Learned and naive natural enemy responses and the interpretation of volatile organic compounds as cues or signals

In response to arthropod herbivory, plants release volatile organic compounds (VOCs), which are attractive to natural enemies. Consequently, VOCs have been interpreted as co-evolved plant-natural enemy signals. This review argues that, while these data are necessary, they are not sufficient to demonstrate a VOC plant-natural enemy signaling function. We propose that evidence that (1) plant fitness is increased as a consequence of natural enemy recruitment, and either (2A) natural enemies preferentially learn prey-induced VOCs or (2B) natural enemies respond innately to the VOCs of the prey-host plant complex, is also required. Whereas there are too few studies to rigorously test hypotheses 1 and 2A, numerous studies are available to test hypothesis 2B. Of 293 tests of natural enemy responses to VOCs, we identified only 74 that were unambiguous tests of naive natural enemies; in the remainder of the tests either natural enemies were experienced with their host in the presence of VOCs, or experience could not be ruled out. Of those 74 tests with naive natural enemies, attraction was observed in 41 and not in 33. This review demonstrates that empirical support for the hypothesized VOC plant-natural enemy signaling function is not universal and presents alternative hypotheses for VOC production.