Skip to main content
Log in

Diversity and interactions of the parasitoids (Hymenoptera: Chalcidoidea) of soft scales from Serbia

  • Research
  • Published:
Phytoparasitica Aims and scope Submit manuscript

Abstract

This research aimed to study the diversity of soft scale parasitoids and examine their potential in the biological control of harmful Coccidae on cultivated and ornamental plants. Forty species of parasitoid wasps from four families (Hymenoptera: Chalcidoidea) were reared and determined from 16 species of soft scales (Hemiptera: Coccidae). A total of 6,249 individuals of parasitoid wasps were collected from 35 localities in Serbia from 2014 to 2017. The most numerous genera are Metaphycus with 10, Coccophagus with 7, and Blastothrix with five reared species. The most abundant species is C. lycimnia, reared from second-instar larvae of all 16 species of scale insects and from females of 11 soft scale species, with a total of 1,053 individuals. Of the 40 identified species, 15 are new to the fauna of Serbia: Coccophagus piceae, Coccophagus proximus, Coccophagus silvestrii, Encarsia gigas (Aphelinidae), Adelencyrtus intersectus, Anagyrus schoenherri, Blastothrix brittanica, Blastothrix erythrostetha, Blastothrix hedqvisti, Encyrtus infidus, Metaphycus hageni, Metaphycus stanleyi, Metaphycus unicolor, Microterys hortulanus (Encyrtidae) and Eunotus obscurus (Pteromalidae). Ninety-nine (99) hymenopteran/coccoid associations were identified in this study, of which 16 associations are new.

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.

Fig. 1

Similar content being viewed by others

References

  • Abd-Rabou, S. (2011). Coccophagus Scutellaris (Hymenoptera: Aphelinidae): A highly effective biological control agent of soft scale insects (Hemiptera: Coccidae) in Egypt. Psyche, 431874. https://doi.org/10.1155/2011/431874

  • Abreu, J. A. S., Rovida, A. S., & Conte, H. (2015). Controle biológico Por insetos parasitoides em culturas agrícolas no Brasil: Revisão De Literatura. Uningá Review,22(2), 22–25.

    Google Scholar 

  • Bartlett, B. R. (1978). Coccidae. In C. P. Clausen (Ed.), Introduced parasites and predators of arthropod pests and weed: A world review. Agriculture Handbook (pp. 57–74). U.S. Department of Agriculture, U.S. Government Printing Office.

  • Ben-Dov, Y., & Hodgson, C. J. (1997). Soft scale insects: Their biology, natural enemies and control. Elsevier.

    Google Scholar 

  • Bernal, J., Luck, R. F., & Morse, J. G. (1999). Host influences on sex ratio, longevity, and egg load of two Metaphycus species parasitic on soft scales: Implications for insectary rearing. Entomologia Experimentalis et Applicata,92, 191–204.

    Article  Google Scholar 

  • Bernal, J. S., Luck, R. F., Morse, J. G., & Drury, M. S. (2001). Seasonal and scale size relationships between citricola scale (Homoptera: Coccidae) and its parasitoid complex (Hymenoptera: Chalcidoidea) on San Joaquin Valley citrus. Biological Control,20, 210–221. https://doi.org/10.1006/bcon.2000.0905

    Article  Google Scholar 

  • Boucek, Z., & Rasplus, J. Y. (1991). Illustrated key to West-Palaearctic genera of Pteromalidae (Hymenoptera: Chalcidoidea). Institut National de la Recherche Agronomique.

  • Clausen, C. P. (1932). The biology of Encyrtus infidus Rossi, a parasite of Lecanium kunoensis Kuw. (Hymen.). Annals of the Entomological Society of America,25(4), 670–687.

    Article  Google Scholar 

  • de Graham, M. W. R. (1991). A reclassification of the European Tetrastichinae (Hymenoptera: Eulophidae): Revision of the remaining genera. Memoirs of the American Entomological Institute,49, 322.

    Google Scholar 

  • Dean, H. A., & Bailey, J. C. (1960). Introduction of beneficial insects for the control of citrus scale insects and mites. Journal of the Rio Grande Valley Horticultural Society,4, 40–46.

    Google Scholar 

  • Dervišević, M., Stojanović, A., & Graora, D. (2021). First record and new hosts of Coccophagus Shillongensis Hayat and Singh, 1989 (Hymenoptera: Aphelinidae) in Serbia. Phytoparasitica,49, 547–551. https://doi.org/10.1007/s12600-021-00886-z

    Article  Google Scholar 

  • García-Morales, M., Denno, B. D., Miller, D. R., Miller, G. L., Ben-Dov, Y., & Hardy, N. B. (2016). ScaleNet: A literature-based model of scale insect biology and systematics. http://scalenet.info/. Accessed 12 June 2023.

  • Gill, R. J. (1988). The scale insects of California, Part I: The soft scales (Homoptera: Coccoidea: Coccidae). Technical Series in Agricultural Biosystematics and Plant Pathology. California Department of Food and Agriculture.

