Natural Enemies of the Pear Psylla, Cacopsylla pyri (Hemiptera: Psyllidae), and the Possibilities for Its Biological Control: A Case Study Review in the Western Balkan Countries
Abstract
:1. Introduction
2. Predators of the Pear Psylla
3. Specialist Predators
4. General Predators (Generalists)
- They are present in sufficient numbers in the agroecosystem;
- They have low intraguild predation;
- Alternative prey is scarce in the agroecosystem, and pest population growth is slow.
4.1. Spiders (Araneae)
4.2. Ants (Formicidae)
4.3. Ladybugs (Coccinellidae)
4.4. Mirid Bugs (Miridae)
4.5. Common Flower Bug (Anthocoris Nemorum)
4.6. Green Lacewings (Chrysopidae)
5. Parasitoids of the Pear Psylla
6. Alternative Biological Solutions for Controlling C. pyri
6.1. Entomopathogenic Fungi as Biological Agents for Controlling C. pyri
6.2. Kaolin as a Non-Chemical Alternative in Controlling C. pyri
6.3. Botanical Insecticides
7. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Tougeron, K.; Iltis, C.; Renoz, F.; Albittar, L.; Hance, T.; Demeter, S.; Le Goff, G.J. Ecology and biology of the parasitoid Trechnites insidiosus and its potential for biological control of pear psyllids. Pest Manag. Sci. 2021, 77, 4836–4847. [Google Scholar] [CrossRef] [PubMed]
- Faostat. Global Fruit Production in 2019, by Selected Variety. 2021. Available online: https://www.statista.com/statistics/264001/worldwide-production-of-fruit-by-variety (accessed on 15 December 2023).
- Monstat. Statistical Yearbook of Montenegro; Statistical Office: Podgorica, Montenegro, 2019.
- Veličković, M.M.; Golijan, J.M. Koncept integralne zaštite jabuke i kruške. J. Agric. Sci. Belgrade 2015, 60, 381–393. [Google Scholar] [CrossRef]
- Kulina, M.; Radović, M.; Berjan, S.; Kraišnik, V. Pomološke i hemijske osobine ploda nekih sorti krušaka gajenih u uslovima Bratunca. AГPOЗHAЊE 2013, 14, 357. [Google Scholar] [CrossRef]
- Tešanović, D.; Spasić, R.; Radović, R. Entomofauna of Pears in East Sarajevo Area (Bosnia and Herzegovina). In Proceedings of the VII International Scientific Agriculture Symposium “Agrosym 2016”, Jahorina, Bosnia and Herzegovina, 6–9 October 2016. [Google Scholar]
- Ebek, G. The Pomological Traits of Autochthonous Pear Varieties in the Area of North Montenegro. Turk. J. Agric. Eng. Res. 2019, 1, 141–151. [Google Scholar]
- Horton, D.R. Monitoring of Pear Psylla for Pest Management Decisions and Research. Integr. Pest Manag. Rev. 1999, 4, 1–20. [Google Scholar] [CrossRef]
- Injac, M.; Dulić, K.; Stamenov, M.; Vlaović, M.; Sudarević, B. Rezultati ogleda suzbijanja zimske i letnje forme kruškine buve (Psylla pyri L.). Zbornik radova Jugoslovenskog savetovanja o primeni pesticida. Opatija 1985, 7, 241–253. [Google Scholar]
- Grbić, M.; Lakić, B.; Mihajlović, L. Predators and parasitoids of Psylla pyri L. (Hom. Psyllidae) in Vojvodina (YU). In Proceedings of the OILB Workshop Lutte Integree en Verger de Poires, Changius (Rac), Switzerland, 28 June–1 July 1989; pp. 1–11. [Google Scholar]
- Seemüller, E.; Schneider, B. ‘Candidatus Phytoplasma mali’, ‘Candidatus Phytoplasma pyri’ and ‘Candidatus Phytoplasma prunorum’, the causal agents of apple proliferation, pear decline and European stone fruit yellows, respectively. Int. J. Syst. Evol. Microbiol. 2004, 54, 1217–1226. [Google Scholar] [CrossRef] [PubMed]
- Conci, C.; Rapisarda, C.; Tamanini, L. Annotated catalogue of the Italian Psylloidea. Second part (Insecta Homoptera). Atti Della Accad. Roveretana Degli Agiati 1996, 5B, 5–207. [Google Scholar]
- Tomaš, V.; Mihaljević, I.; Vuković, D.; Viljevac Vuletić, M.; Galić, V.; Tomeš, V.; Brus, K.; Zdunić, Z. Comparative effect of different insecticides and processed kaolin on Cacopsylla pyri L. population reduction. Poljoprivreda 2022, 28, 3–10. [Google Scholar] [CrossRef]
- Marčić, D.; Perić, P.; Prijović, M.; Ogurlić, I. Field and greenhouse evaluation of rapeseed spray oil against spider mites, green peach aphid and pear psylla in Serbia. Bull. Insectology 2009, 62, 159–167. [Google Scholar]
