Turkish Journal of Zoology Turk J Zool (2017) 41: 113-118 http://journals.tubitak.gov.tr/zoology/ © TÜBİTAK Research Article doi:10.3906/zoo-1602-59

The phenology of Pulvinaria floccifera Westwood (: Coccomorpha: ), a new invasive pest on ornamentals outdoors in Poland

1 1, 1 1 1 2 Bożena ŁAGOWSKA , Katarzyna GOLAN *, Katarzyna KMIEĆ , Izabela KOT , Edyta GÓRSKA-DRABIK , Katarzyna GOLISZEK 1 Department of Entomology, University of Life Sciences, Lublin, Poland 2 Department of Agriculture, Pope John Paul II State School of Higher Vocational Education, Biala Podlaska, Poland

Received: 29.02.2016 Accepted/Published Online: 04.06.2016 Final Version: 25.01.2017

Abstract: The phenology of Pulvinaria floccifera infesting common holly was studied from June 2009 to October 2011 in Central Poland. Live specimens were most abundant on the leaves in July and August, while dead individuals were most numerous in winter and early spring each year. The scale completed one generation per year in the field and both the second and third instar nymphs overwintered. Following the spring molting to the 3rd instar or to the young adult females were observed in April and early May. The young adult females were first recorded in the second 10-day period of May. Oviposition occurred from early June, while egg hatching started in the first 10-day period of July. The second instar nymphs were first observed in the first 10-day period of August, part of them overwintered, mainly on the lower part of leaves, while some of them molted to the third instar nymphs from mid-August through September and October. The overwintering third instar nymphs appeared in late August each year. No adult males or natural enemies were observed during this study. The period of crawler activity is recommended as the optimum time for the successful control of P. floccifera and it occurs in the first 10-day period of July in Poland.

Key words: Cottony camellia scale, life cycle, common holly, control measures, recommendations

