Thysanoptera of Bulgaria

Abstract The present checklist includes data on the species composition, geographic distribution and feeding preferences of thrips species in Bulgaria. In total, 155 species in 48 genera are listed. Of these, 125 species belong to suborder Terebrantia and include 103 species of 33 genera in family Thripidae, 14 species of two genera in Aeolothripidae, seven species of two genera in Melanthripidae and one species in Fauriellidae. In suborder Tubulifera, 30 species of 10 genera in the single family Phlaeothripidae are listed. Of the 155 Bulgarian thrips species, 87.7% are phytophagous, 4.5% are obligate predators, 5.8% are mycophagous and 1.9% are with unknown feeding preferences. Fourteen pest species are listed for Bulgaria, of which Frankliniella occidentalis, Thrips tabaci and Haplothrips tritici are of economic importance. The list provides detailed information on the horizontal and vertical distribution of Thysanoptera in 5 regions and 45 subregions of Bulgaria. The present paper also includes an evaluation of the biodiversity of Thysanoptera and the extent to which each region of the country has been studied.


Introduction
Bulgaria is located on the Balkan Peninsula and extends from the western shore of the Black Sea to Serbia and Macedonia to the west. It lies in the transitional area between the contrasting continental and Mediterranean climatic zones. Its varied relief and the peculiar characteristics of its weather contribute to its biotope diversity. According to the Palaearctic classification (Devillers et al. 2001), 977 distinct habitats from all hierarchical types occur in Bulgaria, 96 of which are unique to the country. This richness of habitats on a relatively small area is a prerequisite for a diverse thysanopteran fauna.
At present, the Bulgarian entomofauna is insufficiently studied and it has been estimated that about 51% of the insect species are known. More than 29 000 species of superclass Hexapoda have been established and it is expected that if rigorous research is performed, their number would increase to 56 000 (Hubenov 2005).
Thrips are small and slender insects that generally feed on plant sap, fungal spores and some on them are predators of small arthropods. Until now about 6000 species have been described worldwide (ThripsWiki 2015). Some are pests of agricultural crops and ornamentals, causing damage to plants either by feeding or via transmission of plant viruses, pathogenic bacteria and fungi.
The biodiversity of thrips on the Balkans has been studied more extensively in Romania (Vasiliu-Oromulu 1998) and Serbia (Andjus et al. 2008) with 215 and 155 reported species respectively. Information is scarce on the thysanopteran fauna in the other neighbours of Bulgaria: Greece, Macedonia and the European part of Turkey. After considering the climate and the number of described species of superclass Hexapoda in Bulgaria's neighbours and on the European continent as a whole, Hubenov (1996) claimed that there should be about 250 species of thrips in the country.
The thysanopterological activities in Bulgaria began at the end of the 19 th century. The first thrips species recognised in the country, Thrips urticae, was recorded on tobacco (Manushev 1897). Malkov recorded Limothrips cerealium and a year later Thrips tabaci (Malkov 1902(Malkov , 1903, and Limothrips denticornis was recorded on rye and barley (Dospevski 1910). Following these, Haplothrips reuteri, Aeolothrips fasciatus, Haplothrips tritici, Heliothrips haemorrhoidalis and Thrips atratus were recorded (Chorbadjiev 1929). In 1958, the Czech entomologist Pelikán conducted a study of the Bulgarian thrips fauna. He was the first to report 13 species of Aeolothripidae, described a new genus and species of Fauriellidae, Ropotamothrips buresi, and two years later recorded Melanthrips paspalevi and Melanthrips titschacki from Bulgaria (Pelikán 1960a(Pelikán , 1960b. In the late 60's, thrips research became more active. Janev (1968 and reported 22 species. In 1967, Genov reported two Haplothrips species on alfalfa. Donchev (1968Donchev ( , 1972Donchev ( , 1976Donchev ( , 1984Donchev ( , 1993Donchev ( and 1996 contributed to the Bulgarian thrips fauna with a series of publications, recording 33 species. Vesselinov (1968Vesselinov ( , 1976 recorded eight species; and. Popov (1973) recorded four thrips species found on medicinal plants which were new to the fauna of Bulgaria. Moreover, Popov (1976;1982a, 19851988) carried out extensive research on the diversity of thrips in Ograzhden mountain and reported 22 further species. He was also the first to document the Bulgarian treeliving thysanopteran fauna, reporting another 13 species from the country (Popov 1982b). Schliephake (1982) reported Thrips fedorovi from this country. Trenchev (1991) reported Frankliniella occidentalis in Bulgaria, and Trenchev and Karadjova (1992) reported its distribution and host plants in Bulgarian greenhouses. In 1996, after revision of microscope slides, the record of Anaphothrips armatus was cancelled because the reference specimens turned out to represent Rubiothrips ferrugineus (Zur Strassen 1996). Echinothrips americanus was first reported in 2003 by Karadjova and Krumov. A recent contribution to the arboreal thrips fauna of Bulgaria is the report of the mulberry thrips, Pseudodendrothrips mori, on the leaves of Morus alba (Trenchev and Trencheva 2007). Jenser and Krumov (2009) newly reported nine species. Krumov (2013) reported Idolimothrips paradoxus and Iridothrips iridis for the first time for the fauna of Bulgaria.
The main aim of this paper is to summarize all published data on thrips from Bulgaria in order to present a full list of known thrips taxa from the entire area of the country. Until now, no comprehensive review of the Bulgarian thrips fauna has been published. The present list includes 125 species of suborder Terebrantia and 30 species of suborder Tubulifera, and provides detailed information on the horizontal and vertical distribution of Thysanoptera in Bulgaria. It is complemented by an evaluation of the biodiversity and the extent to which each region of the country has been studied. The territorial distribution of thysanopteran species is crucial for the understanding of their biology and adaptations to different habitats. Such knowledge is of basic importance to explain the introduction and spread of exotic species, particularly pest species (Marullo and Grazia 2013). Another aim of the paper is to present information on the feeding preferences of thrips in Bulgaria: whether they are predatory, mycophagous or phytophagous and what plant species they have been collected from. This is important in order to understand the role of thrips in ecosystems, to ascertain which plants support phytophagous thrips (Mound and Marullo 1996), to evaluate their pest potential and to assess the impact of different thrips species on populations of other organisms within crops and natural non-cultivated areas

