Summer Flowering Cover Crops Support Wild Bees in Vineyards

Summer Flowering Cover Crops Support Wild Bees in Vineyards Abstract Agricultural expansion and intensification negatively affect pollinator populations and has led to reductions in pollination services across multiple cropping systems. As a result, growers and researchers have utilized the restoration of local and landscape habitat diversity to support pollinators, and wild bees in particular. Although a majority of studies to date have focussed on effects in pollinator-dependent crops such as almond, tomato, sunflower, and watermelon, supporting wild bees in self-pollinated crops, such as grapes, can contribute to broader conservation goals as well as provide other indirect benefits to growers. This study evaluates the influence of summer flowering cover crops and landscape diversity on the abundance and diversity of vineyard bee populations. We showed that diversity and abundance of wild bees were increased on the flowering cover crop, but were unaffected by changes in landscape diversity. These findings indicate that summer flowering cover crops can be used to support wild bees and this could be a useful strategy for grape growers interested in pollinator conservation as part of a broader farmscape sustainability agenda. Through pollination, bees (Apoidea) provide an important ecosystem service that supports both agricultural crops and wild plants. Approximately one-third of the total volume of global food production comes from pollinator-dependent crops (McGregor 1976, Williams 1994, Morse and Calderone 2000, Klein et al. 2007). While a majority of crop pollination is carried out by Apis mellifera L. (Hymenoptera: Apidae), both feral and managed (Delaplane et al. 2000), non-Apis wild bees also make substantial contributions (Parker et al. 1987, Westerkamp and Gottsberger 2000, Klein et al. 2007). In some cases, wild bees have even been shown to be individually more effective pollinators than honey bees (Bosch and Marina 1994, Javorek et al. 2002, Kremen et al. 2002, Greenleaf and Kremen 2006, Winfree et al. 2008). A majority of wild flowering plants also rely heavily on animal pollinators and wild bees, in particular (Kearns et al. 1998, Ollerton et al. 2011, Buchmann and Nabhan 2012). While the relationship between many wild flowering plants and their pollinators is not always obligate (Waser et al. 1996), reductions in the abundance or functional diversity of wild bees are generally linked to declines in wild plant communities (Fontaine et al. 2005, Biesmeijer et al. 2006). In this way, wild bee populations are critical to both agricultural production and the conservation and restoration of natural habitats (Allen-Wardell et al. 1998). It is well established that pollinator populations are in decline globally (Kearns et al. 1998, Steffan-Dewenter et al. 2005, National Research Council 2007, Potts et al. 2010). While losses of A. mellifera have been attributed to a combination of biotic and abiotic stressors (e.g., pathogens, parasites, malnutrition, pesticide exposure) (Cox-Foster et al. 2007, Ellis et al. 2010, Neumann and Carreck 2010, Goulson et al. 2015, Woodcock et al. 2017), the dominant factor affecting wild bees has been habitat loss (Steffan-Dewenter et al. 2002, Brown and Paxton 2009, Winfree et al. 2009, Nicolson and Wright 2017). As such, a relationship exists between habitat loss, wild bee declines and reduced pollination of both crops (Richards 2001, Ricketts et al. 2008, Garibaldi et al. 2013) and wild plants (Aguilar et al. 2006). Agricultural expansion is the largest driver of natural habitat loss (Foley et al. 2005). Within agroecosystems, monocrop practices further reduce the availability of resources for pollinators (e.g., flowering weeds), while the use of agrichemicals can directly affect pollinators within natural habitats (e.g., pesticide drift, nutrient runoff) (Kennedy et al. 2013, Nicholls and Altieri 2013, Woodcock et al. 2017). Yet agricultural habitats, when managed with biodiversity in mind, do have significant conservation and functional potential (Green et al. 2005, Norris 2008, Tscharntke et al. 2012). Increased local and landscape habitat diversity has been shown to increase a variety of ecosystem services to agriculture, including crop pollination (Kremen and Miles 2012, Isbell et al. 2017, Lichtenberg et al. 2017). Diversified cropping systems can also contribute to off-farm biodiversity conservation by improving matrix quality and connectivity between patches of natural habitat (Scherr and McNeely 2008, Perfecto and Vandermeer 2010). In vineyards, many grape growers are experimenting with the use of hedgerows and cover crops to enhance a variety of ecosystem services (Altieri et al. 2005, Fiedler et al. 2008, Gurr et al. 2017), including conservation of pollinators (James et al. 2014). Since Vitis vinifera L. (Vitales: Vitaceae) are self-pollinating, interest in vineyard bee populations has been driven not by concerns over crop productivity or quality, but rather by the intrinsic value of pollinators themselves and the supporting ecosystem services they provide to surrounding natural habitats, such as pollination of wild plants (Kleijn et al. 2015). The use of on-farm habitat provisioning to support bee populations has been studied in a variety of pollinator-dependent cropping systems, such as almond, watermelon, and tomato, but little is known about bee response to these practices in self-pollinated crops, such as grapes. This study evaluates bee response to the use of a summer flowering cover crop that was developed as part of a larger ecologically based pest management program in California’s North Coast wine grape region (Wilson et al. 2017). Materials and Methods Study Sites Over a 2-yr period, paired plots with and without summer flowering cover crops were evaluated at 10 vineyard sites. Experimental blocks >0.8 hectares (2 acres) were located in commercial vineyards in Napa and Sonoma County, California, United States. Vineyards were located on level ground and composed of vines that were at least 5 yr old. All cultivars were red grape varieties (Cabernet Sauvignon, Zinfandel, and Merlot). Each experimental block consisted of 60 vine rows with 50–80 vines per row. Blocks were divided into two, equal-sized plots, and each plot was then randomly assigned to either a control or flowering cover crop treatment. In each plot, all samples were taken from the five middle vine rows. Within each of the five sample rows, no measurements were taken from the first or last 10 vines. There were eight sites in year 1 and two sites in year 2. Each site was a replicate with a block containing two plots, one with and one without the flowering cover crops. Flowering Cover Crop Treatment The flowering cover crop treatment consisted of Phacelia tanacetifolia Benth. (Solanales: Boraginaceae) (purple tansy), Ammi majus L. (Apiales: Apiaceae) (Bishop’s flower), and Daucus carota L. (Apiales: Apiaceae) (wild carrot) sown together in alternate row middles. These flower species have an overlapping bloom sequence (P. tanacetifolia, A. majus and D. carota bloom April–May, May–June, and July–September, respectively) and are compatible with standard vineyard management practices, which requires that flowers do not need any supplemental irrigation and can be sown in the fall. In October or November, row middles were tilled, and flowers then sown 0.32–0.64 cm deep (1/8–1/4 inch) using a compact seed drill. P. tanacetifolia, A. majus, and D. carota