Hymenoptera Complex Associated with Myzus persicae and Hyalopterus spp. in Peach Orchards in Northeastern Spain and Prospects for Biological Control of Aphids
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
AGL2013-49164-C2-2-R and AGL2016-77373-C2-1-R
Ministerio de Ciencia e Innovación
.
CERCA Programme / Generalitat de Catalunya
PhD grant to YA
Consejo Nacional de Ciencia y Tecnología
Research Schoolarship to Y.A.
"la Caixa" Foundation
III43001
Ministarstvo Prosvete, Nauke i Tehnološkog Razvoja
PubMed
30995749
PubMed Central
PMC6523163
DOI
10.3390/insects10040109
PII: insects10040109
Knihovny.cz E-zdroje
- Klíčová slova
- Aphididae, Aphidiinae, IPM, conservation, hyperparasitoids,
- Publikační typ
- časopisecké články MeSH
Aphids are a serious pest for peach crops. They have traditionally been managed with insecticides, but there is increasing concern about the risk that insecticides pose to both humans and the environment. As a first step to use biological control in aphid management, we conducted a 3-year field survey in northeastern Spain to determine which parasitoids and hyperparasitoids were most prevalent on two aphids, Myzus persicae (Sulzer) and Hyalopterus spp. Koch, the most harmful to peach trees. We collected 11 parasitoid species from M. persicae, with Aphidius matricariae (Haliday) being the most abundant. Two parasitoid species were also collected from Hyalopterus spp., Aphidius transcaspicus Telenga and Praon volucre (Haliday). Hyperparasitoid species overlapped between these aphids but their relative abundances differed. We also discuss the possible impacts of hyperparasitoids on parasitoid populations. Our results suggest that it would be feasible to implement biocontrol methods for aphids in integrated pest management programmes in peach orchards. There are a number of primary parasitoid species associated with these aphids, and the nearby crops and wild vegetation in the vicinity and within the orchards may provide a suitable habitat for them. Additionally, some of them are commercially available and might be usable in augmentative releases.
Institut de Recerca i Tecnologia Agroalimentàries Ctra de Cabrils Km 2 08348 Cabrils Barcelona Spain
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Food and Agriculture Organization Statistics (FAOSTAT): Crops. [(accessed on 12 January 2019)];2017 Available online: http://www.fao.org/faostat/en/#data/QC.
Ministerio de Agricultura, Pesca y Alimentación (MAPA) [(accessed on 2 March 2019)];2017 Available online: https://www.mapa.gob.es/es/estadistica/temas/estadisticas-agrarias/agricultura/superficies-producciones-anuales-cultivos/
Alhmedi A., Raymaekers S., Tomanović Ž., Bylemans D., Belien T. Food web structure of aphids and their parasitoids in Belgian fruit agroecosystems. Entomol. Sci. 2018;21:279–291. doi: 10.1111/ens.12303. DOI
Kavallieratos N.G., Tomanović Ž., Starý P., Bogdanović-Mitrovski A. Parasitoids (Hymenoptera: Braconidae: Aphidiinae) attacking aphids feeding on Prunoideae and Maloideae crops in Southeast Europe: Aphidiine-aphid-plant associations and key. Zootaxa. 2008;1793:47–64. doi: 10.5281/zenodo.182566. DOI
Basky Z. Predators and parasites of Hyalopterus pruni and Hyalopterus amygdali populations living on peach, plum and reed. Acta Phytopathol. Acad. Sci. Hung. 1982;17:311–316.
Blackman R.L., Eastop V.F. Aphids on the World’s Crops. 2nd ed. John Wiley & Sons; Chichester, UK: 2000.
Dedryver C.A., Le Ralec A., Fabre F. The conflicting relationships between aphids and men: A review of aphid damage and control strategies. C. R. Biol. 2010;333:539–553. doi: 10.1016/j.crvi.2010.03.009. PubMed DOI
Barbagallo S., Cocuzza G.E.M., Cravedi P., Komazaki S. IPM case studies: Deciduous fruit trees aphids. In: Emden H.F., van Harrington R., editors. Aphids as Crop Pests. 2nd ed. CABI; Wallingford, UK: 2017. pp. 632–642.
