ANTICANCER COMPOUNDS FROM MEDICINAL PLANTS BIOLOGICA NYSSANA 5 (2)  December 2014: 113-121 Ilić Milošević, I. et al.  Tritrophic accociations of Lysiphlebus fabarum… 113 Original Article Received: 5 December 2014 Revised: 18 December 2014 Accepted: 20 December 2014 Tritrophic associations of Lysiphlebus fabarum (Marshall) (Hymenoptera, Braconidae, Aphidiinae) in Serbia Marijana Ilić Milošević1*, Maja Lazarević1, Olivera Petrović-Obradović2, Vladimir Žikić1 1University of Niš, Faculty of Sciences and Mathematics, Department of Biology and Ecology, Višegradska 33, 18000 Niš, Serbia 2Faculty of Agriculture, Nemanjina 6, 11081 Belgrade – Zemun, University of Belgrade, Serbia * Corresponding author: marijanailic83@yahoo.com Abstract: Ilić Milošević, M., Lazarević, M., Petrović-Obradović, O., Žikić, V.: Tritrophic associations of Lysiphlebus fabarum (Marshall) (Hymenoptera, Braconidae, Aphidiinae) in Serbia. Biologica Nyssana, 5 (2), December 2014: 113-121. One hundred and eighty-six tritrophic parasitoid-aphid plant associations were established between Lysiphlebus fabarum and 64 aphids with 148 different plant species from the territory of Serbia. We identified 18 aphid genera of which the genus Aphis was represented by 38 species. The most frequent interactions between the parasitoid and the hosts were the ones of Aphis fabae, A. craccivora and A. ruborum on various plants comprising one third of the total trophic interactions listed here. Key words: parasitoids, trophic chains, distribution, aphids, host plant Apstrakt: Ilić Milošević, M., Lazarević, M., Petrović-Obradović, O., Žikić, V.: Tritrofičke asocijacije vrste Lysiphlebus fabarum (Marshall) (Hymenoptera, Braconidae, Aphidiinae) u Srbiji. Biologica Nyssana, 5 (2), Decembar 2014: 113-121. Na teritoriji Srbije je sada ustanovljeno 186 tritrofičkih asocijacija između parazitoida, biljnih vaši i biljaka. Vrsta Lysiphlebus fabarum je registrovana na 64 vrste biljnih vaši koje napadaju 148 biljnih vrsta. Utvrđeno je da se biljne vaši grupišu u 18 različitih rodova, od kojih je najzastupljeniji bio rod Aphis sa 38 vrsta. Najčešće parazitirane vrste biljnih vaši od strane L. fabarum bile su Aphis fabae, A. craccivora i A. ruborum prikupljene sa mnogih biljaka, formirajući oko jednu trećinu svih zabeleženih trofičkih interakcija. Key words: parazitoidi, trofički lanci, distribucija, biljne vaši, biljke Introduction The subfamily Aphidiinae (Hymenoptera: Aphidiidae) represents a small group of solitary endoparasitoid wasps of aphids including many important species acting as biological control agents (B r e w e r & E l l i o t t , 2004; L e v i e et al., 2005). They are very useful in crop fields, as well as in greenhouses and non-arable fields such as meadows and forests reducing the number of pest aphids 5 (2) • December 2014: 113-121 BIOLOGICA NYSSANA 5 (2)  December 2014: 113-121 Ilić Milošević, I. et al.  Tritrophic accociations of Lysiphlebus fabarum… 114 (S t a r ý , 1970, 1974; H a g v a r & H o f s v a n g , 1991; K a v a l l i e r a t o s et al., 2004). One genus in subfamily Aphidiinae which has been studied in detail is Lysiphlebus Foerster, which comprises about 25 species worldwide, 16 occuring in the European fauna (Y u et al, 2013; van Achterberg, 2013). On the territory of Serbia, ten species were recorded including the two that have already been introduced here: L. orientalis Starý & Rakhshani, 2006 and L. testaceipes (Cresson, 1880) (P e t r o v i ć et al., 2013; Ž i k i ć et al., 2015). According to the wing venation, this genus could fall into two species groups. The “fabarum” group includes the species with a long metacarpal vein while in “testaceipes” group the species have a short metacarpal vein (P e t r o v i ć et al., 2015). Lysiphlebus fabarum (Marshall, 1896) is a polyphagous aphid parasitoid that attacks more than a hundred of