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Surrounding landscape and spatial arrangement of honey bee hives affect pollen foraging and yield in cranberry
Agriculture, Ecosystems and Environment 286 (2019) 106624
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Surrounding landscape and spatial arrangement of honey bee hives affect pollen foraging and yield in cranberry A. Guzmana,1, H.R. Gaines-Daya, A.N. Loisa, S.A. Steffana,b, J. Bruneta,b, J. Zalapaa,b, C. Guédota, a b
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University of Wisconsin-Madison, Madison, WI, 53706, USA Vegetable Crops Research Unit, USDA-ARS, Madison, WI, 53706, USA
A R T I C LE I N FO
A B S T R A C T
Keywords: Apis mellifera Pollen Woodland Vaccinium macrocarpon
Honey bees are the most important managed pollinator in the world. Recent trends suggest, however, that the demand for their pollination services is growing faster than the available supply. Therefore, it is critical to determine the most efficient management practices to maximize their use for crop production. One factor known to influence the efficiency of crop pollination is the availability of alternative, non-crop floral resources. These resources can vary as a function of the landscape surrounding a farm as well as local management practices within a farm. However, little is known about how the foraging behavior of honey bees on the target crop responds to the spatial arrangement of hives or the composition of the surrounding landscape. In this study, we collected pollen from pollen traps on honey bee hives placed on commercial cranberry marshes in central Wisconsin (USA). Individual marshes were selected to fall across a gradient of surrounding landscape from highto low-woodland. Within each marsh, hives were placed either adjacent to wooded habitat, adjacent to a water reservoir, or in the center of the marsh. Honey bees from hives near water reservoirs collected a lower proportion of cranberry pollen than honey bees near the wooded area or at the center of the marsh. However, honey bees collected the same number of cranberry pollen grains and total pollen biomass irrespective of hive location or the surrounding landscape. Honey bees from hives located near water reservoirs, relative to the other two hive locations, tended to collect more pollen from fewer plants (low evenness). Cranberry yield did not vary as a function of the proportion of cranberry pollen collected or total number of cranberry pollen grains collected, but yield was higher at marshes located in low-woodland landscapes relative to those in high-woodland landscapes. We conclude that the location of hives on a cranberry marsh in relation to non-crop habitat does not affect yield allowing growers to place hives where it is convenient, although placing hives near water reservoirs should provide bees with a more diverse pollen diet.
1. Introduction Honey bees (Apis mellifera) are the most widely managed pollinator used in agricultural production, providing pollination services for nearly half of leading global food commodities (Klein et al., 2006; vanEngelsdorp and Meixner, 2010). Commercially managed honey bees are commonly used in agricultural systems because they are generalist foragers, recruit nestmates to floral resources, are managed in large colonies for pollination services, and can be supplied to coincide with crop flowering (Calderone, 2012; Kremen and Chaplin-Kramer, 2007). The agricultural demand for honey bee pollination services is rising, increasing by 50% in developed countries between 1961 and 2006 (Aizen et al., 2009; vanEngelsdorp and Meixner, 2010), while at the same time, the number of managed hives is decreasing (Food and
Agriculture Organization of the United Nations (FAO, 2009; Stokstad, 2007; vanEngelsdorp and Meixner, 2010). These competing trends not only raise the price of pollination services for growers, but suggest that pollinators may become a limiting factor for pollinator-dependent crops going into the future (Aizen and Harder, 2009; vanEngelsdorp and Meixner, 2010). Therefore, a better understanding of the factors that influence the contribution of honey bees to crop pollination is critical. One factor that may influence the pollination efficiency of honey bees is the availability of non-crop flowers in and around a crop field (Blaauw and Isaacs, 2014; Concepción et al., 2012; Morandin and Kremen, 2013; Sardiñas and Kremen, 2015; Vaissière, 1991). On a local on-farm scale, as colony density increases and distance from the nest to the crop decreases, bees forage more on crop plants, resulting in improved yields (Artz et al., 2013; Cunningham et al., 2016; Cunningham
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Corresponding author at: University of Wisconsin-Madison, Department of Entomology, 1630 Linden Drive Madison, WI, 53706, USA. E-mail address: [email protected] (C. Guédot). 1 Current address: University of California-Berkeley, Berkeley, CA 94720, USA. https://doi.org/10.1016/j.agee.2019.106624 Received 23 March 2019; Received in revised form 18 July 2019; Accepted 27 July 2019 Available online 28 August 2019 0167-8809/ © 2019 Elsevier B.V. All rights reserved.
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2. Materials and methods
and Le Feuvre, 2013). However, in some studies, honey bees collected very little, if any, pollen from the target crop (Pettis et al., 2013; Vaissiere, 1991). At a broader scale, the abundance and composition of floral resources in natural or semi-natural habitat surrounding crop fields can also affect the foraging behavior of honey bees (Concepción et al., 2012; Tscharntke et al., 2012). Furthermore, landscapes with more natural habitat may provide a more diverse and nutritious diet to bees and result in better overall bee health (Danner et al., 2016; Donkersley et al., 2014; Pasquale et al. 2013). When alternative resources are present in the landscape, honey bees may preferentially forage on non-crop flowers (Cane and Schiffhauer, 2001; Girard et al., 2012), neglecting the target crop. Cranberry (Vaccinium macrocarpon Aiton, Ericaceae), a fruit crop native to North America, relies on pollinators for fruit production (Delaplane et al., 2000; Eck, 1986; Gaines-Day, 2013; McGregor, 1976). Although honey bees are not the most efficient pollinator on a per visit basis (Cane and Schiffhauer, 2003; MacKenzie, 1994), their large numbers can offset this disparity (Free, 1993; Woodcock et al., 2013). Wisconsin (USA) produces over 60% of the US cranberry crop and nearly all growers use rented honey bee hives for pollination services (Gaines-Day and Gratton, 2016; USDA NASS, 2006). Despite the significant cost of honey bee rentals for cranberry growers ($350-$520 per hectare) (Gaines-Day, 2013; USDA NASS, 2006), honey bee visitation rates to cranberry flowers vary considerably. Indeed in cranberry, honey bees can return to the hive with no cranberry pollen, suggesting that they visited other floral resources (Broussard et al., 2011; Cane and Schiffhauer, 2001; MacKenzie, 1994; Pettis et al., 2013; Shimanuki et al., 1967). To increase visitation to cranberry flowers and subsequent yield, hive densities ranging between 0.25–25 hives per hectare have been suggested (reviewed in Delaplane et al., 2000). In Wisconsin, growers stock their cranberry marshes with, on average, 5–7 hives per hectare (Gaines-Day and Gratton, 2016). Research on how the spatial arrangement of hives within the crop field influences yield, however, is lacking. The location of the hives is important because it determines how accessible non-crop floral resources are to the bees. Theoretically, placing hives far from non-crop habitat should encourage the bees to forage on the crop flower, but previous studies in cranberry have shown that cranberry yield was unaffected by the presence of honey bees or the distance from hive to crop (Kevan et al., 1983) and that the relationship between hive stocking density and yield varies as a function of the surrounding landscape (Gaines-Day and Gratton, 2016). These results also suggest that the honey bees may be visiting alternative floral resources rather than cranberry. Therefore, understanding how these relationships vary as a function of hive location within the cranberry will be valuable for increasing the efficiency of cranberry pollination practices. The objectives of this study were to determine how the foraging of commercial honey bees is influenced by a) the spatial arrangement of hives in relation to adjacent habitats, and b) the composition of habitat in the surrounding landscape (i.e. high- vs. low-woodland). Specifically, we investigated how these factors influenced the amount and percent of cranberry pollen brought back to the hive by honey bees. We also examined how the amount and percent of cranberry pollen brought back to the hive and the surrounding landscape affected yield. We hypothesized that, in high-woodland landscapes, honey bees would forage less on cranberry and return a lower proportion of cranberry pollen to the hive because of the proximity to other non-crop floral resources. We also expected honey bees from hives located in the center of a marsh or near a water reservoir to bring a greater proportion of cranberry pollen back to the hive. The results of this research will increase our understanding of how the hive spatial arrangement and the surrounding landscape influence honey bee behavior in Wisconsin cranberry and will provide recommendations to growers to optimize their pollination services.
2.1. Study site selection and landscape classification This research was conducted in central Wisconsin (USA), the main growing region of cranberries in the world. Wisconsin cranberry marshes are typically embedded within natural ecosystems (Gaines-Day, 2013). Thus, in order to determine the effect of the surrounding landscape composition on cranberry pollen use by honey bees, marshes were selected to span a gradient of high- to low-woodland habitat in the surrounding landscape. For each marsh, we calculated the landscape composition within a 1 km radius using the Cropland Data Layer (CDL) (USDA NASS CDL, 2015) in ArcGIS® (ESRI ArcGIS Desktop, 2011). Land cover was classified into three categories: open semi-natural habitat (grassland, pasture, hay, and herbaceous wetland), woodland habitat (deciduous forest, coniferous forest, mixed forest, wooded wetlands, and shrubland), and other (all remaining CDL categories). We selected ten commercially managed marshes spanning the western edge of the cranberry growing region from Tomah to Black River Falls, Wisconsin, U.S.A., based on the following criteria: 1) the surrounding landscape composed of either more than 60% or less than 40% woodland (GainesDay and Gratton, 2016); 2) the presence of a large water reservoir on the marsh (typical in this growing region); 3) a marsh shape that allowed for the spatial arrangement of a “center” sampling location (i.e., not long and narrow); and 4) the presence of wooded habitat adjacent to at least one side of the marsh. Marshes ranged in size from 4 to 107 ha and each marsh consisted of multiple rectangular beds measuring ˜50 m wide and varying in length.
