470
Views
0
CrossRef citations to date
0
Altmetric
ENTOMOLOGY

Economics of alternative insecticide treatments and pollinators in Winter canola

, , &
Article: 2258859 | Received 12 Jun 2023, Accepted 11 Sep 2023, Published online: 20 Sep 2023

Abstract

In the US central and southern Great Plains, canola (Brassica napus) is a winter annual crop. It is pollinated by insects, particularly native bees and introduced honeybees (Apis mellifera Linnaeus, 1758). Canola is beset by many insect pests. Producers rely on insecticides to kill harmful insects, however, these chemicals can negatively impact pollinators. Our purpose is to provide an economic analysis comparing the positive effects of native bees and introduced honeybees in combination with the pest suppression effects of selective and broad-spectrum insecticides in Oklahoma canola production. We identify the breakeven yield necessary to support the conservation of pollinator habitat in or adjacent to canola fields. Using yields from field experiments, we found that an increase in yield ranging from 28.02 to 162.53 kg/ha from pollination justifies the conservation of pollinator habitat. The number of refuge acres and canola acres dictates the necessary yield increase. Our findings suggest that introducing honeybees for pollination of canola may not be an economically viable choice as pollination services are costly. We include analysis with the base rate of pollination service rate reduced to more closely examine this issue. The breakeven analysis with the reduced rate shows a range of 2.43 to 19.06 hectares of refuge area was needed. This analysis varies with annual crop returns and acres of canola planted. This study provides a deeper understanding of the costs and potential benefits associated with pollinator refuges and canola production and allows producers to make more informed decisions about wild pollinators and reliance on introduced honeybees.

1. Introduction

Pollination is essential to agricultural production worldwide (Klein et al., Citation2007). Pollinators are required for production of some crops and enhance production in others. Furthermore, the diversity of pollinator communities may influence crop yields (Hoehn et al., Citation2008). Their findings across three continents and 33 pollinator-dependent crops show that flower-visitor density is the most important predictor of crop yield. Previous studies in canola (Brassica napus) suggest that although canola is self-compatible (self pollinating), it benefits from insect pollination (Mazzei et al., Citation2021; Sabbahi et al., Citation2005). Sabbahi et al. found that the introduction of honeybee hives increased canola yields (Sabbahi et al., Citation2005).

Many field crops in the United States are grown intensively as monocultures which potentially decreases suitable habitat for native pollinators and foraging efficiency in agricultural landscapes. Flowering field crops may temporarily provide sustenance to pollinator populations such as bees, but long-term resources are often needed to sustain a pollinator population. One such flowering crop in the state of Oklahoma is canola. As the only rotational winter crop in Oklahoma (Elliott et al., Citation2014), canola is highly attractive to pollinators (Diekötter et al., Citation2010) and provides abundant floral resources in early spring when few floral resources are available (Eberle et al., Citation2015) in this region. While it has long been thought that pollination by native bees or introduced honeybees (Apis mellifera) leads to additional yields in crops, research on self-pollinated rapeseed plants like canola indicates variability in yield benefits even when introduced honeybees are utilized (Elzay & Baum, Citation2021; Williams, Citation1985). However, in Canada, canola yields and profits were shown to increase with increased uncultivated land surrounding canola fields because they serve as habitat for pollinators (Morandin & Winston, Citation2006). Morandin & Winston, findings agree with previous research suggesting that bee pollinator services can be conserved in a landscape and sowing arable margins of crop fields with a mixture of wild grass, legumes, and wildflowers or allowing natural regeneration of habitat in these areas may provide necessary habitat heterogeneity for pollinators (Carvell et al., Citation2007; Morandin & Winston, Citation2006). Also, a 2013 survey of the literature (Asbjornsen et al., Citation2014) concluded that within field diversification accomplished using narrow strips of perennial vegetation throughout the field can conserve pollinators as well as insect predators of insect pests. Heterogeneous landscapes such as strips of fallow land growing wild or planted into habitat suitable for pollinators can double as habitat of natural insect predators. Elliott et al. found the predator abundance of cereal aphids (Homoptera: Aphididae) in wheat increases with vegetational diversity within field and by increasing the amount of non-cultivated land surrounding wheat (Triticum aestivum) fields (Elliott et al., Citation1999). Altogether, maintaining or increasing vegetational diversity in agricultural landscapes are ways to conserve beneficial pollinators and natural enemies that have been shown to provide ecosystem services that optimize crop yields.

