The reproduction of aphids depends to a great extent on their host plants, an integration that impacts on the successful expansion of overwintering populations. Therefore, a survey was conducted to evaluate the globally distributed Capsella bursa-pastoris as an overwintering host of economically important aphid species, their parasitoids and hyperparasitoids in the southern and western regions of Turkey from November to March in 2006 to 2013. During this survey, 395 samples of C. bursa-pastoris were collected with 25 aphid species recorded. Among aphids that feed on this host, Myzus persicae, Aphis gossypii, Rhopalosiphum padi, Aphis fabae, Aphis craccivora, Lipaphis erysimi, and Brevicoryne brassicae were the most frequently recorded. In total, 10,761 individual parasitoids were identified. Binodoxys angelicae, Aphidius colemani, Aphidius matricariae, Diaeretiella rapae, Ephedrus persicae, and Lysiphlebus confusus were the most abundant aphidiines that emerged from the aphids collected from C. bursa-pastoris. Alloxysta spp. (Hymenoptera: Cynipoidea), Chalcidoidea (unidentified at genus level), and Dendrocerus spp. (Hymenoptera: Ceraphronoidea) were identified as hyperparasitoids on the parasitoids. These findings indicate that C. bursa-pastoris is a key non-agricultural plant that significantly contributes to the overwintering of numerous aphids and their parasitoids, which should be given serious consideration when biological control strategies are designed.

Biological Control Research Institute Kışla str Adana 01321 Turkey

Biotechnology Research and Application Center Çukurova University Adana 01330 Turkey

Department of Plant Protection Faculty of Agriculture Çukurova University Adana 01330 Turkey

Department of Plant Protection Faculty of Agriculture Turgut Özal University Malatya 44000 Turkey

Directorate of Plant Produce Protection Greek Ministry of Rural Development and Food 150 Sygrou Ave 17671 Athens Greece

Directorate of Plant Protection Central Research Institute Gayret Mahallesi Fatih Sultan Mehmet Bulvarı No 66 Yenimahalle Ankara 06172 Turkey

Institute of Entomology Biology Centre Laboratory of Aphidology AVCR Branišovska 31 37005 České Budějovice Czech Republic

Laboratory of Agricultural Entomology and Zoology Department of Crop Science Agricultural University of Athens 75 Iera Odos str 11855 Athens Greece

Laboratory of Entomology and Agricultural Zoology Department of Agriculture Crop Production and Rural Environment University of Thessaly Phytokou str 38446 Nea Ionia Greece

Zobrazit více v PubMed

Aksoy A., Dixon J.M., Hale W.H. Capsella bursa-pastoris (L.) medikus (Thlaspi bursa-pastoris L., Bursa bursa-pastoris (L.) shull, Bursa pastoris (L.) weber) J. Ecol. 1998;86:171–186. doi: 10.1046/j.1365-2745.1998.00260.x. DOI

Satar S. Ph.D. Thesis. Cukurova University, Faculty of Agricultural, Department of Plant Protection; Adana, Turkey: 2003. Biological Characteristic of Aphis spiraecola Patch (Homoptera: Aphididae) and Relationship with Parasitoid Lysiphlebia japonica (Ashmead) (Hymenoptera: Aphididae)

Ceplitis A.L.F., Su Y., Lascoux M. Bayesian inference of evolutionary history from chloroplast microsatellites in the cosmopolitan weed Capsella bursa-pastoris (Brassicaceae) Mol. Ecol. 2005;14:4221–4233. doi: 10.1111/j.1365-294X.2005.02743.x. PubMed DOI

Blackman R.L., Eastop V.F. Aphids of the World’s Plants: An Online Identification and Information Guide. Host Lists and Keys. [(accessed on 10 October 2020)]; Available online: http://www.aphidsonworldsplants.info/C_HOSTS_Cab_Car.htm#Capsella.

Fox L., Biever K.D., Toba H.H., Duffus J.E., Thomas P.E. Overwintering and monitoring of potato leafroll virus in some wild crucifers. Am. Potato J. 1993;70:505–515. doi: 10.1007/BF02846751. DOI

Stevens M., Smith H.G., Hallsworth P.B. The host-range of beet yellowing viruses among common arable weed species. Plant Pathol. 1994;43:579. doi: 10.1111/j.1365-3059.1994.tb01593.x. DOI

Satar S., Uygun N. Life cycle of Aphis spiraecola Patch (Homoptera: Aphididae) in east Mediterranean region of Turkey and it’s development on some important host plants. IOBC/WPRS Bull. 2007;38:216–224.

Satar S., Kersting U., Uygun N. Transmission of Turkish citrus tristeza virus isolates by Aphis gossypii Glover (Homoptera: Aphididae) in the laboratory condition. IOBC/WPRS Bull. 2007;38:328–335.

