Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-27T07:22:07.311Z Has data issue: false hasContentIssue false

The causes and processes of the mid-summer population crash of the potato aphids Macrosiphum euphorbiae and Myzus persicae (Hemiptera: Aphididae)

Published online by Cambridge University Press:  09 March 2007

A.J. Karley*
Affiliation:
Department of Biology, University of York, Heslington, York, YO10 5YW, UK
J.W. Pitchford
Affiliation:
Department of Biology, University of York, Heslington, York, YO10 5YW, UK
A.E. Douglas
Affiliation:
Department of Biology, University of York, Heslington, York, YO10 5YW, UK
W.E. Parker
Affiliation:
ADAS Woodthorne, Wergs Road, Wolverhampton, WV6 8TQ, UK
J.J. Howardh
Affiliation:
ADAS Woodthorne, Wergs Road, Wolverhampton, WV6 8TQ, UK
*
*Fax: +44 (0)1904 328505 E-mail: [email protected]

Abstract

Populations of many phloem-feeding aphid species in temperate regions increase exponentially in early summer and then ‘disappear’, usually over a time-scale of a few days, in July. To understand these dynamics, empirical investigation of the causes and modelling of the processes underlying population change are required. Numbers of the aphids Myzus persicae (Sulzer) and Macrosiphum euphorbiae (Thomas), monitored over three years in commercial potato fields in the UK, increased to a maximum of 2–2.5 per leaflet on 16 July in 1999 and 2001, and then declined to < 0.25 per leaflet by 26 July. In 2000, aphid numbers remained very low (< 0.25 per leaflet) throughout the season. The onset of the crash in aphid numbers (16–19 July in 1999 and 2001) was consistently associated with changes in the phloem amino acid composition of potato leaflets. Natural enemies, including syrphids, parasitoids, coccinellids, chrysopids and entomopathogenic fungi, increased in abundance throughout the sampling period. The incidence of winged emigrant aphids prior to the crash was low (< 10%). Experimental manipulation during 2001 demonstrated that, during the crash period, the fecundity of aphids (caged on leaves to exclude natural enemies) was depressed by 25–45% relative to earlier in the season, and that presence of natural enemies reduced aphid numbers by up to 68%. Using these data, an excitable medium model was constructed, which provided a robust description of aphid population dynamics in terms of plant development-induced changes in aphid fecundity and temporal change in natural enemy pressure.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2003

