Skip to main content
Log in

Parasitoids (Hymenoptera) as a Mortality Factor for Cameraria ohridella Deschka & Dimić, 1986 (Lepidoptera, Gracillariidae)

  • Published:
Russian Journal of Biological Invasions Aims and scope Submit manuscript

Abstract

This review is devoted to the complexes of parasitoids of Cameraria ohridella Deschka & Dimić, 1986 (Lepidoptera, Gracillariidae) in the secondary range of the leaf miner. Over 30 years of research, 99 species from 6 families of Hymenoptera have been identified. The parasitoids are represented by polyphages. The attractiveness of C. ohridella for parasitoids grows in the following stage order: caterpillar–pronymph–pupa. Egg parasitoids of the miner are not known. Indices of parasitoid infestation in C. ohridella populations are everywhere low. The reasons for the ineffectiveness of the complexes of miner parasitoids are shown.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

REFERENCES

  1. Akimov, I.A., Zerova, M.D., Narol’skii, N.B., Sviridov, S.V., Kokhanets, A.M., Nikitenko, G.N., and Gershenzon, Z.S., Biology of a chestnut mining moth Cameraria ohridella (Lepidoptera, Gracillariidae) in Ukraine. Communication 1, Vestn. Zool., 2003, vol. 37, no. 5, pp. 41–52.

    Google Scholar 

  2. Alekseev, V.N., Belokobylskij, S.A., Chemyreva, V.G., Davidian, E.M., Egorenkova, E.N., Humala, A.E., Kasparyan, D.R., Khalaim, A.I., Kolyada, V.A., Kosheleva, O.V., Kostjukov, V.V., Kotenko, A.G., Lelej, A.S., Melika, G., Samartsev, K.G., Sundukov, Yu.N., Timokhov, A.V., Trjapitsyn, S.V., Trjapitsyn, V.A., Tselikh, E.V., Achterberg, C., and Zerova, M.D., Annotated catalogue of the Hymenoptera of Russia. Aprocrita: Parasitica, Proc. Zool. Inst. Russ. Acad. Sci., St. Petersburg: Zool. Instit. Russ. Acad. Sci., 2019, vol. 2, supplement 8.

  3. Andriescu, I., Ureche, C., Perju, T., and Stolnicu, A.M., Formation of the parasitoid complexes in four invasive mining species of Macrolepidopterans in Romania, in “Sustainable Use, Protection of Animal World and Forest Management in the Context of Climate Change” Dedicated to the 70th Anniversary of the Creation of the First Research Institutions and the 55th Anniversary of the Inauguration and Foundation of the Academy of Sciences of Moldova. IX Int. Conf. of Zoologists, 12–13 October, 2016, Chisinau, 2016, pp. 90–92.

  4. Antyukhova, O.V., and Meshkova, V.L. Fitofagi dekorativnykh drevesno-kustarnikovykh porod v Pridnestrov’e (Phytophages of Ornamental Trees and Shrubs in Transnistria), Tiraspol: Pridnestr. Ped. Univ., 2011.

  5. Askew, R.R. and Shaw, M.R., 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., 1979, vol. 67, pp. 31–49.

    Article  Google Scholar 

  6. Askew, R.R. and Shaw, M.R., Parasitoid communities: Their size, structure, and development, in Insect Parasitoids, Waage J. and Greathead D., Eds., London: Academic, 1986, pp. 225–264.

    Google Scholar 

  7. Backhaus, G.F., Wulf, A., Kehr, R., and Schröder, T., Die Rosskastanien-Miniermotte (Cameraria ohridella)— Biologie, Verbreitung und Gegenmaßnahmen, Nachrichtenbl. Dtsch. Pflanzenschutzdienstes, 2002, vol. 54, no. 3, pp. 56–62.

    Google Scholar 

  8. Balázs, K. and Thuróczy, C., Über den Rarasitoidkomplex von Cameraria ohridella Deschka & Dimič 1986 (Lepidoptera, Lithocolletidae), Entomol. Basiliensia, 2000, vol. 22, pp. 269–277.

    Google Scholar 

  9. Balázs, K., Thuróczy, C., and Ripka, G., Parasitoids of Cameraria ohridella Deschka & Dimic (Lepidoptera: Gracillariidae) in Hungary, in Parasitic Hymenoptera: Taxonomy and Biological Control. Int. Symp., 14–17 May, 2001, Köszeg, 2001, p. 24.

  10. Baur, H., Determination list of entomophagous insects no. 14, Bulletin. Section Regionale Ouest Palaearctique, Organisation Internationale de Lutte Biologique, 2005, vol. 28, no. 11.

  11. Beyarslan, A., Checklist of Turkish Doryctinae (Hymenoptera, Braconidae), Linzer Biol. Beitr., 2017, vol. 49, no. 1, pp. 415–440.

    Google Scholar 

  12. Bhatti, I., Ozanne, C. and Shaw, P., Parasitoids and parasitism rates of the horse chestnut leaf miner Cameraria ohridella Deschka and Dimić (Lepidoptera: Gracillariidae) across four sites in south-west London, Arboricultural Journal: The International Journal of Urban Forestry, 2013, vol. 35, no. 3, p. 147–149.

