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Selection of insectary plants for the conservation of biological control agents of aphids and thrips in fruit orchards

Published online by Cambridge University Press:  26 March 2021

Carmen Denis Open the ORCID record for Carmen Denis [Opens in a new window] ,
Jordi Riudavets Open the ORCID record for Jordi Riudavets [Opens in a new window] ,
Rosa Gabarra Open the ORCID record for Rosa Gabarra [Opens in a new window] ,
Paula Molina Open the ORCID record for Paula Molina [Opens in a new window]  and
Judit Arnó Open the ORCID record for Judit Arnó [Opens in a new window]
Carmen Denis
Affiliation:
IRTA, Ctra. de Cabrils Km 2, 08348 Cabrils, Barcelona, Spain
Jordi Riudavets
Affiliation:
IRTA, Ctra. de Cabrils Km 2, 08348 Cabrils, Barcelona, Spain
Rosa Gabarra
Affiliation:
IRTA, Ctra. de Cabrils Km 2, 08348 Cabrils, Barcelona, Spain
Paula Molina
Affiliation:
IRTA, Ctra. de Cabrils Km 2, 08348 Cabrils, Barcelona, Spain
Judit Arnó*
Affiliation:
IRTA, Ctra. de Cabrils Km 2, 08348 Cabrils, Barcelona, Spain
*
Author for correspondence: Judit Arnó, Email: [email protected]
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Abstract

This study evaluated the potential of flowering plant species naturally occurring to promote the conservation and early establishment of key natural enemies of aphids and thrips in apple and peach orchards. Flowering plants present in the North East of Spain, a main fruit production area in Europe, were sampled to determine their flowering period and to identify potential natural enemies present on each plant species. Thirty-six plant species were found blooming from early March to late May and provided an array of flowers that might ensure food resources for natural enemies. Among them, six species – Eruca vesicaria (L.) Cav., Cardaria draba (L.) Desv., Euphorbia serrata (L.) S.G. Gmel., Malva sylvestris L., Anacyclus clavatus (Desf.) Pers. and Diplotaxis erucoides (L.) DC. – hosted a high diversity of potential natural enemies of aphids and thrips. Their blooming started early in the season and lasted for several sampling weeks and they were widely distributed. Moreover, they had available nectar even in those species with protected nectaries. Therefore, these plant species can be considered as promising candidates for inclusion in the ecological infrastructure designed for fruit orchards in the study area to promote the conservation of the biological control agents of aphids and thrips.

Keywords

Flower architectureflower marginsinsect sizenatural enemiesparasitoidspredators
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 111 , Issue 5 , October 2021 , pp. 517 - 527
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Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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References

Alavi, J and Minaei, K (2018) Studies on the genus Aeolothrips (Thysanoptera: Aeolothripidae) in Iran, with a key to species. Zootaxa 4446, 343–360.CrossRefGoogle ScholarPubMed
Alins, G, Lordan, J, Rodriguez-Gasol, N, Belmonte, J, de Linares, C, Alegre, S, Arnó, J, Avilla, J and Sarasúa, MJ (2019) Guia de plantes per afavorir els enemics naturals de les plagues. Lleida: IRTA.Google Scholar
Aparicio, Y, Gabarra, R and Arnó, J (2018) Attraction of Aphidius ervi (Hymenoptera: Braconidae) and Aphidoletes aphidimyza (Diptera: Cecidomyiidae) to sweet alyssum and assessment of plant resources effects on their fitness. Journal of Economic Entomology 111, 533–541.CrossRefGoogle ScholarPubMed
Aparicio, Y, Gabarra, R, Riudavets, J, Starý, P, Tomanović, Ž, Kocić, K, Pujade Villar, J, Ferrer Suay, M, Cuesta Porta, V and Arnó, J (2019) Hymenoptera complex associated with Myzus persicae and Hyalopterus spp. in peach orchards in Northeastern Spain and prospects for biological control. Insects 10, 109.CrossRefGoogle 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 (in press) toaa298, https://doi.org/10.1093/jee/toaa298.CrossRefGoogle ScholarPubMed