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

Auclair, J.L. (1963) Aphid feeding and nutrition. Annual Review of Entomology 8, 439490.CrossRefGoogle Scholar
Barlow, C.A. (1962) Development, survival and fecundity of the potato aphid, Macrosiphum euphorbiae (Thomas), at constant temperatures. Canadian Entomologist 94, 667671.CrossRefGoogle Scholar
Blackmer, J.L. & Byrne, D.N. (1999) Changes in amino acids in Cucumis melo in relation to life-history traits and flight propensity of Bemisia tabaci. Entomologia Experimentalis et Applicata 93, 2940.CrossRefGoogle Scholar
Boiteau, G. (1986) Native predators and the control of potato aphids. Canadian Entomologist 118, 11771183.CrossRefGoogle Scholar
Boiteau, G. (1997) Comparative propensity for dispersal of apterous and alate morphs of three potato-colonizing aphid species. Canadian Journal of Zoology 75, 13961403.CrossRefGoogle Scholar
Chambers, R.J., Sunderland, K.D., Stacey, D.L. & Wyatt, I.J. (1982) A survey of cereal aphids and their natural enemies in winter wheat in 1980. Annals of Applied Biology 101, 175178.Google Scholar
Colfer, R.G. & Rosenheim, J.A. (2001) Predation on immature parasitoids and its impact on aphid suppression. Oecologia 126, 292304.CrossRefGoogle ScholarPubMed
Crawley, M.J. (1993) GLIM for ecologists. Oxford, Blackwell Science.Google Scholar
Dadd, R.H. (1985) Nutrition: organisms. pp. 313391in Kerkut, G.A. & Gilbert, L.I. (Eds.) comprehensive insect physiology, biochemistry, and pharmacology vol. 4. Oxford, Pergamon Press.Google Scholar
Dahlqvist, A. (1984) a-Glucosidases (disaccharidases). pp. 208217in Bergmeyer, H.U. (Ed.) Methods of enzymatic analysis vol. 4. Weinheim, Verlag Chemie.Google Scholar
Dixon, A.F.G., Wellings, P.W., Carter, C. & Nichols, J.F.A. (1993) The role of food quality and competition in shaping the seasonal cycle in reproductive activity of the sycamore aphid. Oecologia 95, 8992.CrossRefGoogle ScholarPubMed
Douglas, A.E. (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annual Review of Entomology 43, 1737.CrossRefGoogle ScholarPubMed
Fisher, D.B. (2000) Long distance transport. pp. 730784in Buchanan, B.B., Gruissem, W. & Jones, R.L. (Eds.) Biochemistry and molecular biology of plants. Maryland, Rockville, American Society of Plant Physiologists.Google Scholar
Girousse, C. & Bournoville, R. (1994) Role of phloem sap quality and exudation characteristics on performance of pea aphid grown on lucerne genotypes. Entomologia Experimentalis et Applicata 70, 227235.CrossRefGoogle Scholar
Grevstad, F.S. & Klepetka, B.W. (1992) The influence of plant architecture on the foraging efficiencies of a suite of ladybird beetles feeding on aphids. Oecologia 92, 399404.CrossRefGoogle ScholarPubMed
Gross, P. (1993) Insect behavioural and morphological defenses against parasitoids. Annual Review of Entomology 38, 251273.CrossRefGoogle Scholar
Güntner, C., González, A., Dos Reis, R., González, G., Vázquez, A., Ferreira, F. & Moyna, P. (1997) Effect of Solanum glycoalkaloids on potato aphid, Macrosiphum euphorbiae. Journal of Chemical Ecology 23, 16511659.CrossRefGoogle Scholar
Gurney, W.S.C. & Nisbet, R.M. (1998) Ecological dynamics. Oxford, Oxford University Press.Google Scholar
Hacker, S.D. & Bertness, M.D. (1995) A herbivore paradox-why salt-marsh aphids live on poor quality plants. American Naturalist 145, 192210.CrossRefGoogle Scholar
Hairston, N.G., Smith, F.E., & Slobodkin, L.B. (1960) Community structure, population control and competition. American Naturalist 94, 421425.CrossRefGoogle Scholar
Hassell, M.P. (2000) Host-parasitoid population dynamics. Journal of Animal Ecology 69, 543566.CrossRefGoogle Scholar
Hawkins, B.A. & Holyoak, M. (1998) Transcontinental crashes of insect populations? American Naturalist 152, 480484.CrossRefGoogle ScholarPubMed
Hickman, J.M. & Wratten, S.D. (1996) Use of Phacelia tanacetifolia strips to enhance biological control of aphids by hoverfly larvae in cereal fields. Journal of Economic Entomology 89, 832840.CrossRefGoogle Scholar
Holling, C.S. (1959) The components of predation as revealed by a study of small mammal predation of the European sawfly. Canadian Entomologist 91, 293320.CrossRefGoogle Scholar
James, A., Pitchford, J.W. & Brindley, J. (2003) The relationship between plankton blooms, the hatching of fish larvae, and recruitment. Ecological Modelling 160, 7790.CrossRefGoogle Scholar
