Source: AGRICULTURAL RESEARCH SERVICE submitted to
MANAGING HONEY BEES AGAINST DISEASE AND COLONY STRESS
Sponsoring Institution
Agricultural Research Service/USDA
Project Status
NEW
Funding Source
Reporting Frequency
Annual
Accession No.
0425645
Grant No.
(N/A)
Project No.
8042-21000-277-00D
Proposal No.
(N/A)
Multistate No.
(N/A)
Program Code
(N/A)
Project Start Date
Sep 10, 2013
Project End Date
Sep 9, 2018
Grant Year
(N/A)
Project Director
EVANS J D
Recipient Organization
AGRICULTURAL RESEARCH SERVICE
RM 331, BLDG 003, BARC-W
BELTSVILLE,MD 20705-2351
Performing Department
(N/A)
Non Technical Summary
(N/A)
Animal Health Component
40%
Research Effort Categories
Basic
40%
Applied
40%
Developmental
20%
Classification

Knowledge Area (KA)Subject of Investigation (SOI)Field of Science (FOS)Percent
2113010113090%
2113110113010%
Goals / Objectives
The overarching goal of the Bee Research Laboratory (BRL) is to provide beekeepers and regulators practical advice for maintaining sustainable honey bee populations for pollination and hive products. BRL will use integrated laboratory and field approaches to develop novel management strategies for 1) diagnosing and mitigating disease, 2) reducing the impacts on bees of pesticides and other environmental chemicals, and 3) improving bee health through better nutrition. Objective 1: Exploit genetic analyses of parasites, pathogens and bee immunity (including gut microbe interactions) to improve diagnosis and management of bee diseases. [NP305, Component 2, Problem Statement 2B] Subobjective 1.A: Manipulate honey bee immune responses toward disease. Subobjective 1.B: Conduct metagenomic analyses to identify novel pathogens and pathogen webs important for bee disease. Subobjective 1.C: Exploit bacterial gut symbionts to defend honey bees against disease. Objective 2: Use genomic information to develop novel controls for mites and other parasites, e.g., controls based on RNAi strategies or that target parasite vulnerabilities. [NP305, Component 2, Problem Statement 2B] Subobjective 2.A: Produce genome-led control strategies against Varroa mites. Subobjective 2.B: Develop gene-based control strategies for the gut parasite Nosema ceranae. Subobjective 2.C: Reduce the impacts of mite-transmitted viruses on bee health. Objective 3: Determine the impacts of physiological stress on worker and queen development and longevity, including that caused by overwintering and unbalanced diets. [NP305, Component 2, Problem Statement 2A] Subobjective 3.A: Determine the impacts of nutritional components on behavioral development, immune response and susceptibility to disease. Subobjective 3.B: Determine the effects of dietary fatty acids (FAs) on honey bee colony survival. Subobjective 3.C: Improve queen fecundity and longevity through better nutrition. Objective 4: Identify key impacts of in-hive and environmental pesticides on bee health, including sub-lethal effects and interactions with bee pathogens. [NP305, Component 2, Problem Statement 2B] Subobjective 4.A: Define synergisms between chemical exposure and disease. Subobjective 4.B: Determine whether pesticide exposure increases oxidative stress in honey bees, and if so, develop means to reduce the potential negative effects of oxidative damage to honey bees. Subobjective 4.C: Determine the effects of pesticides on honey bee basal metabolic rate (BMR). Objective 5: Develop and test hive-level treatments against mites and other bee threats. [NP305, Component 2, Problem Statement 2B] Subobjective 5.A: Develop best practices for resource availability, mite control, and colony health for migratory commercial beekeepers. Subobjective 5.B: Develop colony management strategies for improved queen health.
Project Methods
Research at the Bee Research Laboratory (BRL) focuses on using microbiological, genomic, physiological, and toxicological approaches to improve the management of bee diseases and parasites, with a mission to develop innovative tools that can be used by beekeepers to build and maintain healthy bee populations. Integrated laboratory and field approaches will be used to develop novel management strategies for 1) diagnosing and mitigating disease, 2) reducing the impacts on bees of pesticides and other environmental chemicals, and 3) improving bee health through better nutrition.

