Secondary leaves of an outbreak-adapted tree species are both more resource acquisitive and more herbivore resistant than primary leaves

The magnitude and frequency of insect outbreaks are predicted to increase in forests, but how trees cope with severe outbreak defoliation is not yet fully understood. Winter deciduous trees often produce a secondary leaf flush in response to defoliation (i.e., compensatory leaf regrowth or refoliation), which promotes fast replenishment of carbon (C) storage and eventually tree survival. However, secondary leaf flushes may imply a high susceptibility to insect herbivory, especially in the event of an ongoing outbreak. We hypothesized that in winter deciduous species adapted to outbreak-driven defoliations, secondary leaves are both more C acquisitive and more herbivore resistant than primary leaves. During an outbreak by Ormiscodes amphimone F. affecting Nothofagus pumilio (Poepp. & Endl.) Krasser forests, we (i) quantified the defoliation and subsequent refoliation by analyzing the seasonal dynamics of the normalized difference vegetation index (NDVI) and (ii) compared the physiological traits and herbivore resistance of primary and secondary leaves. Comparisons of the NDVI of the primary and second leaf flushes relative to the NDVI of the defoliated forest indicated 31% refoliation, which is close to the leaf regrowth reported by a previous study in juvenile N. pumilio trees subjected to experimental defoliation. Primary leaves had higher leaf mass per area, size, carbon:nitrogen ratio and soluble sugar concentration than secondary leaves, along with lower nitrogen and starch concentrations, and similar total polyphenol and phosphorus concentrations. In both a choice and a non-choice bioassay, the leaf consumption rates by O. amphimone larvae were significantly higher (>50%) for primary than for secondary leaves, indicating higher herbivore resistance in the latter. Our study shows that secondary leaf flushes in outbreak-adapted tree species can be both C acquisitive and herbivore resistant, and suggests that these two features mediate the positive effects of the compensatory leaf regrowth on the tree C balance and forest resilience.