Bombus species richness, abundance, and overall diversity were highest in agricultural landscapes characterized by low temperatures and high relative humidity during the growing season, and lowest in urban areas with high temperatures and low relative humidity. Ongoing and future urbanization and climate change may therefore lead to reduced Bombus diversity in Utah. Although some historically uncommon species, such as B. pensylvanicus, may thrive under future landscape and climate scenarios, others (e.g., B. sylvicola, B. californicus, and B. occidentalis) are at increased risk of extirpation due to loss of suitable habitat.
Our finding that Bombus diversity was highest in agricultural landscapes differs from other studies that suggest diversity is negatively impacted by high proportions of agriculture, particularly monocultures, due to a lack of diverse landscapes, reduced availability of floral resources, increased use of agrochemicals, and frequent soil disturbances (e.g., tilling, seeding, and harvest practices) restricting nesting locations (Vanbergen et al. 2013; Pfeiffer et al. 2019; Grocock and Evenden 2020). This may be due to our surveyed corn and alfalfa fields being relatively small (mean of 22 acres) and in close proximity to other crop types (e.g., corn, alfalfa, wheat, and barley) in comparison to other regions of the U.S. where agricultural fields are more expansive (Plourde et al. 2013). This inconsistency may also be driven by differences in agricultural practices, management history, and local environment (Kohler et al. 2020). Additionally, we suspect that increased floral richness within hedge rows surrounding agricultural fields may draw foraging bees away from their nests as these flowering plants provide important nutrients for developing larvae (Tasei and Aupinel 2008; Potts et al. 2009; Roulston and Goodell 2011; Wood et al. 2015; Pfeiffer et al. 2019). This may explain why Bombus are captured in relatively high numbers within crop fields (e.g., corn) that do not necessarily provide ideal floral resources. Since Bombus are fairly vagile foragers (Rao and Strange 2012; Geib et al. 2015) and are not considered to be area sensitive, they can use these small patches of habitat (as little as 2% of semi-natural habitat within agricultural landscapes) to exploit floral and nesting resources in the surrounding area (Westphal et al. 2003; Pfeiffer et al. 2019). However, not all species behave similarly, which may influence the degree to which Bombus travel for floral and nesting resources (Geib et al. 2015).
Despite Bombus diversity being highest in agricultural landscapes, some species were more abundant in agricultural areas with greater urban development (i.e., crop fields in close proximity to suburban housing developments, buildings, roadways, and highways). Urban areas often experience warmer temperatures relative to surrounding rural areas due to the increased prevalence of impervious surfaces (Baldock 2020). Although other studies, including our own, found that Bombus diversity decreased with urbanization (Ahrné et al. 2009), urban habitats with higher temperatures appear to favor some Bombus species (B. appositus, B. fervidus, B. griseocollis, B. huntii, and B. pensylvanicus). This indicates that Bombus species are differently affected by urban agricultural areas (Ahrné et al. 2009; Baldock 2020). The mechanisms driving this response remain unclear, but are likely due to a multitude of factors, such as increased floral resource availability and nesting opportunities within the surrounding environment, and various life history traits (e.g., emergence periods, colony size, and thermal tolerances) (Goulson and Darvill 2004; Goulson et al. 2005; Williams 2005; Benton 2006; Fitzpatrick et al. 2007; Bennett and Lovell 2019; Burdine and McCluney 2019). For example, B. griseocollis is historically known to inhabit open farmlands and fields, urban parks and gardens, and wetlands (Williams et al. 2014). Additionally, they have a relatively small colony size (fewer than 50 workers), which may be advantageous within urban agricultural sites as this reduces their risk of overheating from crowding and insufficient nest ventilation (Weidenmüller et al. 2002). Meanwhile, B. pensylvanicus, a species that normally occurs in the southwestern U.S. (Koch et al. 2012; Williams et al. 2014) but is declining in population size (Cameron et al. 2011; Strange and Tripodi 2019), may be expanding its geographic range to include urban agricultural areas of northern Utah characterized by high temperatures.
Ongoing and future climate change may change Bombus species’ phenology and assemblage composition, which can impact pollination services and ecosystem function. Our collection of Bombus from mid-May to mid-September identified phenological overlap within the Bombus community. This overlap may aid in fostering future resiliency of pollination services as well as ecosystem function. If a particular species is lost due to loss of habitat, other ecologically similar species present within the environment might be available to fill this gap in pollination services (functional redundancy). Meanwhile, species overlap was lower earlier in the season (late April to mid-May), most likely due to differences in time of emergence from winter diapause. Climate warming has been shown to lead to shifts in Bombus emergence periods with bees having earlier springtime activity in the northeastern U.S. (Bartomeus et al. 2011, Pyke et al. 2016). This shift may benefit pollination services earlier in the season when species diversity is low by increasing phenological overlap between pollinator species. However, climate-induced phenological change coupled with shifts in bloom phenology and agricultural cultivation dates can also negatively impact plant-pollinator synchrony, leading to increased competition for floral resources. Adaptive foraging (the ability for pollinators to utilize alternative, less-preferred flowers) may counteract the effects of phenological mismatching between plants and pollinators by preventing the pollinator population from collapsing for long enough to allow for re-synchronization (Valdovinos et al. 2013; Revilla et al. 2015).
In summary, we identified habitat and climatic variables that drive Bombus species abundance and diversity in agroecosystems. Further, this study emphasizes that management strategies should consider the effect of co-occurring factors as opposed to single factors in order to effectively foster future resiliency of Bombus populations in the face of anthropogenic disturbances. Novel ecosystems will continue to emerge as urbanization, agricultural intensification, and climate change continue. These novel ecosystems may be better at withstanding anthropogenic environmental changes, but also have the potential to be ecologically homogenized (Hobbs et al. 2006; Groffman et al. 2014). If the same drivers are applied everywhere such that spatial, functional, and taxonomic similarity increases, beta diversity can decrease leading to homogenization. Therefore, this response will be largely dependent on management practices, geographic location, and changes in species diversity and distribution. Functional groups and species interactions will change as a result; however, key ecological function will not necessarily be lost (i.e., functional redundancy). Additionally, novel ecosystems may alter species interactions (e.g., mutualism, competition), or lead to the loss of regionally unique species further contributing to homogenized ecosystems (Hobbs et al. 2006). Continually monitoring Bombus populations will help document these shifts in assemblages and potential consequential impacts to ecosystem services. Overall, this is a crucial step towards understanding the co-occurring effects of land-use change and climate on pollinator populations.