The orchards in the region are generally established in south facing slopes on well drained soils and surrounded by a heterogeneous landscape comprising forests (>50%), shrubs, field crops and developed land, which is a typical geography of the eastern Appalachian region (Egan and Mortensen, 2012).

For this study, we selected five commercial orchards with similar management programs (such as pesticide, herbicide, and fruit thinning practices) and which did not stock managed honey bees, bumble bees, or solitary bees for pollination. The orchards were mature at 15–20 years, on semi-dwarf rootstocks, with an average spacing of ~4.5 m between trees by ~6 m between rows (average of about 600–700 trees/ha). Within the Golden Delicious, York, and Honey Crisp varieties of each orchard, apple trees (n = 120/orchard, i.e., 600 trees from five orchards) were individually selected by distance from the edge closest to woodland toward the center of the orchard, marked and referenced with a GPS unit for sampling and bee observations. The distance gradients were same in each study orchard, and were 15, 35, 55, 100, and 200 m from the edge of the adjacent wooded area into the orchard.

Observations were made during optimal weather conditions [i.e., low wind speed (>3.5 m/s), temperature above 16°C, partly cloudy or bright overcast for bee flight (Supplementary Material S1). For each of the two sampling dates per orchard, all flowers on each tree were watched by two trained observers for 1 min between 1000 and 1400 h, during good weather conditions. Each observer stood on either side of the tree to capture all visitations to that side of the tree. Three main pollinator taxa were recorded—A. mellifera, Bombus spp., and solitary bees. In addition, syrphid flies were also counted, but were low in numbers across all study years. Immediately after the pollinator visit observations, we net-collected vouchers of all non-Apis bees for 30 min each at 15, 35, 55, 100, and 200 m from the edge of the adjacent wooded area into the orchard. These bee samples were placed in vials, labeled, and chilled in the field and frozen in the lab until they could be pinned, labeled, and identified. All bees were identified to species (see Supplementary Material S2).

The surrounding landscape was assessed with the National Agricultural Statistical Service (NASS) map layer 2012 and groundtruthed in October 2013. The NASS land-use maps were 30 m raster dateset. The maps were first uploaded in ArcGIS 10.1 and buffer layers were created at increasing spatial scales. These buffers started from the edges of the wooded areas where they were adjacent to the orchards and extended out to 250, 500, and 1000 m to reflect the flight ranges of bees from the wooded adjacent areas that are generally nesting habitats of wild bees (Greenleaf et al., 2007; Zurbuchen et al., 2010). These buffers were then uploaded in Fragstats 4.0 and the metrics were generated at the landscape level for each scale (McGarigal et al., 2012; McGarigal, 2014). We assessed collinearity by using a correlation matrix to eliminate collinear metrics. The following landscape metrics were retained for further analyses: (i) number of patches; (ii) edge density; (iii) largest patch index; (iv) mean proximity index (v) landscape shape index; and (vi) contagion. A description of these metrics is available from http://www.umass.edu/landeco/teaching/landscape_ecology/schedule/chapter9_metrics.pdf (accessed November 2013) and in Supplementary Material S3.

Most foraging activity was recorded closer to the natural woodland; lowest activity was recorded farther into the orchard. The proximity of an apple tree to woodland significantly affected distances that bees foraged into apple flowers in 2011 (R² = 0.601, P < 0.001), and 2012 (R² = 0.186, P = 0.008), but the effect was not significant in 2013 (R² = 0.0164, P > 0.05) (Figure 1).

Honey bees and solitary bees were responsible for the significant decline in foraging activity into the orchard from the woodland edge during the mass flowering period of apples in both 2011 and 2012 (Table 1, Figure 2). Bombus spp. contributed to the overall decline in foraging activity into the orchard in 2011, and were responsible for a slight and significant decline observed in 2013 (P < 0.027, Table 1). During 2013, Apis and solitary bee foraging activity did not significantly change with increasing distance from the orchard edge.

Overall, the landscape at low spatial scales (250–500 m) significantly affected numbers of bee visits to apple flowers. The Mean Proximity Index at 500 m had the highest effect on numbers of bee visits, explaining 48.5% of the total variation in the data (Figure 3).

The Number of Patches at 250 m and Largest Patch Index at 500 m explained 42.6 and 8.8% of the total explained variation, respectively. No other landscape factor significantly affected the number of pollinator visits. Solitary bees had a strong relationship with the Mean Proximity Index while Bombus spp. responded more to Largest Patch Index at 500 m and Number of Patches at 250 m in the RDA ordination. A. mellifera were largely unaffected, but showed a weak relationship with the Mean Proximity Index at 500 m (Figure 3).

