A Sustainable Approach to Reducing Pesticide and Antibiotic Use in Honey Bee Colonies

Final Report for LNC02-202

Project Type: Research and Education
Funds awarded in 2002: $99,600.00
Projected End Date: 12/31/2004
Matching Non-Federal Funds: $69,671.00
Region: North Central
State: Minnesota
Project Coordinator:
Marla Spivak
University of Minnesota
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Project Information


The incorporation of the trait, Suppression of Mite Reproduction (SMR), into our line of honey bees bred for hygienic behavior significantly reduced infestation of Varroa destructor mites within two commercial beekeeping operations relative to the pure hygienic line and a control line. We demonstrated that the mechanism of SMR is through adult bee removal of pupae on which mites are reproductively successful, more so than through physiological suppression of mite reproduction by bee pupae. We are developing a web-based course for beekeepers that emphasizes treating colonies for diseases and mites only as a last resort.


The research and extension program in apiculture at the University of Minnesota is the only one in a five state area  (MN, WI, IA, SD, ND). Yet, MN, SD, and ND, are the top honey producing states in the nation based on yield per colony (National Ag. Statistics Service, 2004) and produce over 30% of the total honey production for the nation. The majority of the commercial beekeepers in the Upper Midwest are “migratory,” meaning that they transport their colonies every winter either to southern states where they produce bulk bees and queens for sale, or to CA where the bees pollinate almond and citrus orchards. The beekeepers transport their colonies back to the Upper Midwest for the summer to produce large honey crops.

The number of bee colonies and beekeepers is steadily declining due to the introduction of V. destructor into the U.S. in 1987, which kills bee colonies within 1-2 years if left untreated. To control this mite, beekeepers have been using pesticides (pyrethroids and organophosphates) within their colonies. However, the mites have developed resistance to these compounds. This use of pesticides in honey bee colonies has added an enormous operating expense to beekeepers, and risks contaminating honey and beeswax with pesticide residue.

Since 1994, we (M. Spivak and G. Reuter) have been breeding honey bees for resistance to diseases and V. destructor. The most devastating disease of honey bees is American foulbrood (AFB), a bacterial disease of brood (larvae) caused by Paenibacillus larvae. We have demonstrated that honey bees bred for hygienic behavior, a genetic trait, demonstrate good resistance to AFB and also to a fungal disease, chalkbrood (Spivak and Reuter, 2001a). Hygienic bees are able to detect, uncap, and remove disease-infected brood from the nest before the causative organisms reach the infectious stage, and before the human eye can detect clinical symptoms of disease (Woodrow and Holst, 1942; Rothenbuhler, 1964). Removing the disease in the non-infectious stage prevents it from spreading throughout the colony. We have found that bees bred for hygienic behavior also display resistance to V. destructor because they are able to detect and remove brood infested with the mites (Spivak, 1996). This mite parasite alternates between feeding on hemolymph (blood) of adult bees, and feeding and reproducing on the pupal stage of bees. Bees that remove mite-infested pupae from the nest interrupt the reproductive cycle of the mite by eliminating the progeny of the mite developing within a wax-sealed cell. To select colonies for hygienic behavior, we have used a "freeze-killed brood" assay. This assay involves recording the time it takes a colony to uncap and remove pupae that have been freeze-killed; colonies that remove over 95% of the dead brood within 48 hours are considered hygienic, and daughter queens are propagated from them (Spivak and Downey, 1998).  This is an indirect assay that is correlated with rapid removal of diseased and mite-infested brood. Hygienic behavior is only one of several mechanisms of resistance to the mites (Boecking and Spivak, 1999), and bees selected for this trait on the basis of a freeze-killed brood assay do not have sufficient resistance to maintain colonies under the estimated economic treatment threshold (Spivak and Reuter, 1998; 2001b).

Since 2001, and with support from NCR-SARE, we have been incorporating another trait into our “MN Hygienic” line to increase the degree of resistance to V. destructor.  The trait is “SMR” or Suppression of Mite Reproduction (Harbo and Hoopingarner, 1997; Harbo and Harris 1999a; b).  In breeding for this trait, J. Harbo found colonies in which the mites had very low reproductive success on worker brood, determined by examining the brood just prior to the bees' emergence from the cell as an adult. Colonies were found in which the mites either did not initiate egg-laying, or laid eggs too late for mite offspring to reach maturity and mate.  These colonies provided the genetic basis for his intense selection and breeding program. We tested hybrid crosses between Harbo’s SMR line and our MN Hygienic line with the aim of increasing mite resistance through the SMR trait, while maintaining the high degree of disease resistance, high honey production, good brood viability, and nice temperament of the Hygienic line.

When we began this research, it was not known what mechanism was underlying the SMR trait. Originally, we hypothesized that the mechanism for Suppression of Mite Reproduction was due to behavioral incompatibilities between the mite and the bee larva during the first 12-24 hours after the bee larva is capped with wax which preclude the mite from initiating oogenesis (egg development), based on research by Donze and Guerin (1994). In the course of our investigations, we observed that the SMR line also expressed hygienic behavior. From this surprising finding, we developed a new working hypothesis, which we tested and which yielded very interesting results. The new hypothesis and results are given under Objectve 2.

