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Identity of Schizaphis species (Hemiptera: Aphididae) in the United Kingdom: are they a threat to crops?

Published online by Cambridge University Press:  05 March 2013

Amalia Kati
Affiliation:
Department of AgroEcology, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK
Kevin A. Shufran
Affiliation:
USDA-ARS, 1301 N. Western Road, Stillwater, OK 74075, USA
Mark S. Taylor
Affiliation:
Department of AgroEcology, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK
Shalva Barjadze
Affiliation:
Agricultural University of Georgia, Entomology and Biocontrol Research Centre, 13th km of David Aghmashenebeli Alley, 0131 Tbilisi, Georgia
Victor F. Eastop
Affiliation:
Department of Life Sciences, The Natural History Museum, London SW7 5BD, UK
Roger L. Blackman
Affiliation:
Department of Life Sciences, The Natural History Museum, London SW7 5BD, UK
Richard Harrington*
Affiliation:
Department of AgroEcology, Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK
*
*Author for correspondence Phone: +44 1582 763133 Ext. 2452 Fax: +44 1582 760981 E-mail: [email protected]

Abstract

The greenbug, Schizaphis graminum (Rondani), is a major pest of cereals in some parts of the world and is of particular concern because it can be resistant to some insecticides and overcome the resistance of crops. In the UK, it has never been found on crops, but two rather little-known and closely-related species (Schizaphis holci and Schizaphis agrostis) are associated with the wild grasses, Holcus lanatus and Agrostis stolonifera. Since 1987, winged (alate) aphids morphologically resembling the greenbug have been found in increasing numbers in 12.2 m high suction-trap samples of the Rothamsted Insect Survey (RIS); hence, studies were undertaken to establish their identity. Clones (=asexual lineages) established from populations collected from H. lanatus in southern England showed strong preference for Holcus over Agrostis and Hordeum in laboratory tests and produced sexual morphs when transferred to short-day conditions, the males being apterous, as expected for S. holci. Multivariate morphometric comparisons of alatae caught in UK RIS suction traps in 2007 and 2011 with named specimens from museum collections, including S. graminum from many countries, indicated that the suction-trapped alatae were mostly S. agrostis and S. holci. Cytochrome c oxidase subunit I (COI) mtDNA obtained from 62 UK specimens from suction-traps had 95.4–100% sequence identity with US specimens of S. graminum. Two of the UK specimens had identical COI sequence to the US sorghum-adapted form of S. graminum, and these specimens also had 100% identity with a 640 bp fragment of nDNA CytC, indicating that this form of S. graminum may already be present in the UK. Present and future economic implications of these results are discussed.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2013 