were sown at a rate of 2.2 kg/ha (2 lbs/acre), 0.56 kg/ha (0.5 lbs/acre), and 0.56 kg/ha (0.5 lbs/acre), respectively. The flowers relied on winter/spring rains (October–April) to establish. In the spring, alternate rows of weedy vegetation were tilled under in both treatment and control plots, thereby leaving treatment plots with an alternating set of row middles sown to the flowering cover crops and control plots with an alternating set of row middles with resident weedy vegetation. Resident weedy vegetation primarily consisted of Ipomoea purpurea (L.) Roth (Solanales: Convolvulaceae) (morning glory), Euphorbia spp. (Euphorbiales: Euphorbiaceae) (spurges), Malva parviflora L. (Malvales: Malvaceae) (cheeseweed), Erodium spp. (Geraniales: Geraniaceae) (filaree), and Polygonum arenastrum Boreau (Polygonales: Polygonaceae) (knotweed). Landscape Diversity Metrics Vineyards in this study were situated along a continuum of low to high diversity landscapes, quantified as the proportion of natural habitat within 0.5 km of the vineyard site. In order to do this, ‘rangeland cover type’ was first extracted from the CalVeg dataset (USDA 2013) using ArcGIS 10.1 (ESRI, Redlands, United States). There were 71 possible values for rangeland cover type (Shiflet 1994) and the total area of each type was calculated within a 0.5 km radius around every vineyard. Cover types were then consolidated into five categories: ‘natural habitat’, ‘agriculture’, ‘development’, ‘water’, and ‘no data’. The ‘natural habitat’ category consisted primarily of riparian, oak woodland, and chaparral habitats while the ‘agriculture’ category was almost entirely vineyard. ‘Development’ included all commercial and residential areas, including urban vegetative landscaping. For this analysis, ‘landscape diversity’ is defined as the proportion of ‘natural habitat’ within 0.5 km of the study site. Sampling Bee Populations on Ground Covers Sweep-nets were used to collect bees from ground covers in all plots. Samples were collected from the flowers in the treatment plots and from the resident weedy vegetation in the control plots during peak bloom of P. tanacetifolia, A. majus, and D. carota, which occurred on 22 April, 14 June, and 2 August in 2012 and on 20 April, 30 May, and 25 July in 2013, respectively. During each bloom period, bees were sampled from the ground covers between 10:00 and 14:00 hr using a 30.5 cm diameter sweep-net. In each plot on each sample date, sweep-net sampling consisted of five sets of 30 unidirectional sweeps. All bees were transferred to plastic freezer bags and brought to the laboratory for identification. Bees were identified to species when possible; however, not all of the bees collected in this study have been described to the species level. Bees in the genus Sphecodes could not be identified to species. Bees in the genus Lasioglossum and subgenera Dialictus and Evylaeus were identified to morphospecies, but were grouped at the subgenus level for analysis. Statistical Analysis Diversity of wild bees on the ground covers was quantified using the Shannon index (H′): H′ = −∑(Pi × ln Pi), where Pi is the proportion of individuals in the ith species in the dataset. Higher H′ values indicate greater community diversity. Data on bee abundance, richness, and diversity were evaluated with generalized linear mixed-effects models using a Gaussian distribution and identity-link function. Model comparison (χ2 tests) was then used to evaluate the influence of main effects against a reduced (null) model. To meet the assumption of normality, all of the bee abundance data were log(x + 1) transformed. All analyses were conducted with the ‘lme4’ package in R and post-hoc Tukey contrasts (‘glht’ function in the ‘multcomp’ package) were used to make comparisons between multiple factors (Bates et al. 2015, R Core Team 2016). Bee response to the flowering cover crops and changes in landscape diversity was evaluated with models that included the main effects ‘landscape diversity’ (i.e., proportion of natural habitat within 0.5 km of the study site) and ‘ground cover type’ (i.e., flowering cover crop or resident weedy vegetation). Landscape mediation of flowering cover crop effects was analyzed by evaluating whether differences in bee abundance, richness, and diversity between plots with and without flowering cover crops were more or less pronounced in certain landscapes. For each response variable tested, the difference in values between the treatment and control plot at each site was calculated. These differences were then evaluated as the response variable in a model that included both a linear and nonlinear term (i.e., a quadratic, second-order polynomial) for the main effect ‘landscape diversity’. All analyses included the random effect ‘bloom period’ (i.e., peak bloom of P. tanacetifolia, A. majus, or D. carota) nested within ‘site’ nested within ‘year’. Results We collected a total of 538 A. mellifera and 420 wild bees across five families and nine genera. Total abundance and diversity of wild bees were increased on all three species of flowering cover crop (Table 1). Densities of some bee species or genera were increased only on specific flowers, while others responded to multiple flower species (Table 2, Fig. 1). More specifically, increased density of Bombus vosnesenskii Radoszkowski (Hymenoptera: Apidae), Lasioglossum (Dialictus) spp. (Hymenoptera: Halictidae), L. (Evylaeus) spp. (Hymenoptera: Halictidae), and L. incompletum (Crawford) (Hymenoptera: Halictidae) was observed only on P. tanacetifolia while Hylaeus mesillae (Cockerell) (Hymenoptera: Colletidae) abundance was increased only on D. carota. Alternately, there was greater abundance of A. mellifera on P. tanacetifolia and D. carota, Halictus tripartitus Cockerell (Hymenoptera: Halictidae) on P. tanacetifolia and A. majus, and Ha. ligatus Say (Hymenoptera: Halictidae) on A. majus and D. carota. Finally, Ha. farinosus Smith (Hymenoptera: Halictidae) and L. tegulariforme (Crawford) (Hymenoptera: Halictidae) did not respond to any of the flowering cover crops and densities of Andrena w-scripta Viereck (Hymenoptera: Andrenidae), Ceratina acantha Provancher (Hymenoptera: Apidae), C. tejonensis Cresson (Hymenoptera: Apidae), Heriades occidentalis Michener (Hymenoptera: Megachilidae), Hy. bisunatus Forster (Hymenoptera: Colletidae), Sphecodes sp. (Hymenoptera: Halictidae), and Xylocopa tabaniformis orpifex Smith (Hymenoptera: Apidae) were all too low for statistical analysis. Fig. 1. View largeDownload slide Abundance of wild bees on the ground covers during peak bloom of each flowering cover crop species. Fig. 1. View largeDownload slide Abundance of wild bees on the ground covers during peak bloom of each flowering cover crop species. Changes in landscape diversity did not have any effect on densities of A. mellifera or wild bees nor on overall wild bee diversity (Table 1). Furthermore, differences in wild bee density and diversity between plots with and without flowering cover crops was not mediated in any way by changes in landscape diversity (Table 1). Table 1. Influence of flowering cover crops and landscape diversity on bee density, richness and diversity Organism  Flowers  Landscape  Mediation Effect  Andrenidae   Andrena w-scripta  –  –  –  Apidae         Apis mellifera  290.73***  1.87  0.80   Bombus vosnesenskii  28.40***  0.05  0.01   Ceratina acantha  4.64  1.08  1.89   C. tejonensis  –  –  –   Xylocopa tabaniformis orpifex  –  –  –  Colletidae         Hylaeus bisinuatus  –  –  –   Hy. mesillae  25.57***  2.24  0.02  Halictidae         Halictus farinosus  –  –  –   Ha. ligatus  49.38***  2.47  2.05   Ha. tripartitus  32.54***  0.54  0.16   Lasioglossum (Dialictus) spp.  47.54***  0.14  1.04   L. (Evylaeus) spp.  20.66***  0.01  0.51   L. incompletum  37.02***  1.64  0.02   L. tegulariforme  13.26*  0.67  0.16   Sphecodes sp.  –  –  –  Megachilidae   Heriades occidentalis  –  –  –  Wild Bees   Total  111.44***  0.47  0.04   Richness  100.13***  1.03  0.03   Shannon (H’)  81.12***  0.84  0.05  Organism  Flowers  Landscape  Mediation Effect  Andrenidae   Andrena w-scripta  –  –  –  Apidae         Apis mellifera  290.73***  1.87  0.80   Bombus vosnesenskii  28.40***  0.05  0.01   Ceratina acantha  4.64  1.08  1.89   C. tejonensis  –  –  –   Xylocopa tabaniformis orpifex  –  –  –  Colletidae         Hylaeus bisinuatus  –  –  –   Hy. mesillae  25.57***  2.24  0.02  Halictidae         Halictus farinosus  –  –  –   Ha. ligatus  49.38***  2.47  2.05   Ha. tripartitus  32.54***  0.54  0.16   Lasioglossum (Dialictus) spp.  47.54***  0.14  1.04   L. (Evylaeus) spp.  20.66***  0.01  0.51   L. incompletum  37.02***  1.64  0.02   L. tegulariforme  13.26*  0.67  0.16   Sphecodes sp.  –  –  –  Megachilidae   Heriades occidentalis  –  –  –  Wild Bees   Total  111.44***  0.47  0.04   Richness  100.13***  1.03  0.03   Shannon (H’)  81.12***  0.84  0.05  The table shows χ2 values from generalized linear mixed-effects models. Some organisms were not analyzed due to insufficient abundance. For each response variable in the ‘mediation effect’ analysis, the difference between the treatment and control plot at each site was evaluated with a model that included both a linear and non-linear term (i.e., polynomial) for the main effect ‘landscape diversity’. *P < 0.05, **P < 0.01, ***P < 0.001. View Large Discussion Bee Response to the Flowering Cover Crops In this study, diversity and abundance of wild bees were increased on the summer flowering cover crops relative to resident weedy vegetation. These findings are consistent with multiple studies that have documented a positive relationship between increased on-farm habitat diversity and wild bee abundance, richness and/or diversity (Saunders et al. 2013, Blaauw and Isaacs 2014, Kremen and M’Gonigle 2015, Isbell et al. 2017, Lichtenberg et al. 2017). Positive response of wild bees to the presence of floral resources in vineyards is not unexpected. Even when no significant differences were observed or densities were too low for statistical evaluation, bee abundance on the flowering cover crops was almost always elevated relative to the resident weedy vegetation (Table 2), although not all bees responded equally to all three species of flowering cover crop. Table 2. Summary of bees collected from the flowering cover crop and resident weedy vegetation (mean ± SEM) during peak bloom of each flower species Genus/species  Phacelia tanacetifolia  Ammi majus  Daucus carota  Weeds  Flowers  Weeds  Flowers  Weeds  Flowers  Andrenidae   Andrena w-scripta  0  0.09 (±0.05)  0  0  0  0  Apidae   Apis mellifera  0.02 (±0.02) A  5.83 (±0.68) C  0 A  0.07 (±0.04) A  0.16 (±0.06) A  2.65 (±0.99) B   Bombus vosnesenskii  0 A  0.17 (±0.06) B  0 AB  0.09 (±0.04) AB  0 A  0 A   Ceratina acantha  0.02 (±0.02)  0.06 (±0.04)  0  0  0  0.02 (±0.02)   C. tejonensis  0  0.02 (±0.02)  0  0  0  0   Xylocopa tabaniformis orpifex  0  0.02 (±0.02)  0  0  0  0  Colletidae   Hylaeus bisinuatus  0  0  0  0  0  0.02 (±0.02)   Hy. mesillae  0 A  0 A  0 A  0.11 (±0.05) AB  0.02 (±0.02) A  0.18 (±0.06) B  Halictidae   Halictus farinosus  0  0  0  0  0  0.07 (±0.04)   Ha. ligatus  0.02 (±0.02) AB  0.02 (±0.02) AB  0 A  0.31 (±0.12) BC  0.07 (±0.04) AB  0.62 (±0.15) C   Ha. tripartitus  0.03 (±0.02) AB  0.43 (±0.10) CD  0.07 (±0.05) AC  0.36 (±0.10) BD  0.16 (±0.07) BC  0.15 (±0.05) BC   Lasioglossum (Dialictus) spp.  0.08 (±0.03) A  1.23 (±0.27) B  0.27 (±0.12) A  0.47 (±0.11) AB  0.24 (±0.07) A  0.44 (±0.12) AB   L. (Evylaeus) spp.  0 A  0.11 (±0.04) B  0 A  0.02 (±0.02) AB  0 A  0.02 (±0.02) A   L. incompletum  0.05 (±0.03) A  0.48 (±0.10) C  0.11 (±0.05) AB  0.40 (±0.12) BC  0.05 (±0.03) A  0.18 (±0.06) AB   L. tegulariforme  0 B  0.02 (±0.02) AB  0 AB  0.11 (±0.05) A  0.02 (±0.02) AB  0.09 (±0.06) AB   Sphecodes sp.  0  0  0  0  0  0.04 (±0.04)  Megachilidae   Heriades occidentalis  0  0  0  0.04 (±0.03)  0  0  Wild bees   Total  0.18 (±0.05) A  2.63 (±0.42) C  0.44 (±0.15) AB  1.91 (±0.30) C  0.56 (±0.13) A  1.82 (±0.34) BC   Richness  5 A  11 B  3 A  9 B  6 A  11 B   Shannon (H′)  1.42 A  1.59 B  0.94 A  1.89 B  1.44 A  1.87 B  Genus/species  Phacelia tanacetifolia  Ammi majus  Daucus carota  Weeds  Flowers  Weeds  Flowers  Weeds  Flowers  Andrenidae   Andrena w-scripta  0  0.09 (±0.05)  0  0  0  0  Apidae   Apis mellifera  0.02 (±0.02) A  5.83 (±0.68) C  0 A  0.07 (±0.04) A  0.16 (±0.06) A  2.65 (±0.99) B   Bombus vosnesenskii  0 A  0.17 (±0.06) B  0 AB  0.09 (±0.04) AB  0 A  0 A   Ceratina acantha  0.02 (±0.02)  0.06 (±0.04)  0  0  0  0.02 (±0.02)   C. tejonensis  0  0.02 (±0.02)  0  0  0  0   Xylocopa tabaniformis orpifex  0  0.02 (±0.02)  0  0  0  0  Colletidae   Hylaeus bisinuatus  0  0  0  0  0  0.02 (±0.02)   Hy. mesillae  0 A  0 A  0 A  0.11 (±0.05) AB  0.02 (±0.02) A  0.18 (±0.06) B  Halictidae   Halictus farinosus  0  0  0  0  0  0.07 (±0.04)   Ha. ligatus  0.02 (±0.02) AB  0.02 (±0.02) AB  0 A  0.31 (±0.12) BC  0.07 (±0.04) AB  0.62 (±0.15) C   Ha. tripartitus  0.03 (±0.02) AB  0.43 (±0.10) CD  0.07 (±0.05) AC  0.36 (±0.10) BD  0.16 (±0.07) BC  0.15 (±0.05) BC   Lasioglossum (Dialictus) spp.  0.08 (±0.03) A  1.23 (±0.27) B  0.27 (±0.12) A  0.47 (±0.11) AB  0.24 (±0.07) A  0.44 (±0.12) AB   L. (Evylaeus) spp.  0 A  0.11 (±0.04) B  0 A  0.02 (±0.02) AB  0 A  0.02 (±0.02) A   L. incompletum  0.05 (±0.03) A  0.48 (±0.10) C  0.11 (±0.05) AB  0.40 (±0.12) BC  0.05 (±0.03) A  0.18 (±0.06) AB   L. tegulariforme  0 B  0.02 (±0.02) AB  0 AB  0.11 (±0.05) A  0.02 (±0.02) AB  0.09 (±0.06) AB   Sphecodes sp.  0  0  0  0  0  0.04 (±0.04)  Megachilidae   Heriades occidentalis  0  0  0  0.04 (±0.03)  0  0  Wild bees   Total  0.18 (±0.05) A  2.63 (±0.42) C  0.44 (±0.15) AB  1.91 (±0.30) C  0.56 (±0.13) A  1.82 (±0.34) BC   Richness  5 A  11 B  3 A  9 B  6 A  11 B   Shannon (H′)  1.42 A  1.59 B  0.94 A  1.89 B  1.44 A  1.87 B  For each species or genus, values that share the same letter are not significantly different. Values that are not followed by letters were not analyzed due to insufficient abundance. View Large Variable response to the flowers across taxa is possibly explained by a mismatch between flower phenology and seasonal bee activity periods. For instance, some of the bee species collected in this study tend to fly more frequently in the early spring, such as B. vosnesenskii and Lasioglossum spp. (Thorp et al. 1983, Michener 2007), whereas other taxa like Hy. mesillae and Ha. ligatus are known to come out later in the season (Snelling 1970, Michener and Bennett 1977), while still others like A. mellifera maintain activity throughout the crop year (Seeley 2009). Such differences could result in specific flowers receiving more or less visitation from a given bee species, not because of any specific preference for one flowering cover crop species over another, but rather simply due to overlap (or lack thereof) in flower phenology and primary activity period. Alternately, variable bee response to the flowering cover crops could be the result of changes in the composition and quality of resident weedy vegetation