Bottom–up and top–down drivers influence urbanization effects on insect herbivory in oaks

Abstract

Urban forests provide essential ecosystem services, including pest control, biodiversity conservation, and human health benefits. Herbivory is a widespread biotic interaction that shapes ecosystem functions, such as primary productivity and soil fertility, which underpin these services. Urbanization can disrupt plant–herbivore interactions by altering plant traits, such as nutrient content or phenolic compounds (bottom–up factors), or by changing the abundance of herbivore natural enemies (top–down control), potentially threatening pest regulation and the ecosystem services provided by urban forests. Disentangling these drivers of herbivory is crucial for designing and managing urban forests to enhance resilience. To address this, we examined insect leaf herbivory on Quercus robur trees in urban and rural forest stands across 13 European cities (n = 104 trees). To assess top–down effects on herbivory, we excluded vertebrate (e.g. birds, bats), invertebrate (e.g. ants), or both groups of predators from branches on each tree using different exclosure types. We then measured insect damage on both control and predator-excluded branches. To evaluate bottom–up drivers, we measured leaf traits, specifically nutrients and phenolic compounds, and tested for correlations with leaf damage. Additionally, we recorded temperature within stands, an abiotic factor that may modulate both top–down and bottom–up forcing on herbivory. Herbivory was 24% lower on urban trees compared to rural trees. In turn, excluding vertebrate (but not invertebrate) predators increased herbivory, on average, by 40%, but predator effects were stronger in urban stands. Urban trees also had higher leaf quality, with higher nutrient and lower phenolic concentrations; however, these traits did not correlate with herbivory. Temperature was positively associated with urbanization and correlated positively with predation, but did not correlate with herbivory and did not mediate the bottom–up or top–down effects of urbanization. Overall, we find that urbanization affects herbivory through both bottom–up and top–down processes, independent of temperature-related local conditions. Despite stronger predator effects and higher leaf quality, urban trees experienced lower herbivory, suggesting that unmeasured factors, such as changes in herbivore behaviour or community structure, may play an important role. Further studies are needed to deepen our understanding and inform urban forest management.