- Braham, M.; Pasqualini, E.; Ncira, N. Efficacy of kaolin, spinosad and malathion against Ceratitis capitata in Citrus orchards. Bull. Insectology 2007, 39–47. [Google Scholar]
- Sanchez, J.A.; Ortín-Angulo, M.C. Abundance and population dynamics of Cacopsylla pyri (Hemiptera: Psyllidae) and its potential natural enemies in pear orchards in southern Spain. Crop. Prot. 2012, 32, 24–29. [Google Scholar] [CrossRef]
- A Sanchez, J.; López-Gallego, E.; La-Spina, M. The impact of ant mutualistic and antagonistic interactions on the population dynamics of sap-sucking hemipterans in pear orchards. Pest Manag. Sci. 2019, 76, 1422–1434. [Google Scholar] [CrossRef]
- Gajski, D.; Pekár, S. Assessment of the biocontrol potential of natural enemies against psyllid populations in a pear tree orchard during spring. Pest Manag. Sci. 2021, 77, 2358–2366. [Google Scholar] [CrossRef] [PubMed]
- LE Goff, G.J.; Berthe, J.; Tougeron, K.; Dochy, B.; Lebbe, O.; Renoz, F.; Hance, T. Effect of the instar of the pear psyllid Cacopsylla pyri (Hemiptera: Psyllidae) on the behaviour and fitness of the parasitoid Trechnites insidiosus (Hymenoptera: Encyrtidae). Eur. J. Èntomol. 2021, 118, 279–287. [Google Scholar] [CrossRef]
- Booth, S.R. The Potential of Endemic Natural Enemies to Suppress Pear Psylla, Cacopsylla pyricola Förster, in the Hood River Valley, Oregon. Ph.D. Thesis, Oregon State University, Corvallis, OR, USA, 1992; 155p. [Google Scholar]
- Erler, F. Natural enemies of the pear psylla Cacopsylla pyri in treated vs. untreated pear orchards in Antalya, Turkey. Phytoparasitica 2004, 32, 295–304. [Google Scholar] [CrossRef]
- Jerinić-Prodanović, D.; Protić, L.; Mihajlović, L. Predatori i parazitoidi Cacopsylla pyri (L.) (Hemiptera: Psyllidae) u Srbiji. Pestic Fitomedicina 2010, 25, 29–42. [Google Scholar] [CrossRef]
- Jerinić-Prodanović, D.; Mihajlović, L.; Stojanović, A. Parasitoids of jumping plant-lice (Psylloidea, Hemiptera) from the family Encyrtidae (Hymenoptera, Chalcidoidea) in Serbia. Zootaxa 2019, 4577, 29–50. [Google Scholar] [CrossRef] [PubMed]
- Tomeš, V. Mogućnosti Suzbijanja Kruškine Buhe (Caccopsylla pyri L.) na Biološki Način. Master Thesis, Fakultet Agrobiotehničkih Znanosti Osijek, Osijek, Hrvatska, 2017. [Google Scholar]
- Horton, D.; Lewis, T.M.; Broers, D.A. Ecological and geographic range expansion of the introduced predator. Anthocoris nemoralis (Heteroptera: Anthocoridae) in North America: Potential for Nontarget Effects? Am. Entomol. 2004, 50, 18–30. [Google Scholar] [CrossRef]
- Guerrieri, E.; Noyes, J.S. A review of the European species of the genus Trechnites Thomson (Hymenoptera: Chalcidoidea: Encyrtidae), parasitoids of plant lice (Hemiptera: Psylloidea) with description of a new species. Syst. Entomol. 2009, 34, 252–259. [Google Scholar] [CrossRef]
- Riechert, S.E.; Lockley, T. Spiders as biological control agents. Annu. Rev. Entomol. 1984, 29, 299–320. [Google Scholar] [CrossRef]
- Symondson, W.O.C.; Sunderland, K.D.; Greenstone, M.H. Can generalist predators be effective biocontrol agents? Annu. Rev. Entomol. 2002, 47, 561–594. [Google Scholar] [CrossRef] [PubMed]
- Sigsgaard, L.; Esbjerg, P.; Philipsen, H. Controlling pear psylids by mass releasing Anthocoris nemoralis and A. nemorum (Heteroptera: Anthocoridae). J. Fruit Ornam. Plant Res. 2006, 14, 89–98. [Google Scholar]
- Sigsgaard, L. Habitat and prey preferences of the two predatory bugs Anthocoris nemorum (L.) and A. nemoralis (Fabricius) (Anthocoridae: Hemiptera-Heteroptera). Biol. Control 2010, 53, 46–54. [Google Scholar] [CrossRef]
- Jerinic-Prodanovic, D.; Protić, L. True bugs (Hemiptera, Heteroptera) as psyllid predators (Hemiptera, Psylloidea). ZooKeys 2013, 319, 169–189. [Google Scholar] [CrossRef] [PubMed]
- Pekár, S.; Michalko, R.; Loverre, P.; Líznarová, E.; Černecká, L. Biological control in winter: Novel evidence for the importance of generalist predators. J. Appl. Ecol. 2015, 52, 270–279. [Google Scholar] [CrossRef]
- Ciglar, I. Integrirana Zaštita Voćnjaka i Vinograda; Zrinski: Čakovec, Croatia, 1998; pp. 164–168. [Google Scholar]
- Bandžo, S.; (Institute of Agriculture, Skopje, North Macedonia). Personal communication, 2023.
