New Data on Alien Insect Pests of Ornamental Plants in Bulgaria

Home , Euxinograd, Metcalfa pruinosa, Phoenicococcidae

FORESTRY IDEAS, 2016, vol. 22, No 1 (51): 17–33 NEW DATA ON ALIEN INSECT PESTS OF ORNAMENTAL PLANTS IN BULGARIA

Aneliya Penchevа1* and Mariya Yovkova2 1Department of Plant Pathology and Chemistry, Faculty of Ecology and Landscape Architecture. University of Forestry. 10 St. Kliment Ohridski Blvd., 1756 Sofia, Bulgaria. *E-mail: [email protected] 2Institute of Ornamental Plants – 1222 Sofia, Negovan, Bulgaria. E-mail: [email protected]

Received: 04 December 2015 Accepted: 17 February 2016

Abstract In this study, the results of recent surveys (during the period between 2012 and 2015) on alien insects infesting ornamental plants in Bulgaria are reported. Fourteen species, associated with urban landscape areas and indoor plants, are discussed. Two of them, Ceroplastes sinensis Del Guercio and Lepidosaphes flava (Signoret), are reported for the first time in Bulgaria. Furthermore, Acizzia jamatonica (Kuwayama), Ceroplastes ceriferus (Fabricius), Pseudaulacaspis pentagona (Targioni Tozzetti) and Cydalima perspectalis (Walker) have been found in new localities. Metcalfa pruinosa Say has widened its host range in Bulgaria. Additional distribution data are also provided about Aulacaspis yasumatsui Takagi and Cacoecimorpha pronubana (Hübner). Details on current status, host plants, zoogeographical origin and probable pathways of introduction into Bulgaria are reported for each species. Morphological and biological remarks are given for C. perspectalis and C. sinensis. Key words: box tree moth, Chinese wax scale, De Stefan scale, new pests, scale insects.

Introduction as one of the main factors that lead to a decline in regional biodiversity (FAO 2003, In recent years, due to the active market- Chornesky et al. 2005). ing of ornamental plants and plant mate- As far as phytophagous insects are rial, a large number of non-native insects concerned, more than 25 alien species have penetrated in different continents have been recorded as new pests in the and countries. After introduction into a last decade in Bulgaria (Beshkov et al. new area, they may become acclimatized, 2015, Doychev 2015, Pencheva et al. surviving outdoors. In some cases these 2014, Tomov and Trencheva 2013, Yovko- are very harmful species. They not only va et al. 2013, Yovkova et al. 2015). About cause significant damage to ornamental two thirds of them are ornamental plant plants, reduce their aesthetic and mar- pests and may cause significant damage ket values but also may threaten the na- to cultivated plants both in Bulgaria and tive flora. Thus, their invasion becomes a across Europe. Their unexpected massive global environmental problem regarded appearance in urban habitats is attributed 18 A. Penchevа and M. Yovkova mainly to the introduction and distribution Bulgaria (Fig. 1). Part of the biological ma- of infested plant materials. terials was provided by different specialists The aim of the present study was to in- working in urban parks or in nurseries. vestigate the current status and distribution During the visual inspection of orna- of alien insect recently reported as pests on mental plants, infested plant parts (twigs or ornamentals in Bulgaria, as well as old in- leaves) and insects on them were collected vaders whose populations are increased in and placed separately into plastic bags or in the last years. The survey results will con- 70 % alcohol for further examination in the tribute to get acquainted with alien insect’s laboratory. For each insect’s sample, origin distribution and have a practical application, of infested host plants or pathways of their benefiting producers of ornamental plants. introduction were checked. The surveys were carried out during the active phase of the insects’ life, namely from May to Oc- Materials and Methods tober. Caterpillars of the lepidopteran pest species were reared to adults under labo- The survey was conducted over a period of ratory conditions. Scale insect specimens four years, between 2012 and 2015. Several were mounted for light microscopy accord- localities with ornamental plants (city/urban ing to the procedure detailed by Kosztarab parks, private gardens, ornamental nurser- and Kozár (1988). The species found in ies, greenhouses, garden centres and col- Bulgaria for the first time were identified us- lection in botanical gardens) were surveyed. ing the keys of Danzig (1993), Gimpel et al. They were located in various regions of (1974) and Fetyko and Kozár (2012). The

Fig. 1. Regions and locations in Bulgaria where alien insect pests included in this study were established. New Data on Alien Insect Pests... 19 identification of Ceroplastes ceriferus was Results and Discussion confirmed by J. F. Germain, Plant Health Laboratory, Montpellier, France. The col- Fourteen alien insects associated with lected specimens are preserved in the de- urban green areas were identified in dif- partment of Plant Pathology and Chemistry ferent regions of Bulgaria during the pre- at the University of Forestry, Sofia. sent study (Table 1). They belong to two Table 1. List of surveyed alien pests. First record No Alien insect pest Established localities Type of localities Origin in Bulgaria Petrich, Balchik, Shabla Outdoors (private Metcalfa pruinosa – 2014; Nessebar, 1 2007– Plovdiv gardens and city North America Say Balchik and Varna – parks) 2015 Acizzia jamatonica 2009 – Sofia – 2014; Outdoors (private 2 East Asia (Kuwayama) Nessebar Nessebar – 2015 gardens) 2009 – Outdoors (private Mediterranean 3 Trioza alacris Flor. Aheloy – 2012–2015 Ahtopol gardens) origin

Central and Elatobium abieti- 2014 – nearby Not found in its previous Outdoors in private 4 Northern num (Walker) Sofia localities gardens Europe

Icerya purchasi Indoors in garden 5 1968 – Sofia Ravda – 2012–2015 Australia Maskell centres Phenacoccus Indoors in garden South America 6 peruvianus 2010 –Ravda Ravda – 2013–2014 centres and green- (Argentina, Granara De Willink houses Peru)

