Abstract
The lime leaf miner, Phyllonorycter issikii, is a moth species native to East Asia, which recently invaded considerable part of Europe. A study on the natural enemies of this invasive species was conducted in Bulgaria. Tilia cordata leaves infested with the lime leaf miner were collected in 2015 and 2016 in two public parks in Sofia. A total of eleven eulophid parasitoids (Hymenoptera: Eulophidae) belonging to three subfamilies - Entedoninae, Eulophinae and Tetrastichinae, and one braconid species (Hymenoptera: Braconidae) were recorded. In addition, one unidentified ichneumonid species was reared. Minotetrastichus platanellus was the most abundant species in the samples comprising 76.88% of the parasitoids reared from collected immature and pupal stages of Ph. issikii. It is followed by Sympiesis gordius (6.53%) and S. sericeicornis (6.03%). Three new host-parasitoid associations were established. The entomopathogenic fungi Beuveria bassiana and Metarhizium anisopliae (Hypocreales) were isolated for the first time from cadavers of Ph. issikii larvae and pupae. Based on the presented observation we hypothesized that the lime leaf miner can produce three generations in Bulgaria.
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References
Agassiz DJL, Lasalle J (1996) Minotetrastichus platanellus (Mercet) (Hymenoptera: Eulophidae), a parasitoid new to Britain, tracking an invading host. Entomologist’s Gazette 47:191–194
Aimbetova SI, Ermolaev IV (2016) Parasitoids of four invasive species of leaf miners (Lepidoptera, Gracillariidae) in Bratislava. Bulletin of Udmurt University 26:105–111 (in Russian; English summary)
Askew RR (1968) Hymenoptera, 2 Chalcidoidea, section (b). In: Handbooks for the identification of British insects, 8 (2). Royal Entomological Society, London, UK, pp 1–39
Askew RR, Shaw MR (1979) Mortality factors affecting the leaf-mining stages of Phyllonorycter (Lepidoptera: Gracillariidae) on oak and birch (1. Analysis of the mortality factors). Zool J Linn Soc 67:31–49. https://doi.org/10.1111/j.1096-3642.1979.tb01103.x
Auerbach MJ, Connor EF, Mopper S (1995) Minor miners and major miners: population dynamics of leaf-mining insects (Chapter 5). In: Cappuccino N, Price PW (eds) Population dynamics: new approaches and synthesis. Academic San Diego, California, USA, pp 83–110
Balevski NA (1999) Catalogue of the braconid parasitoids (Hymenoptera: Braconidae) isolated from various phytophagous insect hosts in Bulgaria. Pensoft, Sofia – Moscow
Bednova OV, Belov DA (1999) The lime leafminer (Lepidoptera, Gracillariidae) in forest plantations of Moscow and adjacent areas. Lesnoy vestnik [Forest Gazette] 2:172–177 (in Russian)
Bennett AE (2013) Can plant–microbe–insect interactions enhance or inhibit the spread of invasive species? Funct Ecol 27:661–671. https://doi.org/10.1111/1365-2435.12099
Bouček Z, Askew R (1968) Index of Palearctic Eulophidae (exl. Tetrastichinae). In: Delucchi V, Remaudiere G (eds) Index of entomophagous insects. Paris, France, pp 1–254
Boyadzhiev PS (2003) New records to the fauna of Eulophidae in Bulgaria (Hymenoptera, Chalcidoidea) with a checklist of all the Bulgarian species. Travaux Scientifiques Universite de Plovdiv – Biologie 39:79–96
Boyadzhiev P (2006) Eulophidae (Hymenoptera: Chalcidoidea) of the Western Rhodopes (Bulgaria). In: Beron P (ed) Biodiversity of Western Rhodopes (Bulgaria and Greece) volume I. Biodiversity of Bulgaria 3. Pensoft & National Museum of Nat Hist, Bulgarian Acad Sci, Sofia, Bulgaria, pp 561–580
