Original Article
Response of walnut aphid populations to increasing foliar nitrogen content
Kevi C. Mace,
Nicholas J. Mills,
Corresponding Author
Kevi C. Mace
Department of Environmental Science, Policy and Management, University of California, Mulford Hall, Berkeley, CA, 94720-3114 U.S.A
Correspondence: Kevi Mace. Tel.: +1 707 972 4253; fax: 510 642 5903; e-mail: [email protected]Search for more papers by this authorNicholas J. Mills
Department of Environmental Science, Policy and Management, University of California, Mulford Hall, Berkeley, CA, 94720-3114 U.S.A
Search for more papers by this author
Kevi C. Mace,
Nicholas J. Mills,
Corresponding Author
Kevi C. Mace
Department of Environmental Science, Policy and Management, University of California, Mulford Hall, Berkeley, CA, 94720-3114 U.S.A
Correspondence: Kevi Mace. Tel.: +1 707 972 4253; fax: 510 642 5903; e-mail: [email protected]Search for more papers by this authorNicholas J. Mills
Department of Environmental Science, Policy and Management, University of California, Mulford Hall, Berkeley, CA, 94720-3114 U.S.A
Search for more papers by this authorAbstract
- An understanding of how fertilizer input affects pest populations and, consequently, the need for pesticide use would allow for the development of more effective integrated management strategies.
- The present study addressed the response of walnut aphid Chromaphis juglandicola (Kaltenbach) (Hemiptera: Aphididae) populations to different levels of nitrogen application to walnut seedlings and the relationship between aphid density and chlorophyll content index (CCI), a non-invasive measure of foliar nitrogen, for mature trees in commercial walnut orchards.
- Although added nitrogen significantly increased soluble nitrogen content, CCI and soluble nitrogen : phosphorus ratios in the foliage of walnut seedlings, there was no effect on walnut aphid population growth. Similarly, there was no relationship between aphid density and CCI for mature trees in the field.
- A neutral response suggests that walnut aphid population growth on potted seedlings is limited by factors other than soluble nitrogen, such as other nutrients, amino acid composition or defensive compounds. Consequently, fertilizer management appears unlikely to effectively contribute to the control of C. juglandicola in commercial walnut orchards.
References
- Awmack, C.S. & Leather, S.R. (2002) Host plant quality and fecundity in herbivorous insects. Annual Review of Entomology, 47, 817–844.
- Bates, D. (2011) Linear Mixed Model Implementation in lme4. University of Wisconsin, Wisconsin [WWW document]. URL http://www.icesi.edu.co/CRAN/web/packages/lme4/vignettes/Implementation.pdf [accessed on 1 October 2013].
- Behmer, S.T. (2009) Insect herbivore nutrient regulation. Annual Review of Entomology, 54, 165–187.
- Berry, P.M., Sylvester-Bradley, R., Philipps, L., Hatch, D.J., Cuttle, S.P., Rayns, F.W. & Gosling, P. (2002) Is the productivity of organic farms restricted by the supply of available nitrogen? Soil Use and Management, 18, 248–255.
- Bolker, B.M., Brooks, M.E., Clark, C.J., Geange, S.W., Poulsen, J.R., Stevens, M.H.H. & White, J.S. (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology & Evolution, 24, 127–135.
- Broekgaarden, C., Snoeren, T.A., Dicke, M. & Vosman, B. (2011) Exploiting natural variation to identify insect-resistance genes. Plant Biotechnology Journal, 9, 819–825.
- Chau, A., Heinz, K.M. & Davies, F.T. (2005) Influences of fertilization on population abundance, distribution, and control of Frankliniella occidentalis on chrysanthemum. Entomologia Experimentalis et Applicata, 117, 27–39.
- Cisneros, J.J. & Godfrey, L.D. (2001) Midseason pest status of the cotton aphid (Hemiptera: Aphididae) in California cotton: is nitrogen a key factor? Environmental Entomology, 30, 501–510.
- Couture, J.J., Servi, J.S. & Lindroth, R.L. (2010) Increased nitrogen availability influences predator–prey interactions by altering host-plant quality. Chemoecology, 20, 277–284.
- Crawley, M.J. (2013) The R Book, 2nd edn. John Wiley & Sons, U.K.
- Daglish, C. (1950) The determination and occurrence of a hydrojuglone glucoside in the walnut. Biochemical Journal, 47, 458–462.
- Denno, R.F., Gratton, C., Petterson, M.A., Langelloto, G.A., Finke, D.L. & Huberty, A.F. (2002) Bottom-up forces mediate natural-enemy impact in a phytophagous insect community. Ecology, 83, 1443–1458.
- Dixon, A.F.G. (1998) Aphid Ecology: An Optimization Approach. Chapman & Hall, U.K.
