Figure 3 . Interactive effect of percentage of urbanization and
of local canopy cover (measured as the cover of urban and local canopy
cover within a buffer of 200 and 20 m radius, respectively) on the
incidence of gall-inducing (A) and leaf-mining herbivores (B).
Leaf miners were present in 17.98 ± 0.01 % of the sampled leaves. Model
selection retained the percentage of urbanization, local canopy cover,
their interaction, year and spring precipitation as important predictors
explaining variability in leaf-miner incidence (Figure 2C, Table
A ). Specifically, leaf-miner incidence significantly decreased with
increasing urbanization (from 21.33 to 1.00 % along the range of
urbanization, Figure 2C, Figure B ). The effect of urbanization
on leaf-miner incidence was, however, contingent on local canopy cover
(significant urbanization × local canopy cover interaction;Figure 2C, Figure 3B ): the negative effect of urbanization on
leaf-miner incidence was more pronounced when there was a lower canopy
cover around focal oaks. It was significantly lower in 2019 and 2020 as
compared to 2018 (Figure 2C ). Spring precipitation and local
canopy cover had no consistent effect on leaf-miner incidence
(Figure 2C , Figure B ).
Discussion
Our study revealed that urbanization can consistently reduce insect
herbivory on the pedunculate oak throughout its geographic range. The
effect of urbanization was partially modulated by the percentage of
canopy cover around oaks, with differences among herbivore feeding
guilds. Specifically, we found that urbanization and local canopy cover
had independent and opposite effects on overall leaf damage. In
contrast, effects of urbanization on gall-inducer and leaf-miner
incidence depended on local canopy cover, with a more pronounced
negative effect of urbanization on gall-inducer and leaf-miner incidence
when there was a greater and lower local canopy cover, respectively.
These results show the complexity of plant-herbivore interactions in
urbanized areas, highlighting that local habitat characteristics within
cities have the potential to attenuate or modify the effect of
urbanization on biotic interactions.
Effect of
urbanization on herbivory
We found that the incidence of both gall-inducing and leaf-mining
herbivores decreased with increasing urbanization, suggesting that the
abundance of these species decreased with urbanization. This result
agrees with previous reports that have shown that urbanization reduces
the abundance and diversity of several guilds of insect herbivores (Barr
et al., 2021; Dobrosavljević et al., 2020; Fenoglio et al., 2020;
Herrmann et al., 2012; Kozlov et al., 2017; Moreira et al., 2019) with
the noticeable exception of sap-feeding herbivores (de Andrade and
Rivkin, 2020; Parsons and Frank, 2019). For instance, Herrmann et al.
(2012) found lower species richness of galler communities on the valley
oak (Quercus lobata ) in urban areas than in natural areas.
Similarly, Dobrosavljević et al. (2020) found lower richness, abundance
and diversity of leaf-miner communities on the pedunculate oak in urban
areas than in natural areas.
We also found that leaf damage decreased with increasing urbanization
around focal oaks. Although this result aligns with the observation that
the incidence of gall-inducing and leaf-mining herbivores decreased with
increasing urbanization, it is important to consider that leaf damage
(i.e., the amount of biomass consumed by chewing herbivores) may not
scale proportionally with the abundance and diversity of insect
herbivores. Several other ecological factors that are influenced by
urbanization may determine the amount of damage caused by chewing
herbivores. They include the top-down control of herbivore populations
by their enemies (Kozlov et al., 2017; Planillo et al., 2021; Turrini et
al., 2016) as well as plant defenses and quality (Moreira et al., 2019;
Thompson et al., 2016). The correlative nature of our data does not
allow further robust inferences on the mechanisms underlying the
observed patterns.
Effect of local
canopy cover on herbivory
Herbivory varied with canopy cover in the immediate vicinity of oaks,
but this effect was guild specific: there was an independent positive
effect of local canopy cover on herbivory, a negative effect on
gall-inducing herbivores, and no effect on leaf-mining herbivores.
