Host–parasite–herbivore Interactions: Implications of Host Cyanogenesis

To examine the mediation of host–predator interaction by a parasite, we studied the three-level interactions among a host plant, a root hemiparasitic plant, and their common predator, a generalist snail herbivore. The host species, Trifolium repens, is able to synthesize cyanogenic glucosides that have a significant role in plant herbivore resistance. Some T. repens populations are polymorphic with respect to cyanogenesis. Our second aim was to examine whether the mediation of the host plant–herbivore interaction by the parasitic plant could affect the maintenance of the cyanogenic polymorphism. The parasitic plant (Rhinanthus serotinus) was equally harmful to cyanogenic and acyanogenic hosts and grew equally well on both host types. In a no-choice experiment, both cyanogenesis and root hemiparasitism of the host plant reduced the growth of the herbivore (Arianta arbustorum). The herbivores consumed less leaf area of the parasitized plants than of unparasitized plants, but only when the host plant was acyanogenic. In a multiple-choice experiment, the snails were similarly affected by cyanogenesis but not by parasitic infection of the host. Thus, there was a discrepancy between food choice and performance of the herbivore. Our results suggest that the overall effects of the parasitic plant on the host plant were ameliorated through the indirect effects of the parasitic infection on herbivore performance and food consumption. This indirect effect of the parasitic infection seemed to be more beneficial for the acyanogenic plants: if parasitized, the leaf area of acyanogenic plants consumed by the herbivore was 45% higher than that of cyanogenic plants, whereas in unparasitized plants the corresponding figure was 114%. Thus, parasitism may decrease the advantage cyanogenic plants gain through decreased herbivory. Further, in mainly cyanogenic T. repens populations, cyanogenesis might be a more important feeding deterrent than root parasitism; whereas in mainly acyanogenic populations root parasitism might be relevant to herbivore–T. repens interactions. We are the first to document the effects of a plant parasite on the performance of both the host plant and a host-feeding herbivore. Our results highlight the need to look beyond the direct effect of parasites on their hosts.