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.