Eur. J. Entomol. 112 (4): 591-598, 2015 | DOI: 10.14411/eje.2015.101

Parasitoids of the lime leaf miner Phyllonorycter issikii (Lepidoptera: Gracillariidae) recorded throughout the area it recently colonized

Levente SZŐCS1, Melika GEORGE2, Csaba THURÓCZY3, György CSÓKA1
1 NARIC Forest Research Institute, Department of Forest Protection, H-3232 Mátrafüred, Hungary; e-mails: szocsl@erti.hu; csokagy@erti.hu
2 National Food Chain Safety Office, Directorate of Plant Protection, Soil Conservation and Agri-environment, Plant Health and Molecular Biology Laboratory, H-1118 Budapest, Budaörsi str. 141-14, Hungary; e-mail: melikag@nebih.gov.hu
3 Malomárok str. 27, H-9730 Kőszeg, Hungary; e-mail: thuroczy.cs@freemail.com

Phyllonorycter issikii (Lepidoptera: Gracillariidae) has recently spread over a considerable part of the Eurasian continent. So far, in Europe, unlike in Russia, it has not significantly affected its food plant (Tilia cordata), but its effect may increase over time. The regulating potential of associated parasitoid natural enemies is still low, which probably allows further leaf miner range expansion and population growth. This species is potentially capable of inflicting considerable damage on its host. Therefore, it is important to study its natural enemies, especially their oviposition behaviour and biology. In this paper, we summarize the results of rearing experiments throughout the area it has recently occupied, including our own study in Hungary. Here we list 46 species of parasitoids recorded from P. issikii. None of these species are likely to be able regulate the abundance of P. issikii. Further studies are needed to determine their effect on the abundance of this host.

Keywords: Lepidoptera, Gracillariidae, Phyllonorycter issikii, Tilia cordata, parasitoid assemblages, invasive species

Received: April 27, 2015; Accepted: July 28, 2015; Prepublished online: October 8, 2015; Published: November 21, 2015

Download citation

References

  1. Aebi A., Melika G., Quacchia A., Alma A. & Stone G.N. 2007: Native and introduced parasitoids attacking the invasive chestnut gall wasp Dryocosmus kuriphilus. - OEPP/EPPO Bull. 37: 166-171. Go to original source...
  2. Askew R.R. & Shaw M.R. 1974: An account of the Chalcidoidea (Hymenoptera) parasitising leaf-mining insects of deciduous trees in Britain. - Biol. J. Linn. Soc. 6: 289-335. Go to original source...
  3. Askew R.R. & Shaw M.R. 1979a: 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. Go to original source...
  4. Askew R.R. & Shaw M.R. 1979b: Mortality factors affecting the leaf-mining stages of Phyllonorycter (Lepidoptera: Gracillariidae) on oak and birch (2. Biology of the parasite species). - Zool. J. Linn. Soc. 67: 51-64. Go to original source...
  5. Balázs K., Thuróczy C. & Ripka G. 2002: Parasitoids of the horse chestnut leafminer Cameraria ohridella Deschka et Dimic, 1986 (Lepidoptera: Gracillariidae) in Hungary. In Melika G. & Thuróczy C. (eds): Parasitic Wasps: Evolution, Systematics, Biodiversity and Biological Control. Agroinform, Budapest, pp. 405-412.
  6. Bernardo U., Pedata P.A. & Viggiani G. 2006: Life history of Pnigalio soemius (Walker) (Hymenoptera: Eulophidae) and its impact on a leafminer host through parasitization, destructive host-feeding and host-stinging behavior. - Biol. Contr. 37: 98-107. Go to original source...
  7. Brockerhoff E.G. & Kenis M. 1996: Parasitoids associated with Cydia strobilella (L.) (Lepidoptera: Tortricidae) in Europe, and considerations for their use for biological control in North America. - Biol. Contr. 6: 202-214. Go to original source...
  8. Cornell H.W. & Hawkins B.A. 1993: Accumulation of native parasitoid species on introduced herbivores: A comparison of hosts as natives and hosts as invaders. - Am. Nat. 141: 847-865. Go to original source...
