Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-24T08:48:48.609Z Has data issue: false hasContentIssue false
  • English
  • Français

Leucopis glyphinivora Tanasijtshuk (Diptera: Chamaemyiidae), a new aphidophagous biocontrol agent; development, survival and comparison with Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae)

Published online by Cambridge University Press:  16 October 2018

S. Barriault ,
A.O. Soares Open the ORCID record for A.O. Soares [Opens in a new window] ,
S.D. Gaimari Open the ORCID record for S.D. Gaimari [Opens in a new window]  and
E. Lucas Open the ORCID record for E. Lucas [Opens in a new window]
S. Barriault*
Affiliation:
Laboratoire de Lutte Biologique, Département des Sciences Biologiques, Université du Québec à Montréal (UQAM), CP 8888, succursale Centre-Ville Montréal (Québec, CANADA) H3C 3P8, Canada
A.O. Soares
Affiliation:
cE3c – ABG – Center for Ecology, Evolution and Environmental Changes and Azorean Biodiversity Group, Faculty of Sciences and Technology, University of the Azores, 9501-801 Ponta Delgada, Portugal
S.D. Gaimari
Affiliation:
California Department of Food and Agriculture, Plant Pest Diagnostics Center, 3294 Meadowview Road, Sacramento, CA 95832-1448, USA
E. Lucas
Affiliation:
Laboratoire de Lutte Biologique, Département des Sciences Biologiques, Université du Québec à Montréal (UQAM), CP 8888, succursale Centre-Ville Montréal (Québec, CANADA) H3C 3P8, Canada
*
*Author for correspondence Phone: +1-514-987-3000 Fax: +1-514-987-4647 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The silver fly Leucopis glyphinivora Tanasijtshuk (Diptera: Chamaemyiidae) is an aphidophagous predator during its larval stage. Our study describes the life cycle of L. glyphinivora and evaluates its potential as a biocontrol agent. The development, survival and longevity of L. glyphinivora were observed and compared with those of the aphid gall midge Aphidoletes aphidimyza Rondani (Diptera: Cecidomyiidae). Tests were conducted under laboratory conditions in Petri dishes with the green peach aphid Myzus persicae Sulzer (Hemiptera: Aphididae) on potato leaves. Leucopis glyphinivora has a 42% longer life cycle than A. aphidimyza. Larval development was 27% longer in L. glyphinivora than in A. aphidimyza. Egg hatch rate and pupal emergence rate were similar in both species, but larval survival was 20% lower for L. glyphinivora than for A. aphidimyza. Sex ratio was approximately 50% in both species. A longer development time for L. glyphinivora in the larval stage could be an advantage for biocontrol by providing more time to exert predation pressure against aphids. However, this may be offset by the lower survival rate found in the silver fly larvae.

Keywords

Aphidoletes aphidimyzadevelopment cyclefurtive predatorLeucopis glyphinivoraMyzus persicaesurvival rate
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 109 , Issue 4 , August 2019 , pp. 472 - 478
Check for updates
Copyright
Copyright © Cambridge University Press 2018 