- Stanic, D.; Spasić, R. Entomophagous Fauna—Predators of Pears in East Sarajevo Area (Bosnia and Herzegovina). In Proceedings of the IX International Scientific Agriculture Symposium “Agrosym 2018”, Jahorina, Bosnia and Herzegovina, 4–7 October 2018; pp. 1167–1170. [Google Scholar]
- Barić, B.; Pajač, I.; Bertić, D. Harmful and beneficial entomofauna in Croatian orchards and vineyards. Pestic. Benef. Org. IOBC/Wprs Bull. 2010, 55, 113–115. [Google Scholar]
- Beninato, S.; Morella, S. Control of Cacopsylla pyri with massive releases of Anthocoris nemoralis in pear orchards. Atti. Gior. Fitopatolog. 2000, 1, 367–372. [Google Scholar]
- Warner, G. Anthocorid bugs. In Orchard Pest Management Online; Washington State University: Washington, DC, USA, 1993. [Google Scholar]
- Scutareanu, P.; Lingeman, R.; Drukker, B.; Sabelis, M.W. Cross-correlation analysis of fluctuations in local populations of pear psyllids and anthocorid bugs. Ecol. Èntomol. 1999, 24, 354–363. [Google Scholar] [CrossRef]
- Shaltiel, L.; Coll, M. Reduction of Pear Psylla Damage by the Predatory Bug Anthocoris nemoralis (Heteroptera: Anthocoridae): The Importance of Orchard Colonization Time and Neighboring Vegetation. Biocontrol Sci. Technol. 2004, 14, 811–821. [Google Scholar] [CrossRef]
- Sigsgaard, L. Oviposition preference of Anthocoris nemorum and Anthocoris nemoralis for apple and pear. Entomol. Exp. Et Appl. 2004, 111, 215–223. [Google Scholar] [CrossRef]
- Sigsgaard, L. Oviposition preference of Anthocoris nemoralis and A. nemorum (Heteroptera: Anthocoridae) on pear leaves affected by leaf damage, honeydew and prey. Biocontrol Sci. Technol. 2005, 15, 139–151. [Google Scholar] [CrossRef]
- Civolani, S. The Past and Present of Pear Protection Against the Pear Psylla, Cacopsylla pyri L. In Insecticides—Pest Engineering; IntechOpen: London, UK, 2012. [Google Scholar] [CrossRef]
- Parker, N.J.B. A method for mass rearing the aphid predator Anthocoris nemorum. Ann. Appl. Biol. 1981, 99, 217–223. [Google Scholar] [CrossRef]
- Souliotis, C.; Moschos, T. Effectiveness of some pesticides against Cacopsylla pyri and impact on its predator Anthocoris nemoralis in pear orchards. Bull. Insectology 2008, 61, 25–30. [Google Scholar]
- Kocourek, F.; Holý, K.; Řezáč, M.; Sopko, B.; Stará, J. The effects of various pest control regimes on the community structure and population dynamics of selected natural enemies of Cacopsylla pyri in pear orchards. Biocontrol Sci. Technol. 2021, 31, 632–651. [Google Scholar] [CrossRef]
- Daniel, C.; Pfammatter, W.; Kehrli, P.; Wyss, E. Processed kaolin as an alternative insecticide against the European pear sucker, Cacopsylla pyri (L.). J. Appl. Èntomol. 2005, 129, 363–367. [Google Scholar] [CrossRef]
- EPPO Standard PM 6/3 (5); Biological Control Agents Safely Used in the EPPO Region. European and Mediterranean Plant Protection Organization: Paris, France, 2023.
- Petráková, L.; Michalko, R.; Loverre, P.; Sentenská, L.; Korenko, S.; Pekár, S. Intraguild predation among spiders and their effect on the pear psylla during winter. Agric. Ecosyst. Environ. 2016, 233, 67–74. [Google Scholar] [CrossRef]
- Birkhofer, K.; Gavish-Regev, E.; Endlweber, K.; Lubin, Y.; von Berg, K.; Wise, D.; Scheu, S. Cursorial spiders retard initial aphid population growth at low densities in winter wheat. Bull. Èntomol. Res. 2008, 98, 249–255. [Google Scholar] [CrossRef] [PubMed]
- de Pedro, L.; Ortín-Angulo, M.C.; Miñano, J.; López-Gallego, E.; Sanchez, J.A. Structure of the Assemblages of Spiders in Mediterranean Pear Orchards and the Effect of Intensity of Spraying. Insects 2020, 11, 553. [Google Scholar] [CrossRef] [PubMed]
- Dudić, B.D.; Tomić, V.T.; Sivčev, I.; Buchs, W.; Sivčev, l.; Graora, D.; Gotlin-Čuljak, T. New data on spider fauna from northern Serbia. Arch. Biol. Sci. 2013, 65, 1669–1673. [Google Scholar] [CrossRef]
- Grbić, G.; Hänggi, A.; Krnjajić, S. Spiders (Araneae) of Subotica Sandland (Serbia): Additional arguments in environmental protection. Acta Zool. Acad. Sci. Hung. 2021, 67, 15–61. [Google Scholar] [CrossRef]
- Ripka, G. New data to the knowledge on the Phytoseiid fauna in Hungary (Acari: Mesostigmata). Acta Phytopathol. Et Entomol. Hungarica 1998, 33, 395–405. [Google Scholar]
- Franin, K.; Kuštera, G.; Šišeta, F. Fauna of ground-dwelling arthropods in vineyards of Zadar County (Croatia). Poljoprivreda 2016, 22, 50–56. [Google Scholar] [CrossRef]
