Abstract
Leaf-chewing herbivores select food with a protein/carbohydrate ratio of 0.8–1.5, whereas phloem sap, which aphids feed on, has a ratio of ~0.1. Enhanced N fertilization increases the amino acid concentration in phloem sap and elevates the N/C ratio. The study examines: (1) whether aphids select between plants of different N nutrition, (2) whether feeding time correlates with the amino acid composition of phloem sap, and (3) at which stage of probing aphids identify the quality of the plant. Uroleucon tanaceti (Mordvilko) and Macrosiphoniella tanacetaria (Kaltenbach), specialist aphids feeding on tansy (Tanacetum vulgare L.), were reared on this host plant grown essentially hydroponically (in Vermiculite) in the greenhouse on 1, 3, 6, or 12 mM NH4NO3. One and 3 mM NH4NO3 corresponds to the situation found in natural tansy stands. Aphid stylet penetration was monitored by electrical penetration graphs whilst phloem sap was sampled by stylectomy. Both aphid species settled 2–3 times more frequently on plants fertilized with 6 or 12 mM NH4NO3. The phloem sap of these plants contained up to threefold higher amino acid concentrations, without a change in the proportion of essential amino acids. No time differences were observed before stylet penetration of plant tissue. After the first symplast contact, most aphids penetrated further, except M. tanacetaria on low-N plants, where 50% withdrew the stylet after the first probing. The duration of phloem feeding was 2–3 times longer in N-rich plants and the time spent in individual sieve tubes was up to tenfold longer. Aphids identified the nutritional quality of the host plant mainly by the amino acid concentration of phloem sap, not by leaf surface cues nor the proportion of essential amino acids. However, U. tanaceti infestation increased the percentage of methionine plus tryptophan in phloem tenfold, thus manipulating the plants nutritional quality, and causing premature leaf senescence.
Similar content being viewed by others
References
Abisgold JD, Simpson SJ, Douglas AE (1994) Nutrient regulation in the pea aphid Acyrthosiphon pisum: application of the novel geometric framework to sugar and amino acid consumption. Physiol Entomol 19:95–102
Behmer ST (2009) Insect herbivore nutrient regulation. Annu Rev Entomol 54:165–187
Bergmeyer HU, Bernt E (1974) Sucrose. In: Bergmeyer HU (ed) Methods of enzymatic analysis II (3). Verlag Chemie, Academic Press, Weinheim
Bromley AK, Anderson M (1982) An electrophysiological study of olfaction in the aphid, Nasonovia ribis-nigri. Entomol Exp Appl 32:101–110
Couldridge C, Newbury HJ, Ford-Lloyd B, Bale J, Pritchard J (2007) Exploring plant responses to aphid feeding using a full Arabidopsis microarray reveals a small number of genes with significantly altered expression. Bull Entomol Res 97:523–532
Dadd RH (1985) Nutrition: organisms. In: Kerkut GA, Gilbert LI (eds) Comprehensive insect physiology biochemistry and pharmacology. Regulation: digestion, nutrition, excretion, vol 4. Pergamon Press, Oxford, pp 313–390
Divol F, Vilaine F, Thibivilliers S, Amselem J, Palauqui JC, Kusiak C, Dinant S (2005) Systemic response to aphid infestation by Myzus persicae in the phloem of Apium graveolens. Plant Mol Biol 57:517–540
Douglas AE (1988) Sulphate utilization in an aphid symbiosis. Insect Biochem 18:599–605
Douglas AE (1998) Nutritional interactions in insect-microbial symbioses: aphids and their symbiotic bacteria Buchnera. Annu Rev Entomol 43:17–37
Douglas AE (2003) The nutritional physiology of aphids. Adv Insect Physiol 31:73–140
Douglas AE, Minto LB, Wilkinson TL (2001) Quantifying nutrient production by the microbial symbionts in an aphid. J Exp Biol 204:349–358
Downing N, Unwin DM (1977) A new method for cutting the mouth-parts of feeding aphids, and for collecting plant sap. Physiol Entomol 2:275–277
Epstein E (1972) Mineral nutrition of plants: principles and perspectives. Wiley, New York
Febvay G, Bonnin J, Rahbé Y, Bournoville R, Delrot S, Bonnemain JL (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
Febvay G, Liadouze I, Guillaud J, Bonnot G (1995) Analysis of energetic amino acid metabolism in Acyrthosiphon pisum: a multidimensional approach to amino acid metabolism in aphids. Arch Insect Biochem Physiol 29:45–69
Febvay G, Rahbe Y, Rynkiewicz M, Guillaud J, Bonnot G (1999) Fate of dietary sucrose and neosynthesis of amino acids in the pea aphid Acyrthosiphon pisum, reared on different diets. J Exp Biol 202:2639–2652
Fischer MK (2001) Die Zuckerzusammensetzung des Honigtaus bei verschiedenen Blattlausarten und die Konsequenzen für den Mutualismus Blattlaus-Ameise. Dissertation Universität Bayreuth