    Article  Google Scholar 

  13. Bouček, Z. and Askew, R.R., Index of Palaearctic Eulophidae (excl. Tetrastichinae), in Index of Entomophagous Insects, Paris, 1968.

  14. Bystrowski, C., Celmer-Warda, K., and Tarwacki, G., Effects of horse chestnut (Aesculus hippocastanum L.) site on horse chestnut leafminer (Cameraria ohridella Deschka & Dimić) parazytoids appearance and number in Central Poland, Leśne Prace Badawcze, 2008, vol. 69, no. 1, pp. 49–55.

    Google Scholar 

  15. Cebeci, H.H., Grabenweger, G., and Ayberk, H., Eulophid parasitoids (Hymenoptera: Eulophidae) of the horse chestnut leafminer, Cameraria ohridella (Lepidoptera: Gracillariidae), from Istanbul, Turkey, Turk. J. Zool. 2011, vol. 35, no. 5, pp. 777–780.

    Google Scholar 

  16. Cebeci, H.H., Markovic, C., Grabenweger, G., Ayberk, H., Dobrosavljevic, J., Goltas, M., and Stojanovic, A., Preliminary notes on pupal parasitism rates of the horse chestnut leafminer, Cameraria ohridella (Lepidoptera: Gracillariidae) in Belgrade and Istanbul, Fresenius’ Environ. Bull., 2018, vol. 27, no. 10, pp. 7122–7124.

    CAS  Google Scholar 

  17. Celmer-Warda, K., Bystrowski, C., and Tarwacki, G., Species composition of Cameraria ohridella Deschka & Dimic (Lep., Gracillariidae) parasitoids from Poland, in Alien Invasive Species and International Trade, Evans, H. and Oszako, T., Eds., Warsaw: Forest Research Inst., 2007, p. 163–164.

    Google Scholar 

  18. Clabassi, I., Giugovaz, L., Reggiori, F., and Rama, F., Monitoraggio di Cameraria ohridella Deschka & Dimic (Lep., Gracillariidae) dell’ippocastano nella provincia di Trieste: Primi risultati con l’uso del feromone specifico, Atti Giornate Fitopatologiche, 2002, vol. 1, pp. 513–518.

    Google Scholar 

  19. Cornell, H.V. and Hawkins, B.A., Accumulation of native parasitoids species on introduced herbivores: A comparison of hosts as natives and hosts as invaders, Am. Nat., 1993, vol. 141, no. 6, pp. 847–865.

    Article  CAS  PubMed  Google Scholar 

  20. Czencz, K. and Būrges, Gy., Horse-chestnut leafminer (Cameraria ohridella Deschka et Dimic 1986, Lep. Lithocolletidae), Növényvédelem, 1996, vol. 32, no. 9, pp. 437–445.

    Google Scholar 

  21. Del Bene, G. and Gargani, E., Cameraria ohridella Deschka & Dimic (Lep. Gracillariidae) and its natural enemies in Tuscany, Redia, 2003, vol. 86, pp. 115–127.

    Google Scholar 

  22. Del Bene, G. and Gargani, E., Biology and control of Phyllocnistis citrella and Cameraria ohridella in Central Italy, I International Cameraria Symposium, Cameraria Ohridella and Other Invasive Leaf-Miners in Europe (Praga, 24–27 March, 2004), 2004, p. 8.

  23. Deschka, G., Beitrag zur Populationsdynamik der Cameraria ohridella Deschka & Dimic (Gracillariidae, Lepidoptera, Chalcididae, Ichneumonidae, Hymenoptera), Linzer Biol. Beitr., 1995, vol. 27, no. 1, pp. 255–258.

    Google Scholar 

  24. Deschka, G. and Dimić, N., Cameraria ohridella sp. n. (Lep., Lithocolletidae) aus Mazedonien, Jugoslawien, Acta Entomol. Jugosl., 1986, vol. 22, nos. 1–2, pp. 11–23.

  25. Drosu, S., Chireceanu, C., Ciobanu, M., and Manole, T., Parasitism of the horse-chestnut leafminer Cameraria ohridella Deschka & Dimic (Lepidoptera, Gracillariidae) in Bucharest area, Entomol. Roman., 2007, vol. 12, pp. 251–255.

    Google Scholar 

  26. Ermolaev,  I.V., Yefremova, Z.A. , Rubleva, E.A. , and Kuropatkina, Yu.S., Parasitoids (Hymenoptera, Eulophidae, Braconidae) as a mortality factor for the aspen leafminer Phyllonorycter apparella (Lepidoptera, Gracillariidae) in its outbreak site in Udmurtia, Entomol. Rev., 2019, vol. 99, no. 4, pp. 494–503.

  27. Ermolaev, I.V., Yefremova, Z.A., Kuropatkina, Yu.S., and Yegorenkova, E.N., Changes in the structure of the parasitoid complex (Hymenoptera, Eulophidae, Braconidae) in outbreak focus of the aspen leafminer (Phyllonorycter apparella, Lepidoptera, Gracillariidae), Entomol. Rev., 2022, vol. 102, no. 3 (in press).

