Strong benefits of hedgerows to bats in three European winegrowing regions

Abstract

Bats provide important ecosystem services as natural predators of, for example, lepidopteran pests. Thus, it is crucial to identify ways to enhance bat populations in agricultural landscapes. It has been shown that high landscape heterogeneity can benefit bat communities in arable fields. However, to date, the relationship between bats and the surrounding landscape within a viticultural matrix has received little attention, despite moths being major pests in viticulture. Here, we investigated how bats respond to different landscape elements in three European regions: Rhineland‐Palatinate (Germany), Burgenland (Austria), and Andalusia (Spain). We recorded bat activity using passive acoustic monitoring for four nights in 94 vineyards in total. Additionally, in Germany, we recorded bat activity along transects from hedgerows up to 120 m into the vineyards to describe the change in activity with hedgerow distance. We found that bat activity decreased with distance from the hedgerow, and the strength of the response was guild‐specific. Bat species adapted to foraging in the open space decreased their activity by half at a distance of 120 m from the hedgerow into the center of the vineyard, while bats adapted to foraging along vegetation (edge‐space bats) and those adapted to feeding within and close to vegetation (narrow‐space bats) decreased their mean flight activity by more than 80% at the same distance. Moreover, the presence of hedgerows between vineyards was positively related to a higher bat activity and feeding rate in all three countries, although this effect varied by functional guild and country. For edge‐space foraging bats, hedgerows had a positive impact in all three countries, while open‐space bats only showed a significant response in Spain. Hedgerows had consistent positive effects on bat activity in vineyards across the three study regions. Our study suggests that hedgerows should be conserved and restored as key elements to support a higher bat activity. This would also benefit other important groups of animals such as bees and birds along with the ecosystem services they provide.

INTRODUCTION

On a global scale, the expansion and intensification of agriculture is one of the main drivers of biodiversity decline (Maxwell et al., 2016). In Europe, modern arable management is associated with landscape simplification, which has contributed to a decline in biodiversity (Stoate et al., 2001). Remains of natural vegetation in agricultural landscapes provide important resources such as food, shelter, and connectivity to other habitats for a range of species including arthropods, birds, and small mammals (Graham et al., 2018), many of which deliver ecosystem services such as natural pest control (Paredes et al., 2019). In vineyard landscapes, Rusch et al. (2017) found that the role of birds in biological control increased with a higher proportion of seminatural habitats around vineyards with partial grass cover. Thus, the removal of natural and seminatural habitats can be related to a decrease in the provision of ecosystem services, such as biological control of crop pests by natural enemies (Dainese et al., 2019). Among the species that provide ecosystem services, insectivorous bats play an important role as bioindicators (Jones et al., 2009) and suppressors of pests in agroecosystems (Russo et al., 2018). Recent studies highlighted the potential role of bats as natural enemies of Lobesia botrana, one of the major pests in European vineyards (Baroja et al., 2021; Charbonnier et al., 2021; Tortosa et al., 2023).

Despite their importance, bat populations in Europe have declined since the mid-20th century (Dietz et al., 2009). It is therefore crucial to understand the factors that influence bats in agricultural landscapes. High landscape heterogeneity may benefit bat communities by increasing the length of field boundaries, and by reducing the distances between foraging and roosting sites (Monck-Whipp et al., 2018). In heterogeneous landscapes, bats have smaller home ranges because they can access diverse foraging habitats while reducing distance costs from roosts (Laforge et al., 2021). Hedgerows contribute to structural heterogeneity of the landscape (Toffoli, 2016), and provide orientation and protection during commuting, as well as forage and roosting sites (Boughey et al., 2011; Verboom & Huitema, 1997). The benefit of vegetation structures such as hedgerows, forest edges, and woodland patches in agricultural landscapes for bats has been widely documented. However, most studies have focused on arable lands and grasslands (Boughey et al., 2011; Froidevaux, Boughey, et al., 2019; Heim et al., 2015, 2018; Verboom & Huitema, 1997), and only a few have focused on vineyards (Froidevaux et al., 2017; Kelly et al., 2016; Rodríguez-San Pedro et al., 2018). Therefore, there is still a gap in research on how bats are affected by these vegetation structures in vineyard landscapes (Rodríguez-San Pedro et al., 2018). Perennial crops, such as vineyards, are generally less disturbed and have higher resource continuity over time in comparison with annual crops (Bruggisser et al., 2010). In temperate European vineyards, biodiversity can be high (Costello & Daane, 1998; Isaia et al., 2006), and can host high abundances of lepidopterans (Hahn et al., 2017), an important prey of bats. This may suggest that bats may use vineyards for foraging. Thus, it is important to understand the elements that benefit bats in a viticultural matrix.

