Abstract
Excessive mineral fertilizer input results in little extra yield but exacerbates insect herbivory and affects environmental health and ecosystem services. The use of organic fertilizer is considered to have promise for mitigating those impacts. How organic fertilizer amendment modifies crop resistance to insect herbivory and modulates biocontrol services on a landscape scale has not been well studied. We conducted a series of field experiments on a large spatial scale with three fertilization regimes (mineral fertilizer, mineral fertilizer amended with organic matter, and no fertilizer control) in Shandong Province, northern China. Soil nutrient content, wheat plant metabolism, cereal aphid abundance, parasitism rate, and wheat yield were quantified. Maize straw amendment combined with mineral fertilization significantly reduced cereal aphid abundance and promoted parasitism during the peak aphid period, compared with mineral fertilizer alone and the no fertilizer control. Modeling simulations showed increased biological pest control when a larger proportion of fields were additionally treated with maize straw amendment. Foliar chemical analyses revealed that the types and content of plant free amino acids, rather than plant defensive compounds, most likely accounted for the variation in aphid abundance and biological control efficiency. A mineral fertilization regime plus plant straw amendment may promote wheat resistance to herbivory and benefit biocontrol via bottom-up effects. Heterogeneity in fertilizer regimes between fields may be the key ecological force shaping pest control at a landscape scale.
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References
Altieri MA, Nicholls CI (2003) Soil fertility management and insect pests: harmonizing soil and plant health agroecosystems. Soil Till Res 72:203–211
Aqueel MA, Raza AM, Balal RM, Shahid MA, Mustafa I, Javaid MM, Leather SR (2015) Tritrophic interactions between parasitoids and cereal aphids are mediated by nitrogen fertilizer. Insect Sci 22:813–820
Baillod AB, Tscharntke T, Clough Y, Batary P (2017) Landscape-scale interactions of spatial and temporal cropland heterogeneity drive biological control of cereal aphids. J Appl Ecol 54:1804–1813
Banfield-Zanin JA, Rossiter JT, Wright DJ, Leather SR, Staley JT (2012) Predator mortality depends on whether its prey feeds on organic or conventionally fertilised plants. Bio Control 63:56–61
Bastos LM, Carciochi W, Lollato RP, Jaenisch BR, Rezende CR, Schwalbert R, Vara Prasad PV, Zhang G, Fritz AK, Foster C, Wright Y, Young S, Bradley P, Ciampitti IA (2020) Winter wheat yield response to plant density as a function of yield environment and tillering potential: a review and field studies. Front Plant Sci 11:54
Beduschi T, Kormann UG, Tscharntke T, Scherber C (2018) Spatial community turnover of pollinators is relaxed by semi-natural habitats, but not by mass-flowering crops in agricultural landscapes. Bio Conserv 221:59–66
Bianchi FJJA, Booij CJH, Tscharntke T (2006) Sustainable pest regulation in agricultural landscapes: a review on landscape composition, biodiversity and natural pest control. P Roy Soc B-Biol Sci 273:1715–1727
Bianchi FJJA, Schellhorn NA, Buckley YM, Possingham HP (2010) Spatial variability in ecosystem services: simple rules for predator-mediated pest suppression. Ecol Appl 20:2322–2333
Birkhofer K, Bezemer TM, Bloem J, Bonkowski M, Christensen S, Dubois D, Ekelund F, Fließbach A, Gunst L, Hedlund K, Mäder P, Mikola J, Robin C, Setälä H, Tatin-Froux F, Van der Putten WH, Scheu S (2008) Long-term organic farming fosters below and above ground biota: implications for soil quality, biological control and productivity. Soil Biol Biochem 40:2297–2308
