HISTORIA NATURALIS BULGARICA

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National Museum of Natural History — Bulgarian Academy of Sciences , Published online 30 May 2018 by:

National Museum of Natural History Bulgarian Academy of Sciences 1 Tsar Osvoboditel Blvd 1000 Sofia, Bulgaria http://www.nmnhs.com/historia-naturalis-bulgarica/

ISSN 0205-3640 (print) ISSN 2603-3186 (online) Contents

Boev, Zlatozar — Birds in everyday life and art in Bulgaria (Thracian and Roman periods) ...... 3 Stoianova, Desislava — It is raining bugs: summer dispersal of aquatic bugs (, : ) in (Bulgaria) ...... 41 Simov, Nikolay; Grozeva, Snejana; Langourov, Mario; Georgieva, Margarita; Mirchev, Plamen; Georgiev Georgi — Rapid expansion of the lace bug arcuata (Say, 1832) (Hemiptera: ) in Bulgaria ...... 51 Historia naturalis bulgarica 27: 3–39 ISSN 0205-3640 (print) | ISSN 2603-3186 (online) • http://www.nmnhs.com/historia-naturalis-bulgarica/ publication date [online]: 30 May 2018

Birds in everyday life and art in Bulgaria (Thracian and Roman periods)

Zlatozar Boev

National Museum of Natural History, Bulgarian Academy of Sciences, 1 Tsar Osvoboditel Blvd., 1000 Sofia, Bulgaria; E-mails: [email protected]; [email protected]

Abstract: This paper presents and analyses for the first time all data on the presence of birds (bone finds; 26 sites; 84 species/ genera) and their images in the art works (34 sites; 40 species/genera) from monuments of the ancient Thracian and Roman lands in Bulgaria (2200 BC – 4th c. AD), their utilisation and importance. Data of a total of 96 taxa of 29 families and 18 orders are presented. Differentaspects of the use of birds have been considered: hunting, domestication, falconry, decorative faunisation, including secondary use (as a source of bone material for the production of tools and adornments). The main groups of birds (waterfowl, eagles, pigeons, peacocks, etc.) and their symbolic mythological significance are presented. The images of some monuments represent exotic birds (purple swamphen, Egyptian goose, ring-necked parakeet, hel- meted guineafowl, Abyssinian lovebird, African green pigeon, spur-winged goose) which are now spread beyond the former (and Bulgarian) lands, mainly in East Africa. Their present ranges overlap only in the region of East Africa. They confirm ancient trans-Saharan Roman-“Ethiopian” contacts.

Key words: Birds in antiquity, ancient art, birds-man interrelations, Late Holocene birds, ornithoarchaeology

Introduction Currently, the human-bird interactions in the far. The abundant archaeological records of thou- Thracian (and Roman) period in Bulgaria have not sands of monuments from the Thracian period been studied in details. Only scattered and frag- throughout Bulgarian lands (including all neigh- mentary data exist. Ornithoarchaeological infor- bouring countries) provide an excellent heritage mation is much more abundant. The aim of this and make it the richest art heritage of that period paper is to evaluate the role of birds in the spiritual (15th c. BC – 6th c. AD) in Europe and in the world (especially in the /visual/ art) and everyday life of (Dimitrov, 1978a, b; Bozhkov, 1988, 1993). the Thracians and Romans. Overall, among the most exhaustive studies on Now it is well accepted, that Thrace was un- Thracian art are those of Filov (1918), Tsoncheva der the influence of the Mycenaean civilisation (1971), Venedikov, Gerasimov (1974), Lazarov after the last phase of the Bronze Age. In Thrace (1990) on the Thracian pottery, Dimitrov (1991), existed some state entities which, regardless of the etc. local differences, were fundamentally similar to the Birds alone in the ancient Thracian and Mycenaeans (Tacheva-Hitova, 1976). In the regions Roman lands of Bulgaria have not been a subject of of Western and Eastern Bulgaria, in the interior of special studies until present, although some studies the country, some Thracian state formations existed on the fauna of ancient Thrace, as reflected in the already during the second half of the 2nd millenni- ancient literature, exist (Velkov, 1956 a, b). The only um BC (Velkov, 1979). research on the birds during the Roman period of The Thracian art in Bulgaria has been subject Bulgaria was published by Boev (2006), where data of numerous investigations and interpretations so on 85 avian taxa were presented. 4 Zlatozar Boev

In the last two decades, the ornithoarchaeo- Galabovo logical exploration of several dozens of monuments Gledachevo of Thracian (and early Roman) periods revealed in- Golyamata Peshtera Cave teresting details of exploitation of birds by the an- Kabile cient population in the Bulgarian lands. Kostinbrod Malak Preslavets – 2 Nicopolis-ad-Istrum Material and Methods Novae The Thracian period in the history of Orphey the Bulgarian lands covers the time from Peshterata na strelite approximately 2200 BC – 2nd c. BC (Velkov, 1979). Radnevo In the present study we discuss all preserved im- Ratiaria Serdica ages (pictures, bas-reliefs, statuettes, sculptures, Shipka etc.) of birds, found only in the present (since 1945) Sozopol Bulgarian lands, although former Thrace included Urdoviza parts of present Southern Bulgaria, Westernmost Yassa-Tepe Turkey and Eastern Greece (Velkov, 1979). The nu- Zelenigradska Cave merous archaeological finds in the former lands of the Thracians from the neighbouring countries re- List of the archaeological monuments with bird images main out of the scope of this paper. from the Thracian/Roman period in Bulgaria (Table 1): The subfossil records of the Late Holocene Armira birds of the Late Bronze and Iron Ages and the Borovo Chernozem Early Antiquity are presented in brief, as a number Dolna Koznitsa of special publications present this matter in more Dragodan detail. Durostorum (pr. ) The “eagle-griffons”, “lion-griffons”, “horse- Duvanli roosters” (hippalectrions) and other fantastic crea- Galiche tures are intentionally omitted from this research. Garchinovo Their mythological and art significance are not tak- Garescus (pr. Sandanski) en into account, but they are listed as types only for Ginina Mound, Sveshtari comparison purposes. Although Kovachev, Sirakov Kabile (2016) state that modern scientists still argue about Kralevo the kind of bird, depicted as a hippalectrion, i. e. Letnitsa junglefowl (rooster), vulture or (?) griffon, here we Magurata Cave have to remind that the griffon is not a real Malomirovo species. It is a mythological creature and we could Marcianopolis Morozovo (pr. Gorno Tserkovishte) firmly accept that the hind part of the hippalectrion Mramor Mound, Panagyurishte represents the hind part of the body of a rooster. Nesebar The same applies for the discussed by Kovachev and Oescus Sirakov (2016) rhyton of Taneva mound from the Orsoya Sliven District. In addition, the numerous “eagle- Philippopolis (pr. Plovdiv) griffons” are not accepted and discussed as eagles. Monastery Rogozen List of the archaeological monuments with bird bone remains from the Thracian/Roman period in Bulgaria Seuthopolis (Table 1): Shekerdzha Mound, Kamen Shipka Abritus Sofia Arbanas Sozopol Armira Starosel Bagachina Sveta Sofia Church Chavdarova Cheshma Tazha Ezero Varbitsa Filipovska Cave – 2*

* “Filipovska Cave – 2” and “Malak Preslavets – 2” are listed as they appeared in the original publications. Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 5

General characteristics of the Thracian art and its expressive significance As known, the Thracians did not have their own writing system. On certain occasions they used Ancient Greek writting, for example for the inscrip- tions on their vessels, often decorated with images of , including fine birds. It is notable, that the introduction of elements of the Hellenic iconography coincides with the first attempts for wider use of the Hellenic alphabet and language in the superscripts of the Thracian objects. According to Fol (1975), the art in Thrace was “aristocratic” in the 6th c. BC Fig. 1. Goose’s head from the Chernozem Village (Plovdiv Region; 2nd half of 5th c. BC). After Kisyov (2005). and after. The social fundament of the Thracian art led it to a rapid decline in times of social-political turbulences (Fol et al., 1993). These authors deter- mine the Thracian art as “geometric” in the 8th – 7th c. BC. According to Venedikov (1981), the geometric art and the animal ornaments appear in the western Thracian regions in the 7th and 6th c. BC. Thracian art treats the balance between one or another natural force, as well as that between man and nature, as opposed to the Hellenics, whose prin- ciples compare the relationship between human be- ings or those between humans and deities. From this point of view, two distinctly different systems are dis- tinguished, which suggests radically different sym- bolic structures. In fact, the language of art remains the only authentic “Thracian” language. During the Late Iron Age the Thracian art Fig. 2. Swans of the bronze pitcher-rython of the Borovo has its achievements in the tomb architecture (the treasure (Ruse Region; 4th c. BC). After Ivanov (1975). tombs in Kazanlak, Sveshtari), secular buildings, toreutics (the treasures of Letnitsa, Lukovit, Borovo, of the continent, including the most abundant (and Rogozen), decorations for horse ammunition favourable) faunal resources to man (sea coasts, river (Brezovo, Bukyovtsi, Oryahovo, Orizovo), etc. (Fol estuaries, lagoons, coastal and inland lakes, swamps et al., 1993). and marshes, alpine landscapes and vast plains, rock In general, the Thracian culture reaches its massifs, gorges, dense broad-lived and coniferous peak in the 6th c. BC. It is the time of the great golden forests, meadows, steppes and many others). and silver treasures made to please the aristocracy It is assumed that zoomorphism is one of the (Venedikov, 1982). “codes” of mythology, folklore, epos and pictorial art, through which particular type of texts are created, in The zoomorphism of the Thracian art which animals play a major role. In the early stages of The art of the Thracians is possibly the most art development, the animal code better corresponds “zoomorphic” among the ancient cultures of Europe. to the iconography inherited from the “geometric” era. It is a representation of natural powers and gods with Therefore, zoomorphism is inherent not of thinking the qualities and peculiarities of animals. The zoo- (content) but of expression, and it is a problem of pic- morphism (the so-called “animal style” of Scythians) torial language (Fol et al., 1993). The “animal motif”, is a result of the early religious concepts that convey treated realistically, prevails in the Thracian art. The the meaning of the gods using animal style. This “animal style” of Thracian toreutics is a peculiar expres- stage of the zoomorphic pantheon precedes the stage sion of the aesthetics of the Thracians (Vaklinov, 1973). of the anthropomorphic divine images. Like the other iconic signs, the zoomorphs The lands of the ancient Thracians, situated in have no definite meaning outside the given context. the south-eastern corner of Europe, during the whole Therefore, it is necessary to determine with which Holocene is the region with the richest biodiversity other codes the zoomorphic link is connected to. 6 Zlatozar Boev

Fig. 4. “Eagle” with beaked fish and rabbit in the claws of the Rogozen treasure (Rogozen Village, Vratsa Region; 2nd half of 4th c. BC) After Fol. et . al. (1988).

Early Iron Age, when heels of the cult axes, amulets or forehead plates are decorated with or shaped as the figures of domestic animals: ram, goat, bull. The bird is also among the main symbols. This increased interest in animal figures and their individual parts (mostly the head) are embodied using a new mate- rial – the bronze. Small statuettes are also produced, which may be decorated with cult or social attrib- utes. The animal figures are still geometrically styl- ised: the body is represented as a prism, the head as a “reel”, the eyes are circles and the back becomes a hemisphere. This geometric (stereometric, in fact) style is typical of the art of Middle and South- eastern Europe, the Caucasus and Iran, and includes Fig. 3. Horned eagle of the Rogozen treasure (Rogozen Village, Thracian art culture in the same international com- nd th Vratsa Region; 2 half of 4 c. BC). After Nikolov (1987). munity. In the Late Bronze Age, there is some resem- This makes it possible to understand the particular blance to the decorative repertoire of Mycenaean art meaning of an animal in the pictorial narrative. In (Fol et al., 1993). Fol et al. (1993) summarise, that the “animal style” of Thrace, there are three groups since the end of the Late Bronze Age, the ornamen- of fauna: predators (lion, panther, bear, dog, wolf), tal fund includes spirals, volutes (spiral ornaments), herbivores (deer, horse, wild boar) and birds (most concentric circles with centre point meanders, dia- often predatory and waterfowl; Figs. 1, 2.). monds and triangles (sometimes shaded), points and semicircles. Such geometrical ornaments are According to Venedikov (1974b), such a „zoo- th logical” subject-matter appears from the East in the preserved from as early as the 6 c. BC, when only 6th c. BC, although based on mythical creatures, such the decoration system changes. In many monuments as horned lion, lion-griffon, horned eagle (Fig. 3), of the Roman period we find a number of complex horse-roosters, etc. ornaments, enclosing images of birds in the ancient The zoomorphic decoration takes place either mosaics, for example. as a shaping of the entire object or part of it as a fig- Ornithomorphic symbols in the Thracian art ure of an (vertebrate) animal. In the Late Bronze Age, Zoomorphic symbolism also enters the po- the image of a water bird is most commonly used litical terminology of the ancient world. Thus, in (Fol et al., 1993). Among them, often we find images the emblematic group of the eagle with beaked fish of pond ducks, geese, swans, etc. and hare in the claws (Fig. 4), it is coded by the ani- Zoomorphism develops further during the mal classifiers of the elements of the Achemenian Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 7

an eagle (Fig. 6). The oldest monument in Bulgaria representing the Mother of the gods with the rap- tor bird (with the appearance of an “eagle” again) in Thrace, is the handle of a bronze mirror from the Chukurka Village near Aytos (Burgas Region from the end of the 6th c. BC; Venedikov, 1992). The main animal images of the previous period are later replaced by the victim or prey. The animal images and scenes become a means of expressing mythological and ideological ideas. Among the ar- chaeologists and culturologists there is no doubt about the contribution of the Achaemenid art to ico- nography of animal style. “Bird” as a generalised image is present in nu- merous artworks at many Thracian sites. Usually the “bird” is not a raptor, wader, owl, duck/swan, swan, crane, etc. It is often depicted as a “birdie”, and a good example for it are the two bird images of a phalera plate of Galiche Village (Filov, Velkov 1919- 1920; Fig. 7). Birds on the , in Bulgaria and the former Thracian/ Roman lands The recent avifauna of the Balkan Peninsula numbers circa 516 species (Michev et al., 2013), while the bird fauna of Bulgaria alone includes 420 species (Ivanov et al., 2015). On the other hand, the orni- thoarchaeological data of the Thracian period from Bulgaria cover 84 species/genera (Boev, 1993, 1996a,

