Ecological costs of goldenrod’s ducking strategy in the currency of antixenosis, antibiosis, and indirect resistance to aphids

The evolutionary spread of a trait that benefits individuals of one species in their interactions with a second species may be constrained by “ecological costs” if the trait also has detrimental effects on interactions with a third species in the environment. In particular, the identification of ecological costs may help explain why natural plant populations often display less-than-maximal resistance against natural enemies—even when the plant populations possess substantial genetic variation that could serve as raw material for evolving greater resistance. One such resistance trait that confers an obvious fitness advantage, yet is maintained in populations at intermediate levels, is the strategy of resistance-by-ducking displayed by certain species of goldenrods (Solidago). In a ducking individual, the stem temporarily nods near the apex during a time in spring that coincides with the oviposition season of several herbivores. I investigated whether the fitness benefits of ducking in terms of deterring apex-galling insects may be offset by ecological costs posed by a common sap-sucking specialist—the red goldenrod aphid, Uroleucon nigrotuberculatum. In a controlled outdoor experiment, ducking was associated with significantly lower antixenosis (i.e., reduced preference), antibiosis (reduced performance), and indirect resistance against aphids. Specifically, aphids colonized ducking plants at a higher rate than erect-stemmed plants; populations of aphids on bagged ducking plants increased more quickly than on bagged erect-stemmed plants; and aphid populations on erect-stemmed plants were wiped out more quickly by natural enemies than on ducking plants when bags were removed. To the extent that aphid damage reduces goldenrod’s fitness, these ecological costs may be responsible for limiting the ducking trait to intermediate levels in goldenrod populations. Because most plant species are attacked by multiple types of herbivores, ecological costs of resistance mechanisms are likely to be more widespread than is generally appreciated, though their subtlety may make them challenging to identify.