- Douglas, A.E. & van Emden, H.F. (2007) Nutrition and symbiosis. Aphids as Crop Pests (ed. by H. F. Emden and R Harrington), pp. 115-130. CABI, U.K.
- van Emden, H.F. & Harrington, R. (2007) Aphids as Crop Pests. CABI Publishing, U.K.
10.1079/9780851998190.0000 Google Scholar
- Forkner, R.E. & Hunter, M.D. (2000) What goes up must come down? Nutrient addition and predation pressure on oak herbivores. Ecology, 81, 1588–1600.
- Frazer, B.D. & Van den Bosch, R. (1973) Biological control of the walnut aphid in California: the interrelationship of the aphid and its parasite. Environmental Entomology, 2, 561–568.
10.1093/ee/2.4.561 Google Scholar
- Garratt, M.P., Leather, S.R. & Wright, D.J. (2010) Tritrophic effects of organic and conventional fertilisers on a cereal-aphid-parasitoid system. Entomologia Experimentalis et Applicata, 134, 211–219.
- Gash, A.F. (2012) Wheat nitrogen fertilisation effects on the performance of the cereal aphid Metopolophium dirhodum. Agronomy, 2, 1–13.
10.3390/agronomy2010001 Google Scholar
- Hansen, A.K. & Moran, N.A. (2014) The impact of microbial symbionts on host plant utilization by herbivorous insects. Molecular Ecology, 23, 1473–1496.
- Herms, D.A. & Mattson, W.J. (1992) The dilemma of plants: to grow or defend. Quarterly Review of Biology, 67, 283–335.
- Hosseini, M., Ashouri, A., Enkegaard, A., Goldansaz, S.H., Mahalati, M.N. & Hosseininaveh, V. (2010) Performance and population growth rate of the cotton aphid, and associated yield losses in cucumber, under different nitrogen fertilization regimes. International Journal of Pest Management, 56, 127–135.
- Hougardy, E. & Mills, N.J. (2008) Comparative life history and parasitism of a new colour morph of the walnut aphid in California. Agricultural and Forest Entomology, 10, 137–146.
- Hougardy, E. & Mills, N.J. (2009) Factors influencing the abundance of Trioxys pallidus, a successful introduced biological control agent of walnut aphid in California. Biological Control, 48, 22–29.
- Huberty, A.F. & Denno, R.F. (2004) Plant water stress and its consequences for herbivorous insects: a new synthesis. Ecology, 85, 1383–1398.
- Jones, V.P., Steffan, S.A., Hull, L.A., Brunner, J.F. & Biddinger, D.J. (2010) Effects of the loss of organophosphate pesticides in the US: opportunities and needs to improve IPM programs. Outlooks on Pest Management, 21, 161–166.
- Kagata, H. & Ohgushi, T. (2006) Bottom-up trophic cascades and material transfer in terrestrial food webs. Ecological Research, 21, 26–34.
- Koricheva, J., Larsson, S., Haukioja, E. & Keinänen, M. (1998) Regulation of woody plant secondary metabolism by resource availability: hypothesis testing by means of meta-analysis. Oikos, 83, 212–226.
- Krauss, J., Haerri, S.A., Bush, L., Husi, R., Bigler, L., Power, S.A. & Mueller, C.B. (2007) Effects of fertilizer, fungal endophytes and plant cultivar on the performance of insect herbivores and their natural enemies. Functional Ecology, 21, 107–116.
- Kytö, M., Niemelä, P. & Larsson, S. (1996) Insects on trees: population and individual response to fertilization. Oikos, 75, 148–159.
- Latham, D.R. & Mills, N.J. (2010) Life history characteristics of Aphidius transcaspicus, a parasitoid of mealy aphids (Hyalopterus species). Biological Control, 54, 147–152.
- Maxwell, F. & Jennings, P.R. (1980) Breeding Plants Resistant to Insects. John Wiley & Sons, U.K.
- McCallum, H. (2000) Population Parameters: Estimation for Ecological Models. Wiley-Blackwell, U.K.
- Mediene, S., Jordan, M.O., Pages, L., Lebot, J. & Adamowicz, S. (2002) The influence of severe shoot pruning on growth, carbon and nitrogen status in young peach trees (Prunus persica). Tree Physiology, 22, 1289–1296.
- Miller, R. (1998) Extractable chloride, nitrate, orthophosphate, potassium, and sulfate-sulfur in plant tissue: 2% acetic acid extraction. Handbook of Reference Methods for Plant Analysis, pp. 115–119. CRC Press, Boca Raton, Florida.
- Nakagawa, S. & Schielzeth, H. (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods in Ecology and Evolution, 4, 133–142.