Fig. 5. Eagle’s head from the Tomb of the Seuthes III from the Golyama Kosmatka Mound near town of Shipka (Stara Zagora Region; 2nd half of 4th c. BC). After: https://www.google.bg/ur l?sa=i&rct=j&q=&esrc=s&source=images&cd=&cad=rja&u act=8&ved=0ahUKEwj5jMOztb7QAhUJkRQKHegaA0oQjR wIBw&url=https://www.pinterest.com/pin/45500436858010 9057/&psig=AFQjCNFLks0-f64TyjM5q-EXt7mSybLjXA&u st=1479974585173765 political formula: “Bring Me Water and Land” by which the victor-king turns to the defeated ruler (Fol et al., 1993). The same bird (“eagle”) is repre- sented in the Rogozen treasure (Nikolov et al., 1986, 1987), Seuthopolis (Tsoncheva, 1971), Shipka (Agre, 2006; Marazov, 2010; Fig. 5), Dragodan (Teodosiev, Manov, 1993), Armira (Mladenova, 1991), Nicopolis ad Nestum (Popova-Moroz, 1987) and many other sites (Table 1). According to Popova-Moroz (1987) the pigeons and peafowls in front of the vine kylixes Fig. 6. Griffon, attacking a deer of the treasure of Letnitsa symbolise the communion. The water birds (and (Lovech Region; 2nd half of 4th c. BC). After: https://www. birds with beaked fish) symbolise the new person’s google.bg/url?sa=i&rct=j&q=&esrc=s&source=images&cd= state after the conversion to Christianity. &cad=rja&uact=8&ved=0ahUKEwiU_e381azQAhWBvBQK HaXtBaYQjRwIBw&url=http://trakite.info/traki-sakrovishta/ The “eagle” of the treasure of Letnitsa sakrovishte-letnica.html&psig=AFQjCNHF5OIL85RUPCfYA-- (Venedikov, 1996) is actually a gryffon, rather than Ec4kehFZ7IA&ust=1479364661087056 8 Zlatozar Boev

1996b, 1997a, 1997b, 1999, 2004, 2006; Table 1). (Boev, 2017a) and Chavdarova Cheshma (Boev, These subfossil remains of birds have been found at 2017b); and in – Bagachina (Boev, 27 archaeological sites: in present Southern Bulgaria 1996b, 1999), Nicopolis-ad-Istrum (Boev, 1991, 2006; – Kabile (Boev, Ribarov, 1993), Shipka (Boev, 1999), Boev, Beech, 2007), Abritus (Boev, 2006), Ratiaria Urdoviza (Boev, Ribarov, 1990), Sozopol (Boev, (Iliev et al., 1993; Boev, 2006), Malak Preslavets – 2 1995), Galabovo (Boev, 2004), Radnevo (Boev, 2004), (Boev, 2006), Ezero (Ivanov, Vasilev, 1979) and Novae Yassa-Tepe (Ribarov, Boev, 1990), Gledachevo (Boev, (Schram, 1975, 1979; Walushevska-Bubien, Krupska, 1999, 2006), Zelenigradska Cave (Boev, 2001, 2006), 1983; Bartosiewicz, Choyke, 1991). Most of these 84 Filipovska Cave – 2 (Boev, 2001, 2006), Golyamata species/genera represent game fowl, waterfowl and Peshtera Cave near Kyustendil (Boev, 1999), Serdica other hunting and domestic birds (Table 1). Importance of birds for ancient Thracians and Romans It is well known that different species of birds have different ethnological importance. Always Usually the domestic birds are the most important among the birds in the everyday life (Fig. 8), fol- lowed by the large game birds. Both groups (domestic and game) have been used as a source of meat, eggs, bones, feathers, down, etc. (s. c. “primary utilisation”). Some other aspects of the utilisation of birds in the Thracian period (Late Bronze Age to Iron Age and the Antiquity) are listed by Boev (2011). In the sunken settlement of Urdoviza (near Kiten, Burgas Region) are found three long hollow wing bones of the Great white peli- can (Pelecanus onocrotalus), which have been cut and Fig. 7. Generalised “bird” image of the phalera plate of Galiche wound up as a part of a device for blowing or suck- Village (Vratsa Region) (2nd-1st c. BC). After: https://www. ing/infusion (Boev, Ribarov, 1990; Boev 2011; Fig. 9). google.bg/search?q=%D1%84%D0%B0%D0%BB%D0%B5%D1 In the settlement of Bagachina (near Rasovo %80%D0%B0%D1%82%D0%B0+%D0%BE%D1%82+%D0%B3 %D0%B0%D0%BB%D0%B8%D1%87%D0%B5&dcr=0&tbm=i Village, Montana Region) from the Early Iron Age, a sch&source=iu&ictx=1&fir=y0kfj6VlgI7wLM%253A%252CQa bone ring of the diaphysis of the humeral bone of the uQ4g7UmxRFiM%252C_&usg=__tgmD82SFHQwMVT3XfIb wing of a domestic goose (Anser anser domestica) are RQ0myTto%3D&sa=X&ved=0ahUKEwivzqDegL7ZAhWKqaQ found (Boev, 2011). In Apolonia a flute of long bones KHV_JBZsQ9QEIRDAF#imgrc=y0kfj6VlgI7wLM: of birds have been found in 2007 (Golemanov, 2012).

Fig. 8. Indian peafowl (Pavo cristatus) from the Roman mosaic of the Bishop Basilica in Plovdiv (5-6th c. BC). After: https://www. google.bg/url?sa=i&rct=j&q=&esrc=s&source=images&cd=&cad=rja&uact=8&ved=0ahUKEwifwuKDhZzQAhWDuxQKHfX4C 0gQjRwIBw&url=http://www.dnevnik.bg/razvlechenie/2015/12/15/2670438_proektut_za_episkopskata_bazilika_dobavia_oshte_ edin/?ref=id&bvm=bv.138169073,d.d24&psig=AFQjCNG_F9Nhb3wmsr-Ih2vEKnP-1jceUg&ust=1478793330707090 Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 9 Source Ivanov (1975), Venedikov Ivanov (1975), Venedikov (1992) (present study) Filov (1934) (present study) (present study) Gerasimov Venedikov, (1973) (present study) Apollon (2012) (present study) (present study) Bird images Site Borovo Philippopolis Plovdiv) (pr. Varbitsa Philippopolis Plovdiv) (pr. Philippopolis Plovdiv) (pr. Tazha Philippopolis Plovdiv) (pr. Garescus (pr. Sandanski) Philippopolis Plovdiv) (pr. Philippopolis Plovdiv) (pr. Source Boev, Ribarov (1990) Boev, Schramm (1975) Bartosiewicz, Choyke (1991) Beech (2007) Boev (2006); Boev, Ribarov (1990) Boev, Beech (2007) Boev (2006); Boev, Beech (2007) |Boev (2006); Boev, Ribarov (1990) Boev, Ribarov (1993) Boev, Beech (2007) Boev, Boev (2004) Iliev et al. (1993) Boev (1995) Ribarov (1993); Boev (2006) Boev, Boev (1996b, 1999) Beech (2007) Boev, Boev (1995) Ribarov (1993) Boev, Ribarov (1990) Boev, Beech (2007) Boev (2006); Boev, Bird bone remains Bird bone remains Site Avian records (bone remains, art images) in Thracian/Roman monuments of Bulgaria of monuments in Thracian/Roman art images) remains, (bone records Avian Table 1. Table Urdoviza Novae Novae Nicopolis-ad-Istrum Urdoviza Nicopolis-ad-Istrum Nicopolis-ad-Istrum Urdoviza Kabile Nicopolis-ad-Istrum Galabovo Ratiaria Sozopol Kabile Bagachina Nicopolis-ad-Istrum Sozopol Kabile Urdoviza Nicopolis-ad-Istrum Taxa sp. sp. Cygnus cygnus Cygnus olor Cygnus Alopochen aegyptiaca Anas crecca Anas penelope Anas plathyrhynchos Anas strepera Anas Spatula querquedula gambensis Plectropterus Anser albifrons No ANSERIFORMES Anatidae 1 2 3 4 5 6 7 8 9 10 11 12 10 Zlatozar Boev Source (present study) Kisyov (2005) Bird images Site Philippopolis Plovdiv) (pr. Chernozem Boev, Ribarov Boev, (1990) Source Continued Boev (2017) Ribarov (1990) Boev, Boev (1990) Ribarov, Boev (2004) Beech (2007) Boev, (1979) Vasilev Ivanov, Krupska (1983) Walushevska-Bubien, Boev (2006) Ribarov (1993) Boev, Boev (2004) Krupska (1983) Walushevska-Bubien, Ribarov (1990) Boev, Beech (2007) Boev (2006); Boev, Ribarov (1993) Ribarov (1991); Boev, Beech (2007) Boev, Schramm (1975, 1979) Boev (1996b, 1999) Beech (2007) Boev (2006); Boev, Ribarov (1990) Boev, Beech (2007) Boev, Schramm (1975) Ribarov (1990) Boev, Boev (1995) Krupska (1983) Walushevska-Bubien, Boev (1999) Boev (1997, 2006) Beech (2007) Boev (2006); Boev, Boev (2001) Urdoviza Table 1. Table Bird bone remains Bird bone remains Site Serdica Urdoviza Yassa-Tepe Galabovo Nicopolis-ad-Istrum Ezero Novae Kabile Kabile Galabovo Novae Urdoviza Nicopolis-ad-Istrum Kabile Nicopolis-ad-Istrum Novae Bagachina Nicopolis-ad-Istrum Urdoviza Nicopolis-ad-Istrum Novae Urdoviza Sozopol Novae Armira Arbanas Nicopolis-ad-Istrum Zelenigradska Cave sp. tadorna Taxa cf. sp. Anser anser Anser anser domestica Anser erythropus Anser fabalis Anser Tadorna ferina Aythya nyroca Aythya Aythya Netta/ perdix Perdix No 13 14 15 16 17 18 19 20 21 GALLIIFORMES Phasianidae 22 Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 11 Source Atanasov (2008) (present study) Gorov et al. (1967) (1963) Venedikov Martinova-Kyutova, Raycheva (2013) Ivanov (1955, 1957); Petrov (1986), Boev (1995) (present study) (present study) Bird images Site Durostorum (pr. Durostorum (pr. Silistra) Philippopolis Plovdiv) (pr. Sozopol Rila Monastery Plovdiv Oescus Philippopolis Plovdiv) (pr. Philippopolis Plovdiv) (pr. Source Continued Boev (2006); Boev, Beech (2007) Boev (2006); Boev, Beech (2007) Boev (2006); Boev, Boev (2017) Boev (2004) Boev (2001) Ribarov (1993) Ribarov (1991); Boev, Boev (2017) Beech (2007) Boev (2006); Boev, Iliev et al. (1993) Boev (2006) Boev (1997, 2006) Boev (2001) Boev (2006) Boev (2004) Boev (2006) Krupska (1983); Schramm Walushevska-Bubien, (1975, 1979) Ribarov (1993) Boev, Beech (2007) Boev, Boev (1995) Ribarov (1993) Boev, Iliev et al. (1993) 2001) (Boev, Beech (2007) Boev (2006); Boev, Boev (2004) Ribarov (1991) Table 1. Table Bird bone remains Bird bone remains Site Nicopolis-ad-Istrum Nicopolis-ad-Istrum Serdica Radnevo Zelenigradska Cave Kabile Chavdarova Cheshma Nicopolis-ad-Istrum Ratiaria Gledachevo Arbanas Filipovska Cave – 2 Abritus Galabovo Malak Preslavets – 2 Novae Kabile Nicopolis-ad-Istrum Sozopol Kabile Ratiaria Filipovska Cave – 2 Nicopolis-ad-Istrum Galabovo Kabile Taxa Coturnix coturnix Alectoris graeca Alectoris chukar Gallus gallus domestica Gallus/ Phasianus Phasianus colchicus No 23 24 25 26 27 28 12 Zlatozar Boev Source Martinova-Kyutova, Raycheva (2013) (present study) Apollon (2012) Atanasov (2008) 1989) (Plakidov, Martinova-Kyutova, Raycheva (2013) Bird images Site Plovdiv Philippopolis Plovdiv) (pr. Garescus (pr. Sandanski) Durostorum (pr. Silistra) Armira Plovdiv

