OVERVIEW OF THE STUDY

Commercial honey bee colonies are an integral part of agricultural production in the U.S. Each year, hives are moved across the country to pollinate crops that generate billions of dollars to the agricultural economy. The economic dependence of agricultural sectors on pollination services ranges between $14.2−23.8 billion, but the higher-order economic dependence of industrial sectors that are driven by crop production also is substantial (US $10.3−21.1 billion). The value of crops produced by honey bee pollination cascade through multiple socioeconomic sectors, generating jobs and revenue to small towns and rural areas and to numerous industrial sectors through equipment and machinery manufacturers, agrochemical companies, food processing, shipping and transportation, to name just a few. Honey bee pollinated crops also create export markets that help balance trade deficits. From a perspective of human nutrition, honey bee pollinated crops such as berries, almonds, pome and stone fruits and various seeds are essential to human health and are cornerstones to cancer prevention and heart-healthy diets.

Perhaps no crop is more reliant on honey bees than almonds. Acreages of almonds have been expanding for decades in the Central Valley of California, and by 1973, the pollination needs exceeded the availability of colonies kept in California. Currently, more than a million hives from throughout the U.S. come into the almond growing regions of California to pollinate the nearly 1 million acres (4000 km2) of bearing trees. The almond crop is worth $2.2 billion and adds an estimated $21.5 billion to the California economy and 104,000 jobs in production, processing, manufacturing and marketing.

Though the multibillion-dollar almond crop depends on honey bee pollination, the supply of colonies is unstable. For more than a decade, colony losses have been in excess of 30%. In four of the last five years, losses have been at least 40%. Reasons include poor nutrition, diseases, parasitism by Varroa destructor (Mesostigmata: Varroidae), queen loss, and pesticide exposure. Most colonies are lost from combinations of these factors, and many are lost over the winter. Poor overwintering ​has a particularly strong impact on beekeepers and almond growers, because almonds bloom in February when colonies are naturally at their lowest populations and just beginning to build. Weak colonies cannot rear enough brood to reach sufficient sizes for almond pollination. Colonies that are lost cannot be replaced by splitting stronger ones because in February there are no drones to mate with queens. Therefore, the number of colonies that survive until February are the number available to rent for almond pollination. 

Honey bee colonies have an annual cycle, and management decisions occur within this framework. The cycle begins in the spring with brood rearing, colony growth and reproduction by swarming. Large amounts of forage are needed to optimize colony growth, and almonds can be an excellent early season pollen and nectar source. When almond pollination is over, beekeepers can split their colonies to prevent swarming. The splits also can replace colonies lost over the winter. Throughout the summer, colonies continue to rear brood and grow. However, as fall approaches, egg laying and brood rearing decline and bees store resources in preparation for confinement during winter. In temperate regions, the bees overwinter in a tight thermoregulated cluster surrounding the queen. Alternatively, if colonies are in warmer winter climates typical of southern states or California, bees forage and rear brood throughout the winter. Many colonies used to pollinate almonds are moved from northern latitudes to areas with warmer winters in late fall to overwinter.

There are challenges with placing colonies in areas where bees can rear brood and forage during the winter. Often there are not enough floral resources to keep colonies supplied with nectar and pollen, so beekeepers feed protein supplements and sugar solutions such as high fructose corn syrup (HFCS). Though protein supplements can meet some of the nutritional requirements of honey bees, if pollen is unavailable, colonies will show signs of malnutrition. Populations will decline and there will be increased incidence of disease. HFCS also can present health risks to bees. Keeping colonies in apiaries where bees can forage and rear brood during the winter necessitates monitoring and sampling Varroa populations and possible miticide treatment throughout the fall and winter. If brood is present, Varroa populations can grow as mite reproduction occurs in brood cell. More importantly though, Varroa can migrate intocolonies on foragers particularly in the fall and significantly increase mite populations even in colonies that were previously treated with miticides. Colonies that are infested with mites in the fall have little chance of survival overwinter.

​An alternative overwintering method is to place colonies into cold storage (CS) facilities in the fall. There are advantages to this management strategy. Colonies in CS do not forage, so Varroa cannot enter colonies on foragers after a fall miticide treatment. Bees clustered inside the hive rather than foraging have greater longevity and require fewer resources. The cost of overwintering bees in CS also might be lower than in areas with warm winters if resources are limited and bees need supplemental feeding or additional mite treatments. 

