Understanding the effects of urbanization on bee communities is essential for conservation and management programs for these pollinators. We investigated bee communities in two distinct land-use conditions in Mexico: one within the Bosque el Nixticuil-San Esteban-El Diente Natural Protected Area, which represents a conserved oak forest, and the other in a highly urbanized area in adjacent parks located approximately one kilometer from the conservation area in the Metropolitan Zone of Guadalajara with a population of 5.3 million. The objectives of the study were to 1) record the effects of urbanization on bee communities in terms of species richness, abundance and α and β diversity in an oak forest within a natural protected area and the adjacent urban area, and 2) identify the most susceptible bees and those that benefit from urbanization, and 3) to relate vegetation to bee communities. The results of the rarefaction analysis indicate that the protected natural area exhibited significantly higher richness and diversity than the urbanized area. Beta diversity analysis revealed a low species turnover, accompanied by a high rate of bee loss between conditions. A limited number of species demostrate an increase in abundance within urban areas, mainly Ceratina species, Augochlora smaragdina and Centris nitida. Furthermore, the richness of life history traits of bees was analysed. In all cases, the number of species decreased, with mainly non-eusocial, cavity or wood nesting, and polylectic feeding bees prevailing in the urban area. The richness and abundance of bees is related to the richness of plants, so it was expected to find more species and genera in the natural area. In conclusion, urbanization has a negative impact on the richness and diversity of bee communities, as well as on species composition.

Decline bees, flower resources, pollinators, species richness

Despite the crucial role of bees in maintaining the health of wild and agricultural ecosystems, recent reports indicate a decline in wild bee populations (Potts et al. 2010). Habitat loss due to deforestation, intensive insecticide use in cultivated areas, the expansion of urban areas, the introduction of exotic species that can transmit diseases and increase foraging competition with native bees, and the possible effects of climate change are key factors contributing to this decline (Winfree 2010). Habitat loss, particularly due to the expansion of urban areas, is considered the primary long-term cause of bee decline (Goulson et al. 2015).

The causes of the decline in bee richness due to urbanization are diverse (Wensel et al. 2020). For example, Martins et al. (2013) mention the scarcity of preserved native vegetation in these environments. In addition, the temporal dynamics of these resources differ due to factors such as continuous watering of green spaces and the presence of exotic ornamental plants that flower at different times than native plants, causing changes in pollinator population dynamics (Wray and Elle 2015).

Urbanization also reduces the possible nest substrates for bees (Theodorou et al. 2020b). Ground-nesting bees decline in urban areas due to the reduction of suitable nesting surfaces (Geslin et al. 2016), while cavity-nesting bees take advantage of gaps in human constructions (Prendergast et al. 2022).

Bees belong to different guilds that respond differently to urbanization depending on their life histories (Prendergast et al. 2022). Urbanization simplifies the landscape and reduces the richness, diversity and phylogenetic groups of flowering plants (Theodorou et al. 2020a). This affects bees, as they feed on nectar as adults and require pollen and flower oils to feed their larvae. In addition, they need such plant resources as leaves and resins as nest materials (Michener 2000). Generalist (polylectic) bee species predominate in cities, but some specialists (oligolectic) may proliferate due to the introduction of exotic flora and ornamental plants (Theodorou et al. 2020a).

Better understanding the effects of urbanization on bee communities has become a critical objective. Although the results of research are variable (Birdshire et al. 2020), most studies report a negative impact of urbanization on some attributes of bee communities, including species richness, overall abundance and/or diversity (Martins et al. 2013; Cardoso and Gonçalves 2018; Razo-León et al. 2018; Zattara et al. 2021). In contrast, other studies have documented comparable or even higher levels of richness, abundance, and diversity in urban relative to natural areas (Carper 2014; Fortel et al. 2014; Lowe and Foltz-Sweat 2017). It is challenging to determine the conservation status of bees. However, some studies based on historical records reveal worrying data. For instance, in the United Kingdom and the Netherlands, there has been a generalized decline in the richness and abundance of wild bees and other pollinators (Biesmeijer et al. 2006). According to occurrence data from the Global Biodiversity Information Facility (GBIF) the recorded bee species richness has been continuously decreasing since 1990. Furthermore, comparing records prior to 1990 with records from 2006–2015, a 25% loss of bee species was observed (Zattara et al. 2021).