Bommarco R, Banks JE (2003) Scale as modifier in vegetation diversity experiments: effects on herbivores and predators. Oikos 102:440–448
Bommarco R, Kleijn D, Potts SG (2013) Ecological intensification: harnessing ecosystem services for food security. Trends Ecol Evol 28:230–238
Butler J, Garratt MPD, Leather SR (2012) Fertilizers and insect herbivores: a meta-analysis. Ann Appl Biol 161:223–233
Cao HH, Zhang ZF, Wang XF, Liu TX (2018) Nutrition versus defense: Why Myzus persicae (green peach aphid) prefers and performs better on young leaves of cabbage. PLoS ONE 13:e0196219
Cassman KG (1999) Ecological intensification of cereal production systems: yield potential, soil quality, and precision agriculture. P Natl Acad Sci USA 96:5952–5959
Comadira G, Rasool B, Karpinska B, Morris J, Verrall SR, Hedley PE, Foyer CH, Hancock RD (2015) Nitrogen deficiency in barley (Hordeum vulgare) seedlings induces molecular and metabolic adjustments that trigger aphid resistance. J Exp Bot 66:3639–3655
Comte I, Colin F, Grunberger O, Follain S, Whalen JK, Caliman J (2013) Landscape-scale assessment of soil response to long-term organic and mineral fertilizer application in an industrial oil palm plantation, Indonesia. Agr Ecosyst Environ 169:58–68
Cusumano A, Zhu F, Volkoff A, Verbaarschot P, Bloem J, Vogel H, Dicke M, Poelman EH (2018) Parasitic wasp-associated symbiont affects plant-mediated species interactions between herbivores. Ecol Lett 21:957–967
Douglas AE (2006) Phloem-sap feeding by animals: problems and solutions. J Exp Bot 57:747–754
Englund G, Leonardsson K (2008) Scaling up the functional response for spatially heterogeneous systems. Ecol Lett 11:440–449
Evans EW (2018) Dispersal in host-parasitoid interactions: crop colonization by pests and specialist enemies. Insects 9:134
Evans EW, Bolshakova VLJ, Carlile NR (2015) Parasitoid dispersal and colonization lag in disturbed habitats: biological control of cereal leaf beetle metapopulations. J Appl Entomol 139:529–538
Foley JA, Ramankutty NR, Brauman K, Cassidy ES, Gerber JS, Johnston M, Mueller ND, O’Connell C, Ray DK, West PC, Balzer C, Bennett EM, Carpenter SR, Hill J, Monfreda C, Polasky S, Rockström J, Sheehan J, Siebert S, Tilman D, Zaks DPM (2011) Solutions for a cultivated planet. Nature 478:337–342
Gao J, Guo HJ, Sun YC, Ge F (2018) Differential accumulation of leucine and methionine in red and green pea aphids leads to different fecundity in response to nitrogen fertilization. Pest manag Sci 74:1779–1789
Garratt MPD, Leather SR, Wright DJ (2010) Tritrophic effects of organic and conventional fertilizers on a cereal-aphid-parasitoid system. Entomol Exp Appl 134:211–219
Garratt MPD, Wright DJ, Leather SR (2011) The effects of farming system and fertilizers on pests and natural enemies: a synthesis of current research. Agr Ecosyst Environ 141:261–270
Garratt MPD, Bommarco R, Kleijn D, Martin E, Mortimer SR, Redlich S, Senapathi D, Steffan-Dewenter I, Świtek S, Takács V, van Gils S, van der Putten WH, Pott SG (2018) Enhancing soil organic matter as a route to the ecological intensification of European arable systems. Ecosyst 21:1404–1415
Ghaley BB, Wösten H, Olesen JE, Schelde K, Baby S, Karki YK, Børgesen CD, Smith P, Yeluripati J, Ferrise R, Bindi M, Kuikman P, Lesschen JP, Porter JR (2018) Simulation of soil organic carbon effects on long-term winter wheat (Triticum aestivum) production under varying fertilizer inputs. Front Plant Sci 9:1158
Han P, Desneux N, Michel T, Bot JL, Seassau A, Wajnberg E, Amiens-Desneux E, Lavoir A (2016) Does plant cultivar difference modify the bottom-up effects of resource limitation on plant-insect herbivore interactions? J Chem Ecol 42:1293–1303