Isac M., Preda S., Marcu M. Aphid species—Vectors of plum pox virus. Acta Virol. 1998;42:233–234. PubMed
Penvern S., Bellon S., Fauriel J., Sauphanor B. Peach orchard protection strategies and aphid communities: Towards an integrated agroecosystem approach. Crop Prot. 2010;29:1148–1156. doi: 10.1016/j.cropro.2010.06.010. DOI
Foster S.P., Denholm I., Harling Z.K., Moores G.D. Intensification of insecticide resistance in UK field populations of the peach-potato aphid, Myzus persicae (Hemiptera: Aphididae) in 1996. Bull. Entomol. Res. 1998;88:127–130. doi: 10.1017/S0007485300025694. DOI
Slater R., Paul V.L., Andrews M., Garbay M., Camblin P. Identifying the presence of neonicotinoid-resistant peach-potato aphid (Myzus persicae) in the peach-growing regions of southern France and northern Spain. Pest Manag. Sci. 2012;68:634–638. doi: 10.1002/ps.2307. PubMed DOI
Angalet G.W., Fuester R. The Aphidius parasites of the pea aphid Acyrthosiphon pisum in the eastern half of the United States. Ann. Entomol. Soc. Am. 1977;70:87–96. doi: 10.1093/aesa/70.1.87. DOI
Starý P., Lyon J.P., Lecant F. Biocontrol of aphids by the introduced Lysiphlebus testaceipes (Ceresson) (Hym: Aphidiidae) in Mediterranean France. J. Appl. Entomol. 1988;105:74–87. doi: 10.1111/j.1439-0418.1988.tb00163.x. DOI
Thies C., Roschewitz I., Tscharntke T. The landscape context of cereal aphid–parasitoid interactions. Proc. R. Soc. 2005;272:203–210. doi: 10.1098/rspb.2004.2902. PubMed DOI PMC
Brodeur J., McNeil J.N. Life history of the aphid hyperparasitoid Asaphes vulgaris Walker (Pteromalidae): Possible consequences on the efficacy of the primary parasitoid Aphidius nigripes Ashmead (Aphidiidae) Can. Entomol. 1994;126:1493–1497. doi: 10.4039/Ent1261493-6. DOI
Rosenheim J.A. Higher-order predators and the regulation of insect herbivore populations. Ann. Rev. Entomol. 1998;43:421–447. doi: 10.1146/annurev.ento.43.1.421. PubMed DOI
Sampaio M.V., Korndörfer A.P., Pujade-Villar J., Hubaide J.E.A., Ferreira S.E., Arantes S.O., Bortoletto D.M., Guimarães C.M., Sánchez-Espigares J.A., Caballero-López B. Brassica aphid (Hemiptera: Aphididae) populations are conditioned by climatic variables and parasitism level: A study case of Triângulo Mineiro, Brazil. Bull. Entomol. Res. 2017;107:410–418. doi: 10.1017/S0007485317000220. PubMed DOI
Schooler S.S., De Barro P., Ives A.R. The potential for hyperparasitism to compromise biological control: Why don’t hyperparasitoids drive their primary parasitoid hosts extinct? Biol. Control. 2011;32:172–179. doi: 10.1016/j.biocontrol.2011.05.018. DOI
Sullivan D.J. Insect hyperparasitism. Ann. Rev. Entomol. 1987;32:49–70. doi: 10.1146/annurev.en.32.010187.000405. DOI
Beddington J.R., Hammond P.S. On the dynamics of host-parasite–hyperparasite interactions. J. Anim. Ecol. 1977;46:811–821. doi: 10.2307/3642. DOI
de Vere Graham M.W.R. The Pteromalidae of north-western Europe (Hymenoptera: Chalcidoidea) Bull. Br. Mus. Nat. Hist. Zool. 1969;16:908.
Kamijo K., Takada H. Studies on aphid hyperparasites of Japan. II. Aphid hyperparasites of the Pteromalidae occurring in Japan (Hymenoptera) Insecta Matsumurana. 1973;2:39–76.