  28. Ferracini, C. and Alma, A., Evaluation of the community of native eulophid parasitoids on Cameraria ohridella Deschka and Dimic in urban areas, Environ. Entomol., 2007, vol. 36, no. 5, pp. 1147–1153.

    Article  PubMed  Google Scholar 

  29. Freise, J.F. and Heitland, W., Neue Aspekte zur Biologie und Ökologie der Roßkastanien-Miniermotte, Cameraria ohridella Deschka & Dimic 1986 (Lep., Gracillariidae), einem neuartigen Schädling Aesculus hippocastanum, Mitt. DGaaE, 2001, vol. 13, pp. 135–139.

    Google Scholar 

  30. Freise, J.F. and Heitland, W., Parasitierungsraten: Ermittlung und Interpretation am Fallberispiel der Roßkastanien-Miniermotte, Cameraria ohridella, einer invasiven und faunenfremden Schmetterlingsart in Europa, Mitt. DGaaE, 2004, vol. 14, pp. 347–350.

    Google Scholar 

  31. Freise, J.F., Heitland, W., and Toshevski, I., Parasitism of the horse-chestnut leaf miner, Cameraria ohridella Deschka & Dimic (Lep., Gracillariidae), in Serbia and Macedonia, Anz. Schaedlingskd., 2002, vol. 75, pp. 152–157.

    Article  Google Scholar 

  32. Girardoz, S., Kenis, M., and Quicke, D.L.J., Recruitment of native parasitoids by an exotic leaf miner, Cameraria ohridella: Host-parasitoid synchronization and influence of the environment, Agric. For. Entomol., 2006, vol. 8, pp. 49–56.

    Article  Google Scholar 

  33. Girardoz, S., Tomov, R., Eschen, R., Quicke, D.L.J., and Kenis, M., Two methods of assessing the mortality factors affecting the larvae and pupae of Cameraria ohridella in the leaves of Aesculus hippocastanum in Switzerland and Bulgaria, Bull. Entomol. Res., 2007a, vol. 97, pp. 445–453.

    Article  CAS  PubMed  Google Scholar 

  34. Girardoz, S., Volter, L., Tomov, R., Quicke, D.L.J., and Kenis, M., Variations in parasitism in sympatric populations of three invasive leaf miners, J. Appl. Entomol., 2007b, vol. 131, nos. 9–10, pp. 603–612.

    Article  Google Scholar 

  35. Girardoz, S., Quicke, D.L.J., and Kenis, M., Factors favouring the development and maintenance of outbreaks in an invasive leaf miner Cameraria ohridella (Lepidoptera: Gracillariidae): A life table study, Agric. For. Entomol., 2007c, vol. 9, pp. 141–158.

    Article  Google Scholar 

  36. Gninenko, Yu.I., Kostyukov, V.V., and Kosheleva, O.V., New invasive insects in forests and landscaped areas of the Krasnodar krai, Zashch. Karantin Rast., 2011, no. 4, pp. 49–50.

  37. Golosova, M.A., Gninenko, Yu.I., and Golosova, E.I., Kashtanovyi miner Cameraria ohridella – opasnyi karantinnyi vreditel’ na ob”ektakh gorodskogo ozeleneniya (Chestnut Miner Cameraria ohridella—A Hazardous Quarantine Pest in Urban Green Plantations), Moscow, 2008.

  38. Grabenweger, G., Host-parasitoid-hyperparasitoid interactions in the Cameraria ohridella complex (Lepidoptera: Gracillariidae), Abstracts of Papers. Int. Symp. Parasitic Hymenoptera: Taxonomy and Biological Control, 14–17 May, 2001, Kőszeg, Hungary, 2001, p. 30.

  39. Grabenweger, G., Parasitism of different larval stages of cameraria ohridella, BioControl, 2003, vol. 48, pp. 671–684.

    Article  Google Scholar 

  40. Grabenweger, G., Poor control of the horse chestnut leafminer, Cameraria ohridella (Lepidoptera: Gracillariidae), by native european parasitoids: A synchronization problem, Eur. J. Entomol., 2004, vol. 101, pp. 189–192.

    Article  Google Scholar 

  41. Grabenweger, G. and Grill, R., On the place of origin of Cameraria ohridella Deschka & Dimic (Gracillariidae: Lepidoptera), Beitr. Entomofaunistik, 2000, vol. 1, pp. 9–17.

    Google Scholar 

  42. Grabenweger, G. and Lethmayer, C., Occurrence and phenology of parasitic Chalcidoidea on the horse chestnut leafminer, Cameraria ohridella Deschka & Dimic (Lep., Gracillariidae), J. Appl. Entomol., 1999, vol. 123, pp. 257–260.

    Article  Google Scholar 

  43. Grabenweger, G., Avtzis, N., Girardoz, S., Hrasovec, B., Tomov, R., and Kenis, M., Parasitism of Cameraria ohridella (Lepidoptera: Gracillariidae) in natural and artificial horse-chestnut stands in the Balkans, Agric. For. Entomol., 2005, vol. 7, pp. 291–296.

    Article  Google Scholar 

  44. Grabenweger, G., Hopp, H., Jäckel, B., Balder, H., Koch, T., and Schmolling, S., Impact of poor host-parasitoid synchronization on the parasitism of Cameraria ohridella (Lepidoptera: Gracillariidae), Eur. J. Entomol., 2007, vol. 104, pp. 153–158.