2.2. Study design Commercial honey bee hives rented by the cranberry growers for pollination were used in this study. Hives were evaluated to meet a minimum health standard by evaluating the area covered with the bee cluster on top of the frames (Nasr et al., 1990) and observing bees returning to the hive. Hives that looked healthy and similar in colony strength were selected. At each of the ten selected marshes, one quad of hives were placed at each of three predetermined locations: (1) near the marsh center (“Center”) which was surrounded by cranberry beds, (2) at the edge of the marsh near a wooded edge (“Woodland habitat”), and (3) at a marsh edge adjacent to a water reservoir (“Water reservoir”). All hive locations within a marsh were at least 300 m apart from each other and as much as 2000 m apart, depending on the size of the marsh. To assess the extent of foraging by honey bees on cranberry flowers, we collected pollen brought back to hives by pollen foragers using pollen traps installed on one hive per location (three hives per marsh). Sampling occurred from June 23 to July 14, 2015 to coincide with cranberry bloom and the arrival of honey bee hives on the marshes. At each hive, a yellow plastic pollen trap (Eco-Keeper Inc., Duluth, GA) was mounted on the front entrance of the hive as soon as hives were delivered to marshes (between 16–20 June), and were left for the entire sampling period. All other holes found on hives were blocked off with tape or cardboard pieces to ensure bees would enter the hive through the pollen trap. The traps were activated for 24 -h collection intervals twice a week for the three week duration of cranberry bloom for a total of six collection periods (n = 180 pollen samples). Pollen samples were collected, returned to the laboratory on ice and stored at −20 °C until processed. Each pollen sample was then freeze-dried at ca. −75 °C in a VirTis Benchtop 4 K freezer dryer (model 4 KBTXL-75; SP Scientific, Warminster, PA, USA) equipped with a Pascal 2005SD vacuum pump (Adixen, Pfeiffer Vacuum, worldwide) for 24–48 hrs. Freeze dried samples were carefully cleaned of all debris (i.e., dead insects and leaf pieces) using tweezers, and a total weight for each pollen sample was recorded.
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using generalized and linear mixed models (GLMMs and LMMs; Bates et al., 2015; Kuznetsova et al., 2017). All models included the interaction effect of landscape and hive location (landscape × location) plus marsh and the interaction of marsh and hive location, to account for the six sampling rounds per hive per marsh, as random effects. The impact of cranberry pollen (proportion and number of cranberry grains) collected by honey bees on cranberry yield was examined using pollen count data aggregated over hive location and sampling round. An interaction term between the cranberry pollen variable and landscape type (high-woodland versus low-woodland landscape) was included as fixed effects. The relationship between farm size and landscape type as well as farm size and yield were assessed. For all yield models, LMMs were used and marsh was included as a random effect. All statistical analyses were performed using the lme4 and lmerTest packages in R (Bates, et al., 2015; Kuzentsova and Rune, 2016; R Core team, 2014). In addition, the significance of the fixed effects of the LMMs was determined by an F-test and the method described by Kenward and Roger (1997) was used to calculate the degrees of freedom. For the significance of the fixed effects in the GLMMs, likelihood ratio tests were used. For count response variables (i.e. proportion), models assumed a Poisson distribution and for continuous variables (i.e. number of pollen grains, pollen weight, and diversity indices), models assumed a Gaussian distribution.
2.3. Pollen composition 2.3.1. Diversity of color morphotypes To assess the diversity of pollen collected by each hive, we categorized pollen bundles by color morphotypes. Samples that were clumped due to water damage could not be separated and were excluded from this analysis. For samples that could be separated (n = 143), pollen bundles were sorted by subtle color differences to the closest match utilizing the Sherwin-Williams color palettes (Girard et al., 2012; Pettis et al., 2013) and the dry weight of each color morphotype per sample was recorded. For each color morphotype across marshes, we collected a small amount of pollen from a pollen bundle with the tip of a needle (equivalent to 1/8 mm3 of pollen according to Girard et al., 2012) and mounted it on a microscope slide with 50-50 glycerin-water solution to identify each color morphotype to a unique pollen morphology. 2.3.2. Cranberry vs. non-cranberry pollen Color morphotypes for each pollen sample were then recombined into a single vial, thoroughly mixed, and crushed with a mortar and pestle. A 0.5 g subsample of each recombined sample was taken (n = 141 samples whose total pollen weight was greater than 0.5 g), and placed into a 5 ml centrifuge tube. Three mL of 50-50 glycerinwater solution was added to the tube, and the solution was mixed thoroughly with a metal spatula until homogenous. For each pollen sample, 11 μl of the solution was pipetted onto a hemocytometer slide (LW Scientific©, Lawrenceville, GA, USA) with a 0.100 mm depth and 0.0025 mm2 area. For each slide, three random 1 mm2 squares were examined under a compound microscope (Reichert Scientific Instruments, Buffalo, NY, USA) and the total number of cranberry (identified by the characteristic tetrad pollen grains) and non-cranberry pollen grains (all others) were recorded. We then took an average of the three counts for each sample. To estimate the total number of cranberry pollen grains in each sample, we multiplied our averaged pollen count by 9 to account for the total number of squares on the slide. Then, we divided by the dilution factor (0.5 g/ 3 ml) and multiplied by the original total weight of the pollen sample to determine the total number of cranberry grains in each hive pollen sample.
3. Results Hive location within the marsh significantly affected the proportion of cranberry pollen collected by hives (df = 2; χ2 = 7.868, P = 0.020; Fig. 1a). Hives near the water reservoir had the lowest proportion of cranberry pollen (mean ± SEM: 0.152 ± 0.093) compared to the other hive locations, and hives in high-woodland landscapes had the lowest proportion of cranberry pollen (0.146 ± 0.112). Landscape type did not significantly affect the proportion of cranberry pollen collected by hives although the effect was marginal (df = 1; χ 2 = 3.260, P = 0.071; Fig. 1b). There was no statistically significant interaction between the effect of landscape type and hive location on the proportion of cranberry pollen collected (df = 2; χ 2 = 2.757, P = 0.252; Fig. 1c). For the total number of cranberry pollen grains collected, neither hive location (F2,16 = 1.779, P = 0.201; Fig. 2a), landscape type (F1,8 = 0.329, P = 0.582; Fig. 2b), nor the interaction between them (F2,16 = 0.161, P = 0.852; Fig. 2c) were statistically significant predictors. The total pollen dry weight per sample ranged from 3.450 g to 10.126 g. There was no statistically significant difference in the total weight of pollen collected by hive location (F2,16 = 1.008, P = 0.387; Fig. 3a), landscape type (F1,8 = 0.036, P = 0.854; Fig. 3b), or the interaction between hive location and landscape type (F2,16 = 2.135, P = 0.151; Fig. 3c). We identified a total of 33 pollen color morphotypes across all pollen samples, with a Shannon diversity index ranging from 0.016 to 1.603 (Table 1). There was no effect of hive location (F2,16 = 0.086, P = 0.918), landscape type (F1,7 = 0.033, P = 0.861), or the interaction between hive location and landscape type (F2,16 = 0.460, P = 0.639) on the Shannon diversity index of non-cranberry pollen morphotypes. Similarly, there was no difference in the number of color morphotypes (i.e. richness) collected by hives regardless of hive location (F2,16 = 1.039, P = 0.377), landscape type (F1,8 = 0.035, P = 0.857), or the interaction of hive location and landscape type (F2,16 = 0.777, P = 0.477; Table 1). The evenness of pollen morphotypes was significantly affected by hive location (F2,16 = 3.624, P = 0.051; Table 1 and Fig. 4a). Honey bees tended to collect pollen more frequently from some plant groups (lower pollen evenness) for hives near the water reservoir (0.301 ± 0.051) than hives in the center (0.446 ± 0.052) or near woodland habitat (0.439 ± 0.051). There was no effect of landscape type (F1,8 = 0.151, P = 0.708) or the interaction between hive location
2.4. Cranberry yield Cranberry yield data for each marsh for the 2015 growing season was provided by each grower as the marsh-wide average. 2.5. Statistical analyses The effect of surrounding landscape (high-woodland vs. lowwoodland) and hive location (center, water reservoir, and woodland habitat) was assessed on the proportion of cranberry pollen grains, the number of cranberry pollen grains, and dry pollen weight (box-cox transformed to meet assumptions of normality), as well as the pollen diversity (i.e. diversity, richness, and evenness) and composition of pollen color morphotypes for non-cranberry pollen. Diversity of the non-cranberry pollen was determined using Shannon diversity index on the weight of each pollen color morphotype. Pollen richness was calculated using the Chao1 estimator, (transformed as natural log + 1). Both measures were calculated using the R package vegan (Oksanen et al., 2013). Evenness of non-cranberry pollen color morphotypes was calculated using the R package fundiv (Evar; samples that had ≤ 1 species were dropped; Smith and Wilson, 1996). Further, to evaluate the differences in the composition of pollen color morphotypes across hive location, landscape type, and their interaction, a permutational multivariate analysis of variance (perMANOVA) with Chao1 dissimilarities in the R package vegan (Okansen et al., 2013) was used. All other analyses were conducted 3
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Fig. 1. Mean proportion of cranberry pollen grains ( ± S.E.) collected in pollen traps from honey bee pollen foragers returning to hives placed at three different onfarm locations (near water reservoir, near center, and near woodland habitat) in two landscape types (high- and low-woodland) at ten marshes.