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References

Abdi, H. & Williams, L.J. (2010) Principal component analysis. Wiley Interdisciplinary Reviews. Computational Statistics 2, 433459.Google Scholar
Alsuhaibani, A.L. (1996) Seasonal abundance of two cereal aphids, Rhopalosiphum padi (L.) and Schizaphis graminum (Rondani), (Homoptera, Aphididae) on twelve elite wheat lines in Riyadh, Saudi Arabia. Arab Gulf Journal of Scientific Research 14, 405413.Google Scholar
Aslam, M., Razaq, M., Ahmad, F., Fahemm, M. & Akhter, W. (2004) Population of aphid (Schizaphis graminum R.) on different varieties/lines of wheat (Triticum aestivum L.). International Journal of Agriculture and Biology 6, 974977.Google Scholar
Austin, A.B.M., Tatchell, G.M., Harrington, R. & Bale, J.S. (1991) A method for rearing cereal aphids in a small space. Entomologia Experimentalis et Applicata 61, 9193.Google Scholar
Blackman, R.L. & Eastop, V.F. (2006) Aphids on the World's Herbaceous Plants and Shrubs. London, John Wiley & Sons.Google Scholar
Blackman, R.L. & Eastop, V.F. (2007) Taxonomic issues. pp. 129in van Emden, H.F. & Harrington, R. (Eds) Aphids as Crop Pests. Wallingford, CAB International.Google Scholar
Fargo, W.S., Inayatullah, C., Webster, J.A. & Holbert, D. (1986) Morphometric variation within apterous females of Schizaphis graminum biotypes. Researches on Population Ecology 28, 163172.Google Scholar
Hajibabaei, M., Janzen, D.H., Burns, J.M., Hallwachs, W. & Hebert, P.D.N. (2006) DNA barcodes distinguish species of tropical Lepidoptera. Proceedings of the National Academy of Sciences of the United States of America 103, 968971.Google Scholar
Hammer, Ø., Harper, D.A.T. & Ryan, P.D. (2001) PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4, 19.Google Scholar
Harrington, R. & Woiwod, I. (2007) Foresight from hindsight: the Rothamsted Insect Survey. Outlooks on Pest Management 18, 914.Google Scholar
Harrington, R., Fleming, R.A. & Woiwod, I.P. (2001) Climate change impacts on insect management and conservation in temperate regions: can they be predicted? Agricultural and Forest Entomology 3, 233240.Google Scholar
Harvey, T.L. (1971) Research on greenbug and resistance in sorghums. pp. 8486 in Proceedings of Seventh Biennial Program of the International Grain Sorghum Research and Utilization Conference organized by the Grain Sorghum Producers Association. 2–4 March 1971, Lubbock, Texas.Google Scholar
Harvey, T.L. & Hackerott, H.L. (1969) Recognition of a greenbug biotype injurious to sorghum. Journal of Economic Entomology 62, 776779.Google Scholar
Heie, O. (1986) The Aphidoidea (Hemiptera) of Fennoscandia and Denmark. III Family Aphididae: subfamily Pterocommatinae and tribe Aphidini of subfamily Aphidinae. Fauna Entomologica Scandinavica 17, 5881.Google Scholar
Hill, D. (1987) Agricultural Insect Pests of Temperate Regions and Their Control. Cambridge, Cambridge University Press.Google Scholar
Hille Ris Lambers, D. (1947) On some mainly Western European aphids. Zoologische Mededelingen 28, 291333.Google Scholar
Hullé, M., Coeur d'Acier, A., Bankhead-Dronnet, S. & Harrington, R. (2010) Aphids in the face of global changes. Comptes Rendues Biologies 333, 497503.Google Scholar
Hurst, G.D.D. & Jiggins, F.M. (2005) Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effect of inherited symbionts. Proceedings of the Royal Society B 272, 15241534.Google Scholar
Ilharco, F.A. & van Harten, A. (1987) Systematics. pp. 5177in Minks, A.K. & Harrewijn, P. (Eds). Aphids: Their Biology, Natural Enemies and Control. Amsterdam, Elsevier Science Publishers.Google Scholar
Inayatullah, C., Webster, J.A. & Fargo, W.S. (1987) Morphometric variation in the alates of Greenbug (Homoptera: Aphididae) biotypes. Annals of the Entomological Society of America 80, 306311.Google Scholar
Lapierre, H. & Signoret, P.A. (2004) Viruses and Virus Diseases of Poaceae (Gramineae). Paris, INRA-Editions.Google Scholar
Loxdale, H.D., Vorwerk, S. & Forneck, A. (2013) The unstable ‘clone’: evidence from monitoring AFLP based mutations for short-term clonal genetic variation in two asexual lineages of the grain aphid, Sitobion avenae (F.). Bulletin of Entomological Research 103, 111118.Google Scholar
Macaulay, E.D.M., Tatchell, G.M. & Taylor, L.R. (1988) The Rothamsted Insect Survey 12-metre suction trap. Bulletin of Entomological Research 78, 121129.Google Scholar
Martin, J. (1983) The identification of common aphid pests of tropical agriculture. Tropical Pest Management 29, 395411.Google Scholar
Mittler, T.E. & Gorder, N.K.N. (1991) Variation between clones of Schizaphis graminum (Homoptera: Aphididae) in the photoperiodic induction of sexual morphs. Environmental Entomology 20, 433440.CrossRefGoogle Scholar
