Introduction
Urbanization is one of the major drivers of global change (Lambert et al., 2015; Rossetti et al., 2017). It causes fragmentation, isolation and degradation of natural habitats (Pickett et al., 2001; Zipperer et al., 2000) in addition to creating warmer and drier conditions for both plants and animals (Chai et al., 2019; Taha, 1997; Wang et al., 2017). As a consequence, urbanization results in the simplification of ecological communities and the alteration of ecosystem processes such as biotic interactions (Bang and Faeth, 2011; Fenoglio et al., 2020; Magura et al., 2010; McDonnell and Hahs, 2015). Understanding how the nature and strength of species interactions change along urbanization gradients could help us to unravel the mechanisms driving changes in species distribution and composition, which remain insufficiently known (but see Kozlov, Lanta, Zverev, & Zvereva, 2015; Moreira et al., 2019; Turrini, Sanders, & Knop, 2016).
Plant-herbivore interactions play a pivotal role in ecosystems and consequently are one of the most studied biotic interactions (Jamieson et al., 2012; Stam et al., 2014). Analyses of insect herbivory patterns on woody and herbaceous plants along urban-rural gradients have received increasing attention in recent decades (Dreistadt et al., 1990; Kozlov et al., 2017; Moreira et al., 2019; Raupp et al., 2010). Several studies measured the response of a single herbivore species (Parsons and Frank, 2019; Turrini et al., 2016), that of different herbivore feeding guilds (Cuevas-Reyes et al., 2013; Kozlov et al., 2017; Moreira et al., 2019) or the diversity and abundance of herbivores (Fenoglio et al., 2020) in urban vs rural environments (but see Parsons & Frank, 2019). Although there seems to be a general tendency towards reduced insect abundance and diversity in urban settings as compared to rural environments (Fenoglio et al., 2020), there is no consensus on whether insect herbivory is higher (Parsons and Frank, 2019; Turrini et al., 2016) or lower (Fenoglio et al., 2020; Kozlov et al., 2017; Moreira et al., 2019) in urban compared to rural habitats. Given these mixed findings, a better understanding of the underlying ecological factors driving urbanization effects on insect herbivory is needed.
Several factors may explain the inconsistent effects of urbanization on insect herbivory reported in the literature. First, insect herbivore species vary markedly in their susceptibility to changing abiotic conditions (Van Der Putten et al., 2010) and might therefore exhibit different patterns of abundance and damage on focal host plants in urbanvs rural areas (Kozlov et al., 2017; Moreira et al., 2019). In this sense, urban habitats are often associated with stressful climatic conditions (i.e., cities are warmer and drier than surrounding rural environments; Calfapietra, Peñuelas, & Niinemets, 2015; Dale & Frank, 2014; Meineke & Frank, 2018) where endophagous herbivore guilds, e.g., leaf-mining and leaf-galling herbivores, could outperform exophagous herbivores, e.g., leaf chewers (Koricheva et al., 1998). Second, cities differ greatly in the amount of vegetation they harbour. The local tree cover (i.e., both overall tree density and potential host tree abundance) is a strong driver of urban biodiversity and trophic interactions between trees, insect herbivores and their enemies (Herrmann et al., 2012; Long and Frank, 2020; Meyer et al., 2020; Stemmelen et al., 2020). More isolated trees frequently offer fewer resources to insect herbivores (Chávez-Pesqueira et al., 2015), leading to a decrease in insect herbivory (Long and Frank, 2020). Isolated trees are also key (micro) habitats having a disproportionate importance for foraging predators, especially bats and birds (DeMars et al., 2010; Fischer et al., 2010; James Barth et al., 2015; Le Roux et al., 2018). At the same time, climatic conditions also vary with local tree cover resulting in high temperature and light intensity in more isolated trees, which may also influence insect herbivores (Dale and Frank, 2014; Shrewsbury and Raupp, 2000). In this way, the amount and distribution of green areas – and in particular that of trees – could interfere with the effect of urbanization on leaf herbivory. Thus, the relative importance of all these explanatory mechanisms needs to be confirmed along an urbanization gradient that ranges from ’green islands’ with high tree density to almost fully paved areas with only a few isolated trees.
In this study, we investigated the independent and interactive effects of urbanization and local canopy cover on insect herbivory on the pedunculate oak (Quercus robur L., 1753) throughout most of its geographic range in Europe. To this end, we quantified herbivory as the proportion of leaf area consumed by chewing insect herbivores as well as the incidence of leaf-mining and gall-inducing herbivores in leaf samples collected by professional scientists and schoolchildren in European countries between 2018 and 2020. We specifically predicted that: (a) insect herbivory decreases with urbanization and increases with canopy cover; (b) the effects of urbanization and canopy cover on leaf herbivory vary among the herbivore guilds; and (c) urbanization and local canopy cover have an interactive effect on insect herbivory that vary among herbivore guilds. Overall, this work provides one of the most comprehensive studies yet, testing for effects of urbanization on plant-herbivore interactions and shedding light into potential mechanisms underlying such effects.