Cebeci HH, Grabenweger G, Ayberk H (2011) Eulophid parasitoids (Hymenoptera: Eulophidae) of the horse chestnut leafminer, Cameraria ohridella (Lepidoptera: Gracillariidae), from İstanbul, Turkey. Turk J Zool 35:777–780. https://doi.org/10.3906/zoo-1002-94
De Prins J, De Prins W (2018). Global Taxonomic Database of Gracillariidae (Lepidoptera). World Wide Web electronic publication, http://www.gracillariidae.net. Accessed 5 June 2018
Dobrosavljević J, Marković Č, Stojanović A (2018) Contribution to the knowledge of Phyllonorycter issikii (Kumata, 1963) in Serbia. Acta Entomol Serb. https://doi.org/10.5281/zenodo.1213045
Draganova S, Tomov R (2000a) Entomopathogenic fungi on leafmining moths in orchard ecosystems in Bulgaria. Journal of Balkan Ecology 3:77–80
Draganova S, Tomov R (2000b) Fungal pathogens on Cameraria ohridella Deschka et Dimic (Lepidoptera: Gracillariidae) in Bulgaria. Rastenievadni nauki (Plant Science) 37:316–318
Draganova S, Toshova T, Takov D (2012) Fungal pathogens of grey corn weevil Tanymecus dilaticollis (Coleoptera: Curculionidae) and bioassay with some Beauveria bassiana isolates. Acta Zool Bulg 64:289–294
Ermolaev IV (2014) Biological invasion of the lime leafminer Phyllonorycter issikii Kumata (Lepidoptera, Gracillariidae) in Europe. Contemp Probl Ecol 7:324–333. https://doi.org/10.1134/S1995425514030032
Ermolaev IV (2016) Trophical specialization of the lime leaf blotch miner Phyllonorycter issikii (Kumata, 1963) (Lepidoptera, Gracillariidae). Bulletin of Udmurt University 26:60–68 (in Russian; English summary)
Ermolaev IV, Aimbetova SI (2016) Parasitoids (Hymenoptera, Eulophidae, Ichneumonidae, Braconidae) of lime leafminer Phyllopnorycter issikii (Kumata) (Lepidoptera, Gracillariidae). Bulletin of Udmurt University 26:118–125 (in Russian; English summary)
Ermolaev IV, Rubleva EA (2017) History, rate, and factors of invasion of lime leafminer Phyllonorycter issikii (Kumata, 1963) (Lepidoptera, Gracillariidae) in Eurasia. Rus J Biol Invasions 8:115–130. https://doi.org/10.1134/S2075111717020035
Ermolaev IV, Sidorova OV (2011) Seasonal dynamics of damage to small-leaved lime trees by phyllophagous arthropods. Entomol Rev 91:585–591. https://doi.org/10.1134/S0013873811050034
Ermolaev IV, Sidorova OV (2012) Patterns of damage to Tilia cordata by Phyllonorycter issikii (Lepidoptera, Gracillariidae) in Izhevsk city. Entomol Rev 92:403–408. https://doi.org/10.1134/S0013873812040057
Ermolaev IV, Yefremova ZA (2015) Parasitoids (Hymenoptera, Eulophidae, Braconidae) of the lime leafminer Phyllonorycter issikii (Kumata) (Lepidoptera, Gracillariidae). Euroasian Entomol J 14:217–223 (in Russian; English summary)
Ermolaev IV, Yefremova ZA, Domrachev TB (2018) The influence of parasitoids (Hymenoptera, Eulophidae) on the survival of the lime leafminer (Phyllonorycter issikii, Lepidoptera, Gracillariidae) in Udmurtia. Zool Zh 97:401–407. https://doi.org/10.7868/S0044513418040037. (in Russian; Englih summary)
Ermolaev IV, Yefremova ZA, Izhboldina NV (2011) Parasitoids as a mortality factor for the lime leafminer (Phyllonorycter issikii, Lepidoptera, Gracillariidae). Entomol Rev 91:326–334. https://doi.org/10.1134/S0013873811030067
Ermolaev IV, Zorin DA (2011) Ecological consequences of invasion of Phyllonorycter issikii (Lepidoptera, Gracillariidae) in lime forests in Udmurtia. Entomol Rev 91:592–598. https://doi.org/10.1134/S0013873811050046
