Nitrogen fertilizer promotes the rice pest Nilaparvata lugens via impaired natural enemy, Anagrus flaveolus, performance


The application of nitrogen (N) fertilizers to agricultural crops is a common practice globally and a crucial component in the current levels of productivity. Excessive N use, however, is costly and damaging to ecosystems. It is recognized that overuse of N fertilizer can promote pest herbivores by enhancing host plant nutritional quality, but less is known of the effects of N on natural enemies of pests via improved quality and availability of prey, and how these may cascade to indirect effects on pests. Here, we explored the effects of N fertilizer on a key egg parasitiod of Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) (brown planthopper, BPH). Application of N to rice plants significantly prolonged the development time of Anagrus flaveolus (Hymenoptera: Mymaridae), increased wing size and decreased fecundity of adult females. Importantly, N application to rice plants significantly decreased the per capita parasitism of BPH eggs by A. flaveolus. Utilizing planthopper prey on N-treated rice plants led to reduced searching efficiency of A. flaveolus. Ultimately, the strength of biological control exerted by A. flaveolus was negatively affected by nitrogen application under field conditions. Parasitoids were able to discriminate between BPH infested rice plants with different levels of nitrogen using visual plant cues. We conclude that N fertilizer use can have profound effects on natural enemy efficiency which potentially increase the dependence on insecticides, another potentially hazardous input.

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  1. Aqueel MA, Raza AB, 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.

  2. Brown JWL, Eisner T, Whittaker RH (1970) Allomones and kairomones: transspecific chemical messengers. Bioscience 20:21–22.

  3. Cohen MB, Alam SN, Medina EB, Bernal CC (1997) Brown planthopper, Nilaparvata lugens, resistance in rice cultivar IR64: mechanism and role in successful N. lugens management in Central Luzon, Philippines. Entomol Exp Appl 85:221–229.

  4. Cook AG, Perfect TJ (1989) The population characteristics of the brown planthopper Nilaparvata lugens, in the Philippines. Ecol Entomol 14:1–9.

  5. English-Loeb G, Rhainds M, Martinson T, Ugine T (2003) Influence of flowering cover crops on Anagrus parasitoids (Hymenoptera: Mymaridae) and Erythroneura leafhoppers (Homoptera: Cicadellidae) in New York vineyards. Agric Forest Entomol 5:173–181.

  6. Garratt MPD, Wright DJ, Leather SR (2010) The effects of organic and conventional fertilizers on cereal aphids and their natural enemies. Agric Forest Entomol 12:307–318.

  7. Gurr GM, Liu J, Read DMY, Catindig JLA, Cheng JA, Lan LP, Heong KL (2011) Parasitoids of Asian rice planthopper (Hemiptera: Delphacidae) pests and prospects for enhancing biological control by ecological engineering. Ann Appl Biol 158:149–176.

  8. Gurr GM, Wratten SD, Landis DA, You MS (2017) Habitat management to suppress pest populations: progress and prospects. Annu Rev Entomol 62:91–109.

  9. Heong KL, Hardy B (2009) Planthoppers: new threats to the sustainability of intensive rice production systems in Asia. International Rice Research Institute, Los Baños

  10. Hopper KR, Diers BW (2014) Parasitism of soybean aphid by Aphelinus species on soybean susceptible versus resistant to the aphid. Biol Control 76:101–106.

  11. Liu B, Yang L, Yang F, Wang Q, Yang Y, Lu Y, Gardiner MM (2016) Landscape diversity enhances parasitism of cotton bollworm (Helicoverpa armigera) eggs by Trichogramma chilonis in cotton. Biol Control 93:15–23.

  12. Liu J, Zhu J, Zhang P, Han L, Reynolds OL, Zeng R, Wu J, Shao Y, You M, Gurr GM (2017) Silicon supplementation alters the composition of herbivore induced plant volatiles and enhances attraction of parasitoids to infested rice plants. Front Plant Sci 8:1265.

  13. Loader C, Damman H (1991) Nitrogen content of food plants and vulnerability of Pieris rapae to natural enemies. Ecology 72:1586–1590.

  14. Lou YG, Cheng JA (2001) Host-recognition kairomone from Sogatella furcifera for parasitoid Anagrus nilaparvatae. Entomol Exp Appl 101:59–67.