Progress 10/01/15 to 09/30/16

Outputs
Progress Report Objectives (from AD-416): The overarching goal of the Bee Research Laboratory (BRL) is to provide beekeepers and regulators practical advice for maintaining sustainable honey bee populations for pollination and hive products. BRL will use integrated laboratory and field approaches to develop novel management strategies for 1) diagnosing and mitigating disease, 2) reducing the impacts on bees of pesticides and other environmental chemicals, and 3) improving bee health through better nutrition. Objective 1: Exploit genetic analyses of parasites, pathogens and bee immunity (including gut microbe interactions) to improve diagnosis and management of bee diseases. [NP305, Component 2, Problem Statement 2B] Subobjective 1.A: Manipulate honey bee immune responses toward disease. Subobjective 1.B: Conduct metagenomic analyses to identify novel pathogens and pathogen webs important for bee disease. Subobjective 1.C: Exploit bacterial gut symbionts to defend honey bees against disease. Objective 2: Use genomic information to develop novel controls for mites and other parasites, e.g., controls based on RNAi strategies or that target parasite vulnerabilities. [NP305, Component 2, Problem Statement 2B] Subobjective 2.A: Produce genome-led control strategies against Varroa mites. Subobjective 2.B: Develop gene-based control strategies for the gut parasite Nosema ceranae. Subobjective 2.C: Reduce the impacts of mite-transmitted viruses on bee health. Objective 3: Determine the impacts of physiological stress on worker and queen development and longevity, including that caused by overwintering and unbalanced diets. [NP305, Component 2, Problem Statement 2A] Subobjective 3.A: Determine the impacts of nutritional components on behavioral development, immune response and susceptibility to disease. Subobjective 3.B: Determine the effects of dietary fatty acids (FAs) on honey bee colony survival. Subobjective 3.C: Improve queen fecundity and longevity through better nutrition. Objective 4: Identify key impacts of in-hive and environmental pesticides on bee health, including sub-lethal effects and interactions with bee pathogens. [NP305, Component 2, Problem Statement 2B] Subobjective 4.A: Define synergisms between chemical exposure and disease. Subobjective 4.B: Determine whether pesticide exposure increases oxidative stress in honey bees, and if so, develop means to reduce the potential negative effects of oxidative damage to honey bees. Subobjective 4.C: Determine the effects of pesticides on honey bee basal metabolic rate (BMR). Objective 5: Develop and test hive-level treatments against mites and other bee threats. [NP305, Component 2, Problem Statement 2B] Subobjective 5.A: Develop best practices for resource availability, mite control, and colony health for migratory commercial beekeepers. Subobjective 5.B: Develop colony management strategies for improved queen health. Approach (from AD-416): Research at the Bee Research Laboratory (BRL) focuses on using microbiological, genomic, physiological, and toxicological approaches to improve the management of bee diseases and parasites, with a mission to develop innovative tools that can be used by beekeepers to build and maintain healthy bee populations. Integrated laboratory and field approaches will be used to develop novel management strategies for 1) diagnosing and mitigating disease, 2) reducing the impacts on bees of pesticides and other environmental chemicals, and 3) improving bee health through better nutrition. This project made several important advances relevant to maintaining healthy honey bee populations this year. Along with direct outreach to beekeepers at meetings ranging from county to national and international levels, ARS scientists in Beltsville, Maryland, responded to field colony losses by identifying parasites and pathogens in samples, and helping to determine the impacts of pesticides and nutritional stress. In a total of 26 peer-reviewed papers, the five Bee Research Laboratory scientists described management tools and insights that can help reduce disease and stress on beehives. Specifically, Bee Research Laboratory (BRL) scientists generated unique insights into the effects of abiotic stress on honey bee workers and queens, showing interactions between chemical stress and disease levels. Consistent with the mission to improve honey bee management, advances were made in determining the impacts of nutrition management on disease, and the impacts of traditional miticides on honey bee longevity. Work revealed a novel counter-defense of Nosema parasites when faced with the honey bee immune response, feeding into an effort to use RNA interference and other gene-based techniques to help reduce bee disease. Genomic work identified novel viruses in bees from the U.S. and overseas, and a range of microbes that are candidates for microbial control of Varroa mites. The virus work was immediately relevant to trade decisions enforced by USDA-APHIS, while the Varroa work shows great promise for new control methods. Accomplishments 01 Impacts of improved nutrition on bee disease loads. Honey bees often face limited food availability, requiring beekeepers to supplement their diets. In a collaborative project, ARS researchers in Tucson maintained honey bee colonies on either rich or deficient natural diets. ARS researchers in Beltsville screened worker bees for viruses known to cause worker bee mortality. Bees with limited nutrition showed higher disease loads and those colonies ultimately died at a higher rate. While field experiments are ongoing, preliminary results have been transmitted to beekeepers who have been encouraged to manage forage availability and/or protein supplements in order to maintain bee nutrition. 