Jansen, M.P.T. & Stamp, N.E. (1997) Effects of light availability on host chemistry and the consequences for behaviour and growth of an insect herbivore. Entomologia Experimentalis et Applicata 82, 319333.CrossRefGoogle Scholar
Jarosík, V. & Dixon, A.F.G. (1999) Population dynamics of a tree-dwelling aphid: regulation and density-independent processes. Journal of Animal Ecology 68, 726732.Google Scholar
Jefferies, R.A. & Lawson, H.M. (1971) A key for the stages of development of potato (Solanum tuberosum). Annals of Applied Biology 119, 387389.CrossRefGoogle Scholar
Jones, B.N., Pääbo, S. & Stein, S. (1981) Amino acid analysis and enzymatic sequence determination of peptides by an improved o-phthaldialdehyde precolumn labelling procedure. Journal of Liquid Chromatography 4, 565586.CrossRefGoogle Scholar
Kareiva, P. (1986) Trivial movement and foraging by crop colonizers. pp. 5982in Kogan, M. (Ed.) Ecological theory and integrated pest management practice. New York, John Wiley.Google Scholar
Karley, A.J., Douglas, A.E. & Parker, W.E. (2002) Amino acid composition and nutritional quality of potato leaf phloem sap for aphids. Journal of Experimental Biology 205, 30093018.CrossRefGoogle ScholarPubMed
Kazemi, M.H. & van Emden, H.F. (1992) Partial antibiosis to Rhopalosiphum padi in wheat and some phytochemical correlations. Annals of Applied Biology 121, 19.CrossRefGoogle Scholar
Kift, N.B., Dewar, A.M. & Dixon, A.F.G. (1998) Onset of a decline in the quality of sugar beet as a host for the aphid Myzus persicae. Entomologia Experimentalis et Applicata 88, 155161.CrossRefGoogle Scholar
Kindlmann, P. & Dixon, A.F.G. (1993) Optimal foraging in ladybird beetles and its consequences for their use in biological control. European Journal of Entomology 90, 443450.Google Scholar
King, R.W. & Zeevart, J.A.D. (1974) Enhancement of phloem exudation from cut petioles by chelating agents. Plant Physiology 53, 96103.CrossRefGoogle ScholarPubMed
Losey, J.E. & Denno, R.F. (1998) The escape response of pea aphids to foliar-foraging predators: factors affecting dropping behaviour. Ecological Entomology 23, 5361.CrossRefGoogle Scholar
Losey, J.E. & Denno, R.F. (1999) Factors facilitating synergistic predation: the central role of synchrony. Ecological Applications 9, 378386.CrossRefGoogle Scholar
Ludwig, D., Jones, D.D. & Holling, C.S. (1978) Qualitative analysis of insect outbreak systems: the spruce budworm and forest. Journal of Animal Ecology 47, 315332.CrossRefGoogle Scholar
Mackauer, R.H. & Way, M.J. (1976) Myzus persicae Sulz. an aphid of world importance. pp. 51119in Delucchi, V.L. (Ed.) Studies in biological control. Cambridge, Cambridge University Press.Google Scholar
McVean, R.I.K. & Dixon, A.F.G. (2001) The effect of plant drought-stress on populations of the pea aphid Acyrthosiphon pisum. Ecological Entomology 26, 440443.CrossRefGoogle Scholar
Michels, G.J., Elliott, N.C., Romero, R.A., Owings, D.A. & Bible, J.B. (2001) Impact of indigenous coccinellids on Russian wheat aphids and greenbugs (Homoptera: Aphididae) infesting winter wheat in the Texas Panhandle. Southwestern Entomologist 26, 97114.Google Scholar
Müller, C.B., Adriaanse, I.C.T., Belshaw, R. & Godfray, H.C.J. (1999) The structure of an aphid-parasitoid community. Journal of Animal Ecology 68, 346370.CrossRefGoogle Scholar
Murray, J.D. (1989) Mathematical biology. Biomathematics Vol. 19, Springer-Verlag.Google Scholar
Nakata, T. (1995 a) Seasonal population prevalence of aphids with special reference to the production of alatoid nymphs in a potato field in Hokkaido, Japan. Applied Entomology and Zoology 30, 121127.CrossRefGoogle Scholar
Nakata, T. (1995 b) Population fluctuations of aphids and their natural enemies on potato in Hokkaido, Japan. Applied Entomology and Zoology 30, 129138.CrossRefGoogle Scholar
Parker, W.E. (1998) Forecasting the timing and size of aphid populations (Myzus persicae and Macrosiphum euphorbiae) on potato. Aspects of Applied Biology 52, 3138.Google Scholar
Parker, W.E., Howard, J.J., Karley, A.J. & Douglas, A.E. (2000) Crop growth stage and the phenology of aphid populations on potato. pp. 955960 in The Brighton Crop and Pests Conference 2000.Google Scholar
