culicoides species were identified. Dominant species were С. pulicaris, С. obsoletus, С. simulator, С. fascipennis, С. pallidicornis, and С. subfascipennis. Сulicoides nubeculosus Meigen, Сulicoides riethi Kieffer, Culicoides pictipennis Staeger, С. festivipennis, Сulicoides tentorius

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Austen, and Сulicoides vexans Staeger were also recorded but in fewer numbers. In contrast, Сulicoides stigma Meigen, С. circumscriptus, С. salinarius, С. impunctatus, С. grisescens, С. chiopterus, С. kibunensis, and Сulicoides truncorum Edwards were trapped only rarely or in low numbers. The species, С. fascipennis, С. subfascipennis, and С. vexans were found to exhibit morphological variation in some body parts. Since the species С. riethi, С. stigma, С. circumscriptus, С. pulicaris, С. grisescens, С. obsoletus, С. pictipennis, С. simulator, С. fascipennis, С. pallidicornis, С. subfascipennis, and С. vexans found in Voronezh Oblast had been previously identified further north and south of this region, Degtyareva K.T (1964) suggested these species were common for Voronezh Oblast. The species С. circumscriptus, С. salinarius, С. kibunensis, and С. truncorum were shown to be rare and uncommon. Using a landing catch technique, it was shown that 17 out of the 20 Culicoides species had trophic preferences for humans and animals. The three remaining species that did not attack humans or animals were С. salinarius, C. festivipennis,­­ and С. truncorum (Degtyareva 1964). Isaev (2013) reported 26 Culicoides species found in Ivanovo Oblast. His findings indicate that the midge composition in Ivanovo Oblast is very similar to that described for mixed forests by Gutsevich (1973). The activity season in Voronezh Oblast tended to start in mid-May, continuing through until mid-October, with С. pulicaris, С. obsoletus, С. simulator, С. fascipennis, С. pallidicornis, and С. subfascipennis predominant in collections (Degtyareva 1964). A more extensive entomological study incorporating research work by multiple authors was carried out in Leningradskaya Oblast (Schtakelberg 1951) and Pskovskaya Oblast (Brodskaya 2002). A total of 113 midge species were identified, belonging to 17 genera. Within the genus Culicoides, Сulicoides punctatus Meigen, С. obsoletus, С. grisescens, and С. fascipennis were the most abundant species. С. impunctatus and С. pallidicornis were shown to be abundant in some areas. С. obsoletus and С. chiopterus were also widely distributed and were associated with forest land (Gutsevitch 1952). In Pskovskaya Oblast, 15 Culicoides species were identified; C. obsoletus, С. pallidicornis, C. punctatus, C. grisescens, C. chiopterus, C. impunctatus, C. fascipennis, C. pulicaris, C. nubeculosus, C. riethi, C. stigma, Culicoides scoticus Downes and Kettle, C. salinarius, C. festivipennis, and Culicoides segnis Campbell and Pelham-Clinton. The first eight of these species were trapped on a cow by sweep netting. The authors showed that the fauna was dominated by four species, С. obsoletus, С. pallidicornis, С. punctatus, and С. grisescens. These species accounted for up to 97.9 to 100% of the total catch, with the other species being very low in numbers. It is likely that this was due to trophic preferences of the four most abundant species since they were trapped on a cow (Brodskaya 1992). The findings of Brodskaya (1992) on the seasonal abundance of Culicoides in the Pskovstaya Oblast were consistent with other scientists, showing that Culicoides abundance peaks twice in mixed forest areas with flight activity from May to October (Remm 1955, Krivosheina 1956, Trukhan 1975). In a similar study in collections from

