Larval development and voracity of Eupeodes americanus (Diptera: Syrphidae): comparison of the focal prey Aphis gossypii (Hemiptera: Aphididae) and the banker prey Rhopalosiphum padi (Hemiptera: Aphididae)

Abstract

Unlike European species, the potential of Nearctic syrphids as biological control agents is still poorly studied. However, the American hoverfly, Eupeodes americanus (Wiedemann), has recently demonstrated promising traits as a biocontrol agent, notably against the foxglove aphid, Aulacorthum solani Kaltenbach, on pepper. The present study aims to extend our knowledge of the American hoverfly by evaluating its potential as a biocontrol agent in a banker plant system against the melon aphid, Aphis gossypii Glover, in a greenhouse cucumber crop. The preimaginal development and voracity of E. americanus were compared when preying upon the focal prey/pest (A. gossypii) or the banker prey (bird cherry-oat aphid, Rhopalosiphum padi L.) by daily observations of larvae from egg to adult. Preimaginal development time, survival rate, and occurrence of deformation were similar on both prey species. The weight of third instar and pupae, however, was higher for larvae that fed on the banker prey. The ad libitum voracity of the syrphid larvae was generally very high and did not significantly differ between prey species, except for the third-instar larvae which consumed more focal prey. Results suggest that a banker plant system involving the bird cherry-oat aphid may be a promising tactic for utilizing E. americanus for melon aphid biocontrol.

Keywords

american hoverfly / banker plant system / biological control / bird cherry-oat aphid / greenhouse cucumber / melon aphid

References

[1] Alhmedi,A., Haubruge, E. and Francis,F. (2008) Role of prey–host plant associations on Harmonia axyridis and Episyrphus balteatus reproduction and predatory efficiency. Entomologia Experimentalis et Applicata, 128(1), 4956.

[2] Almohamad,R., Verheggen, F.J. and Haubruge,E. (2009) Searching and oviposition behavior of aphidophagous hoverflies (Diptera: Syrphidae): a review. Biotechnologie, Agronomie, Société Et Environnement, 13(3), 467–481.

[3] Bates,D., Maechler, M., Bolker,B. and Walker,S. (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software, 67(1), 1–48.

[4] Bellefeuille,Y., Fournier, M. and Lucas,E. (2019) Evaluation of two potential biological control agents against the foxglove aphid at low temperatures. Journal of Insect Science, 19(1).

[5] Bellefeuille,Y., Fournier, M. and Lucas,E. (2021) Biological control of the foxglove aphid using a banker plant with Eupeodes americanus (Diptera: Syrphidae) in experimental and commercial greenhouses. Biological Control, 155, 1–9.

[6] Branquart,E. and Hemptinne, J.L. (2000) Development of ovaries, allometry of reproductive traits and fecundity of Episyrphus balteatus (Diptera: Syrphidae). European Journal of Entomology, 97(2), 165170.

[7] Capinera,J.L. (2000) Melon aphid or cotton aphid, Aphis gossypii Glover (Insecta: Hemiptera: Aphididae). University of Florida, Entomology and Nematology Department, 2, 14.

[8] Coppel,H.C. and Mertins, J.W. (1977) Biological Insect Pest Suppression (Vol. 4). Springer Science & Business Media.

[9] Cornelius,M. and Barlow, C.A. (1980) Effect of aphid consumption by larvae on development and reproductive efficiency of a flower fly, Syrphus corollae (Diptera: Syrphidae). The Canadian Entomologist, 112(10), 989992.

[10] Du,Y.Z. and Chen, X.Z. (1993) Influence of different aphid prey on the development of Metasyrphus corollae (Dip.: Syrphidae). Chinese Journal of Biological Control, 9(3), 111113.

[11] Dunn,L., Lequerica, M., Reid,C.R. and Latty,T. (2020) Dual ecosystem services of syrphid flies (Diptera: Syrphidae): pollinators and biological control agents. Pest Management Science, 76(6), 19731979.

[12] El-Serafi,H., Abdel-Salam, A. and Abdel-Baky,N. (2000) Effect of four aphid species on certain biological characteristics and life table parameters of Chrysoperla carnea Stephen and Chrysopa septempunctata Wesmael (Neuroptera: Chrysopidae) under laboratory conditions. Pakistan Journal of Biological Sciences, 3(2), 239245.

[13] Fischer,S. and Leger, A. (1997) Lutte biologique contre les pucerons du concombre en serre au moyen de plantes banques. Revue suisse de Viticulture Arboriculture et Horticulture, 29(2), 119–126.

