Abstract
Cereal aphids (Homoptera: Aphididae) are a periodical threat to winter wheat (Triticum aestivum L.) production worldwide, and outbreaks have been mainly related to increasing inputs of mineral fertilizers. The hypothesis of lower aphid abundance under organic fertilizer treatments, however, has not been tested at the species-specific level. In a 4-year study, we examined cereal aphid populations and plant parameters (dry biomass and nitrogen content) in winter wheat fields under low (legume-based), intermediate (legume-based plus organic liquid manure), and high (mineral) nitrogen intensities; low and intermediate intensities are characteristic of organic fields, while high intensities are inherent in conventional farming systems. Aphid species differed markedly in their response to fertilizer treatment. Unexpectedly, legume-based organic fields were related to higher abundances of the ear-colonizing species Sitobion avenae (F.), whereas manure-fertilized organic fields and conventional fields had significantly higher abundances of Metopolophium dirhodum (Wlk.) and Rhopalosiphum padi (L.). Nitrogen concentration of winter wheat increased with fertilizer intensity, and total aphid abundance (all species) was positively correlated with nitrogen content of grains in manure-fertilized organic fields and conventional fields, but was not correlated in legume-based organic fields dominated by S. avenae (89–96 % of the aphid community). Collectively, we demonstrate strong bottom-up effects that result in an improved performance of S. avenae in low-input systems. As total aphid abundance (all species) simultaneously decreased in legume-based organic fields, crop managers risk to underestimate pest damage by ignoring the impact of a single species, S. avenae, which has the greatest potential to reduce crop yield.
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References
Alyokhin A, Porter G, Groden E, Drummond F (2005) Colorado potato beetle response to soil amendments: a case in support of the mineral balance hypothesis? Agric Ecosys Environ 109:234–244
Altieri MA, Nicholls CI (2003) Soil fertility management and insect pests: harmonizing soil and plant health in agroecosystems. Soil Till Res 72:203–211
Ankersmit GW (1989) Integrated control of cereal aphids. In: Minks AK, Harrewijn P (eds) Aphids, Their Biology, Natural Enemies and Control, vol 2C. Elsevier, Amsterdam, pp 273–277
Aqueel MA, Leather SR (2011) Effect of nitrogen fertilizer on the growth and survival of Rhopalosiphum padi (L.) and Sitobion avenae (F.) (Homoptera: Aphididae) on different wheat cultivars. Crop Prot 30:216–221
Awmack CS, Leather SR (2002) Host plant quality and fecundity in herbivorous insects. Annu Rev Entomol 47:817–844
Basedow T, Poehling H-M, Lauenstein G (1994) Studies on the adaption of the control for non viruliferous cereal aphids attacking winter wheat in summer to the new economic conditions of agriculture. J Plant Dis Prot 101:337–349
Bengtsson J, Ahnstrom J, Weibull AC (2005) The effects of organic agriculture on biodiversity and abundance: a meta-analysis. J Appl Ecol 42:261–269
Birkhofer K et al (2008) Long-term organic farming fosters below and aboveground biota: implications for soil quality, biological control and productivity. Soil Biol Biochem 40:2297–2308
Ciepiela A (1989) Biochemical basis of winter wheat resistance to the grain aphid, Sitobion avenae (F.). Entomol Exp Appl 51:269–275
Ciepiela AP, Sempruch C, Chrzanowski G (1999) Evaluation of natural resistance of winter triticale cultivars to grain aphid using food coefficients. J Appl Entomol 123:491–494
Dangour AD, Dodhia SK, Hayter A, Allen E, Lock K, Uauy R (2009) Nutritional quality of organic foods: a systematic review. Am J Clin Nutr 90:680–685
De Barro PJ, Sherratt TN, David O, Maclean N (1995) An investigation of the differential performance of clones of the aphid Sitobion avenae on two host species. Oecologia 104:379–385
Duffield SJ, Bryson RJ, Young JEB, Sylvester-Bradley R, Scott RK (1997) The influence of nitrogen fertiliser on the population development of the cereal aphids Sitobion avenae (F.) and Metopolophium dirhodum (Wlk.) on field grown winter wheat. Ann Appl Biol 130:13–26
Dumas JB (1981) Sur les procédés de l'analyse organique. Ann Chim 67:195–213
FIBL-IFOAM (2011) The world of organic agriculture. Statistics and emerging trends. FIBL-IFOAM report. IFOAM and Frick, FIBL, Bonn
Freier B, Triltsch H, Möwes M, Moll E (2007) The potential of predators in natural control of aphids in wheat: results of a ten-year field study in two German landscapes. BioControl 52:775–788
Garratt MPD, Wright DJ, Leather SR (2010a) The effects of organic and conventional fertilizers on cereal aphids and their natural enemies. Agr Forest Entomol 12:307–318
Garratt MPD, Leather SR, Wright DJ (2010b) Tritrophic effects of organic and conventional fertilisers on a cereal-aphid-parasitoid system. Entomol Exp Appl 134:211–219
Hambäck PA, Vogt M, Tscharntke T, Thies C, Englund G (2007) Top-down and bottom-up effects on the spatiotemporal dynamics of cereal aphids: testing scaling theory for local density. Oikos 116:1995–2006
Hasken K-H, Poehling M (1995) Effects of different intensities of fertilisers and pesticides on aphids and aphid predators in winter wheat. Agric Ecosys Environ 52:45–50
Honek A (1985) Plant density and abundance of cereal aphids (Hom., Aphidina). J Appl Entomol 100:309–316
Honek A, Martinkova Z (2002) Factors of between- and within- plant distribution of Metopolophium dirhodum (Hom., Aphididae) on small grain cereals. J Appl Entomol 126:378–383