Satar S., Kersting U., Yokomi R. Presence of two host races of Aphis gossypii Glover (Hemiptera: Aphididae) collected in Turkey. Ann. Appl. Boil. 2013;162:41–49. doi: 10.1111/j.1744-7348.2012.00578.x. DOI

Uygun N., Toros S., Ulusoy R., Satar S., Özdemir I. Doğu Akdeniz Bölgesi Aphidoidea (Homoptera) Türleri ile Bunların Parazitoit ve Predatörlerinin Saptanması. Türkiye Bilimsel ve Teknik Araştırma Kurumu, Tarım ve Orman Araştırma Grubu Proje. Ankara University; Ankara, Turkey: 2001. p. 214. No: TÜBİTAK-TOGTAG 1720.

Görür G., Senol O., Geizici G., Akyıldırım Begen H., Parmaksız D. New aphid (Hemiptera: Aphidoidea) records from south eastern parts of Turkey. J. Insect Biodivers. Syst. 2017;3:257–264.

Ng J.C.K., Perry K.L. Transmission of plant viruses by aphid vectors. Mol. Plant Pathol. 2004;5:505–511. doi: 10.1111/j.1364-3703.2004.00240.x. PubMed DOI

Starý P. Aphidiidae. In: Minks A.K., Harrewijn P., editors. Aphids, Their Biology, Natural Enemies and Control. Elsevier; Amsterdam, The Netherland: 1988. pp. 171–184.

Hågvar E.B., Hofsvang T. Aphid parasitoids (Hymenoptera, Aphidiidae): Biology, host selection and use in biological control. Biocontrol. News Inf. 1991;12:13–42.

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

Starý P. Biology of Aphid Parasites (Hymenoptera: Aphidiidae) with Respect to Integrated Control. Dr. W. Junk N.V.; The Hague, The Netherlands: 1970.

Kılınçer N. Der parasitenkomplex der mehligen kohlblattlaus in Ankara umfasst zwei parasiten und vier hyperparasitenarten. Plant Prot. Bull. 1982;22:1–12.

Zeren O., Düzgüneş Z. A study on identification, host plants, effect on host plant and natural enemies of aphids, causing damage on vegetables in Çukurova region. Ministry turkish ministry of agriculture, Ankara, Turkey. Res. Ser. 1989;59:205.

Ölmez S., Ulusoy M.R. A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) in Diyarbakır, Turkey. Phytoparasitica. 2003;31:524–528. doi: 10.1007/BF02979745. DOI

Aslan M.M., Uygun N., Starý P. A survey of aphid parasitoids in Kahramanmaraş, Turkey (Hymenoptera: Braconidae: Aphidiinae and Hymenoptera: Aphelinidae) Phytoparasitica. 2004;32:255–263. doi: 10.1007/BF02979820. DOI

Uysal M., Starý P., Sahbaz A., Özsemerci F. A review of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Turkey. Egypt. J. Biol. Pest Control. 2004;14:355–370.

Güz N., Kılınçer N. Aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) on weeds from Ankara, Turkey. Phytoparasitica. 2005;33:359–366. doi: 10.1007/BF02981302. DOI

Tomanović Ž., Beyarslan A., Erdoğan Ö.Ç. New records of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) from Turkey. Period. Biol. 2008;110:335–338.

Satar S., Karacaoğlu M., Satar G., Uygun N. Studies on introduction of Lysiphlebus testaceipes (Cresson) (Hymenoptera: Braconidae), an important parasitoid of Aphis gossypii Glover (Hemiptera: Aphididae) in citrus orchards of east Mediterranean region of Turkey. Türk. Biyo. Müc. Derg. 2011;2:55–62.

Satar S., Satar G., Karacaoğlu M., Uygun N., Kavallieratos N.G., Starý P., Athanassiou C.G. Parasitoids and hyperparasitoids (Hymenoptera) on aphids (Hemiptera) infesting citrus in east Mediterranean region of Turkey. J. Insect Sci. 2014;14:178. doi: 10.1093/jisesa/ieu040. PubMed DOI PMC

Rakhshani E., Barahoei H., Ahmad Z., Starý P., Ghafouri Moghaddam M., Mehrparvar M., Kavallieratos N.G., Čkrkić J., Tomanović Ž. Review of Aphidiinae parasitoids (Hymenoptera: Braconidae) of the Middle East and North Africa: Key to species and host associations. Eur. J. Taxon. 2019:552. doi: 10.5852/ejt.2019.552. DOI

Starý P., Havelka J. Fauna and associations of aphid parasitoids in an up-dated farmland area (Czech Republic) Bull. Insectol. 2008;61:251–276.

