Abstract
As demand for food increases, agricultural production is poised to increase dramatically. Pesticides are commonly used to maintain high crop yield, though they have several drawbacks, including reduced efficacy over time and harmful effects to human and ecosystem health. Bats are highly effective predators of crop pests and have great potential to reduce crop damage resulting from insects. However, few studies have investigated how pest control by bats might change over large expanses of continuous row crop agriculture, which is common in the Midwest. Agricultural landscapes offer few roosting opportunities and could be difficult for bats to traverse, which might affect the degree of ecosystem services provided by bats. We hypothesized that with increasing distance into uninterrupted row crop agriculture 1) bat activity would decrease and 2) bat species richness would decrease, but that these effects would be buffered when insect pest abundance is high. We deployed 50 acoustic bat detectors over 10 transects in east-central Illinois from July to September 2021. In each transect, we placed detectors on crop field edges at increasing distance from a large riparian corridor assumed to be frequented by bats. Bat activity was high across the landscape but declined by 56% from the forest edge to 4000m into row crop agriculture, while bat diversity decreased by 34%. Pest abundance seemed to decrease overall bat activity but had no effect on bat diversity. These results indicate that bats, although able to have a large effect on crop pest reduction, might not be as efficient in suppressing crop pests in vast uninterrupted agricultural landscapes which offer scant roost availability. Our work will inform recommendations to landowners and private lands managers on ways to increase bat access to roosts and forest cover near agricultural areas, thereby enhancing the potential for bats to provide pest control services.
Keywords : Ecosystem services, Agricultural intensification, Pest suppression, Diversity, Forest management
Introduction
As the human population grows and the demand for food increases, there will be a greater need for more efficient agricultural land use (Godfray et al., 2010). Tilman et al. (2001) predicted that by 2050 one billion hectares of land would be converted to agriculture and anticipated a 2.4–2.7-fold increase in water eutrophication caused by the concomitant increase in fertilizer and pesticide use. Despite intensification via industrial monocropping, agricultural yields have not kept up with demand (Ray et al., 2013). This is in part due to an increase in crop pest abundance as a result of large-scale monocropping, which contributes to so-called yield gaps (Chaplin-Kramer et al., 2011). Harnessing the potential of natural predators to suppress crop pest populations is an efficient and cost-effective strategy to increase yields. Such a process of ecological intensification – increasing agricultural yield without also increasing anthropogenic inputs – would reduce our reliance on pesticides, which are less effective because many pests have developed resistance over time (Bommarco et al., 2013). Bats have been proposed as an important pest control species in agricultural landscapes, potentially worth 3 billion USD to the US agricultural industry alone (Boyles et al., 2011). In this study, we investigate how bat activity patterns change over agricultural landscapes in relation to distance from forested riparian corridors to better understand the spatial scope of crop pest control by bats.
Agricultural pests have pervasive impacts on various forms of agricultural production from animals to crops. Globally, an estimated 30% of crop loss is attributed to pests in both soybeans and corn, the two main crops produced in the Midwest (Oerke, 2005). Protecting crops against animal pests remains difficult and costly, and relies heavily on synthetical chemicals (Oerke, 2005). Globally, the associated costs with controlling for these pests can surpass $10 billion yearly, with an additional $12 billion in external damages (Pimentel, 2009). These estimated costs could be inflated due to forecasted increases in agricultural pest abundance due to climate change (Diffenbaugh et al., 2008). Therefore, efforts to enhance natural pest control are imperative. Ecological intensification of agricultural landscapes reestablishes the ecosystem services derived from natural systems, thereby reducing costs of pest control while increasing crop yield (Bommarco et al., 2013). Using these biodiversity-based methods has been proven to sustainably increase crop yields (Maine and Boyles, 2015; Maslo et al., 2022; Tschumi et al., 2016).