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

Alotaibi, S. (2008) Mass production and utilization of the predatory midge, Aphidoletes aphidimyza rondani for controlling aphids. Global Journal of Biotechnology & Biochemistry 3, 1–7.Google Scholar
Arnqvist, G. & Nilsson, T. (2000) The evolution of polyandry: multiple mating and female fitness in insects. Animal Behaviour 60, 145–164.Google Scholar
Bale, J.S., van Lenteren, J.C. & Bigler, F. (2008) Biological control and sustainable food production. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 363, 761–776.Google Scholar
Borges, I., Hemptinne, J.-L & Soares, A.O. (2013) Contrasting population growth parameters of the aphidophagous Scymnus nubilus and the coccidophagous Nephus reunioni. BioControl 58, 351–357.Google Scholar
Canale, A., Canova, R & Raspi, A. (2002) Leucopis glyphinivora Tanasijtshuk (Diptera Chamaemyiidae): allevameuto di iaboratorio e prove preliminari dell'influenza di temperature costanti sulla durata dello sviluppo preimmaginaie. pp. 529–533 in Atti XIX Congresso nazionale italiano di Entomologia, 10 June-15 June 2002 Catania, Academia Nazionale Italiana di Entomologia.Google Scholar
Coll, M. (1996) Feeding and ovipositing on plants by an omnivorous insect predator. Oecologia 105, 214–220.Google Scholar
Coppel, H.C & Mertins, J.W. (1977) Biological Insect Pest Suppression. New York: Springer-Verlag.Google Scholar
Devine, G.J. & Denholm, I. (2009) Insecticide and acaricide resistance. pp. 505–511 in Resh, V.H. & Cardé, R.T. (Eds) Encyclopedia of Insects. London, Elsevier Academic Press.Google Scholar
Dumont, F., Lucas, E. & Brodeur, J. (2015) Do furtive predators benefit from a selfish herd effect by living within their prey colony? Behavioral Ecology and Sociobiology 69, 971–976.Google Scholar
Elsey, K.D. (1974) Influence of plant host on searching speed of two predators. Entomophaga 19, 3–6.Google Scholar
Fox, C.W. (1993) Multiple mating, lifetime fecundity and female mortality of the bruchid beetle, Callosobruchus maculatus (Coleoptera: Bruchidae). Functional Ecology 7, 203–208.Google Scholar
Fréchette, B., Larouche, F. & Lucas, É. (2008) Leucopis annulipes larvae (Diptera: Chamaemyiidae) use a furtive predation strategy within aphid colonies. European Journal of Entomology 105, 399–403.Google Scholar
Gaimari, S.D. (2010) Chamaemyiidae. pp. 997–1007 in Brown, B.V., Borkent, A., Cumming, J.M., Wood, D.M., Woodley, N.E. & Zumbado, M. (Eds) Manual of Central American Diptera. Volume 2. Ottawa, NRC Research Press.Google Scholar
Gaimari, S.D & Turner, W.J. (1996 a) 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. Proceedings of the Washington State Entomological Society 98, 667–676.Google Scholar
Gaimari, S.D. & Turner, W.J. (1996 b) Methods for rearing aphidophagus Leucopis spp. (Diptera: Chamaemyiidae). Journal of the Kansas Entomological Society 69, 363–369.Google Scholar
Gaimari, S.D. & Turner, W.J. (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). Journal of the Kansas Entomological Society 70, 153–159.Google Scholar
García-Barros, E. (2000) Body size, egg size, and their interspecific relationships with ecological and life history traits in butterflies (Lepidoptera: Papilionoidea, Hesperioidea). Biological Journal of the Linnean Society 70, 251–284.Google Scholar
Grubin, S.M., Ross, D.W. & Wallin, K.F. (2011) Prey suitability and phenology of Leucopis spp. (Diptera: Chamaemyiidae) associated with hemlock woolly adelgid (Hemiptera: Adelgidae) in the Pacific Northwest. Environmental Entomology 40, 1410–1416.Google Scholar
Hagen, K.S., Mills, N.J., Gordh, G. & McMurtry, J.A. (1999) Terrestrial arthropod predators of insect and mite pests. pp. 383–503 in Bellows, T.S., Fisher, T.W., Caltagirone, L.E., Dahlsten, D.L., Gordh, G. & Huffaker, C.B. (Eds) Handbook of Biological Control: Principles and Applications of Biological Control. London, Elsevier Academic Press.Google Scholar
