Positive and negative interspecific interactions between coexisting rice planthoppers neutralise the effects of elevated temperatures

Abstract

Global warming is often predicted to increase damage to plants through direct effects on insect herbivores. However, the indirect impacts of rising temperatures on herbivores, mediated through interactions with their biotic environment, could dampen these effects.Using a series of reciprocal density experiments with gravid females and developing nymphs, we examined interspecific competition between two coexisting phloem feeders Nilaparvata lugens (BPH) and Sogatella furcifera (WBPH), on rice at 25 and 30°C.WBPH performed better (i.e. adults survived longer, nymphs developed faster and grew larger) at 25°C and BPH (i.e. nymphs developed faster) at 30°C. However, contrary to predictions, WBPH had a greater effect in reducing oviposition and nymph performance in BPH at 30°C.A decoupling of resource use by WBPH and its antagonistic effects on BPH at the higher temperature suggests that WBPH feeding induces host defences that reduce BPH fitness (i.e. interference competition). Meanwhile, BPH facilitated WBPH oviposition at 30°C and facilitated WBPH nymph performance at 25 and 30°C. Greater facilitation of feeding in WBPH nymphs by BPH at high densities suggests that mechanical damage and host responses to damage increased the fitness of the heterospecific nymphs.Although BPH also facilitated egg-laying by WBPH, intra- and interspecific crowding countered this facilitation at both temperatures. Simulated life tables for planthoppers at 25 and 30°C depicted significantly lower offspring numbers on rice infested by WBPH alone and from mixed BPH-WBPH infestations than from infestations by BPH alone.Our results indicate how interference competition-mediated through host plant defences-can increase ecosystem resilience to the warmer temperatures predicted under global climate change. A free Plain Language Summary can be found within the Supporting Information of this article.

Keywords: climate change; exploitation competition; facilitation; induced plant defences; interference competition; rice; volatiles.

FIGURE 1

Longevity of adult female BPH (A, B) and WBPH (C, D) on IR22 (A, C) and T65 (B, D) in environmental chambers at three constant temperatures. The corresponding numbers of eggs laid by BPH (E, F) and WBPH (G, H) on IR22 (E, G) and T65 (F, H) are also presented. Error bars are indicated (N = 4). Numbers are based on survival and oviposition by females for up to 20 days at each temperature. Lowercase letters indicate homogenous temperature groups (Tukey: p > 0.05)

FIGURE 2

Survival of BPH (A, B) and WBPH (C, D) nymphs at three temperatures on IR22 (A, C) and T65 (B, D), with development of BPH (E, F) and WBPH (G, H) and dry weight per individual BPH (I, J) and WBPH (K, L) on IR22 (E, G, I, K) and T65 (F, H, J, L). Standard errors are indicated (N = 5). Lowercase letters indicate homogenous temperature groups (Tukey: p > 0.05)

FIGURE 3

Oviposition during reciprocal interspecific competition experiments conducted at 25°C (A, C, E, G) and 30°C (B, D, F, H). In one set of experiments, BPH female densities were increased in the presence of constant densities (four per plant or six per plant at 25 and 30°C, respectively) of WBPH females (A–D). In the second set, WBPH female densities were increased in the presence of constant densities (four and six females per plant at 25 and 30°C, respectively) of BPH females (E–H). Results indicate the total numbers of eggs per planthopper for each species. Experiments were conducted using the varieties IR22 (A, B, E, F) and T65 (C, D, G, H). Brown symbols and lines indicate BPH and blue symbols and lines indicate WBPH. Standard errors are indicated (N = 5). The numbers of eggs laid by planthoppers at constant densities in the same experiments are presented in Figure S1 and results as total eggs per plant are presented in Figure S2

FIGURE 4

Nymph survival during reciprocal interspecific competition experiments conducted at 25°C (A, C, E, G) and 30°C (B, D, F, H) with corresponding development of nymphs at 25°C (I, K, M, O) and 30°C (J, L, N, P), and average nymph dry weights at 25°C (Q, S, U, W) and 30°C (R, T, V, X). The experiments were conducted on varieties IR22 (A, B, E, F, I, J, M, N, Q, R, U, V) and T65 (C, D, G, H, K, L, O, P, S, T, W, X). Brown symbols and lines indicate BPH and blue symbols and lines indicate WBPH. Standard errors are indicated (N = 5). Survival, development and weight gain for nymphs at constant densities in the same experiments are presented in Figure S1 and results as total nymph biomass per plant are presented in Figure S5

FIGURE 5

Estimated number of offspring from 200 BPH nymphs, 200 WBPH nymphs or from a mix of nymphs of both species (100 + 100) after three generations (first generation = A, B, second = C, D, third = E, F) on IR22 (A, C, E) and T65 (B, D, F) at 25°C (shaded) or 30°C (solid). Numbers associated with mixed cohorts indicate the percentage of offspring that were WBPH. Estimates are based on constructed life tables adapted from Liu and Han (2006) using survival rates and fecundities from the competition experiments. Standard errors are indicated by error bars (numbers of hoppers) and in parentheses (percentage of WBPH in the mixed cohorts; N = 5)

FIGURE 6

Exploitation competition (solid lines) and plant‐mediated interference competition or facilitation (dashed lines with ‘−’ or ‘+’, respectively) between BPH (brown planthopper) and WBPH (white planthopper) at 25°C and 30°C as indicated by changes in nymph biomass or eggs per female. Exploitation competition is identified by greater negative impacts at high conspecific (intraspecific competition) or heterospecific (interspecific competition) densities. Interference competition and facilitation are identified by negative and positive effects, respectively, on heterospecifics, regardless of planthopper densities. −/+ indicates a negative effect at low heterospecific density, but positive effect at high heterospecific density, etc.; ‘0’ signifies no effect (see also Figure S6)