  9. Csóka G., Pénzes Z., Hirka A., Mikó I., Matoąević D. & Melika G. 2009: Parasitoid assemblages of two invading black locust leaf miners, Phyllonorycter robiniella and Parectopa robiniella in Hungary. - Period. Biol. 111: 405-411.
  10. De Prins J. & De Prins W. 2014: Global Taxonomic Database of Gracillariidae (Lepidoptera). http://www.gracillariidae.net Accessed 15 February 2015.
  11. Dowden P.B. 1941: Parasites of the birch beaf-mining sawfly (Phyllotoma nemorata). - USDA Tech. Bull. 757: 25-30.
  12. Ellers J. & Jervis M.A. 2004: Why are so few parasitoid wasp species pro-ovigenic? - Evol. Ecol. Res. 6: 993-1002.
  13. Ermolaev I.V. 1977: Eco-faunistic review of leafminers (Lepidoptera, Gracillariidae) of the Southern Primorskii Territory. - Trudy Zool. Inst. Ross. Akad. Nauk 70: 98-116.
  14. Ermolaev I.V. 2014: Biological invasion of the lime leafminer Phyllonorycter issikii Kumata (Lepidoptera, Gracillariidae) in Europe. - Contemp. Probl. Ecol. 7: 324-333. Go to original source...
  15. Ermolaev I.V. & Zorin D.A. 2011: Ecological consequences of invasion of Phyllonorycter issikii (Lepidoptera, Gracillariidae) in lime forests in Udmurtia. - Entomol. Rev. 91: 592-598. Go to original source...
  16. Ermolaev I.V. & Zorin D.A. 2012: Distribution of the lime leafminer Phyllonorycter issikii (Lepidoptera, Gracillariidae) in natural stands. - Entomol. Rev. 91: 1088-1091. Go to original source...
  17. Ermolaev I.V., Yefremova Z.A. & Izhboldina N.V. 2011: Parasitoids as a mortality factor for the lime leafminer (Phyllonorycter issikii, Lepidoptera, Gracillariidae). - Entomol. Rev. 91: 326-334. Go to original source...
  18. Flanders S.E. 1950: Regulation of ovulation and egg disposal in the parasitic Hymenoptera. - Can. Entomol. 82: 134-140. Go to original source...
  19. Freise J.F., Heitland W. & Tosevski I. 2002: Parasitism of the horse chestnut leaf miner, Cameraria ohridella Deschka and Dimic (Lep., Gracillariidae), in Serbia and Macedonia. - J. Pest Sci. 75: 152-157.
  20. Fry J.M. 1989: Natural Enemy Databank, 1987. A Catalogue of Natural Enemies of Arthropods Derived from Records in the CIBC Natural Enemy Databank, 8: 185. CAB International, Wallingford.
  21. Girardoz S., Kenis M. & Quicke D.L.J. 2006: Recruitment of native parasitoids by an exotic leaf miner, Cameraria ohridella: host-parasitoid synchronization and influence of the environment. - Agric. Forest Entomol. 8: 49-56. Go to original source...
  22. Godfray H.C.J. 1994: Parasitoids: Behavioral and Evolutionary Ecology. Princeton University Press, Princeton, N.J., 488 pp.
  23. Grabenweger G. 2004: Poor control of the horse chestnut leafminer, Cameraria ohridella (Lepidoptera: Gracillariidae), by native European parasitoids: a synchronisation problem. - Eur. J. Entomol. 101: 189-192. Go to original source...
  24. Grabenweger G., Stolz M., Augustin S., Guichard S., Avtzis N., Bacher S., Kehrli P., Freise J., Heitland W., Girardoz S., Kenis M., Lethmayer C., Tomov R. & Volter L. 2005: Reasons for and effects of changes in the parasitoid complex of the horse chestnut leafminer, Cameraria ohridella (Lepidoptera: Gracillariidae). In: Plant Protection and Plant Health in Europe: Introduction and Spread of Invasive Species. Symposium Proceedings of the British Crop Protection Council No. 81, Berlin, 9.-11. June, 2005. BCPC, Alton (UK), pp. 179-184.
