Invasive Insect Pests and Their Associated Parasitoids on Ornamental Urban Plants on Corfu Island

Hellenic Plant Protection Journal 7: 53-59, 2014

SHORT COMMUNICATION

Invasive insect pests and their associated parasitoids on ornamental urban plants on Corfu island - Phytoliriomyza jacarandae Steyskal and Spencer 1978 (Diptera, Agromyzidae) a new record in Greece

S. Bella

Summary In this study the results of recent surveys on alien insect pests of ornamental urban plants on the island of Corfu are reported. Overall seven alien species associated with allochthonous ornamental plants were recorded: Acizzia jamatonica (Kuwayama 1908), Glycaspis brimblecombei Moore 1964 (Hemiptera, Psyllidae), Corythucha ciliata (Say 1832) (Hemiptera, Tingidae), Obolodiplosis robiniae (Haldeman 1847) (Diptera, Cecidomyiidae), Phytoliriomyza jacarandae Steyskal and Spencer 1978 (Dip- tera, Agromyzidae), Cacyreus marshalli Butler 1898 (Lepidoptera, Lycenidae) and Leptocybe invasa Fish- er and La Salle 2004 (Hymenoptera, Eulophidae). Particularly, Phytoliriomyza jacarandae, a leafminer of the Blue jacaranda tree Jacaranda mimosifolia D. Don. (Bignoniaceae) is reported for the fi rst time from Greece. Two associated parasitoids, Platygaster robiniae Buhl and Duso 2008 (Hymenoptera, Platyg- astridae) and Psyllaephagus bliteus Riek 1962 (Hymenoptera, Encyrtidae) obtained from Obolodiplosis robiniae and Glycaspis brimblecombei, respectively, are also reported. Details on current distribution, host plants and biological remarks are given for each species.

Additional keywords: alien insects, fi rst record, urban environment

Introduction several invasive insect pests have been introduced, have spread rapidly in the Medi- The introduction of alien insects is a grow- terranean area and are causing serious dam- ing phenomenon especially in countries age to agricultural, forest and ornamental with intensive international movement of plants. Biological invasions by alien insect goods and people. This is particularly evi- species are a great ecological and economic dent in the Mediterranean Basin where cli- threat for their direct and indirect impact on matic conditions are more favourable for indigenous biodiversity. the numerous tropical and subtropical spe- The aim of this work was to identify alien cies to establish themselves. The continu- insect species on urban ornamental plants ously increasing use of numerous species of on Corfu. Field observations were made by plants native to diff erent regions of the plan- the author in the late summer 2013 in public et in European parks and gardens has been gardens in various towns. enriching the European fauna with mainly alien species that develop on the same host plants (Bella, 2013). In the last decade, Materials and methods