- Pajač-Živković, I.; Lemić, D.; Samu, F.; Kos, T.; Barić, B. Spider communities affected by exclusion nets. Appl. Ecol. Environ. Res. 2019, 17, 879–887. [Google Scholar] [CrossRef]
- Loverre, P.; Pekár, S. Functional response of Philodromus (Araneae: Philodromidae) at low temperatures. In Proceedings of the 27th European Congress of Arachnology, Ljubljana, Slovenia, 2–7 September 2012. [Google Scholar] [CrossRef]
- Michálek, O.; Gajski, D.; Pekár, S. Winter activity of Clubiona spiders and their potential for pest control. J. Therm. Biol. 2022, 108, 103295. [Google Scholar] [CrossRef] [PubMed]
- Michalko, R.; Petráková, L.; Sentenská, L.; Pekár, S. The effect of increased habitat complexity and density-dependent non-consumptive interference on pest suppression by winter-active spiders. Agric. Ecosyst. Environ. 2017, 242, 26–33. [Google Scholar] [CrossRef]
- Grbac, I.; Katušić, L.; Lukić, M. Catalogue of spiders (Araneae) deposited in the Croatian Natural History Museum. Nat. Croat. 2019, 28, 185–269. [Google Scholar] [CrossRef]
- Paulson, G.S.; Akre, R.D. Evaluating the Effectiveness of Ants as Biological Control Agents of Pear Phyla (Homoptera: Psyllidae). J. Econ. Èntomol. 1992, 85, 70–73. [Google Scholar] [CrossRef]
- Sanchez, J.A.; Carrasco-Ortiz, A.; López-Gallego, E.; Ramírez-Soria, M.J.; La Spina, M.; Ortín-Angulo, M.C.; Ibáñez-Martínez, H. Ants (Hymenoptera: Formicidae) Reduce the Density of Cacopsylla pyri (Linnaeus, 1761) in Mediterranean Pear Orchards. Myrmecol. News 2020, 30, 93–102. [Google Scholar]
- Pringle, E.G. Ant-Hemiptera Associations. In Encyclopedia of Social Insects; Starr, C.K., Ed.; Springer: Cham, Switzerland, 2021. [Google Scholar] [CrossRef]
- Schläppi, D.; Kettler, N.; Straub, L. Long-term effects of neonicotinoid insecticides on ants. Commun. Biol. 2020, 3, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Franin, K.; Barić, B. Korisne stjenice (Heteroptera) u poljoprivredi. Entomol. Croat. 2012, 16, 61–80. [Google Scholar]
- Pajač, I.; Barić, B.; Milošević, B. Katalog stjenica (Heteroptera: Miridae) Hrvatske. Entomol. Croat. 2010, 14, 23–76. [Google Scholar]
- Warner, G.P. Predatory bugs. In Orchard Pest Management: A Resource Book for the Pacific Northwest; Beers, E.H., Brunner, J.F., Willett, M.J., Warner, G.M., Eds.; Good Fruit Grower: Yakima, WA, USA, 1993; pp. 218–222. [Google Scholar]
- Herard, F. Annotated list of the entomophagous complex associated with pear psylla, Psylla pyri (L.) (Hom. Psyllidae) in France. Agronomie 1986, 6, 1–34. [Google Scholar] [CrossRef]
- Ciglar, I.; Barić, B. Dinamika populacije lisnih uši i njihovih predatora u različitim programima zaštite. Agron. Glas. 2001, 63, 23–30. [Google Scholar]
- Armand, E.; Lyoussoufi, A.; D’arcier, F.F.; Rieux, R. Interrelations entre les populations du psylle du poirier Psylla pyri (L.) (Hom., Psyllidae) et le complexe de ses parasitoïdes dans un verger traité du sud-est de la France. J. Appl. Entomol. 1990, 110, 242–252. [Google Scholar] [CrossRef]
- Armand, E.; Lyoussouf, A.; Rieux, R. Évolution du complexe parasitaire des psylles du poirier Psylla pyri et Psylla pyrisuga (Homoptera: Psyllidae). Entomophaga 1991, 36, 287–294. [Google Scholar] [CrossRef]
- Herard, F. Analysis of parasite and predator populations observed in pear orchards infested by Psylla pyri (L.) (Hom.: Psyllidae) in France. Agronomie 1985, 5, 773–778. [Google Scholar] [CrossRef]
- Bufaur, M.; Harizanova, V.; Stoeva, A. Parasitoids of the pear sucker Cacopsylla pyri L. (Psyllidae) in Bulgaria—Morphology and biology. In Traditions and Challenges of Agricultural Education, Science and Business; Scientific Works of the Agricultural University of Plovdiv: Plovdiv, Bulgaria, 2010; Volume 55, Book 2; pp. 71–76. [Google Scholar]
- Mcmullen, R.D. New Records of chalcidoid parasites and hyperparasites of Psylla pyricola Förster in British Columbia. Can. Entomol. 1966, 98, 236–239. [Google Scholar] [CrossRef]
- Burts, E.C. Effectiveness of a Soft-Pesticide Program on Pear Pests. J. Econ. Èntomol. 1983, 76, 936–941. [Google Scholar] [CrossRef]
- Lacey, L.; Arthurs, S.; Horton, D.; Miliczky, G. Spinosad and Granulovirus Effects on Codling Moth. Final Projekt Report; USDA-ARS, Yakima Agricultural Research Laboratory: Wapato, WA, USA, 2005; 9p. [Google Scholar]
- Bartlett, B.R.; Clausen, C.P.; Debach, P.; Goeden, R.D.; Legner, E.F.; Mcmurtry, J.A.; Oatman, E.R.; Bay, E.C.; Rosen, D. Introduced Parasites and Predators of Arthropod Pests and Weeds: A World Review; Agriculture Handbook No. 480; UDSA: Washington, DC, USA, 1978; 551p.