  25. Harvey J.A., Poelman E.H. & Tanaka T. 2013: Intrinsic inter- and intraspecific competition in parasitoid wasps. - Annu. Rev. Entomol. 58: 333-351. Go to original source...
  26. Hawkins B.A. 2005: Pattern and Process in Host-Parasitoid Interactions. Cambridge University Press, Cambridge, 412 pp.
  27. Hirao T. & Murakami M. 2008: Quantitative food webs of lepidopteran leafminers and their parasitoids in a Japanese deciduous forest. - Ecol. Res. 231: 159-168. Go to original source...
  28. Jervis M.A., Heimpel G.E., Ferns P.N., Harvey J.A. & Kidd N.A.C. 2001: Life-history strategies in parasitoid wasps: a comparative analysis of "ovigeny." - J. Anim. Ecol. 70: 442-458. Go to original source...
  29. Jervis M.A., Ferns P.N. & Heimpel G.E. 2003: Body size and the timing of egg production in parasitoid wasps: a comparative analysis body size and the timing of egg production in parasitoid wasps: a comparative analysis. - Funct. Ecol. 17: 375-383. Go to original source...
  30. Jervis M.A., Ellers J. & Harvey J.A. 2008: Resource acquisition, allocation, and utilization in parasitoid reproductive strategies. - Annu. Rev. Entomol. 53: 361-385. Go to original source...
  31. Jurc M. 2012: The lime leafminer (Phyllonorycter issikii) in Slovenia. - Sumarski List 136: 119-127.
  32. Kamijo K. 1965: Descriptions of five new species of Eulophinae from Japan and other notes (Hymenoptera: Chalcidoidea). - Insecta Matsum. 28: 69-78.
  33. Kamijo K. 1977: Five new species of Cotterellia (Hymenoptera, Eulophidae) from Japan. - Kontyû 45: 253-261.
  34. Kamijo K. 1986: Description of a new species of Desmatocharis Graham (Hymenoptera, Eulophidae), with notes on other species. - Kontyû 54: 243-245.
  35. Kamijo K. & Ikeda E. 1997: A revision of Citrostichus and Mischotetrastichus (Hymenoptera: Eulophidae), with descriptions of a new genus and new species. - Japan. J. Entomol. 65: 562-582.
  36. Kirichenko N.I. 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. Go to original source...
  37. Kumata T. 1963: Taxomonic studies on the Lithocolleinae of Japan (Lepidoptera: Gracillariidae) Part 1. - Insecta Matsum. 25: 53-90.
  38. Kumata T., Kuroko H. & Park K.T. 1983: Some Korean species of the subfamily Lithocolletinae (Gracillariidae, Lepidoptera). - Kor. J. Plant Prot. 22: 213-227.
  39. Lupi D. 2005: A 3 year field survey of the natural enemies of the horse-chestnut leaf miner Cameraria ohridella in Lombardy, Italy. - BioControl 50: 113-126. Go to original source...
  40. Marković Č. & Stojanović A. 2012: Parasitoids of Phyllonorycter platani (Staudinger) (Lepidoptera, Gracillariidae) in Serbia. - J. Plant Stud. 1: 79-84. Go to original source...
  41. Matoąević D. 2007: First record of Phyllnorycter issikii and distribution of invasive leafminer species from the family of Gracillariidae in Croatia. - Sumar. Inst. Jastr. 42: 127-142.
  42. Matoąević D. & Melika G. 2012: Diversity of parasitoid assemblages of native and alien leaf miners in Croatia. - Sumar. List 442: 367-376.
  43. Matoąević D. & Melika G. 2013: Recruitment of native parasitoids to a new invasive host: first results of Dryocosmus kuriphilus parasitoid assemblage in Croatia. - Bull. Insectol. 66: 231-238.
  44. Mészáros Z. & Szabóky C. 2005: The practical album of the Hungarian micromoths. - Növényvédelem (Suppl.): 178 pp. [in Hungarian].