Hoddle, M.S. & Van Driesche, R.G. (2009) Biological control of insect pests. pp. 91–101 in Resh, V.H. & Cardé, R.T. (Eds) Encyclopedia of Insects. London, Elsevier Academic Press.Google Scholar
Holdsworth, R.P. (1970) Aphids and aphid enemies: effect of integrated control in an Ohio apple orchard. Journal of Economic Entomology 63, 530–535.Google Scholar
Howarth, F.G. (1991) Environmental impacts of classical biological control. Annual Review of Entomology 36, 485–509.Google Scholar
Humble, L.M. (1994) Recovery of additional exotic predators of balsam wooly adelgid, Adelges picea (Ratzeburg) (Homoptera: Adelgidae), in British Columbia. The Canadian Entomologist 126, 1101–1103.Google Scholar
Kaiser, M.E., Noma, T., Brewer, M.J., Pike, K.S., Vockeroth, J.R. & Gaimari, S.D. (2007) Hymenopteran parasitoids and dipteran predators found using soybean aphid after its Midwestern United States Invasion. Annals of the Entomological Society of America 100, 196–205.Google Scholar
Karl, I. & Fischer, K. (2008) Why get big in the cold? Towards a solution to a life-history puzzle. Oecologia 155, 215–225.Google Scholar
Kohler, G.R., Wallin, K.F. & Ross, D.W. (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. Bulletin of Entomological Research 106, 546–550.Google Scholar
Le Goff, G.J., Nicolas, A., Al Mohamad, R. & Hance, T. (2016) Impact of humidity on the biological development of Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Journal of Economic Entomology 109, 1482–1486.Google Scholar
Lucas, É & Brodeur, J. (1999) Oviposition site selection by the predatory midge Aphidoletes aphidimyza (Diptera: Cecidomyiidae). Environmental Entomology 28, 622–627.Google Scholar
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.Google Scholar
Mack, R.N., Simberloff, D., Lonsdale, W.M., Evans, H., Clout, M. & Bazzaz, F.A. (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecological Applications 10, 689–710.Google Scholar
McAlpine, J.F. (1978) A remarkable new species of Leucopis from western Canada (Diptera: Chamaemyiidae). Proceedings of the Entomological Society of Washington 79, 14–18.Google Scholar
Mohamed, A.H., Lester, P.J. & Holtzer, T.O. (2000) Abundance and effects of predators and parasitoids on the Russian wheat aphid (Homoptera: Aphididae) under organic farming conditions in Colorado. Environmental Entomology 29, 360–368.Google Scholar
Noma, T., Brewer, M.J., Pike, K.S. & Gaimari, S.D. (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.Google Scholar
Partridge, L. & Farquhar, M. (1981) Sexual activity reduces lifespan of male fruitflies. Nature 294, 580–582.Google Scholar
Paukku, S. & Kotiaho, J.S. (2005) Cost of reproduction in Callosobruchus maculatus: effects of mating on male longevity and the effect of male mating status on female longevity. Journal of Insect Physiology 51, 1220–1226.Google Scholar
Powell, W. & Pell, J.K. (2007) Biological control. pp. 469–513 in van Emden, H.F. & Harrington, R. (Eds) Aphids as Crop Pests. Wallingford, CAB International.Google Scholar
R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available online at https://www.R-project.org/.Google Scholar
Rad, S.G., 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.Google Scholar
Raspi, A. (1996) Thaumatomyia elongatula (Becker) (Chloropidae) and Leucopis annulipes Zetterstedt (Chamaemyiidae): two Diptera Preying on Phloemyzus passerinii (Signoret) (Homoptera: Philoeomyzidae) in Italy. Proceedings of the Entomological Society of Washington 98, 509–516.Google Scholar
Roff, D. (1980) Optimizing development time in a seasonal environment: the “Ups and Downs” of clinal variation. Oecologia 45, 202–208.Google Scholar
Roff, D. (1981) On being the right size. The American Naturalist 118, 405–422.Google Scholar
Ross, D.W., Gaimari, S.D., Kohler, G.R., Wallin, K.F. & Grubin, S.M. (2011) Chamaemyiid predators of the hemlock wooly adelgid from the Pacific Northwest. pp. 97–106 in Onken, B. & Reardon, R. (Eds) Implementation and Status of Biological Control of the Hemlock Woolly Adelgid. Morgantown, USDA Forest Service.Google Scholar