Most previous studies have compared bee diversity between natural and urban areas but have not considered situations where both areas share the same type of vegetation. Furthermore, this study focuses on a unique configuration, in which a highly urbanized area is located next to a protected natural area, the two sharing many of the same plants. These results have the potential to influence urban management strategies by highlighting the importance of urban environmental factors beyond vegetation type and the availability of floral resources. In order to develop effective conservation programs for bee communities and thus mitigate the potential adverse effects on these pollinators (Dalmazzo 2010), it is essential to compare sites with different levels of urbanization. Accordingly, the objectives of the study were to: 1) document the impact of urbanization on bee communities in terms of richness, overall abundance, life history, α and β diversity, when type vegetation is the same as in adjacent natural areas; 2) identify the most susceptible bees and those that benefit from urbanization; and 3) relate vegetation to bee communities.

The response of bees to urbanization depends on intrinsic species traits (Birdshire et al. 2020) as well as local habitat characteristics. We recorded an 84% reduction in bee species richness in the urban relative to the natural area. That is, 15 species in the urban area, 94 in the natural area. These data are consistent with those from other studies; 44 bee species have been recorded from urban metropolitan Guadalajara (Fierros-López 2004), while in the natural areas surrounding the city totals vary between 81 and 94 bee (Fierros-López 1998; Serrano et al. 2015; Razo-León 2024).

In addition, the abundance of bees decreased by 50%, and considering only native bees, a 70% decrease in the number of bees was observed. Short-tongued bee families, such as Andrenidae and Colletidae, are disappearing from urban areas, with Halictidae also showing a significant decline. These bees, often specialized in foraging on flowers with reduced corollas (Fortel et al. 2014). These bees are particularly vulnerable to any reduction in vegetation cover (Banaszak-Cibicka and Żmihorski 2012; Razo-León et al. 2018).

Megachilidae also show a marked decline in both richness and abundance in urban environments. This may be due to their nesting, which requires specific cavities and materials (O´Toole and Raw 1999; Michener 2000). It is likely that these resources are much reduced in urban areas.

In the natural area eusocial bees, mainly represented by A. mellifera, account for about 63% of the total abundance recorded. In contrast, in the urban area, A. mellifera still accounts for 77% of the individuals observed despite the overall decline in bee abundance. Similar results were observed by Guimarães and Gaglianone (2021), who reported that in urban areas, eusocial bees represented 82% of the observations. The decrease in richness and abundance of other bee species causes A. mellifera to become a more dominant species, as also observed by Cardoso and Gonçalves (2018). It seems that eusocial bees are more resilient to urbanization than other bee groups (Graf et al. 2022). This may be attributed to the slight differences in the proportions of eusocial bees between the two areas. However, non-eusocial bees exhibited a notable decline in richness, potentially since numerous species present in the natural area and absent in the urban area possess narrower niches, making it difficult for them to maintain populations in these environments.

The findings revealed that soil-nesting bees exhibited a pronounced sensitivity to urbanization, manifested in a pronounced reduction in their richness and proportion in the urban area relative to the natural area. This is consistent with other studies showing that these bees are underrepresented in urban area, since that they require bare soil in order to establish their nest (Geslin et al. 2016; Prendergast et al. 2022; Theodorou et al. 2022a). These include members of the families Andrenidae, Colletidae and some Halictidae, which may contribute to their decline or scarcity in urban environments (Cane 2006). Conversely, a reduction in the richness, but not in the proportion, of cavity-nesting bees is observed when comparing the two areas. The present study and other authors (Cane 2006; Theodorou et al. 2022b) show that cavity-nesting bees are more prevalent in urban areas, as they can exploit nesting sites associated with building. In contrast, no significant differences in richness were observed among the different areas for wood-nesting bees.

Kleptoparasitic bees, which lay eggs in the nests of other bees (Michener 2000), have shown a reduction in richness and abundance due to their vulnerability to habitat disturbance (Job and Olakkengill 2016). In the urban area, only one species, Mesocheira bicolor, was recorded, with a single individual parasitizing bees of the genus Centris. A decline in oligolectic bees was observed in the urban area. The absence of Cucurbitaceae explains the lack of Peponapis bees, while the scarcity of water and suitable nesting conditions, such as vertical clay walls, likely caused the near absence of Melitoma marginella despite the presence of Convolvulaceae in the urban area (Dalmazzo 2010).

