Abstract
The silver fly Leucopis glyphinivora Tanasijtshuk (Diptera: Chamaemyiidae) is an aphidophagous predator during its larval stage. Few studies have examined the predation habits of this species for biological control. Larval voracity of L. glyphinivora was measured under laboratory and controlled greenhouse conditions and compared with a commercially available biocontrol agent, Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae). Laboratory tests were conducted in Petri dishes using Myzus persicae Sulzer (Hemiptera: Aphididae) on potato leaves. In greenhouse tests, predator voracity was evaluated with various plant-aphid treatments. In the laboratory, silver fly larvae consumed 39% more aphids than A. aphidimyza throughout their larval development. In the greenhouse, L. glyphinivora consumed more aphids than A. aphidimyza regardless of treatment. The highest voracities were obtained on tomato and bell pepper infested with M. persicae. No antagonistic predatory effects were observed when predators were used together. This study provides useful insight on L. glyphinoivora as an efficient aphid predator but more research is needed to establish its potential for biological control.
Similar content being viewed by others
References
Alotaibi S (2008) Mass production and utilization of the predatory midge, Aphidoletes aphidimyza Rondani for controlling aphids. Global J Biotech Biochem 3:1–7
Barriault S, Soares AO, Gaimari SD, Lucas E (2018) Leucopis glyphinivora Tanasijtshuk (Diptera: Chamaemyiidae), a new aphidophagous biocontrol agent; development, survival and comparison with Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae). Bull Entomol Res. https://doi.org/10.1017/S0007485318000767
Begum M, Lees E, Ampt P, Mansfield S (2017) Development of Australian commercial producers of invertebrate biological control agents from 1971 to 2014. BioControl 62:525–533
Blackman RL, Eastop VF (2007) Taxonomic issues. In: van Emden HF, Harrington R (eds) Aphids as crop pests. CAB International, London, pp 1–29
Bokina IG (2009) The influence of vegetation on the abundance of cereal aphid entomophages in the forest-steppe of western Siberia. Entomol Rev 89:757–769
Brewer MJ, Elliott NC (2004) Biological control of cereal aphids in North America and mediating effects of host plant and habitat manipulations. Annu Rev Entomol 49:219–242
Brewer MJ, Noma T (2010) Habitat affinity of resident natural enemies of the invasive Aphis glycines (Hemiptera: Aphididae), on soybean, with comments on biological control. J Econ Entomol 103:583–596
Burgio G, Santi F, Maini S (2002) On intra-guild predation and cannibalism in Harmonia axyridis (Pallas) and Adalia bipunctata L. (Coleoptera: Coccinellidae). Biol Control 24:110–116
Cabral S, Soares AO, Garcia P (2009) Predation by Coccinella undecimpunctata L. (Coleoptera: Coccinellidae) on Myzus persicae Sulzer (Homoptera: Aphididae): effect of prey density. Biol Control 50:25–29
Canale A, Canova R, Raspi A (2002) Leucopis glyphinivora Tanasijtshuk (Diptera Chamaemyiidae): allevamento di laboratorio e prove preliminari dell’influenza di temperature costanti sulla durata dello sviluppo preimmaginale. Atti XIX Congresso nazionale italiano di Entomologia pp 529–533
Carroll DP, Hoyt SC (1984) Natural enemies and their effects on apple aphid, Aphis pomi DeGeer (Homoptera: Aphididae), colonies on young apple trees in central Washington. Environ Entomol 13:469–481
Colares F, Michaud JP, Bain CL, Torres JB (2015) Recruitment of aphidophagous arthropods to sorghum plants infested with Melanaphis sacchari and Schizaphis graminum (Hemiptera: Aphididae). Biol Control 90:16–24
Coppel HC, Mertins JW (1977) Biological insect pest suppression. Springer, New York, pp 234–255
Dixon AFG (1959) An experimental study of the searching behaviour of the predatory coccinellid beetle. J Anim Ecol 28:259–281