aphid species in various habitats (Y u et al., 2013). They often exploit small aphids, usually from the genus Aphis L., including some serious pests, e.g. the black bean aphid, A. fabae Scopoli, the cowpea aphid, A. craccivora Koch and the cotton aphid, A. gossypii (Glover) (K a v a l l i e r a t o s et al., 2004; S t a r ý , 2006) but also the target aphid genus for L. fabarum is Brachycaudus van der Goot, e.g. the plum-thistle aphid, B. cardui (L.) and the leaf-curling plum aphid, B. helichrysi (Kaltenbach). Likewise, the species L. fabarum has a tendency to attacks the ant- protected aphid colonies. Its distribution is very wide, including the whole Palaearctic, as well as Australia and Oceania. In Europe, L. fabarum is found in the fauna of Andorra, Bulgaria, the Canary Islands, Corsica, Croatia, Czech Republic, France, Germany, Great Britain, Greece, Hungary, Italy, Latvia, Lithuania, Madeira, Montenegro, Poland, Russia, Sicily, Slovakia, Slovenia, Spain, and The Netherlands. There are few studies regarding tritrophic associations of L. fabarum, and its diversity in agroecosystems in Serbia (T o m a n o v i ć & B r a j k o v i ć , 2001; K a v a l l i e r a t o s et al., 2004; Ž i k i ć et al., 2012). In this study we present the parasitoid-aphid- plant trophic associations of L. fabarum registered on the territory of Serbia. The knowledge about parasitoid-aphid-plant associations appears to be necessary for a better implementation of programs of biological control of aphids as an economically important group of pests. Also, host-plant associations are important for better knowledge of biodiversity of species L. fabarum. Material and methods We used the data from the collections of Lysiphlebus fabarum sampled during the period 1989-2014 from numerous localities throughout Serbia. Our samples represent cut branches infested by aphids, sometimes with visible signs of parasitization. This plant material., with or without mummified aphids, was put in small plastic mesh- covered boxes to enable ventilation, and then placed in a growth cabinet (22.5°C, 65% relative air humidity, 16:8 h, light:dark photoperiod) until the parasitoid emergence. Before leaving the samples in the growth cabinet, some live adult aphids were preserved in 90% ethyl-alcohol for identification. Parasitoid material and plants were deposited at the Faculty of Sciences and Mathematics, Department of Biology and Ecology, University of Niš, Serbia and the Faculty of Biology, University of Belgrade, Serbia. In order to obtain some data relevant literature was used (Ž i k i ć et al., 2012). The aphids used in this study were from the collection of Dr Olivera Petrović-Obradović (Faculty of Agriculture, University of Belgrade, Serbia). The nomenclature of aphids is given according to R e m a u d i è r e and R e m a u d i è r e (1997), whereas the nomenclature of plants is based on Flora Europaea (1964, 1968, 1972, 1976, 1980) and G r e u t e r et al. (1984, 1986, 1989). Results and discussion The results shown in Appendix 1 refer to the long time period of investigation of Lysiphlebus fabarum and all the interactions with aphids infesting analysed plants on the territory of Serbia. Analysing established trophic chains, we found 186 tritrophic parasitoid-aphid-plant associations including 64 hosts on 148 plants. The aphids belong to 18 genera. It is evident that the species belonging to the genus Aphis, were most frequently recorded in this investigation, about 38 taxa. The species A. fabae and A. craccivora made a great number of associations with different plants. We registered 57 trophic chains for A. fabae together with two subspecies, A. fabae cirsiiacanthoidis Scopoli and A. fabae solanella Theobald, species A. fabae forming 75 interactions with different plant species. As far as the species Aphis craccivora is concerned, we counted 30 associations with plants. The third most commonly encountered host species was A. ruborum, forming 11 associations. BIOLOGICA NYSSANA 5 (2)  December 2014: 113-121 Ilić Milošević, I. et al.  