Entomologia Hellenica

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ENTOMOLOGIA HELLENICA

Vol. 27, 2018

First record of the bug Thaumastocoris peregrinus in Greece

Petrakis Panos Hellenic Agricultural Organization – “Demeter”; Institute for Mediterranean Forest Ecosystem Research, Laboratory of Entomology https://doi.org/10.12681/eh.18703

To cite this article:

Petrakis, P. (2018). First record of the bug Thaumastocoris peregrinus in Greece. ENTOMOLOGIA HELLENICA, 27(1), 1-9. doi:https://doi.org/10.12681/eh.18703

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SHORT COMMUNICATION

First record of the bug Thaumastocoris peregrinus in Greece

P.V. PETRAKIS Hellenic Agricultural Organization – “Demeter”, Institute for Mediterranean Forest Ecosystem Research, Laboratory of Entomology, Athens, Greece

ABSTRACT The Australian bug species Thaumastocoris peregrinus Carpineto et Dellapè (Hemiptera: Thaumastocoridae) is reported for the first time in Greece. This is a sap-sucking consumer (mesophyll feeder) of Eucalyptus spp. foliage. Feeding damage and the egg batches of the insect were found in several locations in 2016. This invasive species recently has been recorded from Portugal, Spain, and Italy. Although in Greece there are no currently forest plantations of eucalypts (experimental plantations exempted), this insect is a serious pest of these trees in roadside verges and city parks.

KEY WORDS: pest distribution, Eucalyptus, invasive species, Thaumastocoris peregrinus.

Introduction considered rare (Cassis et al. 1999) but over the past twenty years, it has exploded to Thaumastocoris peregrinus Carpineto et become a serious pest (Noack and Rose Dellapè (Hemiptera: Thaumastocoridae) 2007, Noack et al. 2011, EPPO 2014). The (bronze bug) is a pest of several Eucalyptus cause of the expansion of the geographical and Corymbia species. This insect is native range of T. peregrinus is not known but in to The Australian state of New South Wales all likelihood, its invasion is mediated by (Cassis and Gross 1995), and is now human commerce and travel. widespread in Queensland and South In this paper I report the first occurrence Australia (Noack et al. 2011). It is spreading of T. peregrinus in Greece. through Africa, Europe and South and Central America (FAO 2012). CABI (2017) Materials and Methods lists its current distribution, highlighting its invasion to most continental regions of the A search of invasive insects, including T. world. Laudonia and Sasso (2012) and peregrinus, was based on examination of Garcia et al. (2013) document its European plant material from across, mostly in central distribution. T. peregrinus is found in and southern Greece. Plant material Portugal, Spain (Vivas et al. 2015), Italy consisted of branches above 3m, with a including Sicily and Sardinia (Laudonia and length of ca.50 cm, which were packed and Sasso 2012), Israel (Novoselsky and sealed in paper bags to prevent escape of Freiberg 2016) and Albania (van der Heyden this insect and simultaneously to avoid 2017). The insect has been moved in the decay. The material was collected by two ‘Alert list’ of EPPO (2012a,b). It was

*Corresponding author: [email protected]

