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NC_OLD1173: Sustainable Solutions to Problems Affecting Bee Health
(Multistate Research Project)
Status: Inactive/Terminating
NC_OLD1173: Sustainable Solutions to Problems Affecting Bee Health
Duration: 10/01/2009 to 09/30/2014
Administrative Advisor(s):
NIFA Reps:
Non-Technical Summary
Statement of Issues and Justification
ISSUES AND JUSTIFICATION
Honey bees provide essential pollination services to US fruit and vegetable growers, adding $8-10 billion annually to farm income. About 2 million colonies are rented by growers each year to service over 50 crops. Almonds alone require 1.3 million colonies and are predicted to require 2.12 million by 2012, a number nearly equal to the number of colonies presently in the US. Increasing demand comes at a time when beekeepers are operating in crisis mode. The supply of healthy colonies is volatile as parasitic mites and the rigors of migratory beekeeping continue to cause catastrophic die-offs. Pesticide resistance and a lack of viable, industry-based honey bee breeding programs contribute to these losses. The problems associated with mites and other factors affecting honey bees are outlined in a 2007 report of the NAS-NRC², Status of Pollinators in North America.
The winter of 2007/08 witnessed another major colony die-off, and while many of the deaths are due to parasitic mites, a large number of colonies exhibited symptoms inconsistent with mites or any known disorder. By last count, 0.75 to 1 million honey bee colonies died over the winter of 2007-2008 (vanEngelsdorp et al. 2008). Migratory beekeepers trucking bees over great distances were especially hard hit. This suggests yet another problem has beset an already beleaguered industry. This new syndrome has been named Colony Collapse Disorder (CCD) in 2007. A list of possible causes for CCD includes new pesticides and pesticide use patterns, nutritional deficits associated with monocultures, loss of immunity to pathogens and exotic pathogens.
According to a survey conducted by the Apiary Inspectors of America (AIA) and the U.S. Department of Agriculture, honey bee colony losses nationwide were approximately 29 percent from all causes from September 2008 to April 2009 (Kaplan 2009). This is less than the overall losses of about 36 percent from 2007 to 2008, and about 32 percent from 2006 to 2007, that have been reported in similar surveys. About 26 percent of apiaries surveyed in the latest survey reported that some of their colonies died of colony collapse disorder (CCD), down from 36 percent of apiaries in 2007 2008. As this was an interview based survey, it was not possible to differentiate between verifiable cases of CCD and colonies lost as the result of other causes that share the "absence of dead bees" as a symptom. However, among beekeepers that reported any colonies collapsing without the presence of dead bees, each lost an average of 32 percent of their colonies in 2008 2009, while apiaries that did not lose any bees with symptoms of CCD each lost an average of 26 percent of their colonies. The survey checked on about 20 percent of the country's 2.3 million colonies.
The NC 508 committee met at the University of Florida, Gainesville on 4 February 2009. Members present represented 14 universities from throughout the US. Committee members discussed ongoing research and plans were made to conduct future research to develop viable solutions to the problems afflicting honey bees in order to ensure the sustainability of the nations food supply.
Most of our committee members are involved in a $4.1 million 4-year CAP project that was funded in 2008 to study the causes of CCD and other maladies affecting bee populations. The CAP funding obtained was a direct result of the establishment of the NC 508 committee in 2007. A second meeting of some NC 508 participants was convened that same year to initiate the proposal writing. The scientists will conduct research that addresses genomics, breeding, pathology, immunology, and applied ecology to investigate and explain the causes of the decline in bee colonies in the US in recent years. In addition, we will investigate the role of ecosystem services provided by native, wild bees in pollinating crops. Native bee pollination can be sufficient to fully pollinate crops in some agricultural contexts (Kremen et al. 2002; Winfree et al. 2007), and even when pollination services are incomplete, can serve as a supplement to or back-up for managed honey bee stocks. Native bee ecologist(s) will investigate the role of native bee species in pollinating several crops and will and identify the land and farm management practices associated with high levels of native bee pollination. Committee members will work closely with the extension community and other stakeholders to develop and implement mitigative strategies that unravel the causes of CCD and other significant bee health problems.
TYPES OF ACTIVITIES
The purpose of this committee has been and will be to coordinate research that is relevant to bee colony health. We are seeking participation of personnel with expertise in bee nutrition, toxicology, parasitology, pathology, breeding, integrated pest management, and non-Apis species. Research and extension personnel will meet annually to discuss coordination and will form subgroups that will coordinate or collaborate on research throughout the year. Extension personnel will coordinate in technology transfer and adoption of research findings to beekeepers.
Related, Current and Previous Work
Most members of the NC508 committee are active in the American Association of Professional Apiculturalists (AAPA) and have been involved in research and extension that pertains to honey bee health. The NC 508 committee met at the Double Tree Hotel, Sacramento, California on 10 January 2008. Members present represented 14 universities from throughout the US. Committee members discussed ongoing research and plans were made to conduct future research to develop viable solutions to the problems afflicting honey bees in order to ensure the sustainability of the nations food supply.
Most of our committee members are involved in a $4.1 million 4-year CAP project that was funded in 2008 to study the causes of CCD and other maladies affecting bee populations. The CAP funding obtained was a direct result of the establishment of the NC 508 committee in 2007. A second meeting of some NC 508 participants was convened that same year to initiate the proposal writing. The scientists will conduct research that addresses genomics, breeding, pathology, immunology, and applied ecology to investigate and explain the causes of the decline in bee colonies in the US in recent years. Committee members will work closely with the extension community and other stakeholders to develop and implement mitigative strategies that unravel the causes of CCD and other significant bee health problems.
Objectives
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To develop and recommend to beekeepers "best practices" for varroa mite control based on currently available methods and strategies for mite management.
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To evaluate the role and causitive mechanisms of parasitic mites and pathogens such as viruses, protozoa and bacteria in honey bee colony deaths.
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To determine the effects of pesticides and other environmental chemicals on honey bee colony health.
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To determine how environmental factors, including nutrition and management practices affect honey bee colony health.
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To determine the effects of interactions among various factors affecting honey bee colony health.
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To coordinate research and extension efforts related to bee colony health.</li>
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To facilitate, through research and extension activities, the development of industry-based honey bee stock selection, maintenance and production programs that demonstrably incorporate traits that confer resistance to pests, parasites and pathogens.
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To focus on non-Apis bees, their conservation, pathology, susceptibility to pesticides, and their contribution to crop pollination including economic value.