We are adamant in our outreach efforts that breeding for resistance is the foundation for all alternative control measures because resistant bees require fewer treatments to control diseases and mites. Our hope is to begin to change the traditional mindset from applying a "quick fix" to emerging problems (e.g., applying a different pesticide when the mites develop resistance to the currently used one) by encouraging beekeepers to adopt the more sustainable approach of maintaining lines of bees that have their own defenses against parasites and diseases. To this end, we have begun developing a web-based course, which will provide continued, interactive instruction to beekeepers on how to breed for resistance with the goal of reducing or eliminating the use of chemical controls.  To our knowledge, this is the first on-line course of its kind. We completed the front-end and one module of the course, and recently we sent it to various beekeepers and extension educators to obtain their feedback and suggestions before developing the rest of the course. The temporary link to this course, and feedback to date, is given under Objective 3 and in the Publications and Outreach section of this report, below.

Project Objectives:

Our goal is to breed honey bees, Apis mellifera, resistant to diseases and parasitic mites to reduce the amount of antibiotic and pesticide used in bee colonies, and to ensure that our breeding methods and stock are accessible to beekeepers everywhere.

Our first objective is to test hybrid crosses between a line of bees resistant to disease (bees bred for hygienic behavior) and a line resistant to the parasitic mite Varroa destructor  (bees bred for "Suppression of Mite Reproduction" or SMR). Our previous research indicated that bees bred for hygienic behavior are only partially resistant to these mites. Thus, our aim is to increase the level of mite resistance while retaining the disease resistance and high honey production of the hygienic line. The crosses will be tested both in apiaries at the University of Minnesota and in apiaries owned by Mr. Darrel Rufer, a commercial beekeeper based in Minnesota.

Our second objective is to determine how bees selected for SMR are able to suppress the reproduction of the mite. We will test the hypothesis that there are behavioral incompatibilities between the mite and the bee larva during the first 12-24 hours after the bee larva is capped with wax which preclude the mite from initiating oogenesis (egg development).  

Our third objective is to develop an interactive web-based course on sustainable  methods of controlling diseases and mite pests of honey bees. The main emphasis will be on promoting the use of resistant bee stocks as the foundation for integrated pest management strategies. This will be the only such course available on-line to beekeepers, and is a crucial link between our research and its successful implementation.


Materials and methods:

Objective 1: We have been incorporating the SMR trait into the hygienic line by establishing colonies that contain “hybrid” worker bees. We began in 2001 by making reciprocal crosses from among our colonies at the University of Minnesota. The crosses were made between the hygienic and SMR lines (hygienic queens were inseminated with semen from SMR males and vice versa). From the reciprocal crosses, we bred new daughter queens from the colonies with the best brood viability, and produced subsequent crosses with varying degrees of the SMR trait (by using varying numbers of drones from both lines to inseminate queens from each line).  

In the summer of 2003, we tested one of the crosses in commercial apiaries in Minnesota and North Dakota, in collaboration with two commercial beekeepers, Mr. Darrel Rufer and Mr. Bill Klett, who are part of a group of MN and ND beekeepers (the “East TX Cartel”) that transport their colonies to eastern TX each winter, and have been using our hygienic line for over six years. In the spring of 2003, they raised daughters from the HYG/SMR hybrid breeder queens and allowed these new queens to mate naturally with the drones (males) in the surrounding area which now carry the hygienic alleles, as they are progeny of the hygienic queens we have been donating to them. The queens produced from the experimental cross produced worker progeny that were approximately 67% hygienic and 33% SMR (each worker bee had this 67:33 HYG/SMR genotypic mixture). As controls, these beekeepers also raised and mated pure HYG queens, and some unselected, control queens in an apiary of a third commercial beekeeper, Larry Jagol. The colonies were transported to MN and ND in May for honey production. Approximately 36 of each colony type were moved to each state, and were distributed among three apiaries in each state. Over the course of the summer, we measured the colonies for: 1) hygienic behavior (using a standard freeze-killed brood assay; Spivak and Downey, 1998); 2) brood areas (sq cm of brood), 3) frames of bees (visual estimations), 4) mite levels of adult bees (by collecting samples of adult bees in alcohol, washing the mites from the bees, and calculating the number of mites per 100 bees), 5) mite infestation in worker brood (by uncapping 200 cells containing worker pupae and determining the proportion infested); 6) mite reproductive success (the number of female offspring in 30 cells that had reached the adult stage by the time the worker was in the "grey wing-pad" stage); and 7) honey production (weight of honey harvested).  

From the HYG/SMR colonies that produced the most honey, the most rapid hygienic behavior, the lowest mite levels on adults and in brood, and the lowest mite reproductive success, we selected new breeder queens for 2004. These colonies (with the queens) were transported to TX in the fall of 2003. The entire process was repeated in the summer of 2004: New colonies produced from the selected HYG/SMR queens, new breeder HYG queens and control queens were transported to MN and ND again in May 2004 and the same measurements were taken.