Rakshani E., Kazemzadeh S., Starý P., Barahoei H., Kavallieratos N.G., Ćetković A., Popović A., Bodlah I., Tomanović Ž. Parasitoids (Hymenoptera: Braconidae: Aphidiinae) of northeastern Iran: Aphidiine-aphid-plant associations, key and description of a new species. J. Insect Sci. 2012;12:143. doi: 10.1673/031.012.14301. PubMed DOI PMC
Rakshani E., Starý P., Tomanović Ž., Mifsud D. Aphidiinae (Hymenoptera, Braconidae) aphid parasitoids of Malta: Review and key to species. Bull. Entomol. Soc. Malta. 2015;7:121–137. doi: 10.17387/BULLENTSOCMALTA.2015.10. DOI
Kavallieratos N.G., Tomanović Ž., Petrović A., Janković M., Starý P., Yovkova M., Athanassiou C.G. Review and Key for the Identification of Parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Aphids Infesting Herbaceous and Shrubby Ornamental Plants in Southeastern Europe. Ann. Entomol. Soc. Am. 2013;106:294–309. doi: 10.1603/AN12090. DOI
Ghaliow M.E., Petrović A., Kocić K., ČkrkiĆ J., Bogdanović A.M., Starý P., Kavallieratos N.G., Tomanović Ž. Key for identification of the parasitoids (Hymenoptera: Braconidae: Aphidiinae) of aphids infesting alfalfa in Europe. Zootaxa. 2018;4378:98–110. doi: 10.11646/zootaxa.4378.1.6. PubMed DOI
Lumbierres B., Starý P., Pons X. Seasonal parasitism of cereal aphids in a Mediterranean arable crop system. J. Pest Sci. 2007;80:125–130. doi: 10.1007/s10340-006-0159-0. DOI
Mackauer M. Insect parasites of the green peach aphid, Myzus persicae Sulz., and their control potential. Entomophaga. 1968;13:91–106. doi: 10.1007/BF02371780. DOI
Remaudière G., Leclant F. Le complexe des ennemis naturels des aphides du pêcher dans la moyenne vallée du Rhône. Entomophaga. 1971;16:255–267. doi: 10.1007/BF02371105. DOI
Starý P., Remaudière G., Leclant F. Les Aphidiidae (Hymenoptera) de France et leurs hôtes (Homoptera: Aphididae) Entomophaga Mémoire Hors Série. 1971;5:1–74.
Michelena J.M., Sanchís A., González P. Afidíinos sobre pulgones de frutales en la Comunidad Valenciana. Bol. San. Veg. Plagas. 1994;20:465–470.
Michelena J.M., González P., Soler E. Parasitoides afidiinos (Hymenoptera, Braconidae, Aphidiinae) de pulgones de cultivos agrícolas en la Comunidad Valenciana. Bol. San. Veg. Plagas. 2004;30:317–326.
Laamari M., Khenissa N., Merouani H., Ghodbane S., Starý P. Importance des Hyménoptères prasitoïdes des pucerons en Algérie; Proceedings of the Colloque International sur la Gestion des Risques Phytosanitaires; Marrakech, Morocco. 9–11 November 2009; pp. 581–587.
Pennacchio F. The Italian species of the genus Aphidius Nees (Hymenoptera: Braconidae: Aphidiinae) Boll. Lab. Entomol. Agraria ‘Filippo Silvestri’. 1989;46:75–106.
Boivin G., Hance T., Brodeur J. Aphid parasitoids in biological control. Can. J. Plant Sci. 2012;92:1–12. doi: 10.4141/cjps2011-045. DOI
Pons X., Comas J., Albajes R. Overwintering of cereal aphids (Homoptera: Aphididae) on durum wheat in a Mediterranean climate. Environ. Entomol. 1993;22:381–387. doi: 10.1093/ee/22.2.381. DOI
Pons X., Starý P. Spring aphid-parasitoid (Hom., Aphididae, Hym., Braconidae) associations and interactions in a Mediterranean arable crop ecosystem, including Bt maize. J. Pest Sci. 2003;76:133–138. doi: 10.1007/s10340-003-0003-8. DOI
Starý P. A review of Aphidius species (Hymenoptera: Aphidiidae) of Europe. Annot. Zool. Bot. Bratislava. 1973;85:1–85.
van Lenteren J.C. The state of commercial augmentative biological control: Plenty of natural enemies, but a frustrating lack of uptake. BioControl. 2012;57:1–20. doi: 10.1007/s10526-011-9395-1. DOI
Kocić K., Tomanović Z. Faculty of Biology, University of Belgrade, Belgrade, Serbia. 2018. Unpublished Data.
Kos K., Trdan S., Petrović A., Starý P., Kavallieratos N.G., Petrović-Obradović O., Tomanović Ž. Aphidiinae (Hymenoptera, Braconidae, Aphidiinae) from Slovenia, with description of a new Aphidius species. Zootaxa. 2012;3456:36–50. doi: 10.11646/zootaxa.3456.1.2. DOI
Starý P. A review of the parasites of aphids associated with Prunus trees in Czechoslovakia (Hymenoptera: Aphidiidae, Homoptera: Aphidoidea) Acta Entomol. Bohemoslov. 1966;63:67–75.
