Silva Balcanica, 17(2)/2016

REVIEW OF GRAY 1828 IN BULGARIA WITH FIRST REPORT OF C. CIRRIPEDIFORMIS COMSTOCK 1881

Aneliya Pencheva University of Forestry, Sofia Mariya Yovkova Institute of Ornamental Plants, Sofia

Abstract

The aim of the publication was to summarize the current status of genus Ceroplastes in Bulgaria. During the last investigation in a garden center in Ravda four Ceroplastes species were identified. They were found infesting 20 ornamental plant species; most of them cultivated in greenhouses. Among collected scale , C. cirripediformis was detected for first time in the country. The basic morphology and biological characters of this wax scale are presented. In addition an identification key to Bulgarian Ceroplastes species is provided. Key words: C. ceriferus, C. cirripediformi, C. japonicus, C. sinensis, first record, new host plants

INTRODUCTION

The wax scales from subfamily Ceroplastinae is one of the largest groups from the family (, , Coccoidea). Their members can be easily recognized by the thick, protective waxy layer. Similarly wax scales are often observed in groups of plants that are readily seen and collected (Gill, 1988). Currently, the subfamily Ceroplastinae includes two genera: Ceroplastes Gray 1828 and Waxiella De Lotto (1971) (Rainato, Pellizzari, 2010). The first genus contains approximately 140 species; most of them are endemic to the Neotropics and Ethiopian Regions and only a few (4 or 5) originate from other zoogeographical regions (Fetyko, Kozár, 2012; García et al., 2016). Ceroplastes species have a worldwide distribution (much of this is perhaps due to human activity) whereas Waxiella ones are distributed mainly in Africa (Rainato, Pellizzari, 2010). Recently many studies have been devoted to Ceroplastes with the aim of clarifying their distribution, pest status, revision of the species or even description of new species (Hodgson, Peronti, 2012; Kaydan, Kondo, 2008; Rainato, Pellizzari, 2008, 2010; Peronti et al., 2008; Ülgentürk, 2016). Currently in Europe there are records of 11 species from the genus Ceroplastes, which have been either established or in a timely manner intercepted (Fetyko, Kozár, 2012; Malumphy, 2010). Several wax scales, like C. japonicus Green 1921, C. rusci L. and C. floridensisComstock 1881 are widespread in many parts of Europe, whereas some others have a restricted known distribution. Often, these wax scales are established in urban areas and here they can increase rapidly due to the absence of their natural enemies (Mazzeo et al., 2014).

37 In regard to Bulgaria, to this day tree wax scales have been recorded as pests of indoor and outdoor ornamental plants: Japanese wax scale (C. japonicus Green); Indian wax scale (C. ceriferus (Fabricius)) and Chinese wax scale (C. sinensis Del Guercio). In their native habitat they are highly polyphagous and infest a wide range of ornamentals and mostly fruit crops (García et al., 2016). A few observations of C. japonicus and C. ceriferus, conducted in the country during recent years, indicated their successful acclimatization in restricted regions around the Black Sea coast (Pencheva, 2009; Pencheva, Yovkova, 2016). In October 2015 and May 2016, transient incursions of Barnacle scale (C. cirripediformis Comstock) were registered first in a garden center and then in a private property. This was the first detection of Barnacle scale in Bulgaria. The aim of the work presented here was: to summarize the current status of the genus Ceroplastes in Bulgaria; to present the basic morphology and biological characteristics of the newly reported wax scale C. cirripediformis; in addition to providing an identification key to Bulgarian Ceroplastes species.