Ceroplastes cer- Nessebar – 2012 and Outdoors (private 7 2011 – Vidin Neotropical iferus (Fabricius) 2013; Sozopol – 2015 gardens) Outdoors (private Ceroplastes 8 2007 – Sofia Ravda – 2014 gardens and garden Eastern Asia japonicus Green centres) Ceroplastes sinen- Indoors (garden Central or South 9 New record Nessebar – 2013 sis Del Guercio centres) America Indoors (green- Aulacaspis yasu- 2009 – Sofia and Sunny Beach 10 houses and garden Southeast Asia matsui Takagi Tsarevo – 2013; Ravda – 2014 centres) Near East and Lepidosaphes Sofia, 2012 Indoors and garden 11 New record Mediterranean flava (Signoret) Burgas, 2013 centres Palaearctic 1968 – Plovdiv, 2013; Sofia, Outdoors (private Pseudaulacaspis Petrich, 2012–2015; Balchik gardens, city parks 12 pentagona Eastern Asia Sandanski, – 2014; Sunny Beach – and botanical gar- (Targioni Tozzetti) Kulata 2013 dens) Cacoecimorpha Outdoors and Ravda, Burgas, Aheloy – Mediterranean 13 pronubana 2009 – Aheloy indoor (garden 2012–2015 region (Hübner) centres) Dragalevtsi, Dobrich – Outdoors (private Cydalima perspec- 2014 – 2014; Burgas, Plovdiv, 14 gardens and city Asia talis Walker Balchik Primorsko, Sofia, Kalofer parks) – 2015 20 A. Penchevа and M. Yovkova orders (Hemiptera and Lepidoptera) and pruinosa mainly infested weeds, including 8 families. Half of them are scale insects Marsdenia erecta (L.) R. Br. and Clematis (Coccoidea), which are able to spread vitalba L. (around Nessebar), and only in easily with infested plant materials, be- Petrich the insect was found on a single cause of their small size and cryptic be- Catalpa bignonioides tree. haviour. Details on detected species are The North-American planthopper M. given further down. pruinosa was accidentally introduced into Metcalfa pruinosa (Say, 1830) [He- Europe (first in Italy), and subsequently miptera, Flatidae] – citrus flatid planthop- caused economic damage to orchards per. and vineyards in some South-European Collected material: 2014: 20 July – countries (Strauss 2010). In Bulgaria it Petrich; 26 August – Balchik and Shabla; was first detected in 2004 on Thuja oc- 2015: 15 July – Ravda and Nessebar; 20 cidentalis L. at a locality near Plovdiv August – Balchik and Varna. (Trenchev et al. 2007). The planthopper In August 2014, in Balchik Botanical is gregarious and extremely polyphagous garden M. pruinosa had infested more species. According to some authors it may than 45 herbaceous, ornamental and fruit feed on 200 to 300 plant species (Soulio- plant species (Fig. 2). The most infested tis et al. 2008, Grozea et al. 2011). Three trees and shrubs were: Acer platanoides of infested plants species determined in L., A. campestre L., Broussonetia papy- Balchik – Lonicera maacki (Rupr.) Herder, rifera (L.) Vent., Catalpa bignonioides Securinega suffruticosa J. F. Gmel. and Prints, C. speciosa Prints, Cornus mas L., Cephalotaxus harringtonia (Knight ex J. Diospyros kaki Thunb., Fraxinus excelsior Forbes) K. Koch – have probably not been L., Ficus carica L., Hibiscus syriacus L., recorded earlier as hosts of M. pruinosa. Parthenocissus tricuspidata (Siebold & This species overwinters as eggs in- Zucc.) Planch., Philadelphus coronarius L. serted in woody tissue or under tree bark. and Vitis vinifera L. The population density The first nymphs were found on the leaves of citrus flatid planthopper was consider- and stems in the beginning of May. The to- ably lower in 2015, but number of infested tal development period of the larval stages host plants increased. At other sites M. takes an average of 42 days (Lucchi and

a b Fig. 2. Metcalfa pruinosa: adults (a) and signs of pest infestation to Cornus mas (b). New Data on Alien Insect Pests... 21