Faeth SH (1991) Novel aspects of host tree resistance to leaf miners. In: Baranchikov YN, Mattson WJ, Hain FP, Payne TL (eds) Forest insects guilds: patterns of interaction with host trees. U.S.D.A. Forest Service, gen. Tech. Rep. NE-153, USA, pp 219–239
Ferracini C, Alma A (2007) Evaluation of the community of native eulophid parasitoids on Cameraria ohridella Deschka and Dimic in urban areas. Environ Entomol 36:1147–1153. https://doi.org/10.1603/0046-225X(2007)36[1147:EOTCON]2.0.CO;2
Francke W, Franke S, Bergmann J, Tolasch T, Subchev M, Mircheva A, Toshova T, Svatos A, Kalinova B, Szőcs G, Tóth M (2002) Female sex pheromone of Cameraria ohridella Desch. And dim. (Lepidoptera: Gracillariidae): structure confirmation, synthesis and biological activity of (8E,10Z)-8,10-tetradecadienal and some analogs. Z Naturforsch C 57:739–752. https://doi.org/10.1515/znc-2002-7-832
Gebiola M, Bernardo U, Burks RA (2010) A reevaluation of the generic limits of Pnigalio Schrank (Hymenoptera: Eulophidae) based on molecular and morphological evidence. Zootaxa 2484:35–44
Gninenko YI, Kostyukov VV, Kosheleva OV, Shcherbakov NA, Nakonechnaya IV, Gunasheva ZM (2014) Parasitoids of Parectopa robiniella Clemens and Phyllonorycter robiniella Clemens in Russia. In: Nadykta VD, Ismailov VYa (eds) Proceedings of 8th International conference “Biological Plant Protection as the basis of ecosystem stabilization”. Krasnodar, 16–18 September, 2014, Russia, pp 126–131 (in Russian; English summary)
Graham MWR de V (1987) A reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae), with a revision of certain genera. Bull Brit Mus (Nat Hist) Entomol 55:1–392
Gramatikov D (1992) Key of the trees and shrubs in Bulgaria. IntelSis Publishing Group, Plovdiv, Bulgaria (in Bulgarian)
Hansson C (1985) Taxonomy and biology of the Palearctic species of Chrysocharis Förster, 1956 (Hymenoptera: Eulophidae). Entomol Scand 26:1–130
Heraty J, Hawks D (1998) Hexamethyldisilazane: a chemical alternative for drying insects. Entomol News 109:369–374
Hirao T, Murakami M (2008) Quantitative food webs of lepidopteran leafminers and their parasitoids in a Japanese deciduous forest. Ecol Res 23:159–168. https://doi.org/10.1007/s11284-007-0351-6
Humber R (1997) Fungi: identification. In: Lacey L (ed) Manual of techniques in insect pathology. Academic Press, London, UK, pp 153–185
Japoshvili G, Kostjukov V (2017) Three new Minotetrastichus (Hymenoptera: Eulophidae) species records from Transcaucasia. J Entomol Res Soc 19(2):95–100
Jurc M (2012) The lime leafminer (Phyllonorycter issikii) in Slovenia. Šumarski list CXXXVI: 119–127 (In Slovenian; English summary)
Kirichenko N, Augustin S, Kenis M (2018) Invasive leafminers on woody plants: a global review of pathways, impact, and management. J Pest Sci. https://doi.org/10.1007/s10340-018-1009-6
Kirichenko N, Triberti P, Ohshima I, Haran J, Byun B-K, Li H, Augustin S, Roques A, Lopez-Vaamonde C (2017) From east to west across the Palearctic: Phylogeography of the invasive lime leaf miner Phyllonorycter issikii (Lepidoptera: Gracillariidae) and discovery of a putative new cryptic species in East Asia. PLoS One 12:e0171104. https://doi.org/10.1371/journal.pone.0171104
Kirichenko NI (2014) The lime leafminer Phyllonorycter issikii in Western Siberia: some ecological characteristics of the population of the recent invader. Contemp Probl Ecol 7:114–121. https://doi.org/10.1134/S1995425514010077