Araj, SE and Wratten, SD (2015) Comparing existing weeds and commonly used insectary plants as floral resources for a parasitoid. Biological Control 81, 15–20.CrossRefGoogle Scholar
Araj, S, Shields, MW and Wratten, SD (2019) Weed floral resources and commonly used insectary plants to increase the efficacy of a whitefly parasitoid. BioControl 64, 553–561.CrossRefGoogle Scholar
Badenes-Pérez, FR (2019) Trap crops and insectary plants in the order Brassicales. Annals of the Entomological Society of America 112, 318–329.CrossRefGoogle Scholar
Balzan, MV, Bocci, G and Moonen, AC (2014) Augmenting flower trait diversity in wildflower strips to optimise the conservation of arthropod functional groups for multiple agroecosystem services. Journal of Insect Conservation 18, 713–728.CrossRefGoogle Scholar
Barbagallo, S, Cocuzza, GE, Cravedi, P and Komazaki, S (2017) IPM case studies: deciduous fruit tree. In van Emden, H and Harrington, R (eds), Aphids as Crop Pests, 2nd edn. Wallingford: CABI Publishing, pp. 651–661.Google Scholar
Bàrberi, P, Burgio, G, Dinelli, G, Moonen, AC, Otto, S, Vazzana, C and Zanin, G (2010) Functional biodiversity in the agricultural landscape: relationships between weeds and arthropod fauna. Weed Research 50, 388–401.CrossRefGoogle Scholar
Bournier, A, Lacasa, A and Pivot, Y (1978) Biologie d'un thrips prédateur Aeolothrips intermedius (Thys.: Aeolothripidae). Entomophaga 23, 403–410.CrossRefGoogle Scholar
Bugg, RL and Waddington, C (1994) Using cover crops to manage arthropods pests of orchards: a review. Agriculture, Ecosystems & Environment 50, 11–28.CrossRefGoogle Scholar
Cahenzli, F, Sigsgaard, L, Daniel, C, Herz, A, Jamar, L, Kelderer, M, Jacobsen, SK, Kruczyńska, D, Matray, S, Porcel, M, Sekrecka, M, Świergiel, V, Tasin, M, Telfser, J and Pfiffner, L (2019) Perennial flower strips for pest control in organic apple orchards – a pan-European study. Agriculture, Ecosystems & Environment 278, 43–53.CrossRefGoogle Scholar
Comba, L, Corbet, SA, Hunt, L and Warren, B (1999) Flowers, nectar and insect visits: evaluating British plant species for pollinator-friendly gardens. Annals of Botany 83, 369–383.CrossRefGoogle Scholar
Corbett, A and Rosenheim, JA (1996) Impact of a natural enemy overwintering refuge and its interaction with the surrounding landscape. Ecological Entomology 21, 155–164.CrossRefGoogle Scholar
DARP, Departament d'Agricultura, Ramaderia, Pesca i Alimentació (2020) Superfícies, rendiments i produccions comarcals dels conreus agrícoles. Available at http://agricultura.gencat.cat/ca/departament/estadistiques/agricultura/estadistiques-definitives-conreus/ (last accessed July 2020).Google Scholar
Dassonville, N, Thiellemans, T and Gosset, V (2013) FresaProtect and Berryprotect: mixes of parasitoids to control all common aphid species on protected soft fruit crops product development and case studies from three years of experience. Aspects of Applied Biology 119, 79–88.Google Scholar
Davidson, MM, Nielsen, M-C, Butler, RC, Castañé, C, Alomar, O, Riudavets, J and Teulon, DAJ (2014) Can semiochemicals attract both western flower thrips and their anthocorid predators? Entomologia Experimentalis et Applicata 155, 54–63.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 ScholarPubMed
Eilenberg, J, Hajek, A and Lomer, C (2001) Suggestions for unifying the terminology in biological control. BioControl 46, 387–400.CrossRefGoogle Scholar
Eurostat (2019) Structure of Orchards in 2017: Two-Thirds of the EU's Fruit Plantation Area is Concentrated in Spain, Italy and Poland. Eurostat newsrelease 32/2019. Available at https://ec.europa.eu/eurostat.Google Scholar
Fitzgerald, JD and Solomon, MG (2004) Can flowering plants enhance numbers of beneficial arthopods in UK apple and pear orchards? Biocontrol Science and Technology 14, 291–300.CrossRefGoogle Scholar
Gobierno de Aragón (2020) Estadísticas Agrícolas. Resumen del sector leñosos 2015–2017. Available at https://www.aragon.es/-/estadisticas-agricolas#anchor4 (last accessed July 2020).Google Scholar
