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.

Plant chemical defense against herbivores is a complex process which involves a number of secondary compounds. It is known that the concentration of leaf surface lipophilic compounds (SLCs), particularly those of flavonoid aglycones are increased with the defoliation treatment of silver birch Betula pendula. In this study we investigated how the alteration of SLCs concentration in the food affects the fitness and innate immunity of the gypsy moth Lymantria dispar. We found that a low SLCs concentrations in consumed leaves led to a rapid larval development and increased females’ pupae weight (= fecundity) compared to larvae fed with leaves with high SLCs content. Inversely, increasing the compounds concentration in an artificial diet produced the reverse effects: decreases in both larval weight and larval survival. Low SLCs concentrations in tree leaves differently affected larval innate immunity parameters. For both sexes, total hemocytes count in the hemolymph increased, while the activity of plasma phenoloxidase decreased when larvae consume leaves with reduced content of SLCs. Our results clearly demonstrate that the concentration of SLCs in silver birch leaves affects not only gypsy moth fitness but also their innate immune status which might alter the potential resistance of insects against infections and/or parasitoids.

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