Methods
1) The CAP program provides the fundamental framework for this effort. The team is made up of several research teams comprehensively addressing causes of bee decline, whether with pathogens or toxins, and feeding this information directly to the Bee Health Community of Practice website at eXtension.org. The public side of this site can be viewed at http://preview.extension.org/bee%20health. Community work pages have been populated with organizational information, website content outline, and 23 pages for the public site. Additional content is being obtained and is in preparation for upload, including bulletins in bee biology, best management practices, and diseases/pests. An online meeting protocol was established and we conducted meetings with the CoP, which included planning for the CAP team. This effort is being managed by a dedicated CAP-funded staffer, Mr. Michael Wilson at University of Tennessee. Collaborations: The Bee Health Community of Practice is so far comprised of 43 members representing scientists and extension workers from CAP, the ARS Areawide project, and numerous non-affiliated experts across North America. 2) Background: This huge effort is a shared goal of members of CAP as well as ARS Areawide and includes a significant fraction of the honey bee scientists of the United States. As this NC 508 project was the synergist for the CAP team, we will limit our reports in this section to objectives of this particular group. Researchers will coordinate their efforts geographically and methodologically in sampling for detecting parasites and pathogens in hives and bees. Pathogen identification in bees will be aided by molecular techniques (e.g. massively parallel DNA sequencing, bioinformatics and PCR). Causative relationships will be evaluated in part by correlating the presence of various biotic agents and colony symptoms over time. Objective 2a - Comparative virulence of Nosema apis and N. ceranae in caged bees. Newly emerged workers will be individually inoculated with 0 (control), 5, 50, 500, 5,000, and 50,000 spores with both species of Nosema. One hundred bees per cage (cage size: 14 × 12 × 16 cm), 4 cages per dosage will be used for each colony. Workers are provided with 50% sugar syrup (changed every 3 days), bee pollen (in which Nosema spores have been inactivated by heating at 60° C for 24 hrs), and distilled water ad libitum. Dead bees will be removed daily and their numbers recorded. The experiment will be repeated with bees from at least three different colonies. Survival analysis will be used to determine the time required for 50% mortality in the three doses of Nosema, for both species. The median infective dosage (ID50) will be calculated using probit analysis (Finney, 1971) for both species of Nosema. (For additional background, rational and significance,sub-objectives, expected outcomes, methods, and collaborators, see full/separate document) 3) Synergism bioassays - The LD50 for 8 miticides (Apistan, CheckMite, Mite Away II, Apiguard, Api Life Var, Mite-A-Thol, Hivastan, and Sucrocide) used in bee hives will be established using 360 worker bees per bioassay. All bioassays will be done by topically applying serial dilutions of compounds with a Hamilton micro syringe. All compounds will be tested singly and in reciprocal tests for all synergism bioassays. Synergistic ratios will be determined by treating bees with LD5 of one compound and then treating with serial dilutions of the second compound to determine whether the dose response curve of second compound shifts position. Synergistic ratios will be determined if synergism is observed. EPA guidelines for the age and diet of bees used in bioassays will be followed. Sperm number and viability and queen survivorship - The LD50 for newly emerged drones will be determined for each of the 8 compounds. Drones will be treated with non-treated controls and a sub-lethal dose as described above. Newly emerged drones will be marked with enamel paint upon emergence. They will be treated, released back into the colony, and then recaptured 14 days later for examination. More drones will be marked and treated than needed for the analysis, so that if some are lost on mating flights enough will remain for the assay. Marked drones will be captured 14 days later and their sperm counts and sperm viability determined by examining their sperm in a hemocytometer. Sperm will be collected from individual drones by applying pressure to the abdomen causing full eversion of the endophallus (Harbo 1985). The semen will be then collected using a capillary tube. Sperm viability will then be assessed using two fluorescent stains (Locke et al. 1990). Propidium iodide will stain the dead cells red and Hoechst No. 33342 (H342) will stain the living cells green. The stains will be added to sperm dilutions, and a drop of the stained solution will be placed on a microscope slide with a cover slip and examined at 400X magnification (Collins 2001). The number of dead (red) and live (green) cells in 2-3 samples per drone will be counted, and a percentage of live cells calculated. We will raise virgin queens for this assay. They will be emerged in caged cells in an incubator. They will be treated and placed in individual queen cages. All queens will be placed into holding frames and transferred to a queen bank. Queen bees will be treated with a dose of each of the 8 compounds that is sub-lethal for worker bees, including non-treated controls. Queens in the queen bank will be examined weekly for at least 30 days for mortality, and emerging brood will be added to the queen bank each week to keep it vigorous. For each compound test, 30 treated queens and 30 untreated queens will be maintained. Collaborators: Ellis, M. (For additional background, rational and significance,sub-objectives, expected outcomes, methods, and collaborators, see full/separate document) 4) Objective 4a Determine whether there is an interaction between nutritional status and Nosema disease. Newly emerged workers will be individually inoculated with 10,000 spores on day 0 and provided with no pollen, mixed-bee pollen or monocultural pollen from a few representative plants important for honey bee pollination (cherry, almond, corn, etc). Bees are provided with 50% sugar syrup (changed every 3 days) and distilled water ad libitum. One hundred bees per cage (cage size: 14 × 12 × 16 cm), 4 cages per treatment will be used for each colony. Longevity of workers will be compared among the treatments by survival analysis using SAS 9.1.3. Collaborators: Huang Other Research: A survey of management practices will be conducted through an eXtension website as part of the honey bee CAP. (For additional background, rational and significance,sub-objectives, expected outcomes, methods, and collaborators, see full/separate document) 5) Objective 5a Effect of pathogens and stresses on survivorship of life-stage and caste cohorts One hundred bees per cage (cage size: 14 × 12 × 16 cm), 4 cages per treatment from three colonies will be obtained (3500 bees or 35 cages = 4 cages per treatment X 3 treatments X 3 colonies). Subject to the treatment variables under investigation, workers are provided with 50% sugar syrup (changed every 3 days), bee pollen and distilled water ad libitum. Dead bees will be removed daily, their numbers recorded and analyzed for pathogens. The experiment will be repeated with bees from at least three different colonies selected based on pathogen profile. To test the impacts of poor nutrition on bees, cage studies will first be tested with a combination of pathogens, using data from above to guide the selection of time points and levels to test. Nutrition will be examined using comparison of honey/bee bread (sterilized via gamma radiation and checked for sterility and nutritional changes), and sugar syrup/artificial bee pollen. The later will be manipulated to obtain diets of different nutritive value for the bees. Newly emerged workers divided into 3 treatments (control with normal diet, optimal artificial diet, and suboptimal diet with known poor bee performance). Temperature will be examined through a design similar as described above. Caged, newly emerged bees in replicates from the same colony will be exposed to temperatures ranging from 15° C to 40° C. These studies will be conducted at Illinois and samples sent for molecular analysis to PSU. Collaborators: Cox-Foster, Ostiguy, Solter (For additional background, rational and significance,sub-objectives, expected outcomes, methods, and collaborators, see full/separate document) 6) Objective 6a Establish a Managed Pollinator Community of Practice with eXtension and populate website with new literatures on Best Management Practices and Bee Conservation The project budgets for a dedicated technician to work under J. Skinner to execute our eXtension initiatives. We will initiate and maintain a Community of Practice (CoP) on Managed Pollinators which will serve interested clienteles the Community of Interest or CoI. The CoP will be the main conduit for media-based deliverables streaming from this CAP. Co-investigators will direct new information to the eXtension technician who will prepare Best Management and Conservations literatures and recommendations to accompany diagnostic reports. We will develop and share this CoP in full collaboration with ARS scientists involved in the Areawide project (J. Pettis, ARS Areawide Coordinator, see Documentation of Collaboration). Collaborators: Skinner (For additional background, rational and significance,sub-objectives, expected outcomes, methods, and collaborators, see full/separate document) 7) Objective 7a Identify genes that confer resistance to Varroa and pathogens, and genes that respond to biotic challenges Gene responses to infection - Two control colonies and two colonies infected with N. ceranae will be established. A second set of experiments will use colonies infected with IAPV. Nurse bees will be collected from brood frames onto dry ice and screened for Nosema or viral infection. RNA