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humans in Leningradkaya Oblast (Brodskaya 2002), a total of six species were identified and found to be common in this territory. These species were C. fascipennis, C. impunctatus, C. helveticus, C. obsoletus, C. punctatus, and Culicoides reconditus Campbell and Pelham-Clinton. The species, C. punctatus, had previously been reported in Leningradstaya Oblast and in southern Finland (Delecolle et al. 1983), but there were no reportings of this species from Estonia (Brodskaya 2002). In Karelia, a northwestern area of Russia, 17 Culicoides species were found: С. obsoletus, С. chiopterus, С. grisescens, C. pulicaris, C. impunctatus, C. fagineus, C. fascipennis, C. subfascipennis, C. pallidicornis, Culicoides albicans Winnertz, Culicoides cunctans Winnertz, C. stigma, C. circumscriptus, C. salinarius, C. sphagnumensis, C. festivipennis, and C. pictipennis (Glukhova 1956, 1962, 1989). In the southern and central part of Karelia, the activity season begins in late May and continues until early October. During this time, there are two peaks; the first in early July and the second from late July until early September. The first part of the summer is dominated by C. impunctatus and С . obsoletus. In contrast, С . grisescens becomes the dominant species during the second half of the summer (Glukhova 1989). In the northern areas of Russia, Culicoides display a different flight activity pattern. In Khibiny (located on the Kolskiy Peninsula), the activity season is shorter and emergence of Culicoides is delayed in comparison with Central Russia (Fridolin 1936). In this study, the first Culicoides were trapped in mid-July, with a single peak in August. In contrast, in the south of Karelia, Estonia, (Remm 1955, 1956) and in Moscow and Ivanovo oblasts (Molev, 1955), the flying season is extended and Culicoides are active from mid-May until October with variation in abundance during this time. In Karelia, Culicoides have one generation per season, with the exception of С. pulicaris and С. stigma that have two generations. In Moscow, Ivanovo and Ryazan oblasts most species have two generations per season, with C. pulicaris having at least three (Krivosheina 1956, 1957, Molev 1955). In Moscow and Ivanovo oblasts, С. pulicaris and С. fascipennis are abundant both in backwoods and urbanized areas, whereas C. grisescens is mainly associated with backwoods (Molev 1955). In Permskiy Kray, Mitrophanova and Burylova (1967) identified 25 Culicoides species and one Lasiohelea species; C. оbsoletus, C. okumensis, C. scoticus, C. pulicaris, C. grisescens, C. pallidicornis, C. subfascipennis, C. fascipennis, C. kibunensis, C. stigma, C. helveticus, Culicoides parroti Kieffer, C. vexans, C. cunctans, Culicoides heliophilus Edwards, C. nubeculosus, C. circumscriptus, C. salinarius, C. pictipennis, C. festivipennis, C. simulator, Culicoides ibericus Dzhafarov, and Forcipomyia (Lasiohelea) sibirica Bujanova. The most abundant species in the region was C. оbsoletus followed by C. pallidicornis. The numerous water reservoirs and wet ground litter in the Cis-Ural region are favorable breeding sites leading to a very common occurrence of Culicoides. Flight activity lasts from May until October with two peaks in mid-June and midAugust. The Culicoides fauna in Krasnoyarskiy Kray comprises