4. Discussion
and landscape type (F2,16 = 0.994, P = 0.393; Table 1 and Fig. 4a) on the evenness of the pollen morphotype distribution. The composition of pollen morphotypes differed among hive locations (F2,2 = 1.791, P = 0.001; Fig. 4b) and landscape type (F1,1 = 3.123, P = 0.001; Fig. 4c) but there was no interaction between the effects of hive location and landscape type on pollen composition (F2,1 = 1.099, P = 0.238). As the average proportion of cranberry pollen collected increased, the increase in yield was marginal (F1,6 = 5.197, P = 0.063; Fig. 5a), but marshes in low-woodland landscape reported higher yield than those in high-woodland landscape (F1,6 = 8.780, P = 0.025; Fig. 5a). There was no significant interaction between the effect of landscape type and the proportion of cranberry pollen collected on yield (F1,6 = 0.197, P = 0.673; Fig. 5a). There was no significant relationship between the total number of cranberry pollen grains collected by honey bees and yield (F1,6 = 0.915, P = 0.376; Fig. 5b). Rather, there was a significant effect of landscape type on yield (F1,6 = 20.433, P = 0.004) and a marginal effect of the interaction between landscape type and the total number of cranberry pollen grains on yield (F1,6 = 5.330, P = 0.060), with marshes in high-woodland landscapes showing a positive effect of total cranberry pollen grains on yield but no effect for marshes in lowwoodland landscapes (Fig. 5b). There was no relationship between farm size and landscape type (F1,8 = 2.917, P = 0.126), and no significant relationship between farm size and yield (F1,6 = 2.716, P = 0.150). There was a significant relationship between landscape type and yield (F1,6 = 9.431, P = 0.022) and no effect of the interaction between farm size and landscape type (F1,6 = 0.490, P = 0.510).
Our results suggest that honey bee foragers returning to hives located near water reservoirs collected a lower proportion of cranberry pollen compared to hives located near the center of marshes or at the edge with adjacent woodland habitat. This result was unexpected as we hypothesized that such water reservoirs on cranberry marshes may act as foraging barriers, similar to roads and railroads (Andersson et al., 2017; Bhattacharya et al., 2003) and may entice honey bees to forage on the target crop. We found no effect of hive location or landscape type on the diversity or the richness of pollen morphotypes collected by honey bees. However, morphotype evenness was significantly lower for hives near water reservoirs than the other hive locations, with a single morphotype representing nearly 50% of the pollen collected from water reservoir hives. Indeed, during cranberry bloom (June-July in the upper Midwest), edges of water reservoirs tend to support alternate floral resources, such as milkweed and clover (Guzman and Guédot, personal observations), which may compete with cranberry (Arenas and Kohlmaier, 2019). Thus, the reduced proportion of cranberry pollen in hives near water reservoirs may be due, at least in part, to the close proximity of abundant shoreline flowers, and/or a preference for such non-crop floral resources. In cranberry, the spatial arrangement of hives affects the foraging behavior of honey bees, at least in regards to the proportion of cranberry pollen they bring back to the hive. Previous studies have suggested that the distribution and density of bee nests affect the foraging efficiency of various managed pollinators in different cropping systems (e.g., faba beans and almonds) (Artz et al., 2013; Cunningham et al., 2016; Cunningham and Le Feuvre, 2013). Distributing honey bee hives to reduce the distance between hives to about 700 m (Cunningham 4
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Fig. 2. Mean number of cranberry pollen grains ( ± S.E.) collected in pollen traps from honey bee pollen foragers returning to hives placed at (A) three different on-farm locations (near water reservoir, near center, and near woodland habitat) in (B) two landscape types (high- and low-woodland) and (C) their interaction at ten marshes.
more in studies in blueberry and oil seed rape (Danner et al., 2017; Girard et al., 2012; Requier et al., 2015). While this study was conducted over one year, our sampling method likely characterized adequately the diversity of the pollen flora in Wisconsin cranberry, since as few as ten samples were shown to represent the entire floral richness in a similar context (Girard et al., 2012). The diversity of plant species from which honey bees collect pollen, both temporally and spatially, has been shown to increase colony health, survival, and brood size, by ensuring a large range of nutrient levels (Alaux et al., 2010; Di Pasquale et al., 2013; Girard et al., 2012) especially in intensive agricultural systems, where mass-flowering crops may not be sufficient for honey bee health (Di Pasquale et al., 2016). Our results suggest that cranberry marshes provide a diversity of alternate pollen resources for honey bees to forage on; however, a closer examination of the pollen morphotypes collected to identify which plant taxa were visited (Girard et al., 2012) and to determine the nutrient composition of pollen loads (Colwell et al., 2017) is needed to assess the impact of these alternate resources on honey bee health. These findings additionally show that although cranberry marshes are intensely managed, they may also offer a diversity of floral resources for wild pollinators, a combination which supports the abundance and richness of native bee communities (Lentini et al., 2012). In our study, both the location of hives within a crop field and the landscape context of that field affected the community of pollen collected by bees, and honey bees tended to forage on different plants in high- versus low-intensity agricultural landscapes (Smart et al., 2017). Studies looking at the effect of landscape on the composition of pollen collected by honey bees have shown mixed results (Danner et al., 2017; Piroux et al., 2014; Smart et al., 2017). For example, several studies found no relationship between landscape composition and pollen diversity (Danner et al., 2017; Piroux et al., 2014; Smart et al., 2017), including our study. While Piroux et al. (2014) found that pollen
et al., 2016; Cunningham and Le Feuvre, 2013) and increasing the density of nest boxes with Osmia lignaria Say (Megachilidae) (Artz et al., 2013) were both shown to influence bee foraging on the target crop. These studies did not account for the impact of on-farm attributes, or of the surrounding landscape, however. The current study is the first to report that the on-farm spatial arrangement of hives based on local attributes (proximity to water, woodland, or target crop) affects the foraging behavior of honey bees, although an increase in the proportion of cranberry pollen collected did not have much of an impact on cranberry yield. Overall, the proportion of cranberry pollen collected by honey bees on cranberry farms in our study was fairly low, 0.36 ± 0.07, but supported results obtained in some other studies: 0.36 (Girard et al., 2012) and 0.46 (Shimanuki et al., 1967), while being higher than that obtained in another study: 0.08 (Colwell et al., 2017). Cane and Schiffhauer (2001) reported proportions ranging from 0.02 to 1, and attributed this variation to daily pollen foraging fluctuations and honey bee genotypes (including a pollen-hoarding genotype); however, other factors, such as colony strength (Delaplane et al., 2013), previous pollen storage in the hive (Fewell and Winston, 1992), brood size (Free, 1967), and pollen nutritional quality (Cook et al., 2003), as well as hive placement and landscape factors (this study), may affect how honey bees forage on a target crop. However, the low proportion of cranberry pollen brought back to the hive, if reflective of the impact of these bees on cranberry pollination, suggests room for improvement of management practices to increase cranberry yield. The botanical richness in the pollen loads observed in our study was relatively high. We identified 33 pollen morphotypes collected by honey bees, which was similar to previous studies in Canada, wherein 33 (Girard et al., 2012) and 20 (Colwell et al., 2017) plant taxa were reported in cranberry. Fewer taxa were reported in other crops, such as apple, blueberry, and fallow sites in Canada (Colwell et al., 2017), yet 5
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Fig. 3. Mean total pollen weight ( ± S.E.) collected in pollen traps from honey bee pollen foragers returning to hives placed at (A) three different on-farm locations (near water reservoir, near center, and near woodland habitat) in (B) two landscape types (high- and low-woodland) and (C) their interaction at ten marshes.