will be extracted from the immune tissues (abdominal fat bodies) of pools of 5 bees of known age. Gene expression of infected and control bees will be compared on whole genome microarrays as described below, with six biological replicates/colony. Gene expression differences will be analyzed using ANOVA. Genes that are significantly different between healthy and infected colonies will be analyzed to determine if any specific functional categories are affected (Gene Ontology analysis). For example, we should be able to determine if specific genes within pathways related to immune response are affected (Aronstein and Salvidar 2005; Evans at al. 2006). Once candidate genes have been identified, qRT-PCR will be used to monitor expression of these genes in a broader range of treatment groups (Aronstein et al. 2006). Mapping disease and parasite resistance genes - QTL influencing VSH will be identified in one backcross family after analyzing a panel of 1,536 SNPs in 192 worker bees using the Illumina BEAD station. We will make a small hole in newly sealed worker pupal cells and infest them with individual Varroa mites. We will sample at least 96 bees on dry ice that are observed opening these cells, and 96 same-age control bees from the same backcross family. For each SNP, genotypes of bees performing the behavior will be compared with control bees in 2X2 Chi-Square tests to identify loci that have significantly different frequencies of marker-alleles in bees performing the behavior (Arechavaleta-Velasco and Hunt 2004). Prior to SNP genotyping, DNA from the drone father of the F1 queen and the F1 queen herself will be subjected to sequencing on an ABI SOLiD sequencer for SNP discovery. Sequence reads will be aligned with genomic contigs and SNPs identified using PolyBayes software, targeting SNPs within or near coding exons to associate specific genes with the trait. Probes for SNP genotyping will be designed. Similar techniques utilizing a backcross family segregating for disease resistance will identify QTL and candidate genes that influence resistance. The quantitative trait measured in this case will be the pathogen levels within bees as determined by qRT-PCR. Mapping eQTL involved in honey bee resistance mechanisms - Genomic DNA will be isolated from abdomens from the backcross family used to map QTL for VSH and from heads and thoraces of bees used to map resistance to pathogens (see above). This will leave heads to be analyzed for gene expression associated with behavior and abdomens containing fat bodies for expression of genes involved in immune responses. cDNA will be obtained from these same individuals, which will then be transcribed into labeled RNA and hybridized to a microarray containing nearly all of the annotated genes in the honey bee genome (Grozinger et al. 2007). eQTL will then be analyzed in the VSH mapping population and the pathogen-resistance QTL population. Crosses to map QTL for VSH and microarrays in this population will be conducted by the Baton Rouge bee lab with separate funding (see Danka, Documentation of Collaboration). Collaborators: Hunt, Spivak, Webster, Aronstein, Grozinger (For addtional background, rational and significance,sub-objectives, expected outcomes, methods, and collaborators, see full/separate document) 8) Objective 8a Identify and characterize pathogens of managed non-Apis bees and determine cross-infectivity of microbes and parasites with Apis Commercially-produced and wild non-Apis bees will be surveyed for microbes (microsporidia, including Nosema; viruses, bacteria, and trypanosomes). Metagenomic methods developed for Apis (CAPS Project) will target microbes present in Koppert Bombus impatiens, US- and Canadian-produced Megachile rotundata, and wild foraging Bombus spp., Osmia spp., and Megachile spp. collected at five geographical locations (Maine, Massachusetts, Florida, Tennessee, New York) in the eastern United States. For commercial Bombus, 10 research colonies will be deployed at crop sites at each state; prior to deployment, 5-10 individuals will be removed and frozen at -20° C until processing. After 6 weeks of foraging in contact with wild bees, all adults will be recaptured and frozen for studies to determine development of pathogen load and presence of new microbe species. For commercial Megachile, 200 adults emerging from each of four vendors will be analyzed. Wild bees will be collected, identified to species, and pooled by species and location for analysis. Prior to processing, each wild bee will be inspected for parasites and assessed for pollen load and age. Information on the wild Bombus species pathogens will augment data produced for Bombus species in the western and Midwestern states by a current NRI grant to Cameron/Solter/Strange/Griswald. These researchers are working on genetic tests to distinguish N. bombi from other microsporidian species. Collaborators: Averill and participants in stationary apiaries, objective 3d) Objective 8b Elucidate lethal and sub-lethal effects of insecticides on non-Apis General rationale and significance Many insecticides are toxic to bumble bees, particularly after direct spray or through exposure to treated foliage (Thompson 2001). However, there is a void in toxicity tables for non-Apis, particularly for newer chemistries. Pesticide toxicities determined for honey bees are not always predictive of toxicities to other bees NRC (2007). There is debate on the extent to which neonicotinoids accumulate in pollen and nectar and impact bee health. In the case of non-Apis bees, the results are mixed, with some showing no effect (Franklin et al. 2004), and others showing sub-lethal impacts on Bombus activity (Gels et al. 2002), behavior, and learning (Morandin and Winston 2003). There is need to expand this knowledge base with the most commonly used insecticides and most commonly cultured non-Apis bees. Expected outcomes To gain: (1) New information on basic toxicology of some of our most common non-Apis managed pollinators and (2) new information on sub-lethal effects of neonicotinoids on non-Apis bees. (For addtional background, rational and significance,sub-objectives, expected outcomes, methods, and collaborators, see full/separate document)Measurement of Progress and Results
Outputs
- Published best management extension manual for IPM of parasitic mites
- Comprehensive educational website on Bee Health on eXtension.org in cooperation with the
- Surveys of incidence and coincidence of pathogens and parasites of honey bees.
- Surveys of environmental contaminants in the field and in colonies and correlations with colony health..
- Studies of effects of sub-lethal doses of environmental contaminants on bees at ambient concentrations.
- 6. Reports on breeding programs that reduce parasite and pathogen impact. 7. Recommendations on the efficacy of non-Apis pollinators for several crops and agricultural settings, and recommendations on non-Apis pollinator conservation. 8. Reports of annual meetings. 9. Reports on breeding programs that reduce parasite and pathogen impact.
Outcomes or Projected Impacts
- Increased beekeeper awareness and adoption of best practices to maintain colony health by controlling Varroa mites with minimum use of pesticides.
- Increased knowledge of pathogen identities and levels within bee hives.
- Increased understanding of causative agents involved in the colony collapses.
- Demonstrable progress towards developing more resistance to Varroa mites and pathogens in breeding stocks of bees.
- Leverage of increased funding for research of colony health issues.
- (For additional expected outcomes and impacts, see full/sepatate document)
Milestones
(2009): Website on bee health on eXtension.org established and populated with bulletin on bee biology Best management practices draft #1 completed. Progress report on all objectives due at annual meeting in January 2010. First year of studies involving cage inoculations and monitoring of pathogens in colonies. Apiaries will be established in six geographic regions. First analyses to identify relatively resistant and susceptible lines for at least one pathogen. Assessment of virulence of pathogens and impact of pesticides. Establishment of eXtension community of practice. Collection of samples to assess genetic diversity in bees.(2010): Research report draft #1 on effect of sub-lethal doses of environmental contaminants. Survey of environmental contaminants in the field and in colonies and correlations with colony health complete. Initial report on recommendations on non-Apis pollinator conservation. Progress report on all objectives due at annual meeting in January 2011. Conducting first crosses to map genes influencing resistance to mites. Successful implementation of eXtension website. Publication of Best Practices guide.
(2011): Complete and publish final research report on effect of sub-lethal doses of environmental contaminants. Initial breeding program report due. Initial report on efficacy of non-Apis pollinators for several crops and agricultural settings. Progress report on all objectives due at annual meeting in January 2012.
(2012): Final report of survey of incidence and coincidence of pathogens and parasites of honey bees and publish on eXtesnion.org. Initial report on the effects of interactions among various factors affecting honey bee colony health. Progress report on all objectives due at annual meeting in January 2013 and plans for submitting new project for next 5-year project (2015-2019).
(2013): Breeding program final report due and published on eXtension.org. Final report on efficacy of non-Apis pollinators for several crops and agricultural settings and publish on eXtension.org. Final report on the effects of interactions among various factors. affecting honey bee colony health and publish on eXtension.org. Final report on recommendations on non-Apis pollinator conservation and publish on eXtension.org. Final report on all objectives due at annual meeting in January 2014. Submit new project proposal for next 5-year cycle.