a b Fig. 3. Psyllids: a – white wax on a leaf of Albizia julibrissin excreted by nymphs of Acizzia jamatonica; b – nymphs and gall of Trioza alacris on a leaf of Laurus nobilis. Santini 1993). Nymphs surround them- rals of white wax on the leaves (Fig. 3a). selves with long, waxy filaments, which The damage caused by A. jamatonica protect them from their copious honeydew was substantial and associated with leaf (Fig. 2b). In 2015 adults were present in discoloration and premature leaf drop. all localities from the beginning of July to The following year (2015) the infested tree the end of September. Besides infested died, probably due to bark necrosis. In the plants, M. pruinosa could be transported middle of July 2015, psyllid nymphs were over long distances on vehicles, which also found around Nessebar. often park along the roadsides near food A. jamatonica is native to East Asia, plants of the pest. Local invasion of the but has rapidly increased its geographi- surrounding area follows and is facilitated cal distribution during the last decade, be- by the presence of uninterrupted belts of coming established in Europe and North host trees and shrubs (Pantaleoni 1989). America (Mifsud et al. 2010). It develops The protected waxy cover of the citrus on Albizia spp. and is most commonly flatid planthopper, the way it spreads and recorded on A. julibrissin. The first occur- its adaptability, are factors that lead to the rence of A. jamatonica in Bulgaria was in development of the species in large pop- July 2009 in Nessebar (Vétek and Rédei ulation density during the last 4 years in 2009). Since then, the insect has rapidly Bulgaria. spread in South-eastern Bulgaria and par- Acizzia jamatonica (Kuwayama, ticularly in the coastal areas (Harizanova 1908) [Hemiptera, Psyllidae] – albizia et al. 2012). psyllid. Trioza alacris Flor, 1861 [Hemiptera, Collected material: Simeonovo (near- Triozidae] – laurel psyllid. by Sofia) – 25 September 2014; Nessebar Collected material: Aheloy, during May – 16 July 2015. – August in 2012 – 2015. In September 2014, psyllid nymphs The abundant leaf galls on Laurus no- and adults were collected on a young bilis L. (used as a hedge), laurel psyllid (about 6–7-year-old) solitary silk tree adults and nymphs have been detected (Albizia julibrissin Durazz.) located on from April to October since its first appear- a private property nearby Sofia. Psyllid ance in 2009 (Pencheva et al. 2009). At nymphs had excreted honeydew and spi- present T. alacris is limited to a locality sit- 22 A. Penchevа and M. Yovkova uated at a private property in Aheloy and has not been found in Bulgaria and why it since 2009 it has hibernated successfully disappeared so quickly remains open, es- for about 6 years. It is suspected that the pecially taking into account that the Picea laurel psyllid has been introduced in Bul- species are often used in landscaping and garia on imported plants originating from in forest wood production and are periodi- the Netherlands. cally investigated. Due to the lack of data The species is most likely of Mediterra- on the presence of Elatobium abietinum in nean origin but was introduced to Central neighbouring countries (Turkey, Greece, and Northern Europe on cultivated bay FYR of Macedonia and Serbia) where, laurel (Mifsud et al. 2010). Generally it de- like in Bulgaria, the aphid’s fauna is com- velops on L. nobilis, but is also reported paratively well investigated, and due to its on L. azoricus (Seub.), producing charac- very local appearance only near Sofia, it teristic large leaf galls by rolling down leaf can be concluded that the green spruce margins (Fig. 3b). T. alacris has two to five aphid was probably introduced into Bul- broods in the year according to the weath- garia via imported infested Picea plants. er (Ossiannilsson 1996), the last one ma- Icerya purchasi Maskell, 1878 [He- turing in the end of October. Its chemical miptera, Monophlebidae] – cottony cush- control is difficult because of the lavishly ion scale. waxy secretion covering the nymphs. Collected material: Ravda: 20 July Elatobium abietinum (Walker, 1849) 2011 and 25 October 2015; Burgas – [Hemiptera, Aphididae] – green spruce 20 May 2015. aphid. During the present study, dense colo- Collected material: 20 April 2014 – nies of cottony cushion scale nymphs nearby Sofia. and adult females have been registered The green spruce aphid was detected on Pittosporum tobira (Thunb.) W. T. Ai- for the first time in April 2014 on three pri- ton, Citrus lemon (L.) Burm, Laurus nobi- vate properties nearby Sofia – Bistritsa, lis, Parrotia persica (DC.) C. A. Mey and Pancharevo and Dragalеvtsi. Dense colo- Liquidambar styraciflua L. (Fig. 4a) in two nies of larvae and apterae females have garden centres in Ravda and in green- been registered on the branches of Picea houses in Burgas. In both locations the abies (L.) Karst. and P. pungens Engelm. host plants were just imported from Italy. The damage to infested plants was sig- I. purchasi was found for the first time in nificant and has led to needle necrosis Bulgaria in 1968, when it was recorded as and premature needle drop (Yovkova et an important pest in the Botanical garden al. 2015). Further observations conducted in Sofia, affecting Acacia spp., Magnolia during growing season in 2015, the aphid sp. and other 4 ornamentals (Tsalev 1968). was not found in either the previous or in Although this species was not detected any of the other aforementioned detected in the following investigations (carried out locations. from 1990 to 1995 in ornamental green- According to Carter and Halldórsson houses) (Pencheva 1995), it has appeared (1998) and CABI (2015a), E. abietinum periodically in garden centres in the last 10 originates from Central and Northern years because of the intensive trade of or- Europe. It is distributed throughout Eu- namental plants (Pencheva 2007). rope (Blackman and Eastop 2015, CABI The cottony cushion scale is an Aus- 2015a). The question why this species still tralian species but now is widespread New Data on Alien Insect Pests... 23

a b Fig. 4. Scale insects: Adult females of Icerya purchasi on Parrotia persica (a) and Phenacoccus peruvianus (b). throughout the world. It has a wide climatic 2014), this species was first detected in tolerance and has become established in May 2010 on the same hosts. Southern Europe and in greenhouses of The mealybug is of Neotropical origin temperate regions. I. purchasi is extreme- (Argentina, Peru) and was recorded to ly polyphagous pest and infested more Europe (Spain) in 1999, prior being de- than 180 plants belonging to 66 families scribed by Granara de Willink. Since then (García et al. 2015). Once introduced into P. peruvianus has been found in different glasshouses, it may become a significant European countries (Sicily, Italy, Corsica, risk for production of ornamentals in Bul- Croatia, Portugal, Monaco, France and garia, because of its ability to rapid distri- Greece) (Beltrà еt al. 2010, Gkounti and bution. The cottony cushion scale spreads Milonas 2013, Masten еt al. 2015). by crawling from plant to plant, via wind, Bougainvillea mealybug feeds mainly on machinery, and with labour crews. Ac- on Bougainvillea plants, which are widely cidental introduction to new territories is cultivated in gardens of the Mediterranean possible through infested live plants, par- region and frequently traded as a potted ticularly in shipments of whole ornamen- plant (Mazzeo et al. 2014). It is also re- tals and fruit trees (CABI 2015b). corded on Alternanthera spp., Araujia Phenacoccus peruvianus Granara sericifera Brot., Aucuba japonica Thunb, de Willink, 2007 [Hemiptera, Pseudococ- Buddleja spp., Solanum vespertilio Ait., cidae] – Bougainvillea mealybug. Plectranthus scutellarioides (L.) R. Br., Collected material: Ravda – May 2012 chilly peppers and others (Beltra еt al. and July 2014; Burgas – May 2012. 2010). Among its hosts P. peruvianus Specimens of Bougainvillea mealybug shows a preference for members of Sola- were detected two times in garden centre naceae and can successfully complete its in Ravda and in greenhouses in Burgas life cycle on Solanum lycopersicum L. and on several Bougainvillea glabra Choisy Nicotiana tabacum L. (Beltrà еt al. 2013). plants (Fig. 4b), imported from Italy. Al- Large mealybug populations cause necro- though P. peruvianus has been record- sis of the foliage, leaf loss, dieback and ed in Bulgaria in 2014 (Pencheva et al. sooty mould development on the excreted 24 A. Penchevа and M. Yovkova