December 2014

14 species: Culicoides sinanoensis Tokunaga, Culicoides sanguisuga Coquillett, Culicoides filicinus Gornostaeva and Gachegova, C. chiopterus, C. pulicaris, C. fagineus, C. grisescens, C. festivipennis, C. subfascipennis, C. riethi, C. stigma, and C. helveticus (Gornostaeva 1978). A total of 17 species of Culicoides have been identified in the south of Tyumenskaya Oblast; C. оbsoletus, C. chiopterus, Culicoides gornostaevae Mirzaeva, C. pulicaris, C. punctatus, C. impunctatus, C. grisescens, C. reconditus, C. fascipennis, C. subfascipennis, C. pallidicornis, C. circumscriptus, C. salinarius, C. manchuriensis, C. nubeculosus, C. stigma, and C. helveticus, with C. punctatus being the most abundant (Savchuk 2004). In the south of Tomskaya Oblast, a total of 34 species were identified with C. grisescens, C. pulicaris, C. оbsoletus, and C. chiopterus dominating the catches. In the forest-steppe zone of Novosibirskaya Oblast, a total of 17 species were recorded; C. оbsoletus, C. chiopterus, C. pulicaris, C. punctatus, C. grisescens, C. reconditus, C. fascipennis, C. pallidicornis, Culicoides stepicola Remm, C. vexans, Culicoides variifrons Glukhova and Ivanov, C. circumscriptus, C. salinarius, C. sphagnumensis, C. manchuriensis, C. nubeculosus, and C. riethi (Mirzaeva 1963, 1969, 1989). In this region, C. riethi, C. circumscriptus, and C. salinarius were demonstrated to be the most abundant species. Western Siberia is rich in riverine habitat, which provides favorable larval habitats for some Culicoides species (Mirzaeva 1969). A study conducted by Mirzaeva in 1969 recorded 11 species from the northern forest tundra; C. obsoletus, C. pulicaris, C. impunctatus, C. fascipennis, Culicoides sensillatus Mirzaeva, C. circumscriptus, C. salinarius, C. manchuriensis, Culicoides sibiricus Mirzaeva, C. riethi, and C. helveticus. C. circumscriptus, C. riethi, and C. salinarius were found to be the dominant species (Mirzaeva 1969). Studies conducted between 1966 and 1969 in Magadanskaya Oblast found seven species of Culicoides; C. stigma, C. helveticus, C. pulicaris, C. grisescens, C. obsoletus, C. okumensis, and C. fascipennis, with C. pulicaris dominating (Mirzaeva et al. 1973). The dominance of C. pulicaris is typical for areas with severe climate (permafrost) characterized by a very short summer and long, cold winters (Mezenev 1968, Mirzaeva, 1969). In these areas, the flight season starts in early July and lasts for two or three months, with the total number of insects caught not exceeding 340 individuals per trap catch. In the Taymyr peninsula, Culicoides are rare and do not play a significant role as blood-sucking insects (Mezenev 1968). They have not been found in alpine tundra and mountain taiga but have been found sporadically in forest tundra under warm weather conditions (Mezenev 1968). In the Sakha Republic, a total of 11 Culicoides species were recorded (Kudryavtseva 1960, Yakuba 1963, Potapov et al. 1967). C. pulicaris and C. fascipennis were found to be the most abundant, with C. grisescens, C. obsoletus, C. okumensis, C. stigma, C. helveticus, C. simulator, C. subfascipennis, C. circumscriptus, and C. manchuriensis collected in fewer numbers. The flight activity started in mid-July and peaked in August. In 1967, blood-sucking midges were studied in Chukotka, where six Culicoides species were collected (Mirzaeva 1969).

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C. pulicaris was the dominant species and the five others (C. grisescens, C. obsoletus, C. fascipennis, C. okumensis, and C. stigma) were found in lower numbers (Mirzaeva 1969). In Western Siberia, Mirzaeva (1987) recorded C. obsoletus, C. gornostaevae, C. sinanoensis, and C. chiopterus. In the Far East and Altai, C. okumensis (=C. actoni) was also trapped. Interestingly, it was abundant in those areas alongside C. grisescens and C. obsoletus. Systematic observations in Dagestan were conducted from 1966 to 1968 using human and horse-landing catch techniques. Culicoides dominated the population of bloodsucking insects in the areas studied (Gutsevich 1937, 1939, Glukhova 1956). A total of ten Culicoides species were found: C. nubeculosus, Culicoides puncticollis Becker, C. riethi, C. parroti, C. circumscriptus, C. pulicaris, C. obsoletus, Culicoides maritimus Kieffer, C. simulator, Сulicoides trivittatus Vimmer, and additionally, a species from the genus Leptoconops (Leptoconops (Holoconops) mediterraneus Kieffer). This was the first recording of С. maritimus, С. simulator, С. trivittatus, and L. (Н) mediterraneus from the Northern Caucasus. Earlier studies carried out in Dagestan in 1967 (Volik 1967), found only four Culicoides species; C. puncticollis, С. pictipennis, C. subfascipennis, and C. punctatus (with the latter referred to as a subspecies of C. pulicaris by the author). Ismailov (1969) showed that the optimum temperature for flight activity was 9 to 11° C, which is higher than the optimum temperature for flight activity in the north. Due to the early onset of spring, Culicoides emerge in April and are then active until October with a peak in May. However, the highest abundance rates are recorded from April to late May, followed by a decrease in catch abundance in July and August down to four to ten midges per 20 min of humanlanding catch time. The author suggests the observed decline in abundance is due to the drying up of water reservoirs that serve as breeding sites. The hot weather also affects the faunal composition of Culicoides across seasons. In May, a total of five species of Culicoides are abundant (С. nubeculosus, С. riethi, С. pulicaris, С. maritimus, С. simulator, L. (H) laurae), whereas in July only С. pulicaris is found in Dagestan. (Ismailov 1969). In a study carried out in Dagestan by Razachanova (2002), 21 species belonging to the genera Culicoides and Leptoconops were detected. A total of six species were recorded in this region for the first time; C. fascipennis, C. tentorius, C. heliophilus, C. vexans, C. festivipennis, and Culicoides longipennis Khalaf. Breeding sites for all documented species included rivers, irrigation canals, saturated soil, and bogs. Most of the Culicoides species were active in the morning and in the evening, whereas Leptoconops species exhibited hostseeking activity during daylight hours. Two seasonal peaks were observed, with the first in May and the second in July and August. There was variation observed in the daily activity of biting midges in different landscape types. In steppe areas, biting midges were active after 13:00 and a low number of adults was observed at sunrise. During the first emergence in May, there were two peaks in daily activity, at sunrise and at sunset. In the summer, activity decreased due to the desiccation of water bodies. In woodland areas, biting midges