http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 20/02/2020 21:51:25 | 2 ENTOMOLOGIA HELLENICA 27 (2018): 1-9 foresters (authorized prefecture plant oil. In general these traps are proved to be sanitary inspectors) in each forest and efficient method for the sampling of T. roadside locale, who forwarded the material peregrinus even for detailed studies (e.g. to the Entomology laboratory in Athens, in population dynamics in Nadel et al. 2014). the Institute for the Mediterranean Forest The identification of the insect was Ecosystems (IMFE). Many roadside planted based on morphological characters given in eucalypts in all prefectures, mostly in central the identification key of Noack et al. (2011) and southern Greece were sampled in this and photomicrographs of Garcia et al. (2013) and Laudonia and Sasso (2012). way. Our laboratory is authorized to Voucher specimens are deposited in the examine eucalypts in Greece for the insect collection at IMFE, Athens. presence of Gonipterus scutellatus Gyllenhal (Coleoptera: Curculionidae), Results under the auspices of the EU program “National survey program for the We examined more than 350 samples (Fig. recognition and maintenance of protected 1). The insect was first found on road zones against organisms harmful to plants margin trees from Itea, Fokis prefecture and (quarantine pests)”. later in the city park at Peristeri, Attica. The When the bronze appearance of leaves insect body is dorso-ventrally compressed was detected together with feeding damage with length 2-3.5 mm. The head is broad and of T. peregrinus then the site revisited to bears pedicellate eyes (Fig. 2A and B). The search for this invasive insect. Further sites mandibular plates are very conspicuous, were inspected with Eucalyptus elongate, and easily seen in the field. The camaldulensis Dehnh., E. sideroxylon color varies from yellow to yellow-greenish A.Cunn. ex Woolls, E. viminalis Labill. in and brownish with sporadically darker areas. the garden of IMFE (Athens, Attica), and The eggs are black and are laid in the Corymbia citriodora Hook. on the island of underside of eucalypt leaves where the Corfu. One to five infested trees per site insect is usually found. The neonate and were sampled two or three times between young nymphs of the insect are straw yellow April and June. Also, insects were collected in color. by fumigating eucalypt trees with summer The number of insects found at Itea is oil (Vicol, Vicchem, Australia) using a 4 x 4 showed in Table 1 as an example. Many meters cloth panel spread on the ground leaves of the tree are damaged and in a few underneath fumigated trees to collect the days, they will become the characteristic bronze color (Fig. 3). No measurement of insects that dislodge from the foliage. leaf photosynthesis or stomatal conductance In places with substantial eucalypt was made but presumably the vegetation (Corinth, Patras [Achaea], photosynthetic rate at these leaves is reduced Vonitsa [Aitolia/Akarnania], Marathon, (Wilcken et al. 2010). Philothei, Maroussi, and Metamorphosis Positive records of T. peregrinus where [Attica]) we sought the presence of T. fumigation took place are the abandoned peregrinus, and other insects as well, by eucalypt plantation in Aitolia/Akarnania means of delta traps bearing the artificial (Vonitsa, Menidi), Corinth, Cyclades attractant 3-methylbut-2-enyl butanoate (Sifnos, Syros, and Tenos), and Attica (Gonzalez et al. 2012) together with three 30 (Peristeri, Philothei, Metamorphosi, Lavrio) x 20 cm sticky boards, bearing no attractant, (Fig. 1). The fumigations of trees with no made by plywood and hung on the same tree signs of leaf damage did not reveal any T. at a height above 3 meters. In these sites, peregrinus individual despite the fact that eucalypt trees without sticky traps, were several insect species were found in the sprayed with summer oil. The trees bearing catch of the ground collection clothes. sticky traps were not treated with summer

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FIG. 1. Sampling sites in Greece with eucalypts. Examined sites are represented by empty circles and full circles are sites with eucalypt foliage bearing with Thaumastocoris peregrinus. A symbol may correspond to more than one site of examination. The site at Itea, Fokis where the insect was found for first time is indicated with an arrow.

TABLE 1. Excerpt from the table listing the individuals of Thaumastocoris peregrinus found on Eucalyptus camaldulensis branches grown at roadsides at one of the sites searched in Itea, Fokis. Each line represents one sample corresponding to one branch on a specific date. Sample Date Tree Branch Branch T. peregrinus (sn) (yyyymmdd) number number mass (g) males females Nymphs 1 20170612 1 1 452 13 8 0 2 20170925 1 2 568 25 37 0 3 20170925 2 1 268 2 8 0 4 20170925 3 1 374 8 12 0 5 20170925 3 3 455 11 10 0

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(A)

(B) FIG. 2. Adult male (A) and penultimate instar nymph (B) of Thaumastocoris peregrinus. Τhe right hemelytron of the adult is removed. Both individuals have been collected from a city park in Peristeri, Attica.

