Hostname: page-component-76fb5796d-x4r87 Total loading time: 0 Render date: 2024-04-26T20:56:11.532Z Has data issue: false hasContentIssue false
  • English
  • Français

Do primary and secondary host plants affect aphid- parasitoid interactions in fruit orchards?

Published online by Cambridge University Press:  21 December 2022

Şahin Kök Open the ORCID record for Şahin Kök [Opens in a new window] ,
Željko Tomanović Open the ORCID record for Željko Tomanović [Opens in a new window] ,
Ersin Karabacak Open the ORCID record for Ersin Karabacak [Opens in a new window]  and
İsmail Kasap Open the ORCID record for İsmail Kasap [Opens in a new window]
Şahin Kök*
Affiliation:
Department of Plant and Animal Production, Çanakkale Onsekiz Mart University, Lapseki Vocational School, 17800, Çanakkale, Turkey
Željko Tomanović
Affiliation:
Faculty of Biology, University of Belgrade, Institute of Zoology, Studenstki trg 16, 11000 Belgrade, Serbia
Ersin Karabacak
Affiliation:
Faculty of Arts and Sciences, Department of Biology, Çanakkale Onsekiz Mart University, 17020, Çanakkale, Turkey
İsmail Kasap
Affiliation:
Faculty of Agriculture, Department of Plant Protection, Çanakkale Onsekiz Mart University, 17020, Çanakkale, Turkey
*
Author for correspondence: Şahin Kök, Email: sahinkok@gmail.com; sahinkok@comu.edu.tr
Get access Rights & Permissions [Opens in a new window]

Abstract

The aim of this study was to investigate how the primary (PHP) and secondary host plants (SHP) in the fruit orchards affect the interactions of aphids and their parasitoids in northwest Turkey during spring and summer 2020 and 2021. In total, 67 tritrophic aphid–parasitoid-host plant interactions, including new association records for Europe and Turkey, were obtained from 16 parasitoid species from the subfamily Aphidiinae (Hymenoptera: Braconidae) reared from 25 aphid species (Hemiptera: Aphididae) on 22 PHP and SHP in the fruit orchards. Also, we evaluated the effect of the PHP and SHP on the parasitoids, aphids and their interactions. We revealed that the species richness and the values of the biodiversity indices of the parasitoids and aphids were significantly higher on the SHP than the PHP. Similarly, the aphid–parasitoid interactions on the SHP showed greater diversity than the PHP. The results of this study clearly show that the interactions of parasitoids and aphids in the fruit orchards were more diverse on the SHP compared to the PHP.

Keywords

Aphidsparasitoidsprimary host plantssecondary host plantstritrophic interaction
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 113 , Issue 3 , June 2023 , pp. 326 - 334
Check for updates
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ahmad, M and Akhtar, S (2013) Development of insecticide resistance in field populations of Brevicoryne brassicae (Hemiptera: Aphididae) in Pakistan. Journal of Economic Entomology 106, 954–958.10.1603/EC12233CrossRefGoogle ScholarPubMed
Albittar, L, Ismail, M, Bragard, C and Hance, T (2016) Host plants and aphid hosts influence the selection behaviour of three aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae). European Journal of Entomology 113, 516–522.CrossRefGoogle Scholar
Alhmedi, A, Raymaekers, S, Tomanović, Ž, Bylemans, D and Beliën, T (2018) Food web structure of aphids and their parasitoids in Belgian fruit agroecosystems. Entomological Science 21, 279–291.Google Scholar
Aparicio, Y, Gabarra, R, Riudavets, J, Starý, P, Tomanović, Ž, Kocić, K, Villar, JP, Suay, MF, Porta, VC and Arnó, J (2019) Hymenoptera complex associated with Myzus persicae and Hyalopterus spp. in peach orchards in northeastern Spain and prospects for biological control of aphids. Insects 10, 109.Google ScholarPubMed