over the course of the season. It may be that during certain periods of the year flowering resident weedy vegetation provided floral resources equivalent to the flowering cover crops and thereby diluted their attractiveness to the wild bees collected in this study, many of which are considered polylectic (Michener 2007). This is probably unlikely though, as most of the resident weedy vegetation recorded in this study did not produce a prolific bloom and none are considered to be great bee attractors. Furthermore, abundance of all bee taxa on the resident weedy vegetation was uniformly low across the entire study period. Finally, incompatibility between bee and flower morphology may have influenced visitation (Campbell et al. 2012). While some bee species did appear to concentrate either on P. tanacetifolia or A. majus and D. carota (Table 2), the latter two having very similar flower morphologies, this response did not correlate with body size or tongue length. For instance, taxa of varying sizes and tongue lengths, such as B. vosnesenskii and Lasioglossum spp., both responded to P. tanacetifolia, while A. mellifera and Hy. mesillae responded to D. carota. As such, we do not think flower morphology had a strong influence on bee response. Influence of Landscape Diversity While the oak woodland, riparian and chaparral habitats found in the landscape do contain a variety of plant species that are attractive to bees, such as Aesculus californica (Spach) Nutt. (Sapindales: Hippocastanaceae), Arctostaphylos spp. (Ericales: Ericaceae), Baccharis pilularis DC. (Asterales: Asteraceae), Ceanothus spp. (Rhamnales: Rhamnaceae), and Heteromeles arbutifolia (Lindl.) M. Roem. (Rosales: Rosaceae), changes in landscape diversity did not have any influence on vineyard bee populations nor did it mediate their response to the flowering cover crops. This is in line with the only other study to evaluate vineyard bee populations in northern California, which found that changes in the area of oak woodland within 1 km of vineyards did not have any influence on Bombus spp. densities (LeBuhn and Fenter 2008). Yet more generally, these findings are in contrast to a majority of studies that have shown that increased distance away from natural habitats frequently tends to have a negative influence on wild bee populations (Ricketts et al. 2008, Garibaldi et al. 2013, Kennedy et al. 2013) and that bee response to local changes in management or habitat diversity can be influenced by landscape context (Rundlöf and Smith 2006, Batáry et al. 2011). Insect response to changes in local and landscape diversity varies by species (Steffan-Dewenter et al. 2002, Duelli and Obrist 2003) and is likely related to the life-history requirements, dispersal capacity and foraging range of the focal organism (With and Crist 1995, Tscharntke et al. 2002). The presence of undisturbed patches of natural habitat is so critical to wild bees because many species are soil- and cavity-nesters that are sensitive to soil disturbance and loss of woody perennial habitat associated with agriculture. Yet in perennial cropping systems, such as grapes, the landscape may play a less critical role in supporting on-farm bee populations due to the relatively minimal tillage that takes place in vineyards compared to annual, tillage intensive crops such as tomato, canola, watermelon and sunflower, where a majority of landscape effects on bees have been observed (Kremen et al. 2004, Greenleaf and Kremen 2006, Bommarco et al. 2012). Such effects are not necessarily exclusive to annual crops though, and there are certainly examples from perennial systems where increased landscape diversity has been shown to positively influence wild bees, including almond (Klein et al. 2012), cherry (Holzschuh et al. 2012) and coffee (Ricketts 2004). Alternately, it may be that the main taxa recovered in this study (Bombus, Halictus, Lasioglossum) are simply very tolerant to disturbance, and more sensitive species present in the region are so tightly linked with natural habitats that they did not show up at all in vineyards, even in high diversity landscapes. Unfortunately, here no collections were made within patches of natural habitat to compare with findings from the vineyards. Finally, it may also be that the wild bees observed in this study experience resource availability in the landscape at different spatial scales (Steffan-Dewenter et al. 2002). In this analysis, landscape diversity was quantified within 0.5 km of study sites, which may possibly over- or under-estimate the availability of natural habitats for bees given that many solitary species are thought to forage within only a few hundred meters of their nesting sites (Eickwort and Ginsberg 1980, Osborne et al. 1999, Greenleaf et al. 2007), while A. mellifera can potentially forage up to several kilometers away from their colony (Visscher and Seeley 1982, Beekman and Ratnieks 2000). Conclusion Summer flowering cover crops attracted an increased diversity, richness and abundance of wild bees in the vineyard relative to resident weedy vegetation while changes in the proportion of natural habitat within 0.5 km of the vineyard had no effect. In the future, characterization of wild bee populations in these natural habitats, as well as closer evaluation of bee movement between natural and cultivated areas, could provide further insight into the relationship between landscape diversity and vineyard bee populations. Furthermore, more frequent sampling of bees on ground covers and other flowering plants in and around vineyards (i.e., not just when cover crops are in bloom) could contribute new information on seasonal population dynamics relative to changes in resource availability. In vineyards, habitat restoration and the use of summer flowering cover crops in particular has typically emphasized biological control of crop pests (Nicholls et al. 2000, Berndt et al. 2006, Irvin et al. 2016) because cultivated grapes are hermaphroditic and do not have an obligate relationship with pollinators, although it has been noted that insect pollination may lead to increased berry size and quality (McGregor 1976). For the most part, wine grape growers have expressed interest in pollinator conservation not out of concern for crop productivity, but rather as part of a broader vineyard and regional sustainability and conservation agenda (Broome and Warner 2008, Lubell et al. 2010). While habitat provision for pollinators within vineyards may not be critical for crop production, this practice could lead to added crop value as a result of increased consumer perceptions of environmental quality associated with farming practices that support biodiversity conservation (Warner 2007, Delmas and Grant 2014). Furthermore, improving the permeability of the agricultural matrix through provision of on-farm resources for pollinators can reduce the functional distance between patches of natural habitat and ultimately support conservation of natural systems through improved pollination of wild plants. 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Summer Flowering Cover Crops Support Wild Bees in Vineyards

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Abstract