Projected Participation
View Appendix E: ParticipationOutreach Plan
Results of the project will be made available on our eXtension website. We have developed a community of practice and are gathering content for the site. This will provide quick turnaround between research trials and extension delivery.
Members of the project will also conduct workshops with beekeepers and speak at beekeeper meetings. We are considering publishing a bimonthly progress report on various aspects of the project in the two biggest apicultural trade journals.
Organization/Governance
We propose to have a chair and a secretary. The secretary is responsible for meeting minutes and annual reports. The chair is responsible for planning and running the annual meeting and coordinating proposal writing.
The secretary is elected at the annual meeting and becomes chair in the following year.
Literature Cited
Citations:
¹2008 CSREES Managed Pollinator Coordinated Agricultural Project
²2007 report of the NAS-NRC, Status of Pollinators in North America.
REFERENCES
Abramson, C.I., J. Squire, A. Sheridan, P.G. Mulder. 2004. The effect of insecticides considered harmless to honey bees (Apis mellifera): proboscis conditioning studies by using the insect growth regulators tebufenozide and diflubenzuron. Environmental Entomology 33: 378-388
Alford, D. V. 1975. Bumblebees. Davis-Poynter Ltd., London, UK
Aliano, N.P. and Ellis, M.D. 2005. A strategy for using powdered sugar to reduce varroa populations in honey bee colonies. J. Apic. Res. 44(2): 547.
Aliano, N.P., M.D. Ellis, B.D. Siegfried. 2006. Acute toxicity of oxalic acid to Varroa destructor (Acari: Varroidae) and their Apis mellifera (Hymenoptera: Apidae) hosts in laboratory bioassays. Journal Economic Entomology 99(5): 1578-1582
Allen, M., B. Ball. 1996. The incidence and world distribution of honey bee viruses. Bee World 77: 141-162
Amir, P., and H. Knipscheer. 1989. Conducting on-farm animal research: Procedures and economic analysis. Morrilton, Arkansas, USA and Ottawa, Canada: Winrock International and International Development Research Center.
Anderson, D.L., A.J. Gibbs. 1988. Inapparent virus infections and their interactions in pupae of the honey bee (Apis mellifera Linnaeus) in Australia. Journal of General Virology 69: 1617-1625
Arechavaleta-Velasco, M.E. and G.J. Hunt. 2004. Binary trait loci that influence honey bee guarding behavior. Annals of the Entomological Society American 97: 177-183.
Aronstein, K., E. Saldivar. 2005. Characterization of a honeybee Toll related receptor gene Am18w and its potential involvement in antimicrobial immune defense. Apidologie 36: 3-14
Aronstein, K., Pankiw, T., Saldivar, E. 2006. SID-1 is implicated in systemic gene silencing in the honey bee. Journal of Apicultural Research 45: 20-24
Atkins, E. L., D. Kellum. 1986. Comparative morphogenic and toxicity studies on the effect of pesticides on honeybee brood. Journal Apicultural Research 25: 242-255
Aupinel, P. et al. 2005. Improvement of artificial feeding in a standard in vitro method for rearing Apis mellifera larvae. Bulletin of Insectology 58:107-111.
Aupinel, P. et al. 2007. Toxicity of dimethoate and fenoxycarb to honey bee brood (Apis mellifera), using a new in vitro standardized feeding method. Pest Management Science 63: 1090-1094.
Bailey, L., B.V. Ball. 1991. Honey Bee Pathology. Academic Press Harcourt Brace Javanovich, Publishers San Diego CA USA
Ball, B. V., M.F. Allen. 1988. The prevalence of pathogens in honey bee (Apis mellifera) colonies infested with the parasitic mite Varroa jacobsoni. Annals of Applied Biology 113: 237-244
Belzunces, L.P., S. Garin, M.E. Colin. 1993. A convenient biological method for evidencing synergies between pesticides and bees: effects of pyrethroid insecticides and azol fungicides applied at sub lethal dose. In Fifth International Symposium on the hazards of pesticides to bees. (Harrisson, E.G., Editor. Wageningen, The Netherlands, 70-75
Berényi, O., T. Bakonyi, I. Derakhshifar, H. Köglberger, N. Nowotny. 2006. Occurrence of six honeybee viruses in diseased Austrian apiaries. Applied and Environmental Microbiology 72(4): 2414-2420 doi 10.1128/AEM.72.4.2414-2420
Beyer, A., Bandyopadhyay, S., Ideker, T. 2007. Integrating physical and genetic maps: from genomes to interaction networks. Nature Reviews Genetics 8: 699-710
Bitterman, M.E., R. Menzel, A. Fietz, S. Schafer. 1983. Classical conditioning of the proboscis extension reflex in honeybees (Apis mellifera L.). Journal of Comparative Physiology 97: 107-19
Bogdanov, S. 2004. Beeswax: quality issues today. Bee World 85: 46-50.
Bogdanov, S., V. Kilchenmann, A. Imdorf. 1998. Acaricide residues in some bee products. Journal of Apicultural Research 37: 57-67
Bogdanov, S., A. Imdorf, V. Kilchenmann. 1998. Residues in wax and honey after Apilife Var Treatment. Apidologie 29: 513-524
Bosch, J. and W. Kemp. 2001. How to manage the blue orchard bee. Sustainable Agriculture Network, National Agriculture Library Beltsville, MD.
Bowen-Walker, P.L., S.J. Martin, A. Gunn. 1999. The transmission of deformed wing virus between honeybees (Apis mellifera L.) by the ectoparasitic mite Varroa jacobsoni Oud. Journal of Invertebrate Pathology 73: 101-106
Brian, A.D. 1951. The pollen collected by bumblebees. J. Anim. Ecology. 20: 919-194.
Cameron, C.E., I. Sela, J. de Miranda, B. Yakobson, Y. Slabzeki. 2005. Characterization of bee viruses and an investigation of their mode of spread. www.bard-isus.com/320501_Cameron_Sela_BeeViruses.pdf
Chen, Y. and J. D. Evans, 2008. Prevalence and levels of Nosema ceranae in healthy and declining honey bee colonies. 41st Annual Meeting of the Society for Invertebrate Pathology and 9th International Conference on Bacillus thuringiensis. August 3-7, 2008 University of Warwick, Coventry, United Kingdom. https://www.ent.iastate.edu/sip/2008/node/417. Visited May 16, 2008.
Chen, Y., Y. Zhao, J. Hammond, H. Hsu, J.D Evans, M. Feldlaufer. 2004. Multiple virus infections in the honey bee and genome divergence of honey bee viruses. Journal of Invertebrate Pathology 87: 84-93
Chen, Y., Evans, J.D. 2007. Historical presence of Israeli acute paralysis virus in the United States. American Bee Journal 147(12): 1027-1028
Chen, Y., Evans, J.D., Smith, I.B., Pettis, J.S. 2007. Nosema ceranae is a long-present and wide-spread microsporidian infection of European honey bees (Apis mellifera) in the United States. Journal of Invertebrate Pathology doi:10.1016/j.jip.2007.07.010
Chen, Y., J. D. Evans, B. Smith, J. S. Pettis. 2008. Nosema ceranae is a long-present and wide-spread microsporidian infection of the European honey bee (Apis mellifera) in the United States. Journal of Invertebrate Pathology 97: 186188
Chittka, L. and J.D. Thomson (eds.). 2001. Cognitive ecology of pollination: animal behavior and floral evolution. Cambridge University Press, Cambridge, UK
Churchill, G.A. 2004. Using ANOVA to analyze microarray data. Biotechniques 37: 173177
Collins, A.M. and J.S. Pettis. 2001. Effect of varroa infestation on semen quality. American Bee Journal 141(8): 590-593.
