Big bats binge bad bugs: Variation in crop pest consumption by common bat species

https://doi.org/10.1016/j.agee.2021.107414Get rights and content

Highlights

  • Three bat species common to the Southeastern US consumed 23 species of crop pests.

  • Crop pest consumption was common: 61% of bats had consumed ≥ 1 pest species.

  • L. seminolus consumed 3X more economically important pests than other bats studied.

  • Likelihood of pest consumption increased with bat size and peaked in late summer.

  • Landscape composition and weather had limited influence on pest consumption.

Abstract

As generalist predators, insectivorous bats exploit fluctuations in prey distribution and abundance. A more nuanced understanding of the influence of bats on arthropod pests requires documentation of the pest species bats consume and of the conditions associated with variation in rates of pest consumption. Here, we used high-throughput metabarcoding of DNA extracted from bat feces to investigate diets of 180 bats representing three Vespertilionidae species common to the southeastern US, a region dominated by agriculture and pine plantations. We detected 23 species of agricultural pests in bat diets, including pests responsible for severe economic damage, such as Helicoverpa zea, Spodoptera frugiperda, Chloridea virescens and Chrysodeixis includens. Incidence of pest consumption was high: 61% of all bats had consumed at least one agricultural pest species, with each bat consuming an average of 1.7 pest species. The likelihood of consumption of pests to row crops and the average size of pests consumed varied by bat species, with a large foliage-roosting species (Lasiurus seminolus) consuming a greater variety of pest species and pest species larger in size than smaller crevice, cavity, and cave roosting bat species (Nycticeus humeralis, Myotis austroriparius). Likelihood of pest consumption also varied among sampling periods (season) and among bats of different sizes (as reflected by wing length and mass). Overall, likelihood of pest consumption was higher in the late summer season than during spring or early summer, and higher among larger bats than smaller bats. Bat characteristics and seasonality were generally more effective than geographic features and weather conditions in predicting pest consumption patterns. Strategies for enhancing pest consumption services by bats in agroecosystems should strive to maintain and enhance diverse bat populations on a landscape scale by protecting and augmenting roost structures appropriate for each species. Our finding of widespread pest consumption by bats contributes to mounting evidence worldwide of the important role bats play in agricultural systems and highlights the value of incorporating bat conservation into integrated pest management programs globally.

Introduction

Arthropod pests have widespread impacts on production of agricultural commodities ranging from food and fiber to timber and livestock (Steelman, 1976, Wang et al., 2008, Dukes et al., 2009, Tabashnik, 2010). Worldwide, arthropods can destroy 25–50% of agricultural crops, representing a threat to productivity and food stability (Pimentel et al., 1978, Pimentel and Zepp, 1991). Control costs can exceed $10 billion per year in direct pesticide costs in addition to the estimated $12 billion in societal and environmental damages (Pimentel, 2009).

Bats are capable of providing valuable pest suppression services, given their unique ecological role as volant and nocturnal consumers of arthropods (Williams-Guillén et al., 2008, Riccucci and Benedetto, 2018). The value of these services has been estimated as high as $53 billion per year in the United States (Maine and Boyles, 2015). This estimate is conservative because it doesn’t take into account indirect effects such as bat reduction of insects that transmit fungi to crops, or reduction in crop damage due to avoidance of crop fields where bats are present by tympanate moths capable of hearing bat echolocation calls (common agricultural pests) (Agee, 1969, Huang et al., 2003).

The impact of pest consumption by bats varies considerably over space and time due to differences in bat foraging capabilities and arthropod habitat use (Belwood and Fenton, 1976, Salinas-Ramos et al., 2015, Braun de Torrez et al., 2019). Previous studies have demonstrated a close spatiotemporal match between abundance of emergent arthropod pests and both bat activity and diet (Lee and McCracken, 2005, Charbonnier et al., 2014). Additionally, experimental studies have demonstrated an increase in crop damage following the exclusion of bats from agricultural systems (Maine and Boyles, 2015). Landscape-scale, multi-taxon studies that evaluate pest consumption across a broad range of land uses are needed to develop effective recommendations for enhancing integrated pest management strategies involving bats (Williams-Guillén et al., 2016).