[14] Frank,S.D. (2010) Biological control of arthropod pests using banker plant systems: past progress and future directions. Biological Control, 52(1), 816.

[15] Gonzalez,N., Fauteux, A., Louis,J.-C., Buitenhuis,R. and Lucas, E. (2023) Oviposition preference of the American hoverfly, Eupeodes americanus, between banker plants and target crops. Insects, 14(3).

[16] Hauge,M.S., Nielsen, F.H. and Toft,S. (1998) The influence of three cereal aphid species and mixed diet on larval survival, development and adult weight of Coccinella septempunctata. Entomologia Experimentalis et Applicata, 89(3), 319322.

[17] Hodek,I. (1993) Habitat and food specificity in aphidophagous predators. Biocontrol Science and Technology, 3(2), 91100.

[18] Hodek,I. and Evans, E.W. (2012) Food relationships. Ecology and Behaviour of the Ladybird Beetles (Coccinellidae), p. 141274. John Wiley & Sons, Ltd.

[19] Honěk,A. (1993) Intraspecific variation in body size and fecundity in insects: a general relationship. Oikos, 66(3), 483.

[20] Huang,N., Enkegaard, A., Osborne,L.S., Ramakers,P.M.J., Messelink, G.J., Pijnakker,J., et al. (2011) The banker plant method in biological control. Critical Reviews in Plant Sciences, 30(3), 259278.

[21] Jiang,S., Li,H., He,L. and Wu, K. (2022) Population fitness of Eupeodes corollae Fabricius (Diptera: Syrphidae) feeding on different species of aphids. Insects, 13(6), 494.

[22] Josephat,P.,K. and Ame, A. (2018) Effect of testing logistic regression assumptions on the improvement of the propensity scores. International Journal of Statistics and Applications, 8(1), 917.

[23] Laubertie,E.A., Wratten, S.D. and Hemptinne,J.-L. (2012) The contribution of potential beneficial insectary plant species to adult hoverfly (Diptera: Syrphidae) fitness. Biological Control, 61(1), 16.

[24] Length,R.V. (2022) Emmeans: estimated marginal means, aka least-squares means. R package version 1.7.2.

[25] Liu,T.-X. and Chen, T.-Y. (2001) Effects of three aphid species (Homoptera: Aphididae) on development, survival and predation of Chrysoperla carnea (Neuroptera: Chrysopidae). Applied Entomology and Zoology, 36(3), 361366.

[26] Manzaroli,G. and Van Lenteren, J.C. (1999) Evaluation and use of predators and parasitoids for biological control of pests in greenhouses. Integrated Pest and Disease Management in Greenhouse Crops (eds. R.Albajes, M.Lodovica Gullino, J. C. van Lenteren, & Y. Elad), Vol. 14, p. 183201. Springer, Netherlands.

[27] Messelink,G.J., Calvo,F.J., Marín,F. and Janssen,D. (2020) Cucurbits. Integrated Pest and Disease Management in Greenhouse Crops (eds. M. L.Gullino, R.Albajes, & P. C.Nicot), p. 537566. Springer International Publishing.

[28] Miller,T.L.P. and Rebek, E.J. (2018) Banker plants for aphid biological control in greenhouses. Journal of Integrated Pest Management, 9(1).

[29] Omkar and Srivastava, S. (2003) Influence of six aphid prey species on development and reproduction of a ladybird beetle, Coccinella septempunctata. BioControl, 48(4), 379393.

[30] Pekas,A., De Craecker, I., Boonen,S., Wäckers,F.L. and Moerkens, R. (2020) One stone; two birds: concurrent pest control and pollination services provided by aphidophagous hoverflies. Biological Control, 149, 16.

[31] Pineda,A. and Ángeles Marcos-García, M. (2008) Introducing barley as aphid reservoir in sweet-pepper greenhouses: Effects on native and released hoverflies (Diptera: Syrphidae). European Journal of Entomology, 105(3), 531535.

[32] Prado,S.G., Jandricic, S.E. and Frank,S.D. (2015) Ecological interactions affecting the efficacy of Aphidius colemani in greenhouse crops. Insects, 6(2), 538575.

[33] Putra,N.S. and Yasuda, H. (2006) Effects of prey species and its density on larval performance of two species of hoverfly larvae, Episyrphus balteatus de Geer and Eupeodes corollae Fabricius (Diptera: Syrphidae). Applied Entomology and Zoology, 41(3), 389397.

[34] R Core Team. (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.

