Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-27T11:19:19.589Z Has data issue: false hasContentIssue false
  • English
  • Français

Flying with a ‘death sentence’ on board: electrophoretic detection of braconid parasitoid larvae in migrating winged grain aphids, Sitobion avenae (F.)

Published online by Cambridge University Press:  04 February 2011

M.P. Walton ,
H.D. Loxdale  and
L.J. Allen-Williams
M.P. Walton
Affiliation:
Department of Biosciences, University of Hertfordshire, Hatfield, Hertfordshire, AL10 9AB, UK Plant & Invertebrate Ecology Division, Rothamsted Research, Harpenden, Hertfordshire, AL5 2JQ, UK
H.D. Loxdale*
Affiliation:
Institute of Ecology, Friedrich-Schiller-University, Dornburger Strasse 159, 07743 Jena, Germany
L.J. Allen-Williams
Affiliation:
Department of Biosciences, University of Hertfordshire, Hatfield, Hertfordshire, AL10 9AB, UK
*
*Authors for correspondence Fax: +49 3641 949 402 E-mail: Hugh.Loxdale@uni-jena.de
Get access Rights & Permissions [Opens in a new window]

Abstract

Polyacrylamide gel electrophoresis of enzymes (carboxylesterases) was used for the first time to monitor rates of parasitism in airborne alate (winged) grain aphid, Sitobion avenae (F.) population samples collected by suction trapping in Hertfordshire, UK. Using previously described electrophoretic ‘keys’, the species of hymenopterous parasitoids present in individual aphids were identified and found to be Aphidius ervi (Haliday) and/or Aphidius rhopalosiphi (De Stephani Perez) (Braconidae). Entomophthoralean fungal infection was also detected using this approach. Aphidiid wasp parasitism was detected from early June to mid-August and fungal infection from late June to late July. The results are discussed in relation to parasitoid population structure and dynamics, especially (i) the fact that winged aphids passively transport the early stages of their braconid parasitoids and fungal pathogens, potentially to newly-founded colonies, which may directly impact on the dual aphid-parasitoid populations genetics; and (ii) the approach used to collect and assay parasitised and fungal infected aphids involving both suction trapping and electrophoretic testing may have potential in assessing the level and efficacy of these biological control agents in integrated pest management (IPM) schemes to combat cereal aphid outbreaks.

Keywords

aphidhymenopterous wasp parasitoidgel electrophoresispercentage parasitismpassive transportintegrated pest management
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 101 , Issue 4 , August 2011 , pp. 443 - 449
Copyright
Copyright © Cambridge University Press 2011