Kollár J, Donoval L' (2013) Diversity of phyllophagous organisms on woody plants in the botanical garden in Nitra, Slovakia. Acta Entomol Serb 18:195–205
Kozlov MV, Koricheva YG (1991) The within-tree distribution of caterpillar mines. In: Baranchikov YN, Mattson WJ, Hain FP, Payne TL (eds) Forest insect guilds: patterns of interaction with host trees. U.S.D.A. Forest Service, report NE-153, USA, pp 240–255
Lacey LA, Solter LF (2012) Initial handling and diagnosis of diseased invertebrates. In: Lacey LA (ed) Manual of techniques in invertebrate pathology, 2nd edn. Academic Press, Elsevier, USA, pp 1–14
Lees D (2010) Phyllonorycter issikii (Kumata, 1963) (Lepidoptera, Gracillariidae). Chapter 14: Factsheets for 80 representative alien species. In: Roques A, Kenis M, Lees D, Vaamonde CL, Rabitsch W, Rasplus JY, Roy D (eds) Alien terrestrial arthropods of Europe. Pensoft Publishers (BioRisk, 4, 2), Sofia Bulgaria, pp 855–1021
Matošević D, Melica G (2013) Recruitment of native parasitoids to a new invasive host: first results of Dryocosmus kuriphilus parasitoid assemblage in Croatia. Bull Insectol 66(2):231–238
Metla Z, Voitkāne S, Sešķēna R, Petrova V, Jankevica L (2013) Presence of entomopathogenic fungi and bacteria in Latvian population of horse-chestnut leaf miner Cameraria ohridella. Acta Biologica Universitatis Daugavpiliensis 13:69–76
Mey W (1991) On the significance of native parasitoid complexes in the current range extension by four Phyllonorycter species into Europe (Insecta, Lepidoptera, Hymenoptera). Mitteilungen aus dem Museum für Naturkunde in Berlin 67:177–194. https://doi.org/10.1002/mmnz.19910670123
Mishchenko AV (2014) New data on parasitism of eulophid wasps (Hymenoptera: Eulophidae) on Phyllonorycter issikii (Kumata, 1963) (Lepidoptera: Gracillariidae), a pest of lime-tree in the middle Volga region (Russia). Caucasian Entomological Bulletin 10:131–136 (in Russian; English summary)
Mishchenko AV (2016) Eulophid species (Hymenoptera: Eulophidae) – parasitoids of the invasive lime leafminer moth (Phyllonorycter issikii) (Kumata, 1963) from the middle Volga Basin. Innov Sci 9:35–39 (in Russian)
Mishchenko AV (2017) Peculiarities of parasitism of Hymenoptera: Eulophidae in the middle Volga region. Samara J Sci 6(3):15–20 (in Russian; English summary)
Mishchenko AV, Yefremova ZA, Yegorenkova EN (2011) Parasitism of Eulophidae (Hymenoptera) on leaf-miners (Lepidoptera). Corporaciya technolohii prodvizheniya, Ulyanovsk, Russia (in Russian)
Noyes JS (2018) Universal Chalcidoidea Database. World Wide Web electronic publication. http://www.nhm.ac.uk/chalcidoids. Accessed 5 September 2018
Pečiulytė D, Kačergius A (2012) Lecanicillium aphanocladii – a new species to the mycoflora of Lithuania and new pathogen of tree leaves mining insects. Bot Lith 18:133–146. https://doi.org/10.2478/v10279-012-0015-5
Peterson RKD, Davis RS, Higley LG, Fernandes OA (2009) Mortality risk in insects. Environ Entomol 38:2–10. https://doi.org/10.1603/022.038.0102
Prenerová E, Zemek R, Weyda F (2008) The first record of Beauveria bassiana (Deuteromycetes) on the hibernating pupae of Cameraria ohridella (Lepidoptera: Gracillariidae). In: 41st annual meeting of SIP and 9th international conference on Bacillus thuringiensis, 3–7 August, vol 2008. University of Warwick, UK, p 63
Rehner S, Minnis A, Sung G-H, Luangsa-Ard JJ, Devotto L, Humber R (2011) Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103:1055–1073. https://doi.org/10.3852/10-302