Tritrophic accociations of Lysiphlebus fabarum… 115 Conclusion Based on such a large number of recorded associations of the parasitoid Lysiphlebus fabarum and the previous studies regarding this species, L. fabarum is a suitable candidate for the biological control programs of various aphid species. Future investigations should be focused on interactions between many aphid species and L. fabarum, especially the very close relation between L. fabarum and polyphagous aphid, Aphis fabae as its host. Through different methods, such as the level of parasitism success, field campaign, and the introduction or detection of bacterial symbionts using suitable molecular markers have already been applied in the pioneering work by V o r b u g e r et al. (2009). Acknowledgements. We wish to thank Dr. Željko Tomanović and Dr. Andjeljko Petrović (Faculty of Biology, University of Belgrade) for the loan of specimens; Saša Stanković (Faculty of Sciences and Mathematics, University of Niš) for his help in sampling material and Dr. Nickolas Kavallieratos (Benaki Phytopathological Institute, Athens, Greece). This study was supported by the Ministry of Education, Science, and Technological Development of the Republic of Serbia (III43001). References Brewer, M. J., Elliott, N. C. 2004: Biological control of cereal aphids in North America and mediating effects of host plant and habitat manipulations. Annual Review of Entomology, 49: 219–242. Greuter, W., Burdet, H. 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Available through: http://www.faunaeur.org Vorburger, C., Sandrock, C., Gouskov, A., Castañeda, L. E., Ferrari, J. 2009: Genotypic variation and the role of defensive BIOLOGICA NYSSANA 5 (2)  December 2014: 113-121 Ilić Milošević, I. et al.  Tritrophic accociations of Lysiphlebus fabarum… 116 endosymbionts in an all-parthenogenetic host– parasitoid interaction. Evolution, 63 (6):1439-50. Yu, D. S., Van Achterberg, C., Horstmann, K. 2013. World Ichneumonoidea 2011. Taxonomy, Biology, Morphology and Distribution. Taxapad (Scientific Names for Information Management), Interactive Catalogue, Ottawa Available on: www.taxapad.com. Žikić, V., Ilić-Milošević, M., Stanković, S., Petrović, A., Petrović-Obradović, O., Kavallieratos, N., Starý, P., Tomanović, Ž. 2012: Aphidiinae (Hymenoptera: Braconidae) of Serbia and Montenegro – Tritrophic interactions. Acta entomologica Serbica, 17 (1/2): 83-105. Žikić, V., Stanković, S. S., Ilić Milošević, M., Petrović-Obradović, O., Petrović, A., Starý, P., Tomanović, Ž. 2015: First detection of Lysiphlebus testaceipes (Cresson) (Hymenoptera: Aphidiinae) in Serbia: an introduced species invading Europe?. North- Western Journal of Zoology, 11 (1): 97-101. Appendix 1. List of registered tritrophic associations plant aphid finding Althaea officinalis L. Aphis fabae Novi Sad, 10.06.1997, ŽT Aphis davletshinae Hille Ris Lambers Surčin, 20.05.1989, OP Aphis fabae Glover Zemun, Galenika, 07.06.2011, AP Amaranthus retroflexus L. Aphis fabae Belgrade, Crveni krst, 05.07.1996, ŽT; Lebane, Konjino, 06.07.2010, SS. Arctium lappa L. Aphis fabae Suva planina Mt., Vetanska reka River, 20.07.1997, ŽT; Sićevačka klisura Gorge, Ostrovica, 23.06.2012, SS; 28.05.2013, MĐ; Tara Mt., Mitrovac, 25.06.2013, VŽ Atriplex patula L. Aphis craccivora Palićko jezero Lake, 06.09.1995; ŽT Zemun, 09.07.1996, OP; Ballota nigra L. Aphis balloticola Szelegiewicz Belgrade, Avala Mt.,01.06.1996, ŽT; Obedska bara Swamp, 07.06.1997, ŽT; Stara Pazova, 10.06.1997, ŽT; Belgrade, Radmilovac, 18.06.1999, ŽT; Niš, Popovac, 25.06.2010, VŽ; Niš, Bubanj, 05.06.2013, MĐ Aphis spp. Zemun, IZBIS, 30.05.2011, AP; Beta vulgaris L. Aphis fabae Zemun, 