Producers can also actively provide pollination services to their crops through use of managed honeybee hives. Reliance upon managed honeybees to provide pollination services has grown as has the frequency of large monocropped farms (Rucker et al., Citation2012). Each year, beekeepers move hives across the United States from farm to farm, charging pollination fees as the crops bloom (Rucker et al., Citation2012). Rucker et al. estimates that pollination services cost growers approximately $350 million each year (Rucker et al., Citation2012). However, pollination services are also provided by native bee species. Some research suggests native pollinators have the capacity to fulfill pollination needs of some crops and enhance the pollination of others. Garibaldi et al. evaluated the difference in fruit set for over 20 different crops when pollinated by native pollinators exclusively versus being pollinated by domesticated honeybees (Garibaldi et al., Citation2013). Their findings suggest flower visitation by native pollinators produces enhanced fruit set and native pollinator abundance is dependent upon available habitat. Therefore, Garibaldi et al. considers wild insect honeybee colonies a supplementary service rather than a substitute service as wild insect visitation increased fruit set more than that of honeybee visitation (Garibaldi et al., Citation2013). It should be noted besides additional costs incurred by introducing managed honeybees, introduced honeybees may have deleterious effects on native populations from the spread of pathogens, parasites, or competition for resources (Mallinger et al., Citation2017). In agricultural landscapes lacking appropriate habitat for native pollinators, producers may rent hives of managed honeybees. In these instances, supplementing pollination efforts with managed honeybees may be an attractive option for producers, however, pollination benefits must increase above the costs associated with utilizing managed honeybee hives.

Multiple studies have documented the negative effects of pesticides on bees. Feltham et al. found a relationship between the neonicotinoid imidacloprid and reduced foraging efficiency in bumble bees (Bombus terrestris Linnaeus, Citation1758) (Feltham et al., Citation2014). Their findings indicate bumblebees exposed to imidacloprid bring back less pollen, a necessary source of protein, to the colony (Feltham et al., Citation2014). Stanley and Raine determined exposure to imidacloprid alters the foraging behavior of bees and consequently prevents learning of how to quickly visit flowers (Stanley et al., Citation2016). These studies clearly indicate lethal dosages of pesticides do not have to occur for a colony to fail, instead pesticides may alter behavior decreasing foraging efficiency, and ultimately bumblebee colony fitness.

Insecticide use on canola in Oklahoma is common because aphid pests regularly cause yield loss (Franke et al., Citation2017). Aphids regularly decrease yields in canola by over 30% (Buntin & Raymer, Citation1994) and electing not to use an insecticide often results in net losses. Available broad-spectrum insecticides labeled for aphid control in winter canola

(Pyrethroids) can directly kill foraging bees, while other insecticides have sublethal (Sulfoxaflor) or no expected effects (Flonicamid) (Morita et al., Citation2007; Royer & Giles, Citation2017; Smith & Stratton, Citation1986). It is plausible that crops which benefit from pollination may have lower net-returns if insecticides kill or potentially impair bee behavior and pollination. In these crops, the choice to rent managed honeybees will also negatively affect net revenue if pollination benefits are less than the costs of renting bees. If no significant difference exists between yields of fields pollinated by native bees exclusively and fields pollinated by managed honeybees, then renting hives leads to a decrease in overall net revenue.

Despite evidence suggesting creating pollinator habitat may lead to crop yield increases, growers may not understand or know the opportunity costs of practice (Nalepa et al., Citation2021). Estimating the economic value of pollinator services would assist producers in making more informed decisions when allocating resources to conserving or creating pollinator habitat in the landscape. Canola producers in Oklahoma and other southern plain states would benefit from an understanding of the relationships among pollinators and their services, landscape habitat diversity, pesticide use, and canola yields.

