*3.2. Environmental Influence*

Six studied UGAs presented more than 50% of their inside area as paved, and only one of the twelve UGAs had less than 50% of the surrounding paved area. The average of flower coverage in each UGA varied between 6.57 m2 (U4) and 82.52 m<sup>2</sup> (U7). The most significant number of trees was registered at the U11 and the highest DBH (median = 63) at the U7 area. Three of the twelve areas studied did not have buildings higher than three floors (Table 2).

In the 12 UGAs, the bees visited 84 plant species belonging to 39 families. The average of flowering plant families among areas over the study period was 10 (ranging from 6 to 14). The families found the most in the studied UGAs were Asteraceae (10 of the 12 areas), Fabaceae (8) and Verbenaceae (8). The total plant richness per UGA ranged between 7 and 18 species. The sampling area with the highest number of plant richness was U11. The plant species with the highest frequency of occurrence in the areas were *Emilia sonchifolia* (83.3% of the areas), *Duranta erecta* (67.7%), *Tridax procumbens* (58.3%) and *Ixora coccinea* (50%). Nectar and pollen were primary floral resources for pollinators in 62 plant species, while 8 species offered only nectar, 6 species only pollen and 1 specie offered pollen and flower oil. Of the sampled bees, 55% come from flowers of plant species considered native to Brazil, and this total was mainly due to visits by Augochlorini (67% of all individuals in this tribe) and Meliponini (59%). In contrast, most bees from the tribes Apini (a species with 55% of the total number of individuals) and Halictini (a species with 58%) relate to 4 exotic plant species.


**Table 2.** Environmental conditions of 12 urban green areas studied in Campos dos Goytacazes/RJ. Inside UGA: percentage of paving (PV), number of trees (NT), diameter at breast height (DBH), plant richness (PR), flower coverage in m<sup>2</sup> (FC). Surrounding conditions measured inside a buffer of 500 m from UGA center: surrounding paved area percentage (SPV) and the number of buildings with more than three floors (NB).

> Trees' flowers received visits from 47% of the bee species, followed by herbaceous (30%) and shrubby plants (23%). Principal component analysis (PCA) showed that solitary bee correlated with herbaceous plants. Specialists, generalists, cavity and intermediate level of sociality were correlated with plants with shrubby habit, while bees from the eusocial showed correlation with trees (Figure 3).

**Figure 3.** Principal Component Analysis (PCA) plot of correlation between bee guilds: SOIL (soil), CAVI (cavity), SPEC (specialist), GENE (generalist), SOLI (solitary), INTE (intermediate), EUSO (eusocial), and plant habits: Arbo (arboreal), Shru (shrubby) and Herb (herbaceous), U1 to U12 represent the urban green areas studied in Campos dos Goytacazes, Brazil.

Flower coverage was the predictor variable that more influenced the guilds analyzed in this study. The number of buildings with more than three floors explained the abundance of solitary and soil bees. The DBH negatively impacted the abundance of specialist and solitary bees. The paving percentage did not influence the bees' responses, and the area and number of trees were excluded from analyses because they presented collinearity (Table 3).


**Table 3.** Parameter estimates of a generalized linear model, explaining abundance and richness of bee guilds in urban green area (UGA) in Campos dos Goytacazes, RJ, Brazil. Inside UGA: flower cover in m2 (FC), diameter at breast height (DBH), plant richness (PR), surrounding percentage of paving (SPV) and the number of buildings with more than three floors (NB).

### **4. Discussion**

The study data suggest that despite being a medium-sized city, the study area is at a high level of urbanization, with percentages of paving above 50% [16] and urban densification. Large paved areas have already replaced the natural areas at this stage, where only low flower covers and few potential nesting places for bees remain, making these areas harmful to the pollinator community [4]. This condition highlights the importance of urban green areas as bees' refuge, functioning as a shelter for different bee species. The lack of previous data does not allow comparisons of community parameters over time. However, the comparison between areas enables us to realize variations in bee composition. The presence of robust bees such as *X. frontalis, X. nigrocincta* and *E. nigrita* in UGA (U2, U5, U6), with a high percentile of paved surrounding (over 90%), corroborates the idea that UGAs can provide resources in scarcity situations. These bees have a long flight range and can cross large distances in the urban matrix searching for food.

Results indicated that the different guilds of bees diverged in responses to the conditions found in urban green areas and their surroundings. The structure of the bee community showed a composition mainly of eusocial and generalist bees, typical in open and highly modified environments. Other studies in Brazil have shown the tendency for eusocial bees to be more abundant in urban areas [32–35]. The fact that the colonies of eusocial species have thousands of individuals and are active throughout the year explains these results, allowing to take advantage of resources from plant species with different phenological cycles [15]. In addition, eusocial bees recruit and can collect a large number of resources quickly. Therefore, in places with little diversity of resources, these eusocial bees usually benefit compared to solitary bees.