Dumont F, Lucas E, Brodeur J (2015) Do furtive predators benefit from a selfish herd effect by living within their prey colony? Behav Ecol Sociobiol 69:971–976
Fréchette B, Larouche F, Lucas É (2008) Leucopis annulipes larvae (Diptera: Chamaemyiidae) use a furtive predation strategy within aphid colonies. Eur J Entomol 105:399–403
Gaimari SD, Turner WJ (1996a) Larval feeding and development of Leucopis ninae Tanasijtshuk and two populations of Leucopis gaimarii Tanasijtshuk (Diptera: Chamaemyiidae) on Russian wheat aphid, Diuraphis noxia (Mordvilko) (Homoptera: Aphididae), in Washington. Proc Entomol Soc Wash 98:667–676
Gaimari SD, Turner WJ (1996b) Methods for rearing Aphidophagous Leucopis spp. (Diptera: Chamaemyiidae). J Kansas Entomol Soc 69:363–369
Gaimari SD, Turner WJ (1997) Behavioral observations on the adults and larvae of Leucopis ninai and L. gaimarii (Diptera: Chamaemyiidae), predators of Russian wheat aphid, Diuraphis noxia (Homoptera: Aphididae). J Kansas Entomol Soc 70:153–159
Griffin ML, Yeargan V (2002) Factors potentially affecting oviposition site selection by the lady beetle Coleomegilla maculata (Coleoptera: Coccinellidae). Environ Entomol 31:112–119
Hindayana D, Meyhofer R, Scholz D, Poehling HM (2001) Intraguild predation among the hoverfly Episyrphus balteatus de Geer (Diptera: Syrphidae) and other aphidophagous predators. Biol Control 20:236–246
Hoddle MS, van Driesche RG (2009) Biological control of insect pests. In: Resh VH, Cardé RT (eds) Encyclopedia of insects, 2nd edn. Elsevier, Burlington, pp 91–101
Humble LM (1994) Recovery of additional exotic predators of balsam wooly adelgid, Adelges picea (Ratzeburg) (Homoptera: Adelgidae), in British Columbia. Can Entomol 126:1101–1103
Kahanpää J (2014) Checklist of the fly families Chamaemyiidae and Lauxaniidae of Finland (Insecta, Diptera). ZooKeys 441:277–283
Kaiser ME, Noma T, Brewer MJ, Pike KS, Vockeroth JR, Gaimari SD (2007) Hymenopteran parasitoids and dipteran predators found using soybean aphid after its Midwestern United States invasion. Ann Entomol Soc Am 100:196–205
Katayama N, Suzuki N (2003) Bodyguard effects for aphids of Aphis craccivora Koch (Homoptera: Aphididae) as related to the activity of two ant species, Tetramorium caespitum Linnaeus (Hymenoptera: Formicidae) and Lasius niger L. (Hymenoptera: Formicidae). Appl Entol Zool 38:427–433
Kohler GR, Wallin KF, Ross DW (2016) Seasonal phenology and abundance of Leucopis argenticollis, Leucopis piniperda (Diptera: Chamaemyiidae), Laricobius nigrinus (Coleoptera: Deridontidae) and Adelges tsugae (Hemiptera: Adelgidae) in the Pacific Northwest USA. B Entomol Res 106:546–550
Latham DR, Mills NJ (2010) Quantifying aphid predation: the mealy plum aphid Hyalopterus pruni in California as a case study. J Appl Ecol 47:200–208
Le Goff GJ, Nicolas A, Al Mohamad R, Hance T (2016) Impact of humidity on the biological development of Aphidoletes aphidimyza (Diptera: Cecidomyiidae). J Econ Entomol 109:1482–1486
Lucas É (2005) Intraguild predation among aphidophagous predators. Eur J Entomol 102:351–364
Lucas É, Brodeur J (1999) Oviposition site selection by the predatory midge Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Environ Entomol 28:622–627
Lucas É, Brodeur J (2001) A Fox in sheep’s clothing: furtive predators benefit from the communal defense of their prey. Ecology 82:3246–3250
Lucas É, Coderre D, Brodeur J (1998) Intraguild predation among aphid predators: characterization and influence of extraguild prey density. Ecology 79:1084–1092
MacGillivray ME, Anderson GB (1957) Three useful insect cages. Can Entomol 89:43–46
Malais MH, Ravensberg WJ (2006) Les pucerons et leurs ennemis naturels. Connaître et reconnaître : la biologie des ravageurs des serres et de leurs ennemis naturels. Koppert B.V, Berkel en Rodenrijs, pp 131–172
Marks RJ (1977) Laboratory studies of plant searching behaviour by Coccinella septempunctata L. larvae. Bull Entomol Res 67:235–241
