The native parasitoids exploiting the invasive leafminer Coptodisca lucifluella (Lepidoptera: Heliozelidae) in Southern Russia and Abkhazia
Abstract
The leafmining moth Coptodisca lucifluella (Lepidoptera: Heliozelidae) is the North American species, which recently invaded Europe. Here, we provide first data on the parasitoid assemblage associated with this leafminer in Southern Russia and Abkhazia. In 2024, altogether 28 parasitoid specimens were reared from the late-instar larvae and pupae of C. lucifluella and identified to seven parasitic wasp species. Among them, six species were from Eulophidae: Pnigalio soemius (Walker), Cirrospilus variegatus (Masi), C. viticola (Rondani), Chrysocharis pentheus (Walker), Closterocerus sp. (presumably new species to science), Minotetrastichus frontalis (Nees) and one from Eupelmidae: presumably Eupelmus kiefferi De Stefani. All these parasitoids are native to the studied area and have been documented on C. lucifluella for the first time. In Russia and Abkhazia, the parasitism rates reached 13% and 31%, respectively. Four species contributed the most to the leafminer mortality: M. frontalis (11 out of 13%) in Sochi (Russia), C. pentheus (12 out of 31%), C. viticola (8%), and C. variegatus (8%) in Gagra (Abkhazia). For the recorded parasitoids, the distribution and hosts are mentioned, and the original photographs of parasitoid adults are provided. Additionally, an exhaustive checklist of parasitoids associated with C. lucifluella in its modern range was compiled, accounting 32 species. Altogether, our findings suggest that during the invasion, C. lucifluella escaped from its aborigine enemies but became a target for the parasitoids naturally present in Southern Russia and Abkhazia.
Downloads
References
Ávila-Rodríguez V, Nava-Camberos U, Reyes-Carrillo JL, García de la Peña C, Márquez-Hernández C, García-Hernández JL (2015) First report of Coptodisca lucifluella in Pecan orchards, Carya illinoinensis in Mexico. (Primer reporte de Coptodisca lucifluella en huertas de nogal, Carya illinoinensis en México.). Southwestern Entomologist 40(2): 419–426. https://doi.org/10.3958/059.040.0215
Belokobylskij SA, Samartsev KG, Il’inskaya AS (Eds) (2019) Annotated Catalogue of the Hymenoptera of Russia. Apocrita: Parasitica. Vol. II. Proceedings of the Zoological Institute RAS 323(Supplement 8): 1–594. https://doi.org/10.31610/trudyzin/2019.supl.8.5 [in Russian]
Bernardo U, Monti MM, Nappo AG, Gebiola M, Russo A, Pedata PA, Viggiani G (2008) Species status of two populations of Pnigalio soemius (Hymenoptera: Eulophidae) reared from two different hosts: an integrative approach. Biological Control 46(3): 293–303. https://doi.org/10.1016/j.biocontrol.2008.05.009
Bernardo U, Pedata PA, 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. Biological Control 37: 98–107. https://doi.org/10.1016/j.biocontrol.2005.11.011
Bernardo U, Sasso R, Gebiola M, Viggiani G (2012) First record of a walnut shield bearer Coptodisca (Lepidoptera: Heliozelidae) in Europe. Journal of Applied Entomology 136: 638–640. https://doi.org/10.1111/j.1439-0418.2011.01693.x
Bernardo U, van Nieukerken E, Sasso R, Gebiola M, Gualtieri L, Viggiani G (2015) Characterization, distribution, biology and impact on Italian walnut orchards of the invasive North-American leafminer Coptodisca lucifluella (Lepidoptera: Heliozelidae). Bulletin of Entomological Research 105: 210–224. http://dx.doi.org/10.1017/S0007485314000947
Bouček Z (1959) A study of central European Eulophidae, II: Diaulinopsis and Cirrospilus (Hymenoptera). Sborník Entomologického Oddeleni Národního Musea v Praze 33: 171–194.
Bouček Z (1974) On the Chalcidoidea (Hymenoptera) described by C. Rondani. Redia 55: 241–283.
Bouček Z (1988) Australasian Chalcidoidea (Hymenoptera). A biosystematic revision of genera of fourteen families, with a reclassification of species. CAB International, Wallingford, 832 pp.
Bouček Z, Askew RR (1968) Palaearctic Eulophidae excl. Tetrastichinae. Index of Entomophagous Insects 3: 1–260.
