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.