MATERIALS AND METHODS

A survey was conducted mainly in October 2016 in a garden center, located in Ravda (southern part of Black Sea coast). During the visual inspection of ornamental plants, infested plant parts (twigs or leaves) and scale insects seen on them were collected. For each of the ’s samples, the origin of infested host plants was checked. The observation included two types of ornamentals. First type was plants grown in botanical collections in greenhouses and the second one were plants, cultivated outdoors. In total seventeen samples of wax scale were collected and studied in our laboratory. The female specimens were slide-mounted according to the method provided by Kosztarab, Kozár (1988). Only young females were used in order to detect some structures such as filamentous ducts, which are impossible to identify in aged females. The newly reported speciesC . cirripediformis was identified using the key of Fetyko, Kozár (2012). The identity of species was confirmed by Dr É. Szita from Department of Zoology, Plant Protection Institute, Hungarian Academy of Sciences, Budapest. The collected specimens are preserved in the department of Plant Pathology and Chemistry at the University of Forestry, Sofia. A key with figures was constructed to differentiate Ceroplastes Bulgarian species, using the description of Gimpel et al. (1974), and identifications keys of Fetyko, Kozár (2012), Gill (1988), Pellizzari, Camporese (1994) and Ülgentürk (2016).

RESULTS

The list of collected wax scales in 2016 is presented in Table 1. The infested host plants, recorded in preceding investigations are mentioned as well (Pencheva, Yovkova, 2016).

38 Four Ceroplastes species infesting a large number of ornamentals in the garden center were identified. During the current study, dense colonies of C. japonicus on 14 host plants were registered; twelve of them are new hosts for this pest in Bulgaria. Japanese wax scale was most abundant on shrubs of Ilex aquifolium L., growing outdoors, as well as on Cinnamomum camphora (L.) J. Presl., benjamina L. and Schefflera actinophylla (Endl.) Harms indoors. They were collected predominantly as young females and only several third instar nymphs. A few C. ceriferus females (Fig. 2a) were detected on a single Photinia × fraseri Dress shrub. The species had settled in a mixed community together with C. japonicus. This is the fifth sample from Indian wax scale in Bulgaria since it has been first reported in 2009 (Pencheva, Yovkova, 2011). Specimens of C. sinensis, predominantly in 2nd nymphal stage, were identified on 5 new hosts: Acca sellowiana (O.Berg) Burret; × limon (L) Osbeck; Caragana arborescens Lam.; Zanthoxylum armatum DC. and Hibiscus syriacus L. Identification of C. cirripediformis was confirmed for first time in 2016, but the material for its identification and confirmation was collected in May and October 2015. The specimens of this scale had infested Ilex aquifolium in a private property around Nessebar and some Citrus spp. in the same greenhouses in Ravda. In October 2016 only dead females with hatched eggs, from previously generation on Citrus×limon and Citrus myrtifolia, were found. Description of a new detected pest Ceroplastes cirripediformis

Table 1. List of Ceroplastes species and their host plants

Host plants in October 2016 Species Previously reported host plants In greenhouses Outdoors Acer palmatum Thunb., Ceroplastes L. A. negundo Euonymus ceriferus s (Thunb.) Siebold, Photinia × fraseri (Fabricius) alatu Ilex aquifolium L. Pyracantha sp.

Ceroplastes C (L), itrus×limon C. myrtifolia L. cirripediformis Raf. Blanco Ilex aqufolium Comstock ,C. reticulate Camellia sasanqua Thunb.,Citrus sp., Cinnamomum camphora L., Ilex aquifolium L., Citrus sp., Ilex aquifolium L., Escallonia sp., Eriobotrya japonica Ceroplastes Laurus nobilis L., Viburnum Citrus spp., Photinia × (Thunb.) Lindl.,Ficus benjamina japonicus thinus L., Pyracantha fraseri, Yucca gigantea L., Ficus elastica Roxb. Ex Hornem, Green coccinea M. Roem, Hedera Lem.,Viburnum Monstera deliciosa Liebm., helix L., Camellia japonica L. rhytidophyllum Hemsl. Schefflera actinophylla (Endl.), Harms, Strelitzia reginae Aiton. Caragana arborescens Ceroplastes Acca sellowiana (O.Berg) Burret, Lam., Hibiscus syriacus sinensis Ilex aquifolium L. Citrus×limon (L) L., Zanthoxylum Del Guercio armatum DC.

