Mistletoe generates non-trophic and trait-mediated indirect interactions through a shared host of herbivore consumers

Abstract

Indirect interactions emerge among a wide range of herbivores sharing the same plant resource. Consumers usually belong to different trophic guilds, from folivores and sapsuckers to parasitic plants. We propose that mistletoes parasitizing pines could play a key role acting as herbivores on host pines and coming indirectly into competition with other herbivores feeding on the same host. Changes caused by mistletoes on its host have been well studied, but its effects running across trophic webs remain unrevealed. In this study, we investigate the effect of European mistletoe (Viscum album subsp. austriacum) on the host-feeding herbivores via trait-mediated indirect interactions (TMIIs) across their shared pine host (Pinus nigra subsp. salzmannii). We performed field and laboratory experiments, and analyzed the net effect of different mistletoe parasite loads on three host-phytophagous species: the sapsucker Cinara pini (Aphididae), the winter folivore Thaumetopoea pityocampa (Thaumetopoeidae), and the summer folivore Brachyderes sp. (Curculionidae), all being members of different functional feeding groups (FFGs). We summarize the mistletoe–host–herbivore interactions by means of a TMII, where mistletoe parasitism causes non-trophic links and detrimental indirect interactions on pine-feeding herbivores across its shared host, suggesting a worsening of host quality as food. These indirect interactions vary according to three parameters. First, the intensity has a non-proportional relation with parasite load, showing an impact threshold on highly parasitized pines. Second, the movement capacity of insect herbivores determines their response, by decreasing the abundance of herbivores with low movement ability (aphids and pine processionary caterpillars) while altering the behavior (plant selection) of more mobile herbivores (pine weevils). Finally, FFG determines the intensity of mistletoe parasitism effects, folivores being more responsive than sapsuckers. Overall, mistletoe generates non-trophic interaction linkages in the forest able to modify community structure by becoming a nexus of the entire herbivore community of the pine canopy.