Dipartimento di Gestione dei Sistemi Agroalimentari e Samplings were carried out in August 2013 Ambientali (DiGeSA), sez. Entomologia applicata, Uni- throughout Corfu. Ornamental exotic plants versità degli Studi di Catania, Via S. Sofi a, 100. 95123 Ca- tania, Italy were investigated to ascertain the presence Email: [email protected] of possible pests, by beating or by careful vis- . © Benaki Phytopathological Institute 54 Bella ual search of specimens or by examination of are produced and can cause some incon- symptoms. Species identifi cation was based venience in urban environments (Sánchez on the morphology of adults and preimagi- García and Burckhardt, 2009). nal stages; important was the observation of the type of galls and leafmines and the asso- Glycaspis brimblecombei Moore 1964 ciation with the host plants. Part of the sam- Native range: species described from Aus- ples was conserved in 75% ethanol and la- tralia. belled. The collected material was studied Distribution: this species has shown inva- in the laboratory, dissected under a binoc- sive behaviour in the last 15 years and has ular microscope and prepared when neces- spread across several continents outside sary. Examined material is preserved in the its native range. It was fi rst detected in the private collection of the author and partly in United States of America (California, Florida the entomological collection of the Depart- and the Hawaiian Islands) and subsequent- ment of Agri-food and Environmental Sys- ly recorded from Mexico, Central and South tems Management, University of Catania. America (Brazil, Uruguay, Ecuador, Venezue- la, Colombia, Peru, Chile and Argentina) and Africa (Morocco, Algeria, Tunisia and South Results Africa). It is also found in the Canary Islands, New Zealand and Mauritius (Bella, 2013). In Detected species Europe, G. brimblecombei is reported from Portugal, Spain, France, Corsica, Italy, Sici- Hemiptera, Psyllidae ly, Sardinia, Greece, Corfu and Montenegro (Bella and Rapisarda, 2013; Reguia and Peris- Acizzia jamatonica (Kuwayama 1908) Felipo, 2013; Ben Attia and Rapisarda, 2014; Native range: species of oriental origin (Chi- Milonas and Partsinevelos, 2014; Tsagkarakis na, Korea and Japan). et al., 2014). Distribution: in Europe, it was fi rst detect- Host plant: associated with diff erent species ed in Italy and later recorded in numerous of Eucalyptus (Myrtaceae) (Brennan et al., European countries, including the Unit- 2001); in the Mediterranean area mainly on ed Kingdom, Portugal, Spain, France, Corsi- the River red gum, E. camaldulensis Dehnh. ca, Switzerland, Germany, Slovenia, Croatia, Material examined: 16-20 August 2013; Ben- Montenegro, Serbia, Slovakia, Greece, Bul- itses, 39° 32΄N, 19° 54΄E, 6 m a.s.l.; Lefkim- garia and Hungary. Since 2006, it has been mi 39° 24΄N, 20° 04΄E, 6 m a.s.l.; Kassiopi, found in the United States of America (Bel- 39° 47΄N, 19° 45΄E, 8 m a.s.l.; Corfu city, 39° la, 2013). 37΄N, 19° 55΄E, 10 m a.s.l.; Roda, 39° 47΄N, 19° Host plant: diff erent species of Albizia (Fa- 48΄E, 27 m a.s.l.; Agios Mattheos, 39° 29΄N, baceae, Mimosoideae); in Europe on the Per- 19° 52΄E, 140 m a.s.l.; Sinarades, 39° 34΄N, 19° sian silk tree, A. julibrissin (Willdenow) Du- 50΄E, 151 m a.s.l.; Kato Garouna, 39° 32΄N, 19° razzini. 51΄E, 225 m a.s.l.; Pelekas, 39° 35΄N, 19° 49΄E, Material examined: Corfu city, 39°37΄N, 247 m a.s.l.; nymphal stage and adults have 19°55΄E, 10 m a.s.l., 17.VIII.2013, adults on A. been observed on E. camaldulensis. julibrissin. Biological remarks: nymph instars construct Biological remarks: the life cycle of A. jama- white conical lerps using wax and honey- tonica includes numerous overlapping gen- dew secretions, while the adults are highly erations; the psyllid overwinters in the adult mobile and live freely on the foliage. It pro- stage. Leaves and shoots can be completely duces copious amounts of wax and honey- colonised by juvenile and adult stages with dew on the infested leaves, causing desicca- serious damage, leading to total or partial tion and premature leaf drop (Laudonia and desiccation. Large amounts of honeydew Garonna, 2010).