Source Continued Boev (2006); Boev, Beech (2007) Boev (2006); Boev, (1979) Vasilev Ivanov, Nikolov – unpubl. data Vasil Boev (2006) Boev (1995) Ribarov (1990) Boev, Beech (2007) Boev (2006); Boev, Ribarov (1990) Boev, Boev (1995) Ribarov (1990) Boev, Boev, Ribarov (1990) Boev, Table 1. Table Bird bone remains Bird bone remains Urdoviza Boev, Ribarov (1990) Urdoviza Boev, Site Urdoviza Nicopolis-ad-Istrum Ezero Golyamata Peshtera Cave Nicopolis-ad-Istrum Sozopol Urdoviza Nicopolis-ad-Istrum Urdoviza Sozopol Urdoviza Taxa Pavo cristatus urogallus Tatrao Numida meleagris Gavia arctica stellata Gavia arctica/ Gavia stellata Podiceps cristatus Podiceps griseigena Podiceps nigricollis No 29 Tetraonidae 30 Numididae 31 GAVIIFORMES Gaviidae 32 33 34 PODICIPEDIFORMES Podicipedidae 35 36 37 Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 13 Source Fol et al. (1988) (1967) Tsanova Getov, Bird images Site Rogozen Morozovo Gorno (pr. Tserkovishte) Source Continued Bartosiewicz, Choyke (1991) Ribarov (1990) Boev, Boev (2006) Schramm (1975) Ribarov (1990) Boev, Boev (1995) Beech (2007) Boev (2006); Boev, Bartosiewicz, Choyke (1991) Ribarov (1990) Boev, Bartosiewicz, Choyke (1991) Boev (1999) Ribarov (1993) Boev, Boev (1995) Schramm (1975) Beech (2007) Boev, Boev (2006) Beech (2007) Boev, Boev (2004) Table 1. Table Bird bone remains Bird bone remains Site Novae Urdoviza Kostinbrod Novae Urdoviza Sozopol Nicopolis-ad-Istrum Novae Urdoviza Novae Armira Kabile Sozopol Novae Nicopolis-ad-Istrum Gledachevo Nicopolis-ad-Istrum Galabovo Taxa Pelecanus onocratalus carbo Phalacrocorax aristotelis Phalacrocorax Ciconia ciconia Ciconia ciconia / nigra Ardeidae cinerea Ardea Pandion haliaetus Accipiter gentilis Accipiter nisus Aquila chrysaetos No PELECANIFORMES Pelecanidae 38 Phalacrocoracidae 39 40 CICONIIFORMES Ciconiidae 41 42 43 ACCIPITRIFORMES Pandionidae 44 Accipitridae 45 46 47 14 Zlatozar Boev Source Tsoncheva (1971) Tsoncheva Agre (2006), Marazov (2010); History Museum – Kazanlak (collection, unpubl.) Manov (1993) Teodosiev, (1996) Venedikov Mladenova (1991) Fol et al. (1986) (unpubl. Maya Avramova data) Regional History Museum (unpubl.) – Yambol Nikolov (1987), et al. (1987); Marazov (1996) Gerasimov Venedikov, (1973) Dimitrova (2012) Kitov (2003) Mario Ivanov – unpubl. data Bird images Site Seuthopolis Shipka Dragodan Letnitsa Armira Ginina Mound, Sveshtari Nesebar Kabile Rogozen Garchinovo Shekerdzha Mound, Kamen Starosel Sofia Source Continued Boev (2006); Boev, Beech (2007) Boev (2006); Boev, Ribarov (1993) Boev, Beech (2007) Boev (2006); Boev, Boev (2006) Beech (2007) Boev (2006); Boev, Ribarov (1993) Boev, Iliev et al. (1993) Bartosiewicz, Choyke (1991) Table 1. Table Bird bone remains Bird bone remains Site Nicopolis-ad-Istrum Kabile Nicopolis-ad-Istrum Abritus Nicopolis-ad-Istrum Kabile Ratiaria Novae

Taxa sp. Circaetus gallicus Circaetus “Aquila” Milvus milvus Buteo buteo cf. Gypaetus barbatus Gyps fulvus Haliaetus albicilla No 48 49 50 51 52 53 54 Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 15 Source Staykova (1997) Ginev (1983, 2000) Agre (2006); Marazov (2010) (present study) Angelov (1994) Apollon (2012) (present study) Bird images Site Dolna Koznitsa Kralevo Malomirovo Philippopolis Plovdiv) (pr. Marcianopolis Garescus Philippopolis Source Continued Boev (2001) Beech (2007) Boev (2006); Boev, Ribarov (1993) Boev, Beech (2007) Boev (2006); Boev, Beech (2007) Boev (2006); Boev, Beech (2007) Boev, Beech (2007) Boev (2006); Boev, Boev (2001) Boev (1997, 2006) Beech (2007) Boev (2006); Boev, Ribarov (1993) Boev, Boev (1990) Ribarov, Bartosiewicz, Choyke (1991) Beech (2007) Boev (2006); Boev, Ribarov (1993) Boev, Ribarov (1990) Boev, Boev (1995) Table 1. Table Bird bone remains Bird bone remains Site Zelenigradska Cave Nicopolis-ad-Istrum Kabile Nicopolis-ad-Istrum Filipovska Cave – 2 Nicopolis-ad-Istrum Nicopolis-ad-Istrum Zelenigradska Cave Arbanas Nicopolis-ad-Istrum Kabile Yassa-Tepe Novae Nicopolis-ad-Istrum Kabile Urdoviza Sozopol Taxa tinnunculus cf. Falco Falco cherrug Falco peregrinus Athene noctua Strix aluco Bubo bubo Grus grus crex Crex Fulica atra Porphyrio porphyrio No FALCONIFORMES Falconidae 55 56 57 STRIGIFORMES Strigidae 58 59 60 GRUIFORMES Gruidae 61 Rallidae 62 63 64 16 Zlatozar Boev Source Filov (1919) Katincharov Dzhambazov, (1974), Gerasimova, Stoychev (1992, 1993) Filov (1934), Venedikov (1994) Atanasov (2008) (1919-1920) Velkov Filov, Filipov (1976); Shalganova (2005) (unpubl. Maya Avramova data) (present study) Anonym (2014) Bird images Site Mramor Mound, Panagyurishte Magurata Cave Duvanli Durostorum (pr. Silistra) Galiche Orsoya Armira Philippopolis Plovdiv) (pr. Sveta Sofia Church Source Continued Boev, Ribarov (1993) Boev, Beech (2007) Boev (2006); Boev, Boev (1990) Ribarov, Beech (2007) Boev (2006); Boev, 2001) (Boev, Boev (1997, 2006) Beech (2007) Boev, Krupska (1983) Walushevska-Bubien, Beech (2007) Boev, Iliev et al. (1993) Beech (2007) Boev, Ribarov (1993) Boev, Beech (2007) Boev, Table 1. Table Bird bone remains Bird bone remains Site Kabile Nicopolis-ad-Istrum Yassa-Tepe Nicopolis-ad-Istrum Filipovska Cave – 2 Arbanas Nicopolis-ad-Istrum Novae Nicopolis-ad-Istrum Ratiaria Nicopolis-ad-Istrum Kabile Nicopolis-ad-Istrum Taxa Otis tarda tetrax Tetrax Columba livia Columba oenas Columba palumbus turtur Streptopelia calva Treron No OTIDIFORMES Otididae 65 66 COLUMBIFORMES Columbidae 67 68 69 70 71 Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 17 Source (present study) (present study) (present study) (present study) (present study) (present study) Bird images Site Philippopolis Plovdiv) (pr. Philippopolis Plovdiv) (pr. Philippopolis Plovdiv) (pr. Philippopolis Plovdiv) (pr. Philippopolis Plovdiv) (pr. Philippopolis Plovdiv) (pr. Source Continued Boev (2006) Beech (2007) Boev (2006); Boev, Ribarov (1990) Boev, Boev (2006) Boev (2006) Boev (1996b, 1999) Boev (2001, 2006) Boev (2001) Boev (2006) Table 1. Table Bird bone remains Bird bone remains Site Peshterata na strelite Cave Nicopolis-ad-Istrum Urdoviza Abritus Gledachevo Bagachina Filipovska Cave – 2 Filipovska Cave – 2 Peshterata na strelite Cave Taxa . sp Caprimulgus europaeus Caprimulgus europaeus fulicarius Phalaropus Larus Psittacula krameri Agapornis taranta apiaster Merops Picus canus Hirundo daurica merula Turdus No CAPRIMULGIFORMES Caprimulgidae 72 CHARADRIIFORMES Scolopacidae 73 Laridae 74 PSITTACIFORMES Psittacidae 75 76 CORRACIIFORMES Meropidae 77 PICIFORMES Picidae 78 PASSERIFORMES Hirundinidae 79 Turdidae 80 18 Zlatozar Boev Source Torbov (2005) Torbov Bird images Site Mogilanska Mound 40 taxa Source Continued Boev (2006) Boev (2006) Beech (2007) Boev (2006); Boev, Beech (2007) Boev (2006); Boev, Boev (1996b, 1999) Beech (2007) Boev (2006); Boev, Beech (2007) Boev, Beech (2007) Boev (2006); Boev, Beech (2007) Boev (2006); Boev, Krupska (1983) Walushevska-Bubien, Beech (2007) Boev (2006); Boev, Boev (2001) Beech (2007) Boev (2006); Boev, 2001) (Boev, Krupska Walushevska-Bubien, Schramm (1975); (1983) Beech (2007) Boev (2006); Boev, Boev (2006) Boev (2006) Boev (2001) Beech (2007) Boev (2006); Boev, Beech (2007) Boev (2006); Boev, Beech (2007) Boev (2006); Boev, Boev (2001) Beech (2007) Boev (2006); Boev, 2001) (Boev, Table 1. Table Bird bone remains Bird bone remains Site Orphey Kabile Nicopolis-ad-Istrum Nicopolis-ad-Istrum Shipka Nicopolis-ad-Istrum Nicopolis-ad-Istrum Nicopolis-ad-Istrum Nicopolis-ad-Istrum Novae Nicopolis-ad-Istrum Filipovska Cave – 2 Nicopolis-ad-Istrum Filipovska Cave – 2 Novae Nicopolis-ad-Istrum Malak Preslavets – 2 Gledachevo Filipovska Cave – 2 Nicopolis-ad-Istrum Nicopolis-ad-Istrum Nicopolis-ad-Istrum Zelenigradska Cave Nicopolis-ad-Istrum Filipovska Cave – 2 84 taxa Taxa sp. sp. Turdus ruficollis Turdus Erithacus rubecula Turdus Fringilla coelebs Linaria cannabina Passer/ Fringilla Passer domesticus Sturnus vulgaris Corvus cornix Corvus monedula Corvus Corvus frugilegus Garrulus glandarius Pica pica Nucifraga caryocatactes graculus Pyrrhocorax Total No 81 82 83 Fringillidae 84 85 86 Passeridae 87 Sturnidae 88 Corvidae 89 90 91 92 93 94 95 96 Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 19

Fig. 9. Ulna and two radius bones of Pelecanus onocrotalus from the sunken settlement of Urdoviza (3000-2000 BC.). Photograph: Victor Hazan.

Fig. 10. Fighting roosters (domestic red junglefowl Gallus gallus domestica) from Ulpia Oescus (2nd c. BC). After Ivanov (1955).

Table 1 shows that in the Thracian-early-Roman 75 BC but Simeonov (1988) states that the oldest evi- time many birds have been part of the feathered dence of falconry in this part of the Balkan Peninsula game: geese, ducks, coots, bustards, grey and rock is from the 4th c. BC. According to Hristovich (1939), partridges, doves, grebes, pheasants, loons, etc. in the lands of present-day Bulgaria (in Thrace) Other birds (eagles, falcons, eagle owls) have hunting with trained diurnal raptors has been known been used for falconry (see below). Some (domestic from a later time – from the 1st c. AD. chicken) have been first used for spectacular fighting Velkov (1956 b) gives the most detailed descrip- (Fig. 10). Much later, they have become a preferred tion of the Thracian falconers: besides for hunting source of meat. mammals, the Thracians also loved to go hunting birds, using trained hawks (or falcons). This used Origin of falconry in Europe in the time to be particularly common practice in the down- of ancient Thracians stream area of the Mesta and Struma Rivers. There, A special kind of utilisation of a group of birds the hunters from the villages went hunting, carrying (diurnal and nocturnal raptors) firstly appeared dur- the falcons with them. Walking around the swamps, ing the Thracian times. According to Boev (1945), the they struck the stems and surrounding bushes with falconry has been practiced by Thracians already in sticks. The birds that were in hiding flew off, and 20 Zlatozar Boev

Fig. 11. Head of a falcon of the treasure Fig. 12. Eagle with a hare on a grave of Kralevo (Targovishte Region; end of of Malomirovo – Zlatinitsa Villages 4th -early 3rd c. BC). After: https://www. (Yambol Region; 2nd half of 4th c. c. BC). google.bg/url?sa=i&rct=j&q=&esrc=s& After Marazov (2010). source=images&cd=&cad=rja&uact=8 &ved=0ahUKEwiZpLyJ-7TRAhXDiRo KHbKQD54QjRwIBw&url=http://www. znam.bg/com/action/showArticle?encID =1&article=792119267&psig=AFQjCN H5DQtxiUOt4gP9nDj07fcjUzFbOA&u st=1484047811958169

Fig. 14. Three ornithomorphic vessels from Orsoya (Montana Region; 14th -12th c. BC) after Bozhkov (1988).

preservation (Fig. 11). Aristotle (384-322 BC) also describes hunting of wading birds in Thrace with domesticated falcons. The hunters moved the stems of the reed with rods Fig. 13. Image of a duck on a vessel from Tazha Village near the town of Kazanlak (Stara Zagora Region; 4th c. BC). and the birds that were hidden in them were captured After Venedikov, Gerasimov (1974). by the hunting hawks waiting for them. According to Arabadzhiev (1962), it can be concluded from the the boys immediately released their falcons, calling testimonies of Aristotle and Pliny the Elder (23-79 them by name. The falcons rose quickly and forced BC) that in the poleis of ancient Greece after the 6th the birds to return back to the bushes where the boys c. BC, the hunting with trained raptors was still un- hunted them by striking them with sticks. Part of known. the hunting was handed over to the falcons. But the Hristovich (1939) refers to Pseudo-Aristotle, most interesting thing was that when they caught a who reports that in the ancient Greek city of bird, they did not tear it, but tossed it to the hunt- Amphipolis, which existed from 436 BC to the 5th ers (Velkov, 1956 b). Images of falcons of that period c. AD at the mouth of the Struma River, the hunt- are not numerous, but some of them are of excellent ing of grey partridges (Perdix perdix) with trained Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 21

Fig. 15. Eagle from a mound burial near Dragodan Village (Kyustendil Region; 2nd c. BC). After Teodosiev, Manov (1993).