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also exhibited two peaks of daily activity. A few species such as Culicoides shaklawensis Khalaf and C. obsoletus were active throughout the day. In autumn, the levels of activity occurring at sunrise decreased. In woodland areas, biting midges showed two peaks of seasonal activity with the first peak in April and May. C. nubeculosus, C. pulicaris, C. riethi, and C. simulator were dominant during that time. The second activity peak was observed in July and then decreased throughout August. In autumn, C. nubeculosus, C. circumscriptus, and C. maritimus were found to be abundant. In the steppe zone, seasonal activity was found to be similar to that of woodland areas (Razahanova 2000). Overall, the Culicoides species recorded in Russia based on the literature reviewed here have been collated and are listed in Table 1. Gutsevitch (1952) focused on the diversity of Culicoides midges in forest areas across the Russian Federation including Primorskii Kray, Khabarovskii Kray, Chita Oblast, Chuvashia Republic and Leningradskaya Oblast. The 23 species found in forest zones by various authors using different trapping techniques are gathered and reviewed by Gutsevitch (1952) and are here summarized in Table 2. For a representation of the geographic locations of regions where midges were studied, see Figure 1. Culicoides biting midges in adjacent territories. An investigation into blood-sucking midges of Ukraine was carried out in 25 regions that included various geographic and climatic zones, including Western Ukraine and Crimea (Schevchenko 1977). It was observed that there was great variation in morphological traits within species across Ukraine, especially in relation to wing pattern, wing length, and antennae characteristics (Schevchenko 1977). Culicoides were captured using various methods, including mouth aspiration directly from the host, catching swarms (sweep netting of host), and by taking larval samples and rearing them under laboratory conditions. The combined results demonstrated the presence of biting midges belonging to three genera: Culicoides, Leptoconops Skuse, and Forcipomyia (Lasiohelea) Kieffer. The genera Leptoconops and Forcipomyia (Lasiohelea) were detected occasionally in the left-bank Ukraine and were of low importance due to low numbers. The genus Culicoides is widespread in Ukraine and includes 58 species (Schevchenko 1977). The species composition in any territory largely depends on the landscape and climatic conditions (Schevchenko 1977). In the broad-leaved forest zone of Ukraine, a total of 37 species were detected with 29 Culicoides species and one Leptoconops species found in Polesia (Leptoconops borealis Gutsevich). С. punctatus, С. fascipennis, and С. pallidicornis were found to be the most abundant species in Polesia and in the left-bank Ukraine. In the latter area, C. simulator was another dominant species (Schevchenko 1977). In the forest zone of the Carpathian Mountains, 28 Culicoides species were recorded. In Trans-Carpathian Ukraine, the following species were found to be most abundant; С. fascipennis, С. obsoletus, Сulicoides achrayi Kettle and Lawson and С. festivipennis. In the Cis-Carpathian part of Ukraine, C. obsoletus, С. pallidicornis, and С. achrayi

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Table 1. Culicoides of Russia.