All bats in the midwestern region of the USA are insectivores (Whitaker and Hamilton, 1998). These bats are voracious arthropod predators that can consume up to their body weight in arthropods over the course of a single night (Kunz et al., 1995). Bats may even exert a stronger top-down effect on insect abundance than do birds, as has been found in forest systems (Kalka et al., 2008). It is widely recognized that bats have significant impacts on crop pest species and therefore provide valuable ecosystem services (Boyles et al., 2011; Maslo et al., 2022; Whitaker, 1995). The diet of common species such as the big brown bat (Eptesicus fuscus ) includes 160 known agricultural pest or disease vectors, including Helicoverpa zea , Spodoptera frugiperda , and Chloridea virescens (Hughes et al., 2021; Maslo et al., 2022). The effects of bats on pest control are multi-layered because by foraging on the adult stages of pests like moths, bats indirectly suppress egg production (McCracken et al., 2012). One study found that bats not only suppressed pest larval densities in corn, they furthermore contributed to the suppression of pest-associated mycotoxins and fungal growth (Maine and Boyles, 2015). These agricultural ecosystem services in the United States alone have been estimated to be worth between 3.7 and 53 billion dollars annually (Boyles et al, 2011). Ironically, bats are threatened by the very industry they help: agricultural intensification is considered a major contributor to pervasive bat declines in Europe and North America (Frick et al., 2020; Wickramasinghe et al., 2003). Bats are further threatened by rampant wind energy development (Davy et al., 2021; Friedenberg and Frick, 2021) and, in North America, white-nose syndrome (Frick et al., 2020; Hoyt et al., 2021). Urgent conservation action is needed to promote these species in agricultural landscapes if they are to continue their significant contribution to pest control.
Bats are not homogeneously distributed across the landscape. For example, bat activity increases with increasing landscape heterogeneity (Burgar et al., 2017; Chaplin-Kramer et al., 2011; Monck-Whipp et al., 2018). Woodland interfaces are important predictors of bat activity (Fill et al., 2022), and one study found that bat activity is 5 times higher in landscapes containing a double row of trees compared to standalone trees (Kalda et al., 2015). Bat species richness also varies with landscape structure. Due to species-specific characteristics, including wing aspect ratio and body size, some species prefer foraging in cluttered habitat (Aldridge and Rautenbach, 1987). Although bats are generalists, different species have specific diet preferences, and larger bats tend to consume larger prey such as agricultural pests (Hughes et al., 2021; Kunz et al., 2011). Because of their structural complexity, woodlands and wooded corridors offer habitat to bats with differing foraging behaviors and, therefore, often have higher bat diversity than uninterrupted row crop agricultural landscapes (Kalda et al., 2015). Indeed, bats prefer to forage along linear features in agricultural landscapes, such as natural vegetation remnants and farmland edges (Lentini et al., 2012). The sometimes surprisingly long distances between potential roost locations (i.e., large trees in forest patches) in the vast agricultural landscapes often found in the Midwest likely presents a formidable challenge to bats foraging over agricultural fields. Higher predation risk from raptors and owls in open landscapes could also decrease the likelihood of bats venturing out into agriculture (Lima and O’Keefe, 2013; Mikula et al., 2016; Murray and Kurta, 2004). To better understand how bats contribute to agricultural pest control, and how we can improve the efficacy, we require more nuanced information on bat activity in relation to landscape characteristics (Boyles et al., 2013).
We studied bat activity and diversity in central Illinois, USA in relation to expansive, uninterrupted agriculture. We hypothesized that both bat activity and bat diversity would decline with increasing distance from forested corridors, but that this effect would be buffered by insect pest abundance. With respect to overall bat activity, we hypothesized that activity would decline with increasing distance from large forested riparian corridors, which we assume to be favorable roosting and foraging areas. However, we suspected this effect would be buffered by pest insect species abundance, such that bats would be more active further away from riparian corridors when pest abundance is high than when pest abundance is low. Furthermore, we hypothesized that there would be variable responses from bat species, such that larger bats would be more active and persistent in areas further into uninterrupted agriculture, while smaller species would be restricted to areas around the riparian corridors, and that larger bat species would increase activity rates in response to high pest abundance more so than smaller bat species. With respect to bat diversity, we hypothesized that bat diversity would decline with increasing distance from riparian corridors, but that the magnitude of this effect would decrease with increasing pest abundance.