Chireceanu C, Mustățea R-V, Teodoru A (2022) The walnut shield bearer Coptodisca lucifluella (Clemens, 1860) (Lepidoptera: Heliozelidae) – the first record in Romania. Romanian Journal of Plant Protection 15: 15–23. https://doi.org/10.54574/RJPP.15.02
Fedina AE (1968) Crimean-Caucasian Mountain country. Physical and geographical zoning of the USSR. Grodzetsky NA (Ed.). Moscow University Press, Moscow, 158–189. [in Russian]
Fuchs G, Guggemoos T, Karle-Fendt A, Morawietz B, Stühmer T, Wolf W (2022) Neue Ergebnisse in der bayerischen Kleinschmetterlingsfaunistik. Beiträge zur bayerischen Entomofaunistik 22: 59–68.
Gebiola M, Gomez-Zurita J, Monti MM, Navone P, Bernardo U (2012) Integration of molecular, ecological, morphological and endosymbiont data for species delimitation within the Pnigalio soemius complex (Hymenoptera: Eulophidae). Molecular Ecology 21(5): 1190–1208. https://doi.org/10.1111/j.1365-294X.2011.05428.x
Gibson GAP (1995) Parasitic wasps of the subfamily Eupelminae: classification and revision of world genera (Hymenoptera: Chalcidoidea, Eupelmidae). Memoirs on Entomology, International 5: i−v + 1−421.
Gibson GAP, Fusu L (2016) Revision of the Palaearctic species of Eupelmus (Eupelmus) Dalman (Hymenoptera: Chalcidoidea: Eupelmidae). Zootaxa 4081(1): 1–331. https://doi.org/10.11646/zootaxa.4081.1.1
Graham MWR de V (1987) A reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae), with a revision of certain genera. Bulletin of the British Museum 55(1): 1–392.
Graham MWR de V (1991) A reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae): revision of the remaining genera. Memoirs of the American Entomological Institute 49: 205–272.
Gröbler BC, Lewis OT (2008) Response of native parasitoids to a range-expanding host. Ecological Entomology 33(4): 453–463. https://doi.org/10.1111/j.1365-2311.2008.00990.x
Gualtieri L, Sasso R, Russo E, Nugnes F, Gebiola M, Bernard U (2015) The complex of parasitoids associated with the invasive leafminer Coptodisca lucifluella: indigenous species and a case of host-tracking. In: 4th International Entomophagous Insect Conference. 4–9 October 2015, Torre del Mar, Malaga, Spain.
Gulia VO, Orlovskaya TV, Adzinba ZI, Chitanava SM (2014) Physical and geographical characteristics of Abkhazia (Communication 1). International Journal of Applied and Fundamental Research 11: 35–38. [in Russian]
Hansson C (1985) Taxonomy and biology of the Palearctic species of Chrysocharis Förster, 1856 (Hymenoptera, Eulophidae). Entomologica Scandinavica 26(Supplement): 1–130. Hansson C (1987) Revision of the New World species of Chrysocharis Forster (Hymenoptera: Eulophidae). Entomologica Scandinavica 31(Supplement): 1–86.
Hansson C (1990) A taxonomic study on the Palaearctic species of Chrysonotomyia Ashmead and Neochrysocharis Kurdjumov (Hymenoptera: Eulophidae). Entomologica Scandinavica 21: 29–52. https://doi.org/10.1163/187631290X00021
Hansson C (1994) Re-evaluation of the genus Closterocerus Westwood (Hymenoptera: Eulophidae), with a revision of the Nearctic species. Entomologica Scandinavica 25: 1–25. https://doi.org/10.1163/187631294X00018
Hansson C (1995) Revision of the Nearctic species of Neochrysocharis Kurdjumov (Hymenoptera: Eulophidae). Entomologica Scandinavica 26(1): 27–46.
Heger T, Jeschke JM, Bernard-Verdier M, Musseau CL, Mietchen D (2024) Hypothesis Description: Enemy Release Hypothesis. Research Ideas and Outcomes 10: e107393. https://doi.org/10.3897/rio.10.e107393
Hesami S, Yefremova Z, Seyedebrahimi S (2006) Report of Cirrospilus variegatus (Hym.: Eulophidae), parasitoid of dipterous leafminers from Iran. Journal of Entomological Society of Iran 26(1): 93–94.
Heyerdahl RH, Dutcher JD (1985) Hymenopterous parasitoids of pecan leafminers. Journal of Entomological Science 20(4): 411–421. https://doi.org/10.18474/0749-8004-20.4.411
Huemer P (2021) Der Walnuss-Erzglanzfalter (Coptodisca lucifluella (Clemens, 1861)) und der Schwarznuss-Erzglanzfalter (Coptodisca juglandiella (Chambers, 1874)) aus Nordamerika erreichen Österreich (Lepidoptera: Heliozelidae). Beiträge zur Entomofaunistik 22: 312–314.