Fig. 16. Eagle statuettes of the necropolis near Dolna Koznitsa Village (Kyustendil Region; 4th c. BC). After Staykova (1997). falcons was spread. It is believed that the Thracians earlier period, at that time have appeared also lions, hunted with trained hawks and falcons 2200 years panthers, and dogs. As before, animals are usually ago (Arabadzhiev, 1962, Denkov, 1988). Numerous displayed on a profile. Bowls with the image of birds, are the images also of the precisely dated Thracian best testified again in Istria (in the westernmost silver objects representing hunting of hares with ea- part of the Balkan Peninsula), are also common in gles/falcons (Rogozen – Nikolov, 1987; Malomirovo Eastern Thrace (Thacia Pontica). There are many – Agre, 2006), which confirms such a view. animal figures represented in the Pontic pottery: It is supposed that the falconry, an aristocratic deer, wild boars, panthers, lions, waterfowl (Fig. 13). way of hunting, has been re-transferred to Europe The Corinthian painted pottery abounds with fan- from the eastern Roman provinces no later than the tastic creatures and monsters: sirens, sphinxes, wings beginning of the 1st c. AD. It is well known that the of dragons (Lazarov, 1990). Roman Emperor Avitus (ca. 450 AD) introduced In hinterland Thrace birds are also present in hunting with trained falcons in order to entertain the the items of treasures, e.g. the Rogozen treasure in Emperor’s Court (Arabadzhiev, 1962). ornaments and palmettes alternating with stylised Although the falconry is known in the ancient birds. The birds’ heads are turned backwards (Fol et Rome, reliable information on this practice dur- al. (1988). ing the Roman rule (168 BC – 3rd c. AD) in today’s In the vicinities of the Drama and Zavoy Villages Bulgarian lands is still missing. (Yambol Region) have been found excellent exam- An eagle holding a hare with its claws is depict- ples of the s. c. “bird bowls“ of the Early Iron Age/ ed on a greave from a grave between the Malomirovo the beginning of the Late Iron Age (second quarter and Zlatinitsa Villages (Fig. 12). – end of 7th c. BC; Karadzhinov, 2012). The author concludes that they are known from “several sites in Bird images on the objects of the Thracian art the Pontic Area, concentrated along the Northern According to Lazarov (1990), in the 7th -5th c. Black Sea coast and the Northern Anatolian hinter- BC (the “archaic” period of the Thracian art), the land” (p. 10). subjects are expanding, along with bulls, deer, boars, It is known, that the “bird bowls” have been goats, eagles, cocks and water birds found in the produced in special bird bowls workshops in the 22 Zlatozar Boev

Fig. 19. Osprey from the Vratsa treasure (Vratsa Region; 2nd half of 4th c. BC). After Torbov (2005).

Fig. 17. Silhouette of an eagle from Me- sembria (pr. Nesebar, Burgas Region; 3rd c. BC). After Maya Avramova (unpubl.). Fig. 18. Osprey of the Rogozen treasure (Rogozen Village, Vratsa Region; 2nd half of 4th c. BC). After Marazov (1996).

Northern Ionia in the 2nd quarter of the 7th to the 1st decades of the 5th c. BC. (Karadzhinov, 2012). The bird motifs are widely spread in the art of the Bronze Age and Early Iron Age in the central parts of the Balkan Peninsula (Vasic, Vasic, 2000). In Eastern Serbia, for example, numerous bird-chariots, bird-vases, bird-rattles, bird-pendants, bird-fibulae, Fig. 20. Image of a “pigeon” from etc. have been found. Waterfowl (ducks) are the Mushovitsa mound, Duvanli Village most often depicted. Vasic and Vasic (2000) defined (Plovdiv Region; 5th c. BC). After Vene- a special cult of ducks as peaceful dwellers of water dikov (1994). bodies close to human settlements. The excellent ce- The image of the “eagle” is the most often de- ramic ornithomorphic vessels from Orsoya near the picted bird image. Images of “eagle” are common town of Lom in NW Bulgaria are of the same type in the Thracian art, as those of lions (Golemanov, (Fig. 14). Filipov (1976) also concludes that in the 2012). late Bronze Age the ornithomorphic vessels are in- Another “eagle”, the fish-eating osprey (Pandion herent in the culture of inlaid ceramics on the Lower haliaetus), is very probably depicted on a vessel of River. They are found mostly in the ne- the Rogozen treasure (Fol et al., 1988, p. 146; Figs. cropoles. There are also a number of other ceramic 18-19). Not only the beacked fish, but some details of ornithomorphic cult objects as chariot models, labs, the image (distinctive separation between head and thrones, tables, anthropomorphic idols, etc. neck and its shape, the beak shape /and its smaller The images of the “eagle“ and the “osprey” size/, the eye-ring, etc.) suggest for an image of os- prey. It is broadly accepted that the “eagle” is a symbol of “the supreme authority in the Iranian-Caucasian The images of the “pigeon” and the “dove” world” (Todorova et al., 2011) and among the The pigeons are an ornithomorphic metaphor Scythians (Melyukova, Moshkova, 1976). The im- of the lasses, while the cut wings of the birds symbol- age of the “eagle” is present in the Thracian art in the ise their lost virginity (Marazov, 2016). Their images Late Iron Age tomb architecture – Sveshtari (Pavlov, are often present on the Thracian (and later Roman) 1982, Golemanov, 2012), toreutics – the treasures monuments (Fig. 20). of Letnitsa (Nikolov, 1974), Lukovit (Chichikova, 1980), Starosel (Kitov, 2003), Borovo (Ivanov, 1975), Roman-Ethiopian influence on the depicted bird Rogozen (Nikolov et al., 1987; Fol et al., 1988), some fauna of the Roman Bishop Basilica in Plovdiv (Roman Philippopolis) other finds (from Stara Zagora /Venedikov, 1974a/) (Figs. 15-17). The exotic birds of the Roman Bishop Basilica Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 23

Fig. 21. Present range of purple swamphen (Porphyrio porphyrio) and the territory of the Roman Empire at the time of its height in 117 AD. (After BirdLife International and Handbook of the Birds of the World 2017 and Anonym (2018).

Fig. 22. Present range of Egyptian goose (Alopochen aegyptiaca) and the territory of the Roman Empire at the time of its height in 117 AD. (After BirdLife International and Handbook of the Birds of the World 2017 and Anonym (2018). 24 Zlatozar Boev

Fig. 23. Present range of ring-necked parakeet (Psittacula krameri) and the territory of the Roman Empire at the time of its height in 117 AD. (After BirdLife International and Handbook of the Birds of the World 2017 and Anonym (2018).

Fig. 24. Present range of helmeted guineafowl (Numida meleagris) and the territory of the Roman Empire at the time of its height in 117 AD. (After BirdLife International and Handbook of the Birds of the World 2017 and Anonym (2018). Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 25

Fig. 25. Present range of Abyssinian lovebird (Agapornis taranta) and the territory of the Roman Empire at the time of its height in 117 AD. (After BirdLife International and Handbook of the Birds of the World 2017 and Anonym (2018).

Fig. 26. Present range of African green pigeon (Treron calvus) and the territory of the Roman Empire at the time of its height in 117 AD. (After BirdLife International and Handbook of the Birds of the World 2017 and Anonym (2018). 26 Zlatozar Boev

Fig. 27. Present range of spur-winged goose (Plectropterus gambienis) and the territory of the Roman Empire at the time of its height in 117 AD. (After BirdLife International and Handbook of the Birds of the World 2017 and Anonym (2018). in Plovdiv are alien to the recent Bulgarian fauna: Morocco (Martinez, 1994) and P. porphyrio occurs Purple swamphen (Fig. 21), Egyptian goose (Fig. 22), also in Southern Spain, France, Italy, Algeria, Tunisia, ring-necked parakeet (Fig. 23), helmeted guineafowl Libya, Egypt and Iran (Taylor, 1996). All these terri- (Fig. 24), Abyssinian lovebird (Fig. 25), African tories were part of the Roman Empire. green pigeon (Fig. 26), spur-winged goose (Fig. 27; The occurrence of the helmeted guineafowl Table 2). These exotic bird species comprise 1/3 of (Fig. 28) needs special attention. According to all recorded species of birds (including domestic Larson, Fuller (2014), N. meleagris occurs natu- forms as peafowl and chicken) among the mosaics rally in the wild through Sub-Saharan Africa, but of this remarkable monument of ancient art. Seven numerous artistic and bone evidence suggests it of the 20 recognised bird species/forms, are exotic may have been domesticated in Mali and Sudan as compared to present day fauna, mainly inhabiting about 2000 ago. In Europe probably it became “ex- Northern and Sub-Saharan Africa. These birds have tinct” in captivity and the species was secondarily unmistakable coloration of their plumage (and habi- domesticated (again in Europe) in the 16th c. AD tus in general) and unquestionably prove the ancient after Portuguese travels in the region of W Africa contacts of the Romans far southward, beyond the (Sossinka, 1982). broadly-accepted borders of the Roman Empire. The complete aridisation of Sahara finished by A striking fact: All exotic birds of the Bishop 3500 BC (Capot-Rey, 1958). Additionally, the most Basilica (except for the domestic peafowl) at present extensive expansion of the Sahara Desert occurred are spread in East Africa: Ethiopia, Eritrea and South in the last two millennia (Cloudsley-Thompson, Sudan. This region has remained beyond the most 1990). As a result, the climate of North Africa has south-eastern limits of the Roman Empire even in not changed tangibly since the Roman colonisation its height in 117 AD and lies at circa 1000 km away (Capot-Rey, 1958). Thus, the northern range limits from the former Roman lands. At present, all these of some present-day “Sub-Saharan” species of birds, exotic birds (except N. meleagris and P. porphyrio) could be much more extended northward, reaching have Sub-Saharan ranges (Figs. 22-27). Besides in the south-eastern corner of the Roman Empire. Sub-Saharan Africa, N. meleagris is spread also in On the other hand, there are a number of evi- Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 27

Table 2. Mosaic images of birds from the of Bishop Basilica of Philippopolis – pr. Plovdiv

No Species Mosaic images ANSERIFORMES Anatidae 1 Alopochen aegyptiaca

2 Anas crecca

3 Spatula querquedula

4 Anas platyrhynchos

28 Zlatozar Boev

No Species Mosaic images 5 Anser anser

6 Plectropterus gambensis

Galliformes Phasianidae 7 Gallus gallus domestica – male

Gallus gallus domestica – male

Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 29

No Species Mosaic images 5 Phasianus colchicus – female

Phasianus colchicus – male

Phasianus colchicus – male

6 Alectoris chukar

7 Coturnix coturnix

30 Zlatozar Boev

No Species Mosaic images 8 Pavo cristatus – male

Pavo cristatus – male

Numididae 9 Numida meleagris

GRUIFORMES Gruidae 10 Grus grus

Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 31

No Species Mosaic images Rallidae 11 Porphyrio porphyrio

Porphyrio porphyrio

Porphyrio porphyrio

Porphyrio porphyrio

CHARADRIIFORMES Scolopacidae 12 Phalaropus fulicarius

32 Zlatozar Boev

No Species Mosaic images Laridae 13 Larus sp.