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FIG. 3. The underside of the leaf blade and the associated leaf damage (chlorotic leaf areas and areas with initiation of bronzing) caused by Thaumastocoris peregrinus is shown. The leaf in a few days becomes bronze in color, hence the vernacular name of the insect ‘bronze bug’.

Discussion (Heteroptera: Reduviidae) (Petrakis and Moulet 2011) were seen to predate upon This work reports T. peregrinus for first caged T. peregrinus (PVP personal time in Greece. This species was recorded at observation). The latter species feeds by several areas and in some cases at high sticking the prey on its front legs or population densities. In the ‘Invasive impeding the movements of T. peregrinus in Species Compendium’ CABI (2017) is a way very similar to the reduviid bug stated that there is a risk of introduction of Atopozelus opsimus Elkins, which predates T. peregrinus in Greece since the climate of the same insect in Brazil (Wilcken et al. Greece is very similar to that of Sydney, 2010). The predatory bug Supputius Australia where T. peregrinus originated and cicnctipes Stal (Heteroptera, Pentatomidae, gave outbreaks since 2002. Similarly, T. Asopinae) has been reported as an efficient peregrinus has been established in South native natural enemy of T. peregrinus in Africa where it is active throughout the year Brazil (Souza et al. 2012). Although the (Nadel et al. 2014). densities of natural enemies in Greece at a We speculate that the main invasion unit area basis are considered high, usually pathway of this insect is through its egg biological control results in difficulties in masses on eucalypt timber and seedlings (as but not the preclusion of the establishment speculated by Souza et al. (2012) for the of invasive insects (Mattson et al. 2007). introduction of the insect in Brazil). An The insect was recorded at high numbers additional pathway could be the compost of and thus, in certain cases management ornamental plants. measures might be required that should be The occurrence of natural enemies, such fully decided by Phytosanitary Authorities. many species of Eupelmidae and Trade-offs associated with the impacts of T. Trichogrammatidae egg parasitoids and peregrinus and the consequences of any adult feeders in Mymaridae may prevent the regulatory action such as the sprayings of spread of T. peregrinus in several Greek road verges, restriction of importation from sites. Moreover, quite common native countries where the insect is already natural enemies such as Nabis viridis Brullé, established or intensification of inspections (Heteroptera: Nabidae) and the introduced associated with imported eucalypts have to Nearctic species Zelus renardii Kolenati be carefully designed. Any application of www.entsoc.gr © 2018 Hellenic Entomological Society