Due to their high mobility, insectivorous bats can adjust their foraging behavior to maximize encounters with suitable prey (Cryan et al., 2012, McCracken et al., 2012). Characteristics of individual bats, such as flight capabilities, echolocation attributes, metabolic/nutritional needs, and bite strength determine which arthropods will be encountered, pursued, captured and consumed by a particular bat (Aldridge and Rautenbach, 1987, Sedlock et al., 2014). These characteristics vary not only across bat species but also within, due to factors such as age and reproductive condition (Norberg and Rayner, 1987, Barclay, 1989, Hughes et al., 1995, Denzinger and Schnitzler, 2013). Individuals with morphological attributes that confer greater maneuverability can utilize areas with more obstructions and pursue more evasive prey than those with less maneuverability (Mendes et al., 2017, Magalhães de Oliveira et al., 2020). Individuals with stronger jaw morphology can consume harder prey more efficiently than those with gracile jaw morphology (Freeman, 1981), which may influence pest consumption given that many of the most economically damaging agricultural pests are soft bodied lepidopterans (Suckling et al., 2017). Finally, bats with larger gape width (associated with larger body size) can consume larger prey more efficiently, which may influence pest consumption given that some of the most economically important pests (Helicoverpa zea and Spodoptera exigua) are large (Tomassini et al., 2014, Montezano et al., 2018; Invasive Species Compendium, 2020).

Geographic characteristics at various spatial scales may influence which arthropod pests are consumed by bats due to the impact of landscape features on arthropod community composition and bat foraging activity (Williams-Guillén et al., 2016, Russo et al., 2018, Bàrberi et al., 2010). For example, the activity of bats within agricultural fields is known to be influenced by the surrounding non-crop matrix, so dominant land cover in the area may be relevant to bat consumption of pests to agricultural crops (Kelly et al., 2016, Olimpi and Philpott, 2018). Since many economically important insect pests of row crops use grass species as alternative hosts when crops are not available (Appendix A), acreage of grasses in agroecosystems may influence pest persistence, which may in turn influence the pest consumption services bats provide. Some evidence suggests that pest consumption by bats may decrease as the degree of local agricultural intensification increases (Kalda et al., 2015, Treitler et al., 2016). Therefore, the proportion of a given landscape devoted to heavily managed crops such as pecan, citrus, corn and cotton may be less influential to bat pest consumption patterns than the proportion of the landscape devoted to less intensively managed crops typically grown across smaller acreages such as berries and forage. The latter may be more influential to pest abundance than the widespread, heavily managed crops given their suitability as host species for a variety of arthropod pest species, the lighter pesticide load used to manage these crops, and the increased habitat heterogeneity typical of landscapes where they are grown (Gianessi and Reigner, 2006, Heim et al., 2015, Olimpi and Philpott, 2018).

Temporally variable characteristics may also dictate the prevalence of arthropod pest consumption by bats (Lee and McCracken, 2005). At short time scales, time of night can influence which arthropod species are active at a given site (Beck, 1980). Similarly, weather factors that vary across short time scales, such as temperature and precipitation, can induce nightly fluctuations in arthropod composition at a given site by triggering hatches or migrations (Honek, 1997, Intachat et al., 2001). Across longer time periods such as seasons, arthropod community composition varies even after accounting for weather, due to arthropod migration patterns and a dietary reliance of arthropods on plants that respond to factors such as day length to determine budding time (Lee and McCracken, 2005). Finally, regional climate influences which arthropod species can persist in a location (Klok et al., 2004).