Collins, A.M., Pettis, J.S., Wilbanks, R, and Feldlaufer, M.F. 2004. Performance of honey bee (Apis mellifera) queens reared in beeswax cells impregnated with coumaphos. Journal of Apicultural Research 43(3): 128-134
Cox-Foster, D. L., S. Conlan, E. C. Holmes, G. Palacios, J. D. Evans, N. A. Moran, P.-L. Quan, T. Briese, M. Hornig, D. M. Geiser, V. Martinson, D. vanEngelsdorp, A. L. Kalkstein, A. Drysdale, J. Hui, J. Zhai, L. Cui, S. K. Hutchison, J. F. Simons, M. Egholm, J.S. Pettis, W. I. Lipkin. 2007. A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318: 283-287
Crowder, M.J. and D.J. Hand. 1990. Analysis of repeated measures. Chapman and Hall/CRC Press, 257 pp.
Decourte, A., C. Armengaud, M. Ranou, J. Devillers, S. Cluzeau, M. Gauthier, M. Pham-Delegue. 2003. Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pesticide Biochemistry and Physiology 78: 83-92
Decourtye, A. et al. 2004a. Imidacloprid impairs memory and brain metabolism in the honey bee (Apis mellifera L.). Pesticide Biochemistry and Physiology 78:83-92.
Decourtye, A. et al 2004b. Effects of imidacloprid and deltamethrin on associative learning in honey bees under semi-field and laboratory conditions. Ecotoxicology and Environmental Safety 57:410-419.
De Graaf, D. C. and F. J. Jacobs. 1991. Tissue specificity of Nosema apis. J. Invertebrate Pathology. 58:277-278.
DeGrandi-Hoffman, G., Curry, R. 2004. A mathematical model of Varroa mite (Varroa destructor Anderson and Trueman) and honeybee (Apis mellifera L.) population dynamics. International Journal of Acarology 30(3): 259-274
Delaplane, K.S. 2007. Sustainable management of Varroa destructor. Bee Craft [UK] 89(11): 15-19
Delaplane, K. S., D.F. Mayer. 2000. Crop pollination by bees. Wallingford, UK: CABI Publishing (2000)
Delaplane, K.S., J.A. Berry, J.A. Skinner, J.P. Parkman, & W.M. Hood. 2005.
Integrated pest management against Varroa destructor reduces colony mite levels
and delays economic threshold. Journal of Apicultural Research 44(4): 117-122
Delaplane, K.S, J.D. Ellis, J.A. Berry. 2007. Profitability of a Varroa IPM system. Book of Abstracts, International Conference on Recent Trends in Apicultural Science, Mikkeli, Finland
Delaplane, K. and W.M. Hood. 1997. Effects of delayed acaricide treatment in honey bee
colonies parasitized by Varroa jacobsoni and a late-season treatment threshold for the southern
USA. Journal of Apicultural Research, 36: 125-132.
Delaplane, K.S. and W.M. Hood. 1999. Economic threshold for Varroa jacobsoni Oud. in the
Southeastern USA. Apidologie, 30: 383-395.
de Miranda, J.R., M. Drebot, S. Tyler, M. Shen, C.E. Cameron, D.B. Stoltz, S.M. Camazine. 2004. Complete nucleotide sequence of Kashmir bee virus and comparison with acute be paralysis virus. Journal of General Virology 85: 2263-2270
Desneux, N., A. Decourtye, J.M. Delpeuch. 2007. The sub lethal effects of pesticides on beneficial arthropods. Annual Review of Entomology 52: 81-106
Dramstad, W.E., G.L.A. Fry, and M.J. Schaffer. 2003. Bumble bee foraging is closer really better? Agriculture Ecosystems and Environment 95: 349-357.
Drummond, F.A. and C.S. Stubbs. 1997. Sampling bee populations in lowbush blueberry in Maine. Proceedings of the Sixth International Symposium on Vaccinium Culture. Acta Horticulturae 446: 101-108
El Hassani, A. 2008. Effects of sublethal doses of acetamirid and thiamethoxam on the behavior of the honey bee (Apis mellifera). Archives of Environmental Contamination and Toxicology 54: 653-661.
Ellis, M.D., F.P. Baxendale. 1997. Toxicity of seven monoterpenoids to tracheal mites (Acari: Tarsonemidae) and their honey bee (Hymenoptera: Apidae) hosts when applied as fumigants. Journal of Economic Entomology 90: 1087-1091
Ellis, M.D., B.D. Siegfried, B. Spawn. 1997. The effects of Apistan® on honey bee (Apis mellifera L.) responses to methyl parathion, carbaryl and bifenthrin exposure. Apidologie 28: 123-127
Evans, J.D., Aronstein. K.A., Chen, Y.P., Hetru, C., Imler, J-L., Jiang, H., Kanost, M., Thompson, G., Zou, Z., Hultmark, D. 2006 Immune pathways and defense mechanisms in honey bees, Apis mellifera. Insect Molecular Biology 15 (5): 645-656
Finney, D.J. 1971. Probit Analysis. 3rd Ed. London, Cambridge University Press.
Free, J.B. Insect Pollination of Crops. 2nd Edition, Academic Press: London, UK
Fries, I. 1988. Infectivity and multiplication of Nosema apis Z. in the ventriculus of the honey bee. Apidologie 19: 319-328
Fries, I. 1993. Nosema apis - a parasite in the honey bee colony. Bee World 74: 5-19
Gardener, K.E., R.L. Foster, S. ODonnell. 2006. Experimental analysis of worker division of labor in bumblebee nest thermoregulation (Bombus huntii, Hymenoptera: Apidae). Behavioral Ecology and Sociobiology 61: 783-792.
Fries, I., F. Feng, A. da Silva, S.B. Slemenda, J. Pieniazek. 1996. Nosema ceranae (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian Honey bee Apis cerana (Hymenoptera, Apidae). European Journal of Protistology. 32: 356-365
Franklin, M.T., M.L. Winston, and L.A. Morandin. 2004. Effects of clothianidin on Bombus impatiens (Hymenoptera: Apidae) colony health and foraging ability. Journal of Economic Entomology 97: 369-373
Frazier, M., Mullin, C., Frazier, J., and Ashcraft, S. 2008. What have pesticides got
to do with it? American Bee Journal 148(6): 521-524
Free, J.B. Insect Pollination of Crops. 1993. 2nd Edition, Academic Press: London, UK
Gels, J.A., D.W. Held, and D.A. Potter. 2002. Hazards of insecticides to the bumble bees Bombus impatiens foraging on flowering white clover in turf. Journal of Economic Entomology 95: 722-728
Ghosh, R., B. Ball, M. Willcocks, M. Carter. 1999. The nucleotide sequence of sacbrood virus of the honeybee: an insect picorna-like virus. Journal of General Virology 80: 1541-1549
Gilliam, M., H. Shimanuki. 1967. IN vitro phagocytosis of Nosema apis spores by honeybee hemocytes. J. Invertebrate Pathology 9: 387-389
Goulson, D. 2003. Bumblebees: their behavior and ecology. Oxford University Press Inc., NY
Goulson, D. 2003b. Effects of introduced bees on native ecosystems. Annual Review of Ecology and Systematics 34: 1-26
Goulson, D., G.C. Lye, and D. Darvill. 2007. Decline and conservation of bumble bees. Annual Review of Entomology 53: 191-208.
Govan, V.A., N. Leat, M. Allsopp, S. Davison. 2000. Analysis of the complete genome sequence of acute bee paralysis virus shows that it belongs to the novel group of insect-infecting RNA viruses. Virology 277: 457-463
Graham (ed.). 2005. The hive and the honey bee. Dadant, Hamilton, IL, 1324 pp.