Here, we are concerned with the relationship between expected cost to produce winter canola and insecticide choice, conserving land as pollinator habitat, and estimated pollination services. Our goal was to develop an economic analysis of these factors at the canola field level, while also comparing pollination services between native bees and introduced honeybees. Budgets and estimated revenues were developed to determine the expected profit maximizing canola system. These budgets were used to evaluate expected revenues from yields during a two-year experiment conducted in north-central Oklahoma. The experiment introduced honeybees during flowering to increase pollination in canola. The fields receiving introduced honeybees may have ambient native bees and the fields without introduced honeybees may still have foraging honeybees in them. The results presented in this study contribute towards ongoing research assessing the optimal location and size of native pollinator habitat, optimal use of pesticides for aphid control in canola, and justified use of introduced honeybees to increase pollination services.

2. Data and assumptions

Yield data were obtained from recent field-level trials by Giles and Baum (Citation2017). Experiments began each fall with the planting of commercial winter canola. Since canola is typically rotated with winter wheat in the state of Oklahoma, field locations changed each year. All fields in the study had native bee communities present. Additionally, some fields had honeybees rented during flowering to increase pollination. Ten canola fields (minimum 40 a) were selected in 2015. Four fields were in Medford, OK, four fields were located near Drummond, OK, one field was located near Perry, OK, and one field was located near Cherokee, OK. There was a minimum distance of 5 km between all fields. Fields either utilized introduced honeybees for pollination or had no honeybees (i.e., the ambient native pollinator community provided pollination). Fields utilizing honeybees may have native pollinator communities and fields with only ambient native pollinator communities may have foraging honeybees. In addition, each field was treated with label recommended rates of either Flonicamid, Sulfoxaflor, a broad-spectrum Pyrethoid insecticide, or left as a control with no insecticide treatment. Sulfoxaflor was applied to pre-flowering canola during 2015 and 2016. Flonicamid and pyrethroid treatments were dependent on the identification of aphid infestations within the fields and application varied based on the plant stage and weather. A summary of the number of fields in each pesticide, bee management combination can be found in Table .

Table 1. Number of canola fields in bee pesticide treatment by year, 2015–2016

Cost per hectare of insecticide was calculated using the amount applied to the fields; the costs per hectare were $34.31, $13.31, and $2.30 for Flonicamid, Sulfoxaflor, and the pyrethroid application, respectively. The cost of pollination services for rented honeybees was assumed to $77.56 per hectare serviced as reported by the USDA (U.S. Department of Agriculture, National Agricultural Statistics Service, Agricultural Statistics Board, Citation2017) for the states of Arkansas, Florida, Louisiana, Missouri, Mississippi, New Mexico, Oklahoma, and Texas.

Budgets for a two-year rotation of winter wheat and canola represent a typical canola producer in Oklahoma. Canola harvest was completed by June each year and yields recorded at the field level. In our budgets, canola was priced at $0.26/kg to reflect prices received in Oklahoma (Farmers Grain Company, Citation2020). Wheat prices are assumed to be $0.20/kg.Footnote1 Prices for anhydrous ammonia, urea, and diammonium phosphate (DAP) are an average of the weekly prices from September 2008 to July 2020 as reported by the Illinois Production Cost Archives. Costs of harvest, hauling, and chemical applications came from (Sahs, Citation2019b). Costs of production such as glyphosate, AMS, seed, crop insurance, and repair came from the Oklahoma Canola Systems vs. Continuous Wheat Systems Budget Comparison (DeVuyst et al., Citation2017). Operating note interest rates were assumed to be 7%.