We conducted a multi-taxon investigation of arthropod consumption by bats across a vast spatial area encompassing a broad range of land uses to better understand factors that influence bat predation on agricultural pests. We used DNA metabarcoding to characterize the diets of three insectivorous bat species common to the southeastern US: Seminole bats (Lasiurus seminolus), evening bats (Nycticeius humeralis) and southeastern myotis (Myotis austroriparius). Because these species are common across one quarter of the US, pest consumption by these species could indicate widespread and substantial impacts on pest populations (Menzel et al., 2000). After documenting which agricultural pests are consumed by these bats, our first objective was to compare pest consumption among the three bat species. We hypothesized that pest consumption across the three bat species would vary predictably according to variation in insect size and hardness, due to differences in bat species size and jaw morphology. We predicted that the largest species, L. seminolus, would consume Lepidopteran pests at higher rates due to the adaptation of their gracile jaw morphology to soft-bodied prey, and that they would consume more of the relatively large pests due to their large gape width (Laerm et al., 1999, Barlow et al., 1997, Freeman, 1981). We predicted N. humeralis would consume the hardest pest species due to their robust jaw morphology (Freeman, 1981). Our second objective was to identify factors other than bat species which were associated with patterns of pest consumption by bats. We hypothesized that pest consumption would vary predictably according to variation in traits of individual bats, environmental conditions, and geographic features. We predicted that bat characteristics and geographic characteristics would be more important than temporally variable characteristics in the rate and diversity of pests consumed, given known relationships between bat and prey characteristics, and the demonstrated influence of landscape features on bat foraging activity (Anthony and Kunz, 1977, Covell, 1984, Honek, 1997, Lee and McCracken, 2005). Identifying factors other than bat species that are associated with pest consumption would enable the prediction of scenarios under which consumption of pests by bats is more likely. An understanding of the factors influencing pest consumption by bats would enable development of more effective strategies to enhance bat pest consumption services in agroecosystems.

Section snippets

Site selection

We used a stratified semi-random selection approach to locate 36 study sites spread across three study regions in the southeastern US, a region with a high prevalence of agriculture and timber production that is experiencing high rates of land use change (Napton et al., 2010). These three study regions spanned southern Alabama, southern Georgia, and north-central Florida, sampled as part of a larger study (Gottlieb et al., 2017, Ober et al., 2020) (Fig. 1). We placed a grid with 3 km x 3 km

Results

We analyzed fecal samples from 180 individual bats of three species across the southeastern US, Lasiurus seminolus [n = 40], Nycticeius humeralis [n = 56], and Myotis austroriparius [n = 84]. We documented that these bats consumed 23 agricultural pest species across four insect orders (Lepidoptera [n = 11], Hemiptera [n = 7], Coleoptera [n = 3], and Diptera [n = 2]), of which 12 had never previously been documented in bat diets and 16 have high economic impact. These included four notable pest

Discussion

We found that the incidence of pest consumption by bats was high, with the majority of individual bats consuming at least one agricultural pest species. We documented that three widespread, common bat species consumed three of the most important crop pests in the US: Helicoverpa zea (Lepidoptera: Noctuidae) (Corn earworm), Spodoptera frugiperda (Lepidoptera: Noctuidae) (Fall armyworm), and Chloridea virescens (Lepidoptera: Noctuidae) (Tobacco budworm). These pests feed on a variety of crops

Conclusions

Our results indicate that common species of bats in the Southeastern US regularly consume a variety of agricultural pests including 12 that have never before been documented in bat diets and 16 that have a substantial economic impact (Appendix A). We provide strong evidence that bats play an important ecological role in agroecosystems throughout the southeastern US. We observed pest consumption in all three species studied but observed the highest rates and diversity of pest consumption in L.

Declaration of Competing Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

The United States Department of Agriculture (USDA) National Institute of Food and Agriculture (NIFA) provided funding in support of this research. Funding in support of Elizabeth Braun de Torrez was provided by the Florida Fish and Wildlife Conservation Commission, and additional equipment and supplies were provided by Georgia Department of Natural Resources. We thank land owners and land managers for providing access to bat capture sites on private and public property; Haley Price, Erika

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