Fifty bee species were recorded in the urban zone, of which nine showed a higher abundance in this environment. Some species within two genera stand out: Ceratina and Centris, which seem to show a preference for urban area; both are polylectic, visiting a wide variety of plants, allowing them to do well in urban areas (Razo-León et al. 2018). Ceratina nests in small hollow stems (Michener 2000), which can be found in urban parks due to the maintenance of plant pruning. Centris nest in pre-existing cavities, allowing them to use holes in buildings as nest sites. And Centris nitida, which is the most abundant native bee in the UA, has been recorded as a common species in other urban areas, where it can be found in gardens and parks (Pemberton and Liu 2008).

Hung et al. (2017) points out that urbanization exerts significant effects on bee beta diversity, which can serve as an index of the impact of anthropogenic disturbances on the communities of these pollinators. It has been reported that natural habitats harbor higher bee diversity and that most species show preference for forested habitats and few species prefer disturbed habitats.

The low similarity between urban and natural areas is mainly explained by loss of species (βSne), rather than their replacement. Pereira et al. (2021) found that differences in bee β diversity in urbanized sites over time were mainly explained by the loss of bee species with specific foraging and nesting habits.

Species turnover (βSim) was low, with only one exclusive bee species found in the urban area and 14 species found in both conditions. This can be explained by the presence of generalist and opportunistic species that can thrive in urbanized areas, along with introduced bee species such as A. mellifera (Collado et al. 2019).

A significant reduction in the richness (q0) and diversity (q1, q2) of plant species visited by bees was observed in the urban area. There was also a positive correlation between the richness of melittophile plants and the number of bee species and their abundance. Flowers as a food resource, in combination with abiotic factors, give rise to two different bee communities in natural and urban areas. Vegetation, including its abundance, herbaceous cover, floral trait diversity, and canopy cover, has been found to directly influence bee communities in terms of their abundance, composition, and diversity (Ayers and Rehan 2021).

Floral resources are among the most important and consistent predictors of bee diversity and pollinator population size (Gruver and CaraDonna 2021). As can be observed, most bees are present in the natural area, as most plant families are also associated with this area. Several plant families, including Commelinaceae, are exclusive to this area, while others, such as Convolvulaceae, which are shared, exhibit greater diversity and are visited by a greater number of bees in the natural area. In contrast, the urban area exhibits a notable association with the Cyperaceae. It has been documented that the implementation of an intensive management strategy for urban green areas, encompassing regular pruning and irrigation, has been observed to facilitate the proliferation of grass species (Aronson et al. 2017). Additionally, the Bignoniaceae, represented by the Tecoma stans, is tolerated in this area as an ornamental tree throughout the city.

Our study reveals that urbanization leads to a drastic reduction in the richness, abundance and diversity of bee communities. Therefore, it is critical to protect areas of native vegetation, as they act as reservoirs of pollinator species essential for reproduction and succession in forest ecosystems and may harbor bee species of great economic importance for crops (Ayers and Rehan 2021). For example, bees of the genus Peponapis are highly efficient pollinators of squash, while megachilids and halictids contribute to the production of crops such as various Asteraceae, Rosaceae, and legumes such as beans and chili. Likewise, bees of the family Colletidae can be important pollinators of chayote (Vergara et al. 2023).

It is essential to strengthen the conservation of the Bosque el Nixticuil-San Esteban-El Diente Protected Natural Area, despite the pressures to change its land use. In addition, it is essential to promote urban planning that considers the creation of large green areas with abundant floral richness and coverage, to mitigate the negative impacts of urbanization on bee communities (Guimarães and Gaglianone 2021).

Finally, it is recommended to create open areas in the study zone where herbaceous patches can develop, including different species of native plants, secondary and ornamental vegetation, but also favoring the presence of different plant families. to promote an increase in bee diversity and prevent the elimination herbaceous plants as part of the maintenance of the urban park, as well as to increase the density of trees. Another proposal to mitigate the effects of urbanization on bee communities could be the creation of bare ground areas with different substrates and degrees of slope hospitable to soil-nesting bees.

However, urban landscapes may be conducive to the conservation of some taxa, particularly solitary, cavity-nesting bees or those favored by anthropized environments, such as the family Halictidae (Razo-León et al. 2018; Ayers and Rehan 2021).

We thank the reviewers (Makaylee Crone and Christopher K. Starr) for critical comment on an earlier version, CONAHCYT and the University of Guadalajara for institutional support, the Municipality of Zapopan for research support, and the students Kenia Isabel Francisco Castro, Leonardo Daniel Meléndez Barajas and Linda Elizabeth Vargas Gutiérrez for their participation in the project, and Gaven Peggs for help with the language.