Remnant trees increase bat activity and facilitate the use of vineyards by edge-space bats
Introduction
Monocultures negatively impact biodiversity and ecosystem processes, frequently resulting in habitat loss, deforestation, and ecological degradation associated with chemical fertilizers and herbicides (Altieri, 2009; Rosset and Altieri, 1997). However, retaining ecological structures in converted landscapes can help maintain biodiversity and ecosystem services such as natural pest control (Fischer et al., 2010; Frey‐Ehrenbold et al., 2013; Kelly et al., 2016; Lumsden and Bennett, 2005; Medina et al., 2007). Remnant trees are important ecological structures in many habitats. They maintain bird and insect diversity by providing nesting, roosting, and foraging habitat, and by promoting connectivity for movement of wildlife within agricultural landscapes (DeMars et al., 2010; Dunn, 2000; Kelly et al., 2016; Manning et al., 2006). Remnant oak trees provide direct ecological services such as enrichment of topsoil nutrients, attenuation of extreme temperatures, protection from erosion, and carbon sequestration (Marañón et al., 2016), in addition to aesthetic, cultural, political, and historical values (Blicharska and Mikusiński, 2014; Lindenmayer et al., 2014; Standiford et al., 1986).
Bats have been shown to provide important natural pest control services in a variety of agricultural systems, including maize (Maine and Boyles, 2015), cotton (Federico et al., 2008; Lee and McCracken, 2005; McCracken et al., 2012;), coffee (Williams-Guillén et al., 2008), walnuts (Long et al., 1996; Pollock, 2015), and pecans (Brown et al., 2015). The role of bats as natural insect pest regulators has been valued at $3.7 billion annually to the U.S. agricultural industry (Boyles et al., 2011; Cleveland et al., 2006; Kunz et al., 2011). Yet bat populations have declined due to disease, habitat loss and fragmentation, and pollution (Jones et al., 2009; Kunz et al., 2011; Weller et al., 2009). Agricultural development contributes to decreases in abundance and diversity of bat species, mainly by reducing roosting and foraging habitat (Park, 2015). It is therefore important to determine the conditions under which agricultural landscapes can benefit bats, and how bats may benefit agricultural enterprises.
Vineyard acreage has expanded rapidly in California over the past four decades (Merenlender, 2000; Volpe et al., 2010), with the highest rates of increase in the Northern and Central coasts of California (Heien and Martin, 2003). We conducted our study in San Luis Obispo County, on the central coast of California. From 2000 to 2015, wine grape area in San Luis Obispo County doubled from 9,300 to 19,800 ha (San Luis Obispo Department of Agriculture, 2016). Although some vineyards are planted in treeless areas or on former cropland (Merenlender, 2000), grape monoculture often replaces natural oak savanna (Grismer and Caitlin, 2012). Studies in other systems have shown that retaining a wide variety of ecological features (riparian buffers, hedgerows, forest edges, and other remnant vegetation) around agricultural areas results in increased bat activity (Boughey et al., 2011; Fuentes-Montemayor et al., 2013; Heim et al., 2015; Kelly et al., 2016; Lumsden and Bennett, 2005; Park, 2015). Individual trees, in particular, have been shown to provide habitat to bat species in other agricultural systems (Fischer et al., 2010; Frey‐Ehrenbold et al., 2013; Heim et al., 2015; Lumsden and Bennett, 2005). However, no study has quantified the value of remnant trees within vineyards for bats.
Isolated trees benefit bats by providing protection from wind and predators, greater insect abundance, and landscape-level connectivity (Frey‐Ehrenbold et al., 2013; Heim et al., 2015; Kelly et al., 2016). However, the value of landscape structures to bats can vary among species (Bernard and Fenton, 2007). Wing morphology, echolocation call and foraging behavior of bat species are adapted to certain habitats (Aldridge and Rautenbach, 1987; Denzinger and Schnitzler, 2013; Neuweiler, 1984; Schnitzler and Kalko, 2001; Schnitzler et al., 2003). Typically, smaller and more maneuverable bats forage close to vegetation or edge habitat using higher frequency echolocation calls (≥ 35 kHz). Their high frequency echolocation calls limit the range of prey detection, making foraging less effective in open areas (Heim et al., 2015). Herein we refer to these as edge-space bats. Larger, less maneuverable species typically forage in open spaces and emit low frequency calls (<35 kHz). These we refer to as open-space bats. Bats that specialize in foraging close to or within vegetation have been found to have higher extinction risks than more flexible aerial hawkers (Jones et al., 2003; Safi and Kerth, 2004).
We investigated whether remnant isolated trees influence bat species activity and diversity, and insect abundance, in 14 vineyards in central-coastal California. We also assessed how characteristics of the surrounding landscape influenced the relationships between bats and remnant trees. We used generalized linear mixed models to compare bat activity, species-specific activity, and insect abundance at remnant trees to nearby open areas in a paired design. We hypothesized that activity of edge-space bat species would be higher around remnant trees in vineyards, and activity of open-space bats would be higher in vineyard areas away from trees. We tested whether prey availability could be driving differences in bat activity. We hypothesized that insect abundance would be higher at trees relative to open areas. We also hypothesized that bat activity would be higher with increasing insect abundance (Dunn, 2000; Ohsawa, 2007). Finally, we hypothesized that overall bat activity at trees would increase with larger tree size, closer proximity to neighboring remnant trees, and with a larger number of remnant trees within 500 m.
Section snippets
Methods
Our study was conducted from 2014 to 2015 in central-coastal California, in northeastern San Luis Obispo County on a study area of approximately 352 km2 (120°39′10.43″W - 120°30′1.76″W, 35°44′45.17″N - 35°31′36.95″N; Fig. 1). The climate is Mediterranean, with mild winters and hot, dry summers. Most rainfall occurs between October and May, varying annually and by microclimate from 200 to 1000 mm (National Oceanic and Atmospheric Administration, 2017). The natural vegetation community is oak
Total bat activity and frequency groups
During 40 recording sessions comprising 206 detector-nights, we recorded 11,465 bat passes, of which 39% were identified as HiF and 61% as LoF species. Total bat activity was 1.45 times higher at trees than open areas (Table 2; Fig. 3). HiF bat activity was 2.39 times higher at trees (Table 2; Fig. 3). LoF bat activity did not significantly differ between tree and open areas (Table 2; Fig. 3). In models of total activity as well as activity of HiF and LoF species, random effect of vineyard,
Discussion
We found that bat activity at remnant isolated oak trees within central California vineyards was greater than at nearby treeless areas of these vineyards. This relationship was driven largely by activity of bats that echolocate at higher frequencies and are typically associated with vegetation edge habitats. In a close ecological analog to our study, a study in northern California found that total bat activity was 2.3 times higher near blocks of remnant vegetation along vineyard edges as
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Conflicts of interest
None.
Acknowledgements
We thank Skylar Giordano and Bernard Fahey for assistance with the initial deployment of detectors and with data analysis. We acknowledge Chris Domschke for conducting a large portion of the initial call analysis. For providing valuable reviews of the manuscript, we thank Bill Zielinski and Rochelle Kelly. The contributions of Scott Steinmaus for valuable statistical advice is appreciated. We thank the vineyard owners for providing access to their vineyards. Insects captured in the vineyards
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