Grozinger, C. M., N.M. Sharabash, C.W. Whitfield, and G.E. Robinson. 2003. Pheromone mediated gene expression in the honey bee brain. Proceedings of the National Academy of Sciences USA 100 (Supplement 2): 14519-25.
Grozinger, C.M., Fan, Y., Hoover, S.E.R. and M.L. Winston. 2007. Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera). Molecular Ecology 16: 4837-48
Haarman, T., Spivak, M., Weaver, D., Glenn, T. 2002. Effects of fluvalinate and coumaphos on queen honey bees (Hymenoptera: Apidae) in two commercial queen rearing operations. Journal of Economic Entomology 95(1): 28-35
Harbo, J.R. 1985. Instrumental insemination of queen bees-part 2. American Bee Journal 125(4):282-287.
Harbo, J.R. and J.W. Harris. 1999.) Heritability in honey bees (Hymenoptera: Apidae) of characteristics associated with resistance to Varroa jacobsoni (Mesostigmata: Varroidae. Journal of Economic Entomology 92: 261-265.
Harbo J.R. and J.W. Harris. 2005 Suppressed mite reproduction linked to the behavior of adult bees. Journal of Apicultural Research 44: 21-23
Harris, J.W. 2008. Effects of brood type on Varroa-sensitive hygiene (VSH) by worker honey bees (Hymenoptera: Apidae). Annals of the Entomological Society America (101): 1137-1144.
Hassanein, M. H. 1951. The influence of Nosema apis on the larval honey bee. Annals of Applied Biology 38:844-846.
Hassanein, M.H. l952. The effects of infection with Nosema apis on the pharyngeal salivary glands of the worker honey bee. Proceedings of Royal Entomological Society of London A 27: 22-27
Higes M, R. Martín, A.J. Meana. 2006. Nosema ceranae, a new microsporidian parasite in honeybees in Europe. Invertebrate Pathology 92(2): 93-5.
Higes, M., P. Garcia-Palencia, R. Martin-Hernandez, A. Meana. 2007. Experimental infection of Apis mellifera honeybees with Nosema ceranae (Microsporidia). Journal of Invertebrate Pathology 94: 211-217
Higes, M, R. Martín-Hernández, E. Garrido-Bailón, P. García-Palencia P, A. Meana. 2008. Detection of infective Nosema ceranae (Microsporidia) spores in corbicular pollen of forager honeybees. Journal of Invertebrate Pathology 97: 76-8.
Higes, M., Martín-Hernández, R., Garrido-Bailón, E., González-Porto, A.V., García-Palencia, P., Meana, A., del Nozal, M.J., Mayo, R., and Bernal, J.L. 2009. Honeybee colony collapse due to Nosema ceranae in professional apiaries. Environmental Microbiology Reports 1(2): 110-113 doi 10.1111/j.1758-2229.2009.00014.x
Honey Bee Genome Sequencing Consortium. 2006. Insights into social insects from the genome of the honey bee, Apis mellifera. Nature 443: 931-949
Hood, W.M. 2006. Evaluation of two small hive beetle traps in honey bee colonies. American Bee Journal 146(10): 873-876
Huang, W.G., J.H. Jiang, Y.W. Chen, C.H. Wang. 2005. Complete rRNA sequence of Nosema ceranae (Apis mellifera). http://gra103.aca.ntu.edu.tw/gdoc/F90632004a.pdf Date: 2005-11-25
Huang, Z.Y., A.V. Hanley, W. Pett, J.J. Duan. 2004. Field and semi-field evaluation of impacts of transgenic canola pollen on survival and development of worker honey bees, Journal of Economic Entomology 97: 1517-1523
Hunt, G.J., Amdam, G.V., Schlipalius, D., Emore, C., Sardesai, N., Williams, C.E., Rueppell, O., Guzmán-Novoa, E., Arechavaleta-Velasco, M., Chandra, S., Fondrk, M.K., Beye, M. and R.E. Page Jr. 2007. Behavioral genomics of honeybee foraging and nest defense. Naturwissenschaften 94: 247-267
Ibrahim, A. and M. Spivak. 2006. The relationship between hygienic behavior and suppression of mite reproduction as honey bee mechanisms of resistance to Varroa destructor. Apidologie. 37: 31-40
Kaplan, K. 2009. Survey reports latest honey bee losses. ARS News Release, 19 May 2009.
Kato, M. 1988. Bumblebee visits to Impatiens spp.: pattern and efficiency. Oecologia 76: 364-370
Kay, Ronald D. 1986. Farm Management: Planning, Control, and Implementation. Second edition. McGraw-Hill, Inc., New York, NY. Pgs 65-82
Klein, A-M., B.E. Vaissiere, J.H. Cane, I. Steffan-Dewenter, A.A. Cunningham, C. Kremen, and T. Tscharntke. 2007. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B. 274: 303-313
Knight, M.E., A. P. Martin, S. Bishop, J. L. Osborne, R. J. Hale, R. A. Sanderson, D., Goulson. 2005. An interspecific comparison of foraging range and nest density of four bumblebee (Bombus) species. Molecular Ecology 14: 18111820
Kosier, A., W. Celary, P. Olenjnicazak, J. Fijal, W. Krol, W. Solarz, and P. Plonka. 2007. The decline of the bumble bees and cuckoo bees (Hymenoptera: Apidae: Bombini) of Western and Central Europe. Oryx 41: 79-88
Koywiwattrakul, P., G.J. Thompson, S. Sitthipraneed, B.P. Oldroyd, R. Maleszka. 2004. Effects of carbon dioxide narcosis on ovary activation and gene expression in worker honeybees, Apis mellifera. J Insect Science 18: 5-36
Kremen, C., N. M. Williams, and R. W. Thorp. 2002. Crop pollination from native bees at risk
from agricultural intensification. Proceedings of the National Academy of Sciences 99:16812
-16816.
Laloi, D. and M-H. Pham-Delegue. 2004. Bumble bees show asymmetrical discrimination between two odors in a classical conditioning procedure. Journal of Insect Behavior 17: 385-396
Lanzi, G., J.R. de Miranda, M.B. Boniotti, C.E. Cameron, A. Lavazza, L. Capucci, S.M. Camazine, C. Rossi. 2006. Molecular and biological characterization of deformed wing virus of honeybees (Apis mellifera L.). Journal of Virology 80: 4998-5009
Leat, N., B. Ball, V. Govan, S. Davison. 2000. Analysis of the complete genome sequence of acute bee paralysis virus shows that it belongs to the novel group of insect-infecting RNA viruses. Virology 277: 457-463
Lin, S.A.Y. 1982. Theory and measurement of economic externalities. Academic press, N.Y.
Liu, T.P. 1989. Juvenile hormone III induced ultrastructural changes in the hypopharyngeal glands of honey bee Apis mellifera L. (Hymenoptera: Apidae) without and with infection by Nosema apis Zander (Microsporidae: Nosematidae). International Journal of Insect Morphology & Embryology 18: 73-83
Liu, T.P. 1990a. Ultrastructural changes in the secretion granules of the hypopharyngeal glands of the honeybee infected by Nosema apis and after treatment with fumagillin. Tissue and Cell 22:523-531
Liu, T.P. 1990b. Ultrastructural analysis on the gland secretion in the extracellular ducts of the hypopharyngeal glands of the honeybee infected by Nosema apis. Tissue and Cell 22: 533-540
Liu, T.P. 1992. Oöcyte degeneration in the queen honey bee after infection by Nosema apis. Tissue and Cell 24: 131-138
Locke, S.J., Y.S. Peng and N.L. Cross. 1990. A supravital staining technique for honey bee spermatozoa. Physiological Entomology 15: 187-192.