39 Fig. 1. C. cirripediformis: a, b – adult female; c – antennae and d – stigmatic setae (original)

Material examined: Ravda – October 2015, 2016; Nessebar – May 2015; 6 female specimens in good condition. Detailed descriptions and illustrations of C. cirripediformis can be found in works of Gimpel et al. (1974), Gill (1988) and Peronti et al. (2008). Only the most important morphological characteristics of the adult female by Gill (1988) are reported here. Unmounted material: Adult females have reddish brown body, 2-5 mm long, convex to hemispherical in form. The body is completely covered with a layer of thick wax, pearly to grayish white in colour (Fig. 1a, b); it is without horn, this is visible in C. ceriferus (Fig. 2a). Morphologically this species is most similar to Chinese wax scale (Fig. 1d). Wet wax oval in dorsal view, hemispherical laterally, divided into 1 dorsal and 6 lateral plates by thin depressed lines. Each plate has a darkened central area (Fig. 1d). At the end of the oviposition, the female is transformed in a capsule filled with eggs. Like another Ceroplastes, C. cirripediformis has three nymphal instars which are reddish with separate conical wax filaments. Mounted material: Mounted female is oval in shape, filamentous ducts absent on venter. Dorsum. With a mediodorsal clear area; cephalic and posterolateral clear areas divided. Pores predominantly triangular and trilocular, a few number of oval trilocular pores, quadrilocular pores and bilocular pores present. Dorsal setae are capitate. Area around anal region is sclerotized, forming protuberance; anal plates rounded, without distinct angles; each anal plate with 1 subapical seta, 3 or 4 apical setae, and 1 subdiscal seta; anal fold with 4 fringe setae. Ventrum. Antennae are 7-segmented (Fig. 1c). Legs are well developed, tibiotarsal articulatory sclerosis present (Fig. 2e); claw without denticle, claw digitules are equal. Tubular ducts with inner filament unexpanded, present on head and near anal opening. Stigmatic setae triangular, with rounded or pointed apices, sides (height) of setae longer than width of base, about 30 of them of each stigmatic furrow, arranged in 3 or 4 rows (Fig. 1d). Quinquelocular pores in stigmatic furrows present in

40 Fig. 2. Morfological characters of Ceroplastes species: adult females of a – C. ceriferus and b – C. sinensis; c – ventral tubular ducts with expanded inner filament and d – flagellate setae of C. japonicus; e – tibiotarsal sclerosis of C. ciripedifurmis leg and f – anal process of C. ceriferus (original) wide bands. Host plants and distribution. The NeotropicalC . cirripediformis is a polyphagous species. Its host-plant list includes about 150 species (García et al., 2016). C. cirripediformis is a pest of many ornamentals in Florida but mostly found on dooryard gardenia plants (Gill, 1988), and one of the more important soft scale pests on guava trees in Egypt (Reda et al., 2010). Common hosts are: Citrus; Gardenia; Ficus; Strelitzia; Monstera; Jasmine; Fuchsia; Pittosporum; Bay laurel; Nandina; Rhus; Shefflera; Guava among others (García et al, 2016). In Europe C. cirripediformis has been reported as an outdoor species in Greece and Italy (Fetyko, Kozár, 2012) Biology. The number of generations produced by wax scales depends onits location. It is univoltine in temperate climate zone and a bivoltine in Egypt (Reda et al., 2010). According to Martin-Loayza, Cisneros-Vera (1995) the duration of a life cycle is in average 108.5 days (from 96.0 to 122.3) in conditions of 22.5°C. The mean fecundity