The conservation and management of habitats that enhance bats and biodiversity in general in farmland are implemented in Europe through Agri-Environmental Schemes (Froidevaux, Boughey, et al., 2019). These schemes are part of the Common Agricultural Policy (CAP) of the European Union, where farmers may receive financial support for voluntary commitments to adopt environmentally friendly agricultural measures through “eco-schemes”. To receive CAP support, farmers have to comply with obligations under “conditionality”, such as the maintenance and protection of nonproductive areas like hedgerows. However, this requirement is specified only for arable crops, while permanent crops such as vineyards have no comparable requirement (European Commission, 2023).

Here, we investigate how hedgerows in vineyard landscapes can contribute to enhancing bat activity and foraging. We study the response of bat activity to distance and presence of hedgerows and other elements in vineyard landscapes. We hypothesize that bat activity response varies according to their foraging habitat preferences (functional guilds). We predict that edge- and narrow-space foraging bats respond positively to the presence of hedgerows. By contrast, we predict that open-space foraging bats respond to the presence of woody elements at a larger landscape scale, for example, in proximity to forests than in predominantly open landscapes. We also hypothesize that a higher proportion of vineyards, that is, a more homogenous surrounding land use, has a negative effect on bat activity. Finally, we hypothesize increased activity near the hedgerows compared to the center of the vineyard, and that the strength of this response will be guild-specific: edge- and narrow-space groups should have a greater decrease in activity at greater distances from the hedgerow than open-space bats.

MATERIALS AND METHODS

Study area and sampling design

The study was conducted in 94 vineyards located in Austria, Germany, and Spain (Figure 1A). In total, 42 of the vineyards had an adjacent hedgerow, which consisted of a linear vegetation structure composed of woody elements, such as a line of trees, small groups of shrubs, or a mixture of both. In Austria, the recording was done in vineyards located along the foot of the Leitha mountains on the western shore of Lake Neusiedl in the federal state of Burgenland (Figure 1B), where 22% of the vineyard area was managed organically, with ground cover vegetation, and the most commonly used products were sulfur-based fungicides. The study area is characterized by a mean annual rainfall of 636 mm and average temperature of 11.3°C. In the study year, March and June were particularly dry (Zentralanstalt für Meteorologie und Geodynamik—ZAMG, 2021). Bat activity was monitored in 32 vineyards, of which 16 were located directly adjacent to a hedgerow and 16 had no woody vegetation adjacent to the edge.

In Germany, the study area was located in the winegrowing region of the Palatinate in the Upper Rhine Plain within a radius of 8 km around the city of Landau (Figure 1C); in this area, around 6% of the vineyards were under organic management, and the most frequently applied products were sulfur-based fungicides. The mean temperature of the region is 9.7°C, and the mean annual rainfall is 779 mm. In the sampling year, April was particularly cold, July experienced heavy rainfall, and summer precipitation was about 41% above average (Klimawandel-RLP, 2021). We monitored 32 vineyards, of which 16 were directly adjacent to a vegetation structure such as a hedgerow, tree line or a small group of trees and shrubs (hereafter: hedgerow), and 16 were located at a distance of more than 200 m from the nearest hedgerow or forest patch.

The Spanish vineyards were located in the region of Andalusia, Cordoba, in the Montilla-Moriles area, where the landscape is dominated by vineyards and olive groves (Figure 1D). In this region, about 2% of the vineyards were under organic management (MAPA, 2022). The region is characterized by a Mediterranean climate with a mean temperature of 17.9°C, and a mean rainfall of 518 mm. In the study year, March and May were particularly dry months (AEMET, 2021). The study was conducted in 30 vineyards, of which 20 had a hedgerow directly adjacent and 10 had no woody vegetation adjacent to the edge.

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Bat recording and species identification

Bat activity was monitored using passive acoustic devices (AudioMoth recorders, Version 1.1.0, Open Acoustic Devices, UK; Hill et al., 2019). For details on AudioMoth configuration and placement in the vineyards, see Appendix S1: Section S1, Figure S1. For the comparison between vineyards, recordings were done during four nights between April and July 2021 in Austria and Germany, and during three nights in June and July 2021 in Spain (Appendix S1: Table S1). One AudioMoth recorder was employed per vineyard 15 m from the edge. To minimize potential influences of weather on the data, recordings were made only during nights with no rain and wind speeds below 3 on the Beaufort scale. To test the effect of distance from the hedgerow on bat activity, we conducted a transect study in six of the German vineyards with hedgerows. Each site was monitored during two nights in July and August 2021. The AudioMoth recorders were installed along a straight line from the hedgerow into the vineyard at distances of 0, 15, 30, 60, and 120 m, at 1.5 m above the ground. The audio files were analyzed with the Kaleidoscope Pro software (Wildlife Acoustics, 2019) using the “Auto ID” function. To verify taxonomic identification, we manually checked all the detected calls and corrected them or assigned them to species groups where necessary (Barataud, 2015; Russ, 2021; Skiba, 2003). Details on species identification are given in Appendix S1: Section S2.