Aparicio, Y, Riudavets, J, Gabarra, R, Agustí, N, Rodríguez-Gasol, N, Alins, G, Blasco-Moreno, A and Arnó, J (2021) Can insectary plants enhance the presence of natural enemies of the green peach aphid (Hemiptera: Aphididae) in Mediterranean peach orchards? Journal of Economic Entomology 114, 784–793.CrossRefGoogle ScholarPubMed
Askar, SI, El-Aw, MA and Draz, KA (2013) Population density of the mealy plum aphid, Hyalopterus pruni (Geoffroy) (Homiptera: Aphididae) and its natural enemies on the weed, Arundo donax, L. at El-Beheira Governorate. Journal of Agricultural and Environmental Science Damanhour University Egypt 12, 93–105.Google Scholar
Aslan, B (2015) Survey of the predatory and parasitoid species-complex of aphids (Hemiptera: Aphididae) at fruit growing areas in Burdur, Turkey. Egyptian Journal of Biological Pest Control 25, 261–265.Google Scholar
Aslan, B and Karaca, İ (2005) Fruit tree aphids and their natural enemies in Isparta region, Turkey. Journal of Pest Science 78, 227–229.CrossRefGoogle Scholar
Barczak, T, Bennewicz, J and Brochocka, A (2014) Reservoirs of parasitoids (Hymenoptera) of the grain aphid Sitobion avenae F. on wild growing plants in Poland. Egyptian Journal of Biological Pest Control 24, 483–490.Google Scholar
Blackman, RL and Eastop, VF (2006) Aphid's on the world's herbaceous plants and shrubs: an identification and information guide. Vol. 1. Host lists and keys. Vol. 2. The aphids. John Wiley & Sons Ltd., Chichester, West Sussex.Google Scholar
Blackman, RL and Eastop, VF (2007) Taxonomic issues. In van Emden, HF and Harrington, R (eds), Aphids as Crop Pests, 2nd Edn. Wallingford: CABI, pp. 1–29.Google Scholar
Blackman, RL and Eastop, VF (2022) Aphids on the world's plants. An online identification and information guide. Available at http://www.aphidsonworldsplants.info/ (Accessed 10 February 2022).Google Scholar
Boivin, G, Hance, T and Brodeur, J (2012) Aphid parasitoids in biological control. Canadian Journal of Plant Science 92, 1–12.Google Scholar
Carroll, DP and Hoyt, SC (1986) Hosts and habitats of parasitoids (Hymenoptera: Aphidiidae) implicated in biological control of apple aphid (Homoptera: Aphididae). Environmental Entomology 15, 1171–1178.Google Scholar
Cheng, S, Lin, R, Yu, C, Sun, R and Jiang, H (2021) Toxic effects of seven pesticides to aphid parasitoid, Aphidius gifuensis (Hymenoptera: Braconidae) after contact exposure. Crop Protection 145, 105634.CrossRefGoogle Scholar
Dedryver, CA, Le Ralec, A and Fabre, F (2010) The conflicting relationships between aphids and men: a review of aphid damage and control strategies. Comptes Rendus Biologies 333, 539–553.CrossRefGoogle Scholar
Dormann, CF, Fründ, J, Gruber, B, Beckett, S, Devoto, M, Felix, G, Iriondo, J, Opsahl, T, Pinheiro, R and Strauss, R (2014) Package ‘bi-partite’. Visualising bipartite networks and calculating some (ecological) indices. R package, version 2.04. Available at https://cran.r-project.org/web/packages/bipartite/index.html (Accessed 20 March 2022).Google Scholar
Favret, C (2021) Aphid species file. Version 5.0/5.0. Available at http://www.aphid.speciesfile.org (Accessed 10 February 2022).Google Scholar
Filajdić, N, Sutton, TB, Walgenbach, JF and Unrath, CR (1995) The influence of the apple aphid/spirea aphid complex on intensity of alternaria blotch of apple and fruit characteristics and yield. Plant Disease 79, 691–694.CrossRefGoogle Scholar
Gontijo, LM, Beers, EH and Snyder, WE (2013) Flowers promote aphid suppression in apple orchards. Biological Control 66, 8–15.CrossRefGoogle Scholar
Hashemi, SM and Damalas, CA (2010) Farmers' perceptions of pesticide efficacy: reflections on the importance of pest management practices adoption. Journal of Sustainable Agriculture 35, 69–85.CrossRefGoogle Scholar
