Grower and farm characteristics

NY and PA demographics were largely similar with some notable differences in farm size, diversity and surrounding habitat (Table 2 summarizes results for questions on grower and farm characteristics). On average, growers in our study region had close to 100 acres in apple production, harboring over 15 varieties. Across states, fewer than 10% of growers had more than 200 acres in apple production. Twice as many PA growers owned orchards smaller than 10 acres than NY growers. Percent grower income derived from apple was distributed evenly among three collapsed categories: 0–25, 25–75, 75–100%, and increased significantly with orchard size (χ₃² = 164.6, P < 0.0001; Fig. 1; question only asked in NY 2012 questionnaire). Crop diversity was higher, but diversity of surrounding habitat types lower for PA growers. Significantly more PA participants grew stone fruit (χ₁² = 39.4, P < 0.001) and vegetables (χ₁² = 8.6, P = 0.003) in addition to apple. NY growers reported a full gradient of habitat types surrounding their orchards with agriculture, mixed and forest being the most common. In contrast, most PA orchards seemed to be surrounded by either forest or agriculture and little in between. Thus, we recorded a continuum of operation size and amount of natural habitat adjacent to orchards across study regions, with more specialized, commercial apple growers in NY than PA.

Fig. 1. Correlation between financial reliance of growers on apple production and amount of land planted in apple.

Table 2. Grower demographics, New York (2009 and 2012) and Pennsylvania apple 2010

s.e.m. provided with means in parentheses. Blanks indicate the questions or specific responses were not included in surveys.

In terms of pest management strategies, a majority of growers in both states reported using primarily IPM practices. Both PA and NY have well-established IPM programs, developed over the last 40 yr for apple production systems by state, land grant institutions (Kovach and Tette, Reference Kovach and Tette1988; Rajotte et al., Reference Rajotte, Bowser, Travis, Crassweller, Musser, Laughland and Sachs1992). By incorporating reduced-risk pesticides (Agnello et al., Reference Agnello, Atanassov, Bergh, Biddinger, Gut, Haas, Harper, Hogmire, Hull, Kime, Krawczyk, Mcghee, Nyrop, Reissig, Shearer, Straub, Villanueva and Walgenbach2009), sex-pheromone-based mating disruption products (Joshi et al., Reference Joshi, Hull, Rajotte, Krawczyk and Bohnenblust2011), as well as pest monitoring and forecasting tools (Damos and Savopoulou-Soultani, Reference Damos and Savopoulou-Soultani2010), IPM offers reduced-risk pest management programs that are environmentally safer than conventional pest management programs in commercial fruit production (Agnello et al., Reference Agnello, Atanassov, Bergh, Biddinger, Gut, Haas, Harper, Hogmire, Hull, Kime, Krawczyk, Mcghee, Nyrop, Reissig, Shearer, Straub, Villanueva and Walgenbach2009; Biddinger et al., Reference Biddinger, Leslie and Joshi2014). Up to a quarter of growers continue to rely on conventional pest management; fewer than 10% of growers manage their orchards organically. Organic apple production is relatively rare in the study region due to high disease and pest pressure (Agnello et al., Reference Agnello, Reissig, Kovach and Nyrop2003). Thus, a majority of growers across the region currently follow pest management programs that encourage diligent use of pesticides, by monitoring pest pressure and spraying only when pest damage causes economic harm (Agnello et al., Reference Agnello, Atanassov, Bergh, Biddinger, Gut, Haas, Harper, Hogmire, Hull, Kime, Krawczyk, Mcghee, Nyrop, Reissig, Shearer, Straub, Villanueva and Walgenbach2009; Jones et al., Reference Jones, Brunner, Grove, Petit, Tangren and Jones2010); such practices have the potential to be readily modified to accommodate pollinators in commercial apple production (Biddinger and Rajotte, Reference Biddinger and Rajotte2015).