We obtained flight and feeding activity by dividing the recordings from a given night into 1-min intervals and then counted the number of 1-min intervals with bat calls (Miller, 2001), including both feeding buzzes and search calls for each species at each location. Thus, species-specific flight activity was obtained by counting the number of intervals (in minutes) with search calls per species on a given night and site. Feeding rate was calculated as a proportion, dividing the number of minutes with feeding buzzes by the number of minutes with bat calls per site.

To avoid misidentification, we grouped species with similar structure and frequency of echolocation calls. We thus grouped the genera Nyctalus and Vespertilio into the group of “Nyctaloid.” Three additional groups were created from the species of the genera Myotis, Eptesicus, and Plecotus, respectively. In Austria, where both Pipistrellus nathusii and Pipistrellus kuhlii occur, these species were lumped together as “P. natkuh.” If only one of the species was known to occur (P. nathusii in the Palatinate and P. kuhlii in Andalusia), they were identified at species level. In addition, the species Barbastella barbastellus, Hypsugo savii, Pipistrellus pipistrellus, and Pipistrellus pygmaeus were also identified to species level (Appendix S1: Table S2).

To study how bats respond to hedgerows and surrounding land use according to their preferred foraging habitat, we grouped the species into functional guilds following Schnitzler and Kalko (2001) as open-space foragers (H. savii, Eptesicus, and “Nyctaloid” groups), edge-space foragers adapted to foraging along vegetation (B. barbastellus, P. pipistrellus, P. pygmaeus, P. kuhlii, and P. nathusii), and narrow-space foragers that hunt within vegetation (Myotis and Plecotus) (Appendix S1: Table S2).

Surrounding land use

Since we were interested in the effect of the hedgerow and other woody elements on a small scale, we created 150 m buffers around the recording points using the Geographic Information System QGIS 3.18 (2021), to represent the differences in the land use surrounding the vineyards. The characterization of the surrounding land use was carried out using digital landscape maps and aerial photographs of the region. To assess the composition of the surrounding land use, we calculated the percentage of land covered by each land use within the buffer area ([Σ land use area/buffer area] × 100%). The calculated areas were classified as follows: urban settlements and any other manmade constructions were defined as “built-up areas,” and woody structures such as small patches of shrubs and trees and hedgerows were classified as “woody areas.” Furthermore, we calculated the closest distance from the recording point to forest (area >15 ha with dominant tree cover, excluding trees of agricultural production systems), and to built-up areas, to characterize the isolation from these habitats that have high importance for many bat species.

Statistical analysis

We performed the statistical analysis separately for each country. Since species of the same functional group share adaptations because they exploit environmental resources in a similar way (Denzinger & Schnitzler, 2013), their responses to landscape variables should be comparable. Therefore, to evaluate the response of flight activity to the presence of hedgerows and other surrounding elements, we performed the analysis by functional guild of bats. Due to the lower overall foraging activity, we decided to perform the analysis on total foraging rate by country and not by functional guild.

When we assessed the effect of the distance to the hedgerow (transect study in six German vineyards), we performed the analysis by functional guild and also by the groups with similar call structures defined in the previous section. We modeled bat flight activity, counted as active minutes per site, in relation to the log-transformed distance from the hedgerow, using generalized linear mixed-effects models (GLMMs) with a negative binomial distribution (function “glmer.nb,” lme4 package; Bates et al., 2015), and feeding rate (Tweedie distribution with “glmmTMB,” GLMMTMB package; Brooks et al., 2017) as response variable, also explained by the log-transformed distance from the hedgerow.

To assess the influence of hedgerow presence and the surrounding land use on flight and feeding activity, we fitted GLMMs (negative binomial or Gaussian distribution, “glmer.nb” or “lmer,” lme4 package; Bates et al., 2015) to test the relationships between (a) flight activity of each functional guild by country explained by the presence of hedgerow and the rest of the landscape variables and (b) the total feeding rate of each country explained by the presence of hedgerow and the other landscape variables.

We first tested Pearson's correlations between the environmental variables. We then modeled the relationship between the response variables and the independent landscape variables, with site as random factor. Distance to forest and distance to built-up areas were log-transformed. Each global model was checked with the “check_model” function (Performance package; Lüdecke et al., 2021). We tested collinearity with variation inflation factor (VIF values <4), and then used an automated model selection computing all the possible models from the global model with the “dredge” function (MuMIn package; Bartoń, 2022). We calculated the average model using the “model.avg” function (MuMIn package; Bartoń, 2022) with corrected Akaike information criterion (AIC_c) < 2 from the average model (Burnham & Anderson, 2002). We considered the estimate values, and associated SEs from the conditional average model. Significant results were defined using 95% CIs (Nakagawa & Cuthill, 2007); however, for the graphical representation of the effect of the hedgerows, we used p values to display the different significance levels. All statistical analyses were conducted in R (R Core Team, 2021). Since our main objective was to evaluate the effect of hedgerows on bats, we present the results of the hedgerow effect in a separate section. The effects of the other surrounding features are evaluated in the subsequent section.