Hawro, V, Ceryngier, P, Tscharntke, T, Thies, C, Gagic, V, Bengtsson, J, Bommarco, R, Winqvist, C, Weisser, WW, Clement, LW, Japoshvili, G and Ulrich, W (2015) Landscape complexity is not a major trigger of species richness and food web structure of European cereal aphid parasitoids. BioControl 60, 451–461.CrossRefGoogle Scholar
Hille Ris Lambers, D (1950) On mounting aphids and other soft skinned insects. Entomologische Berichten 298, 55–58.Google Scholar
Hullé, M, Turpeau, E and Chaubet, B (2006) Encyclop'aphid. INRA. Available at https://www6.inra.fr/encyclopedie-pucerons (Accessed 18 March 2022).Google Scholar
Jado, RH, Araj, SE, Abu-Irmaileh, B, Shields, MW and Wratten, SD (2019) Floral resources to enhance the potential of the parasitoid Aphidius colemani for biological control of the aphid Myzus persicae. Journal of Applied Entomology 143, 34–42.CrossRefGoogle Scholar
Katis, NI, Tsitsipis, JA, Stevens, M and Powell, G (2007) Transmission of plant viruses. In van Emden, HF and Harrington, R (eds), Aphids as Crop Pests, 2nd Edn. Wallingford: CABI, pp. 353–390.CrossRefGoogle Scholar
Kavallieratos, NG, Athanassiou, CG, Stathas, GJ and Tomanović, Ž (2002) Aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) on citrus: seasonal abundance, association with the species of host plant, and sampling indices. Phytoparasitica 30, 365–377.CrossRefGoogle Scholar
Kavallieratos, NG, Tomanović, Ž, Starý, P, Athanassiou, CG, Sarlis, GP, Petrović, O, Niketić, M and Veroniki, MA (2004) A survey of aphid parasitoids (Hymenoptera: Braconidae: Aphidiinae) of Southeastern Europe and their aphid-plant associations. Applied Entomology and Zoology 39, 527–563.CrossRefGoogle Scholar
Kavallieratos, NG, Tomanović, Ž, Starý, P and Bogdanović, AM (2008) Parasitoids (Hymenoptera: Braconidae: Aphidiinae) attacking aphids feeding on Prunoideae and Maloideae crops in Southeast Europe: aphidiine-aphid-plant associations and key. Zootaxa 1793, 47–64.CrossRefGoogle Scholar
Kindt, R and Kindt, MR (2019) Package ‘BiodiversityR’. Package for community ecology and suitability analysis, 2, 11–12.Google Scholar
Kishinevsky, M, Keasar, T, Harari, AR and Chiel, E (2017) A comparison of naturally growing vegetation vs. border-planted companion plants for sustaining parasitoids in pomegranate orchards. Agriculture, Ecosystems & Environment 246, 117–123.CrossRefGoogle Scholar
Kök, Ş (2021) Diversity and plant interactions of aphids (Hemiptera: Aphidomorpha) adjacent to Çardak Lagoon with new aphid and host records for Turkey. Turkish Journal of Entomology 45, 425–439.CrossRefGoogle Scholar
Kök, Ş and Kasap, İ (2022) Interactions of aphids (Hemiptera: Aphididae) with their primary and secondary host plants in orchards in Çanakkale Province, Turkey. Turkish Journal of Entomology 46, 51–62.Google Scholar
Kök, Ş, Aktaç, N and Kasap, İ (2022) Ant (Hymenoptera: Formicidae)- aphid (Hemiptera: Aphididae) interactions in different habitats from Turkey with new mutualistic associations. Agricultural and Forest Entomology 24, 124–136.CrossRefGoogle Scholar
Kos, K, Trdan, S, Petrović, A, Starý, P, Kavallieratos, NG, Petrović-Obradović, O and Tomanović, Ž (2012) Aphidiinae (Hymenoptera, Braconidae, Aphidiinae) from Slovenia, with description of a new Aphidius species. Zootaxa 3456, 36–50.Google Scholar
Letourneau, DK, Bothwell Allen, SG, Kula, RR, Sharkey, MJ and Stireman, JO III (2015) Habitat eradication and cropland intensification may reduce parasitoid diversity and natural pest control services in annual crop fields. Elementa: Science of the Anthropocene 3, 000069.Google Scholar
Margaritopoulos, JT, Skouras, PJ, Nikolaidou, P, Manolikaki, J, Maritsa, K, Tsamandani, K, Kanavaki, OM, Bacandritsos, N, Zarpas, KD and Tsitsipis, JA (2007) Insecticide resistance status of Myzus persicae (Hemiptera: Aphididae) populations from peach and tobacco in mainland Greece. Pest Management Science 63, 821–829.Google ScholarPubMed