​With the increasing costs of managing and transporting honey bee colonies for pollination, combined with the colony losses beekeepers routinely experience, we compared management costs and survival of colonies overwintered either in apiaries or CS. To do this, we followed 190 commercial honey bee colonies starting in April until the following year just prior to almond bloom. We calculated all expenditures incurred by a commercial beekeeper including salaries, transportation and cost of materials. In the fall, we divided the hives into groups that overwintered either in apiaries in Texas or CS facilities in Idaho. When both groups of colonies were moved from their overwintering sites to almond orchards, we compared the cost of each overwintering strategy. We calculated profit margins based on the percentage of colonies that were large enough to rent for pollination, the cost of the overwintering strategy, and the per colony pollination rental fee. We found that overwintering in CS cost less than in the apiary, but still exceeded our colony rental fees for almond pollination. Our only profitable activity was honey production during the summer. Our study underscores the challenges faced by migratory beekeepers, and their untenable economic position especially if the availability of nectar and pollen sources continue to decline. We conclude with recommendations and possible solutions for maintaining a profitable and sustainable commercial beekeeping industry.

OVERVIEW OF THE STUDY

Our study began in Danbury, Texas where 95 colonies returning from almond pollination in California were split into 190 colonies. A laying European queen was introduced in a self-releasing cage to each of the 190 colonies 48 hrs after making the split. We recorded colony sizes (frames of bees and brood) when they were established, and again in June, September and October. Mite populations were estimated in June and September using an alcohol wash of adult bees and in October using a mite drop count on a sticky board. In the fall, all colonies were fed protein patties (mixture of pollen, brewers yeast, vegetable oil, lemon juice and Pro Sweet Liquid Feed) and sugar syrup (Pro Sweet Liquid Feed) to prepare the bees for overwintering. 

MANAGEMENT ACTIONS AND COSTS:  SPRING - FALL

The cost of splitting 95 hives to create 190 new colonies including the cost of the queens, labor, transportation and feeding sugar syrup was $6651 (Table 1). The hives averaged 7.0 ± 0.1 frames of bees, 4.0 ± 0.1 frames of brood and 1.0 ± 0.09 mites per 100 bees. An additional $4871 was spent during June and July for sugar syrup feeding and for moving the hives from Danbury, Texas to Baldwin, North Dakota, and for miticide treatments. Of the 190 colonies we established in April, 158 were alive in July. The colonies averaged 15.1 ± 0.6 frames of bees. Later in June, the colonies were moved to apiaries in North Dakota for honey production. There were 1.3 ± 0.1 mites per 100 bees in alcohol wash samples before application of HopGuard II®, and 0.18 ± 0.03 mites per 100 bees 48hrs later.

From July through August, the colonies grew, and collected surplus honey so additional hive bodies with frames were added (i.e., hives were ‘supered’). The total cost of managing 158 colonies for honey production (i.e., adding supers to the hives), collecting the honey and extracting it was $3245. The 158 colonies produced 12,160 lbs of honey (77 lbs per hive). The year of the study, extracted unprocessed Dakota honeys sold for $1.67 / lb (USDA-AMS Specialty Crops Program Market News Division, Dec. 23, 2016), so the value of the honey crop was $20,307. Between the time when the colonies were established in April and the honey was removed in August, we invested $15,231 in colony management and honey extraction, so our profit from the 158 hives was $5076 or about $32 per hive. 

​ Between August and September an additional 18 colonies were lost so that we had 140 remaining. The colonies averaged 15.5 ± 0.1 frames of bees, 8.2 ± 0.14 frames of brood, 4.6 ± 0.3 mites per 100 bees prior to the miticide treatment (cost = $1142). An additional 20 colonies were lost between September and October. Specifically, the colonies with high mite numbers in September (i.e. > 8.0 mites per 100 bees) either were dead by October or severely weakened so that they would not survive overwintering. The surviving colonies averaged 14.4 ± 0.2 frames of bees. Ambient temperatures were too low to open hives and measure brood frames or collect adult bees from the brood area for alcohol wash samples. Only mite drop from sticky boards is reported. Prior to miticide treatment, an average of 10.8 ± 0.7 mites dropped on to sticky boards; 48hrs after the treatment there were 61.7 ± 3.7 mites per sticky board. Of the 190 colonies we established in April, we had 120 colonies remaining to overwinter (37% summer loss).