Kirichenko N, Augustin S, Kenis M (2019) Invasive leafminers on woody plants: a global review of pathways, impact, and management. Journal of Pest Science 92: 93–106. https://doi.org/10.1007/s10340-018-1009-6
Kirichenko NI, Gomboc S, Piškur B, de Groot M (2023) Use of an arboretum and DNA barcoding for the detection and identification of leaf-mining insects on alien woody plants. Forests 14: 641. https://doi.org/10.3390/f14030641
Kirichenko N, Gomboc S, Sule D (2025) First documentation of the Noth American leaf mining moth, Coptodisca lucifluella (Lepidoptera: Heliozelidae) in Croatia including on the Island of Šolta. Bašćina 34: 253–263.
Kirichenko N, Péré C, Baranchikov Y, Schaffner U, Kenis M (2013) Do alien plants escape from natural enemies of congeneric residents? Yes but not from all. Biological Invasions 15: 2105–2113. https://doi.org/10.1007/s10530-013-0436-9
Kirichenko NI, Shoshina EI, Zhuravleva EN, Khuapshykhu IK, Gomboc S, Ayba LYa, Karpun NN (2024) The North American leaf-mining moth Coptodisca lucifluella (Lepidoptera: Heliozelidae) reached Southern Russia and Abkhazia: genetic variability and potential for further spread. Acta Biologica Sibirica 10: 835–858. https://doi.org/10.5281/zenodo.13442550
Klug T, Meyhöfer R, Kreye M, Hommes M (2008) Native parasitoids and their potential to control the invasive leafminer, Cameraria ohridella DESCH. & DIM. (Lep.: Gracillariidae). Bulletin Entomological Research 98(4): 379–387. https://doi.org/10.1017/S0007485308005695
Kosheleva OV, Belokobylskij SA, Kirichenko NI (2022) The Hymenopterous Parasitoids of the Lime Leaf Miner Phyllonorycter issikii (Kumata) (Lepidoptera: Gracillariidae) from Its Native and Invaded Regions in Asian Russia. Diversity 14: 707. https://doi.org/10.3390/d14090707
Kurashev VN (1991) On some little-known parasitic chalcids (Hymenoptera, Eulophidae) from southern Turkmenia. Izvestiya Akademii Nauk Turkmenskoy SSR (Seriya Biologicheskikh Nauk) 4: 23–30. [in Russian]
LaSalle J (1994) North American genera of Tetrastichinae (Hymenoptera: Eulophidae). Journal of Natural History 28: 109–236. https://doi.org/10.1080/00222939400770091
Laštůvka Z, Laštůvka A (2020) Motýli (Lepidoptera) města Brna – historie a současnost. Mendelova univerzita, Brno, 120 pp.
Lepiforum (2025) Coptodica lucifluella. https://lepiforum.org/wiki/page/Coptodisca_lucifluella
Masi L (1907) Contribuzioni all conoscenza dei Calcididi Italiani. Bollettino del Laboratorio di Zoologia Generale e Agraria della R. Scuola Superiore d'Agricoltura, Portici 1: 231–295.
Muru D, Borowiec N, Thaon M, Ris., Madalina IV, Warot S, N, Vercken E (2020) The open bar is closed: restructuration of a native parasitoid community following successful control of an invasive pest. bioRxiv, version 6, peer-reviewed and recommended by PCI Zoology. http://dx.doi.org/10.1101/2019.12.20.884908
Mustățea R-V, Chireceanu C (2023) Further data on the establishment of Coptodisca lucifluella (Clemens, 1860) (Lepidoptera: Heliozelidae) in Romania. EPPO Bulletin 53: 632–642. https://doi.org/10.1111/epp.12945
Pályi B, Takács A, Szabóky CS (2019) Új diókártevő Kárpátalján. New pest of walnut in Subcarpathia. Kárpátaljai Vállalkozók Lapja 4: 16. [In Hungarian]
Perry RK, Heraty JM (2021) Read between the lineata: a revision of the tattooed wasps, Zagrammosoma Ashmead (Hymenoptera: Eulophidae), with descriptions of eleven new species. Zootaxa 4916(1): 1–108. https://doi.org/10.11646/zootaxa.4916.1.1
Prior KM, Hellmann JJ (2014) Does Enemy Release Contribute to the Success of Invasive Species? A Review of the Enemy Release Hypothesis. In: Keller RP, Cadotte MW, Sandiford D (Eds) Invasive species in a globalized world: ecological, social, and legal perspectives on policy. University of Chicago Press. Chicago Scholarship Online. https://doi.org/10.7208/chicago/9780226166216.003.0012
Rennwald E (2022) Présence de Coptodisca lucifluella (Clemens, 1861) en France (Lepidoptera, Heliozelidae). Revue de l'Association Roussillonnaise d'Entomologie 31 (4): 247–250.