Objective 2: In late summer of 2002, we began testing a new hypothesis about the mechanism of Suppression of Mite Reproduction. While working with the SMR line, we discovered that it is also highly hygienic. This finding is curious and unexpected because Dr. Harbo who bred the SMR line, did not select for hygienic behavior. He bred for colonies in which the mites were not reproducing on worker pupae. Apparently, the presence of the hygienic trait is a by-product of his selection. From our previous research we know that hygienic bees tend to remove infested pupae after the mite has initiated reproduction (when there are offspring in the cell). Noticing that the SMR line was hygienic, we hypothesized that they might be removing infested pupae with reproductive mites, leaving only the pupae with non-reproductive mites. When capped cells containing pre-emergence worker pupae were opened to inspect for mite infestation and successful reproduction, it would appear that the mites did not reproduce, when actually any that did reproduce were previously removed by the bees.  

Our methods were as follows: To determine if SMR bees could detect and remove mite-infested pupae, we collected mites from one infested SMR and one infested HYG source colony and introduced them into three SMR and three HYG colonies; each recipient colony received 40 mites from both source colonies. The mites were introduced onto 5th instar larvae that had been sealed within 4 hours. The cells were marked on a transparency, and the combs were returned to their original colonies. Every two days, we recoreded the number of mite-infested and control cells removed by the bees. Next, to determine if the SMR bees were removing predominantly pupae on which mites had reproduced successfully, we inspected the remaining mites that were not removed by the bees. When the pupae were in the "yellow thorax" stage, we recorded the reproductive success of the remaining mites, defined by the presence of at least one adult daughter and a male (following Martin, 1994). At this stage, this daughter will mate with the male to become a viable female offspring. Finally, to determine if there was another factor, unrelated to adult bee removal that contributed to SMR resistance, we repeated the same methods as above; however, after introducing the mites, the combs were placed in an incubator maintained at hive temperature and humidity (34°C, 50% RH) for 10 days so the adult bees could not remove the infested pupae. The reproductive success of the mites was again recorded. In this way, we could determine if there was an effect of the brood on mite reproductive success; that is, if mites from SMR colonies had the same reproductive success on HYG pupae as on SMR pupae (and vice versa).

Obejctive 3: Under the direction of Dr. Sandra Becker, from Extension’s Information and Learning Technology group, and the help of graphic artists and a programmer, I developed the concept and wrote the text for a web-based course for beekeepers. The theme of the course is "Healthy Bees" and it is geared toward good beekeeping practices to prevent bees from succumbing to diseases and parasitic mites. We emphasize a three-step strategy: Knowledge, Prevention and Control. Beekeepers must have a good knowledge of how diseases and mite pests infect colonies. They must know what they as beekeepers can do to prevent these maladies, and they must know what the bees can do to defend themselves (e.g., bees bred for resistance can "defend themselves"). If a colony does become diseased or parasitized, we emphasize that the first controls should be cultural; i.e., steps the beekeeper take to ameliorate the problem without resorting to antibiotic or pesticide use. Finally, if chemical controls are necessary, they must be used only as a last resort, and chemicals should be chosen that will treat the problem without exacerbating it (e.g., that the diseases and mites won't develop resistance to).  

In the course, the bees are presented as "Super-Heroines" – the "Hive's Angels." The diseases and mites are the "villains." The idea is that the super-heroine has strengths and weaknesses; the beekeeper must play to the bees' strengths so the villains cannot overcome their weaknesses. Likewise, the villains have weaknesses that the bees and beekeepers can overcome. Our hope is that presented in a lively, graphically rich manner, the course will hold beekeepers' attention while helping them learn the concepts. The main goal is to change their mindset away from treating by habit, to treating only as a last resort.

Research results and discussion:

Objective 1: Our results from 2003 indicated that the HYG/SMR colonies had significantly fewer mites than both the HYG and control colonies in ND (ANOVA: P = 0.045). In MN, the HYG/SMR colonies had significantly fewer mites than the control colonies (P = 0.023), while the hygienic colonies had intermediate mite levels.  The percent infestation of mites in worker brood was significantly lower in both the HYG/SMR and HYG colonies than in the controls in both states (P < 0.001 in both). Importantly, the mites had significantly lower reproductive success in the HYG/SMR compared to both the HYG and control colonies (P = 0.05). The brood viability in the HYG/SMR colonies was good, and was statistically equivalent among the three groups. The HYG/SMR colonies also removed as much freeze-killed brood within 24 hours as the hygienic line. In ND the HYG/SMR colonies produced less honey than the HYG and Control colonies, although the differences were not significant. However, in MN, the control colonies produced significantly more honey than the both the HYG/SMR and HYG colonies (P < 0.01).