Monteiro, LB, Souza, A and Belli, EL (2004) Parasitism on Eriosoma lanigerum (Homoptera: Aphididae) by Aphelinus mali (Hymenoptera: Encyrtidae) on apple orchards, in Fraiburgo county, state of Santa Catarina, Brazil. Revista Brasileira de Fruticultura 26, 550–551.CrossRefGoogle Scholar
Monticelli, LS, Koutsovoulos, G, Lasserre, A, Amiens-Desneux, E, Lavoir, AV, Harwood, JD and Desneux, N (2021) Impact of host and plant phylogenies on parasitoid host range. Biological Control 163, 104729.CrossRefGoogle Scholar
Peñalver-Cruz, A, Jaloux, B and Lavandero, B (2021) The host-plant origin affects the morphological traits and the reproductive behavior of the aphid parasitoid Aphelinus mali. Agronomy 12, 101.CrossRefGoogle Scholar
Petermann, JS, Müller, CB, Weigelt, A, Weisser, WW and Schmid, B (2010) Effect of plant species loss on aphid–parasitoid communities. Journal of Animal Ecology 79, 709–720.CrossRefGoogle ScholarPubMed
Plećaš, M, Gagić, V, Janković, M, Petrović-Obradović, O, Kavallieratos, NG, Tomanović, Ž, Thies, C, Tscharntkee, T and Ćetković, A (2014) Landscape composition and configuration influence cereal aphid–parasitoid–hyperparasitoid interactions and biological control differentially across years. Agriculture, Ecosystems & Environment 183, 1–10.CrossRefGoogle Scholar
Rakhshani, E (2012) Aphid parasitoids (Hymenoptera: Braconidae, Aphidiinae) associated with pome and stone fruit trees in Iran. Journal of Crop Protection 1, 81–95.Google Scholar
R Core Team (2022) R: A Language and Environment for Statistical Computing. Vienna, Austria: R foundation for statistical computing. Available at https://www.r-project.org/ (Accessed 20 February 2022).Google Scholar
Rezaei, M, Talebi, AA, Fathipour, Y, Karimzadeh, J and Mehrabadi, M (2019) Foraging behavior of Aphidius matricariae (Hymenoptera: Braconidae) on tobacco aphid, Myzus persicae nicotianae (Hemiptera: Aphididae). Bulletin of Entomological Research 109, 840–848.CrossRefGoogle ScholarPubMed
Rogers, DJ, Sharma, N, Stretton, DC and Walker, JTS (2011) Toxicity of pesticides to Aphelinus mali the parasitoid of woolly apple aphid. New Zealand Plant Protection 64, 235–240.CrossRefGoogle Scholar
Sabahi, Q, Rasekh, A and Michaud, JP (2011) Toxicity of three insecticides to Lysiphlebus fabarum, a parasitoid of the black bean aphid, Aphis fabae. Journal of Insect Science 11, 104.CrossRefGoogle ScholarPubMed
Satar, S, Kavallieratos, NG, Tüfekli, M, Satar, G, Athanassiou, CG, Papanikolaou, NE, Karacaoğlu, M, Özdemir, I and Starý, P (2021) Capsella bursa-pastoris is a key overwintering plant for aphids in the mediterranean region. Insects 12, 744.CrossRefGoogle ScholarPubMed
Simon-Delso, N, Amaral-Rogers, V, Belzunces, LP, Bonmatin, JM, Chagnon, M, Downs, C, Furlan, L, Gibbons, DW, Giorio, C, Girolami, V, Goulson, D, Kreutzweiser, DP, Krupke, CH, Liess, M, Long, E, McField, M, Mineau, P, Mitchell, EAD, Morrissey, CA, Noome, DA, Pisa, L, Settele, J, Stark, JD, Tapparo, A, Van Dyck, H, Van Praagh, J, Van der Sluijs, JP, Whitehorn, PR and Wiemers, M (2015) Systemic insecticides (neonicotinoids and fipronil): trends, uses, mode of action and metabolites. Environmental Science and Pollution Research 22, 5–34.CrossRefGoogle ScholarPubMed
Smith, JP and Schowalter, TD (2001) Aphid-induced reduction of shoot and root growth in Douglas fir seedlings. Ecological Entomology 26, 411–416.CrossRefGoogle Scholar
Stilmant, D, Van Bellinghen, C, Hance, T and Boivin, G (2008) Host specialization in habitat specialists and generalists. Oecologia 156, 905–912.CrossRefGoogle ScholarPubMed
Tizado, EJ and Nunez Perez, E (1998) Fruit treee aphids (Aphididae) and their wild host plants in the Province of Leon (Spain). In Nieto Nafría, JM and Dixon, AFG (eds), Aphids in Natural and Managed Ecosystem. Leon: Universidad de Leon (Secretariado de Publicaciones), pp. 629–633.Google Scholar