Leningradskaya Oblast

Karelia

Permskiy Kray

Krasnoyar-skiy Kray

Tyumenskay Oblast

Tomskay Oblast

Novosibir-skay Oblast

Magadan-skaya Oblast

Republic Sakha

Chucotka

Dagestan

1 2 Genus Culicoides Latreille Subgenus Avaritia Fox 1 C. (A.) actoni Smith (= C. okumensis) 2 C. (A.) chiopterus Meigen 3 C. (A.) dewulfi Goetghebuer 4 C. (A.) filicinus Gornostaeva & Gachegor 5 C. (A.) montanus Shakirzjanova 6 C. (A.) obsoletus Meigen 7 C. (A.) sanguisuga Coguillett 8 C. (A.) scoticus Downes & Kettle 9 C. (A.) sinanoensis Tokunaga 10 C. (A.)gornostaevae Mirzaeva 11 C. sp. aff. obsoletus Subgenus Beltranmyia Vargas  12 C. (B.) circumscriptus Kieffer 13 C. (B.) manchuriensis Tokunaga 14 C. (B.) salinarius Kieffer 15 C. (B.) sibiricus Mirzaeva 16 C. (B.) sphagnumensis Williams Subgenus Culicoides Latreille 17 C. (C.) fagineus Edwards 18 C. (C.) flavus Gornostaeva 19 C. (C.) grisescens Edwards 20 C. (C.) impunctatus Goetghebuer 21 C. (C.) pulicaris Linnaeus 22 C. (C.) punctatus Meigen Subgenus Monoculicoides Khalaf 23 C. (M.) helveticus Callot, Kremer & Deduit 24 C. (M.) nubeculosus Meigen 25 C. (M.) parroti Kieffer 26 C. (M.) puncticollis Becker 27 C. (M.) riethi Kieffer 28 C. (M.) stigma Meigen Subgenus Pontoculicoides Remm 29 C. (P.) ibericus Dzhafarov Subgenus Silvaticulicoides Glukhova 30 C. (S.) achrayi Kettle & Lawson (= C. tentorius) 31 C. (S.) fascipennis Staeger 32 C. (S.) pallidicornis Kieffer 33 C. (S.) subfascipennis Kieffer Subgenus Wirthomyia Vargas 34 C. (W.) reconditus Campbell & Pelham-Clinton 35 C. (W.) segnis Campbell & Peiham-Clinton Unplaced species 36 C. albicans Winnertz 37 C. festivipennis Kieffer 38 C. heliophilus Edwards 39 C. kibunensis Tokunaga (=C. cubitalis) 40 C. maritimus Kieffer 41 C. pictipennis Staeger 42 C. poperinghensis Goetghebuer 43 C. sensilatus Mirzaeva 44 C. simulator Edwards 45 C. stepicola Remm 46 C. trivittatus Vimmer 47 C. truncorum Edwards 48 C. ustinovi Shevchenko 49 C. variifrons Glukhova & Ivanov 50 C. vexans Staeger

Pskov Oblast

Species

Voronesh Oblast

№

Komi Republic

Trapping site

3

4

5

6

7

8

9

10

11

12

12

14

15

16

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Journal of Vector Ecology

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Table 2. The diversity of Culicoides midges identified in forest zones of Russia (Gutsevitch 1952). Species C. riethi

Trapping sites Lake Baskunchak, Astrakhanskaya Oblast

С. nubeculosus С. pulicaris С obsoletus С. pictipennis С. fascipennis С. stigma

Novgorodskaya Oblast,

С. pulicaris

Ussuriyskaya Oblast and (now part of Primirskiy Kray) Evreyskaya avt. Oblast

С. nubeculosus С. pulicaris С. impunctatus C. fascipennis С. arboreus

Chitinskaya Oblast

С. circumscriptus С. pulicaris С. obsoletus С. oxystoma С. arakawai С. impunctatus

Primirskiy Kray

С. nubeculosus С. pulicaris С. obsoletus С. oxystoma С. chiopterus

Khabarovskiy Kray

С. pulicaris С. obsoletus С. oxystoma С. arakawai С. arboreus

Ussuriyskaya Oblast

С. nubeculosus С. circumscriptus С. pulicaris С. pictipennis С. festivipennis С. arboreus С. obsoletus С. obsoletus С. pulicaris С. arboreus

Resp. Chuvashiya

South Sakhalin

С. pulicaris

Ussuriyskaya Oblast (renamed as Zabaykalskiy kray)

С. grisescens

Arkhangelskaya Oblast

were most abundant with occasional dominance by C. fascipennis, C. subfascipennis С. pallidicornis, Culicoides minutissimus Zetterstedt, and C. pulicaris in adjacent districts. (Schevchenko 1977) In the forest-steppe zone of Ukraine, a total of 30 Culicoides, one Leptoconops species (L. borealis), and one Forcipomyia species (F. (L.) sibirica) were documented. This