The HYG/SMR breeder colonies we chose for 2004 all came from the colonies that were transported to ND, and we chose them from among the colonies that produced the most honey and had the lowest mite levels. Although we established colonies in MN and ND, we could only analyze results from the North Dakota apiaries because of an unfortunate mix-up in breeder queens for the MN apiaries which caused us to have to exclude the entire data set. However, the data from 110 colonies in ND demonstrated again that the HYG/SMR colonies had significantly lower mite loads on adults than both the HYG and Control colonies (ANOVA: P = 0.042), were significantly more hygienic than both the hygienic colonies and the controls (P < 0.001), had equivalent honey production to the controls (P > 0.05), and had equivalent colony strengths and brood viability (P > 0.05). These results indicate that we have made progress on increasing mite resistance while maintaining hygienic behavior and good brood viability. Figures of these results are shown in the hard copy of this report. We will be submitting these findings for publication a peer-reviewed journal soon.  

Objective 2: The SMR colonies uncapped and removed significantly more mite-infested pupae than the HYG colonies. Both lines of bees removed significantly more infested pupae than control pupae (Nested ANOVA: P = 0.0438).  Within the SMR colonies, the mites on pupae that were not removed by the bees had significantly lower reproductive success (fewer viable female offspring) compared to mites remaining in the HYG colonies. There was no significant difference in reproductive success between remaining SMR and HYG mites within each line (P > 0.05 each).  

When the bees were not allowed to remove mite-infested pupae, the reproductive success of mites collected from SMR colonies (SMR mites) was significantly lower than mites collected from HYG colonies (HYG mites) [Nested ANOVA P = 0.007].  In addition, the reproductive success of HYG mites was significantly reduced on SMR pupae relative to on HYG pupae (P=0.0163).

These findings show that the main mechanism for Suppression of Mite Reproduction (SMR) involves the active detection and removal by adult bees of pupae on which Varroa destructor produces viable female offspring, and the non-removal of pupae on which the mite does not produce viable female offspring. In this sense, adult SMR bees are applying direct selection pressure on the mites by actively suppressing their reproductive success. Over time, the mites that remain in SMR colonies have reduced reproductive potential.

Another minor component of the SMR trait involves some unknown physiological or behavioral factor associated with SMR worker brood that reduces the reproductive success of mites. This component was originally thought to be the most important factor in explaining the resistance of SMR bees.

In comparison with our colonies bred for hygienic behavior, colonies bred for SMR removed significantly more infested pupae, and were significantly more selective in removing pupae with reproductive mites.  We speculate that this difference is because we selected colonies for hygienic behavior based on an indirect assay (removal of freeze-killed brood; Spivak and Downey, 1998). The SMR line was selected based on the presence of non-reproductive mites in worker brood (Harbo and Hoopingarner, 1997), a direct and specific assay for the bees’ ability to disrupt the reproduction of mites with high reproductive success.

Objective 3: We have completed the front end of the web-based course, which includes the home page, video welcome. We have also completed sections on Healthy Bees, the Strategy, Resources, some Frequently Asked Questions (FAQs), and one disease/pest module on chalkbrood disease. The course can be viewed at:

Before proceeding with the rest of the disease and pest modules, we wanted to obtain some user feedback, so sent the web site and survey form to extension personnel and beekeepers. The form and feedback are attached in the Publications and Outreach section of this report.

Research conclusions:

With the introduction of the destructive parasitic mite, Varroa destructor, into the U.S., beekeepers have had to resort to using pesticides within their beehives to prevent devastating and expensive colony losses. Colony losses have more than doubled in many cases even with the use of the pesticides due to reinfestation and increase in the overall stress imposed on the colonies by the mites. Operating costs have increased dramatically because the pesticides are expensive and more labor is required to apply them. The most sustainable solution is to reduce the dependency on pesticides by  breeding bees that can defend themselves against the mites and diseases.  These bees would be healthier and more able to withstand the stress of continued mite infestation and disease exposure.  

Our research demonstrates that colonies bred for hygienic behavior have good resistance to chalkbrood and American foulbrood diseases, and partial resistance to Varroa mites, particularly under low mite infestation pressure. Combining the hygienic trait with the SMR trait increased the mite and disease resistance by increasing the bees' ability to remove infested brood. Our goal is to eliminate the use of pyrethroids and organophosphates entirely in beehives by using resistant stock, or minimally to reduce the number of treatments required. Most beekeepers treat their colonies twice annually with the synthetic pyrethroid, fluvalinate, or with the organophosphate, coumaphos. In the last severalyears, the mites have developed resistance to both fluvalinate and coumaphos. If beekeepers could half the number of treatments they apply, this small reduction in pesticide use would cut the added operating cost in half.

A reduction in pesticide use by beekeepers will enhance environmental quality and economic viability of individual beekeeping operations, strengthen an agricultural system (beekeeping) which is based on small and moderate-scale owner-operated farms; protect human health and safety by preventing the risk of contaminating honey and hive products; and promote the well-being of honey bees  -- the world’s vital pollinators of crops, gardens, and wildflowers.

