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.
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.
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.
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.
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
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.
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.
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.
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
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.
Glendenning, R. (1933). A successful parasite introduction into British Columbia. Canadian Entomologist,65(8), 169–171.
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.
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.
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.
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
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
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
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
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
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.
Mihajlović, L., & Kozárzhevskaya, E. (1983). Effectivieness of entomophagous in reduction of noxious coccid population (Homoptera: Coccoidea). Plant Protection,64, 295–301.
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.
Mitić-Mužina, N. (1967). Parasites du puceron globuleux (Sphaerolecanium Prunastri Fonsc.) (Homoptera, Coccoidea). Protection Des Plantes,93/95, 183–187.
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.
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.
Santas, L. A. (1985). Parthenolecanium Corni Bouché an orchard scale pest producing honeydew foraged by bees in Greece. Entomologia Hellenica,3, 53–58.
Schmutterer, H. (1956). Zur Morphologie, Systematik Und Bionomie Der Physokermes-Arten an Fichte (Homopt. Cocc). Zeitschrift für Angewandte Entomologie,39, 445–466.
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
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.
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.
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
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
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
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.
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
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
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.
About this article
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
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12600-024-01139-5