Gontijo, LM, Beers, EH and Snyder, WE (2013) Flowers promote aphid suppression in apple orchards. Biological Control 66, 8–15.CrossRefGoogle Scholar
González, E, Alvarado, M, Verlanga, E, Serrano, A and de la Rosa, A (1994) Daños producidos por trips en nectarinas en el Valle del Guadalquivir. Boletín de Sanidad Vegetal. Plagas 20, 229–241.Google Scholar
Grissell, EE and Schauff, ME (1990) A Handbook of the Families of Nearctic Chalcidoidea (Hymenoptera). Washington: Entomological Society of Washington.Google Scholar
Gurr, GM, Wratten, SD and Altieri, MA (2004) Ecological Engineering for Pest Management: Advances in Habitat Manipulation for Arthropods. Collingwood, Vic, Australia: CSIRO Publishing, p. 225.CrossRefGoogle Scholar
Hammer, Ø, Harper, DAT and Ryan, PD (2001) Past: paleontological statistics software package for education and data analysis. Paleontología Electrónica 4, 1–9.Google Scholar
Hanson, PE and Gauld, ID (eds). (2006) Hymenoptera de la Región Neotropical. Gainesville, FL: Memoirs of the American Entomological Institute, vol. 77, pp. 1–994.Google Scholar
Idris, AB and Grafius, E (1997) Nectar-collecting behavior of Diadegma insulare (Hymenoptera: Ichneumonidae), a parasitoid of diamondback moth (Iepidoptera: Plutellidae). Environmental Entomology 26, 114–120.CrossRefGoogle Scholar
Jado, RH, Araj, SE, Irmaileh, BA and Shields, MW (2018) Floral resources to enhance the potential of the parasitoids Aphidius colemani for biological control of the aphid Myzus persicae. Journal of Applied Entomology 143, 34–42.CrossRefGoogle Scholar
Johanowicz, DL and Mitchell, ER (2000) Effects of sweet alyssum flowers on the longevity of the parasitoid wasps Cotesia marginiventris (Hymenoptera: Braconidae) and Diadegma insulare (Hymenoptera: Ichneumonidae). Florida Entomologist 83, 41–47.CrossRefGoogle Scholar
Kavallieratos, NG, Tomanovic, Z, Stary, P, Athanassiou, CG, Sarlis, GP, Petrovic, O, Niketic, 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
Loomans, AJM (2006) Exploration for hymenopterous parasitoids of thrips. Bulletin of Insectology 59, 69–83.Google Scholar
Lordan, J, Alegre, S, Gatius, F, Sarasúa, MJ and Alins, G (2014) Woolly apple aphid Eriosoma lanigerum Hausmann ecology and its relationship with climatic variables and natural enemies in Mediterranean areas. Bulletin of Entomological Research 105, 60–69.CrossRefGoogle ScholarPubMed
Magurran, AE (2004) Measuring Biological Diversity. Oxford, UK: Blackwell, 256p.Google Scholar
MAPA (Ministerio de Agricultura, Pesca y Alimentación) (2020) Available at https://www.mapa.gob.es/es/estadistica/temas/estadisticasagrarias/agricultura/superficies-producciones-anuales-cultivos/ (accessed on 21 March 2020).Google Scholar
Miñarro, M, Hemptinne, JL and Dapena, E (2005) Colonization of apple orchards by predators of Dysaphis plantaginea: sequential arrival, response to prey abundance and consequences for biological control. BioControl 50, 403–414.CrossRefGoogle Scholar
Nave, A, Gonçalves, F, Crespí, AL, Campos, M and Torres, L (2016) Evaluation of native plant flower characteristics for conservation biological control of Prays oleae. Bulletin of Entomological Research 106, 249–257.CrossRefGoogle ScholarPubMed
Papp, N (2004) Nectar and nectary studies on seven Euphorbia species. Acta Botanica Hungarica 46, 225–234.CrossRefGoogle Scholar
Patt, JM, Hamilton, GC and Lashomb, JH (1997) Foraging success of parasitoids wasps on flowers: interplay of insect morphology, floral architecture and searching behaviour. Entomologia Experimentalis et Applicata 83, 21–30.CrossRefGoogle Scholar
Penvern, S, Bellon, S, Fauriel, J and Sauphanor, B (2010) Peach orchard protection strategies and aphid communities: towards an integrated agroecosystem approach. Crop Protection 29, 1148–1156.CrossRefGoogle Scholar
Péricart, J (1972) Hémipteres, Anthocoridae, Cimicidae et Microphsidae de l'ouest-paléartique. Paris: Masson Et Cie; Editeurs.Google Scholar