  15. Lou Y, Hua X, Turlings TJ, Cheng J, Chen X, Ye G (2006) Differences in induced volatile emissions among rice varieties result in differential attraction and parasitism of Nilaparvata lugens eggs by the parasitoid Anagrus nilaparvatae in the Field. J Chem Ecol 32:2375–2387.

  16. Lou YG, Zhang GR, Zhang WQ, Hu Y, Zhang J (2013) Biological control of rice insect pests in China. Biol Control 67:8–20.

  17. Lu ZX, Heong KL (2009) Effects of nitrogen-enriched rice plants on ecological fitness of planthoppers. In: Heong KL, Hardy B (eds) Planthoppers: new threats to the sustainability of intensive rice production systems in Asia. International Rice Research Institute, Los Baños, pp 247–256

  18. Lu ZX, Heong KL, Yu XP, Hu C (2004) Effects of plant nitrogen on ecological fitness of the brown planthopper, Nilaparvata lugens Stål. in rice. J Asia-Pacif Entomol 7:97–104.

  19. Lu ZX, Villareal S, Yu XP, Heong KL, Hu C (2006) Biodiversity and dynamics of planthoppers and their natural enemies in rice fields with different nitrogen regimes. Rice Sci 13:218–226.

  20. Mardani-Talaee M, Nouri-Ganblani G, Razmjou J, Hassanpour M, Naseri B, Asgharzadeh A (2016) Effects of chemical, organic and bio-fertilizers on some secondary metabolites in the leaves of bell pepper (Capsicum annuum) and their impact on life table parameters of Myzus persicae (Hemiptera: Aphididae). J Econ Entomol 109:1231–1240.

  21. Moon DC, Stiling P (2000) Relative importance of abiotically induced direct and indirect effects on a salt-marsh herbivore. Ecology 81:470–481.

  22. Norton GW, Heong KL, Johnson D, Savary S (2010) Rice pest management: issues and opportunities. In: Pandey S, Byerlee D, Dawe D, Dobermann A, Mohanty S, Rozelle S, Hardy B (eds) Rice in the global economy: strategic research and policy issues for food security. International Rice Research Institute, Los Baños, pp 297–332

  23. Pak D, Iverson AL, Ennis KK, Gonthier DJ, Vandermeer JH (2015) Parasitoid wasps benefit from shade tree size and landscape complexity in Mexican coffee agroecosystems. Agric Ecosyst Environ 206:21–32.

  24. Prado SG, Frank S (2014) Optimal foraging by an aphid parasitoid affects the outcome of apparent competition. Ecol Entomol 39:236–244.

  25. Price PW (1991) The plant vigor hypothesis and herbivore attack. Oikos 62:244–251.

  26. Rashid MM, Jahan M, Islam KS (2016) Impact of nitrogen, phosphorus and potassium on brown planthopper and tolerance of its host rice plants. Rice Sci 23:119–131.

  27. 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.

  28. Rodriguez JG, Chaplin CE, Stoltz LP, Lasheen AM (1970) Studies on resistance of strawberries to mites. Part 1 effects of plant nitrogen. J Econ Entomol 63:1855–1858.

  29. Rogers D (1972) Random search and insect population models. J Anim Ecol 41:369–383.

  30. Royama T (1973) A comparative study of models for predation and parasitism. Res Popul Ecol 15:121.

  31. Segoli M (2016) Effects of habitat type and spatial scale on density dependent parasitism in Anagrus parasitoids of leafhopper eggs. Biol Control 92:139–144.

  32. Segoli M, Rosenheim JA (2013) Limits to the reproductive success of two insect parasitoid species in the field. Ecology 94:2498–2504.

  33. Stenberg JA, Heil M, Åhman I, Björkman C (2015) Optimizing crops for biocontrol of pests and disease. Trends Plant Sci 20:698–712.

  34. Van Weelden MT, Wilson BE, Beuzelin JM, Reagan TE, Way MO (2016) Impact of nitrogen fertilization on Mexican rice borer (Lepidoptera: Crambidae) injury and yield in bioenergy sorghum. Crop Protect 84:37–43.