- Nevo, E. & Coll, M. (2001) Effect of nitrogen fertilization on Aphis gossypii (Hemiptera: Aphididae): variation in size, color, and reproduction. Journal of Economic Entomology, 94, 27–32.
- Niks, R.E., Parlevliet, J., Lindhout, P. & Bai, Y. (2011) Breeding Crops with Resistance to Diseases and Pests. Wageningen Academic Publishers, The Netherlands.
10.3920/978-90-8686-171-2 Google Scholar
- Noma, T., Gratton, C., Colunga-Garcia, M., Brewer, M.J., Mueller, E.E., Wyckhuys, K.A. & O'Neal, M.E. (2010) Relationship of soybean aphid (Hemiptera: Aphididae) to soybean plant nutrients, landscape structure, and natural enemies. Environmental Entomology, 39, 31–41.
- Nowak, H. & Komor, E. (2010) 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.
- Olson, D.M., Cortesero, A.M., Rains, G.C., Potter, T. & Lewis, W.J. (2009) Nitrogen and water affect direct and indirect plant systemic induced defense in cotton. Biological Control, 49, 239–244.
- Pickel, C., Grant, J.A., Bentley, W.J., Hasey, J.K., Cotes, W.W. & Van Steenwek, R.A. (2014) UC IPM Pest Management Guidelines: Walnut. University of California, California [WWW document]. URL http://www.ipm.ucdavis.edu/PMG/r881300511.html [accessed on 1 March 2012].
- Piskorski, R., Ineichen, S. & Dorn, S. (2011) Ability of the oriental fruit moth Grapholita molesta (Lepidoptera: Tortricidae) to detoxify juglone, the main secondary metabolite of the non-host plant walnut. Journal of Chemical Ecology, 37, 1110–1116.
- Prokopy, W. (1995) Phosphorus in acetic acid extracts. QuikChem Method, pp. 12–115. Lachat Instruments, Milwaukee, Wisconsin.
- Ramos, D.E. (1997) Walnut Production Manual. University of California Agricultural and Natural Resources Publications, Oakland, California.
- R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Austria [WWW document]. URL http://www.R-project.org/ [accessed on 1 February 2013].
- Richardson, A.D., Duigan, S.P. & Berlyn, G.P. (2002) An evaluation of noninvasive methods to estimate foliar chlorophyll content. New Phytologist, 153, 185–194.
- Ryan, G.D., Rasmussen, S., Xue, H., Parsons, A.J. & Newman, J.A. (2014) Metabolite analysis of the effects of elevated CO2 and nitrogen fertilization on the association between tall fescue (Schedonorus arundinaceus) and its fungal symbiont Neotyphodium coenophialum. Plant, Cell & Environment, 37, 204–212.
- Sauge, M., Grechi, I. & Poëssel, J. (2010) Nitrogen fertilization effects on Myzus persicae aphid dynamics on peach: vegetative growth allocation or chemical defence? Entomologia Experimentalis et Applicata, 136, 123–133.
- Schüepp, C., Uzman, D., Herzog, F. & Entling, M.H. (2014) Habitat isolation affects plant–herbivore–enemy interactions on cherry trees. Biological Control, 71, 56–64.
- Sechtig, A. (1992) Determination of nitrate in 2 M KCl soil extracts by flow injection analysis. QuickChem Method, pp. 12–107. Lachat Instruments, Milwaukee, Wisconsin.
- Shigenobu, S. & Wilson, A.C. (2011) Genomic revelations of a mutualism: the pea aphid and its obligate bacterial symbiont. Cellular and Molecular Life Sciences, 68, 1297–1309.
- Sterner, R. & Elser, J. (2002) Ecological Stoichiometry: The Biology of Elements from Molecules to the Biosphere. Princeton University Press, Princeton, New Jersey.
- Stiling, P. & Rossi, A.M. (1997) Experimental manipulations of top-down and bottom-up factors in a tri-trophic system. Ecology, 78, 1602–1606.
- Tao, L. & Hunter, M.D. (2012) Does anthropogenic nitrogen deposition induce phosphorus limitation in herbivorous insects? Global Change Biology, 18, 1843–1853.
- Vannette, R.L. & Hunter, M.D. (2011) Plant defence theory re-examined: nonlinear expectations based on the costs and benefits of resource mutualisms. Journal of Ecology, 99, 66–76.
- Vos, J. & Bom, M. (1993) Hand-held chlorophyll meter: a promising tool to assess the nitrogen status of potato foliage. Potato Research, 36, 301–308.
- Zehnder, C.B. & Hunter, M.D. (2009) More is not necessarily better: the impact of limiting and excessive nutrients on herbivore population growth rates. Ecological Entomology, 34, 535–543.