Honek A, Martinkova Z (2004) The effect of environmentally induced variation of host-plant vigour on abundance of cereal aphids. In: Simon J-C, Dedryver C-A, Rispe C, Hullé M (eds) Aphids in a new millennium. INRA Editions, Versailles, pp 319–324
Horber E (1980) Types and classification of resistance. In: Maxwell FG, Jennings PR (eds) Breeding plant resistance to insects. Wiley, New York, pp 15–21
Ke X, Scheu S (2008) Earthworms, Collembola and residue management change wheat (Triticum aestivum) and herbivore pest performance (Aphidina: Rhopalosiphum padi). Oecologia 157:603–617
Khan M, Port G (2008) Performance of clones and morphs of two cereal aphids on wheat plants with high and low nitrogen content. Entomol Science 11:159–165
Kowalski R, Visser PE (1979) Nitrogen in a crop-pest interaction: cereal aphids. In: Lee JA (ed) Nitrogen as an ecological parameter. Blackwell Scientific Publications, Oxford, pp 67–74
Leather SR (1993) Overwintering in six arable aphid pests: a review with particular relevance to pest-management. J Appl Entomol 116:217–233
Letourneau DK (1988) Soil management for pest control: a critical appraisal of the concepts. In: Proceedings of the sixth international scientific conference of IFOAM on global perspectives on agroecology and sustainable agricultural systems. Santa Cruz, CA, pp 581–587
Lancashire PD, Bleiholder H, Langelüddecke P, Stauss R, Van den Boom T, Weber E, Witzenberger A (1991) An uniform decimal code for growth stages of crops and weeds. Ann Appl Biol 119:561–601
Merrill MC (1983) Bio-agriculture: a review of its history and philosophy. Biol Agric Hortic 1:181–210
Mattson WJ (1980) Herbivory in relation to plant nitrogen content. Annu Rev Ecol Syst 11:119–168
Niehoff B, Stäblein J (1998) Vergleichende Untersuchungen zum Schadpotential der Getreideblattlausarten Metopolophium dirhodum (WIk.) und Sitobion avenae (F.) in Winterweizen. J Appl Entomol 122:223–229
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
Östman Ö, Ekbohm B, Bengtsson J (2001) Landscape heterogeneity and farming practice influence biological control. Basic Appl Ecol 2:365–371
Phelan PL, Mason JF, Stinner BR (1995) Soil-fertility management and host preference by European corn borer, Ostrinia nubilalis (Hiibner), on Zea mays L.: A comparison of organic and conventional chemical farming. Agric Ecosys Environ 56:1–8
Ponder KL, Pritchard J, Harrington R, Bale JS (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
Powell G, Tosh CR, Hardie J (2006) Host plant selection by aphids: behavioral, evolutionary, and applied perspectives. Annu Rev Entomol 51:309–330
Roschewitz I, Hücker M, Tscharntke T, Thies C (2005) The influence of landscape context and farming practices on parasitism of cereal aphids. Agric Ecosys Environ 108:218–227
Rosswall T, Paustian K (1984) Cycling of nitrogen in modern agricultural systems. Plant Soil 76:3–21
Ruppel RF (1983) Cumulative insect-days as an index of crop protection. J Econ Entomol 76:375–377
Schütz K, Bonkowski M, Scheu S (2008) Effects of Collembola and fertilizers on plant performance (Triticum aestivum) and aphid reproduction (Rhopalosiphum padi). Basic Appl Ecol 9:182–188
Staley JT, Stewart-Jones A, Pope TW, Wright DJ, Leather SR, Hadley P, Rossiter JT, van Emden HF, Poppy GM (2010) Varying responses of insect herbivores to altered plant chemistry under organic and conventional treatments. Proc R Soc Lond B 277:779–786
Suding KN, Collins SL, Gough L, Clark C, Cleland EE, Gross KL, Milchunas DG, Pennings S (2005) Functional- and abundance-based mechanisms explain diversity loss due to N-fertilization. Proc Natl Acad Sci U S A 102:4387–4392
Thies C et al (2011) The relationship between agricultural intensification and biological control: experimental tests across Europe. Ecol Appl 21:2187–2196
Tscharntke T, Klein A-M, Kruess A, Steffan-Dewenter I, Thies C (2005) Landscape perspectives on agricultural intensification and biodiversity-ecosystem service management. Ecol Lett 8:857–874
van Emden HF (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
Zehnder G, Gurr GM, Kühne S, Wade MR, Wratten SD, Wyss E (2007) Arthropod pest management in organic crops. Annu Rev Entomol 52:57–80
Acknowledgments
The study is part of the “Forschungsprojekt Hof Ritzerau” funded by G. Fielmann. We thank Ralf Loges for establishing manure-amended winter wheat plots in 2005 and 2006.
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ESM 1
Parasitoid-host ratios and vegetation-dwelling predator-prey ratios of Syrphidae (larvae), Coccinellidae (larvae), and Chrysopidae (larvae) in conventional and organic winter wheat fields and in manure-fertilized and non-manure-fertilized organic winter wheat plots at different plant growth (BBCH) stages. Arithmetic means ± SD are given. Parasitoid-host ratios were calculated as the number of parasitoids (mummies) divided by the number of all aphids (aphid hosts plus mummies). Predator-prey ratios were calculated as the number of vegetation-dwelling predators divided by the number of all aphids (aphid hosts plus mummies) (DOC 39.5 kb)
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Lohaus, K., Vidal, S. Nitrogen supply in conventional versus organic farming systems: effects on the performance of cereal aphids. Org. Agr. 3, 129–139 (2013). https://doi.org/10.1007/s13165-013-0051-1
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DOI: https://doi.org/10.1007/s13165-013-0051-1