PICIFORMES Picidae 14 Picus canus

PSITTACIFORMES Psittacidae 15 Psittacula krameri

Psittacula krameri

Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 33

No Species Mosaic images 16 Agapornis taranta

COLUMBIFORMES Columbidae 17 Treron calva 34 Zlatozar Boev

dences confirming trans-Saharan commercial ties of (Swanson, 1972: p. 4). They were most intensive in the Roman Empire at least since the 3rd c. BC (Capot- the period of 50 BC to 300 AD. “What was the trade Rey, 1958). After the rule of the emperor Augustus that went on between Rome and Ethiopia over the (63 BC-14 AD), Rome had four provinces in Africa: Saharan trails? It certainly involved animals – the vast Numidia, Africa (Tunisia), Cyrenaica and Egypt quantities of exotic species that were slaughtered in (Swanson, 1972). the arenas of Rome were usually of Ethiopian origin, All this facts unequivocally confirm the brought up from Central Africa via the Sahara and Roman-Ethiopian/Abyssinian contacts. It is wor- the Fezzan.” (Swanson, 1972: p. 28). Hence, the lands thy to mention, that the contacts between Ethiopia of pr. Ethiopia and Sudan were the major source of and the Mediterranean World (3000 BC – 400 AD) animals for the Roman arenas. According the nu- were numerous and intensive, as has been proved by merous evidences, the Ethiopian Kush Kingdom Swanson (1972). The author states that the contacts have exported to Rome (i. e. Egypt in that time) “… between the Roman world and Ethiopia date be- traditional products of the caravan trade, as ivory, tween 50 BC and 300 AD, when Rome began to ex- gold, wild beasts, spices and slaves” (Swanson, 1972: pand onto the African continent. Romans had con- p. 66). Numerous are the historical evidences for the tacts with the State of Kush, the Ethiopian Kingdom ancient contacts between Thrace and Egypt in the (750 BC to 200 AD). The Kushites and their succes- Hellenic epoch, especially in the region between the sors were often militarily and commercially involved Lower Nile River and the Red Sea (Atanasova, 2017). with Rome and these interrelationships were of some Thus, in Central Sahara the contacts between importance during the lifetime of the Roman Empire the Mediterranean world and Ethiopia were es- Birds in everyday life and art in Bulgaria (Thracian and Roman periods) 35 sentially trade contacts. These contacts were quite extensive. Trade by its very nature is a contact be- tween peoples and, although direct physical contact between Romans and Sub-Saharan Ethiopians was probably limited, there is no doubt that the trans- Saharan trade was important to the classical world” (Swanson, 1972: p. 29). While the large mammals of the Ethiopian re- gion have been supplied into the Roman Empire for slaughtering in the arenas, the presence of the colour- ful birds (all of them non-passerine), which are found Fig. 28. Helmeted guineafowl (Numida meleagris) from the in the Roman mosaics in Philippopolis, could only be Roman mosaic of the Bishop Basilica in Plovdiv (5-6th c. BC). explained by their aesthetic value, such as bright colour After: https://www.google.bg/search?q=%D0%B5%D0%BF%D plumage, amazing behaviour, beautiful plumage orna- 0%B8%D1%81%D0%BA%D0%BE%D0%BF%D1%81%D0%BA mentation, etc. All these exotic for Bulgaria birds of %D0%B0+%D0%B1%D0%B0%D0%B7%D0%B8%D0%BB%D African (Ethiopian) origin could not be depicted with- 0%B8%D0%BA%D0%B0+%D0%BF%D0%BB%D0%BE%D0% B2%D0%B4%D0%B8%D0%B2&dcr=0&source=lnms&tbm=isc out direct observation of live individuals. That means h&sa=X&ved=0ahUKEwiW67_zhb7ZAhXLzaQKHfh8AdwQ_ (and proves) that live individuals of the seven exotic AUICigB&biw=1920&bih=888#imgrc=O1M5s7RWG6asEM:& birds (purple swamphen, Egyptian goose, ring-necked spf=1519457936392 parakeet, helmeted guineafowl, Abyssinian lovebird, African green pigeon, and spur-winged goose) have been brought in the ancient Philippopolis and pictured as (basic) elements of the floor mosaic decoration of the Bishop Basilica. Mosaic images of the purple swam- phen exist in another Roman town, Marcianopolis (pr. Devnya; Boev, 1997b) and the Thracian town Garescus (pr. Sandanski; Apollon, 2012). Roman mosaics of Indian peafowl are known in Garescus, Marcianopolis, etc. (Table. 1). Other birds are mentioned among the images of the mosaic in Sandanski (Plakidov, 1989), St. Sofia Basilica (Fig. 29), etc. Plakidov (1989) gives the most synthet- ic overview of the animalistic subjects in the Roman mosaics: The hunting theme treated in the Roman floor mosaics expresses the assertive life understanding. There is no hint of any cruelty, nor killing of the game. On the contrary, animal figures are radiating the immense feeling of artist’s sympa- thy. Here dominate the friendship and the beauty. Fig. 29. Pigeons (? Columba livia). Mosaics of the St. Sofia Perhaps this is due to the ancients’ conviction of the Basilica 4th c. AD; Sofia). After: http://www.google.bg/url? indivisibility of nature, of its unity, in which both sa=i&rct=j&q=&esrc=s&source=images&cd=&cad=rja&u game and hunter constitute a harmonious whole. act=8&ved=0ahUKEwjTzPDu9vLYAhVQb1AKHXLLCXI QjRwIBw&url=http://crhc-sofia.com/bg/content/podova- Discussion and Conclusion mozayka-rayat&psig=AOvVaw2kSZ-zs9cGnO3Q72ccoWN- &ust=1516962853937981 Birds have played an important role both in the everyday and spiritual life of the people in the iously stylised, but sufficiently preserved for reliable Thracian/Roman period and, thus are well present- taxonomic identification (Table 2). ed in the ancient Thracian and Roman art. Usually Most of the depicted bird species of the Roman the Thracian images were symbolic, generalised and mosaics are native and are spread in Bulgaria at pre- stylised and they often lacked important specific di- sent. Although some of them are not breeding in the agnostic features for species identification. country, they are still represented in the nature of the In the Roman period bird images were much present Bulgarian territory as occasional or regu- more realistic. Their specific features were ingen- lar winter visitors: common crane, Colchic pheasant 36 Zlatozar Boev

(wild native, not the hybridised from), grey phalarope. Bone remains of birds alone from the Thracian/ The common crane disappeared as a nesting species Roman sites confirm the presence of the great major- in the 1950s, while the native Colchic pheasant sur- ity of local bird species and domestic forms (84 spe- vived until the early 1990s. The grey Phalarope is an cies/taxa; Table 1). Although rare, some finds prove extremely rare winter visitor. On the other hand, the the secondary use of birds (e. g. their bones). common quail, grey-headed woodpecker, chukar par- tridge, garganey, mallard, common teal and the gray- lag goose occur and breed throughout the country. Acknowledgements:: The author thanks to the archaeol- In general, hunting birds were rarely depicted, ogists Zheni Tankova, Desislava Davidova and Elena except those with colourful decorative (or specific Kantareva-Decheva (Regional Archaeological Muse- contrast) plumage, e. g. the chukar partridge, mute um, Plovdiv) for their assistance in the documenta- swan, helmeted guineafowl, mallard, etc. tion of antique mosaics of the Bishop Basilica in Plov- Other of the recorded birds on various monu- div. I am also grateful to Nikolay Spassov (National ments were used as pets (parrots, Indian peafowl, Museum of Natural History, Bulgarian Academy of chicken, purple swamphen). Some of them are a tra- Sciences, NMNHS), who suggested such a topic of ditional source of meat and subject of poultry breed- a multidisciplinary study within the project: “Thra- ing (chicken, Indian peafowl, helmeted guineafowl, cians – Genesis and Ethnic Development, Cultural geese and ducks). Identities, Civilisation Interactions and Heritage of The precise colourful images of birds in the Antiquity” of the Bulgarian Academy of Sciences. floor mosaics of the Roman Bishop Basilica in Special thanks Georgi Popgeorgiev (NMNHS) for Philippopolis (pr.** Plovdiv) are so realistic that preparing the distribution maps of some birds and Bulgarian Government deposited in 2017 an official to Maya Avramova (National Archaeological Insti- application for their recognition as part of the World tute and Museum, Bulgarian Academy of Sciences) Cultural Heritage of UNESCO (Chaleva, 2017). for the provided photographs of some bird images. They represent a rare proof for the ancient Roman- BirdLife International provided distribution maps of Ethiopian interrelations. some exotic birds.

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It is raining bugs: summer dispersal of aquatic bugs (Hemiptera, Heteroptera: Nepomorpha) in Srebarna Nature Reserve (Bulgaria)

Desislava Stoianova

Institute of Biodiversity and Ecosystem Research (IBER), Bulgarian Academy of Sciences, 2 Yurii Gagarin Street, 1113 Sofia, Bul- garia; e-mail: [email protected]

Abstract: The Srebarna Nature Reserve is a wetland with great conservation value. The dispersal of aquatic bugs in it has not been studied earlier. Acquiring more data about the aquatic bug’s species composition and dispersal activity is a pre- requisite for future studies on phenology or faunistic studies of the group in the wetland. In the present paper, aquatic bugs attracted to UV light near the Srebarna Nature Reserve were quantified. A total of 4589 individuals of aquatic bugs (Heteroptera, Nepomorpha) were collected during 11 nights of light trapping. Dispersing aquatic bugs were almost exclusively (4587 specimens, 13 species in five genera), except for two Notonectidae species. Eleven species, collected during the study have not been registered previously in the Srebarna Nature Reserve. The activity peak of dispersal was registered during the first hour after sunset. Females prevailed in the four most abundant species. The changes in the dispersal activity of the most common species – striata (Linnaeus, 1758), were explained (to a great extent) by changes in air temperature, atmospheric pressure and wind speed.

Key words: Corixidae, light trap, sex ratio, UV, wetland

Introduction True aquatic bugs (Nepomorpha) are not only activity (Popham, 1943a, 1943b; Fernando, 1959; a component of many vertebrates’ diet (Papáček, Campbell, 1979; Weigelhofer et al., 1992; Csabai & 2001), but themselves are predators on a wide range Boda, 2005; Boda & Csabai, 2009a). of smaller invertebrate organisms. They often play a The focus of the present work is on dispersing part in controlling disease vectors by feeding on the aquatic bugs, attracted by light close to the border of larvae of mosquitoes of Anopheles, Culex and Aedes the Srebarna Nature Reserve – a wetland in North- (Quiroz-Martínez & Rodriguez-Castro, 2007; Kweka eastern Bulgaria. The Srebarna Lake was declared a et al., 2012). Despite the significant role of aquatic protected site in 1942 and in 1948 - a nature reserve. bugs in food webs, very little is known about the The area is a Wetland of International Importance dispersal of these . For most of the aquatic (a Ramsar site) and is included in the UNESCO bug species no clear patterns of dispersal activ- list as Biosphere Reserve and as World Natural and ity have been established yet, although different as- Cultural Heritage. It is also a part of the European pects of aquatic bugs dispersal by flight have been Important Bird Areas list and of the ecological net- discussed (mostly for the family of Corixidae): sex work NATURA 2000. According to the current na- ratio of the dispersing individuals (Brown, 1954; tional nature protection legislation, the Srebarna Pajunen & Jansson, 1969a; Benedek & Jászai, 1973; Lake is a managed reserve (Uzunov et al., 2012). Kecső & Boda, 2008), diurnal patterns of flight activ- The great conservation value of the Srebarna Nature ity (Leston, 1953; Leston & Gardner, 1953; Popham, Reserve is defined by its rich biodiversity, including 1964; Csabai et al., 2006; Boda & Csabai, 2009a), both species of conservation significance and prior- influence of environmental variables on the flight ity (from conservation point of view) habitat types. 42 Desislava Stoianova

The main problems for the conservation of the nat- To gain an insight of species collected by in situ ural ecosystems in the reserve could be defined as sampling, a list of aquatic bugs reported in previ- follows: the pollution from agriculture, forestry and ous studies from the Srebarna Nature Reserve and waste water, as well as the application of inappropri- sampled during this study with a kick-net was com- ate technology for usage of natural resources and the posed (Table 2). Data about collected aquatic bugs degradation of the landscape (Updated management using kick-net were used only for checking which of plan for maintained reserve “Srebarna” from 2014). the species collected by the light trap also had been There is available reference data about the true bugs collected from aquatic habitats in the region. In the found in aquatic habitats within the reserve: aquatic present study, the quantities of the collected aquatic bug species are included in three papers contributing bugs using each of the two methods were not com- to the macrozoobentic (Marinov, 2000; Uzunov et al., pared. 2001; Varadinova et al., 2011, 2012) and one to the The collected aquatic bugs were identified ac- fauna (Marinov, 2000), but there are no previ- cording to Jansson (1986) and Kanyukova (2006). ously published data about aquatic bugs dispersing A VANTAGE VUE weather station was mount- in the vicinity of this wetland. Such data could be of ed on the same roof to measure every 15 mins tem- use in future studies on the fauna or phenology of the perature (°C), relative humidity (%), atmospheric aquatic Heteroptera in the wetland. pressure (mb) and wind speed (m/s,). The aim of this study is to answer the follow- The material for the study was collected in ac- ing questions: (1) Are the species, collected at the UV cordance with permission № 48-00-264/26.03.2010, light (original data) different from those collected by issued by the Bulgarian Ministry of Environment in situ sampling (published and original data)? (2) and Water. What is the sex ratio of the collected aquatic bugs? Data analysis: Graphics and analysis were (3) What is the influence of environmental variables completed in R (R Core Team, 2016). Differences (such as air temperature, atmospheric pressure and between the number of collected males and females wind speed) on the aquatic bugs’ dispersal? were tested with Wilcoxon signed-rank test using The efficiency of the light trap method used function wilcox.test from R package MASS (Venables here was also discussed in respect to biodiversity & Ripley, 2002). The same function was used for test- surveys targeting mainly aquatic bugs. ing the three one-hour blocks for differences in the number of collected aquatic bugs. Material and Methods Weather parameters possibly affecting the aer- ial dispersal of Sigara striata (Linnaeus, 1758) were Study area: The study was carried out in the explored by fitting quasi-Poisson generalized linear south-eastern part of the reserve: samples were col- model (GLM). The model building was performed lected from the lake, close to the shore and also from in the package stats (R Core Team, 2016) using the temporary pools near the lake (Table 1). Material function glm. The dependent variable was the num- was collected also in the Srebarna Village, close to ber of captured S. striata individuals for each col- the reserve by a light trap. lecting session. A range of weather variables (tem- Data collection: Aquatic bugs were collected during 11 nights (5–6, 8–9, 11–17 June 2010) of light trapping. Light trapping started at the predicted time of sunset, around 21:30 h, and continued for three hours. In order to examine dispersal changes, the samples were divided into three one hour blocks. A 125 W mercury vapour lamp was mounted on the flat roof of a 3 m high building (44°05’37.66’’ N, 27°04’04.71’’ E) at the edge of the Srebarna Village. The bulb was strung at 1 m above the roof, a white sheet spread out on the surface of the roof (Fig. 1). Aquatic bugs were collected by hand (by Merlijn Jocque and Patricia Caballero) and preserved in 70% ethanol. All specimens are stored at the Institute of Fig. 1. The light trap setup in this study – a car battery Biodiversity and Ecosystem Research, Bulgarian powered UV bulb (125W) strung 1 m above the roof, above a Academy of Sciences, Sofia. white sheet on the ground. It is raining bugs: summer dispersal of aquatic bugs (Hemiptera, Heteroptera: Nepomorpha) in Srebarna... 43

Table 1. Locations where aquatic bugs have been collected by kick-netting in the course of this study in Silistra Province, Bulgaria (April and June 2010).