1. Introduction In recent years, the economic importance of P. floccifera The cottony camellia scale, Pulvinaria floccifera has appeared to increase in Europe, including northern and (Westwood), has an almost worldwide distribution and is central regions. In Britain, it has become more abundant particularly widespread in the Holarctic region (Hodgson and extended its geographical distribution and host range and Henderson, 2000). It is a polyphagous with more (Malumphy and Badmin, 2007), while in the Netherlands than 80 host plant species belonging to 35 families and is it is increasingly important as a pest of ornamentals and considered a serious pest of fruit trees and ornamentals spreads from cultivated areas to natural woodland (Jansen, in many parts of the world, especially in countries with 2000). In Poland, the cottony camellia scale is included in tropical and subtropical climate (Kosztarab and Kozar, the group of alien invasive species (Łagowska et al., 2015). 1988; Garcia et al., 2015). Recently, the cottony camellia Although the cottony camellia scale has become a scale has been reported as the most important pest of serious pest almost all over Europe, the biological data citrus and tea orchards in the Middle East (Abd-Rabou et on this coccid in this area are fragmentary or limited to al., 2012; Hallaji-Sani et al., 2012; Sakineh et al., 2014). its harmfulness and the range of its host plants (Rehaček, In Europe, this coccid has been recorded in almost 1960; Canard, 1965; Masten Milek et al., 2009; Golan et all countries (Kosztarab and Kozar, 1988; Pellizzari and al., 2010; Łagowska et al., 2015). So far, the experimental Germain, 2010). Initially, this species was largely restricted research concerning the biology and ecology of P. floccifera in distribution to greenhouses in Northern and Central in the field was conducted mainly in Iran and Egypt (El- Europe, but, more recently, it has also spread outdoors Minshawy and Moursi, 1976; Abd-Rabou et al., 2012; and has been found on common hollies, common Hallaji-Sani et al., 2012). yews, and other ornamental plants in the Netherlands, The aim of the present study was to provide further Scandinavia, Great Britain, Germany, Ireland, Turkey, and relevant biological data to develop control measures for Poland (Jansen, 2000; Gertsson, 2005, 2013; Malumphy this coccid and prevent further infestations across Poland and Badmin, 2007; Ülgentürk et al., 2008; Forster, 2011; and other countries with similar climate. Phenological O’Connor et al., 2013; Łagowska et al., 2015). details such as the appearance of the 1st instar nymphs, * Correspondence: [email protected] 113 ŁAGOWSKA et al. / Turk J Zool the number of generations, and population peaks may 2009 than in 2010 and 2011. In contrast, the peak number give useful information for the control applications of of dead individuals was observed in the winter months insecticides or release of a biocontrol agent. each year (Figure 1). The life cycle of P. floccifera on I. aquifolium presented 2. Materials and methods in Figure 2 was estimated to last 319–323 days in nature Field experiments were conducted from June 2009 to (Table). This coccid developed one generation per year October 2011 on the cottony camellia scale infesting in the field and both the second and third instar nymphs common hollies (Ilex aquifolium L.) near Warsaw (Central overwintered (Figure 2); however, older nymphs were Poland, 52°10′53″N; 20°52′13″E). The analyses were clearly predominant. The overwintering nymphs were carried out on eight shrubs, 7 years old, about 1.5–2 m found mainly on the underside of the leaves in the bottom high, planted in a back garden of 1000 m2. Weed control parts of shrubs, while only a few specimens were observed in the garden was performed mechanically. No chemicals on the shoots. Following the spring, molting to the 3rd were sprayed in the garden during the study period. instar or to the young adult females was recorded in Random samples of 15 leaves and 10 cuttings of bark April and early May. The young adult females were first (about 2 × 2 cm) were collected every 10 days between observed in the second 10-day period of May, with a peak March and October and every 15 days during the other abundance of this instar in the last 10-day period of May months each year. In total, 81 samples were taken from 8 and early June (Table; Figure 2). No adult males were shrubs and about 1200 leaves and 800 pieces of bark were detected during this study. The first adult females forming examined under a stereomicroscope. Both living and dead ovisacs and laying eggs were observed in the first (2009 scales on the upper and lower leaf surfaces as well as on the and 2010) or the second (in 2011) 10-day period of June wood were assessed in 2009; however, in 2010 and 2011 (Table). In late June, all adult females were egg laying. Egg only the lower surface was examined, as it harbored most hatching started on 1 July in 2009 and 2010 and 5 days of the scales. No natural enemies were observed during later (6 July) in 2011 (Table). By early July, ovisacs with this study; the mortality of scales was probably caused by eggs and crawlers were observed. Newly hatched nymphs weather conditions. had a tendency to stay inside ovisacs for about 24 h and The identification of the developmental stages was then disperse throughout the leaf area to feed. The feeding based on microscopic slides prepared according to the first-instar nymphs were observed in mid and late July and procedures described by Ben-Dov and Hodgson (1997). disappeared by late August in all years of this study (Figure In total about 200 microscopic slides were used for this 2). The second instar nymphs were first observed in the study. The life cycle of P. floccifera in the field, the number first 10-day period of August and picked up by late August of days from hatching to each subsequent instar, and the and early September each year (Table; Figure 2). Some of average number of specimens per sample (on 15 leaves) the second-instar nymphs overwintered mainly on the were recorded. Temperature data were provided by the lower part of evergreen leaves, while some of them molted Warsaw Weather Station database (www.meteo.waw.pl). to third-instar nymphs from late August to September and October. The overwintering third-instar nymphs first 3. Results appeared in late August each year (Table). During the present study, about 85% of P. floccifera specimens were found on the lower leaf surface of I. 4. Discussion aquifolium, while only a few individuals settled on the The current study clearly demonstrates that the cottony upper surface of leaves or on the shoots. Eventually it camellia scale is able to develop, survive, and reproduce was decided to include in this work only the number of successfully outdoors in Poland. We found that this species specimens on the lower leaf surface. The total number of completes one generation per year and both the second- live specimens per sample (on 15 leaves) ranged between and third-instar nymphs overwinter. One generation per 2 (23 May 2010) and 511 (21 July 2009) scales, while the year has been also reported in Slovakia (Rehaček, 1960), total number of dead individuals found per sample was the southern France (Canard, 1965, 1965), Virginia, USA highest (81 specimens) on 26 April 2010 and the lowest (3 (Williams and Kosztarab, 1972), the Netherlands (Jansen, specimens) on 1 August 2011. 2000), northern Iran (Hallaji-Sani et al., 2012), and Japan, Figure 1 shows the average number of P. floccifera although 2 generations have been described on Eurya in specimens per sample together with the temperature data Tokyo (Takahashi, 1955). recorded each month at the study site. It is evident that the We can assume on the basis of our own results and live specimens were most abundant on the leaves in July literature data that P. floccifera overwinters in different and August and their number declined in the following stages in field conditions. In Poland, both the second- and months each year, although they were more numerous in third-instar nymphs overwinter, while in Slovakia and