    Article  Google Scholar 

  45. Grabenweger, G., Hopp, H., Scmolling, S., Koch, T., Balder, H., and Jäckel, B., Laboratory rearing and biological parameters of the eulophid Pnigalio agraules, a parasitoid of Cameraria ohridella, J. Appl. Entomol., Ser. P, 2009, vol. 133, no. 1, pp. 1–9.

    Google Scholar 

  46. Grabenweger, G., Kehrli, P., Zweimūller, I., Augustin, S., Avtzic, N., Bacher, S., Freise, J., Girardoz, S., Guichard, S., Heitland, W., Lethmayer, C., Stolz, M., Tomov, R., Volter, L., and Kenis, M., Temporal and spatial variations in the parasitoid complex of the horse chestnut leafminer during its invasion of Europe, Biol. Invas., 2010, vol. 12, no. 8, pp. 2797–2813.

    Article  Google Scholar 

  47. Graham, M.W.R., A reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae), with a revision of certain genera, Bull. Br. Mus. (Nat. Hist.). Entomol. Ser., 1987, vol. 55, no. 1, pp. 89–210.

    Google Scholar 

  48. Hawkins, B.A., Pattern and Process in Host-Parasitoid Interactions, Cambridge: Cambridge Univ. Press, 1994.

    Book  Google Scholar 

  49. Hellrigl, K., Zum Auftreten der Robinien-Miniermotte, Phyllonorycter robiniella (Clem.) und der Roßkastanien-Miniermotte, Cameraria ohridella Desch. & Dim. (Lep., Gracillariidae) in Südtirol, Anz. Schaedlingskd., Pflanzenschutz, Umweltschutz, 1998, vol. 71, pp. 65–68.

  50. Hellrigl, K., Die Verbreitung der Roßkastanien-Miniermotte Cameraria ohridella Deschka & Dimic, 1986 (Lepidoptera, Gracillariidae) in Sūdtirol, Veröffentlichungen des Tiroler Landesmuseum Ferdinandeum, 1999, vol. 79, pp. 265–300.

    Google Scholar 

  51. Hellrigl, K., Neue Erkenntnisse und Untersuchungen ūber die Roßkastanien-Miniermotte Cameraria ohridella Deschka & Dimic, 1986 (Lepidoptera, Gracillariidae), Gredleriana – Naturmuseum Sūdtirol, 2001, vol. 1, pp. 9–81.

    Google Scholar 

  52. Hernández-López, A., Rougerie, R., Augustin, S., Lees, D.C., Tomov, R., Kenis, M., Çota, E., Kullaj, E., Hansson, C., Grabenweger, G., Roques, A., and López-Vaamonde, C., Host tracking or cryptic adaptation? Phylogeography of Pediobius saulius (Hymenoptera, Eulophidae), a parasitoid of the highly invasive horse-chestnut leafminer, Evol. Appl., 2011.https://doi.org/10.1111/j.1752-4571.2011.00220.x

  53. Holler, C., Borgemeister, C.W., Haardt, H., and Powell, W., The relationship between primary parasitoids and hyperparasitoids of cereal aphids: An analysis of field data, J. Anim. Ecol.,1993, vol. 62, no. 1, pp. 12–21.

    Article  Google Scholar 

  54. Horváth, B. and Benedek, P., Changes in the population density of the horse-chestnut leafminer, Cameraria ohridella and of its parasitoid community at Hédervar during 7 consecutive years (1998–2004), Int. J. Hortic. Sci., 2007, vol. 13, no. 1, pp. 65–73.

    Article  Google Scholar 

  55. Jäckel, B., Grabenweger, G., Hopp, H., Koch, T., Schmolling, S., and Balder, H., Spectrum of hymenopterous parasitoids on urban stands of horse chestnut trees, Plant Protection and Plant Health in Europe: Introduction and Spread of Invasive Species, Humboldt Univ., Berlin, 9–11 June, 2005, pp. 237–238.

  56. Jäckel, B., Balder, H., Grabenweger, G., Hopp, H., Koch, T., and Schmolling, S., Standortabhängiges Parasitierungsverhalten von Gegenspielern der Roßkastanienminiermotte (Cameraria ohridella) in Berlin, Mitt. DGaaE, 2006a, vol. 15, pp. 81–84.

    Google Scholar 

  57. Jäckel, B., Grabenweger, G., Hopp, H., Balder, H., Koch, T., and Schmolling, S., Biologische Parameter von Pnigalio agraules, ein Parasitoid der Kastanienminiermotte, Nachrichtenbl. Dtsch. Pflanzenschutzdienst, 2006b, vol. 58, no. 10, p. 268.

    Google Scholar 

  58. Klug, T., Meyhöfer, R., Kreye, M., and Hommes, M., Native parasitoids and their potential to control the invasive leafminer, Cameraria ohridella Desch. & Dim. (Lep.: Gracillariidae), Bull. Entomol. Res., 2008, vol. 98, pp. 379–387.