Pollination strategies

Concern over reliable pollination was high among all growers. Study-wide, between 36 and 52% growers reported having experienced limited apple pollination due to inadequate visitation by pollinators (see Table 3 for results summary of questions addressing pollination strategies). Several growers commented that bad weather was an important driver of low bee activity. A particularly wet spring in 2011 and cold spring in 2012 may have contributed to higher reports of pollination limitation in 2012 as compared with 2009 in NY. Providing a Likert scale of response options (i.e., always, frequently, sometimes, never, don't know) in the two most recent surveys revealed that for the majority of growers, pollinator limitation occurs only sometimes. Only 2–5% of blossoms, compared with 80% for cherry, need to be set for a viable commercial apple crop; however, growers seek higher pollination rates to maximize fruit quality, which, ultimately, dictates market value (Westwood, Reference Westwood1993). Because the king bloom (the center flower of a five-flower cluster) produces the largest fruit, growers will overpollinate to ensure high set of king bloom and thin blossoms (chemically or mechanically) to avoid biennial bearing.

Table 3. Pollination strategies and concerns among New York and Pennsylvania apple growers

Recent declines in honeybee populations due to CCD were considered a threat to successful apple production by the majority of growers surveyed, but a sizeable percentage were uncertain about the impacts of CCD (Table 3). Grower concerns over the negative impacts of CCD on pollination services echo those found among blueberry growers in Maine (Hanes et al., Reference Hanes, Collum, Hoshide and Asare2015).

To our surprise, only about 50% of growers reported renting honeybees for apple pollination in both NY and PA (χ₁² = 2.1, P = 0.2; Table 3). The probability of renting bees increased directly with farm size (χ₁² = 11.8, P = 0.001, Fig. 2) and was similar between states (state × acre: χ₁² = 2.7, P = 0.1). Because number of pollinators required for adequate pollination increases directly with farm size, smaller orchards likely do not need supplemental honeybees if located near other operations that rent hives or semi-natural habitat that supports native pollinators (Park et al., Reference Park, Blitzer, Gibbs, Losey and Danforth2015). Growers renting honeybees stocked their orchards at similar densities (NY: 2.5 ± 0.4 hives/ac, n = 181; PA: 1.9 ± 0.2 hives/ac, n = 44; t ₂₂₃ = 0.752, P = 0.5) and paid comparable prices per hive (NY: $63.90 ± 2.8; PA: $59.30 ± 4.40; t ₁₅₁ = 0.631, P = 0.5). In NY, regardless of farm size, a majority of growers considered honeybee rentals a minor to moderate expense. Similar results were found for PA growers with <100 acres in apple production; however, most large-scale PA growers, with 100–500 acres in apple (n = 6), described honeybee rentals to be a major expense (within PA, χ₁₅² = 26.6, P = 0.03). For most producers, hive prices may not have yet inflated to the point where growers would be economically motivated to invest in other pollinator strategies, especially if there is perceived risk in doing so. In PA, a network of growers, including large-scale operations, have demonstrated that adequate pollination can be achieved by relying on native bees alone (Biddinger, pers. obs.). Such demonstrated success is testimony that hive rentals are unnecessary in some orchards within the study region and likely inspire others to try alternative pollination even if economic benefits are not major.

Fig. 2. Proportion of apple growers in New York (NY) and Pennsylvania (PA) that reported renting honeybees for pollination increased with farm size. NY grower surveys were conducted in 2009 (NY09) and 2012 (NY12).

Grower adoption of bumble bees, as an alternative managed pollinator, was not trivial; however, use and awareness of mason bees was low. In NY and PA, 16.7 and 24.3% growers, respectively, reported using bumble bees, at least, sometimes. Few growers reported having used commercial mason bees for apple pollination, with a study-wide maximum of 8% growers in PA. Commercial bumble bees are more expensive than honeybees, but forage more reliably in cooler, early spring temperatures (Goulson, Reference Goulson2003). Mason bees specialize on fruit trees and are highly effective pollinators (Bosch and Blas, Reference Bosch and Blas1994). The native blue orchard bee, Osmia lignaria, is rarely collected in NY (Park et al., Reference Park, Blitzer, Gibbs, Losey and Danforth2015) or PA orchards (Joshi et al., Reference Joshi, Leslie, Rajotte, Kammerer, Otieno and Biddinger2015, Joshi et al., Reference Joshi, Otieno, Rajotte, Fleischer and Biddinger2016); however, the introduced Japanese horn-faced bee, O. cornifrons, is well-established throughout the east coast. There is interest in further developing O. cornifrons as an alternative managed pollinator in our study region (Biddinger et al., Reference Biddinger, Joshi, Rajotte, Halbrendt, Pulig, Naithani and Vaughn2013a, Reference Biddinger, Robertson, Mullin, Frazier, Ashcraft, Rajotte, Joshi and Vaughnb; T. Pitts-Singer pers. comm.).

