AGRICULTURAL SCIENCE AND TECHNOLOGY, VOL. 4, No 1, pp 56 - 61, 2012

Agriculture and Environment

Preliminary study on the invasive jamatonica (: ) and its predators in

V. Harizanova*, A. Stoeva, M. Mohamedova

Department of Entomology, Faculty of Plant Protection and Agroecology, Agricultural University , 12 Mendeleev, 4000 Plovdiv, Bulgaria

Abstract. After the psyllid Acizzia jamatonica has been reported for the first time as a pest of julibrissin in Bulgaria in 2009 it hasexpanded its distribution. In Southern Bulgaria in 2010-2011 the pest was recorded on the examined trees in all surveyed regions: , Balgarin, Gorski izvor, Patriarh Eftimovo, Parvomay, Kozanovo, Karadjovo, , Yagodovo, Zvanichevo, Radinovo, Plovdiv, , , Tzarevo, Lozenetz and . Naturally occurring predators from 13 species were observed to feed on the eggs and nymphs of the psyllid. Among the predators the ladybeetles, predatory bugs and soldier beetles were the most numerous. The Asian lady beetle Harmonia axyridis maintained highest population density throughout the season. Heavily infested by the psyllid leaves, buds and shoot tips were observed after the end of June which resulted in serious damages.

Keywords: invasive species, silky , psyllid, natural enemies

Introduction Insecticides can be used but several applications are necessary to control the overlapping generations. In addition, treatments are difficult to perform on ornamental trees in urban environment where The Persiansilktree or silky acacia (Albizia julibrissin only a limited number of active substances are authorized (Alma et Durazzini) from Fabaceae family is thought to be native to eastern al., 2002).The aim of the present study was to establish the spread of Asia (Klimaszewski 1973, Yang 1984, Li,1992).In 1749 the the pest in Southern Bulgaria and the predatory feeding on it. Florentian noble Filippo degli Albizzi brought the species into cultivation in and laterit was introduced also to North America (Cothran 2004). Because of its graceful flowers and umbrella-like canopy, Albizia julibrissin has been widely planted as Material and methods an ornamental tree for landscaping along roads, in public and private gardens. Its wood can be used for building and furniture-making. The presence of the psyllid in different regions in Southern The bark has been utilized as an repellent, and as medicine Bulgaria was established by surveying A. julibrissin trees in parks (Zheng et al., 2004). Although in its native range there are 75 and in private gardens in 2010-2011. The species diversity of listed as feeding on it, until recently there were no serious predatory insects was established by the method of beating on a pests threatening the tree in Europe and North America. In 2009- beating tray and by visual observations on 10 trees in private 2010 two species considered invasive and attacking albizia were gardens in Karadzovo and on 5 trees in Plovdiv once a month in reported in Bulgaria for the first time: the psyllid Acizzia jamatonica June, August and September, 2011. Four lower branches of the tree (Kuwayama) (Vetec and Redei, 2009), damaging the vegetative canopy of each tree were inspected for adults of lacewings and parts and the beetle Bruchidius terrenus (Sharp.) (Stoyanova, 2010) afterwards were tenderly beaten over a beating tray for establishing damaging the seeds. the number of larvae or adults of the predatory insects. After The psyllid was found first in Italy, in Piedmont and the Aosta counting and recording the predators they were released back to the Valley (Alma et al., 2002; Jucker et al., 2008). In 2003 the EPPO tree. secretariat decided to add it to the EPPO Alert List (EPPO reporting service, 2003). Since then the species has been reported from Slovenia (Seljak, 2003; Seljak et al., 2004), Croatia (Simala et al., 2006), France and Switzerland (EPPO reporting service, 2004), Results and discussion Hungary (Penzes et al., 2005), Spain (Sanchez & Burckhardt, 2009), Bulgaria (Vetek and Redei, 2009), Greece (Zartaloudis, 2007, Distribution Pasztor et al., 2010), Slovakia (Lautere et al., 2011). In Europe the In surveys in South Bulgaria the pest was recorded on all the psyllid attacks only A. julibrissin. In 2007 the species was reported in inspected trees in Harmanli, Balgarin, Gorski izvor, Parvomay, the USA (Ulyshen and Miller, 2007). In Europe serious damage (leaf Patriarh Eftimovo, Kozanovo, Karadzovo, Sadovo, Yagodovo, yellowing, defoliation) is observed and A. jamatonica could present a Zvanichevo, Radinovo, Burgas, Ahtopol, Tzarevo, Zosopol and risk to ornamental trees in urban environments and to nurseries Plovdiv. The species was not found only on the trees in the central (Alma et al., 2002). park of (Figure 1) but was present in the nearby village The control of this pest is likely to be difficult in practice. of Kozanovo. *e-mail: [email protected]