Han P, Becker C, Sentis A, Rostás M, Desneux N, Lavoir A (2019a) Global change-driven modulation of bottom-up forces and cascading effects on biocontrol services. Curr Opin Insect Sci 35:27–33
Han P, Desneux N, Becker A, Larbat R, Bot JL, Adamowicz S, Zhang J, Lavoir A (2019b) Bottom-up effects of irrigation, fertilization and plant resistance on Tuta absoluta: implication for Integrated Pest Management. J Pest Sci 92:1359–1370
Honek A, Jarosik V, Dixon AFG (2006) Comparing growth patterns among field populations of cereal aphids reveals factors limiting their maximum abundance. Bull Entomol Res 96:269–277
Isbell F, Adler PR, Eisenhauer N, Fornara D, Kimmel K, Kremen C, Letourneau DK, Liebman M, Polley HW, Quijas S, Scherer-Lorenzen M (2017) Benefits of increasing plant diversity in sustainable agroecosystems. J Ecol 105:871–879
Islam MN, Hasanuzzaman ATM, Zhang ZF, Zhang Y, Liu T (2017) High level of nitrogen makes tomato plants releasing less volatiles and attracting more Bemisia tabaci (Hemiptera: Aleyrodidae). Front Plant Sci 8:466
Jakobs R, Schweiger R, Müller C (2018) Aphid infestation leads to plant part-specific changes in phloem sap chemistry, which may indicate niche construction. New Phytol 221:503–514
Karp DS, Chaplin-Kramer R, Meehan TD et al (2018) Crop pests and predators exhibit inconsistent responses to surrounding landscape composition. P Natl Acad Sci USA 115:7863–7870
Karungi J, Ekbom B, Kyamanywa S (2006) Effects of organic versus conventional fertilizers on insect pests, natural enemies and yield of Phaseolus vulgaris. Agr Ecosyst Environ 115:51–55
Kassambara A (2016) ggcorrplot: visualization of a correlation matrix using ‘ggplot2’. R package version 0.1.1
Lohaus K, Vidal S, Thies C (2013) Farming practices change food web structures in cereal aphid-parasitoid-hyperparasitoid communities. Oecologia 171:249–259
Matson PA, Parton WJ, Power AG, Swift MJ (1997) Agricultural intensification and ecosystem properties. Science 277:504–509
Melbourne BA, Chesson P (2006) The scale transition: scaling up population dynamics with field data. Ecol 87:1478–1488
Morales H, Perfecto I, Ferguson B (2001) Traditional fertilization and its effect on corn insect population in the Guatemalan highlands. Agr Ecosyst Environ 84:145–155
Muneret L, Mitchell M, Seufert V, Aviron S, Djoudi EA, Pétillon J, Plantegenest M, Thiéry D, Rusch A (2018) Evidence that organic farming promotes pest control. Nat Sustain 1:361–368
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara B, Simpson GL, Solymos P, Stevens H, Wagner HH (2016) vegan: community ecology package. R package version 2.3–5
Peresneto PR, Legendre P, Dray S, Borcard D (2006) Variation partitioning of species data matrices: estimation and comparison of fractions. Ecol 87:2614–2625
Petermann JS, Muller CB, Roscher C, Weigelt A, Weisser WW, Schmid B (2010) Plant species loss affects life-history traits of aphids and their parasitoids. PLoS ONE 5:e12053
Petersen MK, Sandström JP (2001) Outcome of indirect competition between two aphid species mediated by responses in their common host plant. Funct Ecol 15:525–534
R core team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Ramsden M, Menendez R, Leather S, Wackers F (2016) Do natural enemies really make a difference? field scale impacts of parasitoid wasps and hoverfly larvae on cereal aphid population. Agr Forest Entomol 19:139–145
Rashid MM, Ahmed N, Jahan M, Islam KS, Nansen C, Willers JL, Ali MP (2017) Higher fertilizer inputs increase fitness traits of Brown Planthopper in rice. Sci Rep-UK 7:4719
Rusch A, Bommarco R, Ekbom B (2017) Conservation biological control in agricultural landscapes. Adv Bot Res 81:333–360
Sandstrom JP, 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