http://epublishing.ekt.gr | e-Publisher: EKT | Downloaded at 20/02/2020 21:51:25 | 6 ENTOMOLOGIA HELLENICA 27 (2018): 1-9 insecticides should be weighed against the and S.J. Frankel. 2010. Historical increase of the implementation costs accumulation of nonindigenous forest together with the suppression of the activity pests in the continental United States. of native natural enemies (Aukema et al. BioScience 60: 886-897. 2010). CABI. 2017. Datasheet report for Further search may focus on testing delta Thaumastocoris peregrinus (bronze traps loaded with the synthetic artificial attractant (Gonzalez et al. 2012) 3- bug). In: Invasive Species Compendium. methylbut-2-enyl butanoate. The attractant Wallingford, UK: CAB International. was applied in cellulose acetate microfibers [www.cabi.org/isc] for 8 weeks (Iliou 2017). Our preliminary Cassis, G. and G.F. Gross. 1995. Hemiptera: results using a nanotechnology-based Heteroptera (Coleorryncha to formulation of the above-mentioned insect Cimicomorpha). In: Houston, W.W.K. attractant supplied by Professor V. Roussis and G.V. Maynard (Eds). Zoological (National Capodistrian University of Catalogue of Australia. Melbourne, Athens, School of Pharmacy, Sector of CSIRO Australia, pp. 1-506. Pharmacognosy) are very promising. Suggestions for future research on this insect Cassis, G., R.T. Schuh and H. Brailovsky. also include DNA barcoding on several 1999. A review of Onymocoris populations to reveal the origin and the time (Heteroptera: Thaumastocoridae), with a passed since its establishment in Greece, new species, and notes on hosts and according to Nadel et al. (2010). distributions of other thaumastocorid species. Acta Soc. Zool. Bohemoslov. Acknowledgements 63: 19-36. EPPO. 2012a. EPPO Reporting Service: The contribution of the great number of 2012/147 Addition of Thaumastocoris foresters collaborating to our Entomology peregrinus to the EPPO Alert List. NO. lab is greatly acknowledged. More precisely 07 PARIS, 2012-07-01. the Phytosanitary Inspectors (foresters) and [http://archives.eppo.int/EPPOReporting/ the Forest Director (forester) of Heraklion, 2012/Rse-1207.pdf] Laconia, Corinth, Achaea, Ilia, Arcadia, Argolis, Cyclades, Dodecanese, Attica, EPPO 2012b. EPPO Reporting Service: Boeotia, Euboea, Fokis, Fthiotis, Aitolia- 2012/147 Addition of Thaumastocoris Acarnania, Cephalonia, Zakynthos, Corfu, peregrinus to the EPPO Alert List. NO. Lesvos, Magnesia, Thessaloniki, Chalkidiki, 12 PARIS, 2012-12-01. Kavala, are acknowledged with thanks. Dr [http://archives.eppo.int/EPPOReporting/ P. Tsopelas, Dr K. Kaoukis, and N. Soulioti 2012/Rse-1212.pdf] photographs and map substrates. EPPO. 2014. EPPO Reporting Service: 2014/110 Thaumastocoris peregrinus found in Sicilia (IT) NO. 06 PARIS, References 2014-06-01. [http://archives.eppo.int/EPPOReporting/ Aukema, J.E., D.G. McCullough, B. von 2014/Rse-1406.pdf] www.entsoc.gr © 2018 Hellenic Entomological Society

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FAO. 2012. Thaumastocoris peregrinus [https://doi.org/10.1007/s10530-009- (Bronze bug) (Hemiptera: 9524-2] Thaumastocoridae). Forest Pest Profiles Nadel, R.L., M.J. Wingfield, M.C. Scholes, August 2012, pp. 2. J.R. Garnas, S.A. Lawson and B. Garcia, A., E. Figueiredo, C. Valenete, J. Slippers. 2014. Population dynamics of Victor, V.J. Monserrat and M. Branco. Thaumastocoris peregrinus in 2013. First record of Thaumastocoris Eucalyptus plantations of South Africa. peregrinus in Portugal and of the J. Pest Sci. 88: 97-106. DOI neotropical predator Hemerobius 10.1007/s10340-014-0558-6 bolivari in Europe. Bull. Insectol. 66: Noack, A.E. and H.A. Rose. 2007. Life- 251-256. history of Thaumastocoris peregrinus Gonzalez, A., M.V. Calvo, V. Cal, V. and Thaumastocoris sp. in the laboratory Hernandez, F. Dono, L. Alves, D. with some observations on behaviour. Gamenara, C. Rossini and G. Martınez. Gen. Appl. Entomol. 36: 27–33. 2012. A male aggregation pheromone in Noack, A.E., G. Cassis and H.A. Rose. the bronze bug, Thaumastocoris 2011. Systematic revision of peregrinus (Thaumastocoridae). Psyche Thaumastocoris Kirkaldy (Hemiptera: 2012: 868474, [doi:10.1155/2012/868474] Heteroptera: Thaumastocoridae). Heyden van der, T. 2017. The first record of Zootaxa 3121: 1-60. Thaumastocoris peregrinus Carpintero Novoselsky, T. and A. Freidberg. 2016. First & Dellapé, 2006 (Hemiptera: record of Thaumastocoris peregrinus Heteroptera: Thaumastocoridae) for (Hemiptera: Thaumastocoridae) in the Albania. Revta. gad. Entomol. VIII Middle East, with biological notes on its 1:133-135. relations with eucalyptus trees. Israel J. Iliou, K. 2017. Electrospun Entomol. 46: 43-55. micro/nanofibrous matrices as prolonged release systems of insect repellents. MSc Petrakis, P.V. and P. Moulet. 2011. First dissertation, School of Pharmacy, record of the Nearctic Zelus renardii National and Kapodistrian University of (Heteroptera, Reduviidae, Athens, 84 pp. Harpactocorinae) in Europe. Entomol. Laudonia, S. and R. Sasso. 2012. The bronze Hell. 20: 75-82. bug Thaumastocoris peregrinus: a new Souza, G.K., T.P. Pikart, F.C. Pikart, J.E. insect recorded in Italy, damaging to Serrão, C.F. Wilcken and J.C. Zanuncio. Eucalyptus trees. Bull. Insectol. 65: 89- 2012. First record of a native 93. heteropteran preying on the introduced Mattson, W.J., H. Vanhanen, T. Veteli, S. Eucalyptus pest, Thaumastocoris Sivonen and P. Niemela. 2007. Few immigrant phytophagous insects on peregrinus (Hemiptera: woody plants in Europe: Legacy of the Thaumastocoridae), in Brazil. Florida European crucible? Biol. Invasion. 9: Entomol. 95: 517-520. 957–974. Vivas, L., J. Crespo and V. Jacinto. 2015. Nadel, R.L., B. Slippers, M.C. Scholes, S.A. Primer registro de la especie invasora Lawson, A.E. Noack, C.F. Wilcken, J.P. Thaumastocoris peregrinus Carpintero Bouvet and M.J. Wingfield. 2010. DNA & Dellapé, 2006 en España y nuevos bar-coding reveals source and patterns of datos para Portugal (Hemiptera: Thaumastocoris peregrinus invasions in Thaumastocoridae). BV news Publ. South Africa and South America. Biol. Cient. 4: 30-35. Invasion. 12: 1067-1077.