27.09.1990, ŽT; Capsella bursa pastoris (L.) Medik. Aphis fabae Čemernik, 04.08.2011, SS; Capsicum annuum L. Myzus persicae Kikinda, 23.06.1997, ŽT; Carduus acanthoides L. Aphis fabae Stara planina Mt., Balta Berilovac, 22.07.1997, ŽT; Slankamen, 24.06.2011, ŽT; Brachycaudus cardui (L.) Zrenjanin, 20.06.1996, ŽT; Užice, Trešnjica, 23.07.1996, ŽT; Beljanica Mt., 03.08.1996, ŽT; Bečej, 03.08.1996, ŽT; Mol, 03.08.1996, ŽT; Rusko Selo, 03.08.1996, ŽT; Sefkerin, 03.08.1996, ŽT; Perlez, 23.06.1997, ŽT; Stara planina Mt., Glogovac, 16.07.1997, ŽT; Stara planina Mt., Balta Berilovac, 20.07.1997, ŽT; Stara planina Mt., Ćuštica, 20.07.1997, ŽT; Beljanica Mt., 12.07.1998, OP; Pčinja Canyon, Prohor Pčinjski, 10.06.2014, VŽ; Uroleucon sp. Mordvilko Surduk, 21.06.2011, ŽT; Carduus crispus L. Brachycaudus carduii (L.) Vlasina Plateau, Čemernik, 04.08.2011, SS; Carduus nutans L. Brachicaudus carduii (L.) Niš, Popovac, 23.06.2012, SS; Carduus sp. Aphis fabae Kragujevac, Ilićevo, 06.06.2011, AMB;Valjevo, Petnica, 12.06.2011, AP; Brachycaudus carduii (L.) Vlasinsko jezero Lake, 06.08.2010, SS;Đerdap, Veliki Kazan, 28.05.2011, ŽT; Valjevo, Petnica, 12.06.2011, AP; Dukat Mt., 06.08.2011, AP; Carlina acaulis L. Aphis carlinae (Borner 1940) Šara Mt., Ošljak, 04.07.1995, OP; Centaurea cyanus L. Aphis celastrii Matsumura Divčibare, 08.08.2000, OP; Lebane, Konjino, 31.05.2014, SS; Aphis fabae Lebane, Konjino, 31.05.2014, SS; Centaurea sp. Brachycaudus cardui (L.) Kopaonik Mt., Brzeće, 29.07.2010, SS; Cephalaria transsylvanica (L.) Schrad. Aphis craccivora Niš, Duvanište, 13.06.2013, PM; Chamaecytisus sp. Aphis craccivora Dukat Mt., 29.06.2012, SS; BIOLOGICA NYSSANA 5 (2)  December 2014: 113-121 Ilić Milošević, I. et al.  Tritrophic accociations of Lysiphlebus fabarum… 117 plant aphid finding Chaenopodium album L. Aphis fabae Zemun, 30.10.1990, OP; Belgrade, Botanical Garden, 29.06.1996, ŽT; Niš, Kunovica, 16.10.1998, VŽ; Niš, Popovac, 22.05.2010, VŽ; Niš, Popovac, 22.05.2010, SS; Niš, Popovac, 10.07.2010, VŽ; Novi Belgrade, Block 62, 28.05.2011, ŽT; Sićevačka klisura Gorge, Sićevo, 04.06.2011, SS; Zemun, Galenika, 07.06.2011,AP; Slankamen, 24.06.2011, ŽT; Lebane, Konjino, 01.06.2013, SS; Sićevačka klisura Gorge, Sićevo, 06.06.2013, VŽ; Tara Mt., Derventa Canyon, 25.06.2013, VŽ; Sićevačka klisura Gorge, Sićevo, 17.07.2013, SS; Aphis spp. Majur, 21.06.2011, ŽT; Chrysanthemum sp. Aphis fabae Glover Kanjiža, 08.06.1995, ŽT; Cichorium intibus L. Aphis intybi Koch Bela Crkva, 13.06.1996, ŽT; Kragujevac, 05.07.2011, AMB; Niš, Matejevac, 23.06.2012, VŽ; Lebane, Konjino, 31.05.2014, SS; Aphis spp. Negotin, 01.07.2011, ŽT; Aphis craccivora Tara, Derventa Canyon, 03.07.2012, VŽ; Cirsium acanthoides L. Aphis fabae Lebane, Konjino, 31.05.2014, SS; Brachycaudus cardui (L.) Lebane, Konjino, 31.05.2014, SS; Cirsium arvense (L.) Scop. Aphis fabae Vlasinsko jezero Lake, 11.08.2006, VŽ; Vlasinsko jezero Lake, 06.08.2010, VŽ; Belgrade, Ostružnica, 06.07.2011, ŽT; Vlasinsko jezero Lake, 03.08.2011, VŽ; Vlasinsko jezero Lake, 28.06.2012, VŽ; Vlasinsko jezero Lake, 15.06.2013, SS; Vlasinsko jezero Lake, 21.07.2013, SS; Merošina, Oblačinsko jezero Lake, 15.06.2014, SS; Aphis fabae cirsiiacanthoidis Scopoli Surčin, 29.05.1993, ŽT; Vlasinsko jezero Lake, 01.08.1996, ŽT; Vlasina Plateau, Čemernik, 24.07.1997, ŽT; Belgrade, Kovilovo, 11.06.1999, ŽT; Belgrade, Radmilovac, 18.06.1999, ŽT; Suva planina Mt., Glogovac, 16.07.1999, ŽT; Zrenjanin, Ečka, 31.05.2001, ŽT; Kopaonik Mt., Brzeće, 29.07.2010, VŽ; Vlasinsko jezero Lake, 06.08.2010, VŽ; Vlasina Plateau, Čemernik, 07.08.2010, SS; Vlasinsko jezero Lake, 21.07.2013, SS; Aphis fabae solanella Theobald Valjevo, Petnica, 12.06.2011, AP; Uroleucon aeneum (Hille Ris Lambers) Kopaonik, 27.07.2010, VŽ; Zemun, 02.06.2011, ŽT; Vlasina Plateau, Čemernik, 1400 m, 04.08.2011, VŽ; Bajina Bašta, 06.07.2012, VŽ; Merošina, Oblačinsko