In preparation for overwintering, the colonies were fed a gallon of sugar syrup with Fumagilan ($490), 2 lbs of protein diet and a gallon of sugar syrup with Fumagilin ($1,047), and protein diet one more time in late October (cost = $507). The colonies were moved to holding yards (cost = $220), and treated with a miticide ($2124). Between the time when the 190 colonies were established in April and they were moved to overwintering sites, $20,837 was invested. The investment was offset by the honey harvested from the hives in August that generated $20,307. Prior to overwintering, expenditures for the 190 hives (of which 120 still remained) exceeded income by $530. 

OVERWINTERING MANAGEMENT AND COSTS

In October, equal numbers of colonies were pre - pared for overwintering in either Texas apiaries or CS in Idaho. We added colonies to increase our sample sizes, and divided these evenly between the two overwintering groups (CS and apiaries, n = 72 per group). The additional colonies belonging to our collaborating beekeeper were positioned in the same apiaries in North Dakota, and were managed using similar procedures as ours including the October miticide treatment.

CS colonies were fed sugar syrup 1 week prior to shipment (cost- $236) (Table 2). On November 15, colonies were loaded on to trucks and taken to the CS facility in Idaho. The fee for CS was $8 per hive ($8* 72 colonies = $576 total). Colonies remained in CS until February 1 when they were loaded on to trucks and taken to California for almond pollination (cost - $1515). The total cost of overwintering 72 colonies in CS including transportation costs and labor to load and unload the colonies was $2793.

​A second set of 72 hives was shipped from North Dakota to Texas to overwinter in apiaries. The cost for shipping the hives was $725. When the hives arrived in the apiaries, they were fed protein pat - ties and sugar syrup (cost-$356). The feeding was repeated monthly until February (4 feedings * $356 = $1424) when the hives were loaded on the trucks and taken to California for almond pollination. Transportation to California and loading/unload - ing fees cost an additional $1784. The total cost for overwintering 72 colonies in apiaries was $3705 or about $900 more than in CS.

Of the 72 colonies put into CS, 54 (75%) survived overwinter, and 33 (61%) of these were large enough for almond pollination (> 6 frames of bees). The hives rented for almond pollination averaged 8.3 ± 0.55 frames of bees, 1.7 ± 0.15 frames of brood, and 0.04 ± 0.04 mites per 100 bees. Of the 72 hives that overwintered outdoors in Texas, 86% survived (i.e., 62 colonies) and all were of suitable size for almond pollination. Colonies averaged 9.1 ± 0.4 frames of bees, 2.6 ± 0.1 frames of brood, and 0.15 ± 0.05 mites per 100 bees. Colonies sizes (frames of bees) did not differ between the two overwintering methods, but those overwintered in apiaries had significantly more frames of brood (Table 3).

Total expenditures per colony from September after the honey harvest until colonies were put in almond orchards in February was $205 for colonies overwintered in CS and $228 for those overwintered in Texas apiaries. The rental fee was $165 per colony, so there was a loss of $40 per hive for those overwintered in CS and $63 per colony for those overwintered in apiaries. The value of the colonies that were rented for almond pollination was $5445 for those overwintered in CS (33 hives * $165/colony) and $10,230 for those overwintered in apiaries (62 colonies * $165). Based on the cost of managing colonies from September to February, rental fees and colony losses, we absorbed a loss of $9315 for the 72 colonies overwintered in CS and $6186 for those overwintered in apiaries (profit = (number of colonies rented * $165) – (72 * overwinter costs)). 

COSTS OF COLONY LOSS

​Between the time when we established the colonies in April, and we put them in either CS or apiaries in Texas, 37% were lost. Due to our increased investment in the colonies as time went on, the cost of losing colonies increased as the season progressed (Fig. 1). In April, we invested $7410 to create the 190 colonies, or $39 per colony. The loss of 32 colonies in June was $1248 ($39 * 32). Between August and September, another 18 colonies were lost. By this point, we invested $81 per colony, so the cost of losing 18 colonies in late summer was $1458 ($81 * 18). An additional 20 colonies were lost between September and October. We invested $136 per colony by October, so the loss of the 20 colonies was $2720 ($136 * 20). Not all of the 72 colonies that overwintered in either CS or in the Texas apiary were sufficient in size to rent for almond pollination. Per colony losses for those that died or were too small to rent were $205 for those in CS and $228 for those overwintered in the Texas apiary. If the loss of rental fee is added, we estimate the loss of a colony overwintered in CS as $370 ($205 + $165 rental fee) and in apiaries as $393 ($228 + $165 rental fee). 