McAlpine JF (1978) A remarkable new species of Leucopis from western Canada (Diptera: Chamaemyiidae). Proc Entomol Soc Wash 79:14–18
McLean IFG (1992) Behaviour of larval and adult Leucopis (Diptera: Chamaemyiidae). Br J Ent Nat Hist 5:35–36
Mehrparvar M, Mansouri SM, Hatami B (2016) Some bioecological aspects of the rose aphid, Macrosiphum rosae (Hemiptera: Aphididae) and its natural enemies. Acta Univ Sap Agr Environ 8:74–88
Messelink GJ, Bloemhard CMJ, Cortes JA, Sabelis MW, Janssen A (2011) Hyperpredation by generalist predatory mites disrupts biological control of aphids by the aphidophagous gall midge Aphidoletes aphidimyza. Biol Control 57:246–252
Messelink GJ, Bloemhard CMJ, Sabelis MW, Janssen A (2013) Biological control of aphids in the presence of thrips and their enemies. BioControl 58:45–55
Messelink GJ, Bloemhard CMJ, Hoogerbrugge H, van Schelt J, Ingegno BL, Tavella L (2015) Evaluation of mirid predatory bugs and release strategy for aphid control in sweet pepper. J Appl Entomol 139:333–341
Miller RL (1928) Biology and natural control of the green citrus aphid Aphis spiraecola Patch. Fla Entomol 12:49–56
Mohamed AH, Lester PJ, Holtzer TO (2000) Abundance and effects of predators and parasitoids on the Russian wheat aphid (Homoptera: Aphididae) under organic farming conditions in Colorado. Environ Entomol 29:360–368
Mustaţă G, Mustaţă M, Andriev S-O, Prelipcean C (2010) The complex of predators controlling the colonies of Aphis fabae Scop. (Homoptera, Aphididae) in eastern Romania. Analele Ştiinţifice ale Universităţii”Al. I. Cuza” Iaşi, s. Biologie animală 56:97–100
Natshuk EP, Bagachanova AK (2013) Silver-flies (Diptera, Chamaemyiidae) of Yakutia, Russia. Eur Entomol J 12:70–78
Noma T, Brewer MJ, Pike KS, Gaimari SD (2005) Hymenopteran parasitoids and dipteran predators of Diuraphis noxia in the west-central Great Plains of North-America: species records and geographic range. BioControl 50:11–97
Osawa N (1992) A life table of the ladybird beetle Harmonia axyridis Pallas (Coleoptera, Coccinellidae) in relation to the aphid abundance. Jpn J Ent 60:575–579
Polis GA, Myers CA, Holt RD (1989) The ecology and evolution of intraguild predation: potential competitors that eat each other. Annu Rev Ecol Syst 20:297–330
Powell W, Pell JK (2007) Biological control. In: van Emden HF, Harrington R (eds) Aphids as crop pests. CAB International, Wallingford, pp 469–513
Preisser EL, Oten KLF, Hain FP (2014) Hemlock woolly adelgid in the eastern United States: what have we learned? Southeast Nat 13:1–15
R Core Team (2016) R: A language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. URL https://www.r-project.org/
Rad SG, Hatami B, Asadi G (2003) Biology of Leucopis glyphinivora Tanas. (Dip.: Chamaemyiidae) and its efficiency in biological control of Aphis fabae Scop. JWSS 6:195–207
Rakhshani H, Ebadi R, Hatami B, Rakhshani E, Gharali B (2010) A survey of alfalfa aphids and their natural enemies in Isfahan, Iran, and the effect of alfalfa strip-harvesting on their populations. J Entomol Soc Iran 30:13–28
Raspi A, Ebejer MJ (2008) New records of Diptera Chamaemyiidae from the Mediterranean and Oman with a description of a new species: Parochthiphila (Euestelia) argentiseta from Turkey and a redescription of Parochthiphila (Parochthiphila) inconstans (Becker). Entomol Fennica 19:55–64
Rosenheim JA, Wilhoit LR, Armer CA (1993) Influence of intraguild predation among generalist insect predators on the suppression of an herbivore population. Oecologia 96:439–449
Satar S, Raspi A, Özdemir I, Tusun A, Karacaoğlu M, Beneli G (2015) Seasonal habits of predation and prey range in aphidophagous silver flies (Diptera chamaemyiidae), an overlooked family of biological control agents. Bull Insectol 68:173–180
Sentis A, Lucas É, Vickery WL (2012) Prey abundance, intraguild predators, ants and the optimal egg-laying strategy of a furtive predator. J Insect Behav 25:529–542
Sloggett JJ (2005) Are we studying too few taxa? Insights from aphidophagous ladybird beetles (Coleoptera: Coccinellidae). Eur J Entomol 102:391–398