Whereas several studies have compared herbivore abundance or diversity,
and sometimes herbivory, between urban and forested environments
(Herrmann et al., 2012; Kozlov et al., 2017; Moreira et al., 2019), only
a handful of them have addressed the effect of urban tree density on
insect herbivores (Barr et al., 2021; Christie et al., 2010; Christie
and Hochuli, 2005; Herrmann et al., 2012; Long and Frank, 2020; Meyer et
al., 2020; Raupp et al., 2010). Their findings were contradictory with
reports of both higher (Christie and Hochuli, 2005) and lower (Herrmann
et al., 2012; Long and Frank, 2020) herbivory in isolated trees as
compared to trees growing in larger forest patches. This effect of local
canopy cover also mirrors variability in the response of herbivory to
the size of forest fragments (De La Vega et al., 2012; Kaartinen and
Roslin, 2011; Simonetti et al., 2007; Valdés-Correcher et al., 2019). We
therefore refrain from putting forth any particular mechanism that may
underlay the patterns we observed. However, we speculate that denser
tree canopies may have buffered micro-climatic variations (Coley and
Barone, 1996; Dale and Frank, 2014; Yamasaki and Kikuzawa, 2003), which
may have been particularly favourable to chewing herbivores that are
external feeders (Savilaakso et al., 2009) and at the same time
unfavorable to leaf-galling herbivores, as they benefit from high
temperatures (Valdés-Correcher et al., 2021). Alternatively, top-down
forces also vary with local canopy cover and may consequently influence
insect herbivory. For instance, predation activity of birds (Stemmelen
et al., 2020) and the abundance of birds (Valdés-Correcher et al., 2019)
increase with increasing local canopy cover. However, if the observed
negative association between herbivory and forest cover would have been
mediated by bird predation, it would have displayed the opposite
pattern. Deciphering the relative importance of the mechanisms acting
upon insect herbivores will represent a major step forward in our
understanding of insect herbivory in urban environments.
Interactive
effect of urbanization and local canopy cover on herbivory
Cities are heterogeneous environments where greenness may vary widely.
The design of our study allowed us to partially disentangle the response
of herbivory to the joint variation in urbanization and local canopy
cover. We found that increasing local canopy cover modulated the effect
of urbanization on some herbivores. Specifically, the negative effect of
urbanization on gall-inducing herbivores strengthened with increasing
local canopy cover, whereas increasing local canopy cover annulled the
effect of urbanization on leaf-mining herbivores. Urbanization and local
canopy cover have antagonistic effects on the microclimate and enemy
pressure. Cities are warmer than the surrounding rural areas as a result
of the “heat island effect” (Kalnay and Cai, 2003; Parker, 2010; Roth
et al., 1989), which is buffered by the presence of trees (Loughner et
al., 2012; Nuruzzaman, 2015). Likewise, forest patches in urban
environments serve as habitats for both herbivores and predators, which
is likely to modify the strength of horizontal (herbivores-herbivores)
and vertical (herbivores-predators) interactions in urban trees (Long et
al., 2019; Long and Frank, 2020). Endophagous herbivores such as
gall-inducers and leaf-miners are more sheltered from the environment
than ectophagous herbivores. Thus, ectophagous herbivores may be more
sensitive to local environmental conditions than endophagous herbivores.
For instance, we found a positive relationship between the incidence of
gall-inducing herbivores and temperature. It is possible that by
buffering the heat island effect, the presence of a denser canopy
reduced the incidence of gall-inducers on oaks. On the contrary,
leaf-mining herbivores were found to be favoured by lower (Gaston et
al., 2004) or intermediate temperatures (Valdés-Correcher et al., 2021).
For these herbivores, a denser canopy could have negated the heat island
effects, creating more favourable habitats. We cannot exclude that the
interactive effect of urbanization and canopy cover was partially
dependent on differential predation rates, but this could not be
investigated in the present study.
Effect of
climate on insect herbivory
Climatic variables were included in the analyses to take into account
that oaks were sampled along a latitudinal gradient. They had a
significant effect on insect herbivory and this effect varied among
feeding guilds. Consistently with previous studies (Kozlov et al., 2016;
Valdés-Correcher et al., 2021), we found that precipitation had a
negative effect on leaf damage; temperature had a positive effect on
gall-inducer incidence, whereas leaf-miner incidence did not vary with
climate. The differences in the effect of climate among feeding guilds
may be due to differences in insect herbivore strategies to survive
different climatic conditions, which was discussed extensively in a
previous paper (see Valdés-Correcher et al., 2021).
Conclusions
Our simultaneous consideration of the effect of urbanization and local
canopy cover on insect herbivory provides novel insights into
plant-herbivore interactions. We found that insect herbivory responds
simultaneously to both urbanization and local canopy cover in the
pedunculate oak in the major part of its geographic range. Importantly,
our results highlight that urbanization has a negative effect on insect
herbivory across the three feeding guilds. However, local canopy cover
as well as its interaction with urbanization influenced insect herbivory
of different feeding guilds differently. Thus, local canopy cover within
cities has the capacity to mitigate or modify the effect of urbanization
on biotic interactions, as it influences the effect of urbanization on
herbivores differently. Therefore, this study supports the importance of
maintaining trees in urban areas as it may consequently contribute to
the preservation of biodiversity of insect herbivores in urban areas.
Important insights will be gained by investigating the mechanisms
driving these patterns, in particular by deciphering the interactive
effects of urbanization and canopy cover on the microclimate and enemy
pressures herbivores are exposed to.