Regardless of year and state, almost all (>93%) surveyed growers reported that they already considered pollinator safety when applying pesticides in orchards. Across the study region, apple is an intensively sprayed fruit crop due to intense pest and disease pressure (Agnello et al., Reference Agnello, Atanassov, Bergh, Biddinger, Gut, Haas, Harper, Hogmire, Hull, Kime, Krawczyk, Mcghee, Nyrop, Reissig, Shearer, Straub, Villanueva and Walgenbach2009). Orchard pesticides have been shown to impact both managed and wild pollinators (Biddinger et al., Reference Biddinger, Robertson, Mullin, Frazier, Ashcraft, Rajotte, Joshi and Vaughn2013b; Mallinger et al., Reference Mallinger, Werts and Gratton2015; Park et al., Reference Park, Blitzer, Gibbs, Losey and Danforth2015). Aside from intrinsic motivations to protect pollinators, growers have many practical reasons to be cognizant of pollinators when considering their pest management options: (1) adequate fruit set for crop production depends on adequate pollination; (2) growers often pay to have bees in the orchard, so harm to bees would be financially counterproductive; and (3) label guidelines restrict the use of insecticides during bloom when bees are most active in orchards. Judicious use of insecticides during bloom is important to reduce pesticide risk for pollinators; however, care should also be taken outside the bloom period. Pollinators are active within orchards before and after apple bloom, foraging ground cover floral resources and/or nesting. Care must also be taken when using pesticides traditionally considered safe for bees, such as fungicides and herbicides. Both fungicides and insecticides applied when apple was not in bloom decreased wild pollinator, but not honeybee, visitation and diversity in NY orchards (Park et al., Reference Park, Blitzer, Gibbs, Losey and Danforth2015). The lack of a measurable response of honeybees to pesticides likely results from placing hives in orchards only during bloom and to the tendency of honeybees to forage on non-apple resources at larger spatial scales than wild bees (McArt et al., Reference McArt, Fersch, Milano, Truitt and Böröczky2017). Precautions taken by growers during bloom are, therefore, inadequate to maximize pollination services by wild bees. Efforts to promote alternative bee pollination services should, therefore, raise awareness of the vulnerability of alternative pollinators to pesticide applications throughout the growing season.

Knowledge and perceptions of native pollinators

Grower estimates of bee diversity were relatively low, and half of our NY 2012 questionnaire respondents chose don't know when given this option. Choosing from a range of values (NY:1, 10, 30, 40, 100; PA:1, 10, 50, 100, 200, 300), growers estimated that apple flowers are visited by a median of ten bee species, compared with 100 and 52 bee species recorded in field surveys in NY and PA, respectively. Grower estimates, however, approached cumulative bee species richness netted within a single orchard (NY: 15–51 and PA: 10–25). Additionally, low species estimates may reflect a lay person's ability to accurately identify bees based on easily recognizable morphological groups. Bee species are commonly distinguished by characteristics only visible under a microscope, making it challenging to differentiate species in the field. For this reason, native bees are commonly lumped into morphological groups (e.g., ‘metallic green bee’) to facilitate observations of bee visitation by lay persons. Following ‘Pennsylvania Citizen Scientist Pollinator Guide’ (Donovall and vanEngelsdorp, Reference Donovall and vanEngelsdorp2008), apple bees in our study region represent 12 distinct morphological groups, which mirror median grower diversity estimates of ten species. In sum, growers demonstrated a wide knowledge gap in terms of sheer diversity of native pollinators, with many simply unwilling to guess. This gap parallels the general public's lack of pollinator literacy, having only recently considered non-honey bee species as important crop pollinators. Of the respondents who did provide diversity estimates, many possessed an accurate local, lay knowledge of the bee fauna visiting their orchards.

