Holly leaf-miners on two continents: what makes an outbreak species?

1. Some herbivore species periodically undergo damaging, high-density outbreak phases followed by less damaging low-density phases. Others maintain steady, low to moderate density levels that do little damage to their hosts. 2. Two closely related holly leaf-miner species were compared that share many ecological traits and have very similar life cycles, but only one of which exhibits outbreaks. Phytomyza ilicicola in the eastern U.S.A. varied widely in mortality and infestation levels, reaching local densities of over 10 mines per leaf In contrast, Phytomyza ilicis in the U.K. showed low infestation and high mortality at all sites. Using data from the literature and from field studies, the factors responsible for these contrasting dynamics were sought. 3. Phytomyza ilicicola oviposits into the leaf lamina, and experiences weak larval competition only at high densities. Phytomyza ilicis oviposits into the leaf midrib, which leads to high mortality of young larvae before mine formation. Multiply mined leaves were therefore very common in P. ilicicola but rare in P. ilicis. 4. Differences in the parasitoid complexes of the two systems accounted for further differences in survival to adulthood. The main (larval) parasitoid, which was found to impose high, density-dependent mortality on P. ilicis, is missing on P. ilicicola. It is replaced by an egg-pupal parasitoid, which varies in its impact at different sites. Multiple emergence of adults from multiply mined leaves is therefore widespread in P. ilicicola but does not occur in P. ilicis. 5. The differences in oviposition behaviour and in the parasitoid complexes are likely to allow P. ilicicola to outbreak when habitat conditions are favourable, while P. ilicis is always tightly regulated.