Hellenic Plant Protection Journal 11: 54-58, 2018 DOI 10.2478/Hppj-2018-0007

Hellenic Plant Protection Journal 11: 54-58, 2018 DOI 10.2478/hppj-2018-0007

SHORT COMMUNICATION

First record of parasitoids associated with insects inhabiting capsules of Papaver rhoeas in Greece

F. Karamaouna1*, M. Samara1, V. Kati1 and M.-D. Mitroiu2

Summary A faunistic complex of chalcidoid parasitoids (Hymenoptera: Chalcidoidea) associated with cynipids and cecidomyids (Hymenoptera: Cynipidae; Diptera: Cecydomyiidae) inhabiting capsules of the annual weed Papaver rhoeas L. (corn poppy) was recorded in Amynteo, Northern Greece (2012) and Orchomenos, Voeotia, Central Greece (2013). The parasitoids are Idiomacromerus papaveris (Forst- er, 1856), Idiomacromerus sp., Pseudotorymus papaveris (Thomson, 1876) (Torymidae), Aprostocetus epicharmus Walker, 1839 (Eulophidae), and Cyrtoptyx sp. (Pteromalidae). Aprostocetus epicharmus was recorded only in Amynteo while Idiomacromerus spp. and Cyrtoptyx sp. only in Voeotia. This is the fi rst record of these parasitoid species in corn poppy capsules in Greece. All parasitoids except the eulo- phid, which probably parasitizes Cecydomyiidae, are most likely parasitoids of Aylax papaveris (Perris, 1840) (Cynipidae).

Additional keywords: Aprostocetus epicharmus, Aylax papaveris, Cyrtoptyx sp., gall, Idiomacromerus papaveris, Pseudotorymus papaveris

A complex of chalcidoids (Hymenoptera: Andriescu, 1962 (Hym.: Torymidae) is the Chalcidoidea) was recovered from mature, only parasitoid species associated with corn dry capsules of the winter annual weed Pa- poppy capsules that has been previously re- paver rhoeas L. (corn poppy, common pop- ported in Greece (Askew et al., 2006). py) (Papaveraceae), which were collected Adult females and males of P. papaveris from Amynteo, Florina, Northern Greece were recorded upon emergence from the P. in 2012, and Orchomenos, Voeotia, South- rhoeas capsules in both regions. In the cap- ern Greece in 2013. The parasitoids are Idi- sules from Amynteo, together with the par- omacromerus papaveris (Förster, 1856), Idi- asitoid specimens, we obtained an adult omacromerus sp., Pseudotοrymus papaveris female of Aylax papaveris (Perris) (Hym.: Cyn- (Thomson, 1875) (Torymidae), Aprostocetus ipidae) and found infestation by Cecidomyi- epicharmus Walker, 1839 (Eulophidae), and idae larvae (Diptera), most likely Dasineura Cyrtoptyx sp. (Pteromalidae). Aprostocetus papaveris Winnertz. epicharmus was recorded only in Amynteo Pseudotorymus papaveris is probably a while Idiomacromerus spp. and Cyrtoptyx sp. parasitoid of A. papaveris and the cecidomy- only in Voeotia. Identifi cations of the parasi- iid while A. epicharmus is a parasitoid of the toids have been made based on Bouček and cecidomyiid (Figure 1). Pseudotοrymus pa- Rasplus (1991) and Medvedev (1978). To our paveris has a Palaearctic geographical dis- knowledge, this is the fi rst record in Greece tribution (Nikol’skaya and Zerova, 1978; of these parasitoids occuring in corn pop- Grissell, 1995; Noyes, 2017). Popescu (2002) py capsules. Chalcimerus borceai Steff an and reported the emergence of P. papaveris from A. papaveris and D. papaveris, infesting P. rhoeas and P. dubium L. capsules, and from 1 Benaki Phytopathological Institute, 8 St. Delta str., GR their predator Lestodiplosis callida Winnertz 145 61 Kifi ssia, Attica, Greece. (Diptera: Cecidomyiidae). Aprostocetus epic- 2 Alexandru Ioan Cuza University of Iasi, Faculty of Biol- ogy, 700505 Iasi, Romania. harmus has been reported (as Tetrastichus * Corresponding author: [email protected] epicharmus (Walker)) parasitising the bras-

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Figure 1. Suggested interrelations a) between the parasitoids Pseudotorymus papaveris and Aprostocetus epicharmus, and the herbivores Aylax papaveris and a cedidomyiid (samples from Northern Greece) and b) between the parasitoids Pseudo- torymus papaveris, Idiomacromerus papaveris and Cyrtoptyx sp., and the host A. papaveris (samples from central Greece), in Papaver rhoeas capsules. Colored arrows indicate the various associations (green for herbivory, blue for parasitism, red for hyper-parasitism) (Images by M. Samara, V. Kati).