Eight scenarios were constructed to mirror the treatments of the experiment. The following scenarios are considered: Sulfoxaflor with native pollinators only, sulfoxaflor with introduced honeybees, Flonicamid with native pollinators only, Flonicamid with introduced honeybees, pyrethroid with native pollinators only, pyrethroid with introduced honeybees, no pesticide treatment with native pollinators only, and no pesticide treatment with introduced honeybees. The canola yields (kg/hectare) for each scenario are the average of yields harvested from experimental fields in 2015 and 2016. Some treatments did not appear in both years, so in that instance, the average yields for the single year reported were used. These yields appear in Table . To assist producers in determining which insecticide and bee management decision is best for their operation, the point estimate of returns and returns from the high and low observation of each scenario are reported.

Table 2. Yield of canola (kg/ha) by bee pesticide treatment by year, 2015–2016

In addition, a breakeven analysis to compute breakeven refuge hectares by outlining annual crop returns necessary for the maintenance of pollinator refuge areas is provided. To compute the breakeven acres of incorporating native bee refuge, some assumptions are necessary. First, the size of the canola field is required. (Note, because canola is grown only every other year, the acreage is divided by two in crop budgets.) We assume acreages of 16.19 (40 acres), 32.37 (80 acres), and 48.56 hectares (120 acres) rotated between winter wheat and winter canola. Second, refuge hectares are assumed to be permanent cover with no potential for income as the size of refuges may be small and fragmented in and around canola fields. In this analysis, we do not allocate any of the refuge acres to CRP. However, this may be a viable option for some producers. The opportunity cost of refuge hectares was assumed to be the rental rate on cropland for Northcentral Oklahoma (Sahs, Citation2019a).

3. Results and discussion

Point estimates of returns to land, labor, and management by scenario are reported in Table . Within each treatment, native bee pollination scenarios had higher yields than introduced honeybee scenarios. Lower yields and higher per hectare production costs, due to the cost of leased honeybee colonies, resulted in lower per hectare returns for the introduced honeybee scenarios. Within each insecticide treatment, native bee pollination returned the associated introduced honeybee scenario from $103.74 to $195.13 per hectare.

Table 3. Point estimates of returns from treatments

There are reasons to be cautious when interpreting these results. Treatments were not (and cannot be) replicated within the same field.Footnote2 Therefore, differences in yields, and thus returns, may not be due to native versus native + introduced honeybees. Underlying fertility, soil type and structure, slope, cropping history, and weather may be more important drivers of yield and return differences, both within and across insecticide treatments. However, there does appear to be a tendency for fields experiencing only native bee pollination to be higher than those including introduced honeybees. Perhaps, competition between native and introduced honeybees reduces pollination (Angelella et al., Citation2021; Badano & Vergara, Citation2011; Grass et al., Citation2018; Müller, Citation2016). Or fields given a nearly $79.04 per acre cost from introduced honeybee colony rental, the introduced honeybee scenarios require over 131.54 kg yield increasesFootnote3 relative to native bee only fields to cover the cost of honeybee colony rental. The substantial differences in production costs suggest that refuge areas for native bee communities are potentially the most economically advisable strategy for canola producers looking to maximize net-profits.

To assess the range of returns to land, labor, and management of each treatment, the lowest and highest observed yields were evaluated with budgets (too few replications were available to determine the variances of each treatment). Returns from low- and high-yield observations are reported in Table . Again, the tendency is for native bee only fields to have higher returns than fields including introduced honeybees under both low- and high-yield scenarios. Differences in returns across insecticide treatments are driven primarily by the price differences between treatments.

Table 4. Treatment returns from low- and high-yield scenarios

The computation of breakeven refuge acres using current wheat and canola prices can be misleading. Because projected returns to land, labor, and management are negative at the current market prices, breakeven refuge acres are multiples of the cropped acres. Essentially, the calculation shows it is advisable to not grow winter crops. We adjusted crop returns to a more typical value, ranging from $49.40 to $86.45 per hectare. Table summarizes breakeven refuge hectares for 16.19, 32.37, and 48.56 hectares canola fields and annualized crop returns increasing in $12.35 per hectare increments. The primary factor driving these results is not yield differences between fields with native bees only and introduce honeybee treatments. Rather, the primary factor is the high cost of honeybee colony rental. So, we re-evaluated breakeven refuge hectares with colony rental cost half of baseline, or $38.78 per hectare. The resulting breakeven refuge hectares are reported in Table .