Abstract Agricultural expansion and intensification negatively affect pollinator populations and has led to reductions in pollination services across multiple cropping systems. As a result, growers and researchers have utilized the restoration of local and landscape habitat diversity to support pollinators, and wild bees in particular. Although a majority of studies to date have focussed on effects in pollinator-dependent crops such as almond, tomato, sunflower, and watermelon, supporting wild bees in self-pollinated crops, such as grapes, can contribute to broader conservation goals as well as provide other indirect benefits to growers. This study evaluates the influence of summer flowering cover crops and landscape diversity on the abundance and diversity of vineyard bee populations. We showed that diversity and abundance of wild bees were increased on the flowering cover crop, but were unaffected by changes in landscape diversity. These findings indicate that summer flowering cover crops can be used to support wild bees and this could be a useful strategy for grape growers interested in pollinator conservation as part of a broader farmscape sustainability agenda. Through pollination, bees (Apoidea) provide an important ecosystem service that supports both agricultural crops and wild plants. Approximately one-third of the total volume of global food production comes from pollinator-dependent crops (McGregor 1976, Williams 1994, Morse and Calderone 2000, Klein et al. 2007). While a majority of crop pollination is carried out by Apis mellifera L. (Hymenoptera: Apidae), both feral and managed (Delaplane et al. 2000), non-Apis wild bees also make substantial contributions (Parker et al. 1987, Westerkamp and Gottsberger 2000, Klein et al. 2007). In some cases, wild bees have even been shown to be individually more effective pollinators than honey bees (Bosch and Marina 1994, Javorek et al. 2002, Kremen et al. 2002, Greenleaf and Kremen 2006, Winfree et al. 2008). A majority of wild flowering plants also rely heavily on animal pollinators and wild bees, in particular (Kearns et al. 1998, Ollerton et al. 2011, Buchmann and Nabhan 2012). While the relationship between many wild flowering plants and their pollinators is not always obligate (Waser et al. 1996), reductions in the abundance or functional diversity of wild bees are generally linked to declines in wild plant communities (Fontaine et al. 2005, Biesmeijer et al. 2006). In this way, wild bee populations are critical to both agricultural production and the conservation and restoration of natural habitats (Allen-Wardell et al. 1998). It is well established that pollinator populations are in decline globally (Kearns et al. 1998, Steffan-Dewenter et al. 2005, National Research Council 2007, Potts et al. 2010). While losses of A. mellifera have been attributed to a combination of biotic and abiotic stressors (e.g., pathogens, parasites, malnutrition, pesticide exposure) (Cox-Foster et al. 2007, Ellis et al. 2010, Neumann and Carreck 2010, Goulson et al. 2015, Woodcock et al. 2017), the dominant factor affecting wild bees has been habitat loss (Steffan-Dewenter et al. 2002, Brown and Paxton 2009, Winfree et al. 2009, Nicolson and Wright 2017). As such, a relationship exists between habitat loss, wild bee declines and reduced pollination of both crops (Richards 2001, Ricketts et al. 2008, Garibaldi et al. 2013) and wild plants (Aguilar et al. 2006). Agricultural expansion is the largest driver of natural habitat loss (Foley et al. 2005). Within agroecosystems, monocrop practices further reduce the availability of resources for pollinators (e.g., flowering weeds), while the use of agrichemicals can directly affect pollinators within natural habitats (e.g., pesticide drift, nutrient runoff) (Kennedy et al. 2013, Nicholls and Altieri 2013, Woodcock et al. 2017). Yet agricultural habitats, when managed with biodiversity in mind, do have significant conservation and functional potential (Green et al. 2005, Norris 2008, Tscharntke et al. 2012). Increased local and landscape habitat diversity has been shown to increase a variety of ecosystem services to agriculture, including crop pollination (Kremen and Miles 2012, Isbell et al. 2017, Lichtenberg et al. 2017). Diversified cropping systems can also contribute to off-farm biodiversity conservation by improving matrix quality and connectivity between patches of natural habitat (Scherr and McNeely 2008, Perfecto and Vandermeer 2010). In vineyards, many grape growers are experimenting with the use of hedgerows and cover crops to enhance a variety of ecosystem services (Altieri et al. 2005, Fiedler et al. 2008, Gurr et al. 2017), including conservation of pollinators (James et al. 2014). Since Vitis vinifera L. (Vitales: Vitaceae) are self-pollinating, interest in vineyard bee populations has been driven not by concerns over crop productivity or quality, but rather by the intrinsic value of pollinators themselves and the supporting ecosystem services they provide to surrounding natural habitats, such as pollination of wild plants (Kleijn et al. 2015). The use of on-farm habitat provisioning to support bee populations has been studied in a variety of pollinator-dependent cropping systems, such as almond, watermelon, and tomato, but little is known about bee response to these practices in self-pollinated crops, such as grapes. This study evaluates bee response to the use of a summer flowering cover crop that was developed as part of a larger ecologically based pest management program in California’s North Coast wine grape region (Wilson et al. 2017). Materials and Methods Study Sites Over a 2-yr period, paired plots with and without summer flowering cover crops were evaluated at 10 vineyard sites. Experimental blocks >0.8 hectares (2 acres) were located in commercial vineyards in Napa and Sonoma County, California, United States. Vineyards were located on level ground and composed of vines that were at least 5 yr old. All cultivars were red grape varieties (Cabernet Sauvignon, Zinfandel, and Merlot). Each experimental block consisted of 60 vine rows with 50–80 vines per row. Blocks were divided into two, equal-sized plots, and each plot was then randomly assigned to either a control or flowering cover crop treatment. In each plot, all samples were taken from the five middle vine rows. Within each of the five sample rows, no measurements were taken from the first or last 10 vines. There were eight sites in year 1 and two sites in year 2. Each site was a replicate with a block containing two plots, one with and one without the flowering cover crops. Flowering Cover Crop Treatment The flowering cover crop treatment consisted of Phacelia tanacetifolia Benth. (Solanales: Boraginaceae) (purple tansy), Ammi majus L. (Apiales: Apiaceae) (Bishop’s flower), and Daucus carota L. (Apiales: Apiaceae) (wild carrot) sown together in alternate row middles. These flower species have an overlapping bloom sequence (P. tanacetifolia, A. majus and D. carota bloom April–May, May–June, and July–September, respectively) and are compatible with standard vineyard management practices, which requires that flowers do not need any supplemental irrigation and can be sown in the fall. In October or November, row middles were tilled, and flowers then sown 0.32–0.64 cm deep (1/8–1/4 inch) using a compact seed drill. P. tanacetifolia, A. majus, and D. carota were sown at a rate of 2.2 kg/ha (2 lbs/acre), 0.56 kg/ha (0.5 lbs/acre), and 0.56 kg/ha (0.5 lbs/acre), respectively. The flowers relied on winter/spring rains (October–April) to establish. In the spring, alternate rows of weedy vegetation were tilled under in both treatment and control plots, thereby leaving treatment plots with an alternating set of row middles sown to the flowering cover crops and control plots with an alternating