Using a univariate linear mixed effects model approach to determine how the above landscape factors affected each bee taxa independent of the other taxas, we found all the bee taxa to be significantly affected by Number of Patches at 250 m, Largest Patch Index at 500 m, and Mean Proximity Index at 500 m (Table 2 and Figure 4).

Generally, solitary bees can fly a few hundred meters, depending on availability of floral resources near their nests (Greenleaf et al., 2007). A. mellifera can forage much further (1100 m) from their nest (Gary et al., 1981) while Bombus spp. forage further away than most species (Greenleaf et al., 2007). Most bee species generally fly further from their nest if food (as floral resources) is in short supply, but fly a short distance to reach a plentiful supply of flowers (such as a mass-flowering apple crop) (Rao and Strange, 2012; Jha and Kremen, 2013; Sheffield, 2014). Pollinators may use natural and semi-natural habitats within agricultural landscapes as refugia. These refugia are important for bees and other insects because they provide alternative habitats for foraging, mating, and nesting (Westrich, 1996). As such, habitats such as woodlands adjacent to apple orchards may be an important source habitat of pollinators that forage on an apple crop (Watson et al., 2011).

In ideal environmental conditions during apple bloom, pollinators constantly move between the natural habitats and crop fields (Garibaldi et al., 2011). Insects that migrate into crop fields to forage for pollen and nectar usually effect pollination in the process (Blitzer et al., 2012). Wild bee species that use semi-natural vegetation will move to crop fields when more resources become available within the crop (such as the mass-flowering apples) than in the natural vegetation (Blitzer et al., 2012). This phenomenon is illustrated in temperate and tropical agroecosystems. In the latter, wild bees from neighboring natural forest fragments increase yields and quality of coffee crops (Klein et al., 2003; Karanja et al., 2010).

Yearly variation in weather and bloom time affected overall bee foraging during our study. In 2011 we observed the highest number of bees foraging on apples. Sampling was done in bright, sunny and warm days and rain did not fall during this period. However, in 2012, spring occurred very early; flowers bloomed early and bees emerged early. Just before apple bloom, temperatures plummeted, and frost occurred (Supplementary Material S1). The bloom period was cold and rainy. Similarly in 2013 frost did not occur during bloom, but was dominated by overcast weather (Supplementary Material S1) and rain. These are not favorable conditions for bee flights (especially smaller solitary bees). Bees require optimal environmental conditions (temperature, humidity, wind) to effectively forage. At the time of apple bloom the only bumble bees we observed were queens in relatively low numbers, so we did not detect a significant association with semi-natural vegetation.

Because bees have limited flight ranges from their nesting locations (Vicens and Bosch, 2000; Kremen et al., 2004; Biddinger et al., 2013), the landscape surrounding a farmland and the resources that the landscape provides, are important for our understanding of bee foraging patterns, bee conservation, and ecosystem services provided by bees. Examination of the landscapes that surround a particular crop has interested landscape ecologists and conservation biologists in order to understand the patterns of bee visitation and pollination services (Kremen et al., 2004; Greenleaf and Kremen, 2006; Winfree et al., 2008; Klein et al., 2012; Cariveau et al., 2013). In this study, we found that landscape composition and configuration positively affected the dominant bee taxa (A. mellifera, Bombus spp., and solitary bees) visiting apple flowers at low spatial scales (up to 500 m around the orchards). Mean Proximity Index at 500 m, the Number of Patches at 250 m, and the Largest Patch Index at 500 m were the three main landscape metrics that correlated positively with bee visitation.

The Mean Proximity Index measures the connectivity of patches within the landscape; it takes into account patch size and distance to neighboring patches (Schweiger et al., 2010). In our study, landscape connectivity at 500 m was positively correlated with bee visitation patterns, especially for solitary bees and A. mellifera, but Bombus spp. visitation to flowers was very low (constituted only 7% of the total 2083 visits by all bees). Habitats that are highly interconnected, i.e., that have a higher Mean Proximity Index, have a better chance to retain high populations of bees and therefore increase pollination activity compared with habitats that are disconnected from one another.

The Largest Patch Index measures the percentage of the total area made up by the largest homogenous patch. Bees in all our study sites preferred to forage in areas with a large homogenous patch up to 500 m around a central point within an apple orchard. This effect can be attributed to the mass flowering of apples that formed the largest proportion of the 500 m spatial scale. In apple production system, large orchards (more than 10 ha per grower, which is >100,000 m²) could easily span beyond 500 m from an orchard's center. Apple bloom period is temporally partitioned so that the mass flowering occurs when few other wild plants or crops are flowering. Furthermore, in our landscape it is not uncommon for mass flowering to have occurred from other rosaceous orchard crops (plum, peach, apricot) in close proximity to apple. However, they do not have much overlap in time. Thus, bees have the opportunity to move temporally among a series of mass flowering tree fruits.

