Evidence of indirect biotic resistance: native ants decrease invasive plant fitness by enhancing aphid infestation.

The biotic resistance hypothesis asserts that native species may hinder the invasion of exotic species, which can occur either directly or indirectly by influencing interactions between exotic and local species. Aphid-tending ants may play a key role in the indirect biotic resistance to plant invasion. Ants may protect aphids, thus increasing their negative effect on exotic plants, but may also deter chewing herbivores, thus benefiting exotic plants. We studied native aphid-tending ants (Dorymyrmex tener, Camponotus distinguendus, and Dorymyrmex richteri) on exotic nodding thistles (Carduus thoermeri), which are attacked by thistle aphids (Brachycaudus cardui) and thistle-head weevils (Rhinocyllus conicus). We evaluated the impact of ants, aphids, and weevils on thistle seed set. We compared ant species aggressiveness towards aphid predators and weevils and performed ant-exclusion experiments to determine the effects of ants on aphid predators and weevils. We analysed whether ant species affected thistle seed set through their effects on aphids and/or weevils. The ant D. tener showed the most aggressive behaviour towards aphid predators and weevils. Further, D. tener successfully removed aphid predators from thistles but did not affect weevils. Excluding D. tener from thistles increased seed set. Analyses supported a negative indirect pathway between the aggressive D. tener and thistle seed set through aphid populations, while the other ant species showed no indirect effects on thistle reproduction. Therefore, aggressive aphid-tending ants may enhance biotic resistance by increasing aphid infestation on exotic invasive plants. This study highlights the importance of indirect biotic resistance in modulating the success of invasive species.

Nectar shortage caused by aphids may reduce seed output via pollination interference.

Herbivores decrease plant fitness by consuming reproductive tissues, limiting resources, and/or affecting mutualisms. Although these mechanisms were extensively tested in chewing herbivores, the impact of other functional groups (e.g., sap-feeders) remains poorly understood. We investigated whether aphids affect plant reproduction via direct resource limitation on seed production and/or pollination interference. We compared plant traits and the seed set of naturally aphid-free vs. aphid-infested plants and then manipulated aphid presence and pollen receipt. We used path models to examine the links between variables. Nectar volume and seed set of aphid-infested plants was 54% and 42% lower than that of aphid-free plants. 72 h after removing aphids, nectar volume was restored to the level of aphid-free plants. When pollinators were excluded, the seed set of aphid-infested and aphid-free plants did not differ, suggesting that direct resource limitation on seed production was not the cause of reduced plant fitness. Manual addition of pollen restored the seed set of aphid-infested plants to the level of aphid-free plants, evidencing that plants were pollen limited. The path analysis showed a negative link between aphids and the seed set via nectar volume, supporting that nectar shortage caused by aphids may interfere with pollination and reduce plant fitness. Since aphids are crop pests and feed on a large number of animal-pollinated plants, the potential of these insects to influence pollination and plant fitness is high. This study emphasizes the ecological importance of aphids and the need to better understand the links between sap-feeding herbivory, pollination, and plant fitness.