© Benaki Phytopathological Institute 56 Karamaouna et al. sica pod midge, Dasineura brassicae (Win- individual gall chambers originate from the nertz) (Diptera: Cecidomyiidae), in Poland transformation of the septum and seeds, (Czajkowska, 1978) and the raspberry cane usually causing deformation and enlarge- midge, Resseliella theobaldi (Barnes) (Dip- ment of the capsules (mainly in P. rhoeas and tera: Cecidomyiidae), in Hungary (Vètek et P. dubium). Internal septa and seeds disap- al., 2006). pear (Pujade-Villar, 2015). Dasineura papav- Aylax papaveris is one of the three Cyn- eris is a monophagous bivoltine gall midge ipidae species inducing capsule galls in P. of Papaver spp. capsules, which have a nor- rhoeas, P. dubium, P. argemone L. and P. som- mal appearance after infestation and only niferum L., the other two species being Bar- when opened the clearly swollen septa are botinia oraniensis (Barbotin) and Aylax mi- visible (Skuhravá and Skuhravý 1997; Pope- nor Hartig, 1840 (Pujade-Villar, 2015; Gómez scu 2002). et al., 2017). Aylax papaveris forms light yel- In the capsules from Voeotia, we en- low fused galls, irregular oval or globular countered galls by the cynipid gall wasp A. in shape, highly variable in size, including papaveris (Figure 2) and the parasitoids Idi- a few dozen larval chambers arranged per- omacromerus spp. (three male specimens, pendicularly to the vertical capsule axis. The probably I. papaveris, although it is diffi cult

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Figure 2. Papaver rhoeas capsules a) infested by cynipid gall wasp, b) capsule with the gall (10x), c) gall with the cynipid gall wasp (10x) and d) Aylax papaveris (Hym.: Cynipidae) before emergence (40x) (Images by M. Samara).

