We also determine whether hedgerow presence affects wild bee abundance and richness in sunflower fields, and if this, in turn, translates into increased sunflower seed set.Field sites were located in Yolo County, an intensively-farmed agricultural region of California’s Central Valley that contains a mixture of conventionally managed row and orchard crops. The majority of natural and semi-natural habitat in the county is concentrated around the borders of agricultural lands and not embedded within them . We sampled 18 sunflower fields between June and July . Half of the fields were adjacent to bare or weedy edges , and half were adjacent to hedgerows . Sites were paired based on the timing of the sunflower bloom, the sunflower variety , and landscape context. Field pairs were a minimum of 900 m apart to maintain independence . To avoid contamination of varieties, sunflower fields are moved every year; therefore no field was sampled in multiple years although two fields were adjacent to the same hedgerow in different years.In Yolo Co., acreage planted in sunflower has increased by over 55% during the past 5 years . It is the 8th most-planted crop in the region, grossing nearly $28 million USD in 2013 . It is produced mainly for hybrid seed, which is then grown for oilseed or confection. While sunflower is native to North America, the breeding system of sunflower grown for hybrid seed has been altered to be artificially gynodioecious, with separate male-fertile plants and male-sterile plants. For hybrid seed production, rows of male plants are interspersed with rows of female plants. Wild bees predominantly visit male plants to collect pollen for nest provisioning . Although honey bees visit both male and female plants,grow bag gardening workers typically either collect nectar from female plants or pollen from male plants which limits cross pollination events .
Honey bee movement between pollen and nectar producing rows of sunflower is often spurred by interference interactions with wild bees. When a wild bee and honey bee meet on a sunflower head, one or both fly to different sunflower heads or rows . These interactions that increase pollen flow between rows also increase honey bee per visit efficiency, therefore have great potential to heighten seed set . Honey bees were stocked at an average rate of approximately 100 hives per field, or 1.5 hives per acre . We did not evaluate pest management because sunflower fields managed by different companies used similar practices. For example, all companies used pre-emergent herbicides prior to planting and seeds were treated with insecticides and either a fungicide or nematicide. Other management practices, including fertilization, tillage, row width and ratio of male to female rows, are also similar between companies , although irrigation practices vary by field, with the majority using furrow irrigation.To quantify the landscape surrounding each site we created 18 land use categorizations . We then hand digitized National Agriculture Imagery Program within a 1 km buffer around study sites in ArcGIS 10.1 . To determine landscape effects on wild bee populations in sunflower, we examined the proportion of habitat within each buffer that could provide resources to wild bees . This included both natural habitats and altered habitats . Potential pollinator habitat around our study sites varied from 1 to 40%, with a median of 5% . Control and hedgerow sites were paired by landscape context to minimize differences.We established two 200 m transects within each field, perpendicular to the field edge or hedgerow and 100 m apart . We netted and observed pollinators at four distances along these transects: 10, 50, 100 and 200 m from the edge.
We varied the starting sampling location within fields and edges at each study site to reduce conflation of distance with temporal variation in bee foraging behavior, which peaks in the morning and late afternoon . Each site was sampled once, during peak bloom , on a clear day with wind speeds <2.5 m/s and temperatures >18 C between 08:00 h and 14:00 h. We visually observed visitation for 2 min each in two malefertile and two male-sterile 2 1 m plots at each distance. Within hedgerows and edges we haphazardly sampled floral visitors for 2 min in eighth plots containing floral blooms. Only insects that contacted the anthers or stigmas were recorded as floral visitors. We also recorded non-bee visits; these accounted for <1% of all visits and were, for simplicity, excluded from analyses. We were unable to identify bees to species in visual observations; therefore we classified them to citizen science categories from Kremen et al. of all records. We did not include feral Apis in our wild bee categorization because we were unable to distinguish them from managed Apis.Sunflower specialists are more effective pollinators of sunflower than generalist species . We therefore also investigated whether sunflower specialists were more abundant in hedgerow or control field edges using an independent data set from 26 hedgerows and 21 control edges in Yolo Co. . Floral visitors were netted for 1 h in hedgerows and control edges during 4–5 sample rounds between April and August in 2012–2013. We queried this specimen database for sunflower specialist bees, which we defined as primary oligoleges . To assess whether the amount of nearby sunflower in the landscape impacted sunflower specialist presence in field edges in the independent dataset, we constructed 1 km buffers around sites in ArcGIS 10.4 and recorded the proportion of sunflower fields around each site using pesticide spray records , which identify which crop is grown on each parcel, and the California crop improvement sunflower isolation map .We used a chao estimator to evaluate species richness within sites in the R package vegan . To determine the impact of hedgerow presence, field location , and surrounding pollinator habitat in the landscape on wild bee species richness and abundance we used general linear models with Poisson and negative binomial distributions respectively in the R package lme4 .