In biological surveys, native bee abundance and species richness were significantly and positively influenced by the amount of semi-natural area close to orchards but not by orchard size (Table 4, Joshi et al., Reference Joshi, Otieno, Rajotte, Fleischer and Biddinger2016). We, therefore, predicted that grower estimates of bee diversity may be higher among growers whose orchards were surrounded by semi-natural areas (i.e., forest, mixed, meadow), but no such relationship was observed (Table 5). Nor did we observe an effect of the number of acres a grower had in apple on their bee diversity estimates. Whether we measured a lack of awareness of the bee fauna visiting orchard or, again, an inability to distinguish bee species is unclear.

Table 4. Effects of orchard size and percent semi-natural areas within a 1 km buffer of orchard on bee abundance (GLMM) and observed bee species richness (GLM) in New York State

For bee abundance [ln(y + 1) transformed], covariates temperature [ln(x) transformed] and year, as well as a random farm factor were included. All predictors but year were mean centered. Coefficients are not back-transformed. ‘–’ indicates the predictor was not included in the full model.

Table 5. Effects of state, operation size and habitat adjacent to orchards on (1) grower estimates of native pollinator diversity in apple orchards, (2) whether growers considered native bees valuable to apple pollination and (3) whether growers had considered relying exclusively on native bees

Habitat categories were collapsed into agriculture, natural and other. ‘Other’ included mixed and suburban habitats. For estimates of bee diversity, a negative binomial GLM was employed and reduced via backwards stepwise regression. Predictors that were not significant (at α = 0.05) but contributed significantly to model fit were retained. Multinomial logistic regressions were conducted on response variables with three levels: yes, no and maybe and were not reduced. Coefficients in multinomial logistic regression are log odds ratios. Significant effects are bolded.

We recorded a high appreciation for native pollinators among grower participants, but again some uncertainty about how much native bees actually contribute to orchard pollination. Native bees were viewed by 85–93% surveyed growers as valuable pollinators in orchards; this high appreciation did not change with farm characteristics or state (Table 5). Blueberry (Hanes et al., Reference Hanes, Collum, Hoshide and Asare2015) and cranberry (Gaines-Day and Gratton, Reference Gaines-Day and Gratton2017) growers shared similarly high appreciation for native pollinators. When asked to rate the value of native bee contributions to apple pollination (PA 2010 and NY 2012 questionnaires), over 50% of growers chose the highest possible ranking (i.e., 53.4% PA: always; 63.6% NY: very important); only 6.4 and 8.2% of NY and PA growers, respectively, reported not knowing the value of native bees for their apple orchards. Across the study region, growers estimated that native bees contribute half of orchard pollination services (NY: 45 ± 1.6%, PA: 51 ± 3.5%; t ₃₀₀ = −1.6, P = 0.1), but individual estimates ranged widely and 20% of respondents expressed that they did not know (available answer in the NY 2012 survey only). When asked whether alternative managed pollinators, such as mason or bumble bees, were important for apple pollination (PA-only question), 68% were evenly split among alternative managed pollinators being always, frequently or sometimes important; 6% reported they were never important; and 29% reported that they did not know. Grower uncertainty in the importance of non-Apis pollinators is understandable: contributions of native bees have only recently been quantified (Ritz et al., Reference Ritz, Biddinger, Rajotte, Sahli and Joshi2012; Mallinger and Gratton, Reference Mallinger and Gratton2015; Blitzer et al., Reference Blitzer, Gibbs, Park and Danforth2016; Park et al., Reference Park, Raguso, Losey and Danforth2016), and efforts to use other managed pollinators are still new.

Over half of the study participants had previously considered relying exclusively on native pollinators (Table 3). As one might expect, more growers who did not rent honeybees (72.4%) had considered relying on native bees than those who did rent honeybees (44.2%, χ² = 63.9, d.f. = 2, P < 0.0001); and yet, almost half the growers who rented honeybees had thought about using alternative pollinators and may be especially receptive to integrated crop pollination (Isaacs et al., Reference Isaacs, Williams, Ellis, Pitts-Singer, Bommarco and Vaughan2017). Whether a grower had considered relying exclusively on native pollinators was most influenced by farm size (Fig. 3, Table 5). As acreage in apple production increased, grower consideration to rely exclusively on native bees decreased (Table 5). In contrast, orchard size did not have a significant effect on bee visitation or diversity in biological surveys (Table 4). Because percent total income derived from apple production increased significantly with acres in apple production (χ² = 151.6, d.f. = 5, P < 0.0001; Fig. 2), we conclude that willingness to risk inadequate pollination decreases as apple becomes a greater source of one's income. Importance of producing high-quality fruit to increase one's crop value and meet consumer expectations likely increases with operation size. Nonetheless, even among the largest apple operations, a third of growers had considered foregoing honeybee rentals.