Fischer MK, Völkl W, Schopf R, Hoffmann KH (2002) Age-specific pattern in honeydew production and honeydew composition in the aphid Metopeurum fuscoviride: implications for ant-attendance. J Insect Physiol 48:319–326
Girousse C, Bournoville R (1994) Role of phloem sap quality and exudation characteristics on performance of pea aphid grown on lucerne genotypes. Entomol Expt Appl 70:227–235
Girousse C, Faucher M, Kleinpeter C, Bonnemain JL (2003) Dissection of the effect of the aphid Acyrthosiphon pisum feeding on assimilate partitioning in Medicago sativa. New Phytol 157:83–92
Matt P, Geiger M, Walch-Liu P, Engels C, Krapp A, Stitt M (2001) The immediate cause of the diurnal changes of nitrogen metabolism in leaves of nitrate-replete tobacco: a major imbalance between the rate of nitrate reduction and the rates of nitrate uptake and ammonium metabolism during the first part of the light period. Plant Cell Environ 24:177–190
McLean DL, Kinsey MG (1964) A technique for electronically recording aphid feeding and salivation. Nature 202:1358–1359
Powell G, Hardie J (2000) Host-selection behaviour by genetically identical aphids with different plant preferences. Physiol Entomol 25:54–62
Prosser WA, Simpson SJ, Douglas AE (1992) How an aphid (Acyrthosiphon pisum) symbiosis responds to variation in dietary nitrogen. J Insect Physiol 38:301–307
Sandström JP, Moran NA (2001) Amino acid budgets in the three aphid species using the same host plant. Physiol Entomol 26:202–211
Sandström J, Telang A, Moran NA (2000) Nutritional enhancement of host plants by aphids—a comparison of three aphid species on grasses. J Insect Physiol 46:33–40
Shambaugh GF, Frazier JL, Castell AEM, Coons LB (1978) Antennal sensilla of seventeen aphids (Homoptera: Aphidinae). Int J Insect Morphol Embryol 7:389–404
Stadler B (2004) Wedged between bottom-up and top-down processes: aphids on tansy. Ecol Entomol 29:106–116
Stadler B, Dixon AFG, Kindlmann P (2002) Relative fitness of aphids: effects of plant quality and ants. Ecol Lett 5:216–222
Telang A, Sandström J, Dyreson E, Moran NA (1999) Feeding damage by Diuraphis noxia results in nutritionally enhanced phloem diet. Entomol Exp Appl 91:403–412
Tjallingii WF (1978) Electronic recording of penetration behaviour by aphids. Entomol Exp Appl 24:521–530
Tjallingii WF (1985) Membrane potentials as an indication for plant cell penetration by aphid stylets. Entomol Exp Appl 38:187–193
Tjallingii WF (1988) Electrical recording of stylet penetration activities. In: Minks AK, Harrewijn P (eds) Aphids, their biology, natural enemies and control. Elsevier, Amsterdam, pp 95–108
Tjallingii WF, Hogen Esch T (1993) Fine structure of aphid stylet routes in plant tissues in correlation with EPG signals. Physiol Entomol 18:317–328
Van Giessen WA, Jackson DM (1998) Rapid analysis of electronical monitored homopteran feeding behaviour. Ann Entomol Soc Am 91(1):145–154
Van Helden M, Tjallingii WF (1993) Tissue localisation of lettuce resistance to the aphid Nasonovia ribisnigri using electrical penetration graphs. Entomol Expt Appl 68:269–278
Van Helden M, Tjallingii WF (2000) Experimental design and analysis in EPG experiments with emphasis on plant resistance research. In: Walker GP, Backus EA (eds) Principles and applications of electronic monitoring and other techniques in the study of homopteran feeding behaviour. Say, Entomological Society of America, Lanham, pp 144–171
Woodring J, Wiedemann R, Fischer MK, Hoffmann KH, Völkl W (2004) Honeydew amino acids in relation to sugar and their role in the establishment of ant-attendance hierarchy in eight species of aphids feeding on tansy (Tanacetum vulgare). Physiol Entomol 29:311–319
Acknowledgments
The work was funded by the Deutsche Forschungsgemeinschaft, Graduiertenkolleg 628. The authors are especially grateful to the following members of the University of Bayreuth: S. Bauer for invaluable help in the EPG and stylectomy techniques, Agniezka Tabak and Dr G. Gebauer for help in the soil analysis, Dr H. Rödel for help in statistical analysis and to Drs K.-H. Hoffmann and W. Völkl for helpful discussion of the results. Dr H. Loxdale, University of Jena, invested much work in improving the English, which is very gratefully acknowledged.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Wolfgang Weisser.
Rights and permissions
About this article
Cite this article
Nowak, H., Komor, E. How aphids decide what is good for them: experiments to test aphid feeding behaviour on Tanacetum vulgare (L.) using different nitrogen regimes. Oecologia 163, 973–984 (2010). https://doi.org/10.1007/s00442-010-1652-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-010-1652-y