Both models included an interaction between hedgerow presence and field location. We used raw species richness because we only sampled each site once and some sites contained too few individuals for estimation or rarefaction . We also assessed factors influencing sunflower visitation rates by honey bees and wild bees. Hedgerow presence, distance from hedgerow, and their interaction, potential pollinator habitat and sunflower sex were independent variables. In species richness, abundance and visitation models, site nested within pair was included as a random effect. We evaluated the differences between the community of bees in control edges, hedgerows and crop fields using a per MANOVA on their Chao1 dissimilarities in the R package vegan . We then determined whether male and female sunflower specialist bees utilized hedgerows or control field edges using the independent data set . We modeled counts of bees as the dependent variable with a Poisson distribution in the R package lme4 . Hedgerow presence, proportion of sunflower and potential pollinator habitat within a 1 km radius, bee specialization on sunflower, bee sex and an interaction between specialization and hedgerow presence were the independent variables. Site nested within pair was included as a random effect. To determine which factors impacted sunflower seed set, we used negative binomial generalized linear models in the R package lme4 that accounted for over dispersion in the seeddata . We examined the effect of wild bee abundance and richness on seed set from net and visitation data separately. We used raw species richness because some site distance combinations contained too few individuals for estimation or rarefaction . In all models, sunflower seed set was the dependent variable. In the model for netted bees, independent variables were hedgerow presence, wild bee abundance, wild bee species richness, sunflower company, distance into the field from the edge, and an interaction between netted wild bee abundance and honey bee visitation . For the model including visitation rates, additional explanatory variables included aggregate wild bee visitation to male-fertile and male-sterile flowers, honey bee visitation, and an interaction term between wild bee visitation and honey bee visitation. Site nested within pair was included as a random effect in both models. All continuous variables were scaled /sd. We checked all variables for collinearity , and no collinear variables were included in any model. For example, sunflower head size was correlated with variety. However, varieties were specific to sunflower company, so only sunflower company was retained in the model.Measuring the levels of ecosystem services derived from field edge habitat management in a variety of contexts is critical to demonstrating their efficacy and flexibility. If services are highly variable over time or from site to site, costs may outweigh the benefits and limit the adoption of diversification practices . Although other studies have found that field-edge diversification increase pollinator populations both in edges and fields and enhance pollination services to crops in adjacent fields ,plastic grow bag we did not detect any differences in rates of seed set in sunflower fields adjacent to hedgerow or control edges.
Wild bee richness and an interaction between wild bee visitation and managed honey bee visitation, however, positively impacted seed set; yet these factors were not influenced by hedgerow presence. Proportion of pollinator habitat in the surrounding landscape did not influence the bee community visiting sunflower, despite a large body of evidence supporting strong positive landscape effects . We did find higher numbers of sunflower specialist bees in hedgerows than in control sites. Based on these findings, we conclude that sunflower in not a good candidate crop for field edge enhancements, at least in our study region, although they exhibit potential for supporting populations of sunflower pollinating bees. We detected distinct differences in community composition of wild bees present in edges versus fields. This difference was likely driven by the fact that the dominant bee species found within fields, sunflower specialists, were either rare visitors to or absent from both hedgerow and control edge habitats. We only sampled each site once, therefore increased sampling could lead to more convergence or divergence between bee communities in these habitats. There can be significant overlap between species found in MFC fields and adjacent hedgerows , however species composition in hedgerows has also been shown to more closely resemble bee communities in forest habitat than adjacent crop fields . One factor likely driving the differences in species composition in our study region is the absence of sunflower planted within hedgerows due to concerns about genetic contamination of sunflower crop varieties. Because female sunflower specialists collect only sunflower pollen to provision their nests, they may not be attracted to the resources in hedgerows during the sunflower bloom period, instead being drawn into fields . Nevertheless, assessment of the independent dataset indicated that hedgerows provide important floral resources to sunflower specialist bees, especially males. Male sunflower specialists have been observed investigating honey bees as potential mates, which increases honey bee movement from male-fertile to male-sterile sunflowers and increases their pollination efficacy . Male bees, therefore, likely contribute to the interactive effect between wild bee richness and honey bees on rates of seed set. We found a slight positive effect of wild bee species richness on seed set rates, indicating that a higher number of bee species benefits pollination function in sunflower. Functional complementarity between species can enhance fruit and seed production in a variety of crops . Bee foraging behavior and bee body size can influence within inflorescence foraging, leading to more complete pollination in a single flower . Bee foraging activity can also be affected by preferences for particular weather conditions , temperatures , or preferences for floral phenology leading to temporal complementarity. In almonds, wild bee presence increases the likelihood that honey bees will move between different rows, which leads to higher pollen tube initiation and subsequent fruit set . Both niche complementarity and interspecific interactions likely underlie the positive relationship we detected between richness and seed set . In agreement with past findings , we detected an interactive effect between wild bee and honey bee visitation on sunflower seed set. We did not, however, detect any main effects of wild bee and honey bee visitation, despite strong evidence that wild bees positively increase seed set regardless of honey bee abundance . In order to evaluate the direct contribution of wild bees, other studies have estimated the contribution of wild and honey bee visitation to seed set separately .