set of row middles with resident weedy vegetation. Resident weedy vegetation primarily consisted of Ipomoea purpurea (L.) Roth (Solanales: Convolvulaceae) (morning glory), Euphorbia spp. (Euphorbiales: Euphorbiaceae) (spurges), Malva parviflora L. (Malvales: Malvaceae) (cheeseweed), Erodium spp. (Geraniales: Geraniaceae) (filaree), and Polygonum arenastrum Boreau (Polygonales: Polygonaceae) (knotweed). Landscape Diversity Metrics Vineyards in this study were situated along a continuum of low to high diversity landscapes, quantified as the proportion of natural habitat within 0.5 km of the vineyard site. In order to do this, ‘rangeland cover type’ was first extracted from the CalVeg dataset (USDA 2013) using ArcGIS 10.1 (ESRI, Redlands, United States). There were 71 possible values for rangeland cover type (Shiflet 1994) and the total area of each type was calculated within a 0.5 km radius around every vineyard. Cover types were then consolidated into five categories: ‘natural habitat’, ‘agriculture’, ‘development’, ‘water’, and ‘no data’. The ‘natural habitat’ category consisted primarily of riparian, oak woodland, and chaparral habitats while the ‘agriculture’ category was almost entirely vineyard. ‘Development’ included all commercial and residential areas, including urban vegetative landscaping. For this analysis, ‘landscape diversity’ is defined as the proportion of ‘natural habitat’ within 0.5 km of the study site. Sampling Bee Populations on Ground Covers Sweep-nets were used to collect bees from ground covers in all plots. Samples were collected from the flowers in the treatment plots and from the resident weedy vegetation in the control plots during peak bloom of P. tanacetifolia, A. majus, and D. carota, which occurred on 22 April, 14 June, and 2 August in 2012 and on 20 April, 30 May, and 25 July in 2013, respectively. During each bloom period, bees were sampled from the ground covers between 10:00 and 14:00 hr using a 30.5 cm diameter sweep-net. In each plot on each sample date, sweep-net sampling consisted of five sets of 30 unidirectional sweeps. All bees were transferred to plastic freezer bags and brought to the laboratory for identification. Bees were identified to species when possible; however, not all of the bees collected in this study have been described to the species level. Bees in the genus Sphecodes could not be identified to species. Bees in the genus Lasioglossum and subgenera Dialictus and Evylaeus were identified to morphospecies, but were grouped at the subgenus level for analysis. Statistical Analysis Diversity of wild bees on the ground covers was quantified using the Shannon index (H′): H′ = −∑(Pi × ln Pi), where Pi is the proportion of individuals in the ith species in the dataset. Higher H′ values indicate greater community diversity. Data on bee abundance, richness, and diversity were evaluated with generalized linear mixed-effects models using a Gaussian distribution and identity-link function. Model comparison (χ2 tests) was then used to evaluate the influence of main effects against a reduced (null) model. To meet the assumption of normality, all of the bee abundance data were log(x + 1) transformed. All analyses were conducted with the ‘lme4’ package in R and post-hoc Tukey contrasts (‘glht’ function in the ‘multcomp’ package) were used to make comparisons between multiple factors (Bates et al. 2015, R Core Team 2016). Bee response to the flowering cover crops and changes in landscape diversity was evaluated with models that included the main effects ‘landscape diversity’ (i.e., proportion of natural habitat within 0.5 km of the study site) and ‘ground cover type’ (i.e., flowering cover crop or resident weedy vegetation). Landscape mediation of flowering cover crop effects was analyzed by evaluating whether differences in bee abundance, richness, and diversity between plots with and without flowering cover crops were more or less pronounced in certain landscapes. For each response variable tested, the difference in values between the treatment and control plot at each site was calculated. These differences were then evaluated as the response variable in a model that included both a linear and nonlinear term (i.e., a quadratic, second-order polynomial) for the main effect ‘landscape diversity’. All analyses included the random effect ‘bloom period’ (i.e., peak bloom of P. tanacetifolia, A. majus, or D. carota) nested within ‘site’ nested within ‘year’. Results We collected a total of 538 A. mellifera and 420 wild bees across five families and nine genera. Total abundance and diversity of wild bees were increased on all three species of flowering cover crop (Table 1). Densities of some bee species or genera were increased only on specific flowers, while others responded to multiple flower species (Table 2, Fig. 1). More specifically, increased density of Bombus vosnesenskii Radoszkowski (Hymenoptera: Apidae), Lasioglossum (Dialictus) spp. (Hymenoptera: Halictidae), L. (Evylaeus) spp. (Hymenoptera: Halictidae), and L. incompletum (Crawford) (Hymenoptera: Halictidae) was observed only on P. tanacetifolia while Hylaeus mesillae (Cockerell) (Hymenoptera: Colletidae) abundance was increased only on D. carota. Alternately, there was greater abundance of A. mellifera on P. tanacetifolia and D. carota, Halictus tripartitus Cockerell (Hymenoptera: Halictidae) on P. tanacetifolia and A. majus, and Ha. ligatus Say (Hymenoptera: Halictidae) on A. majus and D. carota. Finally, Ha. farinosus Smith (Hymenoptera: Halictidae) and L. tegulariforme (Crawford) (Hymenoptera: Halictidae) did not respond to any of the flowering cover crops and densities of Andrena w-scripta Viereck (Hymenoptera: Andrenidae), Ceratina acantha Provancher (Hymenoptera: Apidae), C. tejonensis Cresson (Hymenoptera: Apidae), Heriades occidentalis Michener (Hymenoptera: Megachilidae), Hy. bisunatus Forster (Hymenoptera: Colletidae), Sphecodes sp. (Hymenoptera: Halictidae), and Xylocopa tabaniformis orpifex Smith (Hymenoptera: Apidae) were all too low for statistical analysis. Fig. 1. View largeDownload slide Abundance of wild bees on the ground covers during peak bloom of each flowering cover crop species. Fig. 1. View largeDownload slide Abundance of wild bees on the ground covers during peak bloom of each flowering cover crop species. Changes in landscape diversity did not have any effect on densities of A. mellifera or wild bees nor on overall wild bee diversity (Table 1). Furthermore, differences in wild bee density and diversity between plots with and without flowering cover crops was not mediated in any way by changes in landscape diversity (Table 1). Table 1. Influence of flowering cover crops and landscape diversity on bee density, richness and diversity Organism  Flowers  Landscape  Mediation Effect  Andrenidae   Andrena w-scripta  –  –  –  Apidae         Apis mellifera  290.73***  1.87  0.80   Bombus vosnesenskii  28.40***  0.05  0.01   Ceratina acantha  4.64  1.08  1.89   C. tejonensis  –  –  –   Xylocopa tabaniformis orpifex  –  –  –  Colletidae         Hylaeus bisinuatus  –  –  –   Hy. mesillae  25.57***  2.24  0.02  Halictidae         Halictus farinosus  –  –  –   Ha. ligatus  49.38***  2.47  2.05   Ha. tripartitus  32.54***  0.54  0.16   Lasioglossum (Dialictus) spp.  47.54***  0.14  1.04   L. (Evylaeus) spp.  20.66***  0.01  0.51   L. incompletum  37.02***  1.64  0.02   L. tegulariforme  13.26*  0.67  0.16   Sphecodes sp.  –  –  –  Megachilidae   Heriades occidentalis  –  –  –  Wild Bees   Total  111.44***  0.47  0.04   Richness  100.13***  1.03  0.03   Shannon (H’)  81.12***  0.84  0.05  Organism  Flowers  Landscape  Mediation Effect  Andrenidae   Andrena w-scripta  –  –  –  Apidae         Apis mellifera  290.73***  1.87  0.80   Bombus vosnesenskii  28.40***  0.05  0.01   Ceratina acantha  4.64  1.08  1.89   C. tejonensis  –  –  –   Xylocopa tabaniformis orpifex  –  –  –  Colletidae         Hylaeus bisinuatus  –  –  –   Hy. mesillae  25.57***  2.24  0.02  Halictidae         Halictus farinosus  –  –  –   Ha. ligatus  49.38***  2.47  2.05   Ha. tripartitus  32.54***  0.54  0.16   Lasioglossum (Dialictus) spp.  47.54***  0.14  1.04   L. (Evylaeus) spp.  20.66***  0.01  0.51   L. incompletum  37.02***  1.64  0.02   L. tegulariforme  13.26*  0.67  0.16   Sphecodes sp.  –  –  –  Megachilidae   Heriades occidentalis  –  –  –  Wild Bees   Total  111.44***  0.47  0.04   Richness  100.13***  1.03  0.03   Shannon (H’)  81.12***  0.84  0.05  The table shows χ2 values from generalized linear mixed-effects models. Some organisms were not analyzed due to insufficient abundance. For each response variable in the ‘mediation effect’ analysis, the difference between the treatment and control plot at each site was evaluated with a model that included both a linear and non-linear term (i.e., polynomial) for the main effect ‘landscape diversity’. *P < 0.05, **P < 0.01, ***P < 0.001. View Large Discussion Bee Response to the Flowering Cover Crops In this study, diversity and abundance of wild bees were increased on the summer flowering cover crops relative to resident weedy vegetation. These findings are consistent with multiple studies that have documented a positive relationship between increased on-farm habitat diversity and wild bee abundance, richness and/or diversity (Saunders et al. 2013, Blaauw and Isaacs 2014, Kremen and M’Gonigle 2015, Isbell et al. 2017, Lichtenberg et al. 2017). Positive response of wild bees to the presence of floral resources in vineyards is not unexpected. Even when no significant differences were observed or densities were too low for statistical evaluation, bee abundance on the flowering cover crops was almost always elevated relative to the resident weedy vegetation (Table 2), although not all bees responded equally to all three species of flowering cover crop. Table 2. Summary of bees collected from the flowering cover crop and resident weedy vegetation (mean ± SEM) during peak bloom of each flower species Genus/species  Phacelia tanacetifolia  Ammi majus  Daucus carota  Weeds  Flowers  Weeds  Flowers  Weeds  Flowers  Andrenidae   Andrena w-scripta  0  0.09 (±0.05)  0  0  0  0  Apidae   Apis mellifera  0.02 (±0.02) A  5.83 (±0.68) C  0 A  0.07 (±0.04) A  0.16 (±0.06) A  2.65 (±0.99) B   Bombus vosnesenskii  0 A  0.17 (±0.06) B  0 AB  0.09 (±0.04) AB  0 A  0 A   Ceratina acantha  0.02 (±0.02)  0.06 (±0.04)  0  0  0  0.02 (±0.02)   C. tejonensis  0  0.02 (±0.02)  0  0  0  0   Xylocopa tabaniformis orpifex  0  0.02 (±0.02)  0  0  0  0  Colletidae   Hylaeus bisinuatus  0  0  0  0  0  0.02 (±0.02)   Hy. mesillae  0 A  0 A  0 A  0.11 (±0.05) AB  0.02 (±0.02) A  0.18 (±0.06) B  Halictidae   Halictus farinosus  0  0  0  0  0  0.07 (±0.04)   Ha. ligatus  0.02 (±0.02) AB  0.02 (±0.02) AB  0 A  0.31 (±0.12) BC  0.07 (±0.04) AB  0.62 (±0.15) C   Ha. tripartitus  0.03 (±0.02) AB  0.43 (±0.10) CD  0.07 (±0.05) AC  0.36 (±0.10) BD  0.16 (±0.07) BC  0.15 (±0.05) BC   Lasioglossum (Dialictus) spp.  0.08 (±0.03) A  1.23 (±0.27) B  0.27 (±0.12) A  0.47 (±0.11) AB  0.24 (±0.07) A  0.44 (±0.12) AB   L. (Evylaeus) spp.  0 A  0.11 (±0.04) B  0 A  0.02 (±0.02) AB  0 A  0.02 (±0.02) A   L. incompletum  0.05 (±0.03) A  0.48 (±0.10) C  0.11 (±0.05) AB  0.40 (±0.12) BC  0.05 (±0.03) A  0.18 (±0.06) AB   L. tegulariforme  0 B  0.02 (±0.02) AB  0 AB  0.11 (±0.05) A  0.02 (±0.02) AB  0.09 (±0.06) AB   Sphecodes sp.  0  0  0  0  0  0.04 (±0.04)  Megachilidae   Heriades occidentalis  0  0  0  0.04 (±0.03)  0  0  Wild bees   Total  0.18 (±0.05) A  2.63 (±0.42) C  0.44 (±0.15) AB  1.91 (±0.30) C  0.56 (±0.13) A  1.82 (±0.34) BC   Richness  5 A  11 B  3 A  9 B  6 A  11 B   Shannon (H′)  1.42 A  1.59 B  0.94 A  1.89 B  1.44 A  1.87 B  Genus/species  Phacelia tanacetifolia  Ammi majus  Daucus carota  Weeds  Flowers  Weeds  Flowers  Weeds  Flowers  Andrenidae   Andrena w-scripta  0  0.09 (±0.05)  0  0  0  0  Apidae   Apis mellifera  0.02 (±0.02) A  5.83 (±0.68) C  0 A  0.07 (±0.04) A  0.16 (±0.06) A  2.65 (±0.99) B   Bombus vosnesenskii  0 A  0.17 (±0.06) B  0 AB  0.09 (±0.04) AB  0 A  0 A   Ceratina acantha  0.02 (±0.02)  0.06 (±0.04)  0  0  0  0.02 (±0.02)   C. tejonensis  0  0.02 (±0.02)  0  0  0  0   Xylocopa tabaniformis orpifex  0  0.02 (±0.02)  0  0  0  0  Colletidae   Hylaeus bisinuatus  0  0  0  0  0  0.02 (±0.02)   Hy. mesillae  0 A  0 A  0 A  0.11 (±0.05) AB  0.02 (±0.02) A  0.18 (±0.06) B  Halictidae   Halictus farinosus  0  0  0  0  0  0.07 (±0.04)   Ha. ligatus  0.02 (±0.02) AB  0.02 (±0.02) AB  0 A  0.31 (±0.12) BC  0.07 (±0.04) AB  0.62 (±0.15) C   Ha. tripartitus  0.03 (±0.02) AB  0.43 (±0.10) CD  0.07 (±0.05) AC  0.36 (±0.10) BD  0.16 (±0.07) BC  0.15 (±0.05) BC   Lasioglossum (Dialictus) spp.  0.08 (±0.03) A  1.23 (±0.27) B  0.27 (±0.12) A  0.47 (±0.11) AB  0.24 (±0.07) A  0.44 (±0.12) AB   L. (Evylaeus) spp.  0 A  0.11 (±0.04) B  0 A  0.02 (±0.02) AB  0 A  0.02 (±0.02) A   L. incompletum  0.05 (±0.03) A  0.48 (±0.10) C  0.11 (±0.05) AB  0.40 (±0.12) BC  0.05 (±0.03) A  0.18 (±0.06) AB   L. tegulariforme  0 B  0.02 (±0.02) AB  0 AB  0.11 (±0.05) A  0.02 (±0.02) AB  0.09 (±0.06) AB   Sphecodes sp.  0  0  0  0  0  0.04 (±0.04)  Megachilidae   Heriades occidentalis  0  0  0  0.04 (±0.03)  0  0  Wild bees   Total  0.18 (±0.05) A  2.63 (±0.42) C  0.44 (±0.15) AB  1.91 (±0.30) C  0.56 (±0.13) A  1.82 (±0.34) BC   Richness  5 A  11 B  3 A  9 B  6 A  11 B   Shannon (H′)  1.42 A  1.59 B  0.94 A  1.89 B  1.44 A  1.87 B  For each species or genus, values that share the same letter are not significantly different. Values that are not followed by letters were not analyzed due to insufficient abundance. View Large Variable response to the flowers across taxa is possibly explained by a mismatch between flower phenology and seasonal bee activity periods. For instance, some of the bee species collected in this study tend to fly more frequently in the early spring, such as B. vosnesenskii and Lasioglossum spp. (Thorp et al. 1983, Michener 2007), whereas other taxa like Hy. mesillae and Ha. ligatus are known to come out later in the season (Snelling 1970, Michener and Bennett 1977), while still others like A. mellifera maintain activity throughout the crop year (Seeley 2009). Such differences could result in specific flowers receiving more or less visitation from a given bee species, not because of any specific preference for one flowering cover crop species over another, but rather simply due to overlap (or lack thereof) in flower phenology and primary activity period. Alternately, variable bee response to the flowering cover crops could be the result of changes in the composition and quality of resident weedy vegetation over the course of the season. It may be that during certain periods of the year flowering resident weedy vegetation provided floral resources equivalent to the flowering cover crops and thereby diluted their attractiveness to the wild bees collected in this study, many of which are considered polylectic (Michener 2007). This is probably unlikely though, as most of the resident weedy vegetation recorded in this study did not produce