Pfiffner, L, Cahenzli, F, Steinemann, B, Jamar, L, Bjørn, MC, Porcel, M, Tasin, M, Telfser, J, Kelderer, M, Lisek, J and Sigsgaard, L (2019) Design, implementation and management of perennial flower strips to promote functional agrobiodiversity in organic apple orchards: a pan-European study. Agriculture, Ecosystems & Environment 278, 61–71.CrossRefGoogle Scholar
Pinheiro, LA, Torres, L, Raimundo, J and Santos, SAP (2013) Effect of floral resources on longevity and nutrient levels of Episyrphus balteatus (Diptera: Syrphidae). Biological Control 67, 178–185.CrossRefGoogle Scholar
Pizzol, J, Reynaud, P, Bresch, C, Rabasse, J, Biondi, A, Desneux, N, Parolin, P and Poncet, C (2017) Diversity of Thysanoptera species and associated host plants in Southern France. Journal of Mediterranean Ecology 15, 13–27.Google Scholar
Rodríguez-Gasol, N, Avilla, J, Aparicio, Y, Arnó, J, Gabarra, R, Riudavets, J, Alegre, S, Lordan, J and Alins, G (2019) The contribution of surrounding margins in the promotion of natural enemies in Mediterranean apple orchards. Insects 10, 148.CrossRefGoogle ScholarPubMed
Rueden, CT, Schindelin, J, Hiner, MC, DeZonia, BE, Walter, AE, Arena, ET and Eliceiri, KW (2017) ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics 18, 529.CrossRefGoogle ScholarPubMed
Shanker, C, Mohan, M, Sampathkumar, M, Lydia, C and Katti, G (2013) Selection of flowering forbs for conserving natural enemies in rice fields. Biocontrol Science and Technology 23, 480–484.CrossRefGoogle Scholar
Teulon, DAJ, Davidson, MM, Nielsen, M, Butler, R, Bosch, D, Riudavets, J and Castañé, C (2018) Efficacy of a non-pheromone semiochemical for trapping of western flower thrips in the presence of competing plant volatiles in a nectarine orchard. Spanish Journal of Agricultural Research 16, e10SC01.CrossRefGoogle Scholar
Thomson, LJ, Sharley, DJ and Hoffmann, AA (2007) Beneficial organisms as bioindicators for environmental sustainability in the grape industry in Australia. Australian Journal of Experimental Agriculture 47, 404–411.CrossRefGoogle Scholar
Trdan, S, Andjus, L, Raspudic, E and Kac, M (2005) Distribution of Aeolothrips intermedius Bagnall (Thysanoptera: Aeolothripidae) and its potential prey Thysanoptera species on different cultivated host plants. Journal of Pest Science 78, 217–226.CrossRefGoogle Scholar
Villa, M, Santos, SAP, Mexia, A, Bento, A and Pereira, JA (2017) Wildflower resources and insect honey are potential food items for Elasmus flabellatus. Agronomy for Sustainable Development 37, 15.CrossRefGoogle Scholar
Wäckers, FL (2004) Assessing the suitability of flowering herbs as parasitoid food sources: flower attractiveness and nectar accessibility. Biological Control 29, 307–314.CrossRefGoogle Scholar
Wäckers, FL (2005) Suitability of (extra-)floral nectar, pollen, and honeydew as insect food sources. In Wäckers, FL, van Rijn, PCJ and Bruin, J (eds), Plant-provided Food for Carnivorous Insects: A Protective Mutualism and Its Applications. Cambridge: Cambridge University Press, pp. 17–74.CrossRefGoogle Scholar
Wan, NF, Ji, XY, Gu, XJ, Jiang, JX, Wu, JH and Li, B (2014 a) Ecological engineering of ground cover vegetation promotes biocontrol services in peach orchards. Ecology Engineering 64, 62–65.CrossRefGoogle Scholar
Wan, NF, Ji, XY, Gu, XJ and Jiang, JX (2014 b) Testing the enemies hypothesis in peach orchards in two different geographic areas in Eastern China: the role of ground cover vegetation. PLoS One 9, 6.CrossRefGoogle ScholarPubMed
Winkler, K, Helsen, H and Devkota, BH (2007) Predatory bugs show higher abundance close to flower strips in pear orchards. Proceedings of Netherlands Entomology Society Meeting 18, 31–36.Google Scholar
Winkler, K, Wäckers, FL, Kaufman, LV, Larraz, V and van Lenteren, JC (2009) Nectar exploitation by herbivores and their parasitoids is a function of flower species and relative humidity. Biological Control 50, 299–306.CrossRefGoogle Scholar