jezero Lake, 15.06.2014, SS; Cirsium eriophorum (L.) Scop. Aphis fabae cirsiiacanthoidis Scopoli Vlasinsko jezero Lake, 1250 m, 21.07.2013, SS; Brachycaudus cardui (L.) Suva planina Mt., Korube, 17.07.1997, ŽT; Vlasinsko jezero Lake, 1250 m, 21.07.2013, SS; Cirsium lanceolatum (L.) Scop. Brachycaudus cardui (L.) Beljanica Mt., 12.07.1997, ŽT; Aphis fabae cirsiiacanthoidis Scopoli Stara planina Mt., Balta Berilovac, 20.07.1997, ŽT; Cirsium palustre (L.) Scop. Aphis fabae cirsiiacanthoidis Scopoli Goč Mt., 13.07.2011, ŽT; Brachycaudus cardui (L.) Vlasinsko jezero Lake, 21.07.2013, SS; Cirsium sp. Aphis fabae cirsiiacanthoidis Scopoli Kopaonik Mt., 17.07.2013, SS; Cirsium vulgare (Savi) Ten. Brachycaudus cardui (L.) Bosilegrad, Jarešnik, 22.07.2013, SS; Clematis sp. Aphis spp. Užice, Djetinja Canyon, 26.06.1999, ŽT; Coreopsis verticillata L. Aphis fabae Zemun, 17.10.1991, OP; Coronilla varia L. Aphis craccivora Niš, Pantelej, 28.06.2012, VŽ; Niš, Trošarina, 26.04.2014, VŽ; Corydalis sempervirens (L.) Pers. Aphis fabaei Glover Niš, Pantelej, 01.06.2013, VŽ; Crepis biennis L. Aphis crepidis (Börner) Mol, 23.06.1997, ŽT; Aphis spp. Žitište, 22.07.1997, ŽT; Crepis foetida L. Uroleucon cichorii (Koch) Niš, Jasenovik, 12.06.2011, MĐ; Vlasinsko jezero Lake, 1250 m, 21.07.2013, SS; Aphis gr craccivora Niš, Pantelej, 01.06.2013, VŽ; Crepis sp. Aphis spp. Niš, Bubanj, 31.05.2013, MĐ; Aphis craccivora Niš, Donji Matejevac, 05.06.2013, VŽ; Niš, Tvrdjava, 05.06.2013, MĐ; Aphis crepidis (Börner) Vlasinsko jezero Lake, 1250 m, 28.06.2012, SS; Cucumis sativus L. Aphis fabaei Glover Užice, Carina, 05.08.1996, ŽT; BIOLOGICA NYSSANA 5 (2)  December 2014: 113-121 Ilić Milošević, I. et al.  Tritrophic accociations of Lysiphlebus fabarum… 118 plant aphid finding Daucus carota L. Semiaphis dauci (Fabricius) Carska bara, 02.07.1996, OP; Daucus sp. Semiaphis dauci (Fabricius) Kruševac, Slobodište, 13.07.2012, ZK; Digitalis ambigua Murray Aphis fabae Tara, Derventa Canyon, 03.07.2012, VŽ; Dorycnium herbaceum Vill. Aphis craccivora Zlatarsko jezero Lake, 20.06.1998, ŽT; Epilobium angustifolium L. Aphis spp. Kopaonik Mt., 27.07.2010, VŽ; Epilobium sp. Aphis spp. Sombor, 16.07.1996, OP; Euphorbia cyparissias L. Aphis spp. Niš, Bubanj, 11.05.2013, MĐ; Euonymus japonicus L.f. Aphis fabae Lebane, Konjino, 31.05.2014, SS; Aphis fabae solanella Theobald Lebane, Konjino, 31.05.2014, SS; Euonymus europaeus L. Aphis fabae Belgrade, Botanical Garden, 17.06.1997, ŽT; Filipendula ulmaria (L.) Maxim. Macrosiphum cholodkovskyi (Mordvilko) Dukat Mt., 29.06.2012, VŽ; Foeniculum vulgare Mill. Cavariella sp. Del Guercio Sićevačka klisura Gorge, Sićevo, 28.05.2013, ZK; Galium aparine L. Aphis craccivora Vlasinsko jezero Lake, 06.06.2014, SS; Aphis fabae Belgrade, Dušanovac, 20.05.1993, ŽT; Niš, Tvrdjava, 05.06.2013, MĐ; Vlasinsko jezero Lake, 06.06.2014, SS; Genista tinctoria L. Aphis genistae (Börner) Belgrade, Ostružnica, 17.06.2010, ŽT; Gentiana asclepiadea L. Aphis gentianae (Börner) Stara planina Mt., Babin zub, 19.07.1994, OP; Geranium sp Aphis spp. Zemun, Galenika, 07.06.2011, AP; Hedera helix L. Aphis hederae Kaltenbach Zemun, 13.06.2011, OP; Zemun, 14.06.2011, OP; Niš, Trošarina, 18.05.2013, MĐ; Niš, Pantelej, 01.06.2013, VŽ; Heracleum sphondylium L. Aphis fabae Belgrade, Botanical Garden, 29.06.1996, ŽT; Suva planina Mt., Toponički put, 19.07.1997, ŽT; Hypochaeris radicata L. Uroleucon sp. Mordvilko Adžine livade, Žeželj, 01.06.2011, ŽT; Nasonovia sp. Mordvilko Adžine livade, Žeželj, 01.06.2011, ŽT; Iris germanica L. Aphis newtoni Theobald Belgrade, 13.10.1997, ŽT; Knautia drymeia Heuff. Macrosiphum knautiae Holman Sićevačka klisura Gorge, Ostrovica, 28.05.2013, MĐ; Kochia scoparia (L.) Schrad. Aphis sp. Lebane, Konjino, 06.07.2010, SS; Lactuca sp. Aphis craccivora Lebane, Konjino, 01.06.2013, SS; Lamium sp. Aphis spp. Zemun, 