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

Anon (1988) Rothamsted Experimental Station, Report for 1987. Parts 1 and 2.Google Scholar
Carter, N., McLean, I.F.G., Watt, A.D. & Dixon, A.F.G. (1980) Cereal aphids: a case study. Applied Biology 5, 271–348.Google Scholar
Castañera, P., Loxdale, H.D. & Nowak, K. (1983) Electrophoretic study of enzymes from cereal aphid populations. II. Use of electrophoresis for identifying Aphidiid parasitoids (Hymenoptera) of Sitobion avenae (F.) (Hemiptera: Aphididae). Bulletin of Entomological Research 73, 659–665.CrossRefGoogle Scholar
Chua, T.H. (1977) Population studies of Brevicoryne brassicae (L.), its parasites and hyperparasites in England. Researches on Population Ecology 19, 125–139.CrossRefGoogle Scholar
Dean, G., Dewar, A.M., Powell, W. & Wilding, N. (1980) Integrated control of cereal aphids. IOBC Bulletin (WPRS) 3 (1980), 30–47.Google Scholar
Dean, G.J. (1974) Effects of parasites and predators on cereal aphids Metopolophium dirhodum (wlk.) and Macrosiphum avenae (F.) (Hem., Aphididae). Bulletin of Entomological Research 63, 411–422.CrossRefGoogle Scholar
Dean, G.J. (1978) Observations on the morphs of Macrosiphum avenae and Metopolophium dirhodum on cereals during summer and autumn. Annals of Applied Biology 89, 1–7.CrossRefGoogle Scholar
Dean, G.J. & Luuring, B.B. (1970) Distribution of aphids in cereal crops. Annals of Applied Biology 66, 485–496.CrossRefGoogle Scholar
Dean, G.J.W. & Wilding, N. (1971) Entomophthora infecting cereal aphids Metopolophium dirhodum and Sitobion avenae. Journal of Invertebrate Pathology 18, 169–176.CrossRefGoogle Scholar
Dean, G.J.W. & Wilding, N. (1973) Infection of cereal aphids by fungus Entomophthora. Annals of Applied Biology 74, 133–138.CrossRefGoogle Scholar
Feng, M.G., Chen, C., Shang, S.W., Ying, S.H., Shen, Z.C. & Chen, X.X. (2007) Aphid dispersal flight disseminates fungal pathogens and parasitoids as natural control agents of aphids. Ecological Entomology 32, 97–104.CrossRefGoogle Scholar
Force, D.C. & Messenger, P.S. (1968) Use of laboratory studies of three hymenopterous parasites to evaluate their field potential. Journal of Economic Entomology 61, 1374–1378.CrossRefGoogle Scholar
Gair, R. (1981) A review of cereal pests in the United Kingdom. Proceedings 1981 British Crop Protection Conference. Pests and Diseases 3, 779–785.Google Scholar
Gardner, S.M. (1982) The ecology and behaviour of Aphidius rhopalosiphi. PhD thesis, University of East Anglia, Norwich, UK.Google Scholar
Greenstone, M.H. (2006) Molecular methods for assessing insect parasitism. Bulletin of Entomological Research 96, 1–13.CrossRefGoogle ScholarPubMed
Höller, C. (1990) Overwintering and hymenopterous parasitism in autumn of the cereal aphid Sitobion avenae (F.) in northern FR Germany. Zeitschrift für Angewandte Entomologie 109, 21–28.Google Scholar
Hopper, K.R., Roush, R.T. & Powell, W. (1993) Management of genetics of biological-control introductions. Annual Review of Entomology 38, 27–51.CrossRefGoogle Scholar
Huang, Z.H., Feng, M.G., Chen, X.X. & Liu, S.S. (2008) Pathogenic fungi and parasitoids of aphids present in air captures of migratory alates in the low-latitude plateau of Yunnan, China. Environmental Entomology 37, 1264–1271.CrossRefGoogle ScholarPubMed
Jackson, H.B., Coles, L.W., Wood, E.A. & Eikenbary, R.D. (1970) Parasites reared from greenbug and corn leaf aphid in Oklahoma in 1968 and 1969. Journal of Economic Entomology 63, 733–736.CrossRefGoogle Scholar
Johnson, B. (1959) Effect of parasitisation by Aphidius platensis Brèthes on developmental physiology of its host Aphis craccivora Koch. Entomologia Experimentalis et Applicata 2, 82–99.CrossRefGoogle Scholar
Johnson, C.G. (1954) Aphid migration in relation to weather. Biological Reviews 29, 87–118.CrossRefGoogle Scholar
Jones, M. & Dean, G.J. (1975) Observations on cereal aphids and their natural enemies in 1972. Entomologist's Monthly Magazine 111, 69–77.Google Scholar
Kelly, E.O.G. (1917) The Greenbug (Toxoptera graminum Rond.) outbreak of 1916. Journal of Economic Entomology 10, 233–248.CrossRefGoogle Scholar
Legrand, M.A., Colinet, H., Vernon, P. & Hance, T. (2004) Autumn, winter and spring dynamics of aphid Sitobion avenae and parasitoid Aphidius rhopalosiphi interactions. Annals of Applied Biology 145, 139–144.CrossRefGoogle Scholar
Loxdale, H.D. & Lushai, G. (1998) Molecular markers in entomology. Bulletin of Entomological Research 88, 577–600.CrossRefGoogle Scholar
Loxdale, H.D., Castañera, P. & Brookes, C.P. (1983) Electrophoretic study of enzymes from cereal aphid populations. I. Electrophoretic techniques and staining systems for characterising isoenzymes from six species of cereal aphids (Hemiptera: Aphididae). Bulletin of Entomological Research 73, 645–657.CrossRefGoogle Scholar
Lumbierres, B., Starý, P. & Pons, X. (2007) Seasonal parasitism of cereal aphids in a Mediterranean arable crop system. Journal of Pesticide Science 80, 125–130.Google Scholar
Lushai, G., Markovitch, O. & Loxdale, H.D. (2002) Host-based genotype variation in insects revisited. Bulletin of Entomological Research 92, 159–164.CrossRefGoogle ScholarPubMed