a b

Fig. 5. Adult females of Ceroplastes spp.: C. ceriferus (a) and C. japonicus (b). honeydew (Malumphy and Eyre 2011). has been found also in Netherlands, UK Ceroplastes ceriferus (Fabricius, and Slovenia (Fetyko and Kozár 2012, 1798) [Hemiptera, Coccidae] – Indian wax Seljak 2012). scale. The Indian wax scale may use a wide Collected material: 2013: 3 June and variety of hosts comprising more than 25 July – Nessebar; 2015: 30 October – 120 plant species belonging to 51 fami- Sozopol. lies and 71 genera (García et al. 2015). A few C. ceriferus females (Fig. 5a) Besides fruit crops, it attacks also lots of were detected in two private properties ornamentals (Acer, Berberis, Buxus, Cor- nearby Nessebar in 2013, on single Py- nus, Deutzia, Euonymus, Ficus, Ilex, La- racantha sp. and Ilex aquifolium shrubs. gerstroemia, Laurus, Magnolia, Platanus, This scale was found again in Octo- Pyracantha, Rhododendron, Salix and Vi- ber 2015 on twigs of Euonymus alatus burnum) (EPPO 2015). Like all the others, (Thunb.) Siebold in a private garden in wax scales C. ceriferus secretes large Sozopol. In both localities C. ceriferus amount of honeydew which provides a had been distributed along with plant medium for sooty mould. The sooty mould material imported from Italy two years may become so dense that it interferes ago. with photosynthesis (Hamon and Williams Indian wax scale was detected for the 1984, Seljak 2012). first time in Bulgaria in June 2009 on a pri- The observations over the last three vate property in Vidin on a solitary Acer years indicated that C. ceriferus can suc- palmatum ‘Atropurpureum’ tree (Penche- cessfully overwinter in locations around va and Yovkova 2011). the Black Sea coast. C. ceriferus is most likely to be native Ceroplastes japonicus Green, 1921 to Asia, but it has already been widely dis- [Hemiptera, Coccidae] – Japanese wax tributed all over the world (García et al. scale. 2015). In Europe, it has been intercepted Collected material: 2013: 25 July – several times at the imports of ornamental Ravda and Aheloy; 2015: 20 July – Ah- plants (Pellizzari et al. 2004). C. ceriferus eloy. New Data on Alien Insect Pests... 25

Adult females, first and second instar dish brown in old specimens (Gimpel et nymphs of C. japonicus were detected on al. 1974). leaves and twigs of Ilex aqufolium, Cit- Based on cladistics analysis of wax rus sp., Laurus nobilis, Viburnum thinus scale insects, Qin et al. (1994) predicted L. and Pyracantha coccinea M. Roem that C. sinensis originates from Cen- (Fig. 5b) in garden centre in Ravda and tral or South America. This supposition in private property in Aheloy. The country was supported later by the discovery of origin of infested ornamentals was Italy. heavily parasitized individuals of Chi- Japanese wax scale was found for the nese wax scale in Argentina (Hodgson first time in Bulgaria in 2006 on plant ma- and Peronti 2012). It is a highly poly- terial collected in greenhouses (Penche- phagous pest and can damage more va 2007). than 130 plant species belonging to 54 C. japonicus is native to Eastern Asia families (García et al. 2015). Currently and is currently a pest of significant eco- C. sinensisis is distributed in several nomic impact for citrus and other fruit European countries (Croatia, France, crops in Asia. In Europe it represents a Greece, Italy, Portugal, Spain, Turkey serious phytosanitary threat mainly to and subtropics of the former USSR) (Fe- laurel, holly and ivy (Mazzeo et al. 2014). tyko and Kozár 2012). C. japonicus is widespread on ornamen- Chinese wax scale completed a single tals in several European countries, both annual generation. The optimal condi- outdoors (i.e. Armenia, Croatia, Georgia, tions for its development are: temperature Italy, France, Netherlands, Russia and 22,4–26,0 ºС and air humidity 70–80 %. Slovenia) and indoors (i.e. Hungary, Unit- The pest is not as cold resistant as C. ved Kingdom) (Fetykò and Kozár 2012). japonicus. The mean fecundity of adult The present investigation confirms that females was 3260 ± 770 eggs per female the species is established in the southern (García et al. 2015). The heavy infestation Black Sea coast where it overwinters out- leads to the death of branches and, some- doors (Pencheva 2009). Ceroplastes sinensis Del Guercio, 1900 [Hemiptera, Cocci- dae] – Chinese wax scale. Collected material: 2013: 25 July – Ravda. Specimens of C. sinensis were identified onIlex aquifolium imported from Italy to a garden centre in Ravda (Fig. 6). This is the first record of this scale species in Bul- garia. The adult females are con- vex, reach up to 3–7 mm in length and 2.0–6.0 mm in width. The dorsal wax cover is formed by 7 not very distinctly divided plates – 1 a b dorsal and 6 lateral. The wax cover Fig. 6. Ceroplastes sinensis: a – adult females; b – the is white in young females and red- antenna of Chinese wax scale is 7-segmented. 26 A. Penchevа and M. Yovkova times, plants. Its introduction in Bulgaria europaea L.) grown indoors in two garden may become a problem in ornamental centres. This is the first record of the De plant production. Stefan scale in Bulgaria. Apparently, all Aulacaspis yasumatsui Takagi 1977 infested plants had been imported from [Hemiptera, Diaspididae] – Cycads aulac- Greece and Italy. aspis scale. De Stefan scale is native to Near East Collected material: 2013: 3 April – and Mediterranean Palaearctic. In Eu- Ravda and 28 July – Sofia. rope it is distributed in Cyprus, Greece, A. yasumatsui was detected on a few Italy, Montenegro, France, Spain, Turkey, imported plants of sago cycas (Cycas Ukraine and Russia (Central and South- revoluta Thunb.) in a garden centre in ern) (García et al. 2015). Their females Ravda in April 2013. Although the infes- are brown, elongated and 2.4–3.0 mm tation had not been detected prior to car- long. The male puparium is clear brown, rying the plants to the greenhouse, within 1.8 mm long (Danzig 1993). In Italy L. two months all leaves were covered with a flava has one generation per year and white crust, comprising scales of live and it overwinters as a mature fertilized fe- dead insects. Damage initially appears male. Each female produces 25–30 eggs as chlorotic spots, but most of the fronds (García et al. 2015). This pest prefers eventually become brown and withered. Olea europaea (Pellizzari.et al. 2011) and Later A. yasumatsui was collected in a Ligustrum spp. (Gill 1997) as hosts, and greenhouse in Sofia, also on imported should not be a major risk for Bulgaria sago cycas plants. Although this infesta- since olive trees are grown predominantly tion was not so drastic, in both cases the in greenhouses and interior. plants died. Cycads aulacaspis scale was Pseudaulacaspis pentagona (Tar- first detected in Bulgaria by Trencheva et gioni Tozzetti, 1886) [Hemiptera, Diaspidi- al. (2010a) in 2009 in a garden centre in dae] – white peach scale. Tsarevo, at the southern Black Sea coast. Collected material: Balchik (13 May A. yasumatsui is native to Southeast 2014), Sofia (from May to October in the Asia. Its host plants are from the gymno- period 2012–2015) and Plovdiv (6 June sperm order Cycadales, which consists 2013). of three families – Cycadaceae, Stan- P. pentagona was detected in Balchik geriaceae and Zamiaceae (CABI 2015c). (on Broussonetia papyrifera), Plovdiv It is highly damaging to cycads, which (Platanus × acerifolia (Aiton) Willd.) and include horticulturally important and en- in different private properties on Sofia (on dangered plant species. It is difficult to Cornus alba L. ‘Elegantissima’, Syringa x control, as it forms dense populations and persica L. ‘Alba’, Rosa hybrida L. and 12 spreads quickly to new areas via infested other arboreal hosts) mainly on Catalpa plant trade (Howard et al. 1999). bignonioides and Morus alba f. pendula Lepidosaphes flava (Signoret, 1870) (Fig. 7). The last two hosts were imported [Hemiptera, Diaspididae] – De Stefan from Italy and had been planted in private scale. gardens approximately in 2007 or 2008. Collected material: 2012: 13 April – Heavily infested trees exhibited dieback Sofia and 2013: 26 April – Burgas. and died after a few years. Only sporadically infestations of L. The white peach scale is native to flava were detected on olive trees (Olea Eastern Asia, where it is a pest of Prunus New Data on Alien Insect Pests... 27 and Morus. It was accidentally introduced to Italy in the nineteenth cen- tury, and has nowadays spread to all major continents (CABI 2015d). The scale was first recorded in Bulgaria in 1968 (Tsalev 1968), but its distribution was limited predominantly in south- western regions (Trencheva et al. 2010b) as an important economic pest of peach trees. A batch of infested ornamental shrubs from a single nursery can easily spread the pest widely. In temperate regions, dense populations can form thick crusts of scales on tree trunks Fig. 7. Dense colonies of Pseudaulacaspis pentagona and older branches. In Central Europe on branches of Morus alba. it has colonized both cultivated and rica. At present its range is expanding natural habitats. Heavy outbreaks of the across Europe, having been able to in- scale insect have occurred on ornamental vade even northern countries such as plants in Hungary (Kosztarab and Kozár Lithuania, which is a confirmation of the 1988). P. pentagona can be mentioned great adaptability of this insect (Signorile as a significant invasive scale present in 2012). Over 100 plant species have been the highway margin zone (Bayoumy et al. noted as hosts, however, Dianthus is the 2011). most seriously affected, although other Cacoecimorpha pronubana (Hübner, species have suffered infestations re- 1799) [Lepidoptera, Tortricidae] – carna- garded as serious. In international trade, tion tortrix moth. C. pronubana may be carried on plants for Collected material: Burgas – 26 May planting or cut flowers of carnations, chry- 2012; Aheloy – from May to September santhemums, pelargoniums, roses and in the period during 2012–2015; Ravda – other host plants (CABI 2015e). 2013: May and July. Last four years C. pronubana was detected in Aheloy (in its previous locality) (Pencheva et al. 2009), with a low population density, because of continuous control, including pruning the branches with hibernating caterpillars and pheromone traps. In Burgas and Ravda the species was found in garden centres on Viburnum tinus L. and Aucuba japonica Thunb. (Fig. 8), imported from the Netherlands and Italy. This Mediterranean species is widespread in Europe and North Af- Fig. 8. Adult of Cacoecimorpha pronubana. 28 A. Penchevа and M. Yovkova