Starý P. Aphid Parasitoids of the Czech Republic (Hymenoptera: Braconidae: Aphidiinae) Academia; Prague, Czech Republic: 2006.
Starý P., Lukáš J. Aphid parasitoids and their tritrophic associations in Slovakia (Hymenoptera: Braconidae: Aphidiinae) Folia Hymenopterol. Slovaca. 2009;1:63.
Starý P. Parasites (Hymenoptera, Aphidiidae) of leaf-curling apple aphids in Czechoslovakia. Acta Entomol. Bohemoslov. 1975;72:99–114.
Adisu B., Starý P., Freier B., Büttner C. Aphidius colemani Vier. (Hymenoptera, Braconidae, Aphidiinae) detected in cereal fields in Germany. J. Pest. Sci. 2002;75:89–94. doi: 10.1034/j.1399-5448.2002.02018.x. DOI
Starý P. Field establishment of Aphidius colemani Vier. (Hym., Braconidae, Aphidiinae) in the Czech Republic. J. Appl. Entomol. 2002;126:405–408. doi: 10.1046/j.1439-0418.2002.00663.x. DOI
El-Mali M.U., Starý P., Shahbaz F., Özsemercl F. A review of Aphid parasitoids (Hym. Braconidae, Aphidiinae) of Turkey. Egypt. J. Biol. Pest Control. 2004;14:355–370. doi: 10.4001/003.020.0120. DOI
Gärdenfors U. Taxonomic and biological revision of Palearctic Ephedrus Haliday (Hymenoptera: Braconidae: Aphidiinae) Entomol. Scand. 1986;27:1–95.
Rothschild G.H.L. Records of hymenopterous parasites and hyperparasites of certain fruit-tree aphids. Entomol. Mon. Mag. 1963;99:126–127.
Starý P. A study on the relationship of the Anuraphidina and their aphidiid parasites in Europe (Homoptera, Aphidoidea; Hymenoptera, Aphidiidae) Beitr. Entomol. 1969;19:665–671.
Kavallieratos N.G., Lykouressis D.P., Sarlis G.P., Stathas G.J., Segovia A.S., Athanassiou C.G. The aphidiinae (Hym: Ichneumonidea: Braconidae) of Greece. Phytoparasitica. 2001;29:306–340. doi: 10.1007/BF02981847. DOI
Wang X., Messing R. Potential host range of newly introduced aphid parasitoid Aphidius transcaspicus (Hymenoptera: Braconidae) in Hawaii. Proc. Hawai. Entomol. Soc. 2006;38:81–86.
Lozier J.D., Roderick G.K., Mills N.J. Evolutionarily significant units in natural enemies: Identifying regional populations of Aphidius transcaspicus (Hymenoptera: Braconidae) for use in biological control of mealy plum aphid. Biol. Control. 2008;46:532–541. doi: 10.1016/j.biocontrol.2008.05.002. DOI
Starý P. Integrated control of the mealy plum aphid Hyalopterus pruni (Geoffr.) in Czechoslovakia (Hom. Aphidiidae) Ann. Soc. Entomol. Fr. 1965;1:177–180.
González F.P., Michelena J.M. Relaciones parasitoide-pulgón (Hymenoptera: Aphidiinae; Homoptera:Aphididae) en la provincia de Alicante. Bol. Asoc. Esp. Entomol. 1987;11:245–258.
Starý P. Parasite spectrum and relative abundance of parasites of cereal aphids in Czechoslovakia (Hymenoptera, Aphidiidae; Homoptera, Aphidoidea) Acta Entomol. Bohemoslov. 1976;73:216–223.
Tomanović Ž., Brajkovic M. Aphid parasitoids (Hymenoptera: Aphidiidae) of agroecosystems of the south part of the Pannonian area. Arch. Biol. Sci. 2001;53:57–64.
Ferrer-Suay M., Selfa J., Ribes A., Pujade-Villar J. Contribucions al coneixement dels Charipins de Catalunya (Insecta, Hymenoptera) Orsis. 2012;26:113–134.
Ferrer-Suay M., Selfa J., Ribes A., Pujade-Villar J. A key of the Charipinae (Hymenoptera, Cynipoidea, Figitidae) from Spain, including new records and species. Bol. Asoc. Esp. Entomol. 2013;37:315–341.