Patrick, J.W. (1997) Phloem unloading: sieve element unloading and post-sieve element transport. Annual Reviews of Plant Physiology and Plant Molecular Biology 48, 191222.CrossRefGoogle ScholarPubMed
Pescod, K.V. (2000) An investigation into escape and defence mechanisms of aphids when faced with attack by the syrphid predator. Episyrphus balteatus. MSc thesis, Imperial College of Science, Technology and Medicine, UK.Google Scholar
Pitchford, J.W. & Brindley, J. (1998) Intratrophic predation in simple predator-prey models. Bulletin of Mathematical Biology 60, 937955.CrossRefGoogle Scholar
Ponder, K.L., Pritchard, J., Harrington, R. & Bale, J.S. (2000) Difficulties in location and acceptance of phloem sap combined with reduced concentration of phloem amino acids explain lowered performance of the aphid Rhopalosiphum padi on nitrogen deficient barley (Hordeum vulgare) seedlings. Entomologia Experimentalis et Applicata 97, 203210.CrossRefGoogle Scholar
Power, M.E. (1992) Top-down and bottom-up forces in food webs: do plants have primacy? Ecology 73, 733746.CrossRefGoogle Scholar
Press, W.H., Flannery, B.P., Tuekolsky, S.A. & Vetterling, W.T. (1993) Numerical recipes in C. Cambridge, Cambridge University Press.Google Scholar
Randerath, P.F. (1996) Ordination. pp. 251287in Fry, J.C. (Ed.) Biological data analysis: a practical approach. Oxford, IRLPress.Google Scholar
Raymond, B., Darby, A.C. & Douglas, A.E. (2000) Intraguild predators and the spatial distribution of a parasitoid. Oecologia 124, 367372.CrossRefGoogle ScholarPubMed
Ro, T.H. & Long, G.E. (1999) GPA-phenodynamics, a simulation model for the population dynamics and phenology of green peach aphid in potato: formulation, validation and analysis. Ecological Modelling 119, 197209.CrossRefGoogle Scholar
Sandström, J. & Pettersson, J. (1994) Amino acid composition of phloem sap and the relation to intraspecific variation in pea aphid (Acyrthosiphon pisum) performance. Journal of Insect Physiology 40, 947955.CrossRefGoogle Scholar
Soroka, J.J. & Mackay, P.A. (1990) Growth of pea aphid, Acyrthosiphon pisum (Harris) (Homoptera: Aphididae), populations on caged plants of six cultivars of field peas and the effects of pea aphids on harvest components of caged field peas. Canadian Entomologist 122, 11931199.CrossRefGoogle Scholar
Taylor, C.E. (1955) Growth of the potato plant and aphid colonization. Annals of Applied Biology 43, 151156.CrossRefGoogle Scholar
Truscott, J.E. (1995) Environmental forcing of simple plankton models. Journal of Plankton Research 17, 22072232.CrossRefGoogle Scholar
Truscott, J.E. & Brindley, J. (1994) Ocean plankton populations as excitable media. Bulletin of Mathematical Biology 56, 981998.CrossRefGoogle Scholar
van Emden, H.F. & Bashford, M.A. (1969) A comparison of the reproduction of Brevicoryne brassicae and Myzus persicae in relation to soluble nitrogen concentration and leaf age (leaf position) in the Brussels sprout plant. Entomologia Experimentalis et Applicata 12, 351364.CrossRefGoogle Scholar
van Emden, H.F. & Bashford, M.A. (1971) The performance of Brevicoryne brassicae and Myzus persicae in relation to plant age and leaf amino acids. Entomologia Experimentalis Applicata 14, 349360.CrossRefGoogle Scholar
Viola, R., Roberts, A.G., Haupt, S., Gazzani, S., Hancock, R.D., Marmiroli, N., Machray, G.C. & Oparka, K.J. (2001) Tuberization in potato involves a switch from apoplastic to symplastic phloem unloading. Plant Cell 13, 385398.CrossRefGoogle ScholarPubMed
Watt, A.D. (1979) The effect of cereal growth stages on the reproductive activity of Sitobion avenae and Metopolophium dirhodium. Annals of Applied Biology 91, 147157.CrossRefGoogle Scholar
Weibull, J.H.W. (1988) Free amino acids in the phloem sap from oats and barley resistant to Rhopalosiphum padi. Phytochemistry 27, 20692072.CrossRefGoogle Scholar
Williams, C.T. (1995) Effects of plant age, leaf age and virus yellows infection on the population dynamics of Myzus persicae (Homoptera: Aphididae) on sugarbeet in field plots. Bulletin of Entomological Research 85, 557567.CrossRefGoogle Scholar
Williams, I.S., Dewar, A.M., Dixon, A.F.G. & Thornhill, W.A. (1999) Alate production by aphids on sugar beet-how likely is the evolution of sugar beet-specific biotypes? Journal of Applied Ecology 36, 113.Google Scholar