23.06.1995, OP; Smederevo, Lugavčina, 06.06.1999, OP; Laserpitium halleri Crantz Aphis spp. Zemun, Altina, 09.06.2011, AP; Dobanovci, 17.06.2011, AP; Levisticum officinale W. D. J. Koch Aphis fabae Užice, 14.08.1999, ŽT; Lilium sp. Aphis spp. Belgrade, Zvezdara, 10.05.1997, ŽT; Lolium italicum A. Braun Sitobion avenae (Fabricius) Obrenovac, 15.06.1989, OP; Lolium perene L. Aphis fabae Lebane, Konjino, 06.06.2010, SS; Lotus corniculatus L. Aphis craccivora Kruševac, Slobodište, 22.06.2013, ZK; Lycopus europaeus L. Aphis spp. Valjevo, Petnica, 17.05.1998, ŽT; Lythrum salicaria L. Aphis sp. Dobanovci, 17.06.2011, ŽT; Sićevačka klisura Gorge, Sićevo, 28.05.2013, ZK; Malus domestica Borkh. Aphis pomi De Geer Novi Belgrade, 15.11.1992, OP; Niš, Donji Matejevac, 05.06.2013, VŽ; Dysaphis plantaginea (Passerini) Niš, Pasi Poljana, 27.05.2013, VŽ; Malus sp. Aphis pomi De Geer Zemun, Galenika, 18.06.2011, AP; Malva sylvestris L. Aphis umbrella (Börner) Belgrade, Kalemegdan, 29.09.1990, OP; Novi Belgrade, 23.11.1991, OP; Zemun, 07.12.1991, OP; Belgrade, Radmilovac, 22.06.1995, OP; Višnjica, 15.06.2011, OP; Niš, Mediana, 21.05.2013, SS; Niš, Quay, 02.07.2013, MĐ; Niš, Trošarina, 28.09.2013, VŽ; Niš, Mediana, 25.10.2013, VŽ; Matricaria chamomilla L. pro parte Aphis fabae Lebane, Konjino, 01.06.2013, SS; Matricaria inodora L. Aphis fabae Surčin, 12.05.1989, OP; Matricaria perforata Mérat Aphis fabae Vlasinsko jezero Lake, 05.08.2011, SS; Medicago lupulina L. Aphis craccivora Užice, Djetinja Canyon, 26.06.1999, OP; Medicago minima (L.) Bartal. Aphis craccivora Vlasinsko jezero Lake, 05.08.2011, SS; Medicago sativa L. Aphis craccivora Kosmaj Mt., 24.05.1995, ŽT; Palićko jezero Lake, 06.09.1995, ŽT; Bečej, 20.06.1996, ŽT; Zrenjanin, 20.06.1996, ŽT; Žabalj, BIOLOGICA NYSSANA 5 (2)  December 2014: 113-121 Ilić Milošević, I. et al.  Tritrophic accociations of Lysiphlebus fabarum… 119 plant aphid finding 20.06.1996, ŽT; Belgrade, Besni fok, 10.06.1997, ŽT; Kač, 10.06.1997, ŽT; Perlez, 23.06.1997, ŽT; Senta, 23.06.1997, ŽT; Valjevo, Petnica, 28.06.1997, AP; Zemun, 20.05.2011, AP; Novi Belgrade, Block 45, 06.06.2011, ZK; Bešnjaja Mt., 14.06.2011, ŽT; Zemun, Galenika, 17.06.2011, AP; Slankamen, 24.06.2011, ŽT; Kragujevac, Ilićevo, 06.07.2011, AMB; Melilotus album Medik. Aphis craccivora Vlasinsko jezero Lake, 28.06.2012, VŽ; Melilotus officinalis (L.) Pall. Aphis craccivora Žitište, 22.06.1997, ŽT; Negotin, 01.07.2011, OP; Mentha aquatica L. Aphis affinis Del Geurcio Surčin, 20.05.1989, OP; Belgrade, Radmilovac, 12.06.1995, OP; Užice, Duboko, 18.06.1995, ŽT; Belgrade, Radmilovac, 09.06.2011, OP; Mentha longifolia (L.) Huds. Aphis afinis Del Geurcio Vlasinsko jezero Lake, 15.06.2013, SS; Mentha piperita L. Aphis affinis Del Geurcio Kruševac, 18.06.2013, ZK; Musa sapientia Cavendish Aphis spiraecola Patch Kruševac, 21.06.2013, ZK; Aphis fabae Kruševac, 21.06.2012, ZK; Nepeta nuda L. Aphis nepetae Kaltenbach Bosilegrad, Jarešnik, 22.07.2013, VŽ; Aphis frangulae Kaltenbach Dukat Mt., 06.08.2011, AP; Aphis origani Passerini Beljanica Mt., 12.07.1998, ŽT; Oenanthe stenoloba Schur Aphis fabae Vlasinsko jezero Lake, 05.08.2011, MIM; Oenothera biennis L. Aphis oenotherae Oestlund Novi Belgrade, Block 45, 05.06.2002, ŽT; Onopordum acanthium L. Brachicaudus carduii (L.) Preševo, Slavujevac, 10.06.2014, SS; Papaver somniferum L. Aphis fabae Kanjiža, 08.06.1995, ŽT; Pastinaca sativa L. Aphis fabae Belgrade, Radmilovac, 22.08.1996, OP; Aphis spp. Vlasinsko jezero Lake, 05.08.2011, MIM; Phaseolus vulgaris L. Aphis fabae Kovačica, 22.06.1996, ŽT; Aphis craccivora Užice, Duboko, 18.06.1995, ŽT; Phragmites australis (Cav.) Trin. Hyalopterus pruni (Geoffroy) Belgrade, Radmilovac, 10.05.1995, OP; Picris hieracioides L. Hyperomyzus picridis (Börner & Blunck) Palićko jezero Lake, 06.09.1995, ŽT; Plantago lanceolata L. Aphis fabae Vlasinsko jezero Lake, 