same amount of crop pollen, regardless of hive location. Interestingly, neither the number nor the proportion of crop pollen affected crop yield in cranberry. Rather, yield was influenced by the surrounding landscape, with marshes in low-woodland landscapes experiencing higher yields than marshes in high-woodland landscapes. This result is in agreement with previous work in cranberry (Gaines-Day and Gratton, 2016), although the mechanism behind this pattern is poorly understood. Moreover, the interaction between landscape type and proportion of cranberry collected on yield was marginal, with an increase in yield with increased cranberry pollen collected in high-woodland but
richness was associated with landscape composition, Smart et al. (2017), as well as our study, found no effect of landscape on pollen richness. Despite the lack of relationship between landscape and pollen diversity, honey bees increased their foraging distance as landscape diversity decreased (Danner et al., 2017; Steffan-Dewenter and Kuhn, 2003). Thus, strategically choosing where hives are located within a crop field may help provide honey bees with more diverse floral resources. The mean number of cranberry pollen grains collected was not affected by hive location, suggesting that honey bees overall collected the
Table 1 Mean Shannon diversity ( ± S.E.), mean richness ( ± S.E.), and mean evenness ( ± S.E.) of pollen color morphotypes (excluding cranberry pollen) collected in pollen traps from honey bee pollen foragers returning to hives placed at three different on-farm locations (near water reservoir, near center, and near woodland habitat) in two landscape types (high- and low-woodland) at ten marshes in Central Wisconsin. Values in bold are significant from each other at P < 0.05 (see result section). Shannon Hive location Water reservoir Center Woodland habitat Landscape type High-woodland Low-woodland Hive location x landscape type Water reservoir x high-woodland Water reservoir x low-woodland Center x high-woodland Center x low-woodland Woodland habitat x high-woodland Woodland habitat x low-woodland
Richness
Evenness
mean ± SEM 0.795 0.781 0.753
± ± ±
0.071 0.072 0.071
4.345 3.799 3.946
± ± ±
0.414 0.417 0.415
0.301 0.446 0.439
± ± ±
0.051 0.052 0.052
0.764 0.789
± ±
0.058 0.058
3.965 4.094
± ±
4.094 0.493
0.381 0.410
± ±
0.053 0.054
0.836 0.755 0.754 0.808 0.702 0.803
± ± ± ± ± ±
0.099 0.099 0.101 0.103 0.099 0.103
4.556 4.133 3.641 3.956 3.697 4.194
± ± ± ± ± ±
0.583 0.587 0.588 0.592 0.583 0.592
0.267 0.267 0.481 0.411 0.394 0.484
± ± ± ± ± ±
0.072 0.073 0.073 0.075 0.072 0.074
Values in bold are significant from each other (see result section). 6
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Fig. 4. (A) Distribution of pollen morphotypes collected in pollen traps from honey bee pollen foragers returning to hives placed at three different on-farm locations (near water reservoir, near center, and near woodland habitat) as a proportion of total pollen weight collected. Chao1 dissimilarities of pollen morphotypes between (B) hive locations (near water reservoir, near center, and near woodland habitat), and (C) two landscape types (high- and low-woodland) visualized using non-metric dimensional scaling for the perMANOVA analysis.
In summary, on-farm management decisions such as honey bee hive spatial arrangement can influence honey bee foraging, without having an impact on yield. The pollen diversity and richness collected by honey bees was not influenced by hive location or landscape composition and the presence of alternative flowering plants in the surrounding landscape may promote the health of the colony. While the proportion and number of cranberry pollen grains collected did not affect yield, the amount of woodland did and there was, marginally, a greater increase in yield with more cranberry pollen grains in the high- as opposed to low-woodland landscapes. Future studies should examine the mechanism behind such potential interactions.
not in low-woodland habitats. Gaines-Day and Gratton (2016) showed that the relationship between cranberry yield and honey bee hive stocking densities was dependent on the amount of woodland in the surrounding landscape. On marshes surrounded by high amounts of woodland habitat (> 42% within 1 km), there was no relationship between hive stocking density and cranberry yield. However, on marshes with low-woodland habitat in the surrounding landscape, there was a strong relationship between hive stocking density and yield. These results suggest that proximity to woodland influences honey bee foraging on cranberry but further work should elucidate the mechanism behind these patterns.
Fig. 5. Effect of the proportion of cranberry pollen grains on cranberry yield (A) for marshes separated by landscape types (high- and low-woodland). Effect of the number of cranberry pollen grains on cranberry yield (B) for marshes separated by landscape types (high- and low-woodland). The solid lines show the regression line fit to the data and the gray envelope shows the standard error.
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Declaration of Competing Interest
https://doi.org/10.1016/j.fcr.2013.05.019. Cunningham, S.A., Fournier, A., Neave, M.J., Le Feuvre, D., 2016. Improving spatial arrangement of honeybee colonies to avoid pollination shortfall and depressed fruit set. J. Appl. Ecol. 53 (2), 350–359. https://doi.org/10.1111/1365-2664.12573Danner. Danner, N., Molitor, A.M., Schiele, S., Härtel, S., Steffan‐Dewenter, I., 2016. Season and landscape composition affect pollen foraging distances and habitat use of honey bees. Ecol. Appl. 26 (6), 1920–1929. https://doi.org/10.1890/15-1840.1. Danner, N., Keller, A., Härtel, S., Steffan-Dewenter, I., 2017. Honey bee foraging ecology: season but not landscape diversity shapes the amount and diversity of collected pollen. PLoS One 12 (8), e0183716. https://doi.org/10.1371/journal.pone.0183716. Delaplane, K.S., Mayer, D.R., Mayer, D.F., 2000. Crop Pollination by Bees. CAB Publishing, Wallingford. Delaplane, K.S., Van der Steen, J., Guzman, E., 2013. 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None. Acknowledgements We are thankful for the field and lab assistance provided by Katie Hietala-Henschell, Olivia Bernauer, Tierney Bougie, Elissa Chasen, Miguel Hernandez, Scott Lee, Erin McMahan, Keith Phelps, Emma Pelton, Walter Salazar, Janet Van Zoeren, Kelly Wallin, and Eric Weisman, as well as the University of Wisconsin-Madison Herbarium and the Paskewitz Lab for their support. We are grateful to the cranberry growers and bee keepers for collaborating on this project and so graciously sharing their expertise and resources. We also thank the Wisconsin Cranberry Board Inc., Cranberry Institute, and Ocean Spray Cranberries Inc. for funding this research. Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.agee.2019.106624. References Aizen, M.A., Garibaldi, L.A., Cunningham, S.A., Klein, A.M., 2009. How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Ann. Bot. 103 (9), 1579–1588. https://doi.org/10.1093/aob/mcp076. Aizen, M.A., Harder, L.D., 2009. The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr. Biol. 19 (9), 915–918. https:// doi.org/10.1016/j.cub.2009.03.071. Alaux, C., Ducloz, F., Crauser, D., Le Conte, Y., 2010. Diet effects on honeybee immunocompetence. Biol. Lett. 6 (4). https://doi.org/10.1098/rsbl.2009.0986. Andersson, P., Koffman, A., Sjödin, N.E., Johansson, V., 2017. Roads may act as barriers to flying insects: species composition of bees and wasps differs on two sides of large highway. Nat. Conserv. 18, 41–59. https://doi.org/10.3897/natureconservation.18. 12314. Arenas, A., Kohlmaier, M.G., 2019. Nectar source profitability influences individual foraging preferences for pollen and pollen-foraging activity of honeybee colonies. Behav. Ecol. Sociobiol. 73, 34–43. https://doi.org/10.1007/s00265-019-2644-5. Artz, D.R., Allan, M.J., Wardell, G.I., Pitts-Singer, T.L., 2013. Nesting site density and distribution affect Osmia lignaria (Hymenoptera: Megachilidae) reproductive success and almond yield in a commercial orchard. Insect Conserv. Divers. 6 (6), 715–724. https://doi.org/10.1111/icad.12026. Bates, D., Maechler, M., Bolker, B., Steve Walker, S., 2015. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67 (1), 1–48 < doi:10.18637/jss.v067.i01 > . Bhattacharya, M., Primack, R.B., Gerwein, J., 2003. Are roads and railroads barriers to bumblebee movement in a temperate suburban conservation area? Biol. Conserv. 109 (1), 37–45. https://doi.org/10.1016/S0006-3207(02)00130-1. Blaauw, B.R., Isaacs, R., 2014. Flower plantings increase wild bee abundance and the pollination services provided to a pollination‐dependent crop. J. Appl. Ecol. 51 (4), 890–898. https://doi.org/10.1111/1365-2664.12257. Broussard, M., Roa, S., Stephen, W.P., 2011. Native bees, honeybees, and pollination in Oregon cranberries. HortScience 46 (6), 885–888. https://doi.org/10.21273/ HORTSCI.46.6.885. Calderone, N.W., 2012. Insect pollinated crops, insect pollinators and US agriculture: trend analysis of aggregate data for the period 1992-2009. PLoS One 7 (5), e37235. https://doi.org/10.1371/journal.pone.0037235. Cane, J.H., Schiffhauer, D., 2001. Pollinator genetics and pollination: do honey bee colonies selected for pollen-hoarding field better pollinators of cranberry Vaccinium macrocarpon? Ecol. Entomol. 26 (2), 117–123. https://doi.org/10.1046/j.13652311.2001.00309.x. Cane, J.H., Schiffhauer, D., 2003. Dose-response relationships between pollination and fruiting refine pollinator comparisons for cranberry (Vaccinium macrocarpon [Ericaceae]). Am. J. Bot. 90 (10), 1425–1432. https://doi.org/10.3732/ajb.90.10. 1425. Colwell, M.J., Williams, G.R., Evans, R.C., Shutler, D., 2017. Honey bee‐collected pollen in agro‐ecosystems reveals diet diversity, diet quality, and pesticide exposure. Ecol. Evol. 7 (18), 7243–7253. https://doi.org/10.1002/ece3.3178. Concepción, E.D., Díaz, M., Kleijn, D., Báldi, A., Batáry, P., Clough, Y., Gabriel, D., Herzog, F., Holzschuh, A., Knop, E., Marshall, E.J.P., Tscharntke, T., Verhulst, J., 2012. Interactive effects of landscape context constrain the effectiveness of local agrienvironmental management. J. Appl. Ecol. 49 (3), 695–705. https://doi.org/10. 1111/j.1365-2664.2012.02131.x. Cook, S.M., Awmack, C.S., Murray, D.A., Williams, I.H., 2003. Are honey bees’ foraging preferences affected by pollen amino acid composition? Ecol. Entomol. 28 (5), 622–627. https://doi.org/10.1046/j.1365-2311.2003.00548.x. Cunningham, S.A., Le Feuvre, D., 2013. Significant yield benefits from honeybee pollination of faba bean (Vicia faba) assessed at field scale. Field Crops Res. 149, 269–275.