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region, like others, also showed variation in species diversity and abundance depending on the ecological characteristics of breeding sites and districts. Here, C. simulator, C. subfascipennis, and С. pallidicornis were most abundant with occasional occurrences of Culicoides machardyi Campbell and Pelham-Clinton and C. punctatus (Schevchenko 1977). The steppe zone of Ukraine was shown to have 45 Culicoides species and two Leptoconops species (Leptoconops (Holoconops) popovi Dzhafarov and Leptoconops (Holoconops) pavlowskyi Dzhafarov). The dominant Culicoides species were Culicoides ustinovi Schevschenko, C. vexans, C. simulator, C. machardyi, C. maritimus, Culicoides duddingstoni Kettle and Lawson, Culicoides maritimus var. paucisensillatus Callot, Kremer and Rioux, C. nubeculosus, and C. riethi (Schevchenko 1977). Zhdanova (1982) studied the biting midges of the Polesia region. In this study, larvae collected from breeding sites such as pools, streams, vernal-autumnal ponds and saturated soil were reared. The following species were then documented by adult emergence; С. pulicaris, С. punctatus, С. fascipennis, С. achrayi, С. subfascipennis, С. pallidicornis, С. festivipennis, С. kibunensis, С. vexans, С. reconditus, С. salinarius, С. circumscriptus, С. manchuriensis, С. nubeculosus, С. riethi and С. stigma. Among them, four species were described to be the most abundant; С. nubeculosus, С. salinarius, С. manchuriensis and С. fascipennis. Interestingly, Culicoides midges were shown to overwinter in the larvae stage except for С. grisescens, С. festivipennis and С. obsoletus that overwintered in the egg stage (Glukhova 1956, Dzhafarov 1964, Shevchenko 1971). Dubrovskaya (1970) studied biting midges in the steppe zone of Ukraine and found the presence of the following species; С. nubeculosus, С. riethi, С. puncticollis, С. salinarius, С. circumscriptus, С. manchuriensis, Сulicoides homochrous Remm, С. fascipennis, С. subfascipennis, С. ustinovi, С. maritimus, С. simulator, Сulicoides alazanicus Dzhafarov, С. festivipennis, С. vexans, С. albicans, С. reconditus, and С. punctatus. The author showed that rivers, water patches at the bottom of valleys, and coastal areas of the Sea of Azov acted as breeding sites. In the same study, 30 Culicoides and one Leptoconops species (Leptoconops bidentatus Gutsevich) were recorded in Crimea. Among these, С. riethi, С. machardyi, С. obsoletus, Culicoides similis Carter, Ingram and Macfie, and С. maritimus were found to be the dominant species in various landscape zones. In Kazakhstan, the fauna of biting midges was studied from 1965 to 1992 in the Semipalatinsk region and eastern Kazakhstan (Isimbekov 1994). The studies were carried out in settlements, on poultry farms, cattle farms, and grazing sites located in various climatic zones. A total of 33 Culicoides species were detected in the eastern part of Kazakhstan (Isimbekov 1994). The Irtysh River basin had the most diverse species composition in comparison with other regions of Kazakhstan. Hematophagous insects were abundant in the bottom valleys of the Irtysh River tributaries where 23 biting midge species were detected. These included widespread species such as С. reconditus, С. fascipennis, and С. vexans (Isimbekov 1994). The lowest number of species was detected