Krol, W.J., B.D. Eitzer, T. Arsenault, M.J.I. Mattina. 2007. Pesticide residues in produce sold in Connecticut 2006 including a comparison of two sample preparation methods. Bulletin 1012. The Connecticut Agricultural Experiment Station, New Haven, CT
Lodesani, M., A. Pellacani, S. Bergomi, E. Carpana, T. Rabitti, P. Lasagni. 1992. Residue determination for some products used against varroa infestation in bees. Apidologie 23: 257-272
Macedo, P.A., M.D. Ellis, B.D. Siegfried. 2002. Detection and quantification off fluvalinate resistance in Varroa mites in Nebraska. American Bee Journal 142(7): 523-526
Maori, E., S. Lavi, R. Mozes-Koch, Y. Gantman, Y. Peretz, O. Edelbaum, E. Tanne, I. Sela. 2007. Isolation & characterization of IAPV, a dicistrovirus affecting honeybees in Israel: evidence for diversity due to intra-and inter-species recombination. Journal of General Virology
Martin, S.J. 1998. A population model of the ectoparasitic mite Varroa jacobsoni in honey bee
(Apis mellifera) colonies. Ecological Modelling, 109: 267-281.
Martin, S.J. 1999. Population modelling and the production of a monitoring tool for Varroa
jacobsoni an ectoparasitic mite of honey bees. Aspects of Applied Biology, 53: 105-112.
Mondragón, L., Spivak, M. and R. Vandame. 2005. A multifactorial study of the resistance of honeybees Apis mellifera to the mite Varroa destructor over one year in Mexico. Apidologie 36: 345-358
Morandin, L. and M. Winston. 2003. Effects of novel pesticides on bumble bee (Hymenoptera: Apidae) colony health and foraging ability. Environmental Entomology 32: 555-563
Morse, R. A., K. Flottum. 1997. Honey Bee Pests, Predators, and Diseases, 3rd edition. Medina OH: A.I. Root Company 21-22
Mullin, C. A., J. H. Kim. 2001. Phytochemical action at amino acid chemosensory receptors: An approach to biopesticides, pp. 45-71. In O. Koul and G. S. Dhaliwal [eds.], Phytochemical Biopesticides. Harwood Academic Publishers, Amsterdam
NRC National Research Council. 2007. Status of pollinators in North America. National Academies Press, Washington, DC
Neumann, Peter, Dorothea Hoffmann. 2007. Small hive beetle diagnosis and control in naturally infested honey bee colonies using bottom board traps and CheckMite+ strips. Journal of Pest Science in press
Norman, D., and M. Collinson, 1986. Farming systems research in theory and practice. In J. Remenyi (Ed.), Agricultural Systems Research for Developing Countries, ACIAR Proceedings No. 11. Canberra, Australia: Australian Council for International Agricultural Research. pp. 16-30
NRC National Research Council. 2007. Status of pollinators in North America. National Academies Press, Washington, DC
Olson, K.D. 2003. Farm management: principles and strategies. Blackwell Publ. 429 pp.
Pankiw, T., M.L. Winston, and K.N. Slessor. 1994. Variation in worker response to honey bee
(Apis mellifera L.) queen mandibular pheromone (Hymenoptera: Apidae). Journal of Insect
Behavior 7(1): 1-15.
Paxton, R.J., J. Klee, S. Korpela, I. Fries. 2007. Nosema ceranae has infected Apis mellifera in Europe since at least 1998 and may be more virulent than Nosema apis. Apidologie 28: 558-565
Peng Y. et al. 1992. Effects of chlortetracycline of hone bee worker larvae reared in vitro.
Journal of Invertebrate Pathology 60:127-133
Pilarska, D.K., L. F. Solter, M. Kereselidze, A. Linde, G. Hoch. 2006. Microsporidian infections in Lymantria dispar larvae: Interactions and effects of multiple species infections on pathogen horizontal transmission. Journal of Invertebrate Pathology 93: 105113
Pleasants, J.M. 1981. Bumblebee response to variation in nectar availability. Ecology 62: 1648-166.
Ribbands, C.R. 1950. Changes in the behaviour of honey-bees following their recovery from anaesthesia. Journal of Experimental Biology 27: 302-310
Rinderer, T.E., DeGuzman, L., Lancaster, V., Delatte, G., Stelzer, J.A. 1999. Varroa in the mating yard: The effects of Varroa jacobsoni and Apistan on drone honey bees. American Bee Journal 139: 134-139
SAS Institute. 2008. SAS/STAT users guide, version 9.2. SAS Institute; Cary, NC,
USA
Schenck, F. J., J.E. Hobbs. 2004. Evaluation of the quick, easy, cheap, effective, rugged and safe (QuEChERS) approach to pesticide residue analysis. Bulletin of Environmental Contamination and Toxicology 73:24-30
Schiff, N.M. and W.S. Sheppard. 1995. Genetic analysis of commercial honey bees (Hymenoptera: Apidae) from the southern United States. Journal of Economic Entomology 88: 1216-1220
Schiff, N.M. and W.S. Sheppard. 1996. Genetic differentiation in the queen breeding population of the western United States. Apidologie 27: 77-86
Seehuus, SC, K. Norberg, U. Gimsa, T. Krekling, G.V. Amdam. 2006. Reproductive protein protects functionally sterile honey bee workers from oxidative stress. Proceedings of the National Academy of Sciences, USA. 103: 962-967
Shen, M., L., Cui, N. Ostiguy, D. Cox-Foster. 2005a. Intricate transmission routes and interactions between picorna-like viruses (Kashmir bee virus and sacbrood virus) with the honeybee host and the parasitic varroa mite. Journal of General Virology 86: 85-93
Shen, M.Q., X.L. Yang, D. Cox-Foster, L.W. Cui. 2005b. The role of varroa mites in infections of Kashmir bee virus and deformed wing virus in honey bees. Virology 342: 141-149
Shimanuki, H., K. Flottum, and A. Harman (eds.). 2007. The ABC and XYZ of bee culture. A.I. Root Co., Medina, Ohio, 911 pp.
Shimanuki, H., N. Calderone, D. Knox. 1994. Parasitic Mite. American Bee Journal 134: 827-829
Sieberts, S.K. and E.E. Schadt. 2007. Moving toward a system genetics view of disease. Mammalian Genome 18: 389-401
Siva-Jothy, M.T., J. J. W. Thompson. 2002. Short-term nutrient deprivation affects immune function. Physiological Entomology 27 (3): 206212
Solter, L.F., P. J. Siegel, D.K. Pilarska, M.C. Higgs. 2002. The impact of mixed infection of three species of microsporidia isolated from the gypsy moth, Lymantria dispar L. (Lepidoptera: Lymantriidae). Journal of Invertebrate Pathology 81: 103113
Spivak, M. G.S. Reuter. 1998. Performance of hygienic honey bee colonies in a commercial
apiary. Apidologie 29: 291-302.
Spivak, M. Reuter, GS. 2008. New direction for the Minnesota Hygienic line of bees. Amer.
Bee J. 148: 1085-1086.
Strange, J.P. and N.W. Calderone. 2009. Evaluation of apicultural characteristics of first year colonies initiated from packaged honey bees, Apis mellifera L. (Hymenoptera: Apidae. Journal of Economic Entomology (in press)
Stitt, J.P., R. P. Gaumond, J.L. Frazier, and F.E. Hanson. 2003. Action potential classifiers: A functional comparison of template matching, principal components analysis, and an artificial neural network. Chemical Senses 23: 531-539
Stubbs, C.S., H.A. Jacobson, E.A. Osgood, and F.A. Drummond. 1992. Alternative forage plants for native (wild) bees associated with lowbush blueberry, Vaccinium spp., in Maine. MAES Tech. Bull. 148. 54 pp.
