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

Abstract

1. 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. 2. 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. 3. 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. 4. 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. 5. 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. 6. Our results indicate how interference competition-mediated through host plant defences-can increase ecosystem resilience to the warmer temperatures predicted under global climate change.

The Impact of Climate Change on the Resistance of Rice Near-Isogenic Lines with Resistance Genes Against Brown Planthopper

“…b IR24 and NIL-BPH20. Means in each column followed by a different letter differ significantly (P < 0.05) high temperature (34-35°C, the prediction temperature of 2100) would greatly reduce N. lugens survival rate (Horgan et al 2020;Horgan et al 2021a;Horgan et al 2021b;Wang et al 2010).…”

Higher‐order species interactions cause time‐dependent niche and fitness differences: Experimental evidence in plant‐feeding arthropods

“…This matches prior knowledge that herbivores sharing the same plant resources can interact in many ways. They can compete for space or resources indirectly by diminishing plant nutrition, altering plant morphology or inducing plant defences, which reduces the performance of other herbivores associated with the same plant (Horgan et al., 2021; Stam et al., 2014). All these mechanisms would lead to 0 < $$$ {\mathcal{N}}_i<1 $$$, as such competition is generally stronger within than between species.…”

Intraspecific competition counters the effects of elevated and optimal temperatures on phloem-feeding insects in tropical and temperate rice

“…For example, several studies have indicated that the frequency of aggressive encounters between planthoppers increases at higher temperatures [51,52]. Furthermore, plant-mediated interference competition between WBPH and BPH has been suggested to neutralize the positive effects of elevated temperature (i.e., 30˚C) on BPH population growth on IR22 and T65, despite poor growth and development of WBPH at the same high temperature; the effect was less pronounced at a lower temperature (25˚C) [14]. The decoupling of resource use and both intra-(this study) and interspecific [14] competition suggests that plant defences or other interference mechanisms induced by planthoppers feeding on IR22 and T65 may be more effective at the high temperature.…”

“…However, evidence of increased damage to crops from insect herbivores under warmer climates is rare and often anecdotal, or suffers from the problems of 'cause-and-effect' associated with correlative studies [1,7,11]. Furthermore, several studies have indicated that, whereas higher temperatures can have direct positive effects on many insect herbivores by providing optimal temperatures for growth and development, the indirect negative effects of elevated temperatures-mediated through herbivore interactions with their biotic environment-can sometimes dampen the impacts of a warming climate [12][13][14]. For example, the natural enemies of herbivore pests may have greater attack efficiency at higher temperatures, or may increase the numbers of generations they achieve in a season to a greater extent than observed among their prey [3,15].…”

“…For example, the natural enemies of herbivore pests may have greater attack efficiency at higher temperatures, or may increase the numbers of generations they achieve in a season to a greater extent than observed among their prey [3,15]. Some recent studies have suggested that intra-and interspecific competition can also dampen the effects of higher temperatures on herbivore development and on the damage herbivores cause to crops and other plants [14,16,17]. At optimal temperatures, insect herbivores will develop faster, increase their feeding rates and body mass, and produce more eggs [1,18].…”