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Netherlands only the second- or third-instar nymphs were through a second and third nymphal stage, they developed shown to overwinter, respectively (Rehaček, 1960; Jansen, into adult females and started oviposition without 2000). However, overwintering adult females have been changing their feeding site. Canard (1965) also reported reported in Egypt (Hallaji-Sani et al., 2012). no migration of nymphs. In contrast, Kosztarab (1996) So far, mainly female nymphs and adults of P. floccifera reported that the first-instar nymphs usually settled on the have been observed in most countries, while male nymphs leaves, but moved to twigs as second instars and remained have only been recorded in Georgia (Gogiberidze, 1938) there until maturity. and Slovakia (Rehaček, 1960). We have also collected Relatively high population peaks of P. floccifera were two second-instar male nymphs during this study, but observed in July and August each year and this could be adult males have never been observed. Gavrilov and attributed to the high numbers of newly hatched crawlers Trapeznikova (2008) suggested thelytokous reproduction present at the same time. We also observed a lower number for this species. of this pest in 2010–2011 in comparison to 2009. No Our observation showed that P. floccifera can develop natural enemies were observed during this study, and thus, and overwinter on leaves as well as on woody plant parts, at present, low temperatures during the winter months but most specimens were found on the lower surface of appeared to be the main factor determining P. floccifera leaves in all seasons during this study. Further observations population levels in Poland in the spring and summer the (unpublished data) revealed numerous specimens also following year. High mortality of nymphs was observed on woody shoots, when this pest was present in mass during the winter in 2009/2010 and 2010/2011 and it quantities. We also observed that only crawlers dispersed can be attributed to low temperatures in these periods. over the entire host plants to feed. Once settled, after going In a temperate climate, snow cover and its thickness may

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December April May June July August September October November Stages /March I II III I II III I II III I II III I II III I II III I II III I II III

females

eggs jaja mi

L1

L2

L3 Figure 2. Life cycle of Pulvinaria floccifera Westwood on Ilex aquifolium outdoors in Poland in the years 2009 ( ), 2010 ( ), 2011 ( ), the period of maximum abundance ( ).

Table. The dates of the first appearance of Pulvinaria floccifera Westwood instars in the years 2009–2011 and the number of days from hatching to each following stage.

Young Number of days from hatching to the first appearance of

Year adult Eggs L1 L2 L3

female L2 L3 Young adult female

2009 - 7.06 1.07 3.08 25.08 33 55 320 2010 15.05 5.06 1.07 5.08 27.08 35 57 319 2011 19.05 12.06 6.07 9.08 30.08 34 60 323

provide additional protection for wintering nymphs in the to Poland on holly (Ilex sp.) imported from nurseries in lower parts of shrubs and increase the chance of survival the Netherlands (Łagowska et al., 2015). Although this at low temperatures. However, mild winters are becoming cottony scale is currently found outdoors only on holly, more common in Poland and a massive number of this it should be considered a potential serious pest of many pest was observed in the spring and summer of 2015 when other plant species cultivated in Poland, as it is referred to temperatures were higher and did not drop below zero as a polyphagous species with high reproductive capacity (unpublished data). (Kosztarab and Kozár, 1988; Kosztarab, 1996). It seems Our observations provide some information concerning that evergreen plants are predominantly threatened by this the phenology of P. floccifera, which is a new outdoor pest. Recently, it was found to breed outdoors on Taxus, pest in Poland. Since 1971, this coccid was introduced Euonymus, Magnolia, Mahonia, Olea, Pittosporum, twice in Poland. On the first occasion, this species was Pyracantha, and Rhododendron in several European imported on potted ornamental plants and recorded countries (Jansen, 2000; Malumphy and Badmin, 2007; only in greenhouses on Acalypha wilkesiana Muell Arg, Masten Milek et al., 2009; Forster, 2011), and there is a high Camellia japonica L., Citrus aurantium (L.), and Schefflera probability of its adaptation to these host plants cultivated arboricola (L.). More recently, it has been reintroduced commercially also in Poland.

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The fact that P. floccifera was able to successfully (containing 1% Azadirachtin A, a botanical extract from complete its life cycle outdoors also shows that it has the the tree Azadirachta indica), and local mineral oil (Super potential to damage native plant species in natural habitats Misrona oil 95% EC) provided satisfactory control of P. in Poland, similarly as in the Netherlands, where this floccifera and their parasitoids in Egypt. cottony scale has already been found on Vaccinium in the The most important part of control is forests (Jansen, 2000). timing. To ensure successful control, the treatments In Poland, P. floccifera is included in the group of should be timed to coincide with the period of crawler alien invasive species (Łagowska et al., 2015) and it is activity. Thus, ovipositing females should be overturned important to develop control measures for this pest. to determine whether egg hatching has begun, and sprays This species is a new alien pest in Poland and natural should be timed when most eggs have already hatched. In enemies may currently give only marginal control. In certain cases, a second application may be needed 10 days this situation, treatments with different compounds can after (Pfeiffer, 1997). According to the results of our study, effectively control the population of P. floccifera in Poland. the control of ovisacs should be carried out in late June, Abd-Rabou et al. (2012) reported that Biofly (containing and the first treatment is recommended in the first 10-day Beauveria bassiana, 3 × 107 c.f.u./1 mL), Neem Azal period of July.

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