05.08.2011, MIM; Polygonum aviculare L. Myzus persicae Suva planina Mt., Toponički put, 19.07.1997, ŽT; Aphis polygonata (Nevsky) Zemun, 05.06.2011, AP; Zemun, Galenika, 09.06.2011, AP; Polygonum lapathifolium L. Capitophorus sp. van der Goot Niš, Pantelej, 13.10.3013, VŽ; Populus tremula L. Capitophorus sp. van der Goot Niš, Popovac, 22.05.2010, VŽ; Prunus cerasifera Ehrh. Hyalopterus pruni (Geoffroy) Belgrade, Karađorđev park, 08.06.1996, ŽT; Phorodon humuli Novi Belgrade, 17.06.1993, OP; Prunus cerasifera pisardi (Carrière) L. H. Bailey Phorodon humuli Niš, Mediana, 21.05.2013, VŽ; Prunus cerasus L. Myzus cerasi Niš, PMF, 10.05.2013, VŽ; Brachycaudus helichrysi Belgrade, Radmilovac, 10.05.1995, OP; Prunus persica (L.) Batsch Brachycaudus schwartzi Belgrade, 02.05.1995, OP; Belgrade, Radmilovac, 10.05.1995, OP; Smederevo, Lugavčina, 24.05.1995, OP; Niš, Pasi Poljana, 27.05.2013, VŽ; Punica granatum L. Aphis nasturtii Kaltenbach Belgrade, Crveni krst, 17.07.1996, ŽT; Ranunculus sp. Aphis fabae Sićevačka klisura Gorge, Ostrovica, 28.05.2013, MĐ; Ribes sp. Aphis schilderi (Börner) Belgrade, Konjarnik, 06.06.2011, ŽT; Robinia pseudacacia L. Aphis craccivora Deliblatska peščara Sands, Devojački bunar, 29.06.1992, OP; Niš, PMF, 02.06.2012, VŽ; Slankamen, 24.06.2011, ŽT; Rosa canina L. Aphis spp. Brestovik, 27.05.2011, ŽT; Aphis spp. Smederevo, 27.05.2011, ŽT; Rosa sp. Aphis spp. Koštunići, 17.06.2011, ŽT; Rubus sp. Aphis ruborum Bešnjaja Mt., 14.06.2011, ŽT; Sićevačka klisura Gorge, Ostrovica, 29.05.2010, VŽ; Zemun, 06.06.2011, OP; Koštunići, 17.06.2011, ŽT; Sićevačka klisura Gorge, Sićevo, 01.06.2012, SS; Sićevačka klisura Gorge, Ostrovica, 12.05.2013, VŽ; Tara Mt., Derventa Canyon, 26.06.2014, SS; Rubus caesius L. Aphis ruborum Kragujevac, Čumić, 14.05.2011, AMB; Sićevačka klisura Gorge, Sićevo, 04.06.2011, VŽ; Ivanovići, 05.06.2011, ŽT; Kragujevac, BIOLOGICA NYSSANA 5 (2)  December 2014: 113-121 Ilić Milošević, I. et al.  Tritrophic accociations of Lysiphlebus fabarum… 120 plant aphid finding Grošničko jezero Lake, 05.06.2011, AMB; Ljig, 05.06.2011, ŽT; Kragujevac, Ilićevo, 06.06.2011, AMB; Kragujevac, Košutnjačko brdo, 13.06.2011, AMB; Aphis idaei Sićevačka klisura Gorge, Sićevo, 23.06.2012, VŽ; Rubus discolor Boiss. Aphis ruborum Preševo, Slavujevac, 10.06.2014, SS; Aphis idaei Tara Mt., Derventa Canyon, 03.07.2012, SS; Rubus fruticosus L. Aphis idaei Niš, Matejevac, 23.06.2012, VŽ; Rubus idaeus L. Aphis ruborum Čačak, Zdravljak, 24.05.2000, ŽT; Aphis idaei Valjevo, Petnica, 18.05.1998, ŽT; Banja Vrujci Spa, Berkovac, 30.04.2000, ŽT; Rumex acetosella L. Aphis fabae Kač, 10.06.1997, ŽT; Rumex obtusifolius L. Aphis fabae Belgrade, Dušanovac, 29.05.1993, ŽT; Rumex sp. Aphis fabae Tara Mt., Derventa Canyon, 03.07.2012, VŽ; Niš, Trošarina, 22.05.2013, MĐ; Sićevačka klisura Gorge, Sićevo, 28.05.2013, ZK; Salix cinerea L. Aphis farinosa J. F. Gmelin Šara Mt., 21.07.1995, OP; Aphis farinosa J. F. Gmelin Zlatar Mt., Aljinovići, 12.07.1991, OP; Salvia nemorosa L. Aphis salviae Walker Uzdin, 22.06.1997, ŽT; Salvia officinalis L. Aphis salviae Walker Sićevačka klisura Canyon, Ostrovica, 28.05.2013, MĐ; Salvia sclarea L. Aphis craccivora Niš, Pantelej, 23.06.2012, VŽ; Salvia sp. Aphis craccivora Niš, Bubanj, 05.06.2013, MĐ; Salvia verticillata L. Aphis spp. L. Beljanica Mt., Resava, 11.07.1998, ŽT; Crna trava, 22.07.2001, OP; Dukat Mt., 29.06.2012, SS; Sanguisorba minor Scop. Aphis sp. L. Preševo, 05.06.2011, OP; Kalna, 11.06.2011, OP; Aphis sanguisorbae (Schrank) Niš, Donji Matejevac, 05.06.2013, VŽ; Pčinja Canyon, Gornji Starac, 10.06.2014, SS; Scabiosa argentea L. Aphis sp. L. Pčinja Canyon, Prohor Pčinjski, 10.06.2014, VŽ; Macrosiphum sp. Passerini Pčinja Canyon, Prohor Pčinjski, 10.06.2014, VŽ; Solanum nigrum L. Aphis fabae solanella Theobald Obedska bara Swamp, 15.06.1996, ŽT; Apatin, Prigrevica, 27.09.1997, ŽT; Srbobran, 