Hemiptera, Tingidae locust tree, R. pseudoacacia L. Biological remarks: the larvae form charac- Corythucha ciliata (Say 1832) teristic leaf-margin roll galls. Usually 1-2 lar- Native range: species of Nearctic origin. vae can be found in a gall and 1-3 galls per Distribution: now widespread across Europe leafl et. The larvae of the summer genera- in the United Kingdom, Portugal, Spain, tions pupate inside the galls on the trees, France (including Corsica), Italy (including while those of the autumn generation pu- Sardinia and Sicily), Belgium, Netherlands, pate in the soil after leaf fall. Several gener- Germany, Austria, Switzerland, Croatia, Slo- ations (2, 3 or even 4) of the gall midge may venia, Serbia, Montenegro, Greece, Turkey, develop in a year depending on climatic Czech Republic, Slovakia, Romania, Hunga- conditions (Bella, 2007). ry and Bulgaria. It has been found in Chile, southern Russia, Korea, China, Japan and Diptera, Agromyzidae Australia (Bella, 2013). Host plant: feeds primarily on Sycamore Phytoliriomyza jacarandae Steyskal and trees, Platanus (Platanaceae), especially P. oc- Spencer 1978 cidentalis L.; other host plants are Brousson- Native range: species of South American or- etia papyrifera (L.) Vent., Carya ovata (Mill.) igin. Koch, Tila sp., Chamaedaphne sp., Fraxinus Distribution: it is widespread in Argenti- sp., and Quercus laurifolia Michx. na (Córdoba), the United States of Ameri- Material examined: Corfu city, 39°37΄N, ca (California), Australia, New Zealand and 19°55΄E, 10 m a.s.l., 17.VIII.2013, adults on Pla- South Africa (Spencer, 1990). In the Palaeart- tanus sp. ic region, the only records are in Italy (Ligu- Biological remarks: C. ciliata feeds on the ria and Sicily regions) and Portugal (Bella et underside of leaves desiccating the tissue, al., 2007; Bella, 2013). which may drop prematurely. A single fe- Host plant: monophagous leafminer of the male can lay up to 350 eggs along the leaf Blue jacaranda tree, Jacaranda mimosifolia veins. There are fi ve immature instars, and in D. Don. (Bignoniaceae). Europe one life cycle is completed in just 20 Material examined: Kato Garouna, 39°32΄N, to 50 days and several generations can oc- 19°51΄E, 216 m a.s.l., 16.VIII.2013. cur each year (Malumphy et al., 2006). Biological remarks: the young larva produces a short linear brown mine in a single leaf- Diptera, Cecidomyiidae let developing into an irregular blotch. The aff ected leaves drop and the larva pupate in Obolodiplosis robiniae (Haldeman 1847) the soil. The canopy quickly yellows and de- Native range: species of Nearctic origin. foliates (Bella et al., 2007). Distribution: in Europe, it was fi rst noticed during 2003 in Italy, and subsequently it has Lepidoptera, Lycaenidae rapidly spread throughout a large part of Eu- rope. It has also been observed in South Ko- Cacyreus marshalli Butler 1898 rea, China, Japan, New Zealand, Ucraina and Native range: species of South African ori- Russia (Bella, 2013). For the Corfu the spe- gin (Swaziland, Lesotho, Botswana, Mozam- cies is reported by Skuhravá and Skuhravý bique, Zimbabwe and South Africa). (2006). Distribution: it is widespread in the Balear- Host plant: diff erent species of Robinia (Fa- ic Islands, Portugal, Spain, Netherlands, Nor- baceae: Papilionoideae). way, Finland, Sweden, France, Corsica, Bel- Material examined: Benitses, 39°32΄N, gium, Germany, Switzerland, Great Britain, 19°54΄E, 6 m a.s.l., 16.VIII.2013; Corfu city, Italy, Sardinia, Sicily, Malta, Slovenia, Croa- 39°37’N, 19°55’E, m 10 a.s.l., 17.VIII.2013. Galls tia, Czech Republic, Greece, Romania, Slova- and larvae have been observed on the Black kia, Bulgaria, Turkey, Israel, Estonia, Ukraine,

Uzbekistan, the Canary Islands and Moroc- ly damaging to new growth, due to its pref- co (CABI, 2014). erence for young leaves (including petioles) The fi rst record for mainland Greece is that and stems of new shoots for oviposition: of Martinou et al. (2011), while from the is- plants may become deformed, and growth land of Corfu the species is recorded by may be stunted due to heavy galling. The Parker (2010). wasp produces two or three overlapping Host plant: C. marshalli is a pest of cultivated generations per year. A female lays about Geranium spp. and Pelargonium spp. (Gera- 80-100 eggs shallowly beneath the epider- niaceae), but the butterfl y also has the ca- mis; the larvae complete their development pacity to infest native Geranium spp., and within the gall (Kim, 2008). could cause problems for the wild species. Material examined: Benitses, 39°32΄N, Associated parasitoids 19°54΄E, 6 m a.s.l., 16.VIII.2013, adults on fl owers of Geranium sp. Hymenoptera, Platygastridae Biological remarks: eggs are laid near the fl ower buds or less frequently on the leaves; Platygaster robiniae Buhl and Duso 2008 the hatched larvae penetrate inside the Native range: species of Nearctic origin. stems of the host plant, where they bore Distribution: the parasitoid wasp is present galleries and emerge at the fourth and fi - in France, Italy, Sicily, Switzerland, Denmark, nal larval stage to form light-green to dark- Croatia, Montenegro, Serbia, Slovakia, Czech brown pupae. In favourable conditions they Republic, Bulgaria, Ukraine, South Korea and can produce up to six generations per year. China (Jørgensen, 2009; Sviridov and Bazhe- The fl ight period occurs from the fi rst half nova, 2009; Lu et al., 2010; DAISIE, 2014). of April to the fi rst half of November (Lon- Host: specifi c parasitoid of the locust gall go, 2004). midge, Obolodiplosis robiniae (Diptera, Ceci- domyiidae). Hymenoptera, Eulophidae Material examined: Benitses, 39°32΄N, 19°54΄E, 6 m a.s.l., 16.VIII.2013; Corfu city, Leptocybe invasa Fisher and La Salle 2004 39°37’N, 19°55’E, 10 m a.s.l., 17.VIII.2013, Native range: species described from Aus- found to parasitize larvae of O. robiniae in- tralia. festing Robinia pseudoacacia L. (Fabaceae). Distribution: it is widespread in Europe Biological remarks: P. robiniae is a gregari- (Balearic Islands, Portugal, Spain, France, ous, koinobiont endoparasitoid of O. robin- Corsica, Italy, Sardinia, Sicily, Greece and Ca- iae; it is an egg-larval parasitoid, parasitis- nary Islands); also found in Africa (Morocco, ing eggs of O. robiniae and emerging from Algeria, Uganda, Ethiopia, Kenya, Tanzania, the host larvae. After hatching, the parasi- Mozambique, Zimbabwe and South Africa); toid undergoes only two larval instars, and in Asia (Turkey, Israel, Jordan, Syria, Kurdis- development from egg to adult takes about tan, Iran, Iraq, India, Thailand, Vietnam, Cam- 28 days to complete. The life cycle of a par- bodia and China); in Oceania (Australia and asitoid generation is synchronised with that New Zealand); in South America (Brazil and of its host; the adult wasps’ emergence coin- Argentina) and in the USA (Florida) (Maatouf cides with that of the host, so that they can and Lumaret, 2012). parasitise the host eggs (Kim et al., 2011). Host plant: the pest attacks diff erent species Observed parasitisation: based on person- of Eucalyptus (Myrtaceae). al observations conducted in the town of Material examined: Benitses, 39°32΄N, Corfu, 55 galls were observed (1-3 for single 19°54΄E, 6 m a.s.l., 16.VIII.2013, galls and leafl ets) on a totally of 30 attacked preleved adults on Eucalyptus camaldulensis. leaves, with 32 emerged specimens of P. ro- Biological remarks: L. invasa is particular- biniae.