[35] Rodríguez-Gasol,N., Alins,G., Veronesi, E.R. and Wratten,S. (2020) The ecology of predatory hoverflies as ecosystem-service providers in agricultural systems. Biological Control, 151, 104405.

[36] Rojo,S., Gilbert, F., Marcos-García,M.A., Nieto,J.M. and Mier Durante,M.P. (2003) A World Review of Predatory Hoverflies (Diptera, Syrphidae: Syrphinae) and Their Prey. CIBIO Ediciones, Universidad de Alicante, Alicante, Spain.

[37] Rosagro,R.M., Borges, I., Vieira,V., SoléG.P. and Soares, A.O. (2020) Evaluation of Scymnus nubilus (Coleoptera: Coccinellidae) as a biological control agent against Aphis spiraecola and Cinara juniperi (Hemiptera: Aphididae). Pest Management Science, 76(2), 818826.

[38] Rüzička,Z. (1975) The effects of various aphids as larval prey on the development of Metasyrphus corollae [Dipt.: Syrphidae]. Entomophaga, 20(4), 393402.

[39] Sadeghi,H. and Gilbert, F. (2000) Aphid suitability and its relationship to oviposition preference in predatory hoverflies. Journal of Animal Ecology, 69(5), 771784.

[40] Scott,S.M. and Barlow, C.A. (1984) Effect of prey availability during development on the reproductive output of Metasyrphus corollae (Diptera: Syrphidae). Environmental Entomology, 13(3), 669674.

[41] Sebastião,D., Borges, I. and Soares,A.O. (2015) Effect of temperature and prey in the biology of Scymnus subvillosus. BioControl, 60(2), 241249.

[42] Short,B.D. and Bergh, J.C. (2004) Feeding and egg distribution studies of Heringia calcarata (Diptera: Syrphidae), a specialized predator of woolly apple aphid (Homoptera: Eriosomatidae) in Virginia apple orchards. Journal of Economic Entomology, 97(3), 813819.

[43] Skevington,J.H., Locke,M.M., Young,A.D., Moran, K., Crins,W.J. and Marshall,S.A. (2019) Field Guide to the Flower Flies of Northeastern North America. Princeton University Press, p. 512.

[44] Soares,O.A., Coderre, D. and Schanderl,H. (2005) Influence of prey quality on the fitness of two phenotypes of Harmonia axyridis adults. Entomologia Experimentalis et Applicata, 114(3), 227232.

[45] Tenhumberg,B. (1995) Syrphids as natural enemies of cereal aphids in Germany: aspects of their biology and efficacy in different years and regions. Agriculture, Ecosystems & Environment, 52(1), 3943.

[46] Vacante,V. and Kreiter, S. (Éds.). (2018) Handbook of Pest Management in Organic Farming. CABI, Boston Wallingford.

[47] Van Oystaeyen,A., Tuyttens, E., Boonen,S., De Smedt,L., Bellinkx, S., Wäckers,F., et al. (2022) Dual purpose: predatory hoverflies pollinate strawberry crops and protect them against the strawberry aphid, Chaetospihon fragaefolii. Pest Management Science, 78(7), 30513060.

[48] van Rijn,P.C.J., Kooijman, J. and Wäckers,F.L. (2013) The contribution of floral resources and honeydew to the performance of predatory hoverflies (Diptera: Syrphidae). Biological Control, 67(1), 3238.

[49] Vanhaelen,N., Gaspar, C. and Francis,F. (2002) Influence of prey host plant on a generalist aphidophagous predator: Episyrphus balteatus (Diptera: Syrphidae). European Journal of Entomology, 99(4), 561564.

[50] Verheggen,F., Capella, Q., Schwartzberg,E., Voigt,D. and Haubruge, E. (2009) Tomato-aphid-hoverfly: a tritrophic interaction incompatible for pest management. Arthropod-Plant Interactions, 3, 141149.

[51] Vosteen,I., Gershenzon, J. and Kunert,G. (2018) Dealing with food shortage: larval dispersal behaviour and survival on non-prey food of the hoverfly Episyrphus balteatus. Ecological Entomology, 43(5), 578590.

[52] Whittingham,J. (1991) The effect of size, adult nutrition and flight on longevity and fecundity of a hoverfly, Eupeodes corollae (Fab.) (Diptera: Syrphidae). Thesis submitted to the faculty of graduate Studies and Research in partial fulfilment of the requirements for the degree of Master of Science, p. 77. Carleton University.

[53] Yano,E. (2019) Functions of banker plants for biological control of arthropod pests in protected culture. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources, 14(006).

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