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Surrounding landscape and spatial arrangement of honey bee hives affect pollen foraging and yield in cranberry A. Guzmana,1, H.R. Gaines-Daya, A.N. Loisa, S.A. Steffana,b, J. Bruneta,b, J. Zalapaa,b, C. Guédota, a b
T ⁎
University of Wisconsin-Madison, Madison, WI, 53706, USA Vegetable Crops Research Unit, USDA-ARS, Madison, WI, 53706, USA
A R T I C LE I N FO
A B S T R A C T
Keywords: Apis mellifera Pollen Woodland Vaccinium macrocarpon
Honey bees are the most important managed pollinator in the world. Recent trends suggest, however, that the demand for their pollination services is growing faster than the available supply. Therefore, it is critical to determine the most efficient management practices to maximize their use for crop production. One factor known to influence the efficiency of crop pollination is the availability of alternative, non-crop floral resources. These resources can vary as a function of the landscape surrounding a farm as well as local management practices within a farm. However, little is known about how the foraging behavior of honey bees on the target crop responds to the spatial arrangement of hives or the composition of the surrounding landscape. In this study, we collected pollen from pollen traps on honey bee hives placed on commercial cranberry marshes in central Wisconsin (USA). Individual marshes were selected to fall across a gradient of surrounding landscape from highto low-woodland. Within each marsh, hives were placed either adjacent to wooded habitat, adjacent to a water reservoir, or in the center of the marsh. Honey bees from hives near water reservoirs collected a lower proportion of cranberry pollen than honey bees near the wooded area or at the center of the marsh. However, honey bees collected the same number of cranberry pollen grains and total pollen biomass irrespective of hive location or the surrounding landscape. Honey bees from hives located near water reservoirs, relative to the other two hive locations, tended to collect more pollen from fewer plants (low evenness). Cranberry yield did not vary as a function of the proportion of cranberry pollen collected or total number of cranberry pollen grains collected, but yield was higher at marshes located in low-woodland landscapes relative to those in high-woodland landscapes. We conclude that the location of hives on a cranberry marsh in relation to non-crop habitat does not affect yield allowing growers to place hives where it is convenient, although placing hives near water reservoirs should provide bees with a more diverse pollen diet.
1. Introduction Honey bees (Apis mellifera) are the most widely managed pollinator used in agricultural production, providing pollination services for nearly half of leading global food commodities (Klein et al., 2006; vanEngelsdorp and Meixner, 2010). Commercially managed honey bees are commonly used in agricultural systems because they are generalist foragers, recruit nestmates to floral resources, are managed in large colonies for pollination services, and can be supplied to coincide with crop flowering (Calderone, 2012; Kremen and Chaplin-Kramer, 2007). The agricultural demand for honey bee pollination services is rising, increasing by 50% in developed countries between 1961 and 2006 (Aizen et al., 2009; vanEngelsdorp and Meixner, 2010), while at the same time, the number of managed hives is decreasing (Food and
Agriculture Organization of the United Nations (FAO, 2009; Stokstad, 2007; vanEngelsdorp and Meixner, 2010). These competing trends not only raise the price of pollination services for growers, but suggest that pollinators may become a limiting factor for pollinator-dependent crops going into the future (Aizen and Harder, 2009; vanEngelsdorp and Meixner, 2010). Therefore, a better understanding of the factors that influence the contribution of honey bees to crop pollination is critical. One factor that may influence the pollination efficiency of honey bees is the availability of non-crop flowers in and around a crop field (Blaauw and Isaacs, 2014; Concepción et al., 2012; Morandin and Kremen, 2013; Sardiñas and Kremen, 2015; Vaissière, 1991). On a local on-farm scale, as colony density increases and distance from the nest to the crop decreases, bees forage more on crop plants, resulting in improved yields (Artz et al., 2013; Cunningham et al., 2016; Cunningham
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Corresponding author at: University of Wisconsin-Madison, Department of Entomology, 1630 Linden Drive Madison, WI, 53706, USA. E-mail address: [email protected] (C. Guédot). 1 Current address: University of California-Berkeley, Berkeley, CA 94720, USA. https://doi.org/10.1016/j.agee.2019.106624 Received 23 March 2019; Received in revised form 18 July 2019; Accepted 27 July 2019 Available online 28 August 2019 0167-8809/ © 2019 Elsevier B.V. All rights reserved.
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2. Materials and methods
and Le Feuvre, 2013). However, in some studies, honey bees collected very little, if any, pollen from the target crop (Pettis et al., 2013; Vaissiere, 1991). At a broader scale, the abundance and composition of floral resources in natural or semi-natural habitat surrounding crop fields can also affect the foraging behavior of honey bees (Concepción et al., 2012; Tscharntke et al., 2012). Furthermore, landscapes with more natural habitat may provide a more diverse and nutritious diet to bees and result in better overall bee health (Danner et al., 2016; Donkersley et al., 2014; Pasquale et al. 2013). When alternative resources are present in the landscape, honey bees may preferentially forage on non-crop flowers (Cane and Schiffhauer, 2001; Girard et al., 2012), neglecting the target crop. Cranberry (Vaccinium macrocarpon Aiton, Ericaceae), a fruit crop native to North America, relies on pollinators for fruit production (Delaplane et al., 2000; Eck, 1986; Gaines-Day, 2013; McGregor, 1976). Although honey bees are not the most efficient pollinator on a per visit basis (Cane and Schiffhauer, 2003; MacKenzie, 1994), their large numbers can offset this disparity (Free, 1993; Woodcock et al., 2013). Wisconsin (USA) produces over 60% of the US cranberry crop and nearly all growers use rented honey bee hives for pollination services (Gaines-Day and Gratton, 2016; USDA NASS, 2006). Despite the significant cost of honey bee rentals for cranberry growers ($350-$520 per hectare) (Gaines-Day, 2013; USDA NASS, 2006), honey bee visitation rates to cranberry flowers vary considerably. Indeed in cranberry, honey bees can return to the hive with no cranberry pollen, suggesting that they visited other floral resources (Broussard et al., 2011; Cane and Schiffhauer, 2001; MacKenzie, 1994; Pettis et al., 2013; Shimanuki et al., 1967). To increase visitation to cranberry flowers and subsequent yield, hive densities ranging between 0.25–25 hives per hectare have been suggested (reviewed in Delaplane et al., 2000). In Wisconsin, growers stock their cranberry marshes with, on average, 5–7 hives per hectare (Gaines-Day and Gratton, 2016). Research on how the spatial arrangement of hives within the crop field influences yield, however, is lacking. The location of the hives is important because it determines how accessible non-crop floral resources are to the bees. Theoretically, placing hives far from non-crop habitat should encourage the bees to forage on the crop flower, but previous studies in cranberry have shown that cranberry yield was unaffected by the presence of honey bees or the distance from hive to crop (Kevan et al., 1983) and that the relationship between hive stocking density and yield varies as a function of the surrounding landscape (Gaines-Day and Gratton, 2016). These results also suggest that the honey bees may be visiting alternative floral resources rather than cranberry. Therefore, understanding how these relationships vary as a function of hive location within the cranberry will be valuable for increasing the efficiency of cranberry pollination practices. The objectives of this study were to determine how the foraging of commercial honey bees is influenced by a) the spatial arrangement of hives in relation to adjacent habitats, and b) the composition of habitat in the surrounding landscape (i.e. high- vs. low-woodland). Specifically, we investigated how these factors influenced the amount and percent of cranberry pollen brought back to the hive by honey bees. We also examined how the amount and percent of cranberry pollen brought back to the hive and the surrounding landscape affected yield. We hypothesized that, in high-woodland landscapes, honey bees would forage less on cranberry and return a lower proportion of cranberry pollen to the hive because of the proximity to other non-crop floral resources. We also expected honey bees from hives located in the center of a marsh or near a water reservoir to bring a greater proportion of cranberry pollen back to the hive. The results of this research will increase our understanding of how the hive spatial arrangement and the surrounding landscape influence honey bee behavior in Wisconsin cranberry and will provide recommendations to growers to optimize their pollination services.