Soares AO, Coderre D, Schanderl H (2001) Fitness of two phenotypes of Harmonia axyridis (Coleoptera: Coccinellidae). Eur J Entomol 98:287–293
Soares AO, Coderre D, Schanderl H (2003) Effect of temperature and intraspecific allometry on predation by two phenotypes of Harmonia axyridis Pallas (Coleoptera: Coccinellidae). Environ Entomol 35:939–944
Soluk DA (1993) Multiple predator effects: predicting combined functional response of stream fish and invertebrate predators. Ecology 74:219–225
Sorensen JT (2009) Aphids. In: Resh VH, Cardé RT (eds) Encyclopedia of insects, 2nd edn. Elsevier, Burlington, pp 27–31
Stevenson AB (1967) Leucopis simplex (Diptera: Chamaemyiidae) and other species occurring in galls of Phylloxera vitifoliae (Homoptera: Phylloxeridae) in Ontario. Can Entomol 99:815–820
Stewart-Jones A, Pope TW, Fitzgerald JD, Poppy GM (2008) The effect of ant attendance on the success of rosy apple aphid populations, natural enemy abundance and apple damage in orchards. Agr Forest Entomol 10:37–43
Stiling P, Cornelissen T (2005) What makes a successful biocontrol agent? A meta-analysis of biological control agent performance. Biol Control 34:236–246
Tanasijtshuk VN (1986) Leucopis (Leucopis) glyphinivora. Fauna of the USSR. Nauka Publishers, St. Petersburg, pp 289–295
van Lenteren JC, Woets J (1988) Biological and integrated pest control in greenhouses. Ann Rev Entomol 33:239–269
van Lenteren JC, Bolckmans K, Köhl J, Ravensberg WJ, Urbaneja A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl 63:39–59
van Schelt J, Mulder S (2000) Improved methods of testing and release of Aphidoletes aphidimyza (Diptera: Cecidomyiidae) for aphid control in glasshouses. Eur J Entomol 97:511–515
Völkl W, Mackauer M, Pell JK, Brodeur J (2007) Predators, parasitoids and pathogens. In: van Emden HF, Harrington R (eds) Aphids as crop pests. CAB International, London, pp 187–233
Wallace MS, Hain FP (2000) Field surveys and evaluation of native and established predators of the hemlock woolly adelgid (Homoptera: Adelgidae) in the southeastern United States. Environ Entomol 29:638–644
Wilbert H (1973) Zur Suchfähigkeit der Eilarven von Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Entomol Exp Appl 16:514–524
Yukawa J, Abe J, Mizota K (2008) Improvement in the practical use of an aphidophagous gall midge, Aphidoletes aphidimyza (Diptera: Cecidomyiidae), in greenhouses. In: Mason PG, Gillespie DR, Vincent C (eds) Proceedings of the third international symposium on biological control of aphids. Christchurch, pp 77–87
Zhou H, Yu Y, Tan X, Chen A, Feng J (2014) Biological control of insect pests in apple orchards in China. Biol Control 68:47–56
Acknowledgements
Our deepest thanks go out to Stephen D. Gaimari, California Department of Food and Agriculture, for identification and rearing advice with Leucopis glyphinivora. We would like to extend our gratitude to Jill Vandermeerschen for her help with statistical analysis, Simon Chaussé and Tina Lévesque for technical assistance and the team at LUFA, particularly Javier Campos and Lauren Rathmell. We would also like to thank the Natural Sciences and Engineering Research Council of Canada (NSERC) and the Ministère de l’Agriculture des Pêcheries et de l’Alimentation du Québec (MAPAQ), through their Programme de Soutien à l’Innovation Horticole (PSIH), for funding this research project.
Author information
Authors and Affiliations
Corresponding author
Additional information
Handling Editor: Patrick De Clercq.
Rights and permissions
About this article
Cite this article
Barriault, S., Fournier, M., Soares, A.O. et al. Leucopis glyphinivora, a potential aphidophagous biocontrol agent? Predation and comparison with the commercial agent Aphidoletes aphidimyza. BioControl 64, 21–31 (2019). https://doi.org/10.1007/s10526-018-09909-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10526-018-09909-x