Role of nitrogen content of pea (Pisum sativum L.) on pea aphid (Acyrthosiphon pisum Harris) establishment

Authors

Department of Plant Protection, Faculty of Agriculture, Ferdowsi University of Mashad, P.O.Box 1163, Mashhad, Iran

Abstract

The leaf nitrogen content is generally accepted as an indicator of food quality and as a factor affecting host selection by phytophagous insects. The alate pea aphids (Acyrthosiphon pisum Harris, Aphididae) were given a choice among non-nodulated pea plants (Pisum sativum L.) supplied with one of four nitrate-N levels (0, 3, 15 and 30 mM). When whole plants were exposed to aphids for 7 days, the results indicated that the settling response of alatae, and subsequently the reproduction of alighted aphids, increased as the level of N supply or the concentration of total soluble nitrogen of the leaves increased, with the exception of the highest N supply (30 mM N). However, the density of settled alatae (in terms of number per unit leaf area) increased as the level of N supply decreased, being greatest on N-deficient plants (0 mM N treatment) and lowest density on N-sufficient (15 mM N) and N-excess (30 mM N) plants. In a free-choice experiment, equal-sized leaf discs taken from the different N treatments were exposed to alate adults for 24 h.The settling response of aphids was positively affected by leaf colour (yellowing), with the greatest number settled on yellow leaf discs (N-deficient plants) and fewest settled on green or dark-green discs (N-sufficient and N-excess plants). Relationships between level of N supply, total soluble nitrogen concentration, total chlorophyll concentration, plant growth parameters and aphid abundance (number of alatae per plant) or density (number of alatae per unit leaf area, or per leaf disc) were established. The implications of results for integrated aphid management were discussed.
 
 
REFERENCES
 Allen, S.E. (1989) Chemical Analysis of Ecological Materials. Blackwell Scientific Publications, Oxford, 368 p.
Auclair, J.L., Maltais, J.B. and Cartier, J.J. (1957) Factors in resistance to the pea aphid, Acyrthosiphon pisum (Harr.) (Homoptera: Aphididae). II. Amino acids. Can. Entomol. 89, 457-464.
Belanger, G., Gastal, F. and Lemaire, G. (1992) Growth analysis of a tall fescue sward fertilized with different rates of nitrogen. Crop Sci. 32, 1371-1376.
Bernays, E.A. (1992) Insect - Plant Interactions. CRC Press, Boca Raton,  226 p.
Biddle, A.J., Knott, C.M. and Gent, G.P. (1988) Pea Growing Handbook. Processors & Growers Research Organisation, Peterborough, 264 p.
Brouquisse, R., Masclaux, C. and Feller, U. (2001) Protein hydrolysis and nitrogen remobilisation in plant life and senescence. Plant Nitrogen. (ed. Lea, P.J. and MorotGaudry, J.F.), pp. 275-293. Springer-Verlag, Berlin.
Cartier, J.J. (1963) Varietal resistance of peas to pea aphid biotypes under field and greenhouse conditions. J. Econ. Entomol. 56, 205-213.
Clegg, J.M. and Barlow, C.A. (1982) Escape behaviour of the pea aphid Acyrthosiphon pisum (Harris) in response to alarm pheromone and vibration. Can. J. Zool. 60, 2245-2252.
Conway, E.J. (1962) Microdiffusion Analysis and Volumetric Error. Crosby Lockwood, London,  467 p.
Dixon, A.F.G. (1970) Quality and availability of food for a sycamore aphid population. Animal Populations in Relation to their Food Resources. (ed. Watson, A.), pp. 271- 287. Blackwell, Oxford.
Dixon, A.F.G. (1998) Aphid Ecology. Chapman & Hall, London. pp. 300.
Dowell, R.V. and Steinberg, B. (1990) Influence of host plant characteristics and nitrogen fertilization on development and survival of immature citrus blackfly, Aleurocanthus woglumi Ashby (Hom., Aleyrodidae). J. Appl. Entomol. 109, 113- 119.
Driessche, R.V.D. and Webber, J.E. (1975) Total and soluble nitrogen in douglas fir in relation to plant nitrogen status. Can. J. For. Res. 5, 580-585.
Febvay, G., Bonnin, J., Rahbe, Y., Bournoville, R., Delrot, S. and Bonnemain, J.L. (1988) Resistance of different lucerne cultivars to the pea aphid Acyrthosiphon pisum: influence of phloem composition on aphid fecundity. Entomol. Exp. Appl., 48, 127- 134.