Szabóky Cs, Takács A (2018) New data to the Microlepidoptera fauna of Hungary, part XVIII (Lepidoptera: Depressariidae, Elachistidae, Gelechiidae, Heliozelidae, Tortricidae). Folia Entomologica Hungarica 79: 115–122. https://doi.org/10.17112/FoliaEntHung.2018.79.115
Takács A, Szabóky C, Kutas J (2017) A dióaknázó fényesmoly (Coptodisca lucifluella Clemens, 1860 Lepidoptera: Heliozelidae) magyarországi megjelenése. The appearance of the walnut leafminer (Coptodisca lucifluella Clemens, 1860 Lepidoptera: Heliozelidae) in Hungary. Növényvédelem 78: 539–541. [In Hungarian]
Takács A, Szabóky C, Tóth B, Bozsó M, Kutas J, Molnár S, Richter I (2020) Nearctic walnut leafminers invade Europe: first Coptodisca lucifluella (Clemens, 1860) and now Coptodisca juglandiella (Chambers, 1874) (Lepidoptera, Heliozelidae). Nota Lepidoptero- logica 43: 77–93. https://doi.org/10.3897/nl.43.38686
Tokár Z, Šumpich J, Laštůvka A, Laštůvka Z, Liška J, Elsner J, Lendel A, Štefanovič R, Richter I (2021) Nové druhy drobných motýľov (Microlepidoptera) pre faunu Slovenska. Entomofauna Carpathica 33 (2): 1–20.
Tomov R (2020) First Records of the Walnut Shield Bearer Coptodisca lucifluella (Clemens, 1860) (Lepidoptera: Heliozelidae) in Bulgaria. Acta Zoologica Bulgarica 72: 697–700.
Trjapitzin VA (2009) A brief review of species of the genus Parablastothrix with description of a new species from Mexico (Hymenoptera: Encyrtidae). Zoosystematica Rossica 18(2): 291–294. https://doi.org/10.31610/zsr/2009.18.2.291 [in Russian]
Turnbow RH Jr, Franklin RT (1981) Bionomics of Brachys tessellatus in coastal plain (USA) scrub oak (Quercus laevis) communities. Annals of the Entomological Society of America 74(4): 351–358. https://doi.org/10.1093/aesa/74.4.351
UCD Community (2025) Universal Chalcidoidea Database (UCD) curated in TaxonWorks. https://ucd.chalcid.org/#/ (accessed on: 2025-03).
Vercher R, Costa-Comelles J, Marzal C, García-Marí F (2005) Recruitment of Native Parasitoid Species by the Invading Leafminer Phyllocnistis citrella (Lepidoptera: Gracillariidae) on Citrus in Spain. Environmental Entomology 34(5): 1129–1138. https://doi.org/10.1093/ee/34.5.1129
Yefremova Z, Kosheleva O, Yegorenkova E, Japoshvili G (2024) New records of Eulophidae (Hymenoptera: Chalcidoidea) from Georgia (Sakartvelo). Journal of the Entomological Research Society 26(2): 303–313. https://doi.org/10.51963/jers.v26i2.2589
Yu DSK, van Achterberg C, Horstmann K (2016) Taxapad. Ichneumonoidea 2015. Database on Flash-Drive. Ottawa, ON, Canada. www.taxapad.com (accessed on: 2025-03).
Zhu CD, LaSalle J, Huang DW (2002) A study of Chinese Cirrospilus Westwood (Hymenoptera: Eulophidae). Zoological Studies 41(1): 23–46.
Zuparko RL (1995) Notes on Parablastothrix nearctica (Hymenoptera: Encyrtidae). Proceedings of the Entomological Society of Washington 97(4): 884–886.
Copyright (c) 2025 Oksana V. Kosheleva, Elena N. Zhuravleva, Natalia N. Karpun, Natalia I. Kirichenko
This work is licensed under a Creative Commons Attribution 4.0 International License.
Acta Biologica Sibirica is a golden publisher, as we allow self-archiving, but most importantly we are fully transparent about your rights.
Authors may present and discuss their findings ahead of publication: at biological or scientific conferences, on preprint servers, in public databases, and in blogs, wikis, tweets, and other informal communication channels.
ABS allows authors to deposit manuscripts (currently under review or those for intended submission to ABS) in non-commercial, pre-print servers such as ArXiv.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License (CC BY 4.0) that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).
