Complex Effects of a Land-Use Gradient on Pollinators and Natural Enemies: Natural Habitats Mitigate the Effects of Aphid Infestation on Pollination Services

SIMPLE SUMMARY: Pollination and biological pest control by insects are crucial ecosystem services for agriculture. The activity of pollinators and natural enemies (natural pest control providers), is influenced by land-use and by interactions among these organisms. However, little is known about the combined effects of such factors on the activity of these beneficial organisms and on their ultimate effects on crop yield. We studied how the characteristics of natural habitats, nearby vegetation and the presence of herbivorous pests affect pollination, natural pest control and seed set by model plants. The study was conducted in a Mediterranean agro-ecosystem, where we placed caged and uncaged potted model plants that were either aphid-infested or aphid-free. We quantified the activity of pollinators on model plant flowers, aphid predation and parasitism by natural enemies, as well as fruit and seed set. Our findings revealed a notably stronger positive effect of natural areas on pollinator activity when plants were infested with aphids compared to aphid-free plants. This suggests a potentially crucial role of natural habitats in lessening the negative impact of aphid infestation on pollination services. These results highlight the complex effects of land-use on pollinators, natural enemies and plant productivity. ABSTRACT: Pollinators and natural enemies are essential ecosystem service providers influenced by land-use and by interactions between them. However, the understanding of the combined impacts of these factors on pollinator and natural enemy activities and their ultimate effects on plant productivity remains limited. We investigated the effects of local and landscape vegetation characteristics and the presence of herbivorous pests on pollination and biological control services and their combined influence on phytometer seed set. The study was conducted in a Mediterranean agro-ecosystem, encompassing ten shrubland plots spanning a land-use gradient. Within each plot, we placed caged and uncaged potted phytometer plants that were either aphid-infested or aphid-free. We quantified insect flower visitation, aphid predation and parasitism rates, and fruit and seed set. We found scale-dependent responses of pollinators and natural enemies to land-use characteristics. Flower species richness had a positive impact on aphid parasitism rates but a negative effect on pollinator activity. Notably, we found a more pronounced positive effect of natural areas on pollinator activity in aphid-infested compared to aphid-free plants, indicating a potentially critical role of natural habitats in mitigating the adverse effects of aphid infestation on pollination services. These results highlight the complex and interactive effects of land-use on pollinators and natural enemies, with significant implications for plant productivity.