IDENTIFYING COLONIES TO OVERWINTER

We put colonies into CS without concern for their size or mite numbers. Totaling the costs of maintaining a colony from September until almond bloom, every colony was a $205 bet that it would be large enough to rent. To reduce our losses, we should have put only those colonies in CS with a high probability of achieving populations suitable for almond pollination. To help beekeepers decide which colonies to overwinter in CS, we used our data to create a decision-making tool to identify colonies in September that will be large enough to rent for almond pollination. To develop the tool, we conducted two analyses. In the first, we found that colony size and mite numbers from alcohol washes in September were significantly correlated with colony size in February for hives overwintered in CS. This relationship was not significant in colonies we overwintered in apiaries. In the second analysis, we generated probabilities of colonies overwintered in CS being of suitable size for almond pollination rental based on September colony sizes and mite numbers. In the analysis, we used > 6 frames of bees in February as a successfully overwintered colony (Fig. 2). The matrix indicates that probabilities of meeting the minimum of 6 frames of bees is greatly influenced by September mite numbers. Even large colonies with more than 12 frames of bees (about 30,000 bees) have a less than 0.5 probability of being suitable for almond pollination if they have 5 or more mites per 100 bees in September. The analysis also indicates that mite numbers need to be controlled in August so that colonies have low mite numbers in September.

 A similar analysis as described above was conducted to create a decision-making tool for colonies overwintered in apiaries. Unlike the CS data, the relationships between colony size and mite numbers in September and October and colony size the following February were not significant. Without significant relationships among these factors, we were unable to generate predictions of which colonies to overwinter in apiaries.

CONCLUSIONS

We managed 190 colonies and recorded all costs from the time of establishment in April until they were placed in almond orchards for pollination the following February. Though we expended considerable resources for feeding and parasite/pathogen control, more than 30% of our colonies died by the fall. Some colonies failed within two months after they were established perhaps due to queen failure since colonies had adequate resources, low mite numbers, and were not exposed to pesticides. The acceptance and retention of introduced queens depends on their health and mating success (i.e., number of spermatozoa in the spermatheca). About 14%–19.0% of commercially produced queens are not fully mated. We lost 17% of the colonies we requeened, well within the range of poorly mated commercially reared queens. We probably also lost colonies from Varroa infestations especially in the fall. Though we treated for Varroa in the summer, some colonies had high numbers of mites in September. These colonies were dead by October or if overwintered in CS had populations that were too small for almond pollination rental. Though statistics on colony losses during the summer and overwinter are available, the value of the colonies and dollars invested in their management can differ greatly. Colony deaths over the winter generate the greatest monetary losses, as they are 5-6 higher than in summer particularly if lost pollination fees are included. 

A surprising finding from our study was that the cost of keeping colonies alive from September (after honey harvest) until almond bloom exceeded pollination fees. Overwintering in CS cost less than in apiaries, but did not assure lower losses or more colonies of suitable size for almond pollination. The only profits we realized were from honey production when our colonies were in North Dakota during the summer. Our summer apiaries were in a region that is part of the Northern Great Plains. About 30-40% of the registered colonies in the U.S. spend the summer in this region because the vast expanses of rangeland and pastures, and large acreages of blooming alfalfa and oilseed crops provide abundant forage for the bees (Gallant et al. 2014; Otto et al. 2016). The Great Plains serves as both a respite for colonies stressed by crop pollination practices, and a source of revenue for beekeepers through honey production. In our study, the profits from honey sales provided the funds for late summer and fall colony management in preparation for overwintering. Based on our honey yields though, the costs for overwintering preparations exceeded the honey profits so we had a net loss. The loss could have been avoided by higher per colony honey yields. However, areas with abundant forage that could generate large honey crops are dwindling in the Great Plains. Acreages of crops such as corn and soybean are increasing, and these not only have limited forage value to honey bees, but also may be contaminated with pesticides. The effects of diminishing access to forage reverberate through both the beekeeping and almond industries, as colonies surrounded by non-forage agricultural crops ​are smaller in the fall and for almond pollination than those in grasslands with natural forage.