Hymenoptera, Encyrtidae of these pests, the agromyzid Phytoliriomy- za jacarandae, is new to the Greek fauna. Psyllaephagus bliteus Riek 1962 Moreover, the presence of two parasitoid Native range: species native to Australia. wasps, Platygaster robiniae (Hymenoptera, Distribution: it spread to New Zealand, Bra- Platygastridae) and Psyllaephagus bliteus zil, Spain, Italy (including Sicily and Sardin- (Hymenoptera, Encyrtidae) obtained from ia), Greece (Corfu), Morocco and Algeria and Obolodiplosis robiniae and Glycaspis brimble- is due to an accidental introduction, proba- combei, respectively, are also reported. The bly together with its host (Bella and Rapisar- introduction of all new recorded alien in- da, 2013; Reguia and Peris-Felipo, 2013). For sects must be considered accidental; also psyllid biological control programmes, P. the two associated antagonists were most bliteus has been deliberately introduced to probably introduced together with their the USA (California), Mexico and Chile (Bel- hosts, as has already happened in other Eu- la, 2013). ropean countries. Host: P. bliteus is a specifi c parasitoid of the In the Palaeartic region, the only records invasive Red gum lerp psyllid, Glycaspis brim- of Phytoliriomyza jacarandae are in Italy blecombei, a pest on diff erent species of Eu- (mainland and Sicily) and Portugal; it was calyptus (Myrtaceae). probably imported to these countries and to Material examined: Benitses, 39°32΄N, Greece with infested ornamental Blue jaca- 19°54΄E, 6 m a.s.l., 16.VIII.2013, found to par- randa trees (Bella et al., 2007; Bella, 2013). asitize nymphal instars of G. brimblecombei The detected species show a high level infesting Eucalyptus camaldulensis. of host-plant specifi city, and their dispersion Biological remarks: P. bliteus is an endopar- is related to the presence of their exotic host asitoid that delays development until the plants, thus they should remain restricted to psyllid host reaches the late fourth or fi fth artifi cial habitats, such as nurseries, parks, instars. It pupates within the remains of the gardens and urban areas. However, two spe- host. Adults have a metallic green body, the cies, Corythucha ciliata and Cacyreus mar- female with darker antennae and more pu- shalli, can spread to natural environments bescent than the male. Their lifespan de- and attack spontaneous plants. pends on the temperature. The biological The rapid colonisation in Mediterrane- cycle completes between 16 and 41 days, an countries by the psyllid Glycaspis brimble- depending greatly on weather conditions combei can represent a more serious threat, (Bella and Rapisarda, 2013). with both economic and ecological impacts, Observed parasitisation: personal observa- because of the large diff usion of Eucalyptus tions made during summer 2013 in the town trees used for extensive reforestations (Bella of Benitses: from a total of 713 lerps (500 and Rapisarda, 2013). The spontaneous dis- examined leaves of E. camaldulensis), 168 persal of the psyllid’s exotic parasitoids also nymphs (23.6%) of G. brimblecombei result in Greece leads to a remarkable interest in were parasitised. the biological control of the pest, as already shown in the countries where it has been found. The rapid colonisation of European Discussion countries by alien pests requires continuous investigation of their possible impacts and In the present contribution, seven alien in- population dynamics. sect species (1 Hemiptera, Psyllidae; 1 Hemi- ptera, Tingidae; 1 Diptera, Cecidomyiidae; 1 Diptera, Agromyzidae; 1 Lepidoptera, Lycae- nidae; 1 Hymenoptera, Eulophidae) asso- I thank Paola Giambertone (Sesto S. Giovanni, ciated with non-indigenous ornamental Italy) for the collaboration during collection of plants on Corfu (Greece) are recorded. One samples.