Tomanović, Ž, Kavallieratos, NG, Starý, P, Petrovic-Obradović, O, Tomanović, S and Jovanović, S (2006) Aphids and parasitoids on willows and poplars in Southeastern Europe (Homoptera: Aphidoidea; Hymenoptera: Braconidae, Aphidiinae). Journal of Plant Diseases and Protection 113, 174–180.CrossRefGoogle Scholar
Tomanović, Ž, Rakhshani, E, Starý, P, Kavallieratos, NG, Stanisavljević, LŽ, Žikić, V and Athanassiou, CG (2007) Phylogenetic relationships between the genera Aphidius and Lysaphidus (Hymenoptera: Braconidae: Aphidiinae) with description of Aphidius iranicus sp. nov. The Canadian Entomologist 139, 297–307.CrossRefGoogle Scholar
Tomanović, Ž, Kavallieratos, NG, Starý, P, Stanisavljević, LJ, Ćetković, A, Stamenković, S, Jovanović, S and Athanassiou, CG (2009) Regional tritrophic relationship patterns of five aphid parasitoid species (Hymenoptera: Braconidae: Aphidiinae) in agroecosystem-dominated landscapes of Southeastern Europe. Journal of Economic Entomology 102, 836–854.CrossRefGoogle ScholarPubMed
Tomanović, Ž, Petrović, A, Mitrović, M, Kavallieratos, NG, Starý, P, Rakhshani, E, Rakhshanipour, M, Popović, A, Shukshuk, AH and Ivanović, A (2014) Molecular and morphological variability within the Aphidius colemani group with redescription of Aphidius platensis Brethes (Hymenoptera: Braconidae: Aphidiinae). Bulletin of Entomological Research 104, 552–565.Google ScholarPubMed
Tomanović, Ž, Žikić, V and Petrović, A (2021) Fauna of Parasitoid Wasps (Hymenoptera, Braconidae, Aphidiinae) of Serbia. Monographs, Vol. DCXCVII. Belgrade: Serbian Academy of Sciences and Arts.Google Scholar
TUIK (2021) Turkish Statistical Institute. Data Portal For Statistics. Available at https://biruni.tuik.gov.tr/medas/?kn=92&locale=tr (Accessed 15 April 2022).Google Scholar
Tylianakis, JM, Didham, RK and Wratten, SD (2004) Improved fitness of aphid parasitoids receiving resource subsidies. Ecology 85, 658–666.CrossRefGoogle Scholar
Ulusoy, S, Atakan, E and Dinçer, S (2018) Neonicotinoid resistance of Aphis gossypii Glover, 1877 (Hemiptera: Aphididae) in cotton fields of Çukurova Region, Turkey. Turkish Journal of Entomology 42, 23–31.CrossRefGoogle Scholar
Van Emden, HF, Eastop, VF, Hughes, RD and Way, MJ (1969) The ecology of Myzus persicae. Annual Review of Entomology 14, 197–270.Google Scholar
Völkl, W and Mackauer, M (2000) Oviposition behaviour of aphidiine wasps (Hymenoptera: Braconidae, Aphidiinae): morphological adaptations and evolutionary trends. The Canadian Entomologist 132, 197–212.CrossRefGoogle Scholar
Völkl, W, Mackauer, M, Pell, J and Brodeur, J (2007) Predators, parasitoids and pathogens. In van Emden, HF and Harrington, R (eds), Aphids as Crop Pests, 2nd Edn. Wallingford: CABI, pp. 187–233.CrossRefGoogle Scholar
Wang, KY, Guo, QL, Xia, XM, Wang, HY and Liu, TX (2007) Resistance of Aphis gossypii (Homoptera: Aphididae) to selected insecticides on cotton from five cotton production regions in Shandong, China. Journal of Pesticide Science 32, 372–378.CrossRefGoogle Scholar
Ward, SE, Umina, PA, Macfadyen, S and Hoffmann, AA (2021) Hymenopteran parasitoids of aphid pests within Australian grain production landscapes. Insects 12, 44.CrossRefGoogle ScholarPubMed
Zhang, Y, Zhao, MC, Cheng, J, Liu, S and Yuan, HB (2020) Population dynamics and species composition of maize field parasitoids attacking aphids in northeastern China. Plos One 15, e0241530.CrossRefGoogle ScholarPubMed
Žikić, V, Lazarević, M and Milošević, D (2017) Host range patterning of parasitoid wasps Aphidiinae (Hymenoptera: Braconidae). Zoologischer Anzeiger 268, 75–83.CrossRefGoogle Scholar
Zvereva, EL, Lanta, V and Kozlov, MV (2010) Effects of sap-feeding insect herbivores on growth and reproduction of woody plants: a meta-analysis of experimental studies. Oecologia 163, 949–960.Google ScholarPubMed