Material and methods
The list was prepared after a thorough review of all available publications and individual samples collected by the authors. The review includes all 37 scientific papers on the thysanopteran fauna in Bulgaria, published from 1897 to 2013. The list is arranged systematically and the nomenclature follows ThripsWiki (2015). Genera are listed alphabetically within each family or subfamily, and species are similarly listed within each genus. Each species account includes its taxonomic name, references, locality records within Bulgaria, altitudinal range (in m.a.s.l), plants on which adults have been found, and whether predatory, mycophagous or phytophagous. The geographic regions of Bulgaria and their abbreviations used in the text follow the division of Hubenov (1997), developed for the purposes of faunistic research. It does not consider the administrative territories but rather uses characteristics such as relief and local climatic conditions. The division includes five major territories, further split into subregions. The subheading "Distribution" for each species refers only to localities within Bulgaria.

B
Black

Suborder Terebrantia Haliday
Four families of this suborder are recorded from Bulgaria: Aeolothripidae, Melanthripidae, Fauriellidae and Thripidae. Thripidae is the largest family and includes the most economically important pest species.

Family Aeolothripidae Uzel
The family includes 190 extant species in 23 genera worldwide (ThripsWiki 2015). The adults and larvae of many representatives of this family appear to be facultative predators of small arthropods, although some species are almost certainly solely phytophagous (Tyagi et al. 2008). In the warmer parts of the world, a considerable number of species in family Aeolothripidae are obligate predators (Hoddle 2003). In Bulgaria, 14 species belonging to two genera have been recorded.