Flynn, D.F.B., Sudderth, E.A. and Bazzaz, F.A. (2006) Effects of aphid herbivory on biomass and leaf-level physiology of Solanum dulcamara under elevated temperature and CO2. Environ. Exp. Bot. 56, 10- 18.
Folsom, J.W. (1927) Calcium arsenate as a cause of aphid infestations. J. Econ. Entomol., 20, 840-643.
Jansson, J. and Ekbon, B. (2002) The effect of different plant nutrient regimes on the aphid Macrosiphum euphorbiae growing on petunia. Entomol. Exp. Appl., 104, 109-116.
Jansson, R.K. and Smilowitz, Z. (1986) Influence of nitrogen on population parameters of potato insects: abundance, population growth, and within-plant distribution of the green peach aphid, Myzus persicae (Homoptera: Aphididae). Environ. Entomol., 15, 49-55.
Jauset, A.M., Sarasua, M.J., Avilla, J. and Albajes, R. (1998) The impact of nitrogen fertilization of tomato on feeding site selection and oviposition by Trialeurodes vaporariorum. Entomol. Exp. Appl. 86, 175-182.
Jauset, A.M., Sarasua, M.J., Avilla, J. and Albajes, R. (2000) Effect of nitrogen fertilization level applied to tomato on the greenhouse whitefly. Crop Pro., 19, 255-261.
Karley, A.J., Douglas, A.E. and Parker, W.E. (2002) Amino acid composition and nutritional quality of potato leaf phloem sap for aphids. J. Exp. Biol. 205, 3009-3018.
Kennedy, J.S. (1958) Physiological condition of the host-plant and susceptibility to aphid attack. Entomol. Exp. Appl. 1, 50-65.
Kennedy, J.S. (1976) Host-plant finding by flying aphids. Symposia Biologica Hungarica 16, 121-123.
Kennedy, J.S., Booth, C.O. and Kershaw, W.J.S. (1959) Host finding by aphids in the field. I. Gynoparae of Myzus persicae (Sulzer). Ann. Appl. Biol. 47, 410-423.
Kennedy, J.S., Booth, C.O. and Kershaw, W.J.S. (1961) Host finding by aphids in the field. III. Visual attraction. Ann. Appl. Biol. 49, 1-21.
Kennedy, J.S., Ibbotson, A. and Booth, C.O. (1950) The distribution of aphid infestation in relation to leaf age. I. Myzus persicae (Sulz.) and Aphis fabae Scop. on spindle trees and sugerbeet plants. Ann. Appl. Biol. 37, 651-679.
Kennedy, J.S. and Stroyan, H.L.G. (1959) Biology of aphids. Annu. Rev. Entomol. 4, 139-160.
Kindlmann, P. and Dixon, A.F.G. (1994) Evolution of host range in aphids. Eur. J. Entomol. 91, 91-96.
Knott, C.M. (1987) A key for stages of development of the pea (Pisum sativum). Ann. Appl. Biol. 111, 233-245.
Kutik, J., Natr, L., Demmers-Derks, H.H. and Lawlor, D.W. (1995) Chloroplast ultrastructure of sugar beet (Beta vulgaris L.) cultivated in normal and elevated CO2 concentrations with two contrasted nitrogen supplies. J. Exp. Bot. 46, 1797-1802.
Larson, K.C. and Whitman, T.G. (1991) Manipulation of food resources by a gallforming aphid: the physiology of sinksource interactions. Oecologia. 88, 15-21.
Lawlor, D.W., Boyle, F.A., Keys, A.J., Kendall, A.C. and Young, A.T. (1988) Nitrate nutrition and temperature effects on wheat: a synthesis of plant growth and nitrogen uptake in relation to metabolic and physiological processes. J. Exp. Bot. 39, 329-343.
Lawlor, D.W., Lemaire, G. and Gastal, F. (2001) Nitrogen, plant growth and crop yield. Plant Nitrogen. (ed. Lea, P.J. and Morot-Gaudry, J.F.), pp. 343-367. SpringerVerlag, Berlin.
Legrand, A. and Barbosa, P. (2000) Pea aphid (Homoptera: Aphididae) fecundity, rate of increase, and within-plant distribution unaffected by plant morphology. Environ. Entomol. 29, 987-993. Lichtenthaler, H.K. and Wellburn, A.R. (1983) Determinations of total carotenoids and chlorophylls a and b in leaf extracts in different solvents. Biochem. Soc. Trans. 11, 591-592.
