Tiny predators avoid herbivorous caterpillar traces to prevent revolutionary predation

We report the first example of predators having a strategy to avoid ‘revolutionary predation’ by herbivores, i.e. predation on the higher trophic levels by the lower ones. The predatory mites Neoseiulus womersleyi and Euseius sojaensis are smaller than 0.5 mm and lay eggs on plant leaf surfaces; thus, their immobile eggs would be incidentally consumed along with leaves by voracious lepidopteran caterpillars. We experimentally demonstrated that eggs of both mite species were preyed upon by tested hawkmoth caterpillars (Theretra oldenlandiae, Theretra japonica) along with leaves. Therefore, the ability to avoid such revolutionary predation should confer a selective advantage to mites. We further demonstrated that adult females of both mite species avoided laying eggs on leaves with traces of all tested caterpillars (T. oldenlandiae, T. japonica, Papilio xuthus and Bombyx mori), indicating that eggs may avoid revolutionary predation by voracious caterpillars that may be nearby. This is the first demonstration of a repellent effect of herbivore traces on carnivores. Considering previous studies showing that spider mites as small as predatory mites also avoid caterpillar traces, the same need to avoid predation by huge caterpillars may have led to the development of the same solutions for both spider mites and predatory mites.