Asynchrony between Host Plant and Insects-Defoliator within a Tritrophic System: The Role of Herbivore Innate Immunity

Abstract

The effects of asynchrony in the phenology of spring-feeding insect-defoliators and their host plants on insects’ fitness, as well as the importance of this effect for the population dynamics of outbreaking species of insects, is a widespread and well-documented phenomenon. However, the spreading of this phenomenon through the food chain, and especially those mechanisms operating this spreading, are still unclear. In this paper, we study the effect of seasonally declined leafquality (estimated in terms of phenolics and nitrogen content) on herbivore fitness, immune parameters and resistance against pathogen by using the silver birch Betula pendula—gypsy moth Lymantria dispar—nucleopolyhedrovirus as the tritrophic system. We show that a phenological mismatch induced by the delay in the emergence of gypsy moth larvae and following feeding on mature leaves has negative effects on the female pupal weight, on the rate of larval development and on the activity of phenoloxidase in the plasma of haemolymph. In addition, the larval susceptibility to exogenous nucleopolyhydrovirus infection as well as covert virus activation were both enhanced due to the phenological mismatch. The observed effects of phenological mismatch on insect-baculovirus interaction may partially explain the strong and fast fluctuations in the population dynamics of the gypsy moth that is often observed in the studied part of the defoliator area. This study also reveals some indirect mechanisms of effect related to host plant quality, which operate through the insect innate immune status and affect resistance to both exogenous and endogenous virus.

Phenological asynchrony between host plant and gypsy moth reduces insect gut microbiota and susceptibility to Bacillus thuringiensis

“…The principal design of the experiment was the same as that used in our previous study (Martemyanov, Pavlushin, Dubovskiy, Yushkova, et al., ), and a detailed description can be found in our previous paper. The general design is also presented in Fig.…”

“…Ecologists consider the phenological synchrony between the emergence of overwintering herbivorous insects and the budding of their host plants to represent one of the crucial factors in the population dynamics of herbivores (van Asch & Visser, ; Feeny, ; Foster, Townsend, & Mladenoff, ; Hunter & Lechowicz, ; Ivashov, Boyko, & Simchuk, ; Martemyanov, Pavlushin, Dubovskiy, Belousova et al., ; Martemyanov, Pavlushin, Dubovskiy, Yushkova, et al., ). If the larvae hatch prior to the host plant budburst, the larvae may starve, whereas if the larvae hatch too late, the foliage quality may be reduced (reviewed in van Asch & Visser, and references therein), although the occurrence of this phenomenon is related to studied species (Kharouba, Vellend, Sarfraz, & Myers, ) and global climate processes (Uelmen et al., ).…”

“…We recently showed that phenological asynchrony between Betula pendula Roth. trees and Lymantria dispar L. larvae (an eruptive defoliator related to the spring feeding guild) leads to decreases in herbivore fitness and significant increases in larval susceptibility to baculoviral disease (Martemyanov, Pavlushin, Dubovskiy, Yushkova, et al., ). Moreover, the activation of asymptotic baculoviral infection (covert infection) in an overt form affected approximately 60% of virus‐carrying insects if the larvae were reared asynchronously with the host plant.…”

“…Because baculoviruses can induce spontaneous epizootics in the insect population (Cory & Myers, ), we considered the phenological asynchrony between host plants and insect defoliators to represent a predictor of natural viral epizootics. The modification of insect host innate immunity parameters under the effect of asynchrony has been reported to be one of the mechanisms that drives insect susceptibility to baculoviruses (Martemyanov, Pavlushin, Dubovskiy, Yushkova, et al., ). In addition, dramatic changes in leaf quality during the first 20 days of development have been suggested to represent the main mode of action of asynchrony on insect antiviral immunity (Chernyak et al., ; Martemyanov, Pavlushin, Dubovskiy, Yushkova, et al., ).…”

“…The modification of insect host innate immunity parameters under the effect of asynchrony has been reported to be one of the mechanisms that drives insect susceptibility to baculoviruses (Martemyanov, Pavlushin, Dubovskiy, Yushkova, et al., ). In addition, dramatic changes in leaf quality during the first 20 days of development have been suggested to represent the main mode of action of asynchrony on insect antiviral immunity (Chernyak et al., ; Martemyanov, Pavlushin, Dubovskiy, Yushkova, et al., ). However, the effect of asynchrony on insect bacterial diseases, such as intestinal bacteria Bacillus thuringiensis , which is widely used for the pest management (Garczynski & Siegel, ), remains unclear because different insect immune parameters are affected in different ways by the same trophic factor (Martemyanov, Dubovskiy, Belousova, et al., ; Martemyanov, Dubovskiy, Rantala, et al., ; Martemyanov et al., ; Martemyanov, Pavlushin, Dubovskiy, Belousova et al., ).…”