a prolific bloom and none are considered to be great bee attractors. Furthermore, abundance of all bee taxa on the resident weedy vegetation was uniformly low across the entire study period. Finally, incompatibility between bee and flower morphology may have influenced visitation (Campbell et al. 2012). While some bee species did appear to concentrate either on P. tanacetifolia or A. majus and D. carota (Table 2), the latter two having very similar flower morphologies, this response did not correlate with body size or tongue length. For instance, taxa of varying sizes and tongue lengths, such as B. vosnesenskii and Lasioglossum spp., both responded to P. tanacetifolia, while A. mellifera and Hy. mesillae responded to D. carota. As such, we do not think flower morphology had a strong influence on bee response. Influence of Landscape Diversity While the oak woodland, riparian and chaparral habitats found in the landscape do contain a variety of plant species that are attractive to bees, such as Aesculus californica (Spach) Nutt. (Sapindales: Hippocastanaceae), Arctostaphylos spp. (Ericales: Ericaceae), Baccharis pilularis DC. (Asterales: Asteraceae), Ceanothus spp. (Rhamnales: Rhamnaceae), and Heteromeles arbutifolia (Lindl.) M. Roem. (Rosales: Rosaceae), changes in landscape diversity did not have any influence on vineyard bee populations nor did it mediate their response to the flowering cover crops. This is in line with the only other study to evaluate vineyard bee populations in northern California, which found that changes in the area of oak woodland within 1 km of vineyards did not have any influence on Bombus spp. densities (LeBuhn and Fenter 2008). Yet more generally, these findings are in contrast to a majority of studies that have shown that increased distance away from natural habitats frequently tends to have a negative influence on wild bee populations (Ricketts et al. 2008, Garibaldi et al. 2013, Kennedy et al. 2013) and that bee response to local changes in management or habitat diversity can be influenced by landscape context (Rundlöf and Smith 2006, Batáry et al. 2011). Insect response to changes in local and landscape diversity varies by species (Steffan-Dewenter et al. 2002, Duelli and Obrist 2003) and is likely related to the life-history requirements, dispersal capacity and foraging range of the focal organism (With and Crist 1995, Tscharntke et al. 2002). The presence of undisturbed patches of natural habitat is so critical to wild bees because many species are soil- and cavity-nesters that are sensitive to soil disturbance and loss of woody perennial habitat associated with agriculture. Yet in perennial cropping systems, such as grapes, the landscape may play a less critical role in supporting on-farm bee populations due to the relatively minimal tillage that takes place in vineyards compared to annual, tillage intensive crops such as tomato, canola, watermelon and sunflower, where a majority of landscape effects on bees have been observed (Kremen et al. 2004, Greenleaf and Kremen 2006, Bommarco et al. 2012). Such effects are not necessarily exclusive to annual crops though, and there are certainly examples from perennial systems where increased landscape diversity has been shown to positively influence wild bees, including almond (Klein et al. 2012), cherry (Holzschuh et al. 2012) and coffee (Ricketts 2004). Alternately, it may be that the main taxa recovered in this study (Bombus, Halictus, Lasioglossum) are simply very tolerant to disturbance, and more sensitive species present in the region are so tightly linked with natural habitats that they did not show up at all in vineyards, even in high diversity landscapes. Unfortunately, here no collections were made within patches of natural habitat to compare with findings from the vineyards. Finally, it may also be that the wild bees observed in this study experience resource availability in the landscape at different spatial scales (Steffan-Dewenter et al. 2002). In this analysis, landscape diversity was quantified within 0.5 km of study sites, which may possibly over- or under-estimate the availability of natural habitats for bees given that many solitary species are thought to forage within only a few hundred meters of their nesting sites (Eickwort and Ginsberg 1980, Osborne et al. 1999, Greenleaf et al. 2007), while A. mellifera can potentially forage up to several kilometers away from their colony (Visscher and Seeley 1982, Beekman and Ratnieks 2000). Conclusion Summer flowering cover crops attracted an increased diversity, richness and abundance of wild bees in the vineyard relative to resident weedy vegetation while changes in the proportion of natural habitat within 0.5 km of the vineyard had no effect. In the future, characterization of wild bee populations in these natural habitats, as well as closer evaluation of bee movement between natural and cultivated areas, could provide further insight into the relationship between landscape diversity and vineyard bee populations. Furthermore, more frequent sampling of bees on ground covers and other flowering plants in and around vineyards (i.e., not just when cover crops are in bloom) could contribute new information on seasonal population dynamics relative to changes in resource availability. In vineyards, habitat restoration and the use of summer flowering cover crops in particular has typically emphasized biological control of crop pests (Nicholls et al. 2000, Berndt et al. 2006, Irvin et al. 2016) because cultivated grapes are hermaphroditic and do not have an obligate relationship with pollinators, although it has been noted that insect pollination may lead to increased berry size and quality (McGregor 1976). For the most part, wine grape growers have expressed interest in pollinator conservation not out of concern for crop productivity, but rather as part of a broader vineyard and regional sustainability and conservation agenda (Broome and Warner 2008, Lubell et al. 2010). While habitat provision for pollinators within vineyards may not be critical for crop production, this practice could lead to added crop value as a result of increased consumer perceptions of environmental quality associated with farming practices that support biodiversity conservation (Warner 2007, Delmas and Grant 2014). Furthermore, improving the permeability of the agricultural matrix through provision of on-farm resources for pollinators can reduce the functional distance between patches of natural habitat and ultimately support conservation of natural systems through improved pollination of wild plants. Indirect effects like this are important to highlight in order to promote the value of wild bee conservation in crops that do not have a strong, obligate relationship with pollinators, such as grapes (Kleijn et al. 2015). Acknowledgments This work would not have been possible without the support of many student laboratory assistants at UC Berkeley. We also thank the vineyard managers for use of their farms and access to surrounding natural habitats. This work was supported by grants to H.W. from the Robert Van den Bosch Memorial Scholarship. References Cited Aguilar, R., L. Ashworth, L. Galetto, and Aizen M. A.. 2006. Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol. Lett . 9: 968– 980. Google Scholar CrossRef Search ADS PubMed  Allen-Wardell, G., Bernhardt P., Bitner R., Burquez A., Buchmann S., Cane J., Cox P. A., Dalton V., Feinsinger P., and Ingram M.. 1998. 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