Stubbs, C.S., F.A. Drummond, and E.A. Osgood. 1994. Osmia ribifloris biedermannii and Megachile rotundata (Hymenoptera: Megachilidae) introduced into the lowbush blueberry agroecosystem in Maine. Journal of the Kansas Entomological Society 67(2): 173-185
Stubbs, C.S., E.A. Osgood, J.B. Dimond, and F.A. Drummond. 1996. Hymenoptera diversity in Maine. In: Biological Diversity in Maine. Maine Natural Areas Program, Maine Forest Biodiversity Project (S.C. Gawler, J.J. Albright, P.D. Vickery, and F.C. Smith, eds.). Augusta, ME, pp. 81-86
Stubbs, C.S., F.A. Drummond, and S.L. Allard. 1997. Bee conservation and increasing Osmia spp. in Maine wild blueberry fields. Northeast Naturalist. 4(3): 133-144
Stubbs, C, and Drummond, FA 1997a. Blueberry and Cranberry (Vaccinium spp.) pollination: A comparison of managed and native bee foraging behavior. Proceedings of the International Symposium on Pollination. Acta Horticulturae 437: 341-343
Stubbs, C.S. and F.A. Drummond. 1997b. Pollination of wild lowbush blueberry, Vaccinium angustifolium by the alfalfa leafcutting bee, Megachile rotundata. Proceedings of the Sixth International Symposium on Vaccinium Culture. Acta Horticulturae 446: 189-196
Stubbs, C.S. and F.A. Drummond. 2000. Pollination of lowbush blueberry by Anthophora pallipes villosula and Bombus impatiens (Hymenoptera: Anthophoridae and Apidae). Journal of the Kansas Entomological Society 72 (3): 330-333
Stubbs, C.S. and F.A. Drummond. 2001a. Bombus impatiens (Hymenoptera: Apidae): An alternative to Apis mellifera (Hymenoptera: Apidae) for lowbush blueberry pollination Journal of Economic Entomology 94(3): 609-616
Stubbs, C.S. and F.A. Drummond (Editors). 2001b. Bees and Crop Pollination Crisis, Crossroads, Conservation. Thomas say Publications in Entomology, Entomological Society of America, Lanham, MD 156 pp.
Tarpy, D.R. and T.D. Seeley. 2006. Lower disease infections in honeybee (Apis mellifera) colonies headed by polyandrous vs monandrous queens. Naturwissenschaften 93:195-199
Tentcheva, D., L. Gauthier, N. Zappulla, B. Dainat, F. Cousserans, M.E. Colin, M. Bergon. 2004. Prevalence and seasonal variations of six bee viruses in Apis mellifera L. and Varroa destructor mite populations in France. Applied and Environmental Microbiology 70: 7285-7291
Thompson, H.M. 2001. Assessing the exposure and toxicity of pesticides to bumblebees (Bombus sp.) Apidologie 32: 305-321
Thompson, H. 2003. Behavioral effects of pesticides in bees - their potential for use in risk assessment. Ecotoxicology 12:317330
Thompson, H. and C. Maus. 2007. The relevance of sublethal effects in honey bee testing for pesticide risk assessment. Pest Management Science 63:1058-1061.
Thorp, R. W., M. D. Shepherd. 2005. Profile: Subgenus Bombus. http://www.xerces.org/Pollinator_Red_List/Bees/Bombus_Bombus.pdf
vanEngelsdorp, D., Hayes, J, Jr., Underwood, R.M., and J. Pettis. 2008. A survey
of honey bee colony losses in the U.S., fall 2007 to spring 2008. PLoS ONE 3(12):
e4071. doi:10.1371/journal.pone.0004071
Wallner, K. 1995. The use of varroacides and their influence on the quality of bee products. American Bee Journal 135: 817-821
Wang, D.I. and F.E. Moeller. 1970. The division of labor and queen attendance behavior of Nosema-infected worker honey bees. Journal of Economical Entomology 63: 1539-1541
Wang, D.I. and F.E. Moeller. 1971. Ultrastructural changes in the hypopharyngeal glands of worker honeybees infected by Nosema apis. Journal of Invertebrate Pathology 17: 308-20
Webster, T. C., K. W. Pomper, G. Hunt, E. M. Thacker and S. C. Jones. 2004. Nosema apis infection in worker and queen Apis mellifera. Apidologie 35:49-54
Webster, T.C., K.S. Delaplane (editors). 2001. Mites of the honey bee. Dadant & Sons, Hamilton, Illinois, 280 pp
Webster, T. C., K. W. Pomper, G. Hunt, E. M. Thacker and S. C.. Jones. 2004. Nosema apis infection in worker and queen Apis mellifera. Apidologie 35:49-54
Webster, T. C., E. M. Thacker, K. Pomper, J. Lowe, G. Hunt. 2008. Nosema apis infection in honey bee (Apis mellifera) queens. J. Apic. Res. 47(1):53-57
West, M.A.L., Kim, K., Kliebenstein, D.J., Leeuwen, H.V., Michelmore, R.W., Doerge, R.W., St. Clair, D.A., 2007. Global eQTL mapping reveals complex genetic architecture of transcript-level variation in Arabidopsis. Genetics 175:1441-1450
Westphal, C., I. Steffan-Dewenter, T. Tscharntke. 2003. Mass flowering crops enhance pollinator densities at a landscape scale. Ecology Letters 6(11): 961-965
Westphal, C., I. Steffan-Dewenter, and T. Tscarntke. 2006. Foraging trip duration of bumblebees in relation to landscape-wide resource availability. Ecological Entomology 31: 389
Whitfield, C.W., Behura, S.K., Berlocher, S.H., Clark, A.G., Johnston, J.S., Sheppard, W.S., Smith, D.R., Suarez, A.V., Weaver, D. and N.D. Tsutsui 2006. Thrice out of Africa: Ancient and recent expansions of the honey bee, Apis mellifera. Science 314: 642-645
Whittington, R. and M.L. Winston. 2004. Comparison and examination of Bombus occidentalis and Bombus impatiens (Hymenoptera: Apidae) in tomato greenhouses. Journal of Economic Entomology 97: 13841389
Wilson, E.E., D. Holway, and J.C. Nieh. 2006. Cold anaesthesia decreases foraging
recruitment in the New World bumblebee, Bombus occidentalis. Journal of Apicultural Research 45: 169-172
Winfree, R., N. M. Williams, J. Dushoff, and C. Kremen. 2007. Native bees provide insurance
against ongoing honey bee losses. Ecology Letters 10:1105-1113.
Winfree, R., N. M. Williams, H. Gaines, J. S. Ascher, and C. Kremen. 2008. Wild bee pollinators
provide the majority of crop visitation across land use gradients in New Jersey and
Pennsylvania. Journal of Applied Ecology 45:793-802.
Winter, K., L. Adams, R. Thorpe, D. Inouye, L. Day, J. Ascher, S. Buchmann. 2006. Importation of non-native bumble bees into North America: potential consequences of using Bombus terrestris and other non-native bumble bees for greenhouse crop production in Canada, Mexico, and the United States. www.pollinator.org/Resources/BEEIMPORTATION_AUG2006.pdf
Yang, X., D.L. Cox-Foster 2005. Impact of ectoparasite on the immunity and pathology of an invertebrate: Evidence for host immunosupression and viral amplification. Proceeding of the National Academy of Sciences 102(21): 7470-7475
Zhou, W., Aylor, D.L., Zeng, Z.-B., 2007. eQTL Viewer: visualizing how sequence variation affects genome-wide transcription. BMC Bioinformatics 8: 7 doi:10.1186/1471-2105-8-7