  35. Vankosky MA, VanLaerhoven SL (2017) Does host plant quality affect the oviposition decisions of an omnivore? Insect Sci 24:491–502.

  36. Veromann E, Toome M, Kännaste A, Kaasik R, Copolovici L, Flink J, Kovács G, Narits L, Luik A, Niinemets Ü (2013) Effects of nitrogen fertilization on insect pests, their parasitoids, plant diseases and volatile organic compounds in brassica napus. Crop Prot 43:79–88.

  37. Wang F, Peng SB (2017) Yield potential and nitrogen use efficiency of China’s “Super” rice. J Integr Agric 16:24–32.

  38. Winter TR, Rostás M (2010) Nitrogen deficiency affects bottom-up cascade without disrupting indirect plant defense. J Chem Ecol 36:642–651.

  39. Xiang C, Ren N, Wang X, Sumera A, Cheng J, Lou Y (2008) Preference and performance of Anagrus nilaparvatae (Hymenoptera: Mymaridae): effect of infestation duration and density by Nilaparvata lugens (Homoptera: Delphacidae). Environ Entomol 37:748–754.

  40. Xu HX, Yang YJ, Lu YH, Zheng XS, Tian JC, Lai FX, Fu Q, Lu ZX (2017) Sustainable management of rice insect pests by non-chemical-insecticide technologies in China. Rice Sci 24:61–72.

  41. Yang WH, Peng S, Huang J, Sanico AL, Buresh RJ, Witt C (2003) Using leaf color charts to estimate leaf nitrogen status of rice. Agron J 95:212–217.

  42. Yu XP, Barrion AT, Lu ZX (2001) A taxonomic investigation on egg parasitoid, Anagrus of rice planthopper in Zhejiang province. Rice Sci 9:8–9

  43. Yuan LP (2014) Development of hybrid rice to ensure food security. Rice Sci 21:1–2.

  44. 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.

  45. Zhu PY, Heong KL, Villareal S, Lu ZX (2017) Application of nitrogen fertilizer affects natural control of the rice brown planthopper Nilaparvata lugens (Stål) by arthropod natural enemies. Acta Ecol Sin 37:5542–5549. Chinese)

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This research was supported by the National Key Research & Development Plan of China (Grant No. 2016YFD0200800), the China Agriculture Research System (CARS-01-17) and State Key Laboratory Breeding Base for Zhejiang Sustainable Pest Control (Grant No. 2010DS700124-ZZ1601).

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Correspondence to Geoff M. Gurr or Zhongxian Lu.

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See Figs. 5, 6 and 7

Fig. 5

Field trial design for Experiment 4. 0 N: 0 kg/ha; 100 N: 100 kg/ha; 200 N: 200 kg/ha. Pots with plants treated with nitrogen rates of equivalent to 0, 50, 100 and 200 kg/ha were placed in a nested design in the fields

Fig. 6

Effect of fertilization nitrogen on parasitism rate of Anagrus flaveolus to BPH eggs. The relationship between nitrogen treatment and nitrogen content (N %) under conditions of light (a) and under conditions of darkness (c); Parasitism of A. flaveolus reared on 0 kg/ha (0 N) or 200 kg/ha (200 N) nitrogen treatment plants parasitized BPH eggs on 0 kg/ha (0 N), 50 kg/ha (50 N), 100 kg/ha (100 N) and 200 kg/ha (200 N) nitrogen treatment plants under conditions of light (b) and under conditions of darkness (d)

Fig. 7

Effect of nitrogen on the parasitism rate of Anagrus flaveolus in rice fields. a The relationship nitrogen treatment and nitrogen content (N %); b The parasitism rate of A flaveolus on BPH eggs on plants with 0 kg/ha (0 N), 50 kg/ha (50 N), 100 kg/ha (100 N) and 200 kg/ha (200 N) nitrogen treatment in fields treated with 0, 100 or 200 kg/ha nitrogen

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Zhu, P., Zheng, X., Xu, H. et al. Nitrogen fertilizer promotes the rice pest Nilaparvata lugens via impaired natural enemy, Anagrus flaveolus, performance. J Pest Sci (2020).

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  • Biological control
  • Ecological fitness
  • Parasitism preference
  • Parasitic efficiency
  • Functional response