RESULTS

We recorded a total of 16,284 min with bat calls in the 94 vineyards, 7418 min in Austria, 5789 min in Germany, and 3077 min in Spain. In all three countries, the functional guild with the highest activity was the edge-space foraging group, with Pipistrellus as the most active genus: P. natkuh in Austria (37.6% of the total activity), P. pipistrellus in Germany (72%), and P. pipistrellus and P. pygmaeus in Spain (30.5% and 27.2% of the total activity, respectively, see Appendix S1: Table S3). The functional guild with the lowest activity was the narrow-space group (9% in Austria, 3% in Germany, 1.8% in Spain).

In the transect study, we recorded a total of 3360 min with activity of seven different taxa. P. pipistrellus was the most active species, accounting for 67.6% of the total bat activity, followed by the Nyctaloid group with 18% of the total activity. Thus, edge-space bats were the most frequently recorded guild, followed by the open-space bats (68.9% and 24.4% of the total activity, respectively).

Regarding landscape characterization, Spain had the lowest woody cover as well as the greatest distances to forests, while Austria had the closest distance to the forest. In Germany, the buffers around the recording points were highly dominated by vineyard cover (Table 1).

TABLE 1 Landscape characterization of each studied country.

Country	Woody areas (%)	Vineyards (%)	Built-up (%)	Distance to forest (m)	Distance to built-up (m)
Austria	5.0 ± 1.1	61.2 ± 3.3	1.0 ± 0.6	1251 ± 162.5	816 ± 93.0
Germany	5.6 ± 1.3	86.2 ± 2.8	0.2 ± 0.1	2827 ± 259.1	584 ± 44.0
Spain	1.2 ± 0.3	46.6 ± 3.6	3.4 ± 1.5	19,745 ± 931.5	3148 ± 405.8

Effect of distance from the hedgerow

Bat flight activity decreased with the distance from the hedgerow in a guild-specific manner (Table 2, Figure 2). The mean flight activity of the open-space bats decreased by half at a distance of 30 m from the vineyard edge (0 m) and remained at a similarly low level up to 120 m into the center of the vineyard (Figure 2A), but the pattern was significant only for Eptesicus (Table 2). Flight activity of the edge-space guild was almost sevenfold higher at the edge (0 m) than at 30 m into the vineyard (Figure 2B). A similar pattern was observed for the narrow-space group, where the flight activity was fivefold higher at the edge than 30 m into the vineyards (Figure 2C).

TABLE 2 Results of the generalized linear mixed-effects models (GLMMs) evaluating the effect of the distance from the hedgerow (log-transformed) on bat activity for functional guilds and species.

Species	Estimate (SE)	Z	p	Percentage change
Open space (a)	−0.082 (0.054)	−1.531	n.s	−49.5
Eptesicus (a)	−0.186 (0.066)	−2.796	0.005	−56.0
Nyctaloid (a)	−0.0345 (0.056)	−0.610	n.s	−46.2
Edge space (a)	−0.415 (0.075)	−5.511	<0.001	−84.3
Pipistrellus nathusii (a)	−0.470 (0.130)	−3.637	<0.001	−92.3
Pipistrellus pipistrellus (a)	−0.414 (0.076)	−5.457	<0.001	−84.2
Pipistrellus pygmaeus (a)	−0.445 (0.115)	−3.874	<0.001	−84.6
Narrow space (a)	−0.371 (0.084)	−4.416	<0.001	−80.6
Myotis (a)	−0.392 (0.085)	−4.594	<0.001	−79.6
Plecotus (a)	−0.265 (0.106)	−2.494	0.013	−87.5
Total feeding rate (b)	−0.638 (0.090)	−7.063	<0.001	−90.8

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The feeding rate declined even more strongly into the vineyard than the flight activity. The feeding rate decreased by 90% between the edge (0 m) and 120 m into the center of the vineyard (Table 2), with the strongest decrease during the first 60 m (Figure 2D).

Effect of hedgerows on bat activity

In general, in all investigated countries, all functional groups of bats had a higher flight activity in vineyards with hedgerows than in vineyards without a hedgerow. However, the magnitude of the difference varied, both by functional group and by country (Table 3, Figure 3). The presence of a hedgerow had a significant effect on the flight activity of open-space bats only in Spain where the activity was five times higher in vineyards with a hedgerow than without (Figure 3A). The edge-space foraging group was the guild with the strongest response to the presence of a hedgerow in all three countries. In Austria, flight activity was two times higher in vineyards with a hedgerow, whereas in Germany and Spain, it was almost four and five times higher, respectively, in vineyards with a hedgerow than without (Figure 3B). For the narrow-space group, we only found significant differences in Austria, where flight activity in vineyards with a hedgerow was 1.7 times higher than without (Figure 3C).