Makowski, D., Wallach, D. and Meynard, J.M. (1999) Models of yield, grain protein and residual mineral nitrogen responses to applied nitrogen for winter wheat. Agron. J. 91, 377-385.
Maltais, J.B. (1951) The nitrogen content of different varieties of peas as a factor affecting infestations by Macrosiphum pisi (Kltb.) (Homoptera: Aphididae). A preliminary report. Can. Entomol. 83, 29-33.
Maltais, J.B. and Auclair, J.L. (1957) Factors in resistance of peas to the pea aphid, Acyrthosiphon pisum (Harr.) (Homoptera: Aphididae). I. The sugar-nitrogen ratio. Can. Entomol. 89, 365-370.
Manglitz, G.R., Gorz, H.J., Haskins, F.A., Akeson, W.R. and Beland, G.L. (1976) Interactions between insects and chemical components of sweetclover. J. Environ. Qual. 5, 347-352.
Mattson, W.J. (1982) Herbivory in relation to plant nitrogen content. Annu. Rev. Ecol. Syst. 11, 119-161.
 Mattson, W.J. (1993) Nitrogen - the driving element: a citation classic commentary on herbivory in relation to plant nitrogen. Agric. Biol. Environ. Sci. 16, 8-17.
McClure, M.S. (1980) Foliar nitrogen: a basis for host suitability for elongate hemlock scale, Fiorina externa (Homoptera: Diaspididae). Ecology. 61, 72-79.
McNeill, S. and Southwood, T.R.E. (1978) The role of nitrogen in the development of insect-plant relationships. Biochemical Aspects of Plant and Animal Coevolution. (ed. Harborne, J.B.), pp. 77-98. Academic Press, London & New York.
Minkenberg, O.P.J.M. and Fredrix, M.J.J. (1989) Preference and performance of an herbivorous fly Lyriomiza trifolii (Diptera: Agromyzidae) on tomato plants differing in leaf nitrogen. Ann. Entomol. Soc. Am. 82, 350-354.
Mittler, T.E. (1954) The feeding and nutrition of aphids. Cambrige, University of Cambridge.
Mittler, T.E. (1958) Studies on the feeding and nutrition of Tuberolachnus salignus (Gmelin) (Homoptera, Aphididae). II. The nitrogen and sugar composition of ingested phloem sap and excreted honeydew. J. Exp. Biol. 35, 74-84.
Mittler, T.E. (1958) Studies on the feeding and nutrition of Tuberolachnus salignus 130 Role of nitrogen content of pea on pea aphid (Gmelin) (Homoptera, Aphididae). III. The nitrogen economy. J. Exp. Biol. 35, 626-638.
Moore, J.B. (1935) Studies of the reactions of potato aphids to sprayed and unsprayed potato leaves. J. Econ. Entomol., 28, 436- 442.
Moore, J.B. (1937) Reactions of aphids to colored insecticides. J. Econ. Entomol., 30, 305-309.
Müller, H.J. (1958) The behaviour of Aphis fabae in selecting its host plants, especially different varieties of Vicia faba. Entomol. Exp. Appl. 1, 66-72.
Nooden, L.D., Guiamet, J.J. and John, I. (1997) Senescence mechanisms. Physiol. Plant., 101, 746-753.
Painter, R.H. (1951) Insect Resistance in Crop Plants. Macmillan, New York, 520 p.
Pfeiffer, D.G. and Burts, E.C. (1984) Effect of tree fertilization on protein and free amino acid content and feeding rate of pear psylla (Homoptera, Psyllidae). Environ. Entomol. 13, 1487-1490.
Ponder, K.L., Pritchard, J., Harrington, R. and 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. Entomol. Exp. Appl., 97, 203-210.
Prestidge, R.A. (1982) The influence of nitrogenous fertilizer on the grassland Auchenorrhyncha (Homoptera). J. Appl. Entomol. 19, 735-749.
Raese, J.T. (1977) Response of young 'd'Anjou' pear trees to triazine and triazole herbicides and nitrogen. J. Am. Soc. Hortic. Sci. 102, 215-218.
Ralph, C.P. (1976) Natural food requirements of the large milkweed bug, Oncopeltus fasciatus (Hemiptera: Lygaeidae), and their relation to gregariousness and host plant morphology. Oecologia. 26, 157-175.
Rorison, I.H. and Robinson, D. (1986) Mineral nutrition. Methods in Plant Ecology. (ed. Moore, P.D. and Chapman, S.B.), pp. 145- 213. Blackwell Scientific Publications, Oxford.