Economic Analysis

The number of beekeepers in the North Central States (and the U.S.) is small relative to the number of corn and soybean farmers; beekeeping is a specialized art and life-style that is not attractive to everyone. However, beekeepers play an extremely important role in the ecosystem because bees are such important pollinators of many commercial vegetable and seed crops (e.g., alfalfa, sunflowers, vine crops), commercial fruits (e.g., apples, cranberries, blueberries, strawberries), and home fruit and vegetable gardens. In addition, bees produce honey  - a product well respected for being wholesome and pure. Control measures for diseases and mites have increased operating costs for beekeepers, and in recent years, many commercial beekeepers have gone out of business. Although other commercial and hobbyist beekeepers continue to operate, the combined effects of increased costs of controlling pests and diseases, the depressed honey market, and reduced colony survivorship due to habitat destruction and increased pesticide use on crops, have resulted in a drastic decline in national honey bee colony counts.

A commercial beekeeper with 2500 colonies currently spends $17,900 yearly to treat his/her colonies with fluvalinate(Apistan®), or coumaphos (CheckMite®) to control Varroa mites (2 applications/year; $1.79/strip, 4 strips/yr).  Two thousand five hundred colonies is an average number of colonies necessary to sustain a livelihood. On an aggregate basis, Minnesota beekeepers spend approximately $990,000 each year on these pesticides alone.  When antibiotics are added in to prevent the spread of bee diseases (Terramycin costs:  $268/2500 colonies, or $16,080/150,000 colonies; the total expense per year exceed $1 million.  Clearly, the costs of pesticides and antibiotics are prohibitive for an already challenged group of farmers.

One of the most cost-effective ongoing operating expenses that beekeepers have is the price of introducing new, young queens into their colonies.  Many large commercial operators raise their own queens. Others purchase new queens for $12.00-$15.00 each. New queens are introduced into at least half of the colonies in Minnesota annually. With access to queens from stocks that are mite-resistant and productive, beekeepers could reduce the amount spent on pesticides by one-half, reducing treatments to once a year, without any additional operating costs. Any reduction in pesticide use means increased profit for the beekeeper.

Farmer Adoption

Our MN Hygienic line is currently being sold commercially to beekeepers throughout the US.  We collaborate with a bee breeder in southern CA who helps us maintain the line through artificial insemination of the queens (queen bees mate with 10-20 males, so to fix a trait in a population, the matings must be controlled through insemination). We also have been donating breeder (inseminated) queens to beekeepers in MN who raise daughter queens from them for sale to other beekeepers. They sell the MN Hygienic line both directly and through B&B Honey Farm located in Houston, MN. One prominent group of beekeepers, led by Darrel Rufer and Bill Klett, have been using the MN Hygienic line for over seven years, and have had good success controlling diseases and mites with this stock (See article in Appendix: American Bee Journal 2004, pp 534-5).

Our cooperating beekeepers sell their resistant queen bees to beekeepers in the North Central region and throughout the U.S. either directly, or through B&B Honey Farm, a regional beekeeping supplier based in Houston, MN, so the stock is being distributed widely and successfully.

The fact that we have identified a number of “breeder” colonies in the apiaries of the commercial beekeepers has far reaching implications. A measure of success of our research program is whether the beekeepers adopt the new technology, in this case, increasing disease and mite resistance through bee breeding. Until now, we have been providing breeder (instrumentally inseminated) queen to the beekeepers. However, a more sustainable solution is for the beekeepers to select from among their best colonies instead of relying on University breeder queens. By breeding from their colonies that express both hygienic behavior and SMR, and requeening their colonies with these daughters, the daughters will produce drones that also carry both the hygienic and SMR traits for mating in subsequent generations.  Thus they do not need to instrumentally inseminate queens to propagate the hygienic and SMR traits.  

Participation Summary

Educational & Outreach Activities

Participation Summary:

Education/outreach description:
  • Thesis:  PhD Candidate Abdullah Ibrahim will defend his dissertation in May 2005:  "The Importance of honey bee (Apis mellifera) hygienic behavior as a mechanism of resistance to the parasitic mite, Varroa destructor."  

    We will be submitting two publications from his dissertation research, which are products of our NCR-SARE funding:
    Ibrahim, A., Reuter, G. Spivak, M. Field trials comparing resistance to Varroa destructor by honey bee colonies bred for both Suppression of Mite Reproduction and hygienic behavior.  

    Ibrahim, A. Reuter, G., Spivak, M. Interplay between two honey bee mechanisms of resistance to Varroa destructor mites: Suppression of Mite Reproduction and hygienic behavior.

    Other related publications:
    Flores, JM, Spivak, M., Guiterrez, I. Spores of Ascosphaera apis contained in wax foundation can pass on chalkbrood in honey bees. Submitted Sept; J. Invertebr. Pathol.

    Gekker, G., Hu, S., Spivak, M., Lokensgard, J.R., Peterson, P.K. Anti-HIV-1 activity of propolis in CD4+ lymphocyte and microglial cell cultures. Submitted Aug J. Ethnopharmacology.

    Mondragon, L., Spivak, M., Vandame, R. A multifactorial study of the resistance of Africanized and hybrid honey bees Apis mellifera to the mite Varroa destructor over one year in Mexico. Submitted May - Apidologie.

    Gramacho, KP and Spivak M. 2003. Differences in olfactory sensitivity and behavioral responses among honey bees bred for hygienic behavior.  Behav. Ecol. Sociobiol. 54: 472-479.

