Negative impacts of a vertebrate predator on insect pollinator visitation and seed output in Chuquiraga oppositifolia, a high Andean shrub

Studies on plant-pollinator interactions have largely neglected the potential negative effects of the predators of pollinators on seed output, even though anti-predatory behaviour of pollinators may affect visitation patterns, pollen transfer, and therefore potentially, plant reproductive output. We tested the hypothesis that the presence of lizards and insectivorous birds, by reducing pollinator visitation, can have significant negative effects on seed output in the insect-pollinated, genetically self-incompatible lower alpine Andean shrub, Chuquiraga oppositifolia (Asteraceae). The lower alpine belt supports a high density of territorial Liolaemus (Tropiduridae) lizards and low shrubs interspersed among rocks of varying sizes, the latter inhabited by lizards and commonly used by flycatchers Muscisaxicola (Tyrannidae) as perching sites. In a 2x2 factorial predator-exclusion experiment, visitation rates of the most frequent pollinators of C. oppositifolia (the satyrid butterfly Cosmosatyrus chilensis and the syrphid fly Scaeva melanostoma), the duration of pollinator visits, and seed output, were 2-4 times greater when lizards were excluded, while birds had no effect. In a natural experiment, visits by S. melanostoma were 9 times shorter, and pollinator visitation rates of C. chilensis and S. melanostoma, and C. oppositifolia seed output were 2-3 times lower on shrubs growing adjacent to lizard-occupied rocks compared to those growing distant from rocks. Our results, verified for additional Andean sites, suggest that lizard predators can alter the behaviour of pollinators and elicit strong top-down indirect negative effects on seed output. Such effects may be especially important in high alpine plant communities, where pollinator activity can be low and erratic, and pollen limitation has been reported.