Elevated temperatures diminish the effects of a highly resistant rice variety on the brown planthopper

Abstract

This study compares the effects of temperature (constant at 15, 20, 25, 30 and 35 °C) on adult longevity, oviposition, and nymph development of the brown planthopper, Nilaparvata lugens, on susceptible and resistant rice varieties. The resistant variety contained the BPH32 gene. In our experiments, nymphs failed to develop to adults at 15, 20 and 35 °C on either variety. Host resistance had its greatest effect in reducing adult survival at 20-25 °C and its greatest effect in reducing nymph weight gain at 25 °C. This corresponded with optimal temperatures for adult survival (20-25 °C) and nymph development (25-30 °C). At 25 and 30 °C, adult females achieved up to three oviposition cycles on the susceptible variety, but only one cycle on the resistant variety. Maximum egg-laying occurred at 30 °C due to larger numbers of egg batches produced during the first oviposition cycle on both the susceptible and resistant varieties, and larger batches during the second and third oviposition cycles on the susceptible variety; however, resistance had its greatest effect in reducing fecundity at 25 °C. This revealed a mismatch between the optimal temperatures for resistance and for egg production in immigrating females. Increasing global temperatures could reduce the effectiveness of anti-herbivore resistance in rice and other crops where such mismatches occur.

Figure 1

Daily survival and egg-laying by Nilaparvata lugens on susceptible (IR22: green circles) and resistant (IR62: red circles) rice varieties. Plants were grown at 15 °C (a,f,k,p,u), 20 °C (b,g,l,q,v), 25 °C (c,h,m,r,w), 30 °C (d,i,n,s,x) and 35 °C (e,j,o,t,y). Relative humidity was maintained at 80%. Results for Adult longevity (a–e) and the total number of eggs deposited (f–j) are indicated. The number of eggs per surviving female (k–o), the size of egg batches (p–t) and the number of batches produced per female (u–y) are indicated as components of egg-laying displaying three oviposition cycles on IR22 between 15 and 30 °C. Standard errors are included (N = 4). Lowercase letters indicate homogenous temperature groups for each parameter (Tukey: P ≤ 0.05).

Figure 2

Mean survival and egg-laying by Nilaparvata lugens on susceptible (IR22: green circles) and resistant (IR62: red circles) rice varieties across a range of temperatures. The times to 50% (dashed lines) and 100% (solid lines) mortality of adult females are indicated in a. The total numbers of eggs (b), total number of batches (c), the number of eggs per female (d), batch size (e) and the numbers of batches per female (f) are also indicated. Numbers are based on accumulated data over 20 days of the experiment. Relative humidity was maintained at 80%. Bars indicate standard errors (N = 4). Effects of variety (V), temperature (T) and their interaction (V × T) are indicated as ns (P > 0.05), * (P ≤ 0.05), ** (P ≤ 0.01), *** (P ≤ 0.005); lowercase letters indicate homogenous temperature groups (Tukey, P ≤ 0.05).

Figure 3

Daily survival and biomass of Nilaparvata lugens nymphs on susceptible (IR22: green circles) and resistant (IR62: red circles) rice varieties, with associated nymphs development stages. Plants were grown at 15 °C (a,f,k), 20 °C (b,g,l), 25 °C (c,h,m), 30 °C (d,i,n) and 35 °C (e,j,o). Relative humidity was maintained at 80%. Results for nymph survival, including development to adults (a-e), nymph biomass (f-j), and nymph developmental stages (k–o) are indicated. N2 = second instar, N3 = third instar, etc., A = adult. Standard errors are included (N = 5). Lowercase letters indicate homogenous temperature groups (Tukey, P ≤ 0.05).

Figure 4

Mean survival, biomass and development of Nilaparvata lugens nymphs on susceptible (IR22: green circles) and resistant (IR62: red circles) rice varieties across a range of temperatures. Nymph survival at the end of 15 days is indicated in a. The biomass of surviving nymphs (b) and the time for 50% of nymphs to develop to fourth instars (c) are also indicated. Numbers are based on accumulated data over 15 days of the experiment (23 and 30 days for nymph development at 20 °C and 15 °C, respectively). Relative humidity was maintained at 80%. Bars indicate standard errors (N = 5). Effects of variety (V), temperature (T) and their interaction (V × T) are indicated as ns (P > 0.05), * (P ≤ 0.05), ** (P ≤ 0.01), *** (P ≤ 0.005); lowercase letters indicate homogenous temperature groups (Tukey, P ≤ 0.05).

Figure 5

(a) Densities of yeast-like symbionts (YLS) in planthoppers reared on IR22 (green squares) and IR62 (red squares). Nymphs were maintained in an insectary at 27 °C for 7 days after exposure to 25 °C or 35 °C during 3 days. The corresponding wet weights of the nymphs are indicated in b. Black circles indicate sample means (N = 5).

Figure 6

Reductions in the fitness of Nilaparvata lugens on IR62 over a temperature gradient. Graphs indicate the total reductions (violet circles) in adult longevity (a), the number of eggs laid (b), nymph survival (c) and nymph biomass (d). In each case, this is composed of a fitness reductions due to temperature (blue circles – estimated based on reductions relative to optimal temperatures on a highly susceptible variety) and reductions due to the resistance gene(s) (red circles – estimated as the total reduction minus the temperature-related reduction in fitness). Standard errors are shown (N = 4 for a and b, N = 5 for c and d). Lowercase letters indicate homogenous temperature groups (Tukey, P < 0.05).