Table 5. Breakeven refuge hectares varying annual crop returns and field size

Table 6. Breakeven refuge hectares varying annual crop returns and field size with reduced honeybee colony rental

Breakeven refuge hectares are about one-half of the baseline hectare values.

Another perspective on breakeven analyses is to look at the canola yield increase needed to breakeven on a fixed number of refuge hectares. We considered 2.02- and 4.05-ha refuges with canola field sizes of 16.19, 32.37, and 48.56 ha. Canola price net of harvest and transportation was assumed at $0.20 per kilogram, and the opportunity cost of refuge acres was assumed to be $74.10 per hectare. Table reports the resulting breakeven yield increase required to justify refuge hectares. The results show only modest yield increases are needed to justify maintaining or adding refuge hectares for native bees. Populations of pollinators near and within canola fields are economically advisable at yield increases of at least 28.02 to 162.53 kg per hectare, assuming canola is grown every other year.

Table 7. Breakeven canola yield increase

While refuge hectares potentially increase canola yields and returns, they also have the potential to harm crop yields. Refuges may provide a seed bank for economically damaging weed species, requiring occasional spraying to prevent the spread of seeds. Our experiment provides no data to measure the magnitude of these adverse effects if they are present. However, there is much evidence that restoration of semi-natural areas promotes native pollinator populations (Carvell et al., Citation2007; M’Gonigle et al., Citation2015; Morandin & Kremen, Citation2013). So, some caution is warranted prior to recommending producers establish pollinator refuge areas. Further research is warranted to evaluate these trade-offs. If there are yield and economic advantages because of nearby pollinator refuges, research will need to assess the minimum size area that provides benefit and the range (or distance) of benefits. Clearly, there is a maximum distance pollinators, such as bees, can effectively travel and so limits the range of benefits. Knowing that ceiling and the minimum refuge acreage would allow for the optimal placement of refuge acres in a cropping area. Typical foraging distances for native bees range from a few hundred meters to less than 1 km to maximum foraging distances of a couple km, with body size being a good indicator of flight capacity (Zurbuchen et al., Citation2010). However, greater foraging distances (i.e., those close to the maximum possible) may negatively impact reproduction and longevity (Peterson et al., Citation2006; Zurbuchen et al., Citation2010).

4. Conclusions

Past research shows the importance of pollinator services in many important food crops. However, little has been done to evaluate the potential economic value of pollinator refuges in winter canola in the U.S. southern plains. Using budgeting tools and recent yield data from field level trials from Giles and Baum (Giles & Baum, Citation2017), we evaluate breakeven yield increases necessary to support conservation of pollinator refuge hectares within or adjacent to canola-wheat fields in Oklahoma. While production levels and costs may vary, the largest economic influence on the decision to provide pollinator habitat is the opportunity cost from not producing crops on refuge hectares. Our analysis reveals the cost of honeybee rentals accounts for the primary difference in reduced returns. Results show that modest yield increases justify conservation of refuges for native pollinators. However, trial data are not sufficient at this time to definitively determine the necessary refuge area size to support these yield increases. In addition, the potential detrimental impacts of pollinator refuge (i.e. weed seedbank) are considered. Overall, it appears conserving pollinator refuges adjacent to canola fields is economically viable.

Previous studies suggest landscape diversity includes providing pollinator refuges improves crop yields and decreases pest numbers. However, research on the costs of providing habitat and its impact on producer returns has largely been ignored. Budgets incorporating yield data from field trials are useful tools to assist producers in evaluating the economic advisability of added refuge habitat and/or renting honeybee colonies. Our results reinforce recommendations that producers encourage the presence of native pollinators, independent of insecticide choice.