  • Gill, R. J., & Kosztarab, M. (1997). Economic importance. In Y. Ben-Dov & C. J. Hodgson (Eds.), Soft scale insects, their biology, natural enemies and control (pp. 161–163). Elsevier Science.

    Chapter  Google Scholar 

  • Glendenning, R. (1933). A successful parasite introduction into British Columbia. Canadian Entomologist,65(8), 169–171.

    Article  Google Scholar 

  • Guerrieri, E., & Noyes, J. (2000). Revision of European species of genus Metaphycus Mercet (Hymenoptera: Chalcidoidea: Encyrtidae), parasitoids of scale insects (Homoptera: Coccoidea). Systematic Entomology,25, 147–222.

    Article  Google Scholar 

  • Hayat, M. (1997). Aphelinidae. In Y. Ben-Dov & C. J. Hodgson (Eds.), Soft scale insects, their biology, natural enemies and control (pp. 111–145). Elsevier Science.

    Chapter  Google Scholar 

  • Hayat, M., & Singh, S. (1989). Description of a new Coccophagus of the lycimnia-group (Hymenoptera: Aphelinidae) from the Khasi hills, with some other species records from India. Colemania,5, 29–34.

    Google Scholar 

  • Herrbach, E., Alliaum, A., Prator, C. A., Daane, K. M., Cooper, M. L., & Almeida, R. P. P. (2017). Vector Transmission of Grapevine Leafroll-Associated Viruses. In B. Meng, G. Martelli, D. A. Golino & A. Fuch (Eds.), Grapevine Viruses: Molecular Biology, Diagnostics and Management (pp. 483–503). Springer Cham. https://doi.org/10.1007/978-3-319-57706-7_24

  • Japoshvili, G., & Stathas, G. (2017). New record of Coccophagus Shillongensis Hayat and Singh (Hymenoptera: Aphelinidae) from Europe, with some remarks on morphological variation. Phytoparasitica,45(5), 651–653. https://doi.org/10.1007/s12600-017-0628-4

    Article  Google Scholar 

  • Kakoti, B., Deka, B., Roy, S., & Babu, A. (2023). The scale insects: Its status, biology, ecology and management in tea plantations. Frontiers in Insect Science,2, 1048299. https://doi.org/10.3389/finsc.2022.1048299

    Article  PubMed  PubMed Central  Google Scholar 

  • Kapranas, A., & Tena, A. (2015). Encyrtid parasitoids of soft scale insects: Biology, behavior and their use in biological control. Annual Review of Entomology,60, 195–211. https://doi.org/10.1146/annurev-ento-010814-021053

    Article  CAS  PubMed  Google Scholar 

  • Kapranas, A., Morse, J. G., Pacheco, P., Forster, L. D., & Luck, R. F. (2007). Survey of brown soft scale Coccus hesperidum parasitoids in Southern California citrus. Biological Control,42, 288–299. https://doi.org/10.1016/j.biocontrol.2007.05.012

    Article  Google Scholar 

  • Kapranas, A., Hardy, I. C. W., Luck, R. F., & Morse, J. G. (2011). Parasitoid developmental mortality in the field: Patterns, causes and consequences for sex ratio and virginity. Journal of Animal Ecology,80, 192–203. https://doi.org/10.1111/j.1365-2656.2010.01767.x

    Article  PubMed  Google Scholar 

  • Kosztarab, M., & Kozár, F. (1988). Scale insects of central Europe. Series Entomologica (Vol. 41). Akadémiai Kiadó.

  • Masten-Milek, T. (2007). Fauna of scale insects (Insecta: Coccoidea) in the Republic of Croatia. Dissertation, University in Osijek, Faculty of Agriculture.

  • Mihajlović, L. (2015). Forest entolology. The University of Belgrade-Faculty of Forestry.

    Google Scholar 

  • Mihajlović, L., & Kozárzhevskaya, E. (1983). Effectivieness of entomophagous in reduction of noxious coccid population (Homoptera: Coccoidea). Plant Protection,64, 295–301.

    Google Scholar 

  • Mitić-Mužina, N. (1964). Role des parasites et des predateurs dans la reduction de la population de Lecanium Du Prunier (Parthenolecanium Corni Bouché) en Serbie. Protection Des Plantes,80, 359–378.

    Google Scholar 

  • Mitić-Mužina, N. (1967). Parasites du puceron globuleux (Sphaerolecanium Prunastri Fonsc.) (Homoptera, Coccoidea). Protection Des Plantes,93/95, 183–187.

    Google Scholar 

  • Nikol’skaya, M. N., & Yasnosh, V. A. (1966). Aphelinidae of the European part of U.S.S.R. and Caucasus. Opredeliteli Po Faune SSSR, Izdavaemie Zoologicheskim Institutom Akademii Nauk SSR (Vol. 91). 230 Academy of Sciences, USSR, Moscow and Leningrad.