56 t:)

It',74I rh'4"- g.uzzt-

1.*u PRO

wirbroy.

pf..04.11 - present - not present .4=z4Z,

Figure 1. Surveyed regions for presence of A. jamatonicain Southern Bulgaria in 2011

Morphology the leaves and stems at the shoot tips, causing yellowing, partial or The eggs are yellow to orange, approximately 0.3 mm long, oval complete desiccation, defoliation and die back (Figure 2). The young with the apical end narrower and more pointed than the basal end shoots do not develop and the flower buds do not produce flowers. (Figure 2). They are laid singularly or in groups, preferably along the Both adults and nymphs excrete large quantities of honeydew, which leaflet margins, the central veins and petioles. The nymphal stages is coated with waxy secretions and deposited on the plant. The white (Figure 2) are dorso-ventrally flattened with obvious wing pads. waxy secretion can be found also on all the surfaces under the tree Young nymphs are creamy yellow with reddish eyes, whereas the canopy. The honeydew serves as a medium for the growth of black older nymphs are greenish-yellow with part of the head, wing pads sooty moulds, which blemish the foliage. and the tip of the abdomen all brown in colour. The dorsal surface of the thorax has paired brown spots and abdomen - transverse brown Natural enemies bands. Adults are pale green (Figure 2). More detailed description is In the region of Karadzovo and Plovdiv 13 predatory species given by Vetek and Redei (2009) and Lauterer et al. (2011). A. feeding on A. jamatonica were registered (Table 1), belonging to 6 jamatonica could be confused with another psyllid attacking the silk families from four orders: Coleoptera-ladybeetles (Coccinellidae) tree: acacia sucker (), native to Australia, but and soldier beetles (Cantharidae), Hemiptera-mirid and anthocorid introduced to Europe and present in France, Spain, Italy, , bugs ( and ),Neuroptera-lacewings Portugal, and the former Yugoslavia (Malumphy et al., 2007). (Chrysopidae) and Diptera-hover flies (Syrphidae). In June the Though it has not been reported from Bulgaria yet, it is very likely most abundant were H. axyridis, Rh. fulva, Orius sp. and D. ruber. A soon to be present having in mind the proximity to Serbia and single larva of a syrphid fly was found on a leaf with psyllid eggs and Macedonia and the possibility for dispersal by air currents. nymphs. In August the population density of the predators was lower in comparison with the one in June though the population density of Life cycle the psyllid had increased. The two largest predators - Rh. fulva and InPlovdiv region A. jamatonica has several overlapping D. ruber are no longer present. In September the ladybeetles H. generations per year. Overwintering adults begin laying eggs on the axyridis and Hippodamia variegate were the predominant predatory buds at the end of April. The adults of the first generation emerge in species. The predatory bug Anthocoris nemoralis, which is host- the beginning of June. Later in the season all stages of overlapping specific to psyllids and common predator of the pear sucker generations are found at the same time. Overwintering adults were Cacopsylla pyri L. in Bulgaria, was not recorded. One possible not found but according to Alma et al. (2001) the adults overwinter explanation is that in the region of observation there are no pear under the bark of trees. orchards and the bug is not present. The Asian ladybeetle H. axyridis which is also an invasive Damage species, reported in Bulgaria for the first time in 2009 (Tomov et al., The psyllid is a sap-feeding insect that forms dense colonies on 2009) comprised about one third of the predators (31,72%).