Satar, S., Raspi, A., Özdemir, I., Tusun, A., Karacaoğlu, M. & Benelli, G. (2015) Seasonal habits of predation and prey range in aphidophagous silver flies (Diptera chamaemyiidae), an overlooked family of biological control agents. Bulletin of Insectology 68, 173–180.Google Scholar
Sentis, A., Lucas, É & Vickery, W.L. (2012) Prey abundance, intraguild predators, ants and the optimal egg-laying strategy of a furtive predator. Journal of Insect Behavior 25, 529–542.Google Scholar
Šešlija, D. & Tucić, N. (2003) Selection for developmental time in bean weevil (Acanthoscelides obtectus): correlated responses for other life history traits and genetic architecture of line differentiation. Entomologia Experimentalis et Applicata 106, 19–35.Google Scholar
Sloggett, J.J. (2005) Are we studying too few taxa? Insights from aphidophagous ladybird beetles (Coleoptera: Coccinellidae). European Journal of Entomology 102, 391–398.Google Scholar
Sluss, T.P. & Foote, B.A. (1971) Biology and immature stages of Leucopis verticalis (Diptera: Chamaemyiidae). The Canadian Entomologist 103, 1427–1434.Google Scholar
Sluss, T.P. & Foote, B.A. (1973) Biology and immature stages of Leucopis pinicola and Chamamyia polystigma (Diptera: Chamaemyiidae). The Canadian Entomologist 105, 1443–1452.Google Scholar
Stevenson, A.B. (1967) Leucopis simplex (Diptera: Chamaemyiidae) and other species occurring in galls of Phylloxera vitifoliae (Homoptera: Phylloxeridae) in Ontario. The Canadian Entomologist 99, 815–820.Google Scholar
Stiling, P. & Cornelissen, T. (2005) What makes a successful biocontrol agent? A meta-analysis of biological control agent performance. Biological Control 34, 236–246.Google Scholar
Tanasijtshuk, V.N. (1986) Leucopis (Leucopis) glyphinivora. pp. 289–295 in Fauna of the USSR, new series 134, Dipterans. Zoological Institute of The Russian Academy of Sciences, St. Petersburg, Nauka Publishers.Google Scholar
Tanasijtshuk, V.N. (2005) Studies on Nearctic species of Leucopis (Diptera: Chamaemyiidae). III. L. annulipes zetterstedt and a new sibling species from the Nearctic. Zoosystematica Rossica 13, 281–288.Google Scholar
Tantawy, A.O. & El-Helw, M.R. (1970) Studies on Natural Populations of Drosophila. IX. Some fitness components and their heritabilities in natural and mutant populations of Drosophila melanogaster. Genetics 64, 79–91.Google Scholar
Tracewski, K.T., Johnson, P.C. & Eaton, A.T. (1984) Relative densities of predacious diptera (Diptera: Cecidomyiidae, Syrphidae, Chamaemyiidae) and their aphid prey in New Hampshire apple orchards. Protection Ecology 6, 199–207.Google Scholar
Urban, J. (2002) Occurrence, development and natural enemies of Pemphigus spyrothecae (Homoptera, Pemphigidae). Journal of Forest Science 48, 248–270.Google Scholar
van Lenteren, J.C. (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl 57, 1–20.Google Scholar
van Lenteren, J.C & Woets, J. (1988) Biological and integrated pest control in greenhouses. Annual Review of Entomology 33, 239–269.Google Scholar
van Lenteren, J.C., Bolckmans, K., Köhl, J., Ravensberg, W.J. & Urbaneja, A. (2017) Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl 63, 1–21.Google Scholar
van Schelt, J. & Mulder, S. (2000) Improved methods of testing and release of Aphidoletes aphidimyza (Diptera: Cecidomyiidae) for aphid control in glasshouses. European Journal of Entomology 97, 511–515.Google Scholar
Völkl, W., Mackauer, M., Pell, J.K. & Brodeur, J. (2007) Predators, parasitoids and pathogens. pp. 187–215 in van Emden, H.F. & Harrington, R. (Eds) Aphids as Crop Pests. Wallingford, CAB International.Google Scholar
Yukawa, J., Abe, J & Mizota, K. (2008) Improvement in the Practical Use of an Aphidophagous Gall Midge, Aphidoletes aphidimyza (Diptera: Cecidomyiidae), in Greenhouses. pp. 77–87 in Proceedings of the 3rd International Symposium on Biological Control of Aphids, 8 February–13 February 2008 Christchurch, USDA Forest Service.Google Scholar