© Benaki Phytopathological Institute Parasitoids of insects infesting corn poppy capsules in Greece 57 to be certain without any females, Idiomac- in the West Palearctic. Zootaxa, 1301: 1-60. romerus sp. (1 male) (diff erent from I. papav- Baratella, V. 2008. Biological Control and Integrat- eris in the coloration of tibiae), and Cyrtop- ed Pest Management of olive fl y Bactrocera oleae (Rossi) (Diptera: Tephritidae): A briefl y review. tyx sp. (1 male). Pomologia Croatica, 14: 129-142. A possible scenario is that P. papaveris, I. Bellido, D. and Pujade-Villar, J. 1999. Especies asoci- papaveris and Cyrtoptyx sp. are parasitoids adas a agallas se cinipidos de Pirineo andorrano of A. papaveris, although no Cyrtoptyx sp. (Hym.: Cynipoidea. Chalicidoidea, Ichneumo- has ever been reared from Aylax (Figure 1). noidea). Boletín de Asociación Española de Ento- mología, 23(1-2): 277-291. Cyrtoptyx sp. might as well be a hyperparasi- Bouček, Z. and Rasplus, J.-Y. 1991. Illustrated key to toid of the torymids. Idiomacromerus papav- West-Palaearctic genera of Pteromalidae (Hy- eris has been reported to parasitise A. papav- menoptera: Chalcidoidea). Institut National de eris (in Croatia, France, Hungary, Romania, la Recherche Agronomique Paris. Spain) and A. minor (in Andora, France, Ro- Czajkowska, M. 1978. Investigations on the brassica mania, Spain) in Papaver galls (Askew et al., pod midge (Dasyneura brassicae Winn.). IV. Spe- cies composition and importance of parasites. 2006). Idiomacromerus papaveris is widely Roczniki Nauk Rolniczych (Seria E, Ochrana Ros- distributed from Iran to U.K. (Noyes, 2017). lin) 8(2): 159-175. Some Cyrtoptyx species have been report- Gómez, J.F., Hernández Nieves, M., F. Gayubo, S.F., ed to parasitise cynipid gall wasps e.g. Cyr- Nieves-Aldrey, J.L. 2017. Terminal-instar larval toptyx robustus (Masi, 1907) on Cynips disti- systematics and biology of west European species of Ormyridae associated with insect galls cha Hartig, 1840 on Quercus (Nieves Aldrey, (Hymenoptera, Chalcidoidea). ZooKeys, 644: 51– 1982; Bellido and Pujado-Villar, 1999) in 88 (2017) doi: 10.3897/zookeys.644.10035 http:// Spain; others are parasitoids of fruit fl ies, e.g. zookeys.pensoft.net Cyrtoptyx latipes (Rond.) on the olive fruit fl y, Grissell, E.E. 1995. Torymidae (Hymenoptera: Chalic- Bactrocera oleae (Rossi) (Diptera: Tephriti- idoidea: Torymidae) a redefi nition, generic clas- ifi cation, and adnotated world catalog of spe- dae) (Baratella, 2008). cies. Memoirs of Entomology, International, vol. The sampled parasitoid species and their 2, Associated Publishers, Gainesville, Florida, hosts are associated with the natural vegeta- U.S.A., 470 p. tion in agricultural systems of diff erent inten- Medvedev, G.S. (ed.) 1978. Keys to the Insects of sity in terms of cultivation and pesticide use, the European Part of the USSR. Volume III Hy- aff ecting the abundance and species diver- menoptera, Part II. Academy of Sciences of the USSR, Institute of Zoology, Leningrad. sity of spontaneous plants: P. rhoeas plants Mirumjan, L. 2011. Phytophagous gall midges (Dip- were located in uncultivated land around tera: Cecidomyiidae) of Armenia. Acta Societatis the grape-producing area of Amynteo and Zoologicae Bohemicae, 75: 87-105. in the intensively cultivated arable crop area Nieves-Aldrey, J.L., Gómez, J.F., Askew, R.R. 2007. Two of Voeotia. Our fi ndings highlight the im- New Species of Idiomacromerus (Hymenoptera: portance of natural or semi-natural areas Torymidae) from the Stem Gall Wasp on Papaver somniferum, with Notes on the Parasitoid Com- for the maintenance of these species. Fur- munity. Annals of the Entomological Society of ther studies are necessary to clarify the ex- America, 100(3): 381-389. act trophic relations among the Hymenop- Nikol’skaya, M.N. and Zerova, M.D. 1978. Familiy To- tera pararasitoids and the hosts found in the rymidae (Callimomidae) (Torymids), in Medve- P. rhoeas capsules, as well as their potential dev, G.S. Ed., Keys to the Insects of the Europe- an part of the USSR, 3(2), New Delhi, 651-685 role in ecosystem services through the bio- (transl. from Russian by Amerind Published Co., logical control of the corn poppy. 1987). Noyes, J.S. 2017. Universal Chalcidoidea Data- base, Natural History Museum London. Availa- Literature cited ble from: www.nhm.ac.uk/entomology/ chalcidoids/index.html. (Accessed: 10-04-2017). Askew, R.R., Plantard O., Gomez, J.F., Nieves, M.H., Popescu, I.E. 2002. Contributions to the Knowledge and Nieves-Aldrey, J.L. 2006. Catalogue of par- of the Torymid Wasps (Hymenoptera, Chalci- asitoids and inquilines in galls of Aylacini, doidea, Torymidae) from the “Maritime Dune Diploledidini ans Pediaspidini (hym., Cypinidae) Natural Reserve from Agigea” (Constanţa, Ro-

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ΣΥΝΤΟΜΗ ΑΝΑΚΟΙΝΩΣΗ

Πρώτη καταγραφή παρασιτοειδών σε έντομα Cynipidae και Cecidomyidae σε κάψες παπαρούνας, Papaver rhoeas, στην Ελλάδα

Φ. Καραμαούνα, Μ. Σαμαρά, Β. Κατή και M.-D. Mitroiu

Περίληψη Στην εργασία παρουσιάζεται ένα σύμπλεγμα παρασιτοειδών σε έντομα Cynipidae και Cecydomyiidae που προσβάλλουν τις κάψες του ετήσιου ζιζανίου Papaver rhoeas (κν. παπαρού- να), όπως καταγράφηκε στις περιοχές του Αμύνταιου Φλώρινας (2012) και του Ορχομενού Βοιωτίας (2013). Τα παρασιτοειδή ανήκουν στα είδη Idiomacromerus papaveris (Forster, 1856), Idiomacromerus sp., Pseudotorymus papaveris (Thomson, 1876) (Torymidae), Aprostocetus epicharmus Walker, 1839 (Eulophidae), και Cyrtoptyx sp. (Pteromalidae). Το A. epicharmus καταγράφηκε μόνο στο Αμύνταιο ενώ τα Idiomacromerus spp. και Cyrtoptyx sp. στη Βοιωτία. Πρόκειται για την πρώτη καταγραφή των παρα- σιτοειδών αυτών σε κάψες παπαρούνας στην Ελλάδα. Όλα τα παρασιτοειδή, εκτός από το Eulophidae, το οποίο πιθανόν παρασιτεί δίπτερα της οικογένειας Cecydomyiidae, φαίνεται να είναι παρασιτοειδή του υμενόπτερου Aylax papaveris (Perris, 1840) (Cynipidae).

Hellenic Plant Protection Journal 11: 54-58, 2018