Salyk, R.P. and Sullivan, D.J. (1982) Comparative feeding behaviour of two aphid species: bean aphid (Aphis fabae Scopoli) and pea aphid (Acyrthosiphon pisum (Harris)) (Homoptera: Aphididae). J. New York Entomol. Soc. 90, 87-93.
Sandstrom, J. and Moran, N. (1999) How nutritionally imbalanced is phloem sap for aphids? Entomol. Exp. Appl. 91, 203-210.
Scriber, J.M. and Slansky, F. (1981) The nutritional ecology of immature insects. Annu. Rev. Entomol. 26, 183-211.
Sinclair, T.R. and Horie, T. (1989) Leaf nitrogen, photosynthesis, and crop radiation use efficiency: a review. Crop Sci. 29, 90-98.
Smart, C.M. (1994) Gene expression during leaf senescence. New Phytol. 126, 419-448.
SPSS (1998) SPSS User's guide. SPSS Inc., Chicago, 806 p. S
udderth, E.A., Stinson, K.A. and Bazzaz, F.A. (2005) Host-specific aphid population responses to elevated CO2 and increased N availability. Global Change Biol. 11, 1997- 2008.
Taiz, L. and Zeiger, E. (1998) Plant Physiology. Sinauer Associates, Inc., Sunderland, Massachusetts. pp. 792. Taylor, L.R. (1960) The distribution of insects at low levels in the air. J. Anim. Ecol. 29, 45- 63.
Taylor, L.R. (1965) Flight behaviour and aphid migration. Proceedings North Central Branch Entomological Society of America. 20, 9-19.
Taylor, L.R. (1974) Insect migration, flight periodicity and the boundary layer. J. Anim. Ecol. 43, 225-238.
Ter Steege, M.W., Stulen, I. and Mary, B. (2001) Nitrogen in the environment. Plant Nitrogen. (ed. Lea, P.J. and Morot-Gaudry, J.F.), pp. 379-397. Springer-Verlag, Berlin.
Theobald, J.C., Mitchell, R.A.C., Parry, M.A.J. and Lawlor, D.W. (1998) Estimating the excess investment in ribulose-1, 5- bisphophate carboxylase/ oxygenase in leaves of spring wheat grown under elevated CO2. Plant Physiol. 118, 945-955.
Van Emden, H.F. (1966) Studies on the relations of insect and host plant, III. A comparison of the reproduction of Brevicoryne brassicae and Myzus persicae (Hemiptera: Aphididae) on brussels sprout plants supplied with different rates of nitrogen and potassium. Entomol. Exp. Appl. 9, 444- 460.
Van Emden, H.F. (1972) Aphids as phytochemists. Phytochemical Ecology. (ed. Harborne, J.B.), pp. 25-43. Academic Press, London.
Van Emden, H.F. (1987) Cultural methods: Moravvej and Hatefi 131 The plant. Integrated Pest Management. (ed. Burn, A.J., Coaker, T.H. and Jepson, P.C.), pp. 27-68. Academic Press, London.
Van Emden, H.F. (1990) The interaction of host plant resistance to insects with other control measures. Brighton Crop Protection Conference: Pests and Diseases. 3, 939- 947.
Van Emden, H.F. (1997) Host-plant resistance to insect pests. Techniques for Reducing Pesticide Use. (ed. David, P.), pp. 129-152. John Wiley & Sons, West Sussex, England.
Van Emden, H.F. and 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. Entomol. Exp. Appl. 12, 351- 364.
Van Emden, H.F. and Bashford, M.A. (1971) The performance of Brevicoryne brassicae and Myzus persicae in relation to plant age and leaf amino acids. Entomol. Exp. Appl. 14, 349-360.
Van Emden, H.F. and Bashford, M.A. (1976) The effect of leaf excision on the performance of Myzus persicae and Brevicoryne brassicae in relation to nutrient treatment of the plants. Physiol. Entomol. 1, 67-71.
Van Emden, H.F., Eastop, V.F., Hughes, R.D. and Way, M.J. (1969) The ecology of Myzus persicae. Annu. Rev. Entomol. 14, 197-270.
Van Keulen, H., Goudriaan, J. and Seligman, N.G. (1989) Modelling the effects of nitrogen on canopy development and crop growth. Plant Canopies, their Growth, Form and Function. (ed. Russell, G., Marshall, B. and Jarvis, P.G.), pp. 83-104. Cambridge University, Cambridge.
Wellburn, A.R. (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J. Plant Physiol. 144, 307-313.

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