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Journal of Vector Ecology

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Figure 1. Map of Russian Federation showing the locations of regions where midges were studied in the past. in the desert grazing areas of the Prialakolye and Zaysan. In a study carried out in Turkmenistan, 19 Culicoides species (C. puncticollis, C. parroti, C. circumscriptus, C.ulicoides desertorum Gutsevich, C. pulicaris, Culicoides montanus Shakirzjanova, C. maritimus, Culicoides cataneii Clastrier, C. aff. schultzei, C. similis, C. subfascipennis, C. kibunensis, Culicoides saevus Kieffer, Culicoides odiatus Austin, Culicoides azerbajdzhanicus Dzhafarov, Culicoides firuzae Dzhafarov, Culicodies turanicus Gutsevich and Smatov, and two further Culicoides species that could not be identified to species level) and one Leptoconops species (L. (H.) mediterraneus) were recorded (Muradov 1966). This study was conducted in the area surrounding Ashkhabad and in the foothills of the Kopet Dagh mountains. C. puncticollis, C. circumscriptus, and C. aff. schultzei were found to be the dominant species. Two peaks of Culicoides seasonal activity were observed; the first in May and the second during August and September. In the periods from March to June and from October to November, C. puncticollis was found to be the most abundant species, whereas in August, C. aff. schultzei was the most abundant. Two peaks of activity were also observed in the Kopet Dagh mountains: the first in May and the second in September. Culicoides exhibited two peaks of daily activity. From May to September, host-seeking activity of the most abundant species (C. aff. schultzei and C.  puncticollis) was recorded between 06:00 and 11:00, with a peak between 07:00 and 08:00, and also between 16:00 and 20:00, with a peak between 19:00 and 20:00. During October and November, host-seeking activity started between 08:00 and decreased by 12:00. Evening activity was observed at approximately 14:00

and 17:00 (Muradov 1966). The Culicoides fauna of Belarus included 19 species; C. punctatus, C. pulicaris, C. impunctatus, C. grisescens, C. fascipennis, C. subfascipennis, C. pallidicornis, C. obsoletus, C. chiopterus, C. nubeculosus, C. stigma, C. circumscriptus, C. salinarius, Culicoides festivipennis Austin, C. simulator, C. ustinovi, C. kibunensis, C. cunctans, and C. albicans (Trukhan 1975). Among these, the most abundant species were C. punctatus, C. fascipennis, C. pallidicornis and C. impunctatus. The breeding sites described in the study by Trukhan (1975), were rivers and associated water reservoirs, vernal-autumnal ponds, and numerous wetlands and bogs. Adult Culicoides were active between May and October with two or three peaks throughout this period (Trukhan 1975). A total of 42 species belonging to three genera of Ceratopogonidae were recorded in Nakhichevan Republic (Khudaverdiev 1967). The most abundant species were C. puncticollis, C. riethi, C. circumscriptus, C. pulicaris, C. firuzae, C. saevus, Leptoconops camelorum Kieffer, L. (H) mediterraneus, and L. borealis. In lowland areas, adult biting midges were active from March to November, and in mountain areas they were active from May to October. Breeding sites included various wetlands and bogs, streams, storage ponds, and saturated soil. Biting midges were most abundant in May, June, August and early September in the low-land areas, in July and September in the foothill areas, and in June and July in the montane areas (Khudaverdiev 1967). CONCLUSIONS

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The current knowledge on distribution and diversity of Culicoides midges across the Russian Federation suggests a pan-Russian spread of these insects, with the exception of regions within the range of the far north (Mirzaeva 1984). There is generally higher abundance in forested areas with multiple, favorable breeding sites where flight activity occurs from May to September or October. In most parts of Russia there are generally two peaks of Culicoides activity with the first peak from mid-June until late July and the second peak in August. The second peak is likely to be due to the emergence of the second generation of certain species, as well as the occurrence of late summer species, such as С . grisescens (Mirzaeva 1984, Isaev 2013). A third peak is also possible for C. pulicaris, C. punctatus, and C. nubeculosus in Central Russia (Krivosheina 1957, Molev 1955, Isaev 2013). Flight activity occurs at temperatures ranging from 5° to 30° C, depending on the region, with optimum conditions for flight being between 7° and 22° C (Mirzaeva 1984, Glukhova 1989). Flight activity is also affected by light intensity, with activity occurring between 0 and 40,000 lx. The optimum light intensity for flight is between 100 and 5,000 lx (Mirzaeva 1984). Culicoides exhibit high ecological flexibility throughout Russia in terms of light and temperature tolerance. The lowest observed temperatures for midge activity were 4° C in Karelia, 4.8° C in Tomskaya Oblast, 5° C in Permaskiy kray, 6° C in Moscow Oblast, 8° C in Voronezh Oblast, 8.3° C in Ryazan’ Oblast, and 9° C in the Transcaucasus. Tolerance to cold temperatures in Culicoides declines and tolerance to light intensity increases with decreasing latitude. For example, in Permskii Kray, the highest abundance rates of Culicoides were reported to be between 51 lx and 100 lx compared to between 200 lx and 2,000 lx in the Transcaucasus. In central Russia, Culicoides have been shown to overwinter in the larval stage, with the exception of С. grisescens and С. punctatus that overwintered at the egg stage (Mirzaeva 1984, Isaev 2013). Because the territory of Russia offers a wide range of habitats and weather conditions, Culicoides can play an essential role in the spread of arboviral infections across the Russian Federation. Climatic conditions that influence abundance, activity patterns, and species composition, allow Culicoides to extend their range to northerly regions such as Karelia, Komi, Magadan, and Chukotka. One of the dominant species, C. pulicaris, is found in more northerly regions than C. obsoletus, another highly abundant species. The distribution of bluetongue virus is considered to be between 40° N and 35° S (MacLachlan and Guthrie 2010) and indeed, most cattle farms and dominant vector species in Russia lie outside of these latitudes. However, recent outbreaks of BTV-8 and SBV in Europe suggest a wider distribution is possible for these viruses. With allowance for the factors mentioned above, following an incursion event, BTV or SBV could spread during the period of flight activity (from June to September). The direction of virus movement may be northward or southward, depending on weather variables and host and breeding site availability. However, an incursion, if any, is likely to be short-lived due to severe winters with minus temperatures, extended vector-free periods, and cold