Family Melanthripidae Bagnall
This family includes 65 species of four genera. All representatives feed on flowers, but the distribution of the genera is remarkably fragmented (ThripsWiki 2015). In Bulgaria, 7 species of two genera have been recorded.

Family Fauriellidae Priesner
Five species belonging to four genera have been described worldwide but very little is known about them (ThripsWiki 2015). In Bulgaria, only one species has been reported.

Suborder Tubulifera Haliday
Suborder Tubulifera consists of about 3500 species and 450 genera, placed in the single family Phlaeothripidae and two subfamilies-Idolothripinae and Phlaeothripinae (ThripsWiki 2015). Species in Idolothripinae are considered to feed on fungal spores (Mound and Palmer 1983), while the Phlaeothripidae are considerably diverse with three recognized "lineages": Haplothrips, Liothrips and Phlaeothrips (Mound and Marullo 1996). The Haplothrips lineage is well defined as the tribe Haplothripini (Mound and Minaei 2007). Species in this tribe are often phytophagous but some are predatory on other small arthropods. Although flower-living is relatively unusual among Phlaeothripidae, in the genus Haplothrips a large number of species live in the flowers of Asteraceae, Poaceae and Cyperaceae (Mound and Minaei 2007). Members of the Liothrips lineage are leaf-feeding, and many of these are associated with the induction of leaf galls. Species in the Phlaeothrips lineage are essentially mycophagous, presumably hyphae feeders, and are often associated with dead leaves and branches (ThripsWiki 2015). Some Phlaeothripidae are associated with mosses, and others are predators on mites or on coccids (Mound 2004). Thirty species of 10 genera have been recorded from Bulgaria.