TABLE 3 Results of the conditional average models testing the effects of presence of hedgerow and other landscape variables on bat flight activity per functional guild, and feeding rate for each country.

Response variable	R2	Explanatory variable	Estimate (SE)	Z	95% CI
Austria
Open space (f.a) (a)	0.041	…	…	…	…
Edge space (f.a) (a)	0.504	Hedgerow	0.781 (0.182)	4.100	0.384, 1.160
Distance to forest	0.242 (0.092)	2.505	0.050, 0.450
Vineyard areas	0.011 (0.005)	2.011	0.0003, 0.022
Narrow space (f.a) (a)	0.330	Hedgerow	0.490 (0.213)	2.203	0.057, 0.926
Feeding rate (b)	0.250	Hedgerow	0.023 (0.011)	1.987	0.0004, 0.045
Germany
Open space (f.a) (a)	0.581	Distance to forest	−0.404 (0.136)	2.831	−0.675, −0.068
Distance to built-up areas	0.626 (0.247)	2.410	0.068, 1.158
Vineyard areas	−0.038 (0.008)	4.774	−0.052, −0.018
Edge space (f.a) (a)	0.484	Hedgerow	1.300 (0.274)	4.526	0.716, 1.910
Narrow space (f.a) (a)	0.409	Distance to forest	−0.450 (0.163)	2.636	−0.785, −0.110
Vineyard areas	−0.029 (0.008)	3.208	−0.047, −0.009
Feeding rate (b)	0.322	Hedgerow	0.036 (0.013)	2.600	0.007, 0.067
Distance to forest	−0.020 (0.008)	2.172	−0.037, −0.001
Spain
Open space (f.a) (a)	0.557	Hedgerow	1.817 (0.481)	3.607	0.846, 2.851
Edge space (f.a) (a)	0.412	Hedgerow	1.511 (0.416)	3.465	0.642, 2.382
Narrow space (f.a) (a)	0.610	Distance to built-up areas	1.213 (0.465)	2.504	0.219, 2.238
Feeding rate (b)	0.300	Hedgerow	0.031 (0.012)	2.365	0.005, 0.057

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Feeding rate was also significantly higher in vineyards with a hedgerow (Figure 3D). In Austria, feeding rate was 1.3 times higher. In Germany, the effect was 2.4 times higher in vineyards with hedgerow than without, and in Spain, the feeding rate was almost fourfold higher in vineyards with a hedgerow.

Influence of surrounding land use

When evaluating the relationship between flight activity and surrounding land use, in Germany, we observed that open-space bat activity was negatively related to the distance to forest, proximity to built-up areas, and proportion of vineyards, whereas in Austria, the open-space group was not significantly influenced by any measure of surrounding land use (Table 3).

In Austria, flight activity of the edge-space bats was positively related to the proportion of vineyards in the surrounding area and the distance to forest (Table 3). In Germany, the activity of the narrow-space bats significantly increased with the proximity to forests, and with a lower proportion of vineyards. In Spain, the distance to built-up areas was the only variable that had a significant effect on the flight activity of the narrow-space group; their activity was positively correlated with a greater distance to built-up areas (Table 3). Finally, the total feeding rate in Germany was positively influenced by proximity to the forest (Table 3).

DISCUSSION

This study highlights the important role of hedgerows in vineyard landscapes for bats. Remarkably, the positive effects of hedgerows in our vineyards appeared even stronger than the increase in bats near hedges reported from open agriculture (Frey-Ehrenbold et al., 2013; Krings et al., 2022). Hedgerows provide protection against predators, especially for slow-flying bats, such as narrow-space species (Verboom & Huitema, 1997). In addition, hedgerows provide increased prey availability (Lewis, 1969) and act as acoustic guides or landmarks during movement (Schaub & Schnitzler, 2007). The strong preference for hedgerows in the current study indicates that even for small species such as Pipistrellus sp., the row structure and/or prey availability in vineyards is not sufficient to make them favorable foraging and commuting grounds. We found that for the most abundant guild in our study, edge-space bats, activity was between two and five times higher in vineyards with hedgerow than in vineyards without. These effects are stronger than the 1.4- and 2.5-fold higher bat activity near hedges reported by Frey-Ehrenbold et al. (2013) and Krings et al. (2022), respectively, for the same group of bats in arable fields. This underlines the importance of hedgerows in permanent crops, such as vineyards.