    Spivak, M., Masterman, R., Ross, R., Mesce, KA. 2003. Hygienic behavior in the honey bee (Apis mellifera L.) and the modulatory role of octopamine. J. Neurobiol. 55: 341-354.

    Lapidge, K., Oldroyd, B., Spivak, M. 2002.Seven suggestive quantitative trait loci influence hygienic behavior of honey bees. Naturwissenschaften 89: 565-568.

    Haarmann, T., Spivak, M., Weaver, D., Weaver, B., Glenn, T. 2002. The effects of fluvalinate and coumaphos on queen honey bees (Apis mellifera  L). in two commercial queen rearing operations. J. Econ. Ent. 95: 28-35.

    Education and Outreach Programs;
    Dr. Spivak and Mr. Reuter offer an annual three- day short course on “Beekeeping in Northern Climates”  for the general public at the University of Minnesota. This course targets people that have never kept bees, but that have an interest in learning more about their biology and how to become a beekeeper. The course is based on sustainable practices, and includes discussion of responsible pesticide use and alternatives to chemical treatments. The average enrollment over the last three years has been 115 students. Most attendees were from Minnesota; however, others came from Wisconsin, Iowa, South Dakota, Missouri, and Nebraska. We also offer a course yearly in "Successful Queen Rearing" in which we teach experienced beekeepers how to breed and rear queens. In this course, we stress breeding queens for disease and mite resistance, and demonstrate techniques how this is done. The enrollment for this course is limited to 20 people due to the hands-on nature of the course content.

    Dr. Spivak is regularly invited to speak at Beekeepers meetings throughout the North Central Region, as well as the US. In the last couple years, I have been invited to Mexico, Spain, Paraguay and Brazil to speak to beekeepers about breeding for hygienic stock and disease and mite resistance. The desire for this knowledge is increasing worldwide.

    In addition, I speak at Minnesota and Wisconsin fruit and vegetable growers meetings, and Wisconsin Cranberry Growers meeting, where I emphasize the value of honey bees in vegetable and fruit production, and of the importance of maintaining healthy honey bee colonies for this purpose. Mr. Reuter speaks to over 30 public schools and nature centers annually in the Twin Cities area of Minnesota. In these presentations, he stresses the importance of honey bees to our ecosystem.

    Web-based Course, Survey and Evaluation Feedback
    We have completed the front end of the course (home page, video welcome, sections on Healthy Bees, the Strategy, Resources, some FAQ's, and one disease/pest module on chalkbrood disease.  The course can be viewed at:

    Before proceeding with the rest of the disease and pest modules, we wanted to get some user feedback, so sent the web site and survey form to the following extension personnel and beekeepers:

    University Extension People:
    Dr. Malcolm Sanford: [email protected]
    Dr. Brenda Ball:  [email protected]
    Dr. Steve Sheppard: [email protected]

    Commercial beekeeper: Gus Rouse [email protected]
    Hobby and Master Beekeeper: Landi Simone [email protected]
    Old timer Hobby Beekeeper: Liz Vanoeski [email protected]
    Brand new beekeepers: Val Cervenka  [email protected]  and
    Mike Simone [email protected]

    I have compiled the feedback from those that have responded below, under the survey questions:

    Dear        :
    We have been creating a web-based course for beekeepers on maintaining healthy honey bee colonies. We have the following sections of the course complete:
    Video welcome
    Healthy Bees
    The Strategy
    One disease/pest module (Chalkbrood)

    I’m writing to see if you would be willing to take a look at the course and give us some feedback before we complete the remaining modules on the remaining diseases/pests.

    If you have about fifteen minutes, here is what you’ll need to do.

    1. Go to http://webdev.extension.umn.edu/elms/healthybees/launchpage.html and click to enter the course.
    2. Follow the directions to play the video introduction.
    3. Follow the directions for the course.
    4. After you complete the required modules, click on the Chalkbrood module and work through that.
    5. Explore any other parts of the site you would like.

    After you’ve had time to test drive the course (except the diseases other than Chalkbrood), would you answer the questions on the attached Word document, save the document, and return it to Sandra Becker at this address:  [email protected].  Sandra is a member of the design team who will collect feedback.

    I look forward to your feedback.  Thanks so much.

    Marla Spivak  

    (numbers refer to the number of respondents, writing in italics are comments made by respondents)

    1.  Did you visit all the completed parts of the course?
    ___4 ___Yes                __1___No – video did not play

    2.  To what extent did you find the course easy to navigate.
    ___1__Somewhat easy  promts/links at end of each unit would be helpful
    _____Somewhat difficult

    Please comment on the parts of the course you found confusing:

    1 and 2 – no comments.
    3.  First, I must say I thought the focus and the graphics were absolutely terrific.  The design, with "Hive's Angels" and waving antennae was very engaging.  Graphics were unbelievably good, esp. the hygienic behavior. A few comments:
    ÿ no image appeared for me in "healthy bees" pp. 3, 4, 5
    ÿ video on home page wouldn't play
    ÿ In the self-test following chalkbrood, you might want to mention that they should click on the answer they think is correct.  
    4.  Not confusing but I clicked on the HTMLs in the Resource prt instead of letting the course take me there first.
    5.  It would be nice if there was a link from the end of the healthy bees to the beginning of the Strategy section and so on, since you expect people to go in that order, at least initially.
    Some people may miss the slide within slides in the healthy Bees section.  The info is important, and it is stated to click the arrows above, but people may skip right over it.
    In the Healthy Bee Section, I was wondering why new combs would be indicative of a healthy hive. I found out later, but I wsasn't sure about that initially.