27.09.1997, ŽT; Vršac, 02.10.1997, ŽT; Sonchus oleraceus L. Uroleucon sonchi (L.) Brestovik, 27.05.2011, OP; Symphytum officinale L. Aphis fabaei Glover Obedska bara Swamp, 02.06.2011, OP; Sićevačka klisura gorge, 28.05.2013, MĐ; Aphis spp. Ečka, 31.05.2001, ŽT; Valjevo, Petnica, 20.05.1996, AP; Tamarix sp. Brachyunguis tamaricis (Lichtenstein) Niš, Niška banja Spa, 06.06.2013, VŽ; Tanacetum parthenium (L.) Sch. Bip. Aphis fabae Šara Mt., Muržička reka River, 21.07.1995, OP; Beljanica Mt., Suvaja, 11.07.1997, OP; Tanacetum vulgare L. Metopeurum fuscoviride Stroyan Vlasinsko jezero Lake, 06.08.2010, SS; Vlasinsko jezero Lake, 15.06.2013, SS; Jerma Canyon, 19.07.2013, SS; Vlasinsko jezero Lake, 21.07.2013, SS; Taraxacum officinale Weber Aphis taraxicicola Blackman Belgrade, Dušanovac 08.05.1993, ŽT; Belgrade, Dušanovac, 29.05.1993, ŽT; Belgrade, Crveni krst, 14.06.1997, ŽT; Tecoma radicans (L.) Juss. Aphis spiraecola Patch Niš, PMF, 21.05.2013, SS; Thymus sp Aphis serpylli Koch Zlatar Mt., 13.07.1991, OP; Tordylium maximum L. Aphis spp. Suva planina Mt., Vetanska reka River, 16.07.1997, ŽT; Tragopogon sp. Aphis spp. Belgrade, Botanical Garden, 24.06.1999, ŽT; Trifolium sp. Aphis craccivora Surčin, 15.06.2011, OP; Therioaphis trifolii Monell Surčin, 15.06.2011, OP; Trifolium lagopus Pourr. Aphis craccivora Pčinja Canyon, Prohor Pčinjski, 10.06.2014, BZ; Trifolium pratense L. Aphis craccivora Beljanica Mt., 31.07.1996, OP; Kruševac, Slobodište, 13.07.2012, ZK; Trigonella procumbens (Besser.) Rchb. Aphis craccivora Uzdin, 22.06.1997, ŽT; Kostolac, 02.06.2001, ŽT; Triticum aestivum L. Anoecia corni (Fabricius) Suva planina Mt., Vetanska reka River, 17.06.1997, ŽT; Triticum vulgare Vill. Sitobion avenae (Fabricius) Leskovac, 01.06.2013, VŽ; Typha latifolia L. Rhopalosiphum nymphaeae (L.) Niš, Niška banja Spa, 23.07.2013, VŽ; Urtica dioica L. Aphis fabae Brestovik, 27.05.2011, OP; Smederevo, 27.05.2011, OP; Aphis sp. Niš, Popovac, 22.05.2010, VŽ; Sićevačka klisura Gorge, Sićevo, 29.05.2010, SS; BIOLOGICA NYSSANA 5 (2)  December 2014: 113-121 Ilić Milošević, I. et al.  Tritrophic accociations of Lysiphlebus fabarum… 121 plant aphid finding Aphis urticata J. F. Gmelin Smederevo, Lugavčina, 15.04.1990, OP; Kokin brod, 12.07.1991, ŽT; Belgrade, Dušanovac, 08.05.1993, ŽT; Surčin, 23.05.1993, ŽT; Surčin, 02.05.1995, ŽT; Kanjiža, 08.06.1995, ŽT; Belgrade, Radmilovac, 20.05.1996, ŽT; Omoljica, 13.06.1996, ŽT; Čenta, 20.06.1996, ŽT; Užice, Trešnjica, 23.07.1996, ŽT; Belgrade, Radmilovac, 10.06.1997, ŽT; Novi Sad, 10.06.1997, ŽT; Belgrade, Radmilovac, 13.05.1998, ŽT; Niš, Popovac, 10.05.2010, VŽ; Lebane, Konjino, 06.06.2010, SS; Stara planina Mt., Bojanine vode, 11.07.2010, SS; Sićevačka klisura Gorge, Sićevo, 04.06.2011, VŽ; Rogojevac, 16.06.2011, OP; Sićevačka klisura Gorge, Sićevo, 23.06.2012, SS; Kruševac, Pakašnica, 11.05.2013, ZK; Sićevačka klisura Gorge, Sićevo, 12.05.2013, VŽ; Sićevačka klisura Gorge, Sićevo, 28.05.2013, ZK; Niš, Bubanj, 31.05.2013, MĐ; Lebane, Konjino, 01.06.2013, SS; Sićevačka klisura Gorge, Sićevo, 06.06.2013, VŽ; Sićevačka klisura Gorge, Sićevo, 22.04.2014, VŽ; Urtica urens L. Aphis fabae Kumane, 20.06.1996, ŽT; Valeriana officinalis L. Aphis fabae Vlasinsko jezero Lake, 21.07.2013, SS; Verbascum nigrum L. Aphis verbasci Schrank Vlasinsko jezero Lake, 05.08.2011, VŽ; Verbascum sp. Aphis verbasci Schrank Gornjane, 06.07.1990, OP; Belgrade, 12.10.1990, OP; Kopaonik Mt., Brzeće, 25.08.1998, OP; Lebane, Konjino, 01.07.2012, SS; Niš, Popovac, 08.06.2013, VŽ; Viburnum opulus L. Aphis viburni Scopoli Belgrade, Žarkovo, 19.04.1990, OP; Vicia cracca L. Aphis craccivora Vlasinsko jezero Lake, 05.08.2011, MIM; Lebane, Konjino, 31.05.2014, SS; Prokuplje, Bresničić, 15.06.2014, VŽ; Vicia cordata Wulfen Aphis craccivora Niš, Mediana, 21.05.2013, SS; Zea mays L. Aphis fabae Beljanica Mt., 30.07.1996, OP;