Stenberg J.A. A conceptual framework for integrated pest management. Trends Plant Sci. 2017;22:759–769. doi: 10.1016/j.tplants.2017.06.010. PubMed DOI

Landis D.A., Wratten S.D., Gurr G.M. Habitat management to conserve natural enemies of arthropod pests in agriculture. Annu. Rev. Entomol. 2000;45:175–201. doi: 10.1146/annurev.ento.45.1.175. PubMed DOI

Amoabeng B.W., Stevenson P.C., Mochiah B.M., Asare K.P., Gurr G.M. Scope for non-crop plants to promote conservation biological control of crop pests and serve as sources of botanical insecticides. Sci. Rep. 2020;10:1–15. doi: 10.1038/s41598-020-63709-x. PubMed DOI PMC

Winiarska W. Predatory and parasitic insects in colonies of Aphis/Aphis/ fabae cirsiiacanthoidis Scop. on the thistle, Cirsium arvense (L.) Scop. In: Filipowicz A.J., editor. Materialy Ogolnopolskie Konferencii Naukowej, Nauka y Practyce Ogrodniczej z Okazji XXV-Lecia, Wydaw. Ogrod. Akademii Rolniczej v Lublinie. Adademia Rolnicza; Lublin, Poland: 1995. pp. 403–406.

Starý P. Philadelphus coronarius L. as reservoir of aphids and parasitoids. J. Appl. Entomol. 1991;112:1–10. doi: 10.1111/j.1439-0418.1991.tb01021.x. DOI

Barczak T. Reservoirs and-alternative hosts of aphid parasitoids. Discussion on methods used. Wiad. Entomol. 1996;15:181–187.

Bennewicz J., Kaczorowski G., Barczak T. Aphids in midfield thickets in lower vistula valley landscape park. J. Plant Prot. Res. 2001;41:348–362.

Kavallieratos N.G., Stathas G.J., Athanassiou C.G., Papadoulis G.T. Dittrichia viscosa and Rubus ulmifolius as reservoirs of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) and the role of certain coccinellid species. Phytoparasitica. 2002;30:231–242. doi: 10.1007/BF03039992. DOI

Tomanović Ž., Kavallieratos N.G., Starý P., Petrović O., Tomanović S., Jovanović S. Aphids and parasitoids on willows and poplars in southeastern Europe (Homoptera: Aphidoidea, Hymenoptera: Braconidae: Aphidiinae) J. Plant Dis. Prot. 2006;113:174–180. doi: 10.1007/BF03356176. DOI

Kavallieratos N.G., Tomanović Ž., Starý P., Emmanouel N.E. Vitex agnus-castus and Euphorbia characias ssp. wulfenii as reservoirs of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) Fla. Entomol. 2008;91:179–191. doi: 10.1653/0015-4040(2008)91[179:VACAEC]2.0.CO;2. DOI

Tomanović Ž., Kavallieratos N.G., Starý P., Stanisavljević L.Ž., Ćetković 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

Kavallieratos N.G., Tomanović Ž., Petrović A., Kocić K., Janković M., Starý P. Parasitoids (Hymenoptera: Braconidae: Aphidiinae) of aphids feeding on ornamental trees in southeastern Europe: Key for identification and tritrophic associations. Ann. Entomol. Soc. Am. 2016;109:473–487. doi: 10.1093/aesa/saw003. 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

Eastop V.F., van Emden H.F. The insect material. In: van Emden H.F., editor. Aphid Technology. Academic Press; London, UK: 1972. pp. 1–45.

Krantz G.W. A Manual of Acarology. 2nd ed. Oregon State University Book Stores; Corvallis, OR, USA: 1978.

Rohlf F.J., Sokal R.R. Statistical Tables. Freeman & Company; New York, NY, USA: 1994.

Norris R.F., Kogan M. Interactions between weeds, arthropod pests, and their natural enemies in managed ecosystems. Weed Sci. 2000;48:94–158. doi: 10.1614/0043-1745(2000)048[0094:IBWAPA]2.0.CO;2. DOI

Powell G., Tosh C.R., Hardie J. Host plant selection by aphids: Behavioral, evolutionary, and applied perspectives. Annu. Rev. Entomol. 2006;51:309–330. doi: 10.1146/annurev.ento.51.110104.151107. PubMed DOI

Tamaki G., Olsen D. Evaluation of orchard weed hosts of green peach aphid and the production of winged migrants. Environ. Entomol. 1979;8:314–317. doi: 10.1093/ee/8.2.314. DOI

Cole R.A. The relative importance of glucosinolates and amino acids to the development of two aphid pests Brevicoryne brassicae and Myzus persicae on wild and cultivated brassica species. Entomol. Exp. Appl. 1997;85:121–133. doi: 10.1046/j.1570-7458.1997.00242.x. DOI

Van Emden H.F., Storeck A.P., Douloumpaka S., Eleftherianos I., Poppy G.M., Powell W. Plant chemistry and aphid parasitoids (Hymenoptera: Braconidae): Imprinting and memory. Eur. J. Entomol. 2008;105:477–483. doi: 10.14411/eje.2008.061. DOI

Satar S., Karacaoğlu M., Satar G., Uygun N. Citrus aphids (Hemiptera: Aphididae): Incidence, population fluctuations, host plant and age preferences. Plant Protect. Bull. 2020;60:111–119.