57 The rest of the ladybeetles -P 14-punctata, 0. conglobata, A. from June to September. Our observations lead to the conclusion bipunctata, H. variegate and C. 7-punctata comprise 17,8% that the natural enemies complex is not able to regulate the altogether (Figures 3 and 4). population density of A. jamatonica to levels at which the damage Of the predatory bugs, D. ruber was abundant in June but could be tolerated. Though difficult in practice, chemical control absent after end of July, C. verbasci was more abundant in August should be applied. and 0. majusculus was the most numerous predatory bug species

a) b)

d) e) f)

g) h) i)

1517 Ilerrr' ri0101...41111Prisillinn Ark Tr-17"1 4 -

t4- lir iiTeltti, I I k)

Figure 2. Acizzia jamatonica: a - adult; b - eggs; c - eggs on the shoots; d,e - young and older nymph; f -nymphs ofdifferent color on the leaflets; g,h,i - nymphs and wax secretion on leaflets and flower buds; j,k - yellowing and defoliation

58 Table 1. List of predatory insect species feeding on Acizzia jamatonica eggs and nymphs in the region of Plovdiv

Number on 60 branch tips Order Family/Species 4 June 15 August 6 September

Coleoptera Coccinellidae

Harmonia axyridis (Pallas, 1773) 14L, 62A 4L,50A 8L,26A Adalia bipunctata (L., 1758) 14A, 2L 0 0 Coccinella septempunctata (L., 1758) 4L,32A 0 0 Hippodamia variegata (Goeze, 1777) 8A 0 18A Propylaea quatuordecimpunctata (L., 1758) 8A 0 0 Oenopia conglobata (L., 1758) 6A 0 0 Cantharidae Rhagonycha fulva (Scopoli, 1763) 54A 0 0 Cantharis livida L. 1758 8A 0 0 Anthocoridae Orius sp. 40A 66A 12A Miridae 0 ruber (L., 1758) 38A 0 7A verbasci (Meyer-Dur, 1843) 0 20A

Diptera Syrphidae

Unidentified 1L 0 0

Neuroptera Chrysopidae

Crysoperla carnea (Stephens, 1836) 1A,5L 1A,7L 2A

L-larva; A-adult

0.conglobataIM 1.16

C. Livida 1.55

P14-punctata 1.55

Chr. carnea 3.09

A. bipunctata 3.09

H. variegata 5.03

C. verbasci 5.22

C. 7-punctata 6.96

D. ruber 7.35

Rh. fulva 10.44

Orius sp. 22.82

H. axyridis 31.72 % 0 5 10 15 20 25 30 35

Figure 3. Ratio between the relative population density of the predatory species feeding on A. jamatonica in the region of Plovdiv

59 a) b) c)

g) h) i)

j) k) I)

Figure 4. Predatory insects feeding on A. jamatonica: a - Hippodamia variegata; b - Coccinella 7-punctata; c,d,e,f -

Harmonia axyridis; g - Deraeocoris ruber; h - Rhagonycha fulva; i - Chrysoperla carnea; j - larva of E. balteatus; k - larva of H.axyridis; I -eggs of Chrysopidae

Conclusions potential to become the most dangerous pest of silky acacia. Unfortunately the naturally occurring predators are not able to On the basis of the results from observations carried out in 2011 reduce the population density of the invasive species to an in South Bulgaria a conclusion could be made that the psyllid A. acceptable level, especially in August and September. Without jamatonica is spreading very quickly all over the country and has a control the damages are serous and could influence the lifespan of

60 the trees. Different strategies of control should be tested including the morphological and bionomic characteristics of Agrilus sp. on application of insecticides. Aliizia julibrissin. Plant Protection, 21, 3, 22-23. SanchezI and Burckhardt D, 2009. First record of Acizzia jamatonica (Kuwayama, 1908) (Hemiptera: ) for the Iberian Peninsula. Boletin Sociedad Entomologica Aragonesa, 45, References 525-526.