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spring and autumn temperatures that would significantly limit transmission in most parts of the Russian Federation. Acknowledgments The authors thank Simon Carpenter for valuable comments on the manuscript and Dudorova Marina for technical assistance. Marion England is funded by the UK National Laboratory for Culicoides (Defra). REFERENCES CITED Amosova, I. 1956. Fauna and biology of midges in the genus Culicoides (Fam. Heleidae) in coniferous-deciduous forests in the south of Primorie Territory: Dissertation thesis L.: 187 pp. (in Russian) Arnaud, P. 1956. The Heleid genus Culicoides in Japan, Korea, and Ryukyu islands (Insecta: Diptera). Microentomology 21: 84–207. Boorman, J. 1989. Culicoides (Diptera: Ceratopogonidae) of the Arabian Peninsula with notes on their medical and veterinary importance. Fauna Saudi Arabia 10: 160–224. Borkent, A. 2014. World Species of Biting Midges (Diptera: Ceratopogonidae). Belmont University. The Ceratopogonid web page. 234 pp. Brodskaya, P.K. 1992. Phenology and seasonal variation in the number of common species of the genus Culicoides biting midges in the south of the Pskov region. Parasitology. 3: 257-259. (in Russian ) Brodskaya, N. 2002. Midges (Diptera, Ceratopogonidae), Leningrad Region. Proceedings of the XII Congress of Russian Entomological Society, August 19-24, St. Petersburg. 49. (in Russian) Carpenter S., A. Wilson, and P.S. Mellor. 2009 Culicoides and the emergence of bluetongue virus in northern Europe. Trends Microbiol. 17: 172-178. Cornet, M. and J. Brunhes 1994. Révision des espèces de Culicoides apparentées à C.schultzei (Enderlein, 1908) dans la région afrotropicale (Diptera, Ceratopogonidae). Bulletin de la Société entomologique de France 99: 149– 164. Degtyareva, K.T. 1964. Fauna and ecology of the genus Culicoides biting midges in the conditions of the Voronezh region. Author. dis. kand.biol.nauk; Voronezh: 20 рp.(in Russian) Delecolle, J.-C., M. Brummer-Korvenkontio, and M. Kremer 1983. Culicoides (Diptera, Ceratopogonidae) new to the Finnish fauna light trapped in the Tvarminne area (Hanko, Southern Finland). Notulae Ent. 63: 88-89. (in Russian) Dzhafarov, Sh.М. 1964. Blood-sucking midges (Diptera, Heledae) of Trans Caucasus. Baku. 413 pp. (in Russian) Fridolin, V.Y. 1936. Animal-plant community of the mountain country Heebin. Tr. Kola. Base USSR Academy of Sciences 3: 1-295. (in Russian) Glukhova, V.M. 1956. Fauna and ecology of biting midges (Culicoides) Karelian-Finnish SSR. Dis. kand. biol. nauk L. 151 pp. (in Russian)

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