    Article  CAS  PubMed  Google Scholar 

  59. Kosibowicz, M., Chestnut leafminer Cameraria ohridella Deschka & Dimic (Lepidopera, Gracillariidae), a new invasive pest of white horse chestnut Aesculus hippocastanum L. in Poland – biology and control methods, Lesne Prace Badawcze, 2005, vol. 2, pp. 121–132.

    Google Scholar 

  60. Kostyukov, V.V., Parasitoids complex of Cameraria ohridella Deschka et Dimic in Russia: Second report, in Biologicheskaya zashchita rastenii – osnova stabilizatsii agroekosistem (Proc. Int. Conf. “Biological Plant Protection as the Basis of Ecosystem Stabilization”), Krasnodar, 2016, no. 9, pp. 145–148.

  61. Kostyukov, V.V., Kosheleva, O.V., Nakonechnaya, I.V., and Gunasheva, Z.M., The first report on horse-chestnut leafminer parasites in Russia, Zashch. Karantin Rast., 2014a, no. 9, pp. 41–42.

  62. Kostyukov, V.V., Kosheleva, O.V., Gunasheva, Z.M., and Nakonechnaya, I.V., Parasitoids of Cameraria ohridella Deschka et Dimic (Lepidoptera, Gracillariidae) in the vicinity of Krasnodar, in Biologicheskaya zashchita rastenii – osnova stabilizatsii agroekosistem, Materialy mezhdunarodnoi nauchno-prakticheskoi konferentsii “Innovatsionnye tekhnologii primeneniya biologicheskikh sredstv zashchity rastenii v proizvodstve organicheskoi sel’skokhozyaistvennoi produktsii” (Biological Plant Protection as the Basis of Ecosystem Stabilization, Proc. Int. Conf. “Innovative Technologies for the Application of Biological Plant Protection Agents in Organic Agriculture”), Krasnodar, 2014b, no. 8, pp. 177–181.

  63. Kostyukov, V.V., Kosheleva, O.V., and Nakonechnaya, I.V., Parasites of Cameraria ohridella (Lepidoptera: Gracillariidae) in the vicinity of Krasnodar, in Evroaziatskii simpozium po pereponchatokrylym nasekomym (III simpozium SNG) (Abstr. Eurasian Symp. on Hymenoptera insects (III Symposium of the CIS Countries)), Nizhny Novgorod: Izd. Nizheg. Gos. Univ., 2015, p. 88.

  64. Kuldova, J., Hrdy, I., and Janšta, P., The horse chestnut leafminer Cameraria ohridella: Chemical control and notes on parasitisation, Plant Prot. Sci., 2007, vol. 43, no. 2, pp. 47–56.

    Article  Google Scholar 

  65. Lees, D.C., Lack, H.W., Rougerie, R., Hernandez-Lopez, A., Raus, T., Avtzic, N.D., Augustin, S., and Lopez-Vaamonde, C., Tracking origins of invasive herbivores through herbaria and archival DNA: The case of the horse-chestnut leaf miner, Front. Ecol. Environ., 2011, vol. 9, no. 6, pp. 322–328.

    Article  Google Scholar 

  66. Lethmayer, C., The parasitism of the horse chestnut leafmining moth (Cameraria ohridella) in Austria, in Parasitic Wasps: Evolution, Systematics, Biodiversity and Biological Control. Int. Symp., 14–17 May, 2001, Kőszeg, Hungary, Agroinform Budapest, 2002, pp. 400–404.

  67. Lethmayer, C., Über 10 Jahre Cameraria ohridella (Gracillariidae, Lepidoptera) – neue Nūtzlinge?, Entomol. Austriaca, 2003, vol. 8, pp. 3–6.

    Google Scholar 

  68. Lethmayer, C., 10 years of experience with the invasive horse chestnut leafminer (Cameraria ohridella) in Austria, Plant Protection and Plant Health in Europe: Introduction and Spread of Invasive Species, British Crop Production Council, 2005, vol. 81, pp. 61–66.

    Google Scholar 

  69. Lethmayer, C. and Grabenweger, G., Naturliche Parasitoide der Kastanienminiermotte (Cameraria ohridella), Forstschutz Aktuell, 1997, vol. 21, p. 30.

    Google Scholar 

  70. Lupi, D., A 3 year field survey of the natural enemies of the horse-chestnut leaf miner Cameraria ohridella in Lombardy, Italy, BioControl, 2005, vol. 50, pp. 113–126.

    Article  Google Scholar 

  71. Lupi, D. and Colombo, M., Indagini preliminary sui limitatori naturali di Cameraria ohridella Deschka & Dimic (Lepidopera, Gracillariidae) in Lombardia, Inf. Fitopatol., 2003, vol. 1, pp. 48–52.

    Google Scholar 

  72. Lupi, D. and Jucker, C., Minotetrastichus ecus y Closterocerus trifasciatus dos parasitoides importantes de Cameraria ohridella, Phytoma España, 2002, no. 144, pp. 202–203.

  73. Maini, S. and Santi, F., Cameraria ohridella microlepidottero dannoso all’ippocastano: Prima segnalazione a Bologna e dintorni, Notiziarno sulla protezione delle piante, 1999, vol. 10, pp. 73–77.

  74. Marchesini, E., Pasini, M., and Galbero, G., Parassitoidi della minatrice fogliare degli ippocastani, Inf. Agr., 2002, vol. 58, no. 27, pp. 75–77.