Cydalima perspectalis (Walker, webbing of the branches with frass and 1859) [Lepidoptera, Crambidae] – box residues of moulting. Heavy damage or re- tree moth. peated attacks lead to total defoliation and Collected material: 2014: 25 August may cause the death of the shrubs. The – Balchik, Dragalevtsi (near Sofia); 28 young larvae of the box tree moth feed on August – Dobrich; 2015: 20 May – Bal- the lower surfaces of the leaves, leaving chik and Evksinograd (near Varna); from the upper epidermis intact (Fig. 9b). Older 15 July to 15 October – Balchik, Burgas, caterpillars gnaw roughly on leaves, leav- Kalofer, Primorsko, Sozopol, Plovdiv and ing thick veins only. They can also eat the Sofia. green bark of the young twigs. During the present observations in the The box tree moth was first detected end of August 2014, damage to Buxus in Bulgaria in July 2014 in Balchik Botani- sempervirens, as well as larvae, pupae cal garden and in Varna by Beshkov et al. and moths (Fig. 9a) were found in new (2015). It is a very destructive insect, inju- locations: private gardens in Dobrich and rious to Buxus spp. (B. sempervirens L., Sofia. In summer 2015 the pest was de- B. microphylla Siebold & Zucc. and B. col- tected both in private gardens and in city chica Pojark.). In its native range (China parks located in Burgas, Primorsko, So- and Japan) it feeds on B. sinica (Leuthardt zopol, Sofia, Plovdiv and Kalofer. Plants 2013). In Southern Russia C. perspecta- of different ages – from 5 to 80 and more lis also attacks Ruscus aculeatus L. and years old (in Euxinograd) – were attacked Prunus laurocerasus L. (Skvortsov 2013). in both old plantings and newly created The species is a well-known pest with- sites. The infested box trees were defo- in its original range in Asia. It has spread liated, particularly in lower parts of the widely throughout Europe in recent years, crowns. This damage reduced completely probably introduced with box tree seed- the aesthetic value of plants. Odher’s were lings. Due to a lack of natural enemies