Macaulay, E.D.M., Tatchell, G.M. & Taylor, G.M. (1988) The Rothamsted insect survey 12-metre suction trap. Bulletin of Entomological Research 78, 121–129.CrossRefGoogle Scholar
Nyabuga, F.N., Loxdale, H.D., Heckel, D.G. & Weisser, W.W. (2010) Spatial population dynamics of a specialist aphid parasitoid, Lysiphlebus hirticornis Mackauer (Hymenoptera: Braconidae: Aphidiinae): evidence for philopatry and restricted dispersal. Heredity 105, 433–442.CrossRefGoogle ScholarPubMed
Pennacchio, F., Digilio, M.C., Tremblay, E. & Tranfaglia, A. (1994) Host recognition and acceptance behaviour in two aphid parasitoid species: Aphidius ervi Haliday and Aphidius microlophii Pennacchio & Tremblay (Hymenoptera, Braconidae). Bulletin of Entomological Research 84, 57–64.CrossRefGoogle Scholar
Plumb, R.T. (1971) The control of insect-transmitted viruses of cereals. Proceedings 6th British Insecticide and Fungicide Conference 1, 307–313.Google Scholar
Plumb, R.T. (1976) Barley yellow dwarf virus control on cereals. Annals of Applied Biology 83, 53–59.CrossRefGoogle Scholar
Powell, W. (1982) The identification of hymenopterous parasitoids attacking cereal aphids in Britain. Systematic Entomology 7, 465–473.CrossRefGoogle 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, Oxford, CABI.CrossRefGoogle Scholar
Powell, W. & Wright, A.F. (1988) The abilities of the aphid parasitoids Aphidius ervi Haliday and A. rhopalosiphi De Stephani Perez (Hymenoptera, Braconidae) to transfer between different known host species and the implications for the use of alternative hosts in pest-control strategies. Bulletin of Entomological Research 78, 683–693.CrossRefGoogle Scholar
Powell, W., Wilding, N., Brobyn, P.J. & Clark, S.J. (1986) Interference between parasitoids [Hym, Aphidiidae] and fungi [Entomophthorales] attacking cereal aphids. Entomophaga 31, 293–302.CrossRefGoogle Scholar
Rabasse, J.M. & Dedryver, C.A. (1983) Overwintering of primary parasites and hyperparasites of cereal aphids in western France. pp. 57–64 in Cavalloro, R. (Ed.) Aphid Antagonists, Rotterdam, A.A. Balkema.Google Scholar
Robert, Y. (1979) Ecological researches on the aphids Aulocorthum solani Ktlb., Macrosiphum euphorobiae Thomas and Myzus persicae Sulz. in the west of France. 3. Importance of parasitism by Aphidiidae and Entomophthora on potato. Annales de Zoologie – Ecologie Animale 11, 371–388.Google Scholar
Shirota, Y., Carter, N., Rabbinge, R. & Ankersmit, G.W. (1983) Biology of Aphidius rhopalosiphi, a parasitoid of cereal aphids. Entomologia Experimentalis et Applicata 34, 27–34.CrossRefGoogle Scholar
Starý, P. (1972) Host range of parasites and ecosystem relations, a new viewpoint in multilateral control concept (Homoptera, Aphididae; Hymenoptera, Aphidiidae). Annales de la Société Entomologique de France 8, 351–358.CrossRefGoogle Scholar
Starý, P. (1978) Seasonal relations between lucerne, red clover, wheat and barley agro-ecosystems through aphids and parasitoids (Homoptera, Aphididae; Hymenoptera, Aphidiidae). Acta Entomologica Bohemoslovaca 75, 296–311.Google Scholar
Taylor, L.R. (1955) The standardisation of air-flow in insect suction traps. Annals of Applied Biology 43, 390–408.CrossRefGoogle Scholar
Traugott, M., Bell, J.R., Broad, G.R., Powell, W., Van Veen, J.F., Vollhardt, I.M.G. & Symondson, W.O.C. (2008) Endoparasitism in cereal aphids: molecular analysis of a whole parasitoid community. Molecular Ecology 17, 3928–3938.CrossRefGoogle ScholarPubMed
Vickerman, G.P. (1977a) Monitoring and forecasting insect pests of cereals. Proceedings 1977 British Crop Protection Conference, Pests and Diseases 1, 227–234.Google Scholar
Vickerman, G.P. (1977b) Monitoring the insect fauna of cereals and grasses. The Game Conservancy Annual Review for 1976 8, 43–49.Google Scholar
Vickerman, G.P. (1982) Distribution and abundance of cereal aphid parasitoids (Aphidius spp.) on grassland and winter-wheat. Annals of Applied Biology 101, 185–190.Google Scholar
Vorley, W.T. (1983) The effect of parasitic hymenoptera on cereal aphid population development. PhD thesis, University of Southampton, Southampton, UK.Google Scholar
Vorley, W.T. (1986) The activity of parasitoids (Hymenoptera, Braconidae) of cereal aphids (Hemiptera, Aphididae) in winter and spring in southern England. Bulletin of Entomological Research 76, 491–504.CrossRefGoogle Scholar
Walton, M.P. (1986) The application of gel electrophoresis to the study of cereal aphid parasitoids. PhD thesis, Hatfield Polytechnic, Hatfield, UK.Google Scholar
Walton, M.P., Loxdale, H.D. & Allen-Williams, L. (1990a) Electrophoretic ‘keys’ for the identification of parasitoids (Hymenoptera: Braconidae: Aphelinidae) attacking Sitobion avenae (F.) (Hemiptera: Aphididae). Biological Journal of the Linnean Society 40, 333–346.CrossRefGoogle Scholar
Walton, M.P., Powell, W., Loxdale, H.D. & Allen-Williams, L. (1990b) Electrophoresis as a tool for estimating levels of hymenopterous parasitism in field populations of the cereal aphid, Sitobion avenae. Entomologia Experimentalis et Applicata 54, 271–279.CrossRefGoogle Scholar
Wilding, N., Mardell, S.K., Brookes, C.P. & Loxdale, H.D. (1993) The use of polyacrylamide gel electrophoresis of enzymes to identify entomophthoralean fungi in aphid hosts. Journal of Invertebrate Pathology 62, 268–272.CrossRefGoogle Scholar