    Google Scholar 

  75. Matošević, D., Leafminers of woody plants in Croatia and their parasitoids, Doctorate (For.) Dissertation, Zagreb, 2007.

  76. Matošević, D. and Melika, G., Diversity of parasitoids assemblages of native and alien leaf miners in Croatia, Šumarski List, 2012, nos 7–8, pp. 367–376.

  77. Meshkova, V.L. and Mikulina, I.N., Entomophages of adventive leafminers in green plantations of Kharkiv region, in Sovremennoe sostoyanie i perspektivy okhrany i zashchity lesov v sisteme ustoichivogo razvitiya, Materialy mezhdunarodnoi konferentsii (Current State and Prospects for the Conservation and Protection of Forests in the System of Sustainable Development, Proc. Int. Conf.), Gomel’: Inst. Lesa NAN Belarusi, 2013, pp. 92–96.

  78. Moreth, L., Baur, H., Schönitzer, K., and Diller, E., Zum Parasitoid-Komplex der Roßkastanien-Miniermotte in Bayern (Cameraria ohridella, Gracillariidae, Lithocolletinae), Mitt. DGaaE, 2000, vol. 12, pp. 489–492.

    Google Scholar 

  79. Novákova, P., Holuša, and Horák J., The role of geography and host abundance in the distribution of parasitoids of an alien pest, PeerJ, 2016, vol. 4, p. 1592. https://doi.org/10.7717/peerj.1592

    Article  CAS  Google Scholar 

  80. Oester, P. and Shaw, D., Persistence of introduced parasitoid wasps on larch casebearer (Coleophora laricella) in the Blue Mountains, Oregon, MWM Gazette, 2012, pp. 2–3.

    Google Scholar 

  81. Oltean, I., Soporan, C., Florian, V., Varga, M., Macavei, L., and Florian, T., Results on parasitic of level of larvae and pupae of Cameraria ohridella Deschka-Dimić, Bulletin UASVM Agriculture, 2015, vol. 72, no. 1, pp. 187–192.

    Google Scholar 

  82. Pelov, V., Tomov, R., and Trenchev, G., Cameraria ohridella Deschka et Dimic (Gracillariidae: Lepidoptera)— new pest of Aesculus hippocastanum L. in Bulgaria, Natl. Conf. for Forest Protection, Sofia, 30 March, 1993, pp. 95–99.

    Google Scholar 

  83. Pocock, M., Evans, D., Straw, N., and Polaszek, A., The horse-chestnut leaf-miner and its parasitoids, Br. Wildl., 2011, pp. 305–313.

  84. Poelman, E.H., Bruinsma, M., Zhu, F., Weldegergis, B.T., Boursault, A.E., Jongema, Y., van Loon, J.J.A., Vet, L.E.M., Harvey, J.A., and Dicke, M., Hyperparasitoids use herbivore-induced plant volatiles to locate their parasitoid host, PLOS Biol., 2012, vol. 10, no. 11, 1001435.

  85. Pschorn-Walcher, H., Freiland-Biologie der eingeschleppten Roßkastanien-Miniermotte Cameraria ohridella Deschka & Demic (Lep., Gracillariiadae) im Wienerwald, Linzer Biol. Beitr., 1994, vol. 26, no. 2, pp. 633–642.

  86. Pschorn-Walcher, H., Zur Biologie und Populationsentwicklung der eingeschleppten Roßkastanien-Minermotte, Cameraria ohridella, Forstschutz Aktuell, 1997, vol. 21, pp. 7–10.

    Google Scholar 

  87. Puchberger, K.M., Cameraria ohridella Deschka & Dimić (Lep., Lithocolletidae) in Oberösterreich, Steyrer Entomologenrunde, 1990, vol. 24, pp. 79–81.

    Google Scholar 

  88. Radeghieri, P., Santi, F., and Maini, S., New species for the Italian fauna: Cirrospilus talitzkii (Hymenoptera Eulophidae), a new parasitoid of Cameraria ohridella (Lepidoptera Gracillariidae) (Preliminary note), Bull. Insectol., 2002, vol. 55, nos. 1–2, pp. 63–64.

    Google Scholar 

  89. Rämert B., Kenis M., Kärnestam E., Nyström M., and Rännbäck L.-M., Host plant sutability, population and parasitoids of the horse chectnut leafminer Cameraria ohridella (Lepidoptera: Gracillariidae) in southern Sweden, Acta Agric. Scand., Sect. B: Soil Plant Sci., 2011, vol. 61, no. 5, pp. 480–486.

    Google Scholar 

  90. Reider, S.K.,Thuroczy, Cs., Urfi Fogarasi, E., and Ripka, G., Survey of hymenopyerous pupal parasitoids of horse chestnut leafminer (Cameraria ohridella Deschka et Dimič 1986 (Lepidoptera, Gracillariidae)) in Hungary in 1996–1998, Nauchni Tr.–Vissh Selskostop. Inst. Plovdiv, 1999, vol. 44, no. 2, pp. 121–128.