a b

Fig. 9. Cydalima perspectalis: a – adults; b – damage by a young larva. New Data on Alien Insect Pests... 29 in its invaded range, C. perspectalis can interceptions, with the slight possibility of reach large population sizes and densities outdoors surviving. The species, which (Leuthardt 2013, Hizal et al. 2012, Ramel are able to adapt to outdoor conditions, and Ross 2013). Observation of the dis- are mostly detected as a small sample or persal of European populations of C. in limited localities (with exception of Met- perspectalis in northwest Switzerland al- calfa pruinosa and Pseudaulacaspis pen- lowed an estimate of the natural dispersal tagona). Probably within quite a short peri- velocity of adults to be made at 7–10 km od of time they may release their potential per year (Leuthardt et al. 2010). to be more widely spread and established The box tree moth has two to three gen- on the territory of Bulgaria, especially in erations per year in Europe, while in the its south-western part. Global warming native range up to 5 generations per year and mild winters also indirectly affect ac- are possible (Perny 2010). It overwinters climatization frequencies by increasing as a larva, spinning a cocoon between box the abundance of suitable host plants for leaves in autumn and completes its devel- alien insect species (Mazzeo et al. 2014). opment the following spring. In Balchik, Within Europe, the Mediterranean basin is after overwintering, the larvae continued especially susceptible to insect invasions, feeding until the middle of May 2015 and due to its climatic conditions being favour- pupated in the crown of plants. The first able for the establishment of tropical and generation moths appeared at the begin- subtropical non-native species (Roques ning of June. A new flight of moths was et al. 2009). Currently the greatest part of also detected in the middle of August. In ornamental plants in Bulgaria is produced Sofia defoliation of box trees was detected in Italy, the Netherlands and Hungary. in the middle of July and flight of moths – in The surveying insects in these countries the end of August. The new generation lar- are common pests and their accidental vae were in diapause in the middle of Octo- introduction in Bulgaria is possible via im- ber. The results from the observations car- ported plants because of reduced border ried out in 2015 demonstrate that the box control between EU-countries. tree moth is spreading quickly throughout the country. Its introduction could represent a threat to nurseries, historical parks and Conclusion gardens, as well as to plant hosts growing in the wild. Fourteen insect species associated with The above presented alien insects urban landscape areas have been sur- are mainly polyphagous except for five veyed. Two of them have been reported monophagous ones – A. jamatonica, T. for the first time in Bulgaria – Ceroplastes alacris, the coccids A. yasumatsui and sinensis and Lepidosaphes flava. Three L. flava, and the moth C. perspectalis. species (Cacoecimorpha pronubana, Polyphagous insects are more likely to Ceroplastes ceriferus and Metcalfa prui- become major pests when introduced nosa) have widened their host range in to new areas because the existing plant Bulgaria. Aulacaspis yasumatsui, Acizzia hosts may allow them to successful devel- jamatonica, Pseudaulacaspis pentagona opment and reproduction. and Cydalima perspectalis have been Five of the discussed insects are re- found in new locations. The quick spread stricted to greenhouses or are merely of the box tree moth indicates that the pest 30 A. Penchevа and M. Yovkova will be a serious risk for B. sempervirens Beshkov S., Abadjiev S., Dimitrov throughout the country. D. 2015. Cydalima perspectalis (Walker, The results of investigation indicate 1859) (Lepidoptera: Pyraloidea: Crambidae: that exotic pests and especially scale in- Spilomelinae) – new invasive pest moth in Bulgaria. The entomologist’s record and sects use mainly ornamental plants as a journal of variation 127: 18–22. pathway of introduction in new areas, so Blackman R.L., Eastop V.F. 2015. Aphids that urban landscapes and nurseries are on the world’s plants. Verson 2015. Available: the first habitats in which they become es- http://www.aphidsonworldsplants.info/ tablished. (Accessed on 23 November 2015). CABI 2015a. Elatobium abietinum (green spruce aphid). Available: http://www.cabi. org/isc/datasheet/30897 (Accessed on 24 Acknowledgements November 2015). CABI 2015b. Icerya purchasi (cottony First we thank reviewers for their construc- cushion scale). Available: www.cabi.org/isc/ tive comments. We would like to thank datasheet/28432 (Accessed on 23 November also V. Harizanova, PhD from Agricultural 2015). University, Plovdiv, Bulgaria for confirming CABI 2015c. Aulacaspis yasumatsui the identification of theAcizzia jamatonica; (cycad aulacaspis scale) Available: www.cabi. J. F. Germain, PhD from the Plant Health org/isc/datasheet/18756 (Accessed on 24 Laboratory, Montpellier, France, for con- November 2015). firming the identification of Ceroplastes CABI 2015d. Pseudaulacaspis pentagona (mulberry scale). Available: www.cabi.org/isc/ ceriferus; Ev. Tsavkov, from University of datasheet/45077 (Accessed on 25 November Forestry, Sofia, for the photos of micro- 2015). scope slides and colleagues who provide CABI 2015e. Cacoecimorpha pronubana infested plant materials. (carnation tortrix). Available: www.cabi.org/isc/ datasheet/54205 (Accessed on 23 November 2015). References Carter C.I., Halldórsson G. 1998. Origin and background to the green spruce aphid in Bayoumy M.H., Fetyko K., Tobias I., Europe. In: Day K.R., Halldorsson G., Harding Konczne Benedicty Z., Szita É., Kozar F. S., Straw N. A (Eds.). The Green Spruce Aphid in 2011. A geographical study on Pseudaulacaspis Western Europe: Ecology, Status, Impacts and pentagona and its parasitoids in Hungarian Prospects for Management. Edinburgh, Forestry highway margins using pheromone traps and Commission, Technical Paper 24: 1–14. molecular markers. Entomologia Hellenica 20: Chornesky E.A., Bartuska A.M., Aplet 17–30. G.H., Britton K.O., Cummings-Carlson Beltrà A., Soto A., Germain J.F., Matile- J., Davis F.W., Eskow J., Gordon D.R., Ferrero D., Mazzeo G., Pellizzari G., Gottschalk K.W., Haack R.A., Hansen Russo A., Franco J.C., Williams D.J. 2010. A.J., Mack R.N., Rahel F.J., Shannon M.A., The Bougainvillea mealybug Phenacoccus Wainger L.A., Wigley T.B. 2005. Science peruvianus, a rapid invader from South America priorities for reducing the threat of invasive to Europe. Entomologia Hellenica 19: 137–143. species to sustainable forestry. BioScience Beltrà A., Tena A., Soto A. 2013. 55(4): 335–349. Fortuitous biological control of the invasive Danzig E.M. 1993. Fauna of Russia and mealybug Phenacoccus peruvianus in neighboring countries. Rhynchota. Vol. X. Southern Europe. BioControl 58(3): 309–317 suborder scale insects (Coccinea): families doi: 10.1007/s10526-012-9488-5. Phoenicococcidae and Diaspididae. Nauka New Data on Alien Insect Pests... 31