Rotter M (2005) Motýli Orlických hor a Podorlicka XI. Butterflies and moths of the Orlické hory Mts. and their foothills – XI. Východočeský Sborník Přírodovědný – Práce a Studie 13:219–225 (in Czech; English summary)
Russell DA (1987) A simple method for improving estimates of percentage parasitism by insect parasitoids from field sampling of hosts. New Zealand Entomologist 10:38–40
Samson RA, Evans HC, Latge JP (1988) Atlas of entomopathogenic fungi. Springer-Verlag, London, UK
Santos AMC, Quicke DLJ (2011) Large-scale diversity patterns of parasitoid insects. Entomol Sci 14:371–382. https://doi.org/10.1111/j.1479-8298.2011.00481.x
Schemmer R, Chládeková P, Medo J, Barta M (2016) Natural prevalence of entomopathogenic fungi in hibernating pupae of Cameraria ohridella (Lepidoptera: Gracillariidae) and virulence of selected isolates. Plant Prot Sci 52:199–208. https://doi.org/10.17221/110/2015-PPS
Šefrová H (2002) Phyllonorycter issikii (Kumata, 1963) - bionomics, ecological impact and spread in Europe. Acta Universitatis Agriculturae et Silviculturae Mendelianae Brunensis 50:99–104
Stojanović A, Marković C (2004) Parasitoid complex of Cameraria ohridella (Lepidoptera: Gracillariidae) in Serbia. Phytoparasitica 32:132–140. https://doi.org/10.1007/BF02979778
Stolnicu AM, Ureche C (2007) Data regarding the presence of the. Phyllonorycter issikii (Kumata) (Lepidoptera: Gracillariidae) in Romanian Fauna Analele Ştiinţifice ale Univ. „Al. I. Cuza” Iaşi, Secţiunea I Biologie animală LIII:103–108
Storozheva NA (1982) A key to Palaearctic species of the chalcid genus Sympiesis Förster, 1856 (Hymenoptera, Eulophidae). Entomol Rev 61:164–176
Subchev M, Mircheva A, Pickett J, Wadhams L, Woodcock Ch, dos Sandos A, Franke S, Francke W (2003) Sex pheromone of the leaf-miner Phyllonorycter platani: (Z10)-tetradecenyl acetate. J Chem Ecol 29:2391–2396. https://doi.org/10.1023/A:1026235515607
Szőcs L, Melika G, Thuróczy C, Csóka G (2014) Data on the parasitoid complexes of the invasive lime leafminer moth (Phyllonorycter issikii Kumata, 1963). Növényvédelem 50:445–451 (in Hungarian; English summary)
Szőcs L, George M, Thuróczy C, Csóka G (2015a) Parasitoids of the lime leaf miner Phyllonorycter issikii (Lepidoptera: Gracillariidae) recorded throughout the area it recently colonized. Eur J Entomol 112:591–598. https://doi.org/10.14411/eje.2015.101
Szőcs L, Thuróczy C, Huróczy C, George M, Csóka G (2015b) Faunistic data on the leaf miner parasitoid species composition occurring in the Mátra region (Hymenoptera). Folia Historico-Naturalia Musei Matraensis 39:77–83 (in Hungarian; English summary)
Tobias VI, Belokobylskij SA, Kotenko AG (1986) Family Braconidae. In: Medvedev GS (ed) A key to insects of the European part of the USSR. Vol. 3. Hymenoptera. Nauka, Leningrad (in Russian)
Tomov R (2003) Phyllonorycter robiniella (Clemens, 1859) (Lepidoptera, Gracillariidae), a new pest on black locust Robinia pseudoacacia L. in Bulgaria. In: Proceedings scientific papers, The 50th anniversary of University of Forestry, Sofia, Bulgaria, pp 105–107
Tomov R (2007) Pest status of alien leaf-mining moths (Lepidoptera) in Bulgaria. Plant Protection (Bulgaria) 18:79–81
Tomov R (2009) A review of mortality factors of three invasive leafminer moths (Lepidoptera) in Bulgaria. In: Stojnić B (ed) Abstracts of the VIth congress of plant protection with symposium about biological control of invasive species, Zlatibor, 23–27 November 2009, Serbia, pp 84–85