Sarfraz M, Dosdall LM, Keddie BA (2009) Host plant nutritional quality affects the performance of the parasitoid Diadegma insulare. Biol Control 51:34–41
Schellhorn NA, Bianchi FJJA, Hsu CL (2014) Movement of entomophagous arthropods in agricultural landscapes: links to pest suppression. Annu Rev Entomol 59:559–581
Schellhorn NA, Parry HR, Macfadyen S, Wang Y, Zalucki MP (2015) Connecting scales: achieving in-field pest control from areawide and landscape ecology studies. Insect Sci 22:35–51
Sønderby IE, Geu-Flores F, Halkier BA (2010) Biosynthesis of glucosinolates–gene discovery and beyond. Trends Plant Sci 15:283–290
Tilman D, Fargione J, Wolff B, D’Antonio C, Dobson A, Howarth R, Schindler D, Schlesinger WH, Simberloff D, Swackhamer D (2001) Forecasting agriculturally driven global environmental change. Science 292:281–284
Tittonell P (2014) Ecological intensification of agriculture–sustainable by nature. Curr Opin Environ Sustain 8:53–61
Tscharntke T, Karp DS, Chaplin-Kramer R et al (2016) When natural habitat fails to enhance biological pest control–five hypotheses. Biol Conserv 204:449–458
Tsiafouli MA, Thebault E, Sgardelis SP, de Ruiter PC, Van der Putten WH, Birkhofer K, Hemerik L, de Vries FT, Bardgett RD, Brady MV, Bjornlund L, Jørgensen HB, Christensen S, Hertefeldt DT, Hotes S, Hol WHG, Frouz J, Liiri M, Mortimer SR, Setälä H, Tzanopoulos J, Uteseny K, Pižl V, Stary J, Wolters V, Hedlund K (2015) Intensive agriculture reduces soil biodiversity across Europe. Global Change Biol 21:973–985
Wale M, Schulthess F, Kairu EW, Omwega CO (2006) Cereal yield losses caused by lepidopterous stemborers at different nitrogen fertilizer rates in Ethiopia. J Appl Entomol 130:220–229
Weber D, Egan PA, Muola A, Ericson LE, Stenberg JA (2020) Plant resistance does not compromise parasitoid-based biocontrol of a strawberry pest. Sci Rep 10:5899
Wetzel WC, Kharouba HM, Robinson M, Holyoak M, Karban R (2016) Variability in plant nutrients reduces insect herbivore performance. Nature 539:425–427
Winfree R, Reilly JR, Bartomeus I, Cariveau DP, Williams NM, Gibbs J (2018) Species turnover promotes the importance of bee diversity for crop pollination at regional scales. Science 359:791–793
Zeier J (2013) New insights into the regulation of plant immunity by amino acid metabolic pathways. Plant Cell Environ 36:2085–2103
Zhao ZH, Hui C, He DH, Li BL (2015) Effects of agricultural intensification on ability of natural enemies to control aphids. Sci Rep-UK 5:8024
Zhou SQ, Lou Y, Tzin V, Jander G (2015) Alteration of plant primary metabolism in response to insect herbivory. Plant Physiol 169:1488–1498
Zytynska SE, Preziosi RF (2013) Host preference of plant genotype is altered by intraspecific competition in a phytophagous insect. Arthropod-Plant Inte 7:349–357
Acknowledgements
We thank Yi Wang, Yao Wang, and Yanhui Wang who helped in sample collection. We are also grateful to Chao Li and Fei Qiao for large spatial scale participants’ arrangement, investigation and supplying dataset. This research was funded by National Key Research and Development Plan, Grant/Award Number: 2017YFD0200600 and National Key R&D Program of China (2017YFD0200400). The authors declare that they have no conflict of interests or personal relationships that could have influenced the work reported in this paper.
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Gu, S., Zalucki, M.P., Men, X. et al. Organic fertilizer amendment promotes wheat resistance to herbivory and biocontrol services via bottom-up effects in agroecosystems. J Pest Sci 95, 339–350 (2022). https://doi.org/10.1007/s10340-021-01377-0
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DOI: https://doi.org/10.1007/s10340-021-01377-0