Effect of distance from the hedgerow

We found a clear pattern of decreasing bat activity with increasing distance from the hedgerow, which was similar to those found in previous studies conducted in arable fields (Heim et al., 2018; Kelm et al., 2014). In Mediterranean vineyards, Froidevaux et al. (2017) found a similar negative effect of the distance to the nearest linear feature on bat activity. Furthermore, our results suggest that the effect of hedgerows is guild-specific. As predicted, the decrease in activity into the vineyard was less pronounced for open-space species than for edge- and narrow-space bats. These differences between the functional guilds are in accordance with their different ecological niches, and the different foraging behavior, which are both reflected in their habitat use (Kelm et al., 2014). Open-space bats are adapted to the detection of flying insects over greater distances in the open air, with a fast, but less maneuverable flight (Norberg & Rayner, 1987). Thus, they may be less dependent on linear features, which could explain the less pronounced decline in their activity with an increasing distance from hedgerows. However, the fact that even for this group we observed a higher activity close to the hedgerow indicates that hedgerows are also important for open-space bats in vineyards. Our results for the edge group of a sevenfold decrease in the first 30 m are similar to those obtained by Heim et al. (2018) who found that P. pipistrellus decreased its activity by about 10-fold in the first 50 m from the edge of the woody vegetation in arable fields. For the narrow group, our results also agree with the 4.9-fold decrease reported by Heim et al. (2018) for Myotis sp. but are less pronounced than the about 11-fold decrease in activity reported by Kelm et al. (2014) in arable fields.

Different echolocation calls between species may produce some bias in the data toward open-space bat calls (Kelm et al., 2014). The detection distance for open-space bats is greater than that of the other bat guilds, ranging from 35 to 150 m, while for edge- and narrow-space bats, it is about 30 and 15 m, respectively (Barataud, 2015). The longer detection distance may have contributed to the less sharp decline in open-space bat activity with increasing distance from hedgerows, since individuals calling from along the hedgerow may have been detected at further into the vineyard. However, our comparison between vineyards with and without hedgerow as well as the effects of distance to forest and built-up area appear robust against such differences in detection distances, since they involve much larger distances (Table 1). Our findings of a strong decrease in feeding rate from the hedgerow toward the center of the vineyard are consistent with those of previous studies conducted in arable agricultural landscapes (Downs & Racey, 2006; Heim et al., 2018). This indicates that areas near to hedgerows have a higher prey availability for bats (Verboom & Huitema, 1997), and that foraging close to these structures may involve a lower energetic cost of flight due to the cover from predators or wind (Heim et al., 2015). These results demonstrate that also in perennial crops, such as vineyards, hedgerows are an important landscape feature that promotes bat flight and foraging.

Effect of hedgerow presence

We observed higher activities of all functional guilds in vineyards with hedgerows than in vineyards without hedgerows in the three studied countries. However, our hypothesis that the strength of the effect is guild-dependent was only partially confirmed. Open-space bats had a nonsignificant response in Austria and Germany, which is consistent with our hypothesis that they also utilize open areas. However, in Spain, the differences were highly significant. This may be due to the fact that in Spain the overall cover of wooded areas including hedgerows was lower than in Germany and Austria. In addition, the distance to forests was substantially higher (Table 1). This might reflect that when woody habitats are scarce, bat activity is even more concentrated around them (Fuentes-Montemayor et al., 2013).

In line with our hypothesis, there was a strong positive effect of hedgerows on edge-space bats in all three countries. The most abundant species of this group in all countries were those of the genus Pipistrellus, which is associated with structurally complex habitats such as forests and their edges (Davidson-Watts et al., 2006). These species benefit from wooded hedgerows by taking advantage of the availability of insects (Lewis, 1969). Similar to our findings, previous studies conducted in arable fields showed a significantly higher incidence of Pipistrellus spp. in the presence of hedgerows than in open arable areas (Boughey et al., 2011; Verboom & Huitema, 1997). Krings et al. (2022) found that the activity of the edge-space group was three times higher over the hedgerow than in the center of wheat fields. Thus, the differences were less pronounced than those obtained in our results. This could imply that the positive effects of hedgerows in vineyards are equal to, or even stronger than, those in arable agricultural landscapes.

For the narrow-space bats, contrary to our predictions, only in Austria there was a positive influence of hedgerows, whereas in Germany and Spain, there was no significant effect. These results differ from a previous study conducted in arable fields that found a strong hedgerow effect on this group (Krings et al., 2022). In our case, this might be due to the low number of recorded calls from this guild, especially in Germany and Spain (3% and 1.8% of the total bat activity, respectively); thus, we cannot draw reliable conclusions. Their high sensitivity to landscape disturbance (Duchamp & Swihart, 2008), and the behavior to be more adapted to foraging in cluttered spaces, are probably the main reasons for their low activity, which are also consistent with results obtained in other agricultural landscapes, such as wheat fields, irrigated maize fields, and rice paddies (Froidevaux et al., 2022; Heim et al., 2018).