    3.  To what extent do you think the information will be helpful to the target audience: bee keepers.
    ___3__Very helpful
    ___2__ Helpful
    _____Somewhat helpful
    _____Not helpful

    Please comment on the parts of the course you think will be particularly helpful for the intended audience.

    1. no comment
    2. The strategy and disease modules
    3. I have never seen educational materials with such a strong focus on IPM techniques and avoidance of chemicals except as a last resort.  I would love to see this available to all beekeepers.  The excellence of the graphics make working through the material a very lively experience.  No one's going to fall asleep taking this course!
    4. The details in the chalkbrood section were very good. The quiz a the end really helps reinforce the important points.  Literature references are great for those who want to know more; allow for independent research into various topics of concern. They also show the amount of research being done to help solve current issues. The upbeat graphics and presentation style will keep this fun and not heavilyt academic.  The do-at-your-own pace style is good.
    5. I think the natural defenses a colony has and ways to keep colonies naturally strong and healthy are the most effective parts that keep beekeepers interested.

    Please comment on the parts of the course you do not think will be helpful for the audience.

    1, 2, 3, 5:  no comments

    4. Depending on the level of knowledge the beekeeper has, some may find this too elementary. However, given the changes in  beekeeping practices and treatments for pest and diseases over the years, there will likely be something for everyne here.  At the very least, it will reinforce what the experienced beekeeper already dknows, and be a fun way to review or check out why something is happening in colonies, etc.

    4. What do you think were the central messages of the course?

    1. a) Identify the pest/disease, b) use chemical control as a last resort; c) use hygienic bees.
    2. Good beekeeping, bee biology in game form
    3. IPM and hygienic behavior as key tools to maintaining healthy colonies
    4. Hygiene, hygiene, hygiene!  Use pesticides as a last resort – great message and one that cannot be reinforced too much.
    5. Bees have some natural defenses; learn how these diseases affect the bees and what the bees do to prevent/treat them themselves; help the bees help themselves; hygienic bees are good; don't use chemical treatments unless absolutely necessary.

    5. We are thinking about offering a lifetime membership to the course so that learners could receive updates on new research, techniques, etc. What would you be willing to pay for such a service?

    _____I would not be interested in such an offer

    5. Any other feedback before we complete the rest of the diseases?

    1. I like course ideas; the information is very basic and needed. The emphasis on hygienic bees is good; it seems a big bottle neck is whether producers will supply hygienic bees; I don't see many beekeepers doing the basic tests. My experience in offering information for sale electronically is that the market is not there yet, see http://apis.shorturl.com
    2. I think it is excellent as it is going.  Clearly the rpg format is over the head of beekeepers that are 60 years old and over.  However, it makes it fun for new learners and still quite usable for older ones. I would not change the card format for the diseases, pests.  Note: perhaps useful to think to include other pest modules (yellowjackets, mice, et). One problem: it only played as a small screen on my computer. Should I reduce the resolution to get it full sized?
    3. Did anyone actually feed their bees bleach to treat chalkbrood?
    4. As an employee of a regulatory agency, I am wondering if the language in Resources – Beeswax and Pesticides about beekeepers "avoiding" pesticides when supers are placed is too soft.  Could stronger wording be used, such as "beekeepers must not apply pesticide when supers are placed" or something to that effect?  Again, the emphasis on using pesticides as a last resort is great, but I believe it could be stronger still.
    5. The link to the Villians on the bottom is a little distracting. I want to click on all of those before getting into anything else. The pics are great, as are all the graphics. It's a very attractive site!

    Extension Talks 2002-2004
    Wisconsin Beekeepers Association “Progress in Breeding Bees for Resistance to Diseases and Mites.” Manitowac, WI. Nov 5-6.

    2004 Oregon Beekeepers Assocation “The Interesting Relationship Between SMR and Hygienic Traits in Honey Bees.” Newport, OR. Oct 28-30.

    2004 North Dakota Beekeepers Association “The Interesting Relationship Between SMR and Hygienic Traits in Honey Bees.” Bismarck, ND.  Oct 8-9.

    2004 Congreso Iberolatinoamericano y 1 Congreso Paraguayo de Apicultura. “Como Prevenir y Controlar La Loque Americana” (in Spanish). Asuncion, Paraguay. Sept 24-26.

    2004 Eastern Apicultural Society, Keynote Address: “History of American foulbrood disease in US beekeeping.” Seven Springs Resort, PA. August 9-11.

    2004 Minnesota Honey Producers Assoc. “Progress in Breeding Bees for Resistance to Diseases and Mites.” Walker, MN. July 22-24.