Gómez-Marco F., Urbaneja A., Jacas J.A., Rugman-Jones P., Stouthamer R., Tena A. Untangling the aphid-parasitoid food web in citrus: Can hyperparasitoids disrupt biological control? Biol. Control. 2015;81:111–121. doi: 10.1016/j.biocontrol.2014.11.015. DOI
Suay-Cano V.A., Martínez F.L., Michelena J.M. Parasitoides no afidíinos de pulgones (Chalcidoidea: Aphelinidae) e hiperparasitoides de las superfamilias Chalcidoidea, Ceraphronoidea y Cynipoidea (Hymenoptera: Apócrifa: Parastitica) en la provincia de Valencia. Bol. Asoc. Esp. Entomol. 1998;22:99–113.
Acheampong S., Gillespie D.R., Quiring D. Survey of parasitoids and hyperparasitoids (Hymenoptera) of the green peach aphid, Myzus persicae and the foxglove aphid, Aulacorthum solani (Hemiptera: Aphididae) in British Columbia. J. Entomol. Soc. Br. Columbia. 2012;109:12–22.
Sullivan D.J. Comparative behaviour and competition between two aphid hyperparasites: Alloxysta victrix and Asaphes californicus (Hymenoptera: Cynipidae; Pteromalidae) Environ. Entomol. 1972;1:234–244. doi: 10.1093/ee/1.2.234. DOI
Kanuck M.J., Sullivan D.J. Ovipositional Behavior and Larval Development of Aphidencyrtus aphidivorus (Hymenoptera: Encyrtidae), an Aphid Hyperparasitoid. J. N. Y. Entomol. Soc. 1992;100:527–532.
van Lenteren J.C. Quality Control and Production of Biological Control Agents: Theory and Testing Procedures. CABI; Wallingford, Oxon, UK: 2003.
Alignier A., Raymond L., Deconchat M., Menozzi P., Monteil C., Sarthou J.P., Vialatte A., Ouin A. The effect of semi-natural habitats on aphids and their natural enemies across spatial and temporal scales. Biol. Control. 2014;77:76–82. doi: 10.1016/j.biocontrol.2014.06.006. DOI
Blaauw B.R., Isaacs R. Wildflower plantings enhance the abundance of natural enemies and their services in adjacent blueberry fields. Biol. Control. 2015;91:94–103. doi: 10.1016/j.biocontrol.2015.08.003. DOI
Gagić V., Hänke S., Thies C., Scherber C., Tomanović Ž., Tscharntke T. Agricultural intensification and cereal aphid–parasitoid–hyperparasitoid food webs: Network complexity, temporal variability and parasitism rates. Oecologia. 2012;170:1099–1109. doi: 10.1007/s00442-012-2366-0. PubMed DOI PMC
Tomanović Ž., Kavallieratos N.G., Starý P., Stanisavljević L.Z., Cetković A., Stamenković S., Jovanović S., Athanassiou C.G. Regional tritrophic relationship patterns of five aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae) in agroecosystem-dominated landscapes of southeastern Europe. J. Econ. Entomol. 2009;102:836–854. doi: 10.1603/029.102.0302. PubMed DOI
Vollhardt I.M.G., Bianchi F.J.J.A., Wäckers F.L., Thies C., Tscharntke T. Spatial distribution of flower vs. honeydew resources in cereal fields may affect aphid parasitism. Biol. Control. 2010;53:204–213. doi: 10.1016/j.biocontrol.2009.12.011. DOI
Aparicio Y., Gabarra R., Arnó J. Attraction of Aphidius ervi (Hymenoptera: Braconidae) and Aphidoletes aphidimyza (Diptera: Cecidomyiidae) to sweet alyssum and assessment of plant resources effects on their fitness. J. Econ. Entomol. 2018;111:533–541. doi: 10.1093/jee/tox365. PubMed DOI
Jado R.H., Araj S.E., Irmaileh B.A., Shields M.W. Floral resources to enhance the potential of the parasitoid Aphidius colemani for biological control of the aphid Myzus persicae. J. Appl. Entomol. 2019;143:34–42. doi: 10.1111/jen.12556. DOI
Aparicio Y., Gabarra R., Riudavets J., Arnó J. Sustainable Plant Protection Programme, Institut de Recerca i Tecnologia Agroalimentàries (IRTA), Cabrils, Spain. 2015–2016. Personal Observation.
Hassell M.P., Waage J.K. Host-parasitoid population interactions. Ann. Rev. Entomol. 1984;29:89–114. doi: 10.1146/annurev.en.29.010184.000513. DOI