Importance of green areas connectivity
Using data available in the literature combined with landscape analysis we found that, as we predicted, the connectivity among green areas within the urban landscape is positively related to the richness and abundance of pollinators. Our results show urban green areas host a greater diversity and abundance of pollinators when they are closer to each other (i.e., more connected). Thus, the proximity of green spaces could be promoting and facilitating the movement of urban pollinators among them.
Fenoglio et al. (2020) reported negative effects of urbanization for arthropods in cities and attribute it, in part, to the loss of habitable area and low habitat connectivity. Regardless of connectivity, non-urban sites presented higher pollinator richness than urban and peri-urban sites. These results are partially opposite to those reported by Baldock et al. (2015), who did not register differences in the diversity of pollinators in urban, agricultural and natural sites. However, such differences may be due to the use of different methodologies and criteria to classify the sampling sites. On the other hand, these authors found different responses for several taxonomic groups (bees, flies, hoverflies), with bee species richness higher and fly abundance (except hoverflies) lower in urban sites (Baldock et al. 2015). In our study, most of the analyzed papers included bees as the only or one of the main taxa, and we found a greater richness of these insects in non-urban sites (Geslin et al. 2016; Kratschmer et al. 2018; Sobreiro et al. 2019; Birdshire et al. 2020, among others). Ecological changes (e.g., extended phenology of flowering, availability of nesting sites, increased temperatures) produced by urbanization could generate positive, negative, or null effects on the pollinator communities. For example, Duchenne et al. (2020) classified wild bees as “winners or losers” from urbanization depending on several factors like sociability, nesting substrate and breadth of diet.
Different taxonomic groups of pollinators could be differentially affected by connectivity depending on their dispersal abilities. Hence, less mobile organisms could be more influenced to local scale (e.g., host plants for larvae butterflies) and more mobile organisms (bees, bumblebees, syrphids) to landscape scale (e.g., green areas connectivity) (Braaker et al. 2014). Thus, large bees with high foraging areas might be more affected by landscape connectivity than flies. However, some flies Syrphid species are considered highly mobile groups (Schweiger et al. 2007). On the other hand, butterflies have a relatively short lifespan as adults and moderate dispersal abilities (Soga & Koike 2013). Therefore, it would be reasonable to think that cities with more connected green areas would be beneficial for all insect pollinators regardless their dispersal distances, while those sites with more distant green areas would be disadvantageous for smaller pollinators with low dispersal.
Pollinator richness
Our results showed that landscapes with more connected green areas (i.e., less isolated), are harboring a greater richness of pollinators in all landscapes, regardless of their level of urbanization. This relationship was even more pronounced in urban sites than peri-urban and non-urban ones, which could indicate that landscape connectivity as a maintainer of pollinator richness becomes more useful in environments with a high degree of urbanization, regardless of the size of the green area. This suggests that, beyond the size of the green areas, it is important that they are connected to each other to allow the flow of pollinators between such green spaces.
It is important to highlight that there are more factors that influence the presence of pollinators within the cities, such as the surrounding landscape, temperature, and humidity, among others (Ayers & Rehan, 2021). For example, the impervious surface (roads, buildings, among others) could be generating physical barriers within the landscape and mainly among the vegetation patches, limiting the diversity of pollinators capable of living in such sites, such as those with greater flight ranges or greater body size. Thus, it becomes relevant to consider the connectivity of green areas to evaluate the quality of different anthropogenic landscapes, as well as other landscape variables such as environmental heterogeneity and fragmentation (Ayers & Rehan 2021). On the other hand, we did not analyze the different taxa separately, and the community present in each environment may vary according to their functional traits and life histories (flight ranges, body size, time of emergence, among others) (Luder et al. 2018; Wenzel et al. 2020). Although the general trend of the pollinator community is to increase with increasing connectivity, some taxonomic groups could respond with different magnitude to these variables, or to the urbanization gradient (Baldock et al. 2015).