Seljak G, 2003. Asian psyllid threatening albizia. My "Small" World, Alma A, Tedeschi R and Rossi J, 2002. Acizzia jamatonica 35, 6, 20-21 (Si). (Kuwayama) nuova psilla per ('Europa (Homoptera Psyllidae). Seljak G, Simala M and Stigter H, 2004. Three new non-European Informatore Fitopatologico, 52, 4, 64-65. psyllids (Hemiptera, Psyllidae) in Slovenia and Croatia. Abstracts of EPPO REPORTING SERVICE. 2002/058. Acizzia jamatonica: a the Third European Hemiptera Congress, St Petersburg, 2004 -06- new pest of Albizia found in Italy. 08111, 66-67. EPPO Reporting Service, 2003. EPPO report on notifications of Simala M, Seljak G, Poje I and Masten T, 2006. Newly recorded non-compliance (detection of regulated pests) 175. psyllids (Hemiptera, Psyllidae) on woody ornamental plants in EPPO Reporting Service, 2004. First report of Acizzia jamatonica Croatia. Plan Protection, 6, 1, 16-17 (Sr). in France: addition to the EPPO alert list, 153. Stoyanova A, 2010. Seed Beetle Bruchidius Terrenus (Sharp) Jucker C, Quacchia A, Colombo M and Alma A, 2008. Hemiptera (Coleoptera: Chrysomelidae: Bruchinae) - New Invasive Species to recently introduced into Italy. Bulletin of Insectology, 61, 1, 145-146. the Bulgarian Fauna. Biotechnology & Biotechnological Equipment, Klimaszewski SM, 1973. The jumping plant lice or psyllids 24, 2, 646-647. (Homoptera, Psylloidea) of the Palearctic. An annotated check-list. Tomov R, Trencheva K, Trenchev G and Kenis M, 2009: The Annales zoologici, Warszawa, 30,155-286. Multicolored Invasive Asian Ladybird Harmonia axyridis (Pallas, Lauterer P, Bartos R and Milonas P, 2011. First records of the 1773) (Coleoptera: Coccinellidae) New to the Fauna of Bulgaria. Jumping Plant-Louse Acizzia jamatonica (Kuwayama) (Hemiptera: Acta Zoologica Bulgarica, 61, 307-311. : Psyllidae) in Slovakia and Greece. Plant Protection Ulyshen M and Miller D, 2007. First record of Acizzia jamatonica Science, 47,1, 37-40. (Hemiptera:Psyllidae) inNorth America: friend or foe? Florida Li FS, 1992. Psylloidea (Heteroptera Sternorrhyncha). In: Peng J., Entomologist, 90, 573. Liu Y. (eds.): Iconography of Forest Insects in Hunan China. Science Vetek G and Redei D, 2009. First record of Acizzia jamatonica and Technology Press, Hunan, 204-213. (Kuwayama) (Hemiptera: Psyllidae) in Bulgaria. Acta zoologica Malumphy C, Reid S and Moran H, 2007. Acacia sucker Acizzia Bulgarica, 61, 3, 323-325. uncatoides. Plant Pest Notice. C S L. 48. Acacia sucker. Available at: Yang CT, 1984. Psyllidae of Taiwan. Taiwan Museum Special www.fera.defra.gov.uk/plants/publications/documents/.../acaciaSu Publications Series, 3,1-305. cker.pdf (accessed on 25.08.2011). Zartaloudis Z, 2007. Et1: Species identification-examination of Pasztor B, Redel D and Vetek G, 2010. First record of Acizzia samples.Et1.1:It was identified,the greenpsyllid,Acizzia jamatonica (Kuwayama) (Hemiptera: Psyllidae) in Greece. Hellenic jamatonica (Homoptera:Psyllidae) in the Laboratory of Entomology Plant Protection Journal, 3,25-27. and Zoology, Annual report of Nagref-Plant Protection Institute of Pellizzari G, Mori N, Galbero G and Antonucci C, 2005. Risultati di Thessaliniki, 64. due anni di sperimentazione contro la Psilla dell'Albizzia, Acizzia Zheng H, Wu Y, Ding J, Binion D, Fu W and Reardon R, 2004. jamatonica (Kuwayama). Informatore Fitopatologico, 55, 11, 33-39. Invasive Plants of Asian Origin Established in the United States and Penzes B, Redei D and Vetek G, 2005. The psyllid Acizzia Their Natural Enemies. Beijing, P.R. China, USDA Forest Service, jamatonica in Hungary. Kerteszet es Szoleszet, 54, 39,19 (Hu). Forest Health Technology Enterprise Team U.S.A. Qu Aijun, Zhu Chengmei and Wang Wenli, 1995. Observations on

61