Discussion
In total, 155 species of thrips have been recorded in Bulgaria, in the altitudinal range from 0 to 2925 m a.s.l. Considering the assumption of Hubenov (1996) that there should be about 250 species in the country, order Thysanoptera has been insufficiently studied and research has uncovered merely 60% of its diversity. Currently thrips account for 0.53% of the total number of hexapods reported for Bulgaria. Two species, Rubiothrips vitis and Hoplothrips pallicornis, have been reported for Bulgaria in Fauna Europea but there is no actual evidence of their presence in the country and they have not been included in the list. The inconsistency of the information on R. vitis probably stems from the fact that Bournier (1976) lists R. vitis as a pest of vines in Bulgaria, quoting Zinca (1964). However, the paper of Zinca does not give any information on the presence of this species in the country. No information on the presence of H. pallicornis in Bulgaria was found in the literature. The only reference for this species from Europe is the redescription of Priesner (1964) resulting from its interception by New York harbour quarantine. The author explains that H. pallicornis is found in New York under bark of Juglans regia but originally comes from former Yugoslavia, suggesting that it may have a wider distribution at its origin. The authors of the present paper sent an informal request to Fauna Europea to ask for the source of the information leading to the inclusion of H. pallicornis in the list. The reply was that the only written reference of the species' presence in Europe is Preisner (1964) but it may be in the extensive collection of Pelikan (pers. comm., Bert Vierbergen, Andrea Hastenpflug-Vesmanis, 4 March, 2015) without ever having been published.
As regards the feeding preferences, 136 (87.7%) of the thrips species present in Bulgaria are phytophagous. The majority of them belong to the largest thysanopteran family, Thripidae (101). All seven reported species from family Melanthripidae are plant feeders. In family Aeolothripidae, there are eight phytophagous species which are also facultative predators. Family Phlaeothripidae includes 21 phytophagous species: 1 from genus Liothrips and 20 from genus Haplothrips. H. subtilissimus is also a facultative predator. Seven obligate predators from two families, Aeolothripidae (5) and Thripidae (2), have been reported. All 9 mycophagous thrips species present in Bulgaria belong to the Phlaeothripidae. Four of them are spore feeders (Idolothripinae) and 5 are hyphae feeders, of which Xylaplothrips fuliginosus is also a predator on mites. Three thrips species are with unknown feeding preferences.
Fourteen members of the phytophagous group are considered pests on agricultural crops. Among them, Frankliniella occidentalis and Thrips tabaci have economic importance as pests and vectors of Tomato spotted wilt virus (TSWV) (Karadjova and Krumov 2008), while Haplothrips tritici can cause significant damage to cereal crops (Krasteva et al. 2013).
On Figure 1 the geographical regions and subregions of Bulgaria are presented following the division of Hubenov (1997) and the numbers of thrips species found in each subregion.
Thirteen thrips species have been reported for the region of the Black Sea Coast (B). On the territory of Bulgaria, Amphibolothrips knechteli has been found only in the Northern Black Sea Coast subregion (BN), while Cephalothrips monilicornis, Melanthrips knechteli and Ropotamothrips buresi have been recorded only in the Southern subregion (BS) at altitudes close to 0 m a.s.l.
Forty nine species have been reported from the region of the Danubian Plain (D). A single species, Pseudodendrothrips mori, has been reported in Bulgaria only from its Western subregion (DW). The Middle subregion (DM) is well studied compared to the rest of the Danubian Plain due to the extensive research of the Bulgarian thysanopterologist Donchev during the period 1968-1996. Four species, Aeolothrips albicinctus, Haplothrips biroi, H. marrubiicola and Tenothrips discolor, have only been reported from there, at an altitude of 155 m a.s.l. Iridothrips iridis and Thrips linarius have been reported in Bulgaria only from the Eastern subregion (DE).
The large subregion of the Predbalkan (SP) is scarcely investigated with a total of 18 reported species. In Bulgaria, Haplothrips subtilissimus and Thrips viminalis are only found in the middle part of the Predbalkan (SPM). The parts of the Transitional Region (P) have been investigated to different degrees and are considered separately.
Twelve species have been reported from the Tundja-Strandja Subregion (PB). Currently, only Haplothrips hispanicus, found in the Sakar Mts (PBC), is reported in Bulgaria only from this subregion.
The diversity of thrips in the Thracian Lowland (PT) includes 14 species, none of which are found only in this subregion.
A total of nine species have been established in the vast Srednogorie-Podbalkan Subregion (PS) with no records which are unique for the country. Therefore its thysanopteran fauna is almost unknown.
The thrips of Vitosha District (PV) are better studied with 52 established species. The following have not been found elsewhere on the territory of Bulgaria: Aeolothrips priesneri in the Plana Mts. (PVP); Aptinothrips elegans, Chirothrips aculeatus, Hoplothrips ulmi, Mycterothrips salicis, Thrips calcaratus and T. simplex in the Sofia Basin (PVS); Belothrips morio and Odontothrips intermedius in the Vitosha Mts (PVV).
The Osogovo-Belasitsa region (RO) is the best studied area of Bulgaria, mainly due to the extensive research of T. Popov  The other large southern mountaineous area of the Rhodope Mts. (RR) is poorly studied with 12 recorded thrips species. Aptinothrips stylifer, Chirothrips pallidicornis and Haplothrips dianthinus are currently known only from the Western Rhodope Mts (RRW).
Three of the species in the list, Frankliniella occidentalis, Echinothrips americanus and Heliothrips haemorrhoidalis, have been reported only from greenhouses.
The number of Thysanoptera species recognized from Bulgaria demonstrates that they constitute one of the not very well studied orders of insects. The Bulgarian Thysanoptera represents less than 1% (0.53%) of the Hexapoda living in Bulgaria.
The reported thysanopteran species from Bulgaria are distributed in the altitudinal range from 0 to 2925 m a s l.