2.1. Study site selection and landscape classification This research was conducted in central Wisconsin (USA), the main growing region of cranberries in the world. Wisconsin cranberry marshes are typically embedded within natural ecosystems (Gaines-Day, 2013). Thus, in order to determine the effect of the surrounding landscape composition on cranberry pollen use by honey bees, marshes were selected to span a gradient of high- to low-woodland habitat in the surrounding landscape. For each marsh, we calculated the landscape composition within a 1 km radius using the Cropland Data Layer (CDL) (USDA NASS CDL, 2015) in ArcGIS® (ESRI ArcGIS Desktop, 2011). Land cover was classified into three categories: open semi-natural habitat (grassland, pasture, hay, and herbaceous wetland), woodland habitat (deciduous forest, coniferous forest, mixed forest, wooded wetlands, and shrubland), and other (all remaining CDL categories). We selected ten commercially managed marshes spanning the western edge of the cranberry growing region from Tomah to Black River Falls, Wisconsin, U.S.A., based on the following criteria: 1) the surrounding landscape composed of either more than 60% or less than 40% woodland (GainesDay and Gratton, 2016); 2) the presence of a large water reservoir on the marsh (typical in this growing region); 3) a marsh shape that allowed for the spatial arrangement of a “center” sampling location (i.e., not long and narrow); and 4) the presence of wooded habitat adjacent to at least one side of the marsh. Marshes ranged in size from 4 to 107 ha and each marsh consisted of multiple rectangular beds measuring ˜50 m wide and varying in length.
2.2. Study design Commercial honey bee hives rented by the cranberry growers for pollination were used in this study. Hives were evaluated to meet a minimum health standard by evaluating the area covered with the bee cluster on top of the frames (Nasr et al., 1990) and observing bees returning to the hive. Hives that looked healthy and similar in colony strength were selected. At each of the ten selected marshes, one quad of hives were placed at each of three predetermined locations: (1) near the marsh center (“Center”) which was surrounded by cranberry beds, (2) at the edge of the marsh near a wooded edge (“Woodland habitat”), and (3) at a marsh edge adjacent to a water reservoir (“Water reservoir”). All hive locations within a marsh were at least 300 m apart from each other and as much as 2000 m apart, depending on the size of the marsh. To assess the extent of foraging by honey bees on cranberry flowers, we collected pollen brought back to hives by pollen foragers using pollen traps installed on one hive per location (three hives per marsh). Sampling occurred from June 23 to July 14, 2015 to coincide with cranberry bloom and the arrival of honey bee hives on the marshes. At each hive, a yellow plastic pollen trap (Eco-Keeper Inc., Duluth, GA) was mounted on the front entrance of the hive as soon as hives were delivered to marshes (between 16–20 June), and were left for the entire sampling period. All other holes found on hives were blocked off with tape or cardboard pieces to ensure bees would enter the hive through the pollen trap. The traps were activated for 24 -h collection intervals twice a week for the three week duration of cranberry bloom for a total of six collection periods (n = 180 pollen samples). Pollen samples were collected, returned to the laboratory on ice and stored at −20 °C until processed. Each pollen sample was then freeze-dried at ca. −75 °C in a VirTis Benchtop 4 K freezer dryer (model 4 KBTXL-75; SP Scientific, Warminster, PA, USA) equipped with a Pascal 2005SD vacuum pump (Adixen, Pfeiffer Vacuum, worldwide) for 24–48 hrs. Freeze dried samples were carefully cleaned of all debris (i.e., dead insects and leaf pieces) using tweezers, and a total weight for each pollen sample was recorded.
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using generalized and linear mixed models (GLMMs and LMMs; Bates et al., 2015; Kuznetsova et al., 2017). All models included the interaction effect of landscape and hive location (landscape × location) plus marsh and the interaction of marsh and hive location, to account for the six sampling rounds per hive per marsh, as random effects. The impact of cranberry pollen (proportion and number of cranberry grains) collected by honey bees on cranberry yield was examined using pollen count data aggregated over hive location and sampling round. An interaction term between the cranberry pollen variable and landscape type (high-woodland versus low-woodland landscape) was included as fixed effects. The relationship between farm size and landscape type as well as farm size and yield were assessed. For all yield models, LMMs were used and marsh was included as a random effect. All statistical analyses were performed using the lme4 and lmerTest packages in R (Bates, et al., 2015; Kuzentsova and Rune, 2016; R Core team, 2014). In addition, the significance of the fixed effects of the LMMs was determined by an F-test and the method described by Kenward and Roger (1997) was used to calculate the degrees of freedom. For the significance of the fixed effects in the GLMMs, likelihood ratio tests were used. For count response variables (i.e. proportion), models assumed a Poisson distribution and for continuous variables (i.e. number of pollen grains, pollen weight, and diversity indices), models assumed a Gaussian distribution.
2.3. Pollen composition 2.3.1. Diversity of color morphotypes To assess the diversity of pollen collected by each hive, we categorized pollen bundles by color morphotypes. Samples that were clumped due to water damage could not be separated and were excluded from this analysis. For samples that could be separated (n = 143), pollen bundles were sorted by subtle color differences to the closest match utilizing the Sherwin-Williams color palettes (Girard et al., 2012; Pettis et al., 2013) and the dry weight of each color morphotype per sample was recorded. For each color morphotype across marshes, we collected a small amount of pollen from a pollen bundle with the tip of a needle (equivalent to 1/8 mm3 of pollen according to Girard et al., 2012) and mounted it on a microscope slide with 50-50 glycerin-water solution to identify each color morphotype to a unique pollen morphology. 2.3.2. Cranberry vs. non-cranberry pollen Color morphotypes for each pollen sample were then recombined into a single vial, thoroughly mixed, and crushed with a mortar and pestle. A 0.5 g subsample of each recombined sample was taken (n = 141 samples whose total pollen weight was greater than 0.5 g), and placed into a 5 ml centrifuge tube. Three mL of 50-50 glycerinwater solution was added to the tube, and the solution was mixed thoroughly with a metal spatula until homogenous. For each pollen sample, 11 μl of the solution was pipetted onto a hemocytometer slide (LW Scientific©, Lawrenceville, GA, USA) with a 0.100 mm depth and 0.0025 mm2 area. For each slide, three random 1 mm2 squares were examined under a compound microscope (Reichert Scientific Instruments, Buffalo, NY, USA) and the total number of cranberry (identified by the characteristic tetrad pollen grains) and non-cranberry pollen grains (all others) were recorded. We then took an average of the three counts for each sample. To estimate the total number of cranberry pollen grains in each sample, we multiplied our averaged pollen count by 9 to account for the total number of squares on the slide. Then, we divided by the dilution factor (0.5 g/ 3 ml) and multiplied by the original total weight of the pollen sample to determine the total number of cranberry grains in each hive pollen sample.
3. Results Hive location within the marsh significantly affected the proportion of cranberry pollen collected by hives (df = 2; χ2 = 7.868, P = 0.020; Fig. 1a). Hives near the water reservoir had the lowest proportion of cranberry pollen (mean ± SEM: 0.152 ± 0.093) compared to the other hive locations, and hives in high-woodland landscapes had the lowest proportion of cranberry pollen (0.146 ± 0.112). Landscape type did not significantly affect the proportion of cranberry pollen collected by hives although the effect was marginal (df = 1; χ 2 = 3.260, P = 0.071; Fig. 1b). There was no statistically significant interaction between the effect of landscape type and hive location on the proportion of cranberry pollen collected (df = 2; χ 2 = 2.757, P = 0.252; Fig. 1c). For the total number of cranberry pollen grains collected, neither hive location (F2,16 = 1.779, P = 0.201; Fig. 2a), landscape type (F1,8 = 0.329, P = 0.582; Fig. 2b), nor the interaction between them (F2,16 = 0.161, P = 0.852; Fig. 2c) were statistically significant predictors. The total pollen dry weight per sample ranged from 3.450 g to 10.126 g. There was no statistically significant difference in the total weight of pollen collected by hive location (F2,16 = 1.008, P = 0.387; Fig. 3a), landscape type (F1,8 = 0.036, P = 0.854; Fig. 3b), or the interaction between hive location and landscape type (F2,16 = 2.135, P = 0.151; Fig. 3c). We identified a total of 33 pollen color morphotypes across all pollen samples, with a Shannon diversity index ranging from 0.016 to 1.603 (Table 1). There was no effect of hive location (F2,16 = 0.086, P = 0.918), landscape type (F1,7 = 0.033, P = 0.861), or the interaction between hive location and landscape type (F2,16 = 0.460, P = 0.639) on the Shannon diversity index of non-cranberry pollen morphotypes. Similarly, there was no difference in the number of color morphotypes (i.e. richness) collected by hives regardless of hive location (F2,16 = 1.039, P = 0.377), landscape type (F1,8 = 0.035, P = 0.857), or the interaction of hive location and landscape type (F2,16 = 0.777, P = 0.477; Table 1). The evenness of pollen morphotypes was significantly affected by hive location (F2,16 = 3.624, P = 0.051; Table 1 and Fig. 4a). Honey bees tended to collect pollen more frequently from some plant groups (lower pollen evenness) for hives near the water reservoir (0.301 ± 0.051) than hives in the center (0.446 ± 0.052) or near woodland habitat (0.439 ± 0.051). There was no effect of landscape type (F1,8 = 0.151, P = 0.708) or the interaction between hive location
2.4. Cranberry yield Cranberry yield data for each marsh for the 2015 growing season was provided by each grower as the marsh-wide average. 2.5. Statistical analyses The effect of surrounding landscape (high-woodland vs. lowwoodland) and hive location (center, water reservoir, and woodland habitat) was assessed on the proportion of cranberry pollen grains, the number of cranberry pollen grains, and dry pollen weight (box-cox transformed to meet assumptions of normality), as well as the pollen diversity (i.e. diversity, richness, and evenness) and composition of pollen color morphotypes for non-cranberry pollen. Diversity of the non-cranberry pollen was determined using Shannon diversity index on the weight of each pollen color morphotype. Pollen richness was calculated using the Chao1 estimator, (transformed as natural log + 1). Both measures were calculated using the R package vegan (Oksanen et al., 2013). Evenness of non-cranberry pollen color morphotypes was calculated using the R package fundiv (Evar; samples that had ≤ 1 species were dropped; Smith and Wilson, 1996). Further, to evaluate the differences in the composition of pollen color morphotypes across hive location, landscape type, and their interaction, a permutational multivariate analysis of variance (perMANOVA) with Chao1 dissimilarities in the R package vegan (Okansen et al., 2013) was used. All other analyses were conducted 3
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Fig. 1. Mean proportion of cranberry pollen grains ( ± S.E.) collected in pollen traps from honey bee pollen foragers returning to hives placed at three different onfarm locations (near water reservoir, near center, and near woodland habitat) in two landscape types (high- and low-woodland) at ten marshes.