Our results of the positive influence of hedgerows on feeding rate underline their role as foraging areas for bats. Hedgerows support a higher prey abundance by providing insects with food, breeding substrate, and a favorable microclimate within agricultural matrices (Pollard & Holland, 2006). Furthermore, meteorological conditions such as those that occurred during the monitoring year, including a dry spring in Austria and Spain and a cold spring in Germany, could lead to food shortages (Sendor & Simon, 2003), enhancing the role of hedgerows as a food source for insectivorous bats. These findings are relevant because bats are highly mobile animals, which can travel over many kilometers per night (Müller et al., 2012). However, because flying is energetically costly, foraging implies a trade-off between the energy gain when foraging in areas with abundant prey, and the energy loss when commuting to those locations (Baroja et al., 2021). Thus, if foraging sites are lost, bats may not be able to meet the energetic requirements of prehibernal fattening or reproduction, compromising overwinter survival or even the population's persistence (Mackie & Racey, 2007).

Previous studies conducted in arable land showed nonsignificant (Krings et al., 2022) and slightly significant (Toffoli, 2016) differences between feeding activity in hedgerows and open fields, while a study in Chilean vineyards found a significantly higher feeding activity along the woody vegetation edge than in the interior of the vineyard (Rodríguez-San Pedro et al., 2018). Thus, our results suggest that hedgerows in a perennial vineyard landscape are equally important as in other agricultural habitats.

Influence of surrounding land use

As expected, the activity of open-space bats in Germany was influenced by the wider landscape. These species adapted for fast and inexpensive flight are able to make long commutes, that is, they can exploit several patches within a landscape covering a greater distance (Mendes et al., 2016), likely due to their high mobility (Fuentes-Montemayor et al., 2017). Their negative relationship to the distance to forests and proximity to built-up areas may be explained by the preference of Nyctalus species for roosting in tree cavities rather than in man-made structures (Ruczyński & Bogdanowicz, 2008). Other studies have shown a similar pattern concerning the effect of the distance to forests (Froidevaux et al., 2022; Heim et al., 2018). Furthermore, Fuentes-Montemayor et al. (2017) showed that Nyctalus bats had higher activities in woodlands with smaller proportion of urban edges, indicating a negative effect of built-up areas. However, our prediction was not fulfilled in Austria and Spain. In Austria, no landscape variable had an influence on the activity of open-space bats, and in Spain, hedgerows were the only element that had an effect on this group. The surroundings of the vineyards were possibly too uniform in these two countries to result in significant landscape effects.

Narrow-space bats emit short echolocation calls, relying on linear structures for flight navigation. They forage more intensively in more cluttered environments (Fuentes-Montemayor et al., 2013) and are thus more likely to be influenced by woody biomass in the surrounding landscape at smaller scales (Lacoeuilhe et al., 2016). Therefore, we predicted a highly positive effect of hedgerows and of wooded areas in the nearest surrounding environment. In Germany, narrow-space bats were positively influenced by the proximity to forests. In the same line, in Spain, narrow-space bats were positively related to the distance to built-up areas as these areas do not provide suitable roosting sites for this guild. Our results are in line with Blary et al. (2021), who also found increased activity of Myotis spp. with closer proximity to forests, and greater distance from built-up areas.

The feeding rate in Germany was positively related to the proximity to forests. Forest edges may represent attractive feeding grounds for bats (Heim et al., 2018) as insects can accumulate due to the windbreak they create (Lewis, 1969). Our results are in agreement with Treitler et al. (2016), who also found a decrease in feeding attempts at greater distances from the forest. This may also be related to landscape connectivity, which facilitates access to potentially suitable foraging sites for bats (Treitler et al., 2016).

Finally, as hypothesized, a higher vineyard cover had a negative effect on bats when it was associated with a more homogeneous landscape, as in Germany, where mean vineyard cover within the 150-m buffer areas was about 80%. This effect was significant only for narrow and open-space bats, probably due to the habitat flexibility of P. pipistrellus (Russ & Montgomery, 2002), the dominant species in the German edge-space group. In the same line, in Austria, where vineyard cover was comparably lower, and all monitored sites were closer to forest, the effect of vineyards was positive for edge-space bats, as was the distance to the forest. This might be explained by the general importance of a heterogeneous landscape for bat movement and activity (Monck-Whipp et al., 2018).

Implications for conservation

Hedgerows are an important element for biodiversity conservation in an agricultural context (Graham et al., 2018). Our findings support the importance of hedgerows for bats within wine-growing landscapes. Although perennial crops may be less disturbed and have greater resource continuity than annual crops (Bruggisser et al., 2010), bats generally use vineyards only rarely, which may result from a preference for better foraging habitats (Stahlschmidt et al., 2012) such as hedgerows.

The decline in European bat populations during the 20th century, caused in part by landscape simplification associated with agricultural intensification, underlines that bats require conservation and research attention. Their decline also impairs their important role as pest control agents, in particular, the potential function as predators of the European grapevine moth (Charbonnier et al., 2021; Tortosa et al., 2023). Paredes et al. (2021) found that infestation with L. botrana decreased with surrounding shrub cover in Spanish vineyards. This might be related to a higher foraging activity of bats and other predators like birds in vineyards with nearby wooded areas, which could lead to a lower level of infestation by the grapevine moth.