    Google Scholar 

  91. Ryan, R.B., Evaluation of biological control: Introduced parasites of larch casebearer (Lepidoptera: Coleophoridae) in Oregon, Environ. Entomol., 1990, vol. 19, no. 6, pp. 1873–1881.

    Article  Google Scholar 

  92. Ryan, R.B., Before and after evaluation of biological control of the larch casebearer (Lepidoptera: Coleophoridae) in the Blue Mountains of Oregon and Washington, 1972–1995, Environ. Entomol.,1997, vol. 26, no. 3, pp. 703–715.

    Article  Google Scholar 

  93. Salleo, S., Nardini, A., Raimondo, F., lo Gullo, M.A., Pace, F., and Giacomich, P., Effects of defoliation caused by the leaf miner Cameraria ohridella on wood production and efficiency in Aesculus hippocastanum growing in north-eastern Italy, Trees, 2003, vol. 17, pp. 367–375.

    Article  Google Scholar 

  94. Sedlak, E. and Melber, A., Die Rosskastanien-Miniermotte (Cameraria ohridella) im Raum Hannover and ihre Parasiten, Ber. Naturhist. Ges., Hannover, 2007, vol. 149, pp. 83–106.

    Google Scholar 

  95. Šefrova, H., Control possibility and additional information on the horse-chestnut leafminer Cameraria ohridella Deschka & Dimić (Lepidoptera, Gracillariidae), Acta Univ. Agric. Silvic. Mendelianae Brun., 2001, vol. 49, no. 5, pp. 121–127.

    Google Scholar 

  96. Šefrova, H. and Laštůvka, Z., Dispersal of the horse-chestnut leafminer, Cameraria ohridella Deschka & Dimić, 1986, in Europe: Its course, ways and causes (Lepidoptera: Gracillariidae), Entomol. Z. Stuttgart, 2001, vol. 111, no. 7, pp. 194–198.

    Google Scholar 

  97. Šefrova, H. and Skuhravý, V., The larval morphology of Cameraria ohridella Deschka & Dimić compared with the genus Phyllonorycter Hūbner (Lepidoptera, Gracillariidae), Acta Univ. Agric. Silvic. Mendelianae Brun., 2000, vol. 48, no. 4, pp. 23–30.

    Google Scholar 

  98. Skuhravy, V., Zusammenfassende Betrachtung der Kenntnisse ūber die Roßkastanien-Miniermotte, Cameraria ohridella Desch. & Dem. (Lep., Gracillariiadae), Anz. Schaedlingskd., 1999, vol. 72, no. 4, pp. 95–99.

    Article  Google Scholar 

  99. Stojamović A. and Marković, C., Parasitoid complex of Cameraria ohridella (Lepidoptera: Gracillariidae) in Serbia, Phytoparasitica, 2004, vol. 32, no. 2, pp. 132–140.

    Article  Google Scholar 

  100. Stolz, M., Untersuchungen ūber Larval- und Puppenparasitoide von Cameraria ohridella in Hinblick auf ihre Eignung zur Laborzucht, Forstschutz Aktuel, 1997, vol. 21, p. 31.

    Google Scholar 

  101. Stolz, M., Untersuchungen zur Befallsregulierung der Kastanienminiermotte (Cameraria ohridella) durch natūrliche Gegenspieler, Förderungsdienst, 2000a, vol. 48, pp. 193–195.

    Google Scholar 

  102. Stolz, M., Untersuchungen zur Befallsregulierung der Kastanienminiermotte (Cameraria ohridella) durch natūrliche Gegenspieler, Abschlußbericht des Forschungsprojektes no. L 1061/96, 2000b.

  103. Szabóky, C., Verbreitung der Roßkastanienminiermotte in Ungarn, Forstschutz Aktuell, 1997, vol. 21, p. 4.

    Google Scholar 

  104. Tarwacki, G., Bystrowski, C., and Celmer-Warda, K., Effect of sun-exposure of the horse chestnut (Aesculus hippocastanum L.) on the occurrence and number of parasitoids of the horse chestnut leafminer (Cameraria ohridella Deschka & Dimic) in central Poland in 2004–2006, Folia For. Pol., Ser. A, 2012, vol. 54, no. 1, pp. 56–62.

    Google Scholar 

  105. Thalmann, Ch., Freise, J., Heitland, W., and Bacher, S., Effects of defoliation by horse chestnut leafminer (Cameraria ohridella) on reproduction in Aesculus hippocastanum, Trees, 2003, vol. 17, pp. 383–388.

    Article  Google Scholar 

  106. Thomas, W.P. and Hill, R.L., Phyllonorycter messaniella (Zeller), oak leaf-miner (Lepidoptera; Gracillariidae), in A Review of Biological Control of Invertebrate Pest and Weeds in New Zealand 1974 to 1987, Cameron, P.J., Hill, R.L., and Thomas, W.P., Eds., CAB Int. Inst. Biol. Control DSIR Entomol. Division, Walligford, Aukland, 1989, pp. 289–293.

  107. Tobias, V.I., Parasitic entomophagous insects, their biological characteristics, and types of parasitism, in Trudy Russkogo entomologicheskogo obshchestva (Proc. Russ. Entomol. Soc.), St. Petersburg: Zool. Inst. Ross. Akad. Nauk, 2004, vol. 75, no. 2.