Date Locality Depth (m) Vegetation Latitude Longitude Temporary pool connected 11 April 2010 0.45 0 44° 05' 19" N 27° 03' 52" E to Srebarna Lake 7 June 2010 Srebarna Lake 1 1 44° 05' 54" N 27° 04' 15" E 10 June 2010 Ditch near Srebarna Lake 1 1 44° 06' 11" N 27° 03' 49" E 17 June 2010 Srebarna Lake close to the shore 1 1 44° 05' 36" N 27° 04' 08.5" E

Table 2. Species and abundance of aquatic bugs collected using the light trap in this study. The species recorded in previous papers are marked with: “1” for Marinov, 2000 and “2” for Varadinova et al., 2012. Kick-net collections (April and June 2010) are included.

Light trapping Kick-net Ref. Family Species f m f m juv Corixidae coleoptrata (Fabricius, 1777) 1 0 0 0 0 1, 2 Cymatia rogenhoferi (Fieber, 1864)* 207 110 0 0 0 affinis Leach, 1817* 0 1 0 0 0 Corixa panzeri Fieber, 1848* 0 1 0 0 0 Corixa punctata (Illiger, 1807)* 1 0 0 0 0 Hesperocorixa linnaei (Fieber, 1848), 1, 2 5 4 50 31 0 (as H. limnaei (F.) in: 2) concinna (Fieber, 1848)* 59 7 0 1 0 Sigara (Halicorixa) stagnalis pontica Jaczewski, 1961* 26 5 1 0 0 Sigara (Pseudovermicorixa) nigrolineata (Fieber, 1848) 0 0 1 0 0 1, 2 Sigara (Retrocorixa) limitata (Fieber, 1848) * 0 1 0 0 0 Sigara (s.str.) assimilis (Fieber, 1848) * 3 5 0 0 0 Sigara (s.str.) striata (Linnaeus, 1758) 1435 566 20 21 0 1, 2 Sigara (Subsigara) falleni (Fieber, 1848) 0 0 0 0 0 1, 2 Sigara (Subsigara) iactans Jansson, 1983* 395 263 3 3 0 Sigara (Vermicorixa) lateralis (Leach, 1817) 858 634 4 3 0 1, 2 Corixidae gen. sp. 0 0 0 0 18 Naucoridae Ilyocoris cimicoides (Linnaeus, 1758) 0 0 1 3 47 Notonectidae Notonecta (s.str.) glauca (Linnaeus, 1758)* 1 0 5 2 4 Notonecta (s.str.) viridis (Delcourt, 1909)* 1 0 0 0 0 Nepa cinerea Linnaeus, 1758 Nepidae 0 0 0 0 0 1, 2 (as N. rubra Linnaeus. in 1, 2) Ranatra (s.str.) linearis (Linnaeus, 1758) 0 0 0 0 5 2 Pleidae Plea minutissima Leach, 1817 0 0 2 0 0 1, 2 *New records for the Srebarna Nature Reserve perature, air pressure, wind speed, humidity) were lected predictor variables was below the commonly considered as predictors. In the first step for building accepted threshold of 10. In the second step, the vari- the generalized linear model, the selected predictor ables without significant contribution to the model variables were tested for correlation by calculating were omitted stepwise, starting with the least signifi- Spearman correlation matrix using function rcorr cant variable. 3.17-2 in the package Hmisc (Harrell, 2016) and for collinearity using the function vif from the package Results rms (Harrell, 2017). No significant correlation or Species composition and abundance: A total of multicollinearity was detected – the variance of the 4814 individuals of 19 aquatic bug species belonging inflation factor (ranging from 1 to 7.9) for the se- to nine genera and five families were collected dur- 44 Desislava Stoianova ing the study (Table 2). The majority (4589 individu- Influence of environmental variables: During als) was collected using UV light: 4587 of Corixidae all of the light trap sessions the temperature was above (13 species, five genera and two subfamilies) and 14°C and the hourly average wind speed was not more two of Notonectidae (two species, one genus). The than 1.6 m/s (with two exceptions: 5.6 m/s on 5th of remaining 225 individuals, belonging to 11 species June and 4.8 m/s on 17th of June). Corixids were ob- of nine genera and five families, were collected us- served at each of the sampling nights, even when the ing a kick-net (Table 2). Seven species captured using hourly average wind speed was above 4.0 m/s. the light trap were not found in the kick-net samples, According to the performed GLM, the number while four species collected using kick-net were not of collected S. striata increased proportionally with observed in the light trap (Table 2). the decrease of the minimum air temperature in the The majority (97%) of the specimens, collected evening. The model also revealed significant influ- at the light trap, belonged to four species - Sigara stri- ence of the atmospheric pressure and wind speed ata, S. lateralis (Leach, 1817), S. iactans Jansson, 1983, during the light trap sessions on the number of col- Cymatia rogenhoferi (Fieber, 1864). These four spe- lected dispersing S. striata (Table 4). The residuals cies constituted 44%, 32%, 14% and 7% of all aquat- were normally distributed (Fig. 3a) and were equally ic bugs collected at the light trap, respectively. The spread along the predictor ranges (Fig. 3b). numeric dominance of these four species changed The highest numbers of migrating S. striata over the survey nights. On four nights (see Table 3), were collected on two of the nights: 5th and 6th of June S. striata was the most abundant species, represent- with 866 and 1135 observed individuals, respective- ing 39-75% of the collected individuals per night. On ly. These values were 180% and 270% higher than five nights, S. lateralis was the prevailing species and the average S. striata individuals collected per night constituted 51-67% of the individuals per night. On during the study. These were the two nights with the rest two nights of the study, the most numerous the lowest minimum air temperature (18.4°C and species was S. iactans, representing 35% and 39% of 14.2°C) and highest air pressure (1052 mb and 1014 the individuals per night, respectively. mb) recorded during light trap sessions in the study. Sex ratio: Females were dominant for 11 of the On these two nights, maximums of dispersing in- 15 species, collected at the light trap. For S. striata sects were not observed for the rest of the Corixidae and S. iactans the number of females exceeded the species (except for S. lateralis). On 16th of June there number of males during all sampling sessions and was a peak of the flight activity of all four most nu- the sex ratio males:females varied over the study merous species. That night, the numbers of collected from 12:88 to 43:56 and from 33:67 to 46:54, respec- S. striata and S. lateralis were with about 60% and tively. For C. rogenhoferi, the males were dominant these of S. iactans and C. rogenhoferi with over 140% (52:48) on one of the nights, on the rest – females prevailed (sex ratio from 0:100 to 44:56). Females of S. lateralis prevailed at a ratio from 20:80 to 47:53, except for two nights when the ratios were 56:44 and 76:24, respectively. The difference between the number of collected males and females (per session) was significant for S. iactans (V = 55, P = 0.006) and S. striata (V = 66, P = 0.004), and marginally significant for C. rogenhoferi (V = 53, P = 0.01) and S. lateralis (V = 55, P = 0.05). Flight activity by hours: During all sampling ses- sions, most of the individuals (77–100%) were collected in the first hour after sunset – between 21:30 and 22:30 h (Fig. 2). Significant difference between the collected insects from 21:30 to 22:30 h and those collected in the two following hours was detected, respectively: from 22:30 to 23:30 (V = 65, P = 0.002); from 23:30 to 00:30 Fig. 2. Average number of Corixidae collected using the light (V = 66, P = 0.001). The difference in the aquatic bug trap in each of the three hour blocks after sunset. Averages are abundance between the second (22:30–23:30h) and the calculated over all the sample events over 11 nights. Asterisk marks the hour block in which the number of collected corixids third (22:30–23:30h) hour after sunset was marginally is significantly different from the number of corixids collected significant (V = 53, P = 0.011). during each of the two other hour blocks. It is raining bugs: summer dispersal of aquatic bugs (Hemiptera, Heteroptera: Nepomorpha) in Srebarna... 45

Fig. 3. Diagnostic plots for general linear model with a dependent variable the number of S. striata specimens and independent variables recorded during each light trapping session: lowest temperature (°C), average atmospheric pressure (mb), maximal wind speed (m/s): a) normal quantile-quantile plot, b) spread-location plot. higher than their average numbers in the study, re- Dispersing by flight individuals of I. cimicoides and spectively. This was the session with the lowest av- P. minutissima have been reported in very few studies erage wind speed and there was a decrease in the (e. g. Csabai et al., 2006, 2012). Most of the speci- minimal air temperature during this session (21.3°C) mens of I. cimicoides are incapable of flight as their compared to the previous four nights, during which flight muscles are reduced (Brown, 1951). The dis- the minimum temperature for a session raised from persion ability of P. minutissima has not been studied 23.1°C to 26.2°C. in detail yet (Aukema et al., 2002). The prevalence of Corixidae species among the aquatic bugs collected using the light trap is not Discussion surprising as this group has remarkable potential for Species composition and abundance: Nine dispersal by flight (Stonedahl, 1986). The ability to species of Corixidae and two of Notonectidae were move from one habitat to another allows Corixidae found for the first time in the region of the Srebarna species to occupy a wide variety of habitats, including Nature Reserve during the present study. Six of temporary ones (Stonedahl, 1986). Corixidae spe- the corixid species have been reported previously cies differ in their dispersal potential (Macan, 1939; from this wetland (Marinov, 2000; Uzunov et al., Popham, 1964; Benedek & Jászai, 1973; Weigelhofer 2001; Varadinova et al., 2011, 2012) and only two of et al., 1992) and species frequent in temporary habi- them, Sigara falleni (Fieber, 1848) and S. nigroline- tats usually have higher migration rates than those in ata (Fieber, 1848), were not collected at the light trap permanent water bodies (Macan, 1939; Brown, 1951, in the present study. Instead of S. falleni in the sam- 1954; Fernando, 1959; Pajunen & Jansson, 1969b). ples was found its sibling species S. iactans, observed Sigara lateralis and S. striata were the two species mainly in South-eastern Europe (Fent et al., 2011), collected in the greatest numbers during the pre- which could be expected for this region. sent study. Sigara lateralis inhabits mostly temporary Four species were collected using kick-net aquatic habitats and is a migratory species, often ob- but not observed at the light trap: S. nigrolineata, served flying en mass (Fernando, 1959; Popham, 1964; Ilyocoris cimicoides (Linnaeus, 1758), Ranatra lin- Benedek & Jászai, 1973; Macan, 1976; Weigelhofer earis (Linnaeus, 1758) and Plea minutissima Leach, et al., 1992; Boda & Csabai, 2009b). Sigara striata is 1817. All individuals of S. nigrolineata are capable found mostly in permanent water bodies, including of flight. However the females of the summer gen- running waters, and according to Leston (1953), al- erations develop their flight muscles when the egg though the species is commonly found at UV traps, formation is completed (Young, 1965). Flying adult has little tendency to migrate. In the present study, S. individuals of R. linearis have been registered (e.g. striata was very abundant at only two of the nights. Aukema et al., 2002). However, in the kick-net sam- During the rest of the period, on average S. striata ples we found only nymphs of R. linearis. Probably was represented by fewer specimens (71 per night) the study in Srebarna was performed too early for than S. lateralis (122 per night). The current results observation of flying S. nigrolineata and R. linearis. to a great extent confirm the previous observations 46 Desislava Stoianova

Table 3. Number of specimens per night for the four most abundant species in the study.