  45. Mey W. 1991: On the significance of native parasitoid complexes in the current range extension by four Phyllonorycter species into Europe (Insecta, Lepidoptera, Hymenoptera). - Mitt. Zool. Mus. Berl. 67: 177-194. Go to original source...
  46. Noyes J.S. 2015: Universal Chalcidoidea Database. http://www.nhm.ac.uk/research-curation/research/projects/chalcidoids/database/ Accessed 1 January 2014.
  47. Pennacchio F. & Strand M.R. 2006: Evolution of developmental strategies in parasitic Hymenoptera. - Annu. Rev. Entomol. 51: 233-258. Go to original source...
  48. Perny B. 2007: Lindenminiermotte Phyllonorycter issikii: Vorkommen in Österreich nach mehreren Verdachtsfällen nun bestätigt. - Forstsch. Aktuell 38: 9-11.
  49. Pigott C.D. 1975: Natural regeneration of Tilia cordata in relation to forest-structure in the forest of Bialowieza, Poland. - Phil. Transact. R. Soc. Lond. (B) 270: 151-179. Go to original source...
  50. Pinto M.L., Salerno G. & Wajnberg E. 2005: Biology and behaviour of Cirrospilus diallus and Cirrospilus pictus, parasitoids of Phyllocnistis citrella. - BioControl 50: 921-935. Go to original source...
  51. Reinhardt R. & Rennwald E. 2008: Phyllonorycter issikii (Kumata, 1963) jetzt auch in Sachsen-Anhalt: mit einem Überblick über den gegenwärtigen Stand der Arealerweiterung in Deutschland (Lepidoptera, Gracillariidae). - Entomol. Nachr. Ber. 51: 233-233.
  52. Rodeland J. 2007: Erstnachweis von Phyllonorycter issikii (Kumata, 1963) (Lepidoptera: Gracillariidae) für Rheinland-Pfalz. - Mainz. Naturwiss. 45: 279-281.
  53. Sato H. 1990: Parasitoid complexes of Lepidopteran leaf miners on oaks (Quercus dentata and Quercus mongolica) in Hokkaido, Japan. - Ecol. Res. 5: 1-8. Go to original source...
  54. Schönrogge K., Stone G.N. & Crawley M.J. 1995: Spatial and temporal variation in guild structure: parasitoids and inquilines of Andricus quercuscalicis (Hymenoptera: Cynipidae) in its native and alien ranges. - Oikos 72: 51-60. Go to original source...
  55. Schönrogge K., Stone G.N. & Crawley M.J. 1996: Alien herbivores and native parasitoids: rapid development of guild structure in an invading gall wasp, Andricus quercuscalicis (Hymenoptera: Cynipidae). - Ecol. Entomol. 21: 71-80. Go to original source...
  56. Schönrogge K., Begg T., Williams R., Melika G., Randle Z. & Stone G.N. 2011: Range expansion and enemy recruitment by eight alien gallwasp species in Britain. - Insect Conserv. Div. 5: 298-311. Go to original source...
  57. ©efrová H. 2002: Phyllonorycter issikii (Kumata, 1963) - bionomics ecological impact and spread in Europe (Lepidoptera, Gracillariidae). - Acta Univ. Agric. Silvic. Mendel. Brun. 50: 99-104.
  58. ©efrová H. 2003: Invasions of Lithocolletinae species in Europe - causes, kinds, limits and ecological impact (Lepidoptera, Gracillariidae). - Ekologia (Bratislava) 22: 132-142.
  59. Segerer A. 2008: Der Lindenminierfalter Phyllonorycter issikii (Kumata, 1963) - ein wenig bekanntes Neozoon in Bayern - (Lepidoptera: Gracillariidae). - Nachrichtenbl. Bayer. Entomol. 57: 74-78.
  60. Stolnicu A.-M. & Ureche C. 2007: Data regarding the presence of the Phyllonorycter issikii (Kumata) (Lepidoptera: Gracillariidae) in romanian fauna. - Anal. Ştiinţ. Univ. Al. I. Cuza 53: 103-108.
