Figure 4 . The relationships between bat species diversity (number of species/groups per detector per night) and distance to nearest forest (in meters) with high relative pest abundance (RPA; dark grey) and low RPA (light grey). Lines indicated predicted mean; shaded areas represent 95% confidence intervals.
Discussion
We studied bat activity and bat species diversity in relation to distance from forested riparian corridors in a landscape dominated by row-crop agriculture and assessed how both activity and diversity might be affected by crop pest species abundance. Our results show that while bat activity and diversity decline with increasing distance from riparian corridors, increasing crop pest abundance does not increase activity or diversity. We also show that bat activity in agricultural landscapes is nuanced and that bats may require forest corridors in relatively close proximity if they are to provide valuable ecosystem services to agriculture.
Overall, bat activity declined with increasing distance from riparian corridors (Fig. 3A). This result supports our hypothesis and corroborated findings from previous studies, indicating bat activity to be higher in agricultural landscapes when forested corridors are present (Boughey et al., 2011; Davidai et al., 2015; Kalda et al., 2015) and when habitat heterogeneity is higher in general (Frey-Ehrenbold et al., 2013; Monck-Whipp et al., 2018; Russo et al., 2018). On organic farms, greater bat activity was attributed to higher landscape heterogeneity and improved water quality when compared to conventional farms (Wickramasinghe et al., 2003). Because bats provide considerable ecosystem services to agriculture (Boyles et al., 2011), in part by suppressing pest species, our results stress the importance of increasing habitat heterogeneity in agricultural landscape to ensure producers maintain or increase the pest control benefit provided by bats.
We found that a change in pest abundance altered the distribution of bats across the landscape (Fig. 3A). Our results indicate that when pest abundance is low, bats aggregate at the forest edge, resulting in much higher activity close to forests. However, when pest abundance is high, bats are more equally distributed across the landscape, resulting in lower activity at the forest edge and a smaller decline in activity further over uninterrupted agriculture. Importantly, overall bat activity was still lower farther from the forest edge, indicating that although bats may exploit increased foraging opportunities when pest abundance is high, their contribution to crop pest control still decreases with increasing distance from forest cover. This corroborates previous studies which have found that, crop pests make up a significant proportion of bats’ diets in agricultural areas (Hughes et al., 2021; Kolkert et al., 2020a). Indeed, bats have been shown to track the changes in pest species abundance, exploiting the inflated prey availability (McCracken et al., 2012).
Unfortunately, we only have data on the temporal variation in pest abundance and lack information on any spatial or species patterns. If pest species abundance accumulated closer to forest edges, for example, or was higher further away from roads and into crop fields, our bat detectors would not necessarily detect the increased activity if bats did exploit the increase in pest abundance. However, there is evidence that pest abundance does not correlate with landscape complexity, suggesting that pest abundance might be more homogenous across the landscape than bat activity (Chaplin-Kramer et al., 2011). Furthermore, bats prefer to forage along linear features, such as hedges or grassy waysides (Lentini et al., 2012), suggesting that the majority of the bat activity in agricultural landscapes would be along linear features, and not over uninterrupted agricultural fields (Boughey et al., 2011).
We found that low-frequency bats, which are larger in size, were more active at greater distances into uninterrupted agriculture compared to smaller, high-frequency bats, supporting our hypothesis (Fig. 3B). Larger bat species typically have higher wing loading and higher wing aspect ratios, allowing them to travel further and faster over open space such as agricultural fields (Kalda et al., 2015). Foraging bats generally stay close to vegetated corridors, possibly to avoid predation (Lima and O’Keefe, 2013), but the faster flight speeds of larger bats could lessen the potential risks of venturing away from corridors and out into open fields. Our results corroborate previous findings that smaller bats are more sensitive to habitat fragmentation (Frey-Ehrenbold et al., 2013; Murray and Kurta, 2004), and are less likely to forage in open habitats (Ford et al., 2005; Henderson and Broders, 2008).
We also predicted that larger bats would benefit more from high pest abundance than smaller bat species, as larger bats prefer larger prey, and agricultural pest species are often large in size (Hughes et al., 2021). While bat activity of low-frequency bats declined with increasing pest abundance, activity of mid- and low-frequency bats was generally very low and unaffected by pest abundance (Fig. 3C). This corroborates findings that smaller bats are generally absent from large-scale agricultural landscapes and rarely forage on agricultural pest species (Ford et al., 2005; Heim et al., 2016).
Lastly, we found that bat species diversity declined with increasing distance into uninterrupted row crop agriculture (Fig. 4). This supports our hypothesis and corroborates previous studies that show that habitat heterogeneity in agricultural landscapes correlates with bat species diversity (Kolkert et al., 2020b; Monck-Whipp et al., 2018).
We also predicted that the decline in bat diversity further from riparian corridors would be buffered by pest abundance such that, with high pest abundance, bat diversity would be higher further away from riparian corridors. Lentini et al. (2012) found that bat species diversity increases with increased dry pest species biomass, and bats have been shown to seasonally expand and retract their range over cultivated landscapes in response to fluctuations in prey availability (Smith et al., 2021). However, our analysis found no effect of pest abundance on bat diversity (Fig. 4). Thus, the observed higher bat activity further from riparian corridors when pest abundance is high (Fig. 3A,B) is likely due to greater activity by a few larger species. Though bat dietary niches overlap to some degree (Cravens et al., 2018), species-specific prey preferences mean that increased bat species diversity could amplify their pest regulation ecosystem services (Maslo et al., 2022).
Conclusion
This study showed that both bat activity and species diversity in agricultural landscapes decrease with increasing distance from forest corridors. Habitat heterogeneity was most important for bats, regardless of crop pest abundance – an important food source for bats, as bat activity still declined from the forest edge even when pest abundance was high. Increasing habitat heterogeneity and natural features is important to promote bat activity in agricultural landscapes (Davidai et al., 2015; Kalda et al., 2015), and has also been shown to strongly increase biodiversity, including pollinators and birds (Cerezo et al., 2011; Eeraerts et al., 2019). As agricultural systems are increasingly expected to meet the growing demand for food production globally, it becomes pertinent to employ strategies that maximize output while limiting environmental damage. Bats benefit agricultural systems through intensive insect consumption, thereby decreasing the damage to crops caused by pests, while minimizing the need for pesticides (Kunz et al., 2011). We argue that agricultural landscapes lacking habitat heterogeneity do not currently optimally benefit from natural pest control by bats due to the lack of foraging and roosting habitat that would facilitate bat presence, and emphasize the importance of increasing habitat heterogeneity for natural pest suppression strategies. Additional work is needed to further explore the relationship between bats and landscape features that promote foraging activity, and methods of increasing bat occupancy and activity within agricultural landscapes should be further investigated.