Fig. 3. Grower consideration to rely exclusively on native pollinators decreased with farm size. NY grower surveys were conducted in 2009 (NY09) and 2012 (NY12).

Grower openness to relying exclusively on native pollinators also depended on state and habitat types adjacent to orchards (Table 5). PA growers (67.2%) were significantly more likely to have considered relying on native bees than NY growers (2010: 51.4%; 2012: 60%). We speculate two compatible reasons for this: (1) PA growers had greater exposure to native bee crop pollination, and (2) growers accurately perceived increased native pollinator activity in orchards surrounded by semi-natural habitat. PA growers may have gained more exposure to the idea of relying on native bees from a network of growers already using such practices successfully and from increased extension activities. First, even before hive rental fees had tripled after CCD hit in 2006, a few large PA growers had successfully experimented with not renting honeybees and relying exclusively on native bees; this success provided other growers with a real demonstration that such a pollination strategy was a viable option for commercial production (Biddinger, pers. obs.). Secondly, pollinator extension in PA was likely more active, before and during the study period, due to the presence of the Center for Pollinator Research at Pennsylvania State University (http://ento.psu.edu/pollinators). Native pollinator extension was conducted by Biddinger, an established, fruit entomologist stationed at the Pennsylvania State University Fruit Research and Extension Center. Native pollinator extension in NY was largely conducted by Park, a student at the time, from 2010 to 2012, in the form of annual grower talks, a pollinator booklet, and a Department of Entomology website (entomology.cornell.edu/wildpollinators). Finally, PA respondents may have represented a more biased pool of participants given they were surveyed at extension events.

Increased PA grower openness to relying on native pollinators could also be linked to PA grower ownership of smaller orchards located near semi-natural areas (Table 2), a documented source of wild pollinators visiting orchards (Watson et al., Reference Watson, Wolf and Ascher2011; Park et al., Reference Park, Blitzer, Gibbs, Losey and Danforth2015). Amount and proximity of adjacent natural areas, primarily forest, was a strong predictor of native pollinator abundance and diversity in our field surveys in NY (Table 4) and PA (Kammerer et al., Reference Kammerer, Biddinger, Joshi, Rajotte and Mortensen2016b; Joshi et al., Reference Joshi, Otieno, Rajotte, Fleischer and Biddinger2016). Congruently, consideration to rely exclusively on native pollinators was significantly lower for growers whose orchards were surrounded by agriculture than for those whose orchards were near natural or mixed/suburban areas (Table 5). Regardless of state differences, these results suggest an awareness among growers about the levels of native pollinator activity occurring within orchards, and a surprising openness to relying exclusively on native pollinators.

To gauge willingness of growers to enhance native pollination, we asked if they would consider low-cost land management practices that would increase native bees in their orchard. Consistent across surveys, a majority of growers indicated that they would consider such action, with 85% PA compared with 50–68% NY growers responding yes. Growers were also asked about their knowledge of and participation in federal cost-share programs, designed to aid grower efforts to create or maintain pollinator habitat. The Food, Conservation and Energy Act of 2008 provided federal funding to conserve and protect pollinators in agricultural ecosystems (Whittingham, Reference Whittingham2011). As a result, growers receive government financial incentives and technical support to adopt pollinator-friendly production practices (Decourtye et al., Reference Decourtye, Mader and Desneux2010). In our study region, native bees are pollen foragers, and a continuous source of mixed floral resources near orchards could be important in conserving and maintaining healthy population of these bees (Kammerer et al., Reference Kammerer, Biddinger, Rajotte and Mortensen2016a, Reference Kammerer, Biddinger, Joshi, Rajotte and Mortensenb). A high proportion of growers (NY: 91%, PA: 75%) reported not knowing about government cost-share programs; of those who did, only 8% of NY and 16% PA growers were enrolled. Thus, apple growers seemed generally open to relying more on native pollinators; however, many were not aware of the resources available to them to enhance native bee habitat in their orchards.