Given their high potential to support bat communities in vineyards, hedgerows and wooded areas should be restored and conserved. They contribute to biodiversity conservation at local and regional scales by providing suitable habitats, food, and shelter in the landscape for a wide range of species (Weibull & Östman, 2003) Thus, the conservation of hedgerows may also benefit other species, such as bees (Eckerter et al., 2022) and birds and the ecosystem services that they provide. For example, Barbaro et al. (2017) found higher abundances of insectivorous birds in vineyards with a higher proportion of seminatural habitats, suggesting a positive relationship between their contribution to pest control and landscape heterogeneity. Similarly, Thomson and Hoffmann (2013) showed that the abundance of arthropod predators and parasitoids of grape moths increased near woody habitats. Currently, the European Union requires farmers to devote parts of their arable land to nonproductive habitats, such as hedgerows (European Commission, 2023). This measure, however, is only mandatory for annual crops. Our results suggest that also permanent crops should be obliged to establish non-crop elements such as hedgerows to increase biodiversity and pest control.

OUTLOOK

Our findings suggest that hedgerows are important elements for bat conservation, providing shelter, connectivity, and food (Verboom & Huitema, 1997). However, further research into these elements is important, as not all hedgerow types may offer the same benefits, and their biodiversity value depends on their structure, composition, and management (Graham et al., 2018; Homberger et al., 2017; Merckx & Berwaerts, 2010). Hedgerows with greater structural complexity (variety of heights, vegetation layers) and plant species diversity may be more beneficial for bats and their prey (Froidevaux et al., 2016; Maudsley et al., 2002). Frequency of trimming, and height and width of the hedge are important factors affecting its quality as bat habitat (Froidevaux, Boughey, et al., 2019). Management that reduces pruning and maintains the complex structure of the hedgerow can have a positive effect on bats directly or indirectly by increasing prey availability, which could also benefit insectivorous birds (Froidevaux, Boughey, et al., 2019; Froidevaux, Broyles, & Jones, 2019). We therefore emphasize the importance of continuing hedgerow research in agricultural landscapes to determine which hedgerow types provide the greatest benefits for bats, and how best to manage them to promote their conservation. Also, other types of agriculture, such as agroforestry (Edo et al., 2024) or permaculture (Reiff et al., 2024), may have similar benefits for bat conservation by introducing woody elements into otherwise open agricultural areas.

AUTHOR CONTRIBUTIONS

Martin H. Entling and Verena Rösch conceived the ideas and designed the methodology. Rafael Alcalá Herrera, Emilio Benitez, Fernanda Chávez, Stefan Möth, Jo Marie Reiff, and Silvia Winter collected the data. Fernanda Chávez analyzed the data. Fernanda Chávez, Martin H. Entling, and Verena Rösch led the writing of the manuscript. All authors contributed critically to the drafts and gave final approval for publication.

ACKNOWLEDGMENTS

We acknowledge the funders of this project; this study is part of the project “SECBIVIT” funded through the 2017/2018 Belmont Forum and BiodivERsA joint call for research proposals, under the BiodivScen ERA-Net COFUND program, and with the following funding organizations: Agencia Estatal de Investigación (Ministerio de ciencia e innovación/Spain), Austrian Science Fund (FWF grant number I 4025-B32), Federal Ministry of Education and Research (BMBF/Germany), French National Research Agency (ANR), Netherlands Organization for Scientific Research (NWO), National Science Foundation (NSF), and Romanian Executive Agency for Higher Education, Research, Development, and Innovation Funding (UEFISCDI). We would also like to thank all winegrowers for allowing us to collect data at the study sites. Furthermore, we thank to Dr. Olga Heim for helping us during all the study with confirmation on the identification of the bat calls, and to Dr. Fulgencio Lisón for his insights into the Spanish bats.

CONFLICT OF INTEREST STATEMENT

The authors declare no conflicts of interest.

DATA AVAILABILITY STATEMENT

Data (Chávez et al., 2024) are available from Figshare: .

References

AEMET. 2021. “Agencia Estatal de Meteorología—AEMET. Gobierno de España.” https://www.aemet.es/es/portada.

Barataud, M. 2015. Acoustic Ecology of European Bats: Species Identification, Study of Their Habitats and Foraging Behaviour. Mèze: Biotope.

Barbaro, L., A. Rusch, E. W. Muiruri, B. Gravellier, D. Thiery, and B. Castagneyrol. 2017. “Avian Pest Control in Vineyards Is Driven by Interactions Between Bird Functional Diversity and Landscape Heterogeneity.” Journal of Applied Ecology 54(2): 500–508. [DOI: https://dx.doi.org/10.1111/1365-2664.12740].