  108. Tomiczek, Ch. and Krehan, H., The horsechestnut leafmining moth (Cameraria ohridella): A new pest in Central Europe, J. Arboric., 1998, vol. 23, no. 3, pp. 144–148.

    Google Scholar 

  109. Tomov, R.I., Parasitoid community attacking invading leafminer Cameraria ohridella Deshka et Dimic (Lepidoptera: Gracillariidae) in region of Sofia, 7th Eur. Congr. Entomol., October 7–13, 2002, Thessaloniki, Greece, 2002, p. 12.

  110. Tomov, R. and Hristov, B., Parasitoids of Cameraria ohridella Deschka et Dimic (Lep., Gracillariidae) in artificial stands of horse-chestnut of Bulgaria, Alien Arthropods in South East EuropeCrossroad of Three Continents. Proc. Int. Conf., 19–21 September, 2007, Sofia, Bulgaria, 2007, pp. 77–87.

  111. Toth, P. and Lukas, J., Parasitic Ichneumonoidea on the horse chestnut leaf miner, Cameraria ohridella (Lepidoptera: Gracillariidae) in Slovakia, J. Pest Sci., 2005, vol. 78, pp. 151–154.

    Article  Google Scholar 

  112. Toth, P., Kohlmajerova, J., and Lukas, J., First records of some Chalcidoidea species (Hymenoptera) parasiting on horse chestnut leaf miner, Cameraria ohridella (Lepidoptera, Gracillariidae), in Slovakia, Biologia (Bratislava), 2006, vol. 61, no. 5, pp. 495–496.

    Article  Google Scholar 

  113. Tribel’, S.O., Gamanova, O.M., and Sventoslavski, Ya., The Horse-Chestnut Leaf Miner, Kyiv: Kolobig, 2008.

    Google Scholar 

  114. Turoch, Ch., Balash, K., and Shaly, R., Changes in the parasite complex of the Ohrid leafminer Cameraria ohridella Deschka et Dimic in connection with the appearance of the pest in Hungary, in Informatsionnyi byulleten’ № 2 postoyannoi komissii po biologicheskoi zashchite lesa. Biologicheskaya zashchita lesa i lesopatologicheskii monitoring (Inf. Bull. no. 2 of the Permanent Commission for the Biological Protection of Forests. Biological Control of Forests and Forest Pathology Monitoring), Pushkino, 2003, pp. 164–171.

  115. Viggiani, G., Morpho-biologia di Pediobius saulius Walk. (Hym. Eulophidae) e considerazioni sulle specie congeneri europee, Bollettino del Laboratorio di Entomologia Agraria “Filipo Silvestri” di Portici, 1964, vol. 22, pp. 205–244.

  116. Volter, L. and Kenis, M., Parasitoid complex and parasitism rates of the horse chestnut leafminer, Cameraria ohridella (lepidoptera: gracillariidae) in the Czech Republic, Slovakia and Slovenia, Eur. J. Entomol., 2006, vol. 103, pp. 365–370.

    Article  Google Scholar 

  117. Universal Chalcidoidea Database, 2022. www.nhm.ac.uk/ our-science/data/chalcidoids/database/index.dsml. Accessed February, 7, 2022.

  118. Zerova, M.D., Nikitenko, G.N., Narol’skii, N.B., Gershenzon, Z.S., Sviridov, S.V., Lukash, O.V., and Babidorich, M.M., Kashtanovaya miniruyushchaya mol’ v Ukraine (The Horse-Chestnut Lefminer in Ukraine), Kyiv: Inst. Zool. im. I.I. Shmal’gauzena, 2007.

  119. Zhu, F., Cusumano, A., Bloem, J., Weldegergis, B.T., Villela, A., Fatouros, N.E., van Loon, J.J.A., Dicke, M., Harvey, J.A., Vogel, H., and Poelman, E.H., Symbiotic polydnavirus and venom reveal parasitoid to its hyperparasitoids, Proc. Natl. Acad. Sci. U. S. A., 2018, vol. 115, no. 20, pp. 5205–5210.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. Zini, M., II microlepidottero Cameraria ohridella Deschka & Dimic (Lepidopt., Gracillariidae) in città di trento nel 2001: Monitoraggio del volo e prove di controllo con trattamenti endoterapici, Gredleriana, 2002, vol. 2, pp. 147–162.

    Google Scholar 

Download references

ACKNOWLEDGMENTS

I am grateful to S.Yu. Sinev (Zoological Institute, Russian Academy of Sciences) and A.V. Selikhovkin (St. Petersburg State Forestry University) for supporting the work at different stages of its implementation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to I. V. Ermolaev.

Ethics declarations

Conflict of interest. The author declare that he has no conflicts of interest.Statement of the welfare of animals. The article does not contain any studies involving animals in experiments performed by the author.

Additional information

Translated by T. Kuznetsova

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ermolaev, I.V. Parasitoids (Hymenoptera) as a Mortality Factor for Cameraria ohridella Deschka & Dimić, 1986 (Lepidoptera, Gracillariidae). Russ J Biol Invasions 13, 284–300 (2022). https://doi.org/10.1134/S2075111722030031

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2075111722030031

Keywords:

Navigation