Species 5 June 6 June 8 June 9 June 11 June 12 June 13 June 14 June 15 June 16 June 17 June S. striata f 410 604 37 85 22 28 24 23 8 184 10 S. striata m 98 249 28 42 6 8 16 3 2 108 6 S. lateralis f 113 79 55 70 55 124 113 94 4 143 8 S. lateralis m 143 50 49 29 32 69 86 70 1 76 25 S. iactans f 28 44 83 39 23 52 25 10 7 84 0 S. iactans m 24 22 48 24 15 36 21 8 4 60 0 C. rogenhoferi f 15 27 22 14 24 5 4 44 2 50 0 C. rogenhoferi m 16 14 3 7 8 4 3 32 0 23 0

Table 4. Results of quasi-Poisson generalised linear models (GLM) exploring factors affecting the abundance ofS. striata in the light trap samples. Explained deviance = 93.1%.

Factors/intercept Estimate Standard error t Pr(>|t|) Min T (°C) -0.29671 0.03972 -7.470 0.000141 ***

Atmospheric pressure (mb) 0.08607 0.01911 4.504 0.002784 **

Max wind speed (m/s) -0.26010 0.06688 -3.889 0.005984 ** Intercept -74.71377 18.89530 -3.954 0.005503 ** *** significance at the 0.001 level, **significance at the 0.01 level of S. lateralis dispersing more actively than S. stria- results could be due to “differential survival-rate of ta (Brown, 1951; Popham, 1964; Benedek & Jászai, the sexes over the winter” (Brown, 1954). Based on 1973; Macan, 1976; Weigelhofer et al., 1992; Boda & data about corixids attracted by light in Hungary, Csabai, 2009b). Nevertheless, flying S. striata could Benedek & Jászai (1973) conclude that there is a de- be observed also in extremely high numbers, at least crease in the ratio males:females towards the end of during short periods. the warmer period of the year (May-October). In the Sex ratio: The sex ratios of dispersing indi- same study, in July the four most numerous species viduals can reveal the relation between reproduc- (S. lateralis, C. rogenhoferi, S. striata, and S. falleni) tive cycle and migration of aquatic insects (Boda & have been represented by more males (up to about Csabai, 2009b), including aquatic bugs. In Corixidae, 80%) than females. Kecső & Boda (2008), contrast- dispersal differences between sexes have been dis- ingly, report female prevalence on almost each of the cussed only for few species (Brown, 1954; Pajunen sampling days in most of the aquatic bugs (including & Jansson, 1969a; Benedek & Jászai, 1973; Kecső S. lateralis) collected using shiny black plastic sheets & Boda, 2008; Boda & Csabai, 2009b). In a study in Hungary. by mark-recapture technique on the dispersal of In the present study, for the first time observa- carinata (Sahlberg, 1819) and Callicorixa tions on the sex ratio of dispersing by flight S. iactans producta (Reuter, 1880), Pajunen & Jansson (1969a) are reported. We registered prevalence of the females report no difference in dispersal activity of the two not only for this species but also for most of the col- sexes. Weigelhofer et al. (1992) used Jermy-type light lected Corixidae species. To a great extent the current trap to study the night migration activity of aquatic paper confirms the observations of Kecső & Boda bugs near the banks of the Danube River in Austria (2008). Sex differences in the developmental rates of and found significant dominance of males over fe- some species could serve as an explanation for the males for Hesperocorixa linnaei (Fieber, 1848). For observed ratio. In a number of corixid species, pop- the rest of the collected species Weigelhofer et al. ulation seasonal changes in the sex ratio have been (1992) has reported no significant deviation from reported (Pajunen & Jansson, 1969b; Aiken, 1982; 1:1 sex ratio. Earlier Brown (1954) reports ratio close Aiken & Malatestinic, 1995; Barahona et al., 2005) to 1:1 between the sexes for migrating corixids col- and, therefore, it is unclear whether the higher num- lected in the autumn, but female prevalence for those ber of females collected in the present study is due to collected in the spring. According to the author, these sex-related differences in dispersal activity or due to It is raining bugs: summer dispersal of aquatic bugs (Hemiptera, Heteroptera: Nepomorpha) in Srebarna... 47 an asymmetric sex ratio of the adult individuals in periods (mostly in the summer). In Bulgaria, C. punc- the population. tata specimens were observed migrating between Flight activity by hours: In Great Britain, an 13:06 and 13:45 from the Dragashka bara River near emigration of corixids was observed in the after- the Dragash Voyvoda Village (Northern Bulgaria, noon: Corixa punctata migrating from a small pond close to the Danube River) on October 25th 2016 (N. between 11:00 and 14:30 h during an unusually Simov in litt.). During a spring day (mid-April 2005), warm September day (Richardson, 1907) and be- around noon, many Corixidae specimens were ob- tween 13:15 and 16:30 h in April (Fernando, 1959), served landing on the surface of a car (metallic dark migration of S. lateralis between 16:30 and 17:30 h in red colour) near State Hunting Area “Voden-Iri a warm day in May (Macan, 1939). Popham (1964) Hissar” (close to the Ostrovo Village, North-eastern describes migration of C. punctata – individuals fly- Bulgaria: N. Simov in litt.). These observations sug- ing off the surface of a pond between 10:00 h and gest that in Bulgaria, during the spring and autumn, 13:30 h, on three consecutive days at the end of the temperatures in the noon hours could be high August. The highest migration rates have been reg- enough to enable corixids to fly. Therefore, during istered between 12:00 h and 13:30 h. In a number of these seasons more intensive migration of corixids studies in Hungary, with the use of polarising surfac- could be expected at midday. es for attraction and sampling carried out between Influence of environmental variables: March and July (or later) during a twenty-four-hour According to Popham (1964), corixids move between period every week, most specimens of all observed habitats exclusively during periods with little or no corixid species (except S. lateralis) were collected in wind. In recent studies, migration of aquatic beetles the evening hours around sunset (Csabai et al., 2006; and bugs (Csabai & Boda, 2005) and of S. lateralis Boda & Csabai, 2009a, 2009b, 2013; Csabai et al., (Boda & Csabai, 2009b) has not been observed dur- 2012). Most specimens of S. lateralis, similarly, were ing periods with wind speed above 3.3 m/s and 3.1 collected in the evening at 21:00, but also a local peak m/s, respectively. The occurrence of wind with speed in the morning was observed (Csabai et al., 2012). from 1.6 to 3.3 m/s and from 0.55 m/s to 3.1 m/s was In accordance with the described above pattern of negatively correlated with the number of collected corixids’ flight activity (Csabai et al., 2012), we ob- migrating aquatic bugs and beetles (Csabai & Boda, served maximal dispersal immediately after sunset 2005) and S. lateralis (Boda & Csabai, 2009b), respec- (between 21:30 h and 22:30 h) and it was followed tively. The authors explain the lower threshold for S. by a rapid decrease through the next two hours. The lateralis with higher sensitivity of smaller species to rare stragglers later during the night confirm the the effect of wind speed (Boda & Csabai, 2009b). observation of Boda & Csabai (2009a, 2009b) that In the present study, corixids (including S. lat- dispersing individuals could be observed also by eralis) were observed even when the hourly average moonlight during the night. However, in the present wind speed was higher (5.6 m/s) than the threshold study the numbers of the individuals collected dur- values observed in the above-cited studies (Csabai & ing the darker collecting period were very low. The Boda, 2005; Boda & Csabai, 2009b). Nevertheless, hour after sunset coincides with one of the three pe- the best fitted GLM confirmed the previous results riods (around nightfall, mid-morning, around noon) (Popham, 1964; Csabai & Boda, 2005; Boda & Csabai, optimal for positively polarotactic aquatic insects to 2009b) by connecting the decrease in the wind speed disperse and detect new aquatic habitats (Csabai et with an increase of the collected migrating S. striata. al., 2006). The flight activity of Corixidae could be Temperature also could significantly influ- strongly influenced by the insect’s ability to tolerate ence corixids’ flight initiation and dispersal activ- desiccation (Oloffs & Scudder, 1966 after Stonedahl, ity (Popham, 1964; Weigelhofer et al., 1992; Boda & 1986). At high air temperatures water loss could be Csabai, 2009b). Popham (1964) suggests that corix- especially rapid because of instability of the cuticular ids initiate flight only when the surrounding tem- wax layer (Oloffs & Scudder, 1966 after Stonedahl, perature exceeds a minimum value. For example, S. 1986). In the morning and at nightfall, usually air lateralis and S. nigrolineata fly out of the water when temperature is low and humidity is high, while, at its temperature is at least 12°C and S. falleni and C. noon, usually air temperature is maximal and hu- praeusta when it is at least 15°C. On the banks of the midity is low (Csabai et al., 2006). As higher humid- Danube River in Austria, in a Jermy type light trap ity is advantageous for flying aquatic insects, due to no Corixidae were collected at nights with average the reduced risks of dehydration, dawn and dusk are air temperatures below 12.2°C (Weigelhofer et al., optimal for flight (Csabai et al., 2006) during warm 1992). In the same study, positive correlation be- 48 Desislava Stoianova tween air temperature and the number of collected mens could be collected at nights with relatively low corixids has been detected. A study in Hungary, con- air temperatures, higher atmospheric pressure and trastingly, shows a negative correlation between the lower maximal speed of the wind (compared to the air temperature and the number of S. lateralis attract- previous or the following couple of nights). ed to polarizing surfaces (Boda & Csabai, 2009b), Efficiency of the UV light trap method: In the but in agreement with Weigelhofer et al. (1992) also present study, seven of the 11 new for the studied area in Hungary migrating individuals were not observed species, were found only in the light trap catch (dis- bellow 12.98°C. persing individuals), but not in aquatic habitats, sam- During each of the light trapping sessions in pled by hybrobiological net earlier (Marinov, 2000; the present study, the temperature was above 14°C Uzunov et al., 2001; Varadinova et al., 2011, 2012) or and corixids were observed on each of the sam- during the study. Before including these seven species pling nights. In accordance with Boda and Csabai to the Heteroptera fauna list of the Srebarna Nature (2009b) the best fitted GLM shows that a decrease Reserve, an additional study of aquatic bugs from in the minimum air temperature during the three aquatic habitats in the studied area is needed. Light hours after sunset could result in an increase of the trapping could be very useful for phenological stud- dispersing S. striata. During periods with high tem- ies as it gives a solid proof of adult corixids’ presence peratures, Corixidae could be dispersing more in- during the sampling period. In studies on the biodi- tensively on cooler nights to minimize water loss. versity of wetlands, light trapping could give a rough Campbell (1979) mentions similar influence of idea about the corixid fauna of the habitats drying out temperature on dispersal of Trichocorixa vertica- in the studied region (Popham & Lansbury, 1960); lis (Fieber, 1851) – an invasive corixid species for therefore it could be an appropriate addition to the Europe. sampling in aquatic habitats. In the present study, the highest numbers of S. striata have been collected on the two nights with the Acknowledgements: The author wishes to thank Merlijn Jocque highest atmospheric pressure, registered per session. (Royal Belgian Institute of Natural Sciences) for providing mate- The GLM confirms that an increase in the atmos- rial and the environmental data used in this study and to Patri- cia Caballero for the dedicated help with light trapping. Mer- pheric pressure could result in increase in the num- lijn Jocque was a WETLANET fellow (FP7 CAPACITIES Grant ber of the migrating S. striata. 229802). Thanks to Nikola Draganov and his wife for allowing According to the present study, corixids could the use of their garage roof for light trapping. Special thanks to disperse also in periods when wind speed exceeds PhD Merlijn Jocque, prof. Snejana Grozeva (IBER-BAN) and the previously observed thresholds (Csabai & Boda, anonymous reviewer for the valuable comments on the manu- script, and also to Nikolay Simov (National Museum of Natu- 2005; Boda & Csabai, 2009b). It could be speculat- ral History in Sofia) for sharing his observations of migrating ed that during warm periods more S. striata speci- Corixidae from two locations in Bulgaria.

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Rapid expansion of the Oak lace bug Corythucha arcuata (Say, 1832) (Hemiptera: Tingidae) in Bulgaria

Nikolay Simov1, Snejana Grozeva2, Mario Langourov1, Margarita Georgieva3, Plamen Mirchev3, Georgi Georgiev3

1National Museum of Natural History, Bulgarian Academy of Sciences, 1 Tsar Osvoboditel Blvd., 1000 Sofia, Bulgaria; E-mail: [email protected]; [email protected] 2Institute of Biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 1 Tsar Osvoboditel Blvd., 1000 Sofia, Bulgaria; E-mail: [email protected] 3Forest Research Institute, Bulgarian Academy of Sciences, 132 St. Kl. Ohridski Blvd., 1756 Sofia, Bulgaria; E-mails: [email protected]; [email protected]; [email protected]

Abstract: New records, host associations, damages on and the potential threat of alien oak lace bug (Corythucha arcuata) to native forests in Bulgaria are reported and briefly discussed.