- Dupont, T.S.; Strohm, C.J. Integrated pest management programmes increase natural enemies of pear psylla in Central Washington pear orchards. J. Appl. Entomol. 2020, 144, 109–122. [Google Scholar] [CrossRef]
- Jaworska, K.; Olszak, R.W.; Zajac, R.Z. Parasitization rate on the larvae of pear (Cacopsylla pyri) in orchards with differing intensity of chemical control. Acta Horticult. 1996, 422, 334–335. [Google Scholar] [CrossRef]
- Oudeh, B.; Kassis, W.; Abu-Tara, R. Seasonal Activity of the Predator, Anthocoris nemoralis (F.) and the Parasitoid, Trechnites psyllae (R.) against the Pear Psylla Cacopsylla pyricola (F.) (Hemiptera: Psyllidae). Egypt J. Biol. Control. 2013, 23, 17–23. [Google Scholar]
- Unruh, T.R.; Westigard, P.H.; Hagen, K.S. Pear psylla. In Biological Control in the Western United States; Nechols, J.R., Ed.; DNR Publ. 3361; University of California: Oakland, CA, USA, 1994; pp. 95–100. [Google Scholar]
- Stouthamer, R.; Hu, J.; van Kan, F.J.; Platner, G.R.; Pinto, J.D. The utility of internally transcribed spacer 2 DNA sequences of the nuclear ribosomal gene for distinguishing sibling species of Trichogramma. BioControl 1999, 43, 421–440. [Google Scholar] [CrossRef]
- Ivezić, A.; Stouthamer, R.; Rugman-Jones, P.; Ignjatovic-Ćupina, A. Molecular identification of Trichogramma egg parasitoids of Ostrinia nubilalis in the north eastern Serbia. Arch. Biol. Sci. 2018, 70, 425–432. [Google Scholar] [CrossRef]
- Pavićević, B. Morfologija i biologija vrsta roda Psylla (Psyllidae, Homoptera) na kruškama u Srbiji. In Doktorska Disertacija; Univerzitet u Beogradu, Poljoprivredni Fakultet: Belgrade, Serbia, 1977. [Google Scholar]
- Ferriere, C. Encyrtides paleartiques parasites de psylles. Entomophaga 1961, 6, 39–51. [Google Scholar] [CrossRef]
- Global Biodiversity Information Facility (GBIF). Available online: https://www.gbif.org/species/1373550 (accessed on 10 February 2024).
- Noyes, J.S.; Hanson, P. Encyrtidae (Hymenoptera, Chalcidoidea) of Costa Rica: The genera and species with jumping plant lice (Homoptera: Psylloidea). Bull. Br. Mus. Entomol. 1996, 65, 105–164. [Google Scholar]
- Hrnčić, S. (Biotechnical Faculty, University of Montenegro, Podgorica, Montenegro). Personal communication, 2023. [Google Scholar]
- Delvare, G. Cycle biologique et reproduction de Prionomitus mitratus Dalman, un important parasite des psylles du Poirier (Psylla pyri L.; Psylla pyrisuga Förster) et de L’aubepine (Psylla melanoneura Förster, Psylla crataegi Shrank). IOBC/WPRS Bull. 1984, 7, 184–190. [Google Scholar]
- Laborda, R.; Galán-Blesa, J.; Sánchez-Domingo, A.; Xamaní, P.; Estruch, V.D.; Selfa, J.; Guerrieri, E.; Rodrigo, E. Preliminary study on the biology, natural enemies and chemical control of the invasive Macrohomotoma gladiata (Kuwayama) on urban Ficus microcarpa L. trees in Valencia (SE Spain). Urban For. Urban Green. 2015, 14, 123–128. [Google Scholar] [CrossRef]
- Franz, J.M. Influence of environment and modern trends in crop management on microbial control. In Microbial Control of Insects and Mites; Burges, H.D., Hussey, N.W., Eds.; Academic Press: New York, NY, USA, 1971; pp. 407–445. [Google Scholar]
- Puterka, G.J. Fungal pathogens for arthropod pest control in orchard systems: Mycoinsecticidal approach for pear psylla control. BioControl 1999, 44, 183–209. [Google Scholar] [CrossRef]
- Majchrowicz, I.; Poprawski, T.J. Effects in vitro of nine fungicides on growth of entomopathogenic fungi. Biocont. Sci. Tech. 1993, 3, 321–336. [Google Scholar] [CrossRef]
- Forić, N.; Sarajlić, A.; Vrandečić, K.; Majić, I. Potencijal entomopatogenih gljiva Metarhizium spp. u suzbijanju štetnih kukaca. Glas. Zaštite Bilja 2018, 41, 22–30. [Google Scholar] [CrossRef]
- Santos, A.C.d.S.; Diniz, A.G.; Tiago, P.V.; de Oliveira, N.T. Entomopathogenic Fusarium species: A review of their potential for the biological control of insects, implications and prospects. Fungal Biol. Rev. 2019, 34, 41–57. [Google Scholar] [CrossRef]
- Grgić, S.; Ćosić, J.; Sarajlić, A. Entomopatogene gljive roda Fusarium: Potencijal u biološkoj kontroli kukaca. Poljoprivreda 2022, 28, 51–57. [Google Scholar] [CrossRef]
- Humber, R.A. Entomophthoromycota: A New Overview of Some of the Oldest Terrestrial Fungi. In Biology of Microfungi. Fungal Biology; Li, D.W., Ed.; Springer: Berlin/Heidelberg, Germany, 2016. [Google Scholar]
- Keller, S. Arthropod-pathogenic Entomophthorales: Biology, Ecology, Identification. COST Action 2007, 842, 155. [Google Scholar]
- Gryganskyi, A.; Humber, R.; Smith, M.; Hodge, K.; Huang, B. Phylogenetic lineages in Entomophthoromycota. Persoonia 2013, 30, 94–105. [Google Scholar] [CrossRef] [PubMed]
- Barta, M.; Cagáň, L. Observations on the Occurrence of Entomophthorales Infecting Aphids (Aphidoidea) in Slovakia. BioControl 2006, 51, 795–808. [Google Scholar] [CrossRef]
- Muskat, L.C.; Görg, L.M.; Humbert, P.; Gross, J.; Eilenberg, J.; Patel, A.V. Encapsulation of the psyllid-pathogenic fungus Pandora sp. nov. inedit. and experimental infection of target insects. Pest Manag. Sci. 2021, 78, 991–999. [Google Scholar] [CrossRef] [PubMed]