Tomov R, Krusteva S (2007) Contribution to the leafmining insect fauna of Bulgaria (part I). Acta Entomol Bulg 13:21–28
Triapitsyn V, Kostjukov V (1978) Eulophidae. In: Medvedev GS (ed) Opredelitel Nasekomykh Evropeyskoy Chasti SSR 3. Nauka, Leningrad, pp 381–467 (in Russian)
van Achterberg C (1993) Illustrated key to the subfamilies of the Braconidae (Hymenoptera: Ichneumonoidea). Zoologische Verhandenlingen 283:1–189
van Achterberg C (2013) Fauna Europaea: Hymenoptera, Apocrita. Fauna Europaea version 2017.06. https://fauna-eu.org. Accessed 4 June 2018
van Achterberg C, Berry J (2004) Neptihormius gen. nov. (Hymenoptera: Braconidae: Hormiinae), a parasitoid of Nepticulidae (Lepidoptera) from New Zealand. Zoologische Mededelingen 78:291–299
Vercher R, Costa-Cimelles J, Marzal C, García-Marí F (2005) Recruitment of native parasitoid species by the invading leafminer Phyllocnistis citrella (Lepidoptera: Gracillariidae) on citrus in Spain. Environ Entomol 34(5):1129–1138. https://doi.org/10.1093/ee/34.5.1129
Yefremova ZA, Krayushkina AV, Mishchenko AV (2009) Parasitoid complexes (Hymenoptera, Eulophidae) of species of the genus Phyllonorycter (Lepidoptera, Gracillariidae) in the middle Volga Basin. Entomol Rev 89:903–911. https://doi.org/10.1134/S0013873809080041
Yefremova ZA, Mishchenko AV (2008) The parasitoid complex (Hymenoptera, Eulophidae) of the leafminer Phyllonorycter issikii (Kumata) (Lepidoptera, Gracillariidae) from the middle Volga Basin. Entomol Rev 88:178–185. https://doi.org/10.1134/S001387380802005X
Yefremova ZA, Mishchenko AV (2010) The dynamics of the populations of dominant parasitoids (Hymenoptera, Eulophidae) of moth Phyllonorycter issikii (Kumata) (Lepidoptera, Gracillariidae) in the Middle Volga Basin. In: Krivokhatsky VA (ed) Proceedings of the Russian Entomological Society St. Petersburg, 2010, Vol. 80 (2), Russian Entomological Society, Russia, pp 64–75 (in Russian; English summary)
Yefremova ZA, Myartseva SN (2004) Eulophidae (Hymenoptera: Chalcidoidea) of Turkmenistan, with emphasis on the genera Elachertus Spinola, 1811 and Hyssopus Girault, 1916. Entomologist’s Monthly Magazine 140:113–122
Zemek R, Prenerová E, Volter L, Weyda F, Skuhravý V (2007) Perspectives for the biological control of Cameraria ohridella. Commun Agric Appl Biol Sci 72:521–527
Zhu C-D, Huang D-W (2001) A study of Chinese Elachertus Spinola (Hymenoptera: Eulophidae). Zool Stud 40:317–354
Zúbrik M, Hajek A, Pilarska D, Špilda I, Georgiev G, Hrašovec B, Hirka A, Goertz D, Hoch G, Barta M, Saniga M, Kunca A, Nikolov C, Vakula J, Galko J, Pilarski P, Csóka G (2016) The potential for Entomophaga maimaiga to regulate gypsy moth Lymantria dispar (L.) (Lepidoptera: Erebidae) in Europe. J Appl Entomol 140:565–579. https://doi.org/10.1111/jen.12295
Acknowledgments
We thank Dr. Boyan Zlatkov (Institute of Biodiversity and Ecosystem Research, Bulgaria) for the identification of Ph. issikii and Dr. Mark Young (University of Aberdeen, UK) for helpful comments. The study was partially supported by ANIDIV-3 project (Institute of Biodiversity and Ecosystem Research, Bulgaria).
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Toshova, T.B., Boyadzhiev, P., Todorov, I. et al. Parasitoids and fungal pathogens of Phyllonorycter issikii (Kumata, 1963) from Bulgaria. Biologia 73, 1237–1245 (2018). https://doi.org/10.2478/s11756-018-0141-3
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DOI: https://doi.org/10.2478/s11756-018-0141-3