Competing interests

The authors declare none.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Additional information

Funding

Funding provided by the US Department of Agriculture (NIFA: 2017-67019-25919), the Oklahoma Center for the Advancement of Science and Technology PS14-010, and the Oklahoma Agricultural Experiment Station Hatch project OKL03162.

Notes on contributors

Abby ShalekBriski

Abby ShalekBriski is a PhD candidate in the Department of Agricultural Economics and a MS student in the Department of Statistics at Oklahoma State University. Additionally, she is the Assistant Director of Statistical and Data Analysis at the American Veterinary Medical Association. Her research areas includes production and veterinary economics.

Eric A. DeVuyst

Eric A. DeVuyst is a professor and Rainbolt Chair in the Department of Agricultural Economics at Oklahoma State University. His research and extension focus on production economics and farm management.

Kirsten A. Baum

Kristen Baum is a Professor of Integrative Biology and Associate Dean for Research for the College of Arts and Sciences at Oklahoma State University. Her research focuses on the effects of land use and management practices on pollinators.

Kristopher L. Giles

Kristopher Giles is a Regents Professor, Department of Entomology and Plant Pathology, Oklahoma State University, Stillwater, Oklahoma. His research works include studies on Integrated Pest Management, Insect Sampling and Biological Control.

Notes

1. Wheat prices were varied over a range of values with little difference in qualitative results.

2. Bees do not honor treatment boundaries.

3. Includes the added cost of harvest and transportation for the additional yield and interest on operating cost.

References

  • Angelella, G. M., McCullough, C. T., & O’Rourke, M. E. (2021). Honey bee hives decrease wild bee abundance, species richness, and fruit count on farms regardless of wildflower strips. Scientific Reports, 11(1), 1–13. https://doi.org/10.1038/s41598-021-81967-1
  • Asbjornsen, H., Hernandez-Santana, V., Liebman, M., Bayala, J., Chen, J., Helmers, M., Ong, C. K., & Schulte, L. A. (2014). Targeting perennial vegetation in agricultural landscapes for enhancing ecosystem services. Renewable Agriculture and Food Systems, 29(2), 101–125. https://doi.org/10.1017/S1742170512000385
  • Badano, E. I., & Vergara, C. H. (2011). Potential negative effects of exotic honey bees on the diversity of native pollinators and yield of highland coffee plantations. Agricultural and Forest Entomology, 13(4), 365–372. https://doi.org/10.1111/j.1461-9563.2011.00527.x
  • Buntin, D. G., & Raymer, P. L. (1994). Pest status of aphids and other insects in winter canola in Georgia. Journal of Economic Entomology, 87(4), 1097–1104. https://doi.org/10.1093/jee/87.4.1097
  • Carvell, C., Meek, W. R., Pywell, R. F., Goulson, D., & Nowakowski, M. (2007). Comparing the efficacy of agri-environment schemes to enhance bumble bee abundance and diversity on arable field margins. Journal of Applied Ecology, 44(1), 29–40. https://doi.org/10.1111/j.1365-2664.2006.01249.x
  • DeVuyst, E., Epplin, F., Peeper, T., & Boyles, M. (2017). Oklahoma canola systems vs. continuous wheat budget comparison AGEC-257. Oklahoma State University Extension Service.
  • Diekötter, T., Kadoya, T., Peter, F., Wolters, V., & Jauker, F. (2010). Oilseed rape crops distort plant–pollinator interactions. Journal of Applied Ecology, 47(1), 209–214. https://doi.org/10.1111/j.1365-2664.2009.01759.x