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Wilcken, C.F., E.P. Soliman, de Sá La peregrinus Carpintero and Dellapé Nogueira, L.R. Barbosa, T.K.R. Dias, (Hemiptera: Thaumastocoridae) on P.J. Ferreira-Filho and R.J.R. Oliveira. Eucalyptus in Brazil and its distribution. 2010. Bronze bug Thaumastocoris J. Plant Prot. 50: 210-205.

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Πρώτη αναφορά του Thaumastocoris peregrinus στην Ελλάδα

Π.B. ΠΕΤΡΑΚΗΣ Ελληνικός Γεωργικός Οργανισμός – «ΔΗΜΗΤΡΑ», Ινστιτούτο Μεσογειακών Δασικών Οικοσυστημάτων, Εργαστήριο Εντομολογίας, Αθήνα

ΠΕΡΙΛΗΨΗ Το Αυστραλιανό έντομο Thaumastocoris peregrinus Carpineto et Dellapè (Hemiptera: Thaumastocoridae) αναφέρεται πρώτη φορά στην Ελλάδα. To έντομο απομυζά τα φύλλα του ευκαλύπτου. Η προσβολή των φύλλων και οι ωομάζες βρέθηκαν σε αρκετές περιοχές της χώρας. Το εισβλητικό αυτό είδος έχει αναφερθεί επίσης από την Πορτογαλία, Ισπανία και Ιταλία. Αν και στην Ελλάδα δεν υπάρχουν πλέον φυτείες ευκαλύπτου (με εξαίρεση τις πειραματικές φυτείες), το έντομο αποτελεί σοβαρό παράσιτο αυτών των δένδρων σε παρόδια βλάστηση και σε αστικά πάρκα. Στην παρούσα εργασία παρουσιάζονται όλες οι περιοχές αναζήτησης του εντόμου και οι αναφορές παρουσίας / απουσίας. Επίσης παρουσιάζονται φωτογραφίες μερικών βιολογικών σταδίων του εντόμου.

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