4. Discussion
and landscape type (F2,16 = 0.994, P = 0.393; Table 1 and Fig. 4a) on the evenness of the pollen morphotype distribution. The composition of pollen morphotypes differed among hive locations (F2,2 = 1.791, P = 0.001; Fig. 4b) and landscape type (F1,1 = 3.123, P = 0.001; Fig. 4c) but there was no interaction between the effects of hive location and landscape type on pollen composition (F2,1 = 1.099, P = 0.238). As the average proportion of cranberry pollen collected increased, the increase in yield was marginal (F1,6 = 5.197, P = 0.063; Fig. 5a), but marshes in low-woodland landscape reported higher yield than those in high-woodland landscape (F1,6 = 8.780, P = 0.025; Fig. 5a). There was no significant interaction between the effect of landscape type and the proportion of cranberry pollen collected on yield (F1,6 = 0.197, P = 0.673; Fig. 5a). There was no significant relationship between the total number of cranberry pollen grains collected by honey bees and yield (F1,6 = 0.915, P = 0.376; Fig. 5b). Rather, there was a significant effect of landscape type on yield (F1,6 = 20.433, P = 0.004) and a marginal effect of the interaction between landscape type and the total number of cranberry pollen grains on yield (F1,6 = 5.330, P = 0.060), with marshes in high-woodland landscapes showing a positive effect of total cranberry pollen grains on yield but no effect for marshes in lowwoodland landscapes (Fig. 5b). There was no relationship between farm size and landscape type (F1,8 = 2.917, P = 0.126), and no significant relationship between farm size and yield (F1,6 = 2.716, P = 0.150). There was a significant relationship between landscape type and yield (F1,6 = 9.431, P = 0.022) and no effect of the interaction between farm size and landscape type (F1,6 = 0.490, P = 0.510).
Our results suggest that honey bee foragers returning to hives located near water reservoirs collected a lower proportion of cranberry pollen compared to hives located near the center of marshes or at the edge with adjacent woodland habitat. This result was unexpected as we hypothesized that such water reservoirs on cranberry marshes may act as foraging barriers, similar to roads and railroads (Andersson et al., 2017; Bhattacharya et al., 2003) and may entice honey bees to forage on the target crop. We found no effect of hive location or landscape type on the diversity or the richness of pollen morphotypes collected by honey bees. However, morphotype evenness was significantly lower for hives near water reservoirs than the other hive locations, with a single morphotype representing nearly 50% of the pollen collected from water reservoir hives. Indeed, during cranberry bloom (June-July in the upper Midwest), edges of water reservoirs tend to support alternate floral resources, such as milkweed and clover (Guzman and Guédot, personal observations), which may compete with cranberry (Arenas and Kohlmaier, 2019). Thus, the reduced proportion of cranberry pollen in hives near water reservoirs may be due, at least in part, to the close proximity of abundant shoreline flowers, and/or a preference for such non-crop floral resources. In cranberry, the spatial arrangement of hives affects the foraging behavior of honey bees, at least in regards to the proportion of cranberry pollen they bring back to the hive. Previous studies have suggested that the distribution and density of bee nests affect the foraging efficiency of various managed pollinators in different cropping systems (e.g., faba beans and almonds) (Artz et al., 2013; Cunningham et al., 2016; Cunningham and Le Feuvre, 2013). Distributing honey bee hives to reduce the distance between hives to about 700 m (Cunningham 4
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Fig. 2. Mean number of cranberry pollen grains ( ± S.E.) collected in pollen traps from honey bee pollen foragers returning to hives placed at (A) three different on-farm locations (near water reservoir, near center, and near woodland habitat) in (B) two landscape types (high- and low-woodland) and (C) their interaction at ten marshes.
more in studies in blueberry and oil seed rape (Danner et al., 2017; Girard et al., 2012; Requier et al., 2015). While this study was conducted over one year, our sampling method likely characterized adequately the diversity of the pollen flora in Wisconsin cranberry, since as few as ten samples were shown to represent the entire floral richness in a similar context (Girard et al., 2012). The diversity of plant species from which honey bees collect pollen, both temporally and spatially, has been shown to increase colony health, survival, and brood size, by ensuring a large range of nutrient levels (Alaux et al., 2010; Di Pasquale et al., 2013; Girard et al., 2012) especially in intensive agricultural systems, where mass-flowering crops may not be sufficient for honey bee health (Di Pasquale et al., 2016). Our results suggest that cranberry marshes provide a diversity of alternate pollen resources for honey bees to forage on; however, a closer examination of the pollen morphotypes collected to identify which plant taxa were visited (Girard et al., 2012) and to determine the nutrient composition of pollen loads (Colwell et al., 2017) is needed to assess the impact of these alternate resources on honey bee health. These findings additionally show that although cranberry marshes are intensely managed, they may also offer a diversity of floral resources for wild pollinators, a combination which supports the abundance and richness of native bee communities (Lentini et al., 2012). In our study, both the location of hives within a crop field and the landscape context of that field affected the community of pollen collected by bees, and honey bees tended to forage on different plants in high- versus low-intensity agricultural landscapes (Smart et al., 2017). Studies looking at the effect of landscape on the composition of pollen collected by honey bees have shown mixed results (Danner et al., 2017; Piroux et al., 2014; Smart et al., 2017). For example, several studies found no relationship between landscape composition and pollen diversity (Danner et al., 2017; Piroux et al., 2014; Smart et al., 2017), including our study. While Piroux et al. (2014) found that pollen
et al., 2016; Cunningham and Le Feuvre, 2013) and increasing the density of nest boxes with Osmia lignaria Say (Megachilidae) (Artz et al., 2013) were both shown to influence bee foraging on the target crop. These studies did not account for the impact of on-farm attributes, or of the surrounding landscape, however. The current study is the first to report that the on-farm spatial arrangement of hives based on local attributes (proximity to water, woodland, or target crop) affects the foraging behavior of honey bees, although an increase in the proportion of cranberry pollen collected did not have much of an impact on cranberry yield. Overall, the proportion of cranberry pollen collected by honey bees on cranberry farms in our study was fairly low, 0.36 ± 0.07, but supported results obtained in some other studies: 0.36 (Girard et al., 2012) and 0.46 (Shimanuki et al., 1967), while being higher than that obtained in another study: 0.08 (Colwell et al., 2017). Cane and Schiffhauer (2001) reported proportions ranging from 0.02 to 1, and attributed this variation to daily pollen foraging fluctuations and honey bee genotypes (including a pollen-hoarding genotype); however, other factors, such as colony strength (Delaplane et al., 2013), previous pollen storage in the hive (Fewell and Winston, 1992), brood size (Free, 1967), and pollen nutritional quality (Cook et al., 2003), as well as hive placement and landscape factors (this study), may affect how honey bees forage on a target crop. However, the low proportion of cranberry pollen brought back to the hive, if reflective of the impact of these bees on cranberry pollination, suggests room for improvement of management practices to increase cranberry yield. The botanical richness in the pollen loads observed in our study was relatively high. We identified 33 pollen morphotypes collected by honey bees, which was similar to previous studies in Canada, wherein 33 (Girard et al., 2012) and 20 (Colwell et al., 2017) plant taxa were reported in cranberry. Fewer taxa were reported in other crops, such as apple, blueberry, and fallow sites in Canada (Colwell et al., 2017), yet 5
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Fig. 3. Mean total pollen weight ( ± S.E.) collected in pollen traps from honey bee pollen foragers returning to hives placed at (A) three different on-farm locations (near water reservoir, near center, and near woodland habitat) in (B) two landscape types (high- and low-woodland) and (C) their interaction at ten marshes.
