Tri-trophic interactions among grapevines, a fungal pathogen, and a mycophagous mite

Grapevines are grown commercially in many parts of the world. The biotrophic pathogen of grapevine and causal agent of grapevine powdery mildew (Uncinula necator) is likewise distributed, and a serious constraint on production. We discovered in previous work that a tydeid mite (Orthotydeus lambi) suppressed U. necator on riverbank grapevine (Vitis riparia). In the present study, we quantified the direct and interactive effects among the host plant, pathogen, and mite. We planted 15 grape genotypes selected from three Vitis species, plus interspecific hybrids, in a common garden. The genotypes displayed significant variation in a morphological trait known to influence mite population densities: the size of domatia, the tufts of nonglandular trichomes at vein axils of the abaxial leaf surface. Vines were either experimentally infested with O. lambi ("release" vines) or kept free of mites. Over a four-year period we quantified the severity of powdery mildew on foliage as well as the density of O. lambi. In the absence of O. lambi, disease severity was highest among genotypes of the European grape species V. vinifera. Susceptibility varied from high to moderate among Vitis interspecific hybrids, while genotypes from the native North American species, V. riparia and V. labrusca, were generally resistant. O. lambi successfully established on release vines quickly, achieving densities similar to those found on wild V. riparia one year after release. O. lambi significantly suppressed foliar disease for genotypes of all grape species, although the magnitude of suppression varied. Moreover, there was a significant effect of grape species and grape genotype on O. lambi abundance that was positively correlated with the size of domatia. In some years, the positive association between domatia size and density of O. lambi translated into less severe foliar disease, after controlling for differences in inherent resistance. Although the importance of host-plant genetics and abiotic environmental factors in plant disease is well recognized, this study shows that natural enemies of pathogenic fungi, and their interactions with the host plant, can play a significant role. A more complete understanding of the complex interactions within this system may enhance the efficacy of mycophagous mites as biological agents for powdery mildew.