  61. Stone G.N., Schönrogge K., Crawley M.J. & Fraser S. 1995: Geographic variation in the parasitoid community associated with an invading gallwasp, Andricus quercuscalicis (Hymenoptera: Cynipidae). - Oecologia 104: 207-217. Go to original source...
  62. Szabóky C. & Csóka G. 2003: The occurrence of the lime leafminer (Phyllonorycter issikii Kumata, 1963; Lep. Gracillariidae) in Hungary. - Növényvédelem 39: 23-24 [in Hungarian].
  63. Szőcs L., Melika G. & Csóka G. 2013: Data on the parasitoid complexes of leaf mining insects on oaks. - Erdészettudományi Közlemények 3: 251-259 [in Hungarian].
  64. 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].
  65. Thomson L.J., Macfadyen S. & Hoffmann A.A. 2010: Predicting the effects of climate change on natural enemies of agricultural pests. - Biol. Contr. 52: 296-306. Go to original source...
  66. Tomov R. 2009: A review of mortality factors of three invasive leafminer moths (Lepidoptera) in Bulgaria. In Stojnić B. (ed.): VI. Congress of Plant Protection with Symposium about Biological Control of Invasive Species, Zlatibor, 23.-27. November 2009. Book of Abstracts and Papers II. Plant Protection Society of Serbia, Beograd, pp. 83-85.
  67. Urbaneja A., Hinarejos R., Llácer E., Garrido A. & Jacas J.A. 2002: Effect of temperature on life history of Cirrospilus vittatus (Hymenoptera: Eulophidae), an ectoparasitoid of Phyllocnistis citrella (Lepidoptera: Gracillariidae). - J. Econ. Entomol. 95: 250-255. Go to original source...
  68. Volter L. & Kenis M. 2006: Parasitoid complex and parasitism rates of the horse chestnut leafminer, Cameraria ohridella(Lepidoptera: Gracillariidae) in the Czech Republic, Slovakia and Slovenia. - Eur. J. Entomol. 103: 365-370. Go to original source...
  69. Yefremova Z.A. & Kravchenko V.D. 2015: Interactions among host plants, Lepidoptera leaf miners and their parasitoids in the forest-steppe zone of Russia (Insecta: Lepidoptera, Hymenoptera). - SHILAP Revta Lepidopterol. 43: 271-280.
  70. Yefremova Z.A. & Mishchenko A.V. 2008: The parasitoid complex (Hymenoptera, Eulophidae) of the leafminer Phyllonorycter issikii (Kumata) (Lepidoptera, Gracillariidae) from the Middle Volga Basin. - Entomol. Rev. 88: 178-185. Go to original source...
  71. Yefremova Z.A. & Mishchenko A.V. 2012: The preimaginal stages of Minotetrastichus frontalis (Nees) and Chrysocharis laomedon (Walker) (Hymenoptera: Eulophidae), parasitoids associated with Phyllonorycter issikii (Kumata) (Lepidoptera, Gracillariidae). - J. Nat. Hist. 46: 1283-1305. Go to original source...
  72. Yefremova Z.A., Krayushkina A.V. & Mishchenko A.V. 2009: Parasitoid complexes (Hymenoptera, Eulophidae) of leafminers of the genus Phyllonorycter (Lepidoptera, Gracillariidae) in the Middle Volga Basin. - Entomol. Rev. 89: 903-911. Go to original source...
  73. Yefremova Z.A., Yegorenkova E.N. & Mishchenko A.V. 2013: Eulophid wasps (Hymenoptera, Eulophidae), parasitoids of leaf-mining moths (Lepidoptera: Gracillariidae, Nepticulidae, Tischeriidae) on the English oak in the Middle Volga area. - Entomol. Rev. 93: 591-597. Go to original source...
  74. Yegorenkova E.N., Yefremova Z.A. & Kostjukov V.V. 2007: Contributions to the knowledge of Tetrastichine wasps (Hymenoptera, Eulophidae, Tetrastichinae) of the Middle Volga region. - Entomol. Rev. 87: 1180-1192. Go to original source...