Publishing House, St. Petersburg, Russia. 452 Florida and Neighboring Land Areas. p. (in Russian). Gainesville, Florida Department of Agriculture Doychev D. 2015. First record of the & Consumer Services, Division of Plant invasive Elm sawfly Aproceros leucopoda Industry. 194 p. Available: http://ufdc.ufl.edu/ Takeuchi (Hymenoptera: Argidae) in Bulgaria. UF00000091/00001/1j Silva Balcanica 16(1): 108–112. Harizanova V., Stoeva A., Mohamedova EPPO 2015. Global Database, Ceroplastes M. 2012. Preliminary study on the invasive ceriferus (CERPCE), Host plants. Available: Acizzia jamatonica (Hemiptera: Psyllidae) and https://gd.eppo.int/taxon/CERPCE/hosts its predators in Bulgaria. Agricultural science (Acccesed on 26 November 2015). and technology 4(1): 56–61. FAO 2003. Biological risk management in Hizal E., Kose M., Yesil C., Kaynar D. food and agriculture: scope and relevance. 2012. The new pest Cydalima perspectalis Document to the Technical consultation (Walker, 1859) (Lepidoptera: Crambidae) on biological risk management in food and in Turkey. Journal of Animal and Veterinary agriculture, Bangkok, Thailand, 13–17.I.2003, Advances 11(3): 400–403. doi: http://dx.doi. Rome, 2003. Available: ftp://ftp.fao.org/es/esn/ org/10.3923/javaa.2012.400.403 food/tc_bangkok/tc_brm_03_2en.doc Hodgson C.J., Peronti A.L.B.G. 2012 A Fetyko K., Kozar F. 2012. Records revision of the wax scale insects (Hemiptera: of Ceroplastes Gray 1828 in Europe, with Sternorrhyncha: Coccoidea: Ceroplastinae) of identification key to species in the Palearctic the Afrotropical Region Zootaxa 3372: 1–265. Region. Bulletin of Insectology 65(2): 291–295. Howard F.W., Hamon A., McLaughlin García M., Denno B., Miller D.R., M., Weissling T., Yang S. 1999. Aulacaspis Miller G.L., Ben-Dov Y, Hardy N.B. 2015. yasumatsui (Hemiptera: Sternorrhyncha: ScaleNet: A Literature-based model of scale Diaspididae), a scale insect pest of cycads insect biology and systematics. http://scalenet. recently introduced into Florida. Florida info (Accessed on 26 November 2015). Entomologist 82(1): 14–27. Gill R.J. 1997. The Scale Insects of Kosztarab M., Kozár F. 1988. Scale California: Part 3. The Armored Scales Insects of Central Europe. Akademiai Kiado, (Homoptera:Diaspididae).California. Depart Budapest. 456 p. ment of Food & Agriculture, Sacramento, CA. Leuthardt F.L.G. 2013. Cydalima 307 p. perspectalis (box tree moth). Invasive Species Gimpel W.F., Miller D.R., Davidson Compendium. Available: www.cabi.org/isc/ J.A. 1974. A Systematic Revision of the Wax datasheet/118433. (Accessed on 23 November Scales, Genus Ceroplastes, in the United 2015). States (Homoptera; Coccoidea; Coccidea). Leuthardt F.L.G., Billen W., Baur B. Maryland Agricultural Experiment Station. 2010. Ausbreitung des Buchsbaumzünsler Miscellaneous publication: 841–885. Diaphania perspectalis (Lepidoptera: Gkounti V., Milonas P. 2013. First record Pyralidae) in der Region Basel – eine fur of the bougainvillea mealybug Phenacoccus die Schweiz neue Schadlingsart. Entomo peruvianus in Greece. Entomologia Hellenica Helvetica 3: 51–57. 22: 16–18. Lucchi A., Santini L. 1993. Note morfo- Grozea J., Gogan A., Virteiu A.M., biologiche sugli stadi preimmaginali di Metcalfa Grozea A., Stef R., Molnar L., Carabet pruinosa (Say) (Hemiptera, Flatidae). Frustula A., Dinnesen S. 2011. Metcalfa pruinosa Say Entomologica (N.S.) 16(29): 175–185. (insecta: homoptera: flatidae): A new pest Malumphy C., Eyre D. 2011. Bougainvillea in Romania. African Journal of Agricultural Mealybug Phenacoccus peruvianus. The Research 6(27): 5870–5877. Food and Environment Research Agency Hamon A.B., Williams M.L. 1984. The (Fera). Available: http://fera.co.uk/plantClinic/ soft scale insects of Florida (Homoptera: documents/factsheets/bougainvillea.pdf Coccoidea: Coccidae). Arthropods of (Accessed on 03 December 2015). 32 A. Penchevа and M. Yovkova