The Number of Patches per unit area at 250 m was positively correlated with bee visitation. More bees, especially Bombus spp., responded to landscapes with more habitat patches, probably because these areas had more nutritional or nesting resources required by these bees. Bombus spp., Apis and some solitary bees are generalist foragers and may require additional resources beyond apple pollen and nectar to supplement their nutritional needs. In areas with multiple habitats, but within the vicinity of a large focal patch (i.e., the mass flowering apple crop), pollinators are moving across crop/non-crop interfaces. The largest diversity and abundance of pollinators is highest at the interface between crop fields and natural vegetation (the ecotone) because these habitats offer more floral and/or nesting resources compared to natural vegetation (e.g., forests, Hagen and Kraemer, 2010). Agricultural and other managed landscapes surely affect the pollinator-plant interactions of adjacent natural habitats.

Results of this study reveal that the effects of landscape configuration on bee visitation were more apparent at smaller spatial scales in apple production system. In general, the landscape in Pennsylvania and the other Mid-Atlantic States is quite heterogeneous. The Mid-Atlantic region is unique in that the landscape therein is a mosaic of different habitats and various land cover types are closer to each other, potentially providing season-long diverse floral resources required by pollinators, which explains the lack of significant results of landscape factors of bee visitation beyond 500 m of an orchard. This landscape structure supports the results of Winfree et al. (2007) with watermelon in the Mid-Atlantic region, who reported no effect of proximity to semi-natural habitats at a high spatial scale (>1000 m), and attributed it to the high heterogeneity of the Pennsylvania and New Jersey landscape. Similar patterns were reported by Lonsdorf et al. (2009) who used a predictive model to map pollination services based on pollinators nesting and floral resource availability and foraging ranges. Their model best fit areas dominated by highly intensive agriculture with low natural or semi-natural cover left (i.e., California and Costa Rica), but not our region (Pennsylvania and New Jersey). They attributed their results for this region to the small-scale heterogeneity defined by high plant diversity and interconnection between similar land cover types offering more nesting and floral resources than in highly intensified landscapes (Tscharntke et al., 2005). Bee foraging behavior in complex heterogeneous landscape (such as Pennsylvania apple orchards) may be more accurately predicted by the refined version of Lonsdorf model, which consider behavioral component into the model (Olsson et al., 2015). At larger spatial scales (e.g., more than 500 m), within heterogeneous landscapes, resources become more abundant and have marginal effects on pollinator visitation because the bees are already meeting their needs without having to forage far from their nests.

In regions with less heterogeneous landscapes such as California, for example, the abundance and diversity of bees strongly influenced by spatial characteristics of the landscape (Collinge, 2010). Farms that are surrounded by a low proportion natural habitat cover (<1% within 1 km of the farm) has a low diversity and abundance of bees and low pollination of crops as a consequence (Collinge, 2010). Bees in such landscapes must fly further from their nests to meet their nutritional requirements. In such scenarios, they may be influenced by landscape context at much higher spatial scales than bees in heterogeneous settings such as Pennsylvania.

To conclude, our study revealed that the magnitude of feral A. mellifera and solitary bee foraging within an apple orchard depends on the proximity of the orchard to an unmanaged habitat such as natural woodland. For purposes of conservation, retention of unmanaged habitats near agricultural areas seems useful in maintaining biodiversity within the landscapes and therefore may help insure pollination. Furthermore, conserving unmanaged habitats in such landscape would also provide additional resources required by pollinators and other beneficial insects such as syrphids and other predatory flies, predatory beetles, spiders, and parasitoids, which in turn help to maintain a healthier community in and near the orchard. Economically, conserving natural areas near the apple orchard system and maintaining standard management practices that are safe to pollinators will ensure sustainable pollination and steady economic returns due to crops receiving sufficient pollination. Our results from landscape structure studies further support and complement the findings of the relationship between bee foraging activity during apple bloom period and the proximity of orchards to unmanaged habitats. We found landscape configuration at smaller spatial scales to be a significant positive determinant of bee visitation. Measures aimed at restoring natural pollinator visitation in and around apple orchards would be more successful if suitable habitats were provided at a smaller spatial scale (i.e., farm level) in heterogeneous landscapes such as Pennsylvania.

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.