Interactions between Rice Resistance to Planthoppers and Honeydew-Related Egg Parasitism under Varying Levels of Nitrogenous Fertilizer

Abstract

Host plant resistance is the most researched method for the management of planthoppers and leafhoppers in tropical rice. For optimal effects, resistance should be resilient to fertilizer inputs and work in synergy with natural enemies. In field plot experiments, we examined how rice resistance and fertilizer inputs affect mortality of planthopper and leafhopper eggs by hymenopteran parasitoids. We used IR62 as a variety with resistance to Nilaparvata lugens (Stål) [BPH], Sogatella furcifera (Horváth) [WBPH] and Nephotettix virescens (Distant) [GLH], and IR64 as a susceptible control. The herbivores were more abundant during wet season sampling in low-nitrogen plots. During this study, parasitoids killed between 31 and 38% of BPH eggs and 24 and 52% of WBPH eggs during four days of field exposure. Parasitism, mainly due to Oligosita spp., was generally higher in high-nitrogen and IR64 plots. Similar densities of eggs in exposed plants suggest that these trends were mediated by semiochemicals and therefore support the Optimal Defense Hypothesis. Honeydew from BPH on IR62 had more xylem-derived wastes than honeydew on IR64. We applied honeydew from both varieties to sentinel plants. Parasitism by Anagrus spp. was higher on plants of either variety treated with honeydew derived from IR62; however, the effect was only apparent in high-nitrogen plots. Results suggest that Anagrus spp., by responding to honeydew, will counter the nitrogen-induced enhancement of planthopper fitness on resistant rice.

Keywords: Anagrus spp.; BPH32 gene; Nephotettix spp.; Nilaparvata lugens; Sogatella furcifera; conservation biological control; honeydew; host plant resistance; integrated pest management; nectar.

Figure 1

Numbers of planthoppers (A,B), leafhoppers (A,B) and free-living egg parasitoids (C,D) collected at plots of resistant (IR62) and susceptible (IR64) rice under low (gray bars: 0 added) and high (yellow bars: 150 kg N ha⁻¹) levels of nitrogenous fertilizer. Sampling was conducted using sweep nets during the 2013 dry (A,C) and wet (B,D) seasons. Standard errors are indicated (N = 6); note differences in scales; results of GLM are indicated as ** = p ≤ 0.05 and *** = p ≤ 0.001; BPH = brown planthopper, WBPH = whitebacked planthopper, and GLH = green leafhopper; S = season.

Figure 2

Effects of nitrogen (0 or 150 kg ha⁻¹ of nitrogen) and variety (IR62: resistant and IR64: susceptible) on percentage parasitism of BPH (A,B), WBPH (C,D) and GLH (E,F) eggs in rice field plots. Experiments were conducted during the dry (A,C,E) and wet (B,D,F) seasons of 2013. Standard errors are indicated (N = 6); results of GLM are indicated as ns = p > 0.05, * = p ≤ 0.05 and *** = p ≤ 0.001. BPH = brown planthopper, WBPH = whitebacked planthopper, and GLH = green leafhopper; S = season, N = nitrogen and V = variety.

Figure 3

Effects of nitrogen (0 or 150 kg ha⁻¹ of nitrogen) and variety (IR62: resistant and IR64: susceptible) on parasitism of WBPH and BPH eggs by Anagrus spp. and Oligosita spp. in field plots. Experiments were conducted during the dry (A,C) and wet (B,D) seasons of 2013. Standard errors are indicated (N = 6); results of GLMs are indicated as * = p ≤ 0.05 and *** = p ≤ 0.001. BPH = brown planthopper and WBPH = whitebacked planthopper.

Figure 4

Parasitism of BPH eggs by Anagrus spp. (A,B) and Oligosita spp. (C,D) on plants with one of three honeydew treatments (IR62-derived honeydew added = hatched bars; IR64-derived honeydew added = cross-hatched bars; honeydew removed = open bars). Sentinel IR62 (resistance) and IR64 (susceptible) plants with BPH eggs were exposed in field plots with low (0 added) and high (150 kg ha⁻¹) nitrogenous fertilizer during the dry (A,C) and wet (B,D) seasons of 2013. Standard errors are indicated (N = 6); results of GLMs are indicated as ns = p > 0.05, * = p ≤ 0.05, ** = p ≤ 0.01 and *** = p ≤ 0.001.