Mazzeo G, Longo S., Pellizzari G., Pencheva А. 2007. New and little known Porcelli F., Suma P. Russo A. 2014. Exotic pests in greenhouses for ornamental plants in Scale Insects (Coccoidea) on Ornamental Bulgaria. Acta Entomologica Bulgarica 13(3– Plants in Italy: a Never-Ending Story. Acta 4): 35–43 (in Bulgarian). Zoologica Bulgarica, Suppl. 6: 55–61. Pencheva А. 2009. Ceroplastes japonicus Masten M. T., Šimala M., Markotić V. (Green) (Hemiptera: Coccoidea: Coccidae) – 2015. First records of bougainvillea mealybug a new pest on Ilex in Bulgaria. Forestry Ideas Phenacoccus peruvianus Granara de Willink, 15(1): 226–232 (in Bulgarian). 2007 and madeira mealybug Phenacoccus Pencheva A., Velcheva N., Yovkova M. madeirensis Green, 1923 (Hemiptera: 2009. New species on Bay laurel (Laurus nobilis Pseudococcidae) in Croatia. In Trdan S. L.) in Bulgaria. Proceedings of International (edit.): Lectures and papers presented at 12th scientific conference “Good practices in Slovenian conference on plant protection. Ptuj, sustainable agriculture”, 12–13 November, March 3–4: 318–322. 2009, Sofia, Bulgaria: 312–320 (in Bulgarian). Mifsud D., Cocquempot C., Pencheva A., Yovkova M. 2011. Review Mühlethaler R., Wilson M., Streito of alien insect pests on ornamental plants J.C. 2010. Other Hemiptera Sternorrhyncha in Bulgaria. Proceedings of Anniversary (Aleyrodidae, Phylloxeroidea, and Psylloidea) International conference: 60 years specialty and Hemiptera Auchenorrhyncha. Chapter “Landscape architecture”, Sofia: Sezhani: 9.4. In: Roques A. et al. (Eds.). Alien terrestrial 112–117 (in Bulgarian). arthropods of Europe. BioRisk 4(1): 511–552. Pencheva А., Yovkova M., Kozarov D. doi: 10.3897/biorisk.4.63. 2014. Insect Pests on Bougainvillea glabra Ossiannilsson F. 1996. The Psylloidea with Description of Phenacoccus peruvianus (Homoptera) of Fennoscandia and Denmark, Granara De Willink – A New Species in Bulgarian Leiden, New York Koln. 350 p. Greenhouses. Plant sciences LI(6): 90–93. Pantaleoni R.A. 1989. Ways of invasion Perny B. 2010. Mass outbreak of box tree of a new area by Metcalfa pruinosa (Say, pyralid Diaphania perspectabitis in the East of 1830) (Auchenorrhyncha, Flatidae). Bollettino Austria. Forstschutz aktuell 50: 17–19. dell’Istituto di Entomologia dell’Universita degli Qin T.K., Gullan P.J., Beattie G.A.C., Studi di Bologna 43: 1–8. Trueman J.W.H., Cranston P.S., Fletcher Pellizzari G., Camporese P. 1994. The M.J., Sands D.P.A. 1994. The current distribution Ceroplastes species (Homoptera, Coccoidea) and geographical origin of the scale insect pest of the Mediterranean Basin with emphasis on Ceroplastes sinensis (Hemiptera: Coccidae). C. japonicus Green. Annales de la Société Bulletin of Entomological Research 84: 541–549. Entomologique de France 30(2): 175–192. Ramel J.M., Ross J.P. 2013. Geographical Pellizzari G., Galbero G., Mori N., range of Cydalima perspectalis (Walker, Antonucci C. 2004. Biologia di Ceroplastes 1859) [Lepidoptera: Pyraloidea: Crambidae: ceriferus (Fabricius) (Hemiptera, Coccoidea) Spilomelinae] and its recent expansion e possibilità di lotta. Informatore fitopatologico in France. XVIII European Congress of 54(9): 39–46. Lepidopterology, July 29 – August 04, 2013. Pellizzari G.P., Seljak F. G., Kozar F. Blagoevgrad, Bulgaria. Available: http://www. 2011 Some additions to the Scale insect fauna ecl18.eu. (Hemiptera: Coccoidea) of Crete with a check Seljak G. 2012 Six new alien list of the species known from the island None. phytophagous insect species recorded Journal 292 of Entomological and Acarological in Slovenia in 2011. Acta Entomologica Research Ser. II 43(3): 291–300. Slovenica 20(1): 31–44. Pencheva A. 1995. The species structure and Signorile L. 2012. An unusual, new larval significance on the scale insects (Homoptera, host-plant for Cacoecimorpha pronubana Coccinea) in the greenhouses in Bulgaria. (Hübner, 1799) (Lepidoptera: Tortricidae). Forestry Ideas 1(3–4): 141–151 (in Bulgarian). Entomologist’s Gazette 63: 49–51. New Data on Alien Insect Pests... 33

Skvortsov M.M. 2013. The Box Tree yasumatsui Takagi, 1977 (Hemiptera: Moth in the Krasnodar region of Russia – three Diaspididae) in Bulgaria. Rastenievadni Nauki years after invasion. Federal Forestry Agency, 47(3): 206–209. Center of Forest Health of Krasnodar Region. Trencheva К., Trenchev G., Tomov Available: http://czl23.ru/news.php?extend.102 R., Wu S.-A. 2010b. Non-indigenous scale (Accessed on 26 November 2015). insects on ornamental plants in Bulgaria and Souliotis C., Papanikolaou N.E., China: A survey. Entomologia Hellenica 19: Papachristos D., Fatouros N. 2008. Host 114–123. plants of the planthopper Metcalfa pruinosa Tsalev М. 1968. Contribution to the study (Say) (Hemiptera: Flatidae) and observations of scale insects (Homoptera, Coccidea) in the on its phenology in Greece. Hellenic Plant urban parks and ornamental plants in Bulgaria. Protection Journal 1: 39–41. Izvestia na zoologicheskia institut s muzei 28: Strauss G. 2010 Pest risk analysis of 205–218 (in Bulgarian). Metcalfa pruinosa in Austria. Journal of Pest Vétek G., Rédei D. 2009. First record of Science 83(4): 381–390. Acizzia jamatonica (Kuwayama) (Hemiptera: Tomov R., Trencheva K. 2013. A review Psyllidae) in Bulgaria. Acta Zoologica Bulgarica of pest status of recently recorded alien 61(3): 323–325. insects in Bulgaria. Proceeding of IV ESENIAS Yovkova M., Pencheva A., Petrović- Workshop: International Workshop on IAS in Obradović O. 2016. First Report of Elatobium Agricultural and Non-Agricultural Areas in abietinum (Walker, 1849) (Hemiptera, ESENIAS Region, 16–17 December 2013, Sternorrhyncha, Aphididae) on Picea spp. in Çanakkale, Turkey: 108–114. Bulgaria. Acta zoologica Bulgarica 68(1): 135– Trenchev G., Ivanova I., Nikolov P., 138. Trencheva K. 2007. Metcalfa pruinosa (Say, Yovkova М., Petrović-Obradović O., 1830), new species in Bulgaria. Plant Science Tasheva-Terzieva E., Pеncheva A. 2013. 34(3): 195–198. Aphids (Aphididae, Hemiptera) on ornamental Trencheva K., Trenchev G., Tomov R., plants in greenhouses in Bulgaria. ZooKeys Wu S.-A. 2010a. First report of Aulacaspis 319, special issue: 347–365.