  • Noyes, J. S. (1982). Collecting and preserving chalcid wasps (Hymenoptera: Chalcidoidea). Journal of Natural History,16, 315–334.

    Article  Google Scholar 

  • Noyes, J. S. (2019). Universal Chalcidoidea database. World Wide Web electronic publication. http://www.nhm.ac.uk/chalcidoids. Accessed 12 June 2023.

  • Prinsloo, G. L. (1997). Encyrtidae. In Y. Ben-Dov & C. J. Hodgson (Eds.), Soft scale insects: Their biology, natural enemies and control (pp. 69–109). Elsevier Science.

    Chapter  Google Scholar 

  • Santas, L. A. (1985). Parthenolecanium Corni Bouché an orchard scale pest producing honeydew foraged by bees in Greece. Entomologia Hellenica,3, 53–58.

    Article  Google Scholar 

  • Schmutterer, H. (1956). Zur Morphologie, Systematik Und Bionomie Der Physokermes-Arten an Fichte (Homopt. Cocc). Zeitschrift für Angewandte Entomologie,39, 445–466.

    Article  Google Scholar 

  • Schweizer, H., Luck, R. F., & Morse, J. G. (2003). Augmentative releases of Metaphycus sp. nr. Flavus against citricola scale on oranges in the San Joaquin Valley of California: Are early releases better than late ones? Journal of Economic Entomology,96, 1375–1387. https://doi.org/10.1093/jee/96.5.1375

    Article  PubMed  Google Scholar 

  • Stepaniuk, K., & Lagowska, B. (2006). Number and arrangement variation of submarginal tubercles in adult females parthenolecanium corni group (Hemiptera, Coccidae) and its value as a taxonomic character. Polish Journal of Entomology,75(2), 293–301.

    Google Scholar 

  • Tena, A., & Garcia-Marí, F. (2008). Suitability of citricola scale Coccus Pseudomagnoliarum (Hemiptera: Coccidae) as host of Metaphycus Helvolus (Hymenoptera: Encyrtidae): Influence of host size and encapsulation. Biological Control,6, 341–347.

    Article  Google Scholar 

  • Tena, A., & Garcia-Marí, F. (2009). Brood size, sex ratio and egg load of Metaphycus Lounsburyi (Hymenoptera: Encyrtidae) when parasitizing adult females of black scale Saissetia oleae (Hemiptera: Coccidae) in the field. Biological Control,51, 110–115. https://doi.org/10.1016/j.biocontrol.2009.06.007

    Article  Google Scholar 

  • Trjapitzin, V. A. (1989). Parasitic Hymenoptera of the Fam. Encyrtidae of Palaearctics, Academy of Sciences of The USSR, pp. 488. (in Russian).

  • Ülgentürk, S., & Çanakçioğlu, H. (2004). Scale insect pests on ornamental plants in urban habitats in Turkey. Journal of Pest Science,77(2), 79–84. https://doi.org/10.1007/s10340-003-0031-4

    Article  Google Scholar 

  • Ülgentürk, S., Cosic, B., Özdemir, I., İpek, A., & Sorkun, K. (2020). Honeydew producing insects in some forests of Turkey and their potential to produce of honeydew honey. Baltic Forestry,26(1), id397. https://doi.org/10.46490/BF397

    Article  Google Scholar 

  • Wajnberg, E., Bernstein, C., & van Alphen, J. J. M. (2008). Behavioral ecology of insect parasitoids-from theoretical approaches to field applications. Blackwell Publishing Ltd. https://doi.org/10.1002/9780470696200

  • Wolff, V. R. S., Pulz, C. E., Silva, D. D., Mezzomo, J. B., & Prade, C. A. (2004). Inimigos Naturais Associados à Diaspididae (Hemiptera, Sternorrhyncha), ocorrentes em Citrus sinensis (Linnaeus) Osbeck, no Rio Grande do sul, Brasil: I – joaninhas e fungos entomopatogênicos. Arquivos do Inst tuto Biologico,71, 55–361.

    Google Scholar 

Download references

Acknowledgements

This research was funded by the Ministry of Science and Technological Development of the Republic of Serbia, Grant No. 451-03-47/2023-01/200214.

Author information

Authors and Affiliations

Authors

Contributions

M. Dervišević: Conceptualisation, Investigation, Data Curation, Formal analysis, Writing - original draft. A. Stojanović: Methodology, Investigation. Lj. Mihajlović: Supervision, Writing - review & editing. D. Graora: Conceptualisation, Methodology, Supervision, Writing - review & editing. All authors have read and approved the fnal manuscript for publication.

Corresponding author

Correspondence to Marina Dervišević.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dervišević, M., Stojanović, A., Mihajlović, L. et al. Diversity and interactions of the parasitoids (Hymenoptera: Chalcidoidea) of soft scales from Serbia. Phytoparasitica 52, 18 (2024). https://doi.org/10.1007/s12600-024-01139-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12600-024-01139-5

Keywords

Navigation