- Eilenberg, J.; Keller, S.; Humber, R.A.; Jensen, A.H.; Jensen, A.B.; Görg, L.M.; Muskat, L.C.; Kais, B.; Gross, J.; Patel, A.V. Pandora cacopsyllae Eilenberg, Keller & Humber (Entomophthorales: Entomophthoraceae), a new species infecting pear psyllid Cacopsylla pyri L. (Hemiptera: Psyllidae). J. Invertebr. Pathol. 2023, 200, 107954. [Google Scholar] [CrossRef] [PubMed]
- Chen, C.; Ye, S.; Wang, D.; Hatting, J.L.; Yu, X. Alginate embedding and subsequent sporulation of in vitro-produced Conidiobolus thromboides hyphae using a pressurised air-extrusion method. Biol. Control. 2014, 69, 52–58. [Google Scholar] [CrossRef]
- Przyklenk, M.; Vemmer, M.; Hanitzsch, M.; Patel, A. A bioencapsulation and drying method increases shelf life and efficacy of Metarhizium brunneum conidia. J. Microencapsul. 2017, 34, 498–512. [Google Scholar] [CrossRef]
- Ramírez-Godoy, A.; Puentes-Peréz, G.; Restrepo-Díaz, H. Evaluation of the effect of foliar application of kaolin clay and calcium carbonate on populations of Diaphorina citri (Hemiptera: Liviidae) in Tahiti lime. Crop. Prot. 2018, 109, 62–71. [Google Scholar] [CrossRef]
- Soldo, T.; Duralija, B.; Benčić, Đ.; Mešić, A. Upotreba kaolinske gline u uzgoju voća. Glas. Zaštite Bilja 2022, 45, 70–76. [Google Scholar] [CrossRef]
- Pasqualini, E.; Civolani, S.; Corelli-Grappadelli, L. Particle film technology; approach for a biorational control of Cacopsylla pyri (Rynchota: Psyllidae) in Northern Italy. Bull. Insectology 2007, 55, 39–42. [Google Scholar]
- Gajger, I.T.; Dar, S.A. Plant Allelochemicals. Insects 2021, 12, 189. [Google Scholar] [CrossRef] [PubMed]
- Iqbal, T.; Ahmed, N.; Shahjeer, K.; Ahmed, S.; Al-Mutairi, K.A.; Khater, H.F.; Ali, R.F. Botanical Insecticides and Their Potential as Anti-Insect/Pests: Are They Successful against Insects and Pests? In Global Decline of Insects; IntechOpen: London, UK, 2021. [Google Scholar] [CrossRef]
- Erler, F.; Yegen, O.; Zeller, W. Field Evaluation of a Botanical Natural Product Against the Pear Psylla (Homoptera: Psyllidae). J. Econ. Entomol. 2007, 100, 66–71. [Google Scholar] [CrossRef] [PubMed]
- Barman, J.C.; Zeng, X. Effect of Guava Leaf Extract on Citrus Attractiveness to Asian Citrus Psyllid, Diaphorina citri Kuwayama. Pak. J. Zool. 2014, 46, 1117–1124. [Google Scholar]
- Sarajlić, A.; Majić, I.; Raspudić, E.; Baličević, R.; Ravlić, M. Učinkovitost suzbijanja stjenica Nezara viridula i Halyomorpha halys vodenim ekstraktom ambrozije. Entomol. Croat. 2022, 21, 17–24. [Google Scholar] [CrossRef]
- Flores-Dávila, M.; González-Villegas, R.; Guerrero-Rodríguez, E.; Mendoza-Villarreal, R.; Cárdenas-Elizondo, A.; Cerna-Chavez, E.; Aguirre-Uribe, L. Insecticidal Effect of Plant Extracts on Bactericera cockerelli (Hemiptera: Psyllidae) Nymphs. Southwest. Èntomol. 2011, 36, 137–144. [Google Scholar] [CrossRef]
- Granados-Echegoyen, C.; Pérez-Pacheco, R.; Bautista-Martínez, N.; Alonso-Hernández, N.; Sánchez-García, J.A.; Martinez-Tomas, S.H.; Sánchez-Mendoza, S. Insecticidal Effect of Botanical Extracts on Developmental Stages of Bactericera cockerelli (Sulc) (Hemiptera: Triozidae). Southwest. Èntomol. 2015, 40, 97–110. [Google Scholar] [CrossRef]
- Sharma, S.K.; Sharma, P.C. Laboratory Evaluation of Local Plant Extracts and an Organophosphate Insecticide against Seabuckthorn Psyllid. Chem. Sci. Rev. Lett. 2017, 6, 947–955. [Google Scholar]
- Ivezić, A.; Rugman-Jones, P.; Malausa, T.; Ris, N.; Ignjatović-Ćupina, A. Molecular identification of Trichogramma species parasitizing Ostrinia nubilalis in corn and pepper in south–east border of Europe. Int. J. Pest Manag. 2020, 67, 346–357. [Google Scholar] [CrossRef]
- Ivezić, A.; Rugman-Jones, P.F.; Trudić, B. Rapid molecular identification of Trichogramma (Hymenoptera: Trichogrammatidae) parasitizing the eggs of the European corn borer, Ostrinia nubilalis (Lepidoptera: Crambidae) in Serbia. Egypt. J. Biol. Pest Control. 2021, 31, 74. [Google Scholar] [CrossRef]
Project Name/Acronym | Keywords | Start Date/End Date | EU Contribution in Euros Per Project | Source |
---|---|---|---|---|
HORIZON2020 projects | ||||
Stepping-up IPM decision support for crop protection/IPM Decisions | IPM, crop protection, pest management, DSS, computer and information science, agro-meteorological network | 1 June 2019–31 May 2024 | 4,998,096.19 | https://cordis.europa.eu/project/id/817617 (accessed on 1 February 2024) |
An EU-wide farm network demonstrating and promoting cost-effective IPM strategies/IPMworks | Agroecology, advisors, pesticides, holistic, sustainability, farmers, peer-to-peer | 1 October 2020–30 September 2024 | 6,000,005.00 | https://cordis.europa.eu/project/id/101000339 (accessed on 1 February 2024) |
EcoStack | Biocontrol agents, barcoding, plant defence priming, sustainability, interaction | 10 September 2020–9 March 2024 | 9,963,866.00 | https://cordis.europa.eu/project/id/773554 (accessed on 1 February 2024) |
