Associational effects of closely related insect galls on rodent predators mediated by predator learning

While experiments have explored shared predator effects on multiple prey, frequency-dependent foraging in natural settings remains understudied. We investigated whether predator learning induces negative frequency-dependent predation and associational effects among galls formed by two aphid species, Hamamelistes miyabei and H. betulinus, on Hamamelis japonica. Field observations revealed that rodent predation (mainly by Apodemus argenteus and Glirulus japonicus) shifted with the relative frequency of the two gall types: as the proportion of H. miyabei galls increased, predation on H. betulinus galls decreased. Laboratory experiments with A. argenteus showed that naive individuals exhibited no preference and consumed both gall types equally. However, after repeated exposure, they preferred H. miyabei galls due to higher foraging efficiency. This learned preference resulted from short handling time and higher predation efficacy on H. miyabei, while the more structurally complex H. betulinus galls conferred protection because of their lower predation efficiency. These findings suggest that gall structural complexity and predator learning interact to create associational effects that reduce predation on less frequent gall types. This mechanism may promote the coexistence of closely related galling aphids and maintain morphological diversity. Our results indicate that associational effects mediated by predator learning contribute to gall diversity by potentially creating novel ecological niches.