Palumbi, S.R. (1996) Nucleic acids II: the polymerase chain reaction. pp. 205247in Hillis, D.M., Moritz, C. & Mable, B.K. (Eds) Molecular Systematics. Sunderland, MA, Sinauer Inc. Publishers.Google Scholar
Payne, R.W., Murray, D.A., Harding, S.A., Baird, D.B. & Soutar, D.M. (2009) GenStat for Windows Introduction. 12th edn. Hemel Hempstead, VSN International.Google Scholar
Porter, D.R., Burd, J.D., Shufran, K.A., Webster, J.A. & Teetes, G.L. (1997) Greenbug (Homoptera: Aphididae) biotypes: selected by resistant cultivars or preadapted opportunists? Journal of Economic Entomology 90, 10551065.CrossRefGoogle Scholar
Radchenko, E.E. & Lychagina, N.S. (2003) Physiological and genetic variation in Schizaphis graminum (Sternorrhyncha: Aphididae) populations. Acta Societatis Zoologicae Bohemicae 67, 1523.Google Scholar
Rubin-de-Celis, V.E., Gassen, D.N., Callegari-Jacques, S.M., Valente, V.L.S. & Oliveira, A.K. (1997) Morphometric observations on three populations of Schizaphis graminum (Rondani), a main wheat aphid pest in Brazil. Anais da Sociedade Entomológica do Brasil 26, 417428.Google Scholar
Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual. New York, Cold Spring Harbor Laboratory Press.Google Scholar
Shufran, K.A. (2011) Host race evolution in Schizaphis graminum (Hemiptera: Aphididae): nuclear DNA sequences. Environmental Entomology 6, 13171322.Google Scholar
Shufran, K.A. & Puterka, G.J. (2011) DNA barcoding to identify all life stages of holocyclic cereal aphids (Hemiptera: Aphididae) on wheat and other Poaceae. Annals of the Entomological Society of America 104, 3942.Google Scholar
Shufran, R.A., Wilde, G.E. & Sloderbeck, P.E. (1996) Description of three isozyme polymorphisms associated with insecticide resistance in greenbug (Homoptera: Aphididae) populations. Journal of Economic Entomology 89, 4650.Google Scholar
Shufran, R.A., Wilde, G.E., Sloderbeck, P.E. & Morrison, W.P. (1997) Response of three greenbug (Homoptera: Aphididae) strains to five organophosphorous and two carbamate insecticides. Journal of Economic Entomology 90, 15771583.CrossRefGoogle Scholar
Shufran, K.A., Burd, J.D., Anstead, J.A. & Lushai, G. (2000) Mitochondrial DNA sequence divergence among greenbug (Homoptera: Aphididae) biotypes: evidence for host-adapted races. Insect Molecular Biology 9, 179184.Google Scholar
Sloderbeck, P.E., Chowdhury, M.A., Depew, L.J. & Buschman, L.L. (1991) Greenbug (Homoptera, Aphididae) resistance to parathion and chlorpyrifos-methyl. Journal of Kansas Entomological Society 64, 14.Google Scholar
Stroyan, H.L.G. (1984) Aphids – Pterocommatinae and Aphidinae (Aphidini), Homoptera, Aphididae. pp. 3641 in Handbooks for the Identification of British Insects. London, Royal Entomological Society.Google Scholar
Tabachnick, B.G. & Fidell, L.S. (2006) Using Multivariate Statistics. 5th edn.Boston, Allyn & Bacon.Google Scholar
Tamura, K. & Nei, M. (1993) Estimation of the number of nucleotide substitutions in the control region of the mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512526.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28, 27312739.Google Scholar
Taylor, L.R. (1986) Synoptic dynamics, migration and the Rothamsted Insect Survey. Journal of Animal Ecology 55, 138.Google Scholar
Thompson, J.D., Higgins, D.G. & Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.CrossRefGoogle ScholarPubMed
Tomanovic, Z., Kavallieratos, N., Stary, P., Petrovic-Obradovic, O., Athanassiou, C.G. & Stanisavljevic, Z. (2008) Cereal aphids (Hemiptera: Aphidoidea) in Serbia: seasonal dynamics and natural enemies. European Journal of Entomology 105, 495501.Google Scholar
Tsitsipis, J.A., Katis, N.I., Margaritopoulos, J.T., Lykouressis, D.P., Avgelis, A.D., Gargalianou, I., Zapras, K.D., Perdikis, D.C. & Papapanayiotou, A.P. (2007) A contribution to the aphid fauna of Greece. Bulletin of Insectology 60, 3138.Google Scholar
Walker, P.T. (1954) The influence of climate on an outbreak of wheat aphid in Kenya. Empire Journal of Experimental Agriculture 22, 293304.Google Scholar
Webster, F.M. & Phillips, W.J. (1912) The spring grain-aphis or ‘green bug’. Bulletin, Bureau of Entomology, United States Department of Agriculture 110, 1153.Google Scholar
Wood, E.A. Jr. & Starks, K.J. (1972) Effect of temperature and host plant interaction on the biology of three biotypes of the greenbug. Environmental Entomology 1, 230234.Google Scholar
Wyatt, I.J. & White, P.F. (1977) Simple estimation of intrinsic increase rates for aphids and tetranychid mites. Journal of Applied Ecology 14, 757766.Google Scholar
Zhang, D.-X. & Hewitt, G.M. (1996) Nuclear integrations: challenges for mitochondrial DNA markers. Trends in Ecology and Evolution 11, 247251.Google Scholar