Pollinator abundance
The abundance of pollinators increases with the connectivity of green areas in urban and peri-urban sites (Plascencia & Philpott 2017, but see Cohen et al. 2020), but no relationship was found in non-urban sites. In the same way as for pollinator richness, the abundance of pollinators is higher in non-urban sites compared to urban and peri-urban ones. This result contrasts with those reported by Zaninotto et al. (2021), who studied the general composition of floral visitors of two focal plant species; these authors observed a greater abundance of pollinators in urban environments compared to rural ones. They attributed such results to the greater dominance of social species (Apis mellifera and Bombus pascorum) in urban sites. In our study we included other taxonomic groups of pollinators in addition to bees (as syrphids, other flies, butterflies). Persson et al. (2020) showed that hoverflies and wild bees respond differently to urbanization, being urban hoverfly assemblages a subset of rural ones, and the solitary bee species richness higher in urban than in rural gardens. However, Desaegher et al. (2018) mentioned Syrphidae as an “urbanoneutral” family. On the other hand, in a review of urban diurnal Lepidoptera, Ramírez-Restrepo & MacGregor-Fors (2017) showed that most studies revealed a negative impact of urbanization intensity on richness and abundance of butterflies.
Generally, within the cities there exists a more homogenized fauna mainly composed by a small subset of cosmopolitan species adapted to urban conditions (Patitucci et al. 2011). These synanthropic species (generally, exotic and dominant) are associated with human settlements (Nuorteva 1963) and can reach high population densities (e.g., Musca domestica [Muscidae], Eristalis tenax [Syrphidae], among others). Also, urbanization is positively correlated with increased prevalence of exotic, social bees (e.g., Apis mellifera and Bombus spp.) and native, solitary (e.g., Anthidium manicatum [Megachilidae]) bees (Fitch et al. 2019). In an urban context, these synanthropic species could be responsible for the increase in the abundance of pollinators. So, in the same way as for pollinator richness, regardless of size, good connectivity between green areas is a fundamental requirement to maintain high abundances of pollinators and allow their movement between these spaces.
Resources for pollinators
Although urban settlements are disturbed and heterogeneous landscapes, they offer nesting sites and floral resources (primarily ornamental and exotic species, but several native species are also present) for pollinators (Matteson et al. 2008; Fortel et al. 2014; Hülsmann et al. al. 2015). In our study we did not include floral diversity as a variable because less than 10% of the studied work reported this data. However, we understand that this variable could influence our results. As a result of a SPIPOLL protocol (Photographic monitoring of pollinating insects, a citizen science project from the Museum national d’Histoire naturelle (MNHN)) carried out in France, floral morphology was the main driver of the 46 most frequent flower-feeding insect families (Desaegher et al. 2018). In addition, the distribution of floral resources could be driving the distribution of pollinators throughout cities (Krahner & Greil, 2020) since they represent an abundant and constant resource over time due to the presence of ornamental plants in gardens and private squares (Garbuzov et al. 2017; Corcos et al. 2019).
Study limitation
A possible limitation of our work is that only a radius of 500 meters was considered. We carried out a systematic review of published works in which the sampled sites were already established. We tried to use larger radii (750 and 1000 meters), even though delimited areas for higher radii from many UGAs overlapped, so we had to rule out sites, and little information remained. In addition, although it is known that the feeding distances of pollinating insects can exceed this working radius, the literature suggests that, in urban environments, the distances traveled to feed are smaller than in natural environments (López-Uribe et al. 2008). For example, foraging ranges of some bumblebees species within urban environments do not exceed 500 meters (Osborne et al. 2008). On the other hand, the movement of pollinators not only depends on the spatial distance that separates patches of vegetation (green areas), but also on the presence of restrictions imposed by physical barriers such as buildings and other vertical constructions (Peralta et al. 2011), which limits the movement of individuals.