Literature cited Longo, S. 2004. Note sul Licenide sud-africano dei gerani Cacyreus marshalli (Lepidoptera Lyceni- Bella, S. 2007. Presenza di Obolodiplosis robiniae dae) nell’Italia meridionale. Tecnica Agricola, (Haldeman, 1847) in Italia centro meridionale e 55(4) (2003): 3-11. in Sicilia (Diptera Cecidomyiidae). Bollettino di Lu, C.K., Buhl, P.N., Duso, C., Zhao, C.M., Zhang, J.S., Zoologia agraria e di Bachicoltura, Ser. II 39 (3): Ji, Z.X., Gao, S.H., Yu, J.Y. and Wen X.L. 2010. First 239-242. discovery of Platygaster robiniae (Hymenoptera: Bella, S. 2013. New alien insect pests to Portugal on Platygastridae) parasitizing the invasive Obo- urban ornamental plants and additional data lodiplosis robiniae (Diptera: Cecidomyiidae), a on recently introduced species. Annales de la gall maker in China. Acta Entomologica Sinica, Société entomologique de France (N.S.), 49(4): 53(2): 233-237. 374-382. Maatouf, N. and Lumaret, J.P. 2012. Eco-ethology of Bella, S. and Rapisarda, C. 2013. 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The red gum lerp psyllid, Glycaspis brimblecombei, a new exotic pest of Eucalyptus camaldulensis in Italy. Bulletin of Insectology, 63: 233-236. Received: 6 June 2014; Accepted: 9 July 2014

Χωροκατακτητικοί εντομολογικοί εχθροί και τα παρασιτοειδή τους σε καλλωπιστικά φυτά του αστικού περιβάλλοντος της Κέρκυρας - Phytoliriomyza jacarandae Steyskal and Spencer 1978 (Diptera, Agromyzidae) νέα καταγραφή στην Ελλάδα

S. Bella

Περίληψη Η παρούσα εργασία παρουσιάζει τα αποτελέσματα πρόσφατων επισκοπήσεων για ξενι- κά είδη εντόμων σε καλλωπιστικά φυτά στο αστικό περιβάλλον της Κέρκυρας. Συνολικά καταγράφη- καν επτά ξένα είδη τα οποία σχετίζονται με αλλόχθονα καλλωπιστικά φυτά: Acizzia jamatonica (Ku- wayama 1908), Glycaspis brimblecombei Moore 1964 (Hemiptera, Psyllidae), Corythucha ciliata (Say 1832) (Hemiptera, Tingidae), Obolodiplosis robiniae (Haldeman 1847) (Diptera, Cecidomyiidae), Phyto- liriomyza jacarandae Steyskal and Spencer 1978 (Diptera, Agromyzidae), Cacyreus marshalli Butler 1898 (Lepidoptera, Lycenidae) και Leptocybe invasa Fisher and La Salle 2004 (Hymenoptera, Eulophidae). Αυτή είναι η πρώτη αναφορά του Phytoliriomyza jacarandae, υπονομευτής του Jacaranda mimosifolia D. Don. (Bignoniaceae), στην Ελλάδα. Επίσης καταγράφηκαν δύο υμενόπτερα παρασιτοειδή, Platyg- aster robiniae Buhl and Duso 2008 (Hymenoptera, Platygastridae) και Psyllaephagus bliteus Riek 1962 (Hymenoptera, Encyrtidae), των Obolodiplosis robiniae και Glycaspis brimblecombei, αντίστοιχα. Παρου- σιάζονται λεπτομέρειες για την τρέχουσα γεωγραφική κατανομή, ξενιστές και βιολογικά χαρακτηρι- στικά κάθε είδους.

Hellenic Plant Protection Journal 7: 53-59, 2014