  • Eberle, C. A., Thom, M. D., Nemec, K. T., Forcella, F., Lundgren, J. G., Gesch, R. W., Riedell, W. E., Papiernik, S. K., Wagner, A., Peterson, D. H., & Eklund, J. J. (2015). Using pennycress, camelina, and canola cash cover crops to provision pollinators. Industrial Crops and Products, 75, 20–25. https://doi.org/10.1016/j.indcrop.2015.06.026
  • Elliott, N. C., Backoulou, G. F., Giles, K. L., & Royer, T. A. (2014). Parasitism of aphids in canola fields in central Oklahoma 1. Journal of Agricultural and Urban Entomology, 30(1), 59–64. https://doi.org/10.3954/1523-5475-30.0.59
  • Elliott, N. C., Kieckhefer, R. W., Lee, J. H., & French, B. W. (1999). Influence of within-field and landscape factors on aphid predator populations in wheat. Landscape Ecology, 14(3), 239–252. https://doi.org/10.1023/A:1008002528345
  • Elzay, S. D., & Baum, K. A. (2021). Landscape characteristics predict body sizes in wild bees: Implications for pollination services and foraging range. Journal of Insect Conservation, 25(2), 243–253. https://doi.org/10.1007/s10841-021-00294-y
  • Farmers Grain Company. Retrieved September 29, 2020. https://farmersgraincompany.com/markets/cash-grain-bids/
  • Feltham, H., Park, K., & Goulson, D. (2014). Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology, 23(3), 317–323. https://doi.org/10.1007/s10646-014-1189-7
  • Franke, T. C., Kelsey, K. D., & Royer, T. A. (2017). Pest management needs assessment for Oklahoma canola producers March 2017 EPP-7085. Oklahoma State University Extension Service.
  • Garibaldi, L. A., Steffan-Dewenter, I., Winfree, R., Aizen, M. A., Bommarco, R., Cunningham, S. A., Kremen, C., Carvalheiro, L. G., Harder, L. D., Afik, O., Bartomeus, I., Benjamin, F., Boreux, V., Cariveau, D., Chacoff, N. P., Dudenhöffer, J. H., Freitas, B. M., Ghazoul, J. … Klein, A. M. (2013). Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science, 339, 1608–1611. https://doi.org/10.1126/science.1230200
  • Giles, K., & Baum, K. (2017). OCAST pollinator dataset. Unpublished data.
  • Grass, I., Meyer, S., Taylor, P. J., Foord, S. H., Hajek, P., & Tscharntke, T. (2018). Pollination limitation despite managed honeybees in South African macadamia orchards. Agriculture, Ecosystems & Environment, 260, 11–18. https://doi.org/10.1016/j.agee.2018.03.010
  • Hoehn, P., Tscharntke, T., Tylianakis, J. M., & Steffan-Dewenter, I. (2008). Functional group diversity of bee pollinators increases crop yield. Proceedings of the Royal Society B: Biological Sciences, 275(1648), 2283–2291. https://doi.org/10.1098/rspb.2008.0405
  • Klein, A. M., Vaissiere, B. E., Cane, J. H., Steffan-Dewenter, I., Cunningham, S. A., Kremen, C., & Tscharntke, T. (2007). Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences, 274(1608), 303–313. https://doi.org/10.1098/rspb.2006.3721
  • Linnaeus, C. (1758) Systema Naturae per Regna Tria Naturae, Secundum Classes, Ordines, Genera, Species, cum Characteribus, Differentiis, Synonymis, Locis. 10th edition.
  • Mallinger, R. E., Gaines-Day, H. R., Gratton, C., & Raine, N. E. (2017). Do managed bees have negative effects on wild bees?: A systematic review of the literature. PloS One, 12(12), 12. https://doi.org/10.1371/journal.pone.0189268
  • Mazzei, M. P., Vesprini, J. L., & Galetto, L. (2021). Seminatural habitats and their proximity to the crop enhances canola (Brassica napus) pollination and reproductive parameters in Argentina. Crop Science, 61(4), 2713–2721. https://doi.org/10.1002/csc2.20450
  • M’Gonigle, L. K., Ponisio, L. C., Cutler, K., & Kremen, C. (2015). Habitat restoration promotes pollinator persistence and colonization in intensively managed agriculture. Ecological Applications, 25(6), 1557–1565. https://doi.org/10.1890/14-1863.1