same amount of crop pollen, regardless of hive location. Interestingly, neither the number nor the proportion of crop pollen affected crop yield in cranberry. Rather, yield was influenced by the surrounding landscape, with marshes in low-woodland landscapes experiencing higher yields than marshes in high-woodland landscapes. This result is in agreement with previous work in cranberry (Gaines-Day and Gratton, 2016), although the mechanism behind this pattern is poorly understood. Moreover, the interaction between landscape type and proportion of cranberry collected on yield was marginal, with an increase in yield with increased cranberry pollen collected in high-woodland but
richness was associated with landscape composition, Smart et al. (2017), as well as our study, found no effect of landscape on pollen richness. Despite the lack of relationship between landscape and pollen diversity, honey bees increased their foraging distance as landscape diversity decreased (Danner et al., 2017; Steffan-Dewenter and Kuhn, 2003). Thus, strategically choosing where hives are located within a crop field may help provide honey bees with more diverse floral resources. The mean number of cranberry pollen grains collected was not affected by hive location, suggesting that honey bees overall collected the
Table 1 Mean Shannon diversity ( ± S.E.), mean richness ( ± S.E.), and mean evenness ( ± S.E.) of pollen color morphotypes (excluding cranberry pollen) collected in pollen traps from honey bee pollen foragers returning to hives placed at three different on-farm locations (near water reservoir, near center, and near woodland habitat) in two landscape types (high- and low-woodland) at ten marshes in Central Wisconsin. Values in bold are significant from each other at P < 0.05 (see result section). Shannon Hive location Water reservoir Center Woodland habitat Landscape type High-woodland Low-woodland Hive location x landscape type Water reservoir x high-woodland Water reservoir x low-woodland Center x high-woodland Center x low-woodland Woodland habitat x high-woodland Woodland habitat x low-woodland
Richness
Evenness
mean ± SEM 0.795 0.781 0.753
± ± ±
0.071 0.072 0.071
4.345 3.799 3.946
± ± ±
0.414 0.417 0.415
0.301 0.446 0.439
± ± ±
0.051 0.052 0.052
0.764 0.789
± ±
0.058 0.058
3.965 4.094
± ±
4.094 0.493
0.381 0.410
± ±
0.053 0.054
0.836 0.755 0.754 0.808 0.702 0.803
± ± ± ± ± ±
0.099 0.099 0.101 0.103 0.099 0.103
4.556 4.133 3.641 3.956 3.697 4.194
± ± ± ± ± ±
0.583 0.587 0.588 0.592 0.583 0.592
0.267 0.267 0.481 0.411 0.394 0.484
± ± ± ± ± ±
0.072 0.073 0.073 0.075 0.072 0.074
Values in bold are significant from each other (see result section). 6
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Fig. 4. (A) Distribution of pollen morphotypes collected in pollen traps from honey bee pollen foragers returning to hives placed at three different on-farm locations (near water reservoir, near center, and near woodland habitat) as a proportion of total pollen weight collected. Chao1 dissimilarities of pollen morphotypes between (B) hive locations (near water reservoir, near center, and near woodland habitat), and (C) two landscape types (high- and low-woodland) visualized using non-metric dimensional scaling for the perMANOVA analysis.
In summary, on-farm management decisions such as honey bee hive spatial arrangement can influence honey bee foraging, without having an impact on yield. The pollen diversity and richness collected by honey bees was not influenced by hive location or landscape composition and the presence of alternative flowering plants in the surrounding landscape may promote the health of the colony. While the proportion and number of cranberry pollen grains collected did not affect yield, the amount of woodland did and there was, marginally, a greater increase in yield with more cranberry pollen grains in the high- as opposed to low-woodland landscapes. Future studies should examine the mechanism behind such potential interactions.
not in low-woodland habitats. Gaines-Day and Gratton (2016) showed that the relationship between cranberry yield and honey bee hive stocking densities was dependent on the amount of woodland in the surrounding landscape. On marshes surrounded by high amounts of woodland habitat (> 42% within 1 km), there was no relationship between hive stocking density and cranberry yield. However, on marshes with low-woodland habitat in the surrounding landscape, there was a strong relationship between hive stocking density and yield. These results suggest that proximity to woodland influences honey bee foraging on cranberry but further work should elucidate the mechanism behind these patterns.
Fig. 5. Effect of the proportion of cranberry pollen grains on cranberry yield (A) for marshes separated by landscape types (high- and low-woodland). Effect of the number of cranberry pollen grains on cranberry yield (B) for marshes separated by landscape types (high- and low-woodland). The solid lines show the regression line fit to the data and the gray envelope shows the standard error.
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Declaration of Competing Interest
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None. Acknowledgements We are thankful for the field and lab assistance provided by Katie Hietala-Henschell, Olivia Bernauer, Tierney Bougie, Elissa Chasen, Miguel Hernandez, Scott Lee, Erin McMahan, Keith Phelps, Emma Pelton, Walter Salazar, Janet Van Zoeren, Kelly Wallin, and Eric Weisman, as well as the University of Wisconsin-Madison Herbarium and the Paskewitz Lab for their support. We are grateful to the cranberry growers and bee keepers for collaborating on this project and so graciously sharing their expertise and resources. We also thank the Wisconsin Cranberry Board Inc., Cranberry Institute, and Ocean Spray Cranberries Inc. for funding this research. Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.agee.2019.106624. References Aizen, M.A., Garibaldi, L.A., Cunningham, S.A., Klein, A.M., 2009. How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Ann. Bot. 103 (9), 1579–1588. https://doi.org/10.1093/aob/mcp076. Aizen, M.A., Harder, L.D., 2009. The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr. Biol. 19 (9), 915–918. https:// doi.org/10.1016/j.cub.2009.03.071. Alaux, C., Ducloz, F., Crauser, D., Le Conte, Y., 2010. Diet effects on honeybee immunocompetence. Biol. Lett. 6 (4). https://doi.org/10.1098/rsbl.2009.0986. Andersson, P., Koffman, A., Sjödin, N.E., Johansson, V., 2017. Roads may act as barriers to flying insects: species composition of bees and wasps differs on two sides of large highway. Nat. Conserv. 18, 41–59. https://doi.org/10.3897/natureconservation.18. 12314. Arenas, A., Kohlmaier, M.G., 2019. Nectar source profitability influences individual foraging preferences for pollen and pollen-foraging activity of honeybee colonies. Behav. Ecol. Sociobiol. 73, 34–43. https://doi.org/10.1007/s00265-019-2644-5. Artz, D.R., Allan, M.J., Wardell, G.I., Pitts-Singer, T.L., 2013. Nesting site density and distribution affect Osmia lignaria (Hymenoptera: Megachilidae) reproductive success and almond yield in a commercial orchard. Insect Conserv. Divers. 6 (6), 715–724. https://doi.org/10.1111/icad.12026. Bates, D., Maechler, M., Bolker, B., Steve Walker, S., 2015. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67 (1), 1–48 < doi:10.18637/jss.v067.i01 > . Bhattacharya, M., Primack, R.B., Gerwein, J., 2003. Are roads and railroads barriers to bumblebee movement in a temperate suburban conservation area? Biol. Conserv. 109 (1), 37–45. https://doi.org/10.1016/S0006-3207(02)00130-1. Blaauw, B.R., Isaacs, R., 2014. Flower plantings increase wild bee abundance and the pollination services provided to a pollination‐dependent crop. J. Appl. Ecol. 51 (4), 890–898. https://doi.org/10.1111/1365-2664.12257. Broussard, M., Roa, S., Stephen, W.P., 2011. Native bees, honeybees, and pollination in Oregon cranberries. HortScience 46 (6), 885–888. https://doi.org/10.21273/ HORTSCI.46.6.885. Calderone, N.W., 2012. Insect pollinated crops, insect pollinators and US agriculture: trend analysis of aggregate data for the period 1992-2009. PLoS One 7 (5), e37235. https://doi.org/10.1371/journal.pone.0037235. Cane, J.H., Schiffhauer, D., 2001. Pollinator genetics and pollination: do honey bee colonies selected for pollen-hoarding field better pollinators of cranberry Vaccinium macrocarpon? Ecol. Entomol. 26 (2), 117–123. https://doi.org/10.1046/j.13652311.2001.00309.x. Cane, J.H., Schiffhauer, D., 2003. Dose-response relationships between pollination and fruiting refine pollinator comparisons for cranberry (Vaccinium macrocarpon [Ericaceae]). Am. J. Bot. 90 (10), 1425–1432. https://doi.org/10.3732/ajb.90.10. 1425. Colwell, M.J., Williams, G.R., Evans, R.C., Shutler, D., 2017. Honey bee‐collected pollen in agro‐ecosystems reveals diet diversity, diet quality, and pesticide exposure. Ecol. Evol. 7 (18), 7243–7253. https://doi.org/10.1002/ece3.3178. Concepción, E.D., Díaz, M., Kleijn, D., Báldi, A., Batáry, P., Clough, Y., Gabriel, D., Herzog, F., Holzschuh, A., Knop, E., Marshall, E.J.P., Tscharntke, T., Verhulst, J., 2012. Interactive effects of landscape context constrain the effectiveness of local agrienvironmental management. J. Appl. Ecol. 49 (3), 695–705. https://doi.org/10. 1111/j.1365-2664.2012.02131.x. Cook, S.M., Awmack, C.S., Murray, D.A., Williams, I.H., 2003. Are honey bees’ foraging preferences affected by pollen amino acid composition? Ecol. Entomol. 28 (5), 622–627. https://doi.org/10.1046/j.1365-2311.2003.00548.x. Cunningham, S.A., Le Feuvre, D., 2013. Significant yield benefits from honeybee pollination of faba bean (Vicia faba) assessed at field scale. Field Crops Res. 149, 269–275.
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