41 of adults in average is 2790 eggs per female, depending on the temperature and female size. Males are rarely established. C. cirripediformis crawlers normally settle on the upper leaf surfaces along the main veins. Third instars usually migrate from the leaves to the stems soon after molting (Gimpel et al., 1974). Key to species of Ceroplastes in Bulgaria, based on adult females 1. Antennae 6-segmented. Tibiotarsal sclerosis absent...... 2 Antennae 7-segmented (Fig. 1c). Tibiotarsal sclerosis present (Fig. 2e)...... 3 2. Ventral tubular ducts with expanded inner filament (Fig. 2 c). Stigmatic setae (about 110 on each margin side) with pointed apices and forming continuous row, with 1-7 flagellate setae interspersed among them (Fig. d)...... japonicus Green - Tubular ducts with narrow inner filament, on head and near anal opening. Stigmatic setae (about 50-52) are bullet shaped, arranged in 6 irregular rows. Anal process short, less than 1/5 of the body (Fig. 2f)...... ceriferus (Fabricius) 3. Filamentous ducts present on ventral submargin. Multilocular pores absent from thorax and anterior abdominal segments. Stigmatic setae are about 30 (27-36), hemispherical, in rows of 2 intergrading sizes. Largest seta conical with slightly rounded apex...... sinensis Del Guercio - Filamentous ducts absent. Multilocular pores present on all abdominal segments and near coxae of meso- and meta-thoracic legs. Stigmatic setae in 3 irregular rows; all setae robust, bluntly rounded, conical, each twice as long as wide (Fig. 1d)...... ciripedifurmis Comstock

DISCUSSION

The presented wax scales are only a small sample, which demonstrates the trend of exponential rise of new alien insects introduced into Bulgaria. This has resulted due to the increased interest in ornamentals, as well as active commercial exchange of live plants material in a world-wide scale. Like the rest of the coccid members, the wax scales are able to spread easily with infested plant host. Because of their small size and cryptic behaviour they go often unnoticed at border control centers (Mazzeo et al., 2014). Ceroplastes are extremely polyphagous and the existing plant hosts found in new habitats allow them to successfully develop and reproduce. Often, they reach large population density before even being noticed. The results obtained from this study indicate the increased distribution of C. japonicus. Eight years since its first detection in Bulgaria, Japanese wax scale is currently found established both indoors and outdoors in south coastal area of Black Sea. Once introduced into glasshouses, it may bring a significant risk for production of ornamentals in Bulgaria. In the investigated greenhouses the population density of this species can be compared to densities seen in other cosmopolitan polyphagous species such as Cocus hesperidum L. and Pseudococcus longispinus (Targioni Tozzetti). The speciesC . ceriferus, which are able to adapt to outdoor conditions, are mostly

42 detected in small quantities or in limited localities. It was recorded in North Italy in 2001 and is considered as established, but minor, pest of various ornamental and wild plants (Pellizzari et al., 2004). Recently C. ceriferus was detected also in Turkey on plants in city parks (Ülgentürk, 2016). In Europe the species has been intercepted by quarantine services in the Netherlands and Slovenia (Seljak, 2012). Because of their lesser economic importance it was removed from the EPPO Alert List in 2005. At the same time, C. ceriferus is a pest of economic importance affecting ornamentals in the USA and has been described in the invasive and Exotic Insect List of North America (Ülgentürk, 2016). The large number of possible hosts in addition to the high rate of reproduction are reasons enough not to dismiss the risk of invasion of these species, especially in the warmer regions of our country. In regard to C. sinensis and C. cirripediformis, theirs detection in Bulgaria is considered only as an interception and it is impossible to predict whether this species could become acclimatized in Bulgaria. Changes in climate and mild winters promote not only the northward expansion of some insect species in central Europe, but also increase the chances of survival of species introduced from warmer parts of the world (Pellizzari, Porcelli, 2014). Within Europe, the Mediterranean basin is especially susceptible to wax scale invasions, due to its favourable climatic conditions for the establishment of tropical and subtropical non-native species (Mazzeo et al., 2014). Currently the majority of ornamental plants in Bulgaria are produced and imported from Italy, the Netherlands and Hungary. The surveying wax scales are common pests in the aforementioned countries and their accidental introduction in Bulgaria is possible via imported plants because of reduced border control between EU countries. The real impending danger of invasion from other species in the genus Ceroplastes in Bulgaria such as C. floridensis and C. rusci should not be ignored. These species have exhibited a wide range of distribution in various European countries, but are more commonly encountered in the warmer parts of the continent (Fetyko, Kozar, 2012).

Acknowledgements: We would like to thank Dr É. Szita from Hungarian Academy of Sciences, Budapest for confirming the identification of C. cirripediformis.

REFERENCES

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