  • Morandin, L. A., & Kremen, C. (2013). Hedgerow restoration promotes pollinator populations and exports native bees to adjacent fields. Ecological Applications, 23(4), 829–839. https://doi.org/10.1890/12-1051.1
  • Morandin, L. A., & Winston, M. L. (2006). Pollinators provide economic incentive to preserve natural land in agroecosystems. Agriculture, Ecosystems & Environment, 116(3–4), 289–292. https://doi.org/10.1016/j.agee.2006.02.012
  • Morita, M., Ueda, T., Yoneda, T., Koyanagi, T., & Haga, T. (2007). Flonicamid, a novel insecticide with a rapid inhibitory effect on aphid feeding. Pest Management Science: Formerly Pesticide Science, 63(10), 969–973. https://doi.org/10.1002/ps.1423
  • Müller, H. T. 2016. Interaction between Bombus terrestris and honeybees in red clover fields reduces abundance of other bumblebees and red clover yield [ Master’s thesis]. Norwegian University of Life Sciences, Ås.
  • Nalepa, R. A., Epstein, G., Pittman, J., & Colla, S. R. (2021). Perceptions of wild bees and farm characteristics associated with the uptake of pollinator-supporting land management practices among Canadian apple growers. Renewable Agriculture and Food Systems, 36(4), 1–10. https://doi.org/10.1017/S1742170520000344
  • Peterson, J. H., Roitberg, B. D., & Peterson, J. H. (2006). Impacts of flight distance on sex ratio and resource allocation to offspring in the leafcutter bee, megachile rotundata. Behavioral Ecology and Sociobiology, 59(5), 589–596. https://doi.org/10.1007/s00265-005-0085-9
  • Royer, T., & Giles, K. (2017). Management of insect and mite pests in canola CR-7667. Oklahoma State University Extension Service.
  • Rucker, R. R., Thurman, W. N., & Burgett, M. (2012). Honey bee pollination markets and the internalization of reciprocal benefits. American Journal of Agricultural Economics, 94(4), 956–977. https://doi.org/10.1093/ajae/aas031
  • Sabbahi, R., DeOliveira, D., & Marceau, J. (2005). Influence of honey bee (Hymenoptera: Apidae) density on the production of canola (Crucifera: Brassicacae). Journal of Economic Entomology, 98(2), 367–372. https://doi.org/10.1093/jee/98.2.367
  • Sahs, R. (2019a). Oklahoma cropland rental rates: 2018-19 CR-230. Oklahoma State University Extension Service.
  • Sahs, R. (2019b). Oklahoma farm and ranch custom rates, 2017-2018 CR-205. Oklahoma State University Extension Service.
  • Smith, T. M., & Stratton, G. W. (1986). Effects of synthetic pyrethroid insecticides on nontarget organisms. In F. A. Gunther (Ed.), Residue reviews (pp. 93–120). Springer New York. https://doi.org/10.1007/978-1-4612-4934-4_4
  • Stanley, D. A., Raine, N. E., & Ayasse, M. (2016). Chronic exposure to a neonicotinoid pesticide alters the interactions between bumblebees and wild plants. Functional Ecology, 30(7), 1132–1139. https://doi.org/10.1111/1365-2435.12644
  • U.S. Department of Agriculture, National Agricultural Statistics Service, Agricultural Statistics Board. (2017). Cost of pollination. USDA National Agricultural Statistics Service.
  • Williams, I. H. (1985). The pollination of Swede rape (Brassica napus L.). Bee World, 66(1), 16–22. https://doi.org/10.1080/0005772X.1985.11098817
  • Zurbuchen, A., Cheesman, S., Klaiber, J., Müller, A., Hein, S., & Dorn, S. (2010). Long foraging distances impose high costs on offspring production in solitary bees. The Journal of Animal Ecology, 79, 674–681. https://doi.org/10.1111/j.1365-2656.2010.01675.x
  • Zurbuchen, A., Landert, L., Klaiber, J., Müller, A., Hein, S., & Dorn, S. (2010). Maximum foraging ranges in solitary bees: Only few individuals have the capability to cover long foraging distances. Biological Conservation, 143(3), 669–676. https://doi.org/10.1016/j.biocon.2009.12.003