Optimised Pest Integrated Management to precisely detect and control plant diseases in perennial crops and open-field vegetables/OPTIMA | IPM DSS, prediction models, early diseases detection, smart precision spraying technologies | 1 August 2018–30 June 2022 | 3,425,600.00 | https://cordis.europa.eu/project/id/773718 (accessed on 1 February 2024) |
Agri and food waste valorisation co-ops based on flexible multi-feedstocks biorefinery processing technologies for new high added value applications/AgriMax | Agriculture, pilot plant, food, packaging, multi-feedstock biorefinery, agricultural and food processing waste valorization | 1 October 2016–30 September 2021 | 12,484,461.46 | https://cordis.europa.eu/project/id/720719 (accessed on 1 February 2024) |
Trapview—Automated pest-monitoring system for sustainable growing with optimal insecticide use/Trapview | Sustainable agriculture, resource-efficient eco-innovations in agriculture, automated pest insect monitoring, insecticide spraying optimization, statistical forecasting models | 1 September 2016–31 September 2018 | 1,141,350.00 | https://cordis.europa.eu/project/id/733979 (accessed on 1 February 2024) |
Coordinated Integrated Pest Management in Europe/C-IPM | IPM, pesticides, sustainability, plant protection, agriculture | 1 December 2014–31 December 2016 | 1,998,215.00 | https://cordis.europa.eu/project/id/618110 (accessed on 1 February 2024) |
Innovative biological products for soil pest control/INBIOSOIL | Pesticide reduce, agriculture, biocontrol agents, sustainability | 1 July 2012–31 December 2015 | 4,984,654.20 | https://cordis.europa.eu/project/id/282767/it (accessed on 1 February 2024) |
Cost Action projects | ||||
CA21134—Towards zer0 Pesticide AGRIculture: European Network for sustainability (T0P-AGRI-Network) | chemical pesticides, agroecology, sustainable agriculture, crop protection, transition | 19 September 2022–18 September 2026 | n.a. | https://www.cost.eu/actions/CA21134 (accessed on 25 January 2024) |
FA1405—Using three-way interactions between plants, microbes and arthropods to enhance crop protection and production | Plant–arthropod–microorganism interactions, pest and disease management, plant growth and defence promoting microorganism, plant production | 10 March 2015–9 March 2019 | n.a. | https://www.cost.eu/actions/FA1405 (accessed on 25 January 2024) |
FA1104—Sustainable production of high-quality cherries for the European market | sweet and sour cherry, rootstocks, climate change, sustainable agriculture | 16 April 2012–15 April 2016 | n.a. | https://www.cost.eu/actions/FA1104 (accessed on 25 January 2024) |
849—Parasitic Plant Management in Sustainable Agriculture | Agriculture, biocontrol, parasitic plants | 22 March 2001–21 September 2006 | n.a. | https://www.cost.eu/actions/849 (accessed on 25 January 2024) |
Problems | Solutions |
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P.1.1. Lack of inventory of the predators/parasitoid complex of C. pyri in most Western Balkan countries, resulting in P.1.2. a lack of (any) recent data on the diversity of pear psylla predators/parasitoids. | S.1.1. Conducting detailed field research to inventory the predators/parasitoid complex of C. pyri in Western Balkan countries. S.1.2. Also, supporting and encouraging research projects focused on this topic will result in new data on the biodiversity of pear psylla predators/parasitoids. S.1.3. Determining the precise taxonomic affiliation and population genetic diversity of C. pyri and its natural enemies in Western Balkan countries using available molecular and biochemical markers. |
P.2.1. A thorough understanding of all relevant ecological factors at the level of each agroecosystem/landscape is necessary for the successful application of biological control of the common pear psylla on pears in Western Balkan countries, which involves an analysis of climate, geographical characteristics, the presence of other insects or predators, as well as the impact of agricultural practices on the diversity of this pest insect. | S.2.1. Conducting detailed research that would cover all ecological factors specific to each agroecosystem/landscape where pears are grown (domesticated or wild types) in Western Balkan countries. S.2.2. Integrating these studies into interdisciplinary collaborative regional and cross-border projects, including EU HORIZON2020 and COST Action programmes, among others. S.2.3. Integrating proven practices that benefit the survival and development of pear psylla natural enemies (i.e., planting Rhamnus and Laurus trees around pear orchards and maintaining grass vegetation, which both attract A. nemoralis, or installing cardboard belts on pear tree trunks and branches in order to enhance the overwintering of spiders). |
