We examined the effect of natural host‐plant quality on immune resistance in the autumnal moth, Epirrita autumnata (Borkhausen) (Lepidoptera: Geometridae). The division of mountain birches [Betula pubescens ssp. czerepanovii (Orlova) Hämet‐ahti (Betulaceae)] into two categories, high‐ and low‐quality food for larvae, was based on previous years’ results on the relative growth rate of the autumnal moth on the trees selected. The strength of the immune defence of autumnal moths was determined by measuring their encapsulation rate to exposure to a foreign antigen and the phenoloxidase (PO) activity of the pupal haemolymph. We found that individuals reared as larvae on naturally low‐quality food had a significantly higher encapsulation rate at the pupal stage than individuals reared on high‐quality food. Females also had a higher encapsulation rate than males. Food quality did not have statistically significant effect on PO activity, nor did this response variable show any differences between the sexes. Using half‐sib analyses, we found significant heritable variation in the encapsulation rate; the heritable variation in PO activity was near to significant, although equally strong. Heritability estimates (h2: 0.19–0.27) for immune defence traits were relatively low and only moderate when compared to other studies with insects. We also found a negative genetic correlation between pupal mass and PO activity, but not between PO activity and encapsulation rate. Our results suggest that the quality of food affects immune defence in the autumnal moth. Thus an intricate tritrophic relationship exists between the folivorous insect, the host tree, and the insect's natural enemies (e.g., pathogens, parasites, and parasitoids). This study demonstrates that natural variation within a food plant species has an effect on the innate immune system of an herbivorous insect.

Populations of the autumnal moth, Epirrita autumnata, exhibit cycles with high amplitudes in northernmost Europe, culminating in devastating outbreak densities at favourable sites. Parasitism by hymenopteran parasitoids has been hypothesised to operate with a delayed density dependence capable of producing the observed dynamics. It has also been hypothesised that insects in crowded conditions invest greatly in their immunity as a counter‐measure to increased risk of parasitism and pathogen infections. Furthermore, inducible plant defences consequent to grazing by herbivorous insects may be linked to the performance of parasitoids and pathogens through increased immunocompetence of the herbivore feeding on the foliage, in which the defence induction has taken place. At ten sampling sites, we quantified larval abundance, outbreak status and percentage larval parasitism during an extended peak phase of a population cycle. These population level covariates, together with an individual pupal mass, were used to explain differences in the immune defence, measured as an encapsulation reaction to artificial antigen. We also conducted a field study for an investigation of the susceptibility of autumnal moth pupae to naturally occurring pupal parasitoids. We did not find obvious differences between the encapsulation rate of autumnal moths originating from the sites with different past and current larval densities and risks for parasitism. The best ranked statistical models included pupal mass and outbreak status as explanatory variables, although both showed only slight effects on the encapsulation rate. The host resistance test revealed positive relationships between the encapsulation rate, body size and percentage parasitism of the exposed pupae, indicating that pupal parasitoids chose, and/or survived better, in large host individuals irrespective of their encapsulation ability. Thus, our results do not provide support for the hypothesis that variation in the immune function drives or modulates population cycles of autumnal moths.

Abstract. Population cycles of herbivores are thought to be driven by trophic interaction mechanisms, either between food plant and herbivore or between the herbivorous prey and its natural enemies. Observational data have indicated that hymenopteran parasitoids cause delayed density-dependent mortality in cyclic autumnal moth (Epirrita autumnata) populations. We experimentally tested the parasitism hypothesis of moth population cycles by establishing a four-year parasitoid-exclusion experiment, with parasitoid-proof exclosures, parasitoid-permeable exclosures, and control plots. The exclusion of parasitoids led to high autumnal moth abundances, while the declining abundance in both the parasitoid-permeable exclosures and the control plots paralleled the naturally declining density in the study area and could be explained by high rates of parasitism. Our results provide firm experimental support for the hypothesis that hymenopteran parasitoids have a causal relationship with the delayed density-dependent component required in the generation of autumnal moth population cycles.

Host plant quality has a major influence on the performance, and ultimately on the fitness of an herbivorous insect, but may also have indirect effects on the third trophic level by affecting an herbivore's defensive ability against natural enemies. In a three-year field study, we examined the effects of natural food quality on the ability of autumnal moths, Epirrita autumnata (Lepidoptera, Geometridae), to defend themselves against parasitoids. In each year, we confirmed the variation in quality of host trees (mountain birch, Betula pubescens ssp. czerepanovii) by determining the mass of pupae reared in mesh bags attached to the trees and the water content of leaves. Individuals grown on high quality trees possessed significantly higher encapsulation rate of a foreign antigen as pupae compared to those on low quality trees during the first and third study years; a parallel trend was also found in the second study year, although this difference was not statistically significant. However, in spite of observed differences in encapsulation rates, individuals reared on high and low quality trees did not differ in their levels of parasitisation when exposed to hymenopteran parasioids in the wild and thus were equally vulnerable. Accordingly, the encapsulation response seems not to play a major role on the population ecology scale in the studied system. Our findings also stress the importance of direct resistance tests, which should be conducted along with tests of insect immune function.

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