In 50% of UGAs, the most abundant species was *Apis mellifera* (32% of individuals sampled). The more remarkable plasticity of *A. mellifera* favors the increase of its abundance in urban areas and the competitive pressure on native species, which can lead to the homogenization of the structure of the bee community in these areas [36] through the replacement of native bee species by this exotic one [37]. Although several human activities promote biotic homogenization, urbanization is the one that most favors this process [38,39]. Cities are made to attend to human needs, and therefore have a uniform nature, repeated throughout the world, with buildings, roads and houses. The construction of cities destroys the habitat of many native species, but on the other hand, creates habitats for other species, such as the exotic *A. mellifera* that can use cavities in human constructions to build nests. Consequently, more vulnerable species tend to disappear, decreasing the community species richness [38,39].

The similarity of 67% between U7 and U8 draws attention, as they are about 5 km apart. Their surrounding conditions are similar, with lower percentages of surrounding paving (41% and 51%, respectively) and low numbers of buildings with more than three floors (*n* = 4 and *n* = 0). Both are in the city borderline connected with vegetated areas. On the other hand, U7 and U4—the less similar areas, are only 700 m apart, and U4 is surrounded by a high percentage of paved areas (71%) and buildings (*n* = 14) and had low flower coverage (6%). These environmental conditions can compromise the movement of bees between areas and influence the composition of the bee's community since it responds in small scales to the characteristics of the environment associated with the supply of resources and nesting site [40].

The distribution of bees between native and exotic plant species did not explain the abundance and richness of the different guilds between the areas. The average flower coverage was 32%, and considering that this variable can measure the available resource, it is possible that the bees are using exotic plants as an alternative to obtain resources. This behavior is present in bees studied in an environmental gradient in the United States, aiming to examine the importance of exotic plants for native bee species [41]. In environments with anthropogenic disturbances, bees used many exotic species, and the authors found a correlation between visits to exotic plants and the low abundance of plants in the environment. This study corroborates this idea because 23% of bees sampled in our study were in shrub species, with 16% sampled in three species: *Duranta erecta*, *Ixora coccinea* and *Ruellia simplex*. All three are exotic species widely used in urban afforestation in the region. Resistant to heat and lack of water, they bloom year-round and have often been one of the few resource sources for pollinators in the UGAs.

Plant habit appears as a determinant in the distribution of bee guilds. The work highlights the importance of herbaceous plants for maintaining the solitary bees and those that nest in the soil. Among them 63% were collected in herbaceous plant species (25% solitary, 38% soil-nesting bees). Herbaceous plants were considered an essential source of resources and attractive to a large number of visitors in a study carried out in a restinga (coastal sand area) conservation unit in the state of Rio de Janeiro (Brazil) [42]. According to the authors, naturally born herbaceous/pioneers were associated with higher richness and abundance of floral visitors in restoration areas in restinga remnants. Different herbaceous plants offer various resources that can benefit wild bees when supplying their brood cells [43]. As herbaceous plants are born spontaneously in areas of exposed soil, their presence in UGAs represents potential resources of foraging and nesting places for bees that nest in the soil.

The abundance of eusocial bee appears associated with plant species of arboreal habit. Eusocial bees forage in groups and demand a greater abundance of flowers. Among the eusocial species are the stingless bees considered the primary pollinators of tropical trees with "mass" flowering [44]. Furthermore, eusocial species nest in pre-existing cavities in tree trunks, increasing the importance of tree species to native eusocial species.

Among the guilds that demonstrate greater vulnerability to the urban environment are the specialist bees. In this study, we found 1% of specialist bees in the community, similar to that described by other studies in the urban area [16]. The decline of specialist bees can be directly related to the loss of the host plant, as described in a study that found the decline of specialist bees associated with the decline of Fabaceae plants caused by the management of agricultural areas and the removal of native vegetation [45].

Analyzing the abundance of bees that nest in the soil, we found a sensitivity related to the number of buildings with more than three floors. Of the 39 species of bees sampled in this study, 16% nest in the soil. As the number of buildings increases, there is less abundance of bees from this guild in the UGAs. These high buildings are usually in large areas of paving surface that limit nesting sites as a consequence of the replacement of exposed soil areas by paved areas and the removal of small bushes or spontaneous vegetation that provide food resources [35]. However, for bees that nest in the soil, the availability of nesting sites is a decisive factor in the establishment and growth of their populations [46].

Considering that 60% of solitary bees are also soil-nesting bees, they are also influenced by a variable "number of buildings with more than three floors" on richness and abundance. A lower abundance of solitary bees appeared overall, with only 11% of the captured bees belonging to solitary species. The urban environment is composed of mosaics of vegetation and buildings that probably prevent or hinder the circulation of bees with a small flight radius, such as species of Augochlorini that we found in this study. Few individuals in this group reach long flight ranges, which increases the dependence of solitary bees on the resources available near the nests. The distance from the resource determines the ability to maintain the species [47]. According to the authors, the number of descendants generated by the species *Osmia lignaria* was more significant when the nest was close to areas with a good supply of resources. We can expect a similar situation for solitary bees in the studied areas.

The results of the solitary, soil and intermediate bees influenced by the "number of buildings with more than three floors" and by the surrounding pavement demonstrate the importance of creating green corridors that increase the possibility of bees' movement, avoiding isolation. According to a recent study [48], it is not urban environments that negatively influence the response of bee communities, but the way cities are organized act as filters that limit the presence of some species. Our results corroborate this affirmation as they indicated that the green areas and surroundings do not consider the necessities of different bee species.