The costliest management action we performed after colony establishment was treating for Varroa. We used HopGuard II® during the honey flow at a cost of about $8 per colony in material, and Apivar in the fall at about $10 per colony. We could have reduced our costs by using other mite treatments such as formic acid or thymol (e.g., $4-5 in material per application). Though we applied miticides at regular intervals, mite populations increased in during late summer and fall. The increase may have been from the migration of mites into hives on foragers. Mites can enter hives when foragers rob weak colonies that are heavily infested with Varroa. Foragers with mites also can drift into hives when returning from a foraging flight. Our study site (a commercial apiary) had hundreds of colonies that could have been sources of mites. The weakening and loss of colonies from Varroa in the fall and overwinter are well documented, but because management costs were recorded in our study, we could quantify the financial burden caused by this pest. There was a loss of $80-140 per colony for those lost in the fall, and more than $350 (if rental fees are included) over the winter. Since losses from Varroa most often occur in the fall and winter, the mite is financially devastating to beekeepers and a great threat to the solvency of their operations. 

One way to reduce financial losses from Varroa is to select colonies to overwinter in CS based on their size and Varroa populations in September since these are correlated to colony size in February. We constructed a decision matrix containing probabilities of colonies reaching sufficient sizes for almond pollination given their size and mite numbers in September. Beekeepers can use the decision matrix to select colonies to overwinter in September, and reduce financial losses associated with preparing, transporting and overwintering hives that are unlikely to reach sizes needed for almond pollination. We will continue to refine the predictions from the decision matrix by collecting data with broader ranges of colony sizes and mite populations to improve the decision tool we created for beekeepers. 

Our study began as an economic analysis comparing outcomes of two overwintering strategies. What came to the fore is that reducing colony losses and stabilizing the economics of beekeeping will be difficult, and require cooperation among beekeepers, land managers, growers and federal agencies. A multifaceted approach is required because the challenges beekeepers face arise from a convergence of factors staged in ecosystems that are changing more rapidly and extensively in the second half of the 20th century than in any comparable period in human history. Honey bees and other pollinators along with beekeeping businesses are particularly vulnerable to ecosystem alteration. Acreage of pollen and nectar resources are shrinking, and warmer temperatures have altered bloom patterns, and reduced the nutritional values of pollens. In combination with severe stress from pathogens and parasites, and fewer locations protected from pesticide exposure, beekeepers that pollinate almonds and perhaps other crops are experiencing a financial burden not explicitly captured in reports of yearly colony losses. This burden threatens the sustainability of commercial beekeeping and has the potential to impact food production and consumers across institutional scales. 

​The cost of nationwide colony losses over the winter based on an estimate of 2.8 million colonies, a 35% loss rate, and our costs from September to almond bloom, translates into a $186 – 223 million USD loss for the U.S. beekeeping industry. What can be done to reduce these losses and improve the economics of migratory beekeeping? From our analysis, CS costs less per colony than overwintering in apiaries, and could potentially expand profit margins for colonies used in almond pollination. However, best management practices for CS need to be developed that improve overwinter survival. Those methods should include decision-support tools to improve selection of colonies to overwinter. The optimal timing for placing colonies in CS and the amount of resources required for overwintering also need to be determined. Establishing and enhancing pollinator habitat in the summer and fall are a key part of the solution because colony growth and honey yields are linked to the economic viability of commercial beekeeping. Furthermore, overwintering losses could be reduced with greater forage availability as fat body mass and vitellogenin levels critical for successful overwintering are enhanced when bees have access to fall pollens. The wide-angle view of an economic perspective should generate a sense of urgency to address the challenges faced by the beekeeping industry, so this vital sector of the agricultural economy can remain profitable and sustainable. 

ACKNOWLEDGEMENTS

The authors thank Randy Verhoek and Harvest Honey for collaborating with us on this project and for providing us colonies and information that made this study possible. We also thank Zac Browning for providing data for the study. We thank Drs. Vanessa Corby-Harris and Chelsea Cook for valuable reviews and suggestions on earlier versions of the manuscript. This work was funded by a USDAAPHIS Grant - 60-2022-6-006.

The journal article on which this manuscript was based can be found at: https://academic.oup.com/jee/article/112/6/2524/5559417

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