Satar S., Kersting U., Uygun N. Effect of temperature on population parameters of Aphis gossypii Glover and Myzus persicae (Sulzer) (Homoptera: Aphididae) on pepper. J. Plant Dis. Prot. 2008;115:69–74. doi: 10.1007/BF03356241. DOI

Manachini B., Casati P., Cinanni L., Bianco P. Role of Myzus persicae (Hemiptera: Aphididae) and its secondary hosts in plum pox virus propagation. J. Econ. Entomol. 2007;100:1047–1052. doi: 10.1603/0022-0493(2007)100[1047:ROMPHA]2.0.CO;2. PubMed DOI

Plećaš M., Gagić V., Janković M., Petrović Obradović O., Kavallieratos N.G., Tomanović Ž., Thies C., Tscharntke T., Ćetković A. Landscape composition and configuration influence cereal aphid-parasitoid-hyperparasitoid interactions and biological control differentially across years. Agric. Ecosyst. Environ. 2014;183:1–10. doi: 10.1016/j.agee.2013.10.016. DOI

Bayhan S.Ö., Ulusoy M.R. Adana ilinde lahana unlu yaprakbiti (Brevicoryne brassicae L. (Hemiptera: Aphididae) ‘nin bazı curiciferae familyasına bağlı bitkilerdeki populasyon gelişimi. Harran Üni. Zir. Fak. Der. 2010;14:37–46.

Powell W., Wright A.F. The influence of host food plants on host recognition by four aphidiine parasitoids (Hymenoptera: Braconidae) Bull. Entomol. Res. 1992;81:449–453. doi: 10.1017/S0007485300032028. DOI

Decker U.M. Ph.D. Thesis. University of Hohenheim; Stuttgart, Germany: 1988. Evidence for Semiochemicals Affecting the Reproductive Behaviour of the Aphid Parasitoids Aphidius rhopalosiphi De Stefani-Perez and Praon volucre Haliday (Hymenoptera: Aphidiidae)—A Contribution towards Integrated Pest Management in Cereals.

Vinson S.B. Host selection by insect parasitoids. Annu. Rev. Entomol. 1976;21:109–133. doi: 10.1146/annurev.en.21.010176.000545. DOI

de Vos M., Jander G. Volatile communication in plant-aphid interactions. Curr. Opin. Plant Boil. 2010;13:366–371. doi: 10.1016/j.pbi.2010.05.001. PubMed DOI

Kos M., Houshyani B., Wietsma R., Kabouw P., Vet L.E., van Loon J.J., Dicke M. Effects of glucosinolates on a generalist and specialist leaf-chewing herbivore and an associated parasitoid. Phytochemistry. 2012;77:162–170. doi: 10.1016/j.phytochem.2012.01.005. PubMed DOI

Kos M., Houshyani B., Achhami B.B., Wietsma R., Gols R., Weldegergis B.T., Kabouw P., Bouwmeester H.J., Vet L.E.M., Dicke M., et al. Herbivore-mediated effects of glucosinolates on different natural enemies of a specialist aphid. J. Chem. Ecol. 2012;38:100–115. doi: 10.1007/s10886-012-0065-2. PubMed DOI PMC

Murali Baskaran R.K., Sharma K.C., Kaushal P., Kumar J., Parthiban P., Senthil Nathan S., Mankin R.W. Role of kairomone in biological control of crop pests—A review. Physiol. Mol. Plant Path. 2018;101:3–15. doi: 10.1016/j.pmpp.2017.07.004. DOI

Singh R., Tripathi R.N. Records of aphid hyperparasitoids in India. Bioved. 1991;1:141–150.

Brodeur J., McNeil J.N. Host behavior modification by the endoparasitoid Aphidius nigripes: A strategy to reduce hyperparasitism. Ecol. Entomol. 1992;17:97–104. doi: 10.1111/j.1365-2311.1992.tb01164.x. DOI

Müller C.B., Völkl V., Godfray H.C.J. Are behavioural changes in parasitised aphids a protection against hyperparasitism? Eur. J. Entomol. 1997;94:221–234.