To identify obstacles preventing growers from actively enhancing native pollinator populations in orchards, we asked growers to rank the importance of several factors (from not at all important to very important) that would influence their decision to implement land management changes for native bees (Fig. 4). Of the top three factors, proven effectiveness of native pollinators was most important, clear guidelines to implement management practices was second and environmental stewardship was third. Recent empirical studies now provide strong evidence for the effectiveness and importance of native pollinators for apple production (Ritz et al., Reference Ritz, Biddinger, Rajotte, Sahli and Joshi2012; Mallinger and Gratton, Reference Mallinger and Gratton2015; Martins et al., Reference Martins, Gonzalez and Lechowicz2015; Park et al., Reference Park, Blitzer, Gibbs, Losey and Danforth2016; Blitzer et al., Reference Blitzer, Gibbs, Park and Danforth2016; Russo et al., Reference Russo, Park, Blitzer and Danforth2017). Pollination provided by native bees depends directly on their abundance (i.e., the more bee visits the better the pollination); abundance of native bees varies across orchards due to differences in pesticide use and amount of natural area in the surrounding landscape (Mallinger et al., Reference Mallinger, Werts and Gratton2015; Park et al., Reference Park, Blitzer, Gibbs, Losey and Danforth2015). In order for growers to assess the native pollination services available in orchards, accessible protocols to monitor native bee populations need to be developed (Hanes et al., Reference Hanes, Collum, Hoshide and Asare2015). Citizen science projects, such as the Northeast Pollinator Partnership (http://www.northeastpollinatorpartnership.org/), are a plausible approach to forward such efforts, by (1) gathering large amounts of data on bee abundances, and (2) making data-informed recommendations back to growers about what pollinator strategies they should adopt. Making the scientific evidence on contributions of native pollinators accessible to growers should be a primary goal of future extension efforts.

Fig. 4. Importance of factors that would influence grower decisions to adopt new land management practices to protect or enhance native pollinators.

Growers need adequate technical support and guidance to implement bee-friendly practices (Biddinger and Rajotte, Reference Biddinger and Rajotte2015; Isaacs et al., Reference Isaacs, Williams, Ellis, Pitts-Singer, Bommarco and Vaughan2017). Because native pollination services vary among orchards, depending on pesticide use and surrounding habitat, one cannot prescribe a single strategy that fits all. Site-specific assessment of grower pollination management options would be ideal. For example, growers with orchards near large tracts of forest could potentially rely exclusively on native bee pollination and focus on minimizing impacts of pesticides. In contrast, a grower whose orchards are surrounded by intense agriculture would focus on creating more pollinator habitat. Habitat enhancements for pollinators require technical support, to identify appropriate seed mixes and manage weeds. Growers enrolled in CRP receive technical advice from their local NRCS office, and non-profit organizations are providing increasing guidance nationally (e.g., The Xerces Society). Local extension programs with established ties to the apple industry also have potential to provide technical assistance and are poised to help balance grower needs to control pests and maximize pollination services (Biddinger and Rajotte, Reference Biddinger and Rajotte2015).

Willingness of growers to manage orchards in a manner that would support native pollinators was motivated more by a sense of environmental stewardship than by cost. First, honeybee rentals were not perceived as a major expense by most growers, so if they were considering making changes, it makes sense that motivations not be financial and rather driven by concern for pollinators and their services. Secondly, the fact that cost was not one of the top three motivations may help explain grower lack of interest/awareness in government cost-share programs. Thirdly and most importantly, if a large pool of growers are motivated by environmental stewardship, they are also likely receptive to outreach and support for managing lands in more bee-friendly ways. Pollinator habitat creation at the landscape scale has been forwarded as a means by which society can increase food sustainability, by enhancing native pollination services for crops, and can conserve diversity in agricultural landscapes (Potts et al., Reference Potts, Biesmeijer, Bommarco, Felicioli, Fischer, Jokinen, Kleijn, Klein, Kunin, Neumann, Penev, Petanidou, Rasmont, Roberts, Smith, Sørensen, Steffan-Dewenter, Vaissière, Vilà, Vujić, Woyciechowski, Zobel, Settele and Schweiger2011). For such a coordinated vision to become a reality, additional outreach and extension support on crop pollination are needed (Hanes et al., Reference Hanes, Collum, Hoshide and Asare2015).