    2004 TriState Master Gardener Conference. “Beekeeping 101 for Master Gardeners” and “Enhancing Bee Pollination.” June 21.

    2004 XV Congresso Brasileiro de Apicultura, Natal, BRASIL.  “Seleção de Abelhas para Resistência a Doenças e ao ácaro Varroa destructor” (In Portuguese). May 18-21.

    2004 North Carolina State Beekeepers Assoc. “Successful Introduction of Queen Bees” and “Breeding Bees for Resistance to Varroa destructor.” New Bern, NC. March 12-13.

    2004 Aerial Pesticide Applicators Recertification. “Protecting Pollinators.”  Morton, MN. March 5.

    2004 Maryland Beekeepers Association. “Successful Introduction of Queen Bees” and “Breeding Bees for Resistance to Varroa destructor.”  Howard Co. Fairgrounds, Maryland. Feb 20-21.

    2004 51st Annual Fruit and Vegetable Growers Conference. “Bumblebee Pollination in Blueberries.” St. Cloud, MN. Feb 6.

    2004 WI Cranberry Growers Assoc. Cranberry School. “Beekeeping 101 for Cranberry Growers” and “Pollination Contracts.”  Wisconsin Rapids, WI. January 21.

    2003 Beekeeping Association of Andalucia, SPAIN. “Selección de abejas para resistencia a enfermedades y a Varroa destructor” (in Spanish). Dec 9-11.

    2003 Minnesota Honey Producers Association. “Research Updates.” Willmar, MN. July 15-17. St. Cloud, MN. Dec 4-6.

    2003 Iowa Bekeepeers Association “Breeding Bees.” Marshalltown, IA. Nov 8-9.

    2003 Kansas Beekeepers Association “Nothing less than a Revolution…” and “Questions and Qualms about Queens.” McPherson, KS. Oct 17-18.

    2003 North Dakota Beekeepers Association “Research Update.” Bismarck, ND. Oct 10-11.

    2003 Southeastern Minnesota Beekeeping Association. “Nothing less than a Revolution…”  Rochester, MN. Sept 27.

    2003 Eastern Apicultural Society Levels 1 and 2 Short Course: “Questions and Qualms about Queens.” Brunswick, Maine. Aug 4-8.

    2003 10th International Congress of “Actualizacion Apicola” (“Practical Beekeeping”). “Breeding Honey Bees for Resistance to Diseases and Varroa destructor” (in Spanish) Txlacala, MEXICO. May 29-31.

    2003 New Jersey Beekeeping Association. “Are Hygienic Bees Super-Heroines?” Columbus, NJ. Feb 1.

    2003 American Beekeeping Federation. “Nothing Less than a Revolution:  Radical Change or Full Circle.” Kansas City, MO. Jan 14-17.

    2003 Ag Crops Pesticide Recertification Workshop (General Ground and Ag Crops Pest Management) “Beekeeping and Pesticides.” Willmar, Morris, Alexandria, St. Cloud, MN. Jan 6-9.

    2002 Illinois State Beekeeper’s Assoc. “Are Resistant Queens Super-Heroines?” and “Stinging and Stingless Bees in Brasil.” Springfield, IL. Nov 9.

    2002 North Dakota Beekeepers Assoc. “Research Update.” Bismarck, ND. Nov 11-12.

    2002 Eastern Apicultural Society. Participated in teaching 2 workshops in Short Course for Beekeepers, and presented 2 talks to general audience: “Breeding for Varroa Control,” and “Hygienic Behavior: How much is enough?”

    2002 University Illinois Beekeeping Short Course. 3 workshops given on Beekeeping Management. Urbana, IL. July 16-18.

    2002 MN Honey Producers Assoc. Research Update. Alexandria, MN. July 12-14.

    2002 South Dakota Beekeeping Assoc. “Are Hygienic Bees Super-heroines?” Pierre, SD. June 28-30.

Project Outcomes


Areas needing additional study

I have submitted a proposal for continued NCR-SARE funding in 2005-2008. The continuing, long-term goal of this research is to reduce the amount of pesticide use in honey bee colonies for the control of the parasitic mite, Varroa destructor. Most commercial beekeepers do not sample their colonies to determine if the mite levels have reached an economic threshold, and hence to determine whether to treat or not, which has led to the overuse of pesticides and the subsequent development of resistance by the mites to the chemicals. To foster more sustainable beekeeping practices, and in response to beekeeper demand, we propose the following objectives:

Objective 1: Develop a simple and standardized sampling plan for commercial beekeepers to help them determine the economic treatment level for Varroa destructor mites (short-term outcome).

Objective 2: Compare mite levels and economic thresholds between our line of bees bred for both Hygienic Behavior (HYG) and Suppression of Mite Reproduction (SMR) with an unselected, commercial line of bees (short-term outcome), to demonstrate that the use of resistant bees can reduce mite loads and thus, the frequency of pesticide application (intermediate-term outcome).

Objective 3: Develop published guidelines for migratory beekeepers on making educated treatment decisions for the mite based on the sampling plan (intermediate- to long-term outcome).

Any opinions, findings, conclusions, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture or SARE.