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.

Hemiparasites drive heterogeneity in litter arthropods: Implications for woodland insectivorous birds

“…), making host leaves less attractive for herbivorous insects (Lázaro‐González et al . ). These differences in resource quantity and quality can be expected to increase the abundance of herbivores and detritivores likely represented in the most responsive arthropod groups found in pit‐fall traps – that is, Coleoptera, Hemiptera, Diplopoda, and litter‐dwelling Lepidoptera larvae.…”

Secondary foundation species foster novel plant–animal interactions in the forest canopy: evidence from mistletoe

“…Qualitatively, mistletoe brings to the forest stand new species, mostly belonging to the orders Hymenoptera, Diptera, Lepidoptera (floral visitors) and Hemiptera (herbivores and predator), while quantitatively it provides twice as many arthropods as appear in the canopy of the unparasitised pines. While mistletoe attracts a new community of specialists, different from host pine (Lázaro‐González et al ., 2017), mistletoe parasitism causes detrimental indirect effects on pine‐feeding herbivores across its shared host, suggesting a worsening of host quality as food (Lázaro‐González et al ., 2019a, b). These changes (i.e.…”

“…In functional terms, mistletoe adds to the pine canopy two plant–animal interactions with mutualistic consequences that do not occur in the pine forest without mistletoe: the pollination derived from floral visitor's activities during the early spring, and the dispersion of seeds derived from the frugivorous bird activity during autumn and winter (Mellado & Zamora, 2014, 2016, 2017). Thus, with mistletoe, a relatively simple pine canopy, dominated by antagonistic plant–herbivorous interactions with a limited number of species involved (Lazaro‐González et al ., 2017, 2019b), becomes a complex bank ( sensu Darwin, 1859) of plant–animal interactions of different signs, with a marked role of mutualistic interactions such as pollination and zoochory. In this way, mistletoe creates conditions that support the co‐occurrence of functionally distinct organisms in the canopies, fostering pine forest biodiversity and complexity.…”

“…These changes (i.e. detrimental effects on pine herbivores and novel niche for specialised mistletoe fauna) reorganise the canopy herbivore community of the pine forest (Lázaro‐González et al ., 2019a, b, 2020). Additionally, mistletoe increases the diversity of consumers in the forest canopy by providing floral resources at a time of the year (early spring) when there are still no other flowers in the floral market.…”

Can sticky plants reduce herbivory of neighboring plants?

“…Parasitism by the hemiparasitic plant mistletoe decreases the food quality of the host by causing enhanced indirect defense (Lázaro‐González et al 2019 a ) and reductions in mineral nutrient availability (Mutlu et al 2016). Lázaro‐González et al (2019 b ) demonstrated that parasitism by the mistletoe Viscum album subsp. austriacum reduced feeding damage to pine caused by aphids, moth larvae, and weevils.…”