Key words: Corythucha arcuata, host plants, new localities, spreading

Introduction Materials and Methods The oak lace bug, Corythucha arcuata The field studies were conducted in the period (Say, 1832) (Heteroptera: Tingidae), is of North 2015-2017. Many visual observations of infested oak American origin and is widely distributed in the trees were performed within the ESENIAS-TOOLS United States of America and the southern part and TUNESinURB project activities. The biologi- of Canada. It is an invasive species in Europe and cal material was collected using an entomological has been firstly recorded in Italy (Bernardinelli & beating sheet and by hand – after searching leaves Zandigiacomo, 2000) and Switzerland (Forster et of infested host trees or hibernating places in bark al., 2005). Corythucha arcuata has spread to a large crevices or under tree bark. Damages, adult in- part of Turkey (Mutun et al., 2009) and it was ex- sects, nymphs and eggs were photographed with a pected the alien species to reach Bulgaria in a short Panasonic Lumix DMC-FZ200 and Olympus E-30 time (Simov et al., 2012). In 2012, the oak lace bug cameras. was found for the first time on the Balkan Peninsula in Plovdiv City and Zlati dol Vill. near the town of Results and Discussion Simeonovgrad (Dobreva et al., 2013). In the next During the study period, C. arcuata was observed in many few years, the species penetrated in many regions of new localities in Bulgaria. the country (Georgiev et al., 2017). Material examined: Burgas District: The present paper is a continuation of a previ- Primorsko Town, 26 m a.s.l., 42.24620°N, ous study of alien true bugs in Bulgaria and summa- 027.75087°E, host Quercus frainetto Ten., Q. ries data on the rapid expansion of C. arcuata in the hartwissiana Steven, Q. cerris L., 08.10.2016, G. country. 52 Nikolay Simov, Snejana Grozeva, Mario Langourov, Margarita Georgieva, Plamen Mirchev, Georgi Georgiev

Georgiev, P. Mirchev, M. Georgieva obs.; Kiten Vill., 166 m a.s.l., 42.12167°N, 024.52228°E, host Town, 34 m a.s.l., 42.23610°N, 027.77933°E, host Q. robur, Castanea sativa Mill., 15.07.2016, G. Q. frainetto, 09.10.2016, G. Georgiev, P. Mirchev, Georgiev, P. Mirchev, M. Georgieva obs.; Trilistnik M. Georgieva obs.; Malko Tarnovo Town, 337 m Vill., 161 m a.s.l., 42.22228°N, 024.86248°E, host Q. a.s.l., 41.97931°N, 027.53238°E, host Q. frainetto, pedunculiflora K.Koch, 27.07.2016, N. Simov, M. Q. hartwissiana, Q, cerris, 10.10.2016, G. Georgiev, Langourov, R. Bekchiev obs.; Plovdiv Town, Greben P. Mirchev, M. Georgieva obs.; Brashlyan Vill., Chanel, 165 m a.s.l., 42.143472°N, 024.71014°E, 240 m a.s.l., 42.045659°N, 027.426628°E, host host Q. robur, 06.08.2016, S. Grozeva obs.; Plovdiv Q. polycarpa Schur, 08.08.2016, S. Grozeva obs.; Town, Bunardzhika Hill, 180 m a.s.l., 42.146104°N, Haskovo District: Simeonovgrad Town, 89 m a.s.l., 024.740166°E, host Q. robur, 06.08.2016, S. Grozeva 42.0312°N, 025.8265°E, host Q. robur L., 26.06.2016, obs.; Blagoevgrad District: Sandanski Town, 262 S. Grozeva leg.; near Simeonovgrad Town., 99 m m a.s.l., 41.34194°N, 023.17061°E, host Q. petraea, a.s.l., 42.048243°N, 025.872616°E, host Q. robur, 28.08.2016, G. Georgiev, P. Mirchev, M. Georgieva 20.11.2015, S. Grozeva leg.; Svilengrad Town, 58 obs.; Gotse Delchev Town, 538 m a.s.l., 41.34227°N, m a.s.l., 41.774558°N, 026.145344°E, host Q. robur, 023.44058°E, host Q. pubescens Willd., Q. robur, 27.06.2016, S. Grozeva leg.; Harmanli Town, 75 29.08.2016, G. Georgiev, P. Mirchev, M. Georgieva m a.s.l., 41.89095°N, 025.965609°E, host Q. robur, obs.; Gotse Delchev Town, Park in the center of the 27.06.2016, S. Grozeva leg.; west of Brod Vill., 140 town, 510 m a.s.l., 41.573392°N, 023.736502°E, host m a.s.l., 42.063854°N, 025.66100°E, host Q. robur, Q. pubescens, Q. robur, 16.10.2015, S. Grozeva obs.; Q. petraea (Matt.) Liebl., 21.06.2016, N. Simov obs.; ibid., 02.07.2016, N. Simov obs.; west of Blatska Vill., District: Kardzhali Town, 275 m a.s.l., 516 m a.s.l., 41.536184°N, 023.876637°E, host Q. pube- 41.38371°N, 025.22406°E, host Q. cerris, Q. petraea, scens, 03.08.2015, N, Simov obs.; Sofia District: Sofia 18.08.2016, G. Georgiev, P. Mirchev, M. Georgieva City, 550 m a.s.l., 42.694398°N, 023.336582°E, host obs.; Yambol District: Topolovgrad Town, 320 m Q. robur, 01.06.2017, N. Simov obs.; Sofia City, 550 a.s.l., 42.077351°N, 026.324859°E, host Quercus sp., m a.s.l., 42.685744°N, 023.335938°E, host Q. robur, 08.08.2016, G. Georgiev, P. Mirchev, M. Georgieva 21.06.2017, S. Grozeva obs.; Sofia City, 556 m a.s.l., obs.; Sliven District: Sliven Town – park in the 42.694707°N, 023.33667°E, host Q. robur, 11.09.2016, town, 243 m a.s.l., 42.680516°N, 026.317874°E, host S. Grozeva obs.; Sofia City, 556 m a.s.l., 42.694697°N, Q. robur L., 30.08.2015, S. Grozeva leg.; Stara Zagora 023.33667°E, host Q. robur, 11.11.2017, N. Simov District: north of Gurkovo Town, 310 m a.s.l., obs.; Pleven District: near Koilovtsi Vill., 177 m a.s.l., 42.66050°N, 025.77243°E, host Q. cerris, 27.10.2015, 43.48032°N, 024.73766°E, host Q. robur, 23.10.2015, N. Simov obs.; east of Nikolaevo Vill., 285 m a.s.l., N. Simov obs.; Belene Town, 26 m a.s.l., 43.64133°N, 42.630158° N, 025.829975°E, host Q. cerris, Q. robur, 025.12346°E, host Quercus sp., 24.10.2015, N. Simov 27.10.2015, N. Simov obs.; Zhrebchevo Dam, 287 obs.; Ruse District: west of Obretenik Vill., 161 m m a.s.l., 42.57736°N, 025.88972°E, host Q. frainet- a.s.l., 43.57083°N, 025.75651°E, host Q. robur, Q. to, 27.10.2015, N. Simov obs.; Plovdiv District: frainetto, 26.10.2015, N. Simov obs.; Ivanovo Vill., Manole Vill., 157 m a.s.l., 42.10096°N, 024.55540°E, 117 m a.s.l., 43.69156°N, 025.95144°E, host Q. cerris, host Q. robur, 10.06.2016, G. Georgiev, P. Mirchev, 26.10.2015, N. Simov obs.; Batakliata hunting area, M. Georgieva obs.; Kalekovets Vill., 179 m a.s.l., 200 m a.s.l., 43.64582° N, 026.11861°E, host Q. cerris, 42.14202°N, 024.49163°E, host Q. robur, 15.07.2016, Q. robur, 26.10.2015, N. Simov obs.; Veliko Tarnovo G. Georgiev, P. Mirchev, M. Georgieva obs.; Trilistnik District: east of Polski Trumbesh Vill., 37 m a.s.l.,

Table 1. Host plants of Corythucha arcuata in Bulgaria

Hosts with restricted distribution in Common hosts with massively found symptoms Occasional hosts Bulgaria Quercus robur L. Castanea sativa Mill. Lysimachia punctata L. Quercus petraea (Matt.) Liebl. Rosa canina L. Quercus pubescens Willd. Rubus caesius L. Quercus cerris L. Rubus sp. Quercus frainetto Ten. Acer platanoides L. Quercus hartwissiana Steven Quercus pedunculiflora K.Koch Quercus polycarpa Schur Rapid expansion of the Oak lace bug Corythucha arcuata (Say, 1832) (Hemiptera: Tingidae) in Bulgaria 53

Fig. 1. Recorded localities of Corythucha arcuata in Bulgaria. Semicircles – first records in 2012, black circles – new records 2015-2017.

43.37957°N, 025.65186°E, host Q. robur, 27.10.2015, Quercus species (Fig. 2A), the oak lace bug was also N. Simov obs.; Gorsko Kalugerovo Vill., 200 m established to develop on sweet chestnut, Castanea a.s.l., 43.111531°N, 025.274208°E, host Q. robur, sativa (Fig. 2B). During hibernation, the species was 25.06.2016, S. Grozeva obs.; Momin sbor Vill., 220 found under bark and in bark crevices of Q. robur m a.s.l., 43.087834° N, 025.496340°E, host Q. robur, and Pinus sylvestris L. Among the occasional hosts 25.06.2016, S. Grozeva obs.; Voneshta Voda Vill., 420 of the species in Bulgaria, Lysimachia punctata, Rosa m a.s.l., 42.876428°N, 025.637565°E, host Q. robur, canina, Acer platanoides and Rubus caesius (Fig. 2C) 25.06.2016, S. Grozeva obs.; Voneshta Voda Vill., 410 were recorded. In Slovenia, C. arcuata was also found m a.s.l., 42.876216°N, 25.637647°E, host Q. robur, on other host plants: Malus sylvestris and Ulmus spp. 01.09.2015, S. Grozeva obs.; Voneshta Voda Vill., (Jurc & Jurc, 2017). 401 m a.s.l., 42.87836°N, 25.64047°E, host Q. robur, Five years after the first record on the Balkan Lysimachia punctata L., Rosa canina L., Rubus cae- Peninsula, the oak lace bug has invaded most of sius L., 27.10.2015, N. Simov obs.; Sevlievo District: Bulgaria. The species has spread rapidly, occupying south of Dobromirka Vill., 385 m a.s.l., 43.061900°N, urban areas and oak forests in the country. In the 025.286349°E, host Q. robur, 17.08.2016, N. Simov case of heavy infestation, the oak trees turn yellow in obs.; Razgrad District: Loznitsa Vill., 220 m the middle of the summer and lose their leaves ear- a.s.l., 43.362905°N, 026.605182°E, host Q. cerris, lier than usual (Fig. 2D). In heavy attacked trees in 02.08.2017, N. Simov obs. mid-July about all of the leaves suffer damage due to The localities of the oak lace bug in Bulgaria C. arcuata feeding activity. About 85% of the leaves (Fig. 1) are situated in the lowland and hill zone of display discoloration, that can be spread over half of the country, in the belt of xerothermic oak forests up the leaf surface (Fig. 2E). The high population den- to 600-700 m a.s.l. sity of the oak lace bug appears to be the major threat In this study, 14 tree, shrub and herbaceous to the native sucking insects in oak forests, such as species were detected as common or occasional hosts honeydew producers, especially in the Strandzha of C. arcuata in Bulgaria (Table 1). Besides eight Mt. (Georgiev et al., 2008). Corytucha arcuata causes 54 Nikolay Simov, Snejana Grozeva, Mario Langourov, Margarita Georgieva, Plamen Mirchev, Georgi Georgiev

Fig. 2. Host plants of Corythucha arcuata in Bulgaria and impact on them: A – C. arcuata on Quercus robur; B – C. arcuata on Castanea sativa; C – C. arcuata on Rubus caesius; D – Strongly damaged Q. pedunculiflora stand in the beginning of July; E – heavy leaf discoloration due to C. arcuata feeding activity; F – strongly attacked solitary Q. robur trees; G – strongly attacked solitary Q. fainetto trees; I, J – strongly attacked one-year-old oak seedlings. Rapid expansion of the Oak lace bug Corythucha arcuata (Say, 1832) (Hemiptera: Tingidae) in Bulgaria 55 strong damages to oak trees in urban green infra- Russia (Neimorovats et al., 2017). Almost all of our structure, as well (Fig. 2F). In forest stands, the highly records are close to the main European roads E-80, attacked young oak seedlings are particularly threat- E-79, E-85, E-87,and this fact supports our hypoth- ened (Fig. 2I, J). Castanea sativa in the Belasitsa Mt. esis of human mediated dispersal mechanism of oak has not yet been attacked by the pest. However, the and sycamore lace bugs in Bulgaria as stowaways chestnut stands in the region are in poor health con- (Simov et al., 2012; Dobreva et al., 2013). dition due to the negative impact of Cryphonectria parasitica (Murrill.) Barr. (Georgieva et al., 2013) Acknowledgments: The study was supported by the Financial and, therefore, are potentially threatened during fu- Mechanism of the European Economic Area (2009-2014), Pro- ture calamities of C. arcuata. gramme BG03 Biodiversity and Ecosystem Services: Project ‘East The expansion of the oak lace bug is already and South European Network for Invasive Alien Species – A tool to registered in Turkey (Mutun, 2003; Mutun et al., support the management of alien species in Bulgaria’ (ESENIAS- 2009; Küçükbasmacı, 2014), Croatia (Hrašovec et al., TOOLS), D-33-51/30.06.2015; Project ‘Improving the Bulgarian Biodiversity Information System’ (IBBIS), D-33-72/20.07.2015; 2013; Nikl, 2017), Serbia (Pap et al., 2015), Project ‘Toward better understanding of ecosystem services in ur- (Chireceanu et al., 2017), Slovenia (Jurc & Jurc, ban environment through evaluation and mapping of ecosystem 2017), Hungary (Csepelényi et al., 2017a, b) and services, (TUNESinURB), D-33-82/14.08.2015.

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