P.3.1. Insufficient information on the presence of biodiversity among the natural enemies of C. pyri and the degree of predation and parasitism for each of them. | S.3.1. A more detailed inventory of all significant biological enemies of C. pyri within the entire WB region, including climate data modelling and species distribution predictions. S.3.2. Determining the degree of predation and parasitism for each species to understand the available biological potential and to set a basis for further research and application actions. |
P.4.1. Lack of research involving experimental application of commercial predators/parasitoids, i.e., laboratory-bred individuals, to evaluate their effectiveness and field performance in controlling the common pear psylla. | S.4.1. Piloting local biocontrol experiments over C. pyri using drones and other available robotic technologies through the aforementioned cross-border research initiatives. S.4.2. Developing a study on the economic cost–benefit analysis of using the aforementioned biocontrol technologies in regular agricultural practice compared to other available chemical and non-chemical treatments. |
P.5.1. EU candidate and non-candidate countries of Western Balkans (Albania, Bosnia and Herzegovina, Kosovo *, Montenegro, North Macedonia, Serbia) national agricultural policies are still not aligned enough and effectively with relevant EU Acquis Communautaire and negotiation chapters’ recommendations (chapter 11). Some of the examples of poor agricultural rule of law in the mentioned countries that need to be changed and intervened upon are corrupted government structures and decision makers, a lack of political will for EU-based reforms in the area of agriculture, unreformed national policies regulating local realities that damage the environment and IPM, etc. | S.5.1. Relevant stakeholders involved in the negotiation process need to be more involved and advocate intensively for the successful implementation of chapters’ recommendations and closing them. Structural dialogue among decision makers and relevant stakeholders from the agricultural sector needs to be intensified. |
P.6.1. The capacity of relevant subjects in the agricultural sector in the above-mentioned countries is poor in terms of applying for adequate funds that support agricultural research and development. P.6.2. The countries of the Western Balkans and their responsible government offices, agencies, and ministries for the agricultural sector do not recognise nor involve IPM measures and biocontrol in relevant national strategies and action plans; therefore, funding of the same is intensively lacking. P.6.3. Taking into account that IMP and biocontrol measures alike are weakly supported and implemented in the above-mentioned WB countries, their contribution to achieving sustainable development goals of the UN (SDGs), especially 2, 12, 13, 15, and 17, is also weak and invisible. | S.6.1. Relevant country government offices and ministries for international cooperation, EU accession, and agricultural questions need to intensify capacity building of relevant subjects for applying to projects at EU programmatic schemes. S.6.2. Biocontrol practitioners need to advocate intensively to decision makers on the benefits of the usage of IPM regulatory practices and biocontrol. S.6.3. An SDG achievement study with which IPM and biocontrol in agriculture are contributing (so far) and an assessment of their potential needs to be conducted. From this, a clearer picture of IPM presence in the agricultural sector in WB countries will be visible, and, therefore, action plans for achieving the mentioned SDGs could be set. |
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Krndija, J.; Ivezić, A.; Sarajlić, A.; Barošević, T.; Kuzmanović, B.; Petrović, K.; Stojačić, I.; Trudić, B. Natural Enemies of the Pear Psylla, Cacopsylla pyri (Hemiptera: Psyllidae), and the Possibilities for Its Biological Control: A Case Study Review in the Western Balkan Countries. Agronomy 2024, 14, 668. https://doi.org/10.3390/agronomy14040668
Krndija J, Ivezić A, Sarajlić A, Barošević T, Kuzmanović B, Petrović K, Stojačić I, Trudić B. Natural Enemies of the Pear Psylla, Cacopsylla pyri (Hemiptera: Psyllidae), and the Possibilities for Its Biological Control: A Case Study Review in the Western Balkan Countries. Agronomy. 2024; 14(4):668. https://doi.org/10.3390/agronomy14040668
Chicago/Turabian StyleKrndija, Jovan, Aleksandar Ivezić, Ankica Sarajlić, Tijana Barošević, Boris Kuzmanović, Kristina Petrović, Isidora Stojačić, and Branislav Trudić. 2024. "Natural Enemies of the Pear Psylla, Cacopsylla pyri (Hemiptera: Psyllidae), and the Possibilities for Its Biological Control: A Case Study Review in the Western Balkan Countries" Agronomy 14, no. 4: 668. https://doi.org/10.3390/agronomy14040668
APA StyleKrndija, J., Ivezić, A., Sarajlić, A., Barošević, T., Kuzmanović, B., Petrović, K., Stojačić, I., & Trudić, B. (2024). Natural Enemies of the Pear Psylla, Cacopsylla pyri (Hemiptera: Psyllidae), and the Possibilities for Its Biological Control: A Case Study Review in the Western Balkan Countries. Agronomy, 14(4), 668. https://doi.org/10.3390/agronomy14040668