Seasonality elicits herbivores' escape from trophic control and favors induced resistance in a temperate macroalga

Abstract

Strong seasonality in temperate marine littoral environments triggers fluctuation in grazing and in trophic cascades. Variation in species interactions arising from seasonality may favor the evolution of induced resistance in macroalgae, but the coupling of induced resistance with temporally varying grazing pressure remains equivocal. Here we present a study where we manipulated the natural densities of herbivores and predatory fish to quantify seasonal variation in herbivory, induction of resistance, and cascading third‐trophic‐level effects on herbivory in the brown alga Fucus vesiculosus, a foundation species of the rocky littoral in the northern Baltic Sea. Our results demonstrate a vast seasonal variation in grazing triggered by highly synchronized reproduction of the main mesograzer in the area, Idotea balthica. High I. balthica density in autumn resulted in an 88% grazing loss and a strong induction of resistance to further feeding in F. vesiculosus. By the next spring, I. balthica densities had decreased by 95% and the low herbivore density caused minor grazing loss and no induction of resistance in the algae. During the herbivory peak in autumn, both the overall resistance to herbivores and induced resistance varied among F. vesiculosus genotypes. Herbivores escaped from the trophic control of fish in autumn, leading to a herbivory peak, while in spring, fish decreased the low herbivore density even further and had a cascading beneficial effect on the algae. In autumn, the presence of fish predators was connected, however, to fewer algae, showing induced resistance. We emphasize the seasonal dynamics of herbivore populations as an important factor affecting the outcomes of three‐trophic interactions by promoting herbivore escapes from top‐down control and by generating periods of strong selection for resistance traits in macroalgae in temperate marine littoral environments. Induced resistance may be critical to survival of the algae, and is thus likely to be an adaptation to the strong seasonality of herbivory.