02 Determination of Nosema defenses and counter-defenses in bees. The impacts of honey bee parasites, including the worldwide gut parasite Nosema ceranae, can be reduced by host immune responses. Nosema has been implicated in colony declines and yet there are few options available for controlling this parasite. A controlled experiment by ARS scientists in Beltsville, Maryland used RNA sequencing to show how Nosema battles honey bee immune responses with its own attacking proteins and RNA. The goal is to use this understanding to design better treatments against this key parasite, including RNA interference and breeding markers for honey bees. ARS scientists will work with industry to test products and delivery of control methods. 03 Characterization of disease threats from overseas. Parasites and pathogens are a key driver of honey bee declines. Many of the most important honey bee parasites, including Nosema ceranae and Varroa mites, reached the U.S. from overseas, and the threat of new introductions remains high. Quarantines and border regulation can be used to reduce the impacts of these threats. Along with a longstanding partnership between ARS scientists in Beltsville, Maryland and the USDA- APHIS-sponsored National Honey Bee Disease Survey, Beltsville scientists carried out genetic screens for viruses in Asia that are potential risks for U.S. honey bees. They also identified core bacterial communities on bumble bees and honey bees, with the aim of managing these associates of bees in order to improve disease resistance and nutritional health. 04 Combined impacts of chemical and disease stress on honey bees. Honey bees face significant threats from biological and chemical agents. Among the chemical agents, compounds used to control bee pests and to control pests or microbes on crop plants can inadvertently add to honey bee losses. ARS scientists in Beltsville, Maryland have carried out long-lasting work regarding the interactive effects of chemical and disease stress on bee health, most recently showing the combined effects of the neonicitinoid pesticide imidacloprid and mite stress on bee health. They showed an increase in disease loads of worker bees and lower survival for these bees when exposed to chemicals. These results can inform beekeepers and regulators, leading to better avoidance of chemical stress and mitigation strategies for exposed bees. 05 Impacts of pesticide exposure on honey bee queens. Using field- realistic exposure to neonicotinoid chemicals used to control crop pests and miticides used in the hive to control Varroa, ARS scientists in Beltsville, Maryland determined a negative impact on genes expected to determine honey bee queen health and longevity. This work connects with ongoing efforts to measure sperm viability in order to ensure that queens are vital and productive. The results can provide guidance to queen breeders regarding which chemicals are most likely to impact the health and fertility of the queens they sell. 06 Characterization of the development of honey bee queens. Honey bee queen health is integral to the longevity of honey bee colonies. Queen longevity can be impacted through the environment faced by developing honey bee queen-destined larvae. In a review and synthesis, an ARS scientist in Beltsville, Maryland identified key genetic changes in queen and worker larvae that are responsible for healthy queen development. The results offer new insights into the timing of queen development and the nutritional and energetic needs of healthy queens. Queen breeders can benefit from precise data showing how quality queens are produced within the colony and how the grafting age of these queens affects their future success.

Impacts
(N/A)

Publications

  • Gong, H., Chen, X., Chen, Y., Hu, F., Zhang, J., Lin, Z., Yu, J., Zhang, H. 2016. Evidence of Apis cerana sacbrood virus infection in Apis mellifera. Applied and Environmental Microbiology. doi: 10.1128/AEM.03292-15.
  • Li, Z., Huang, S., Huang, W., Geng, H., Zhao, Y., Li, M., Chen, Y., Su, S. 2016. A scientific note on detection of honey bee viruses in the darkling beetle (Alphitobius diaperinus), an inhabitant in Apis cerana colonies. Apidologie. doi: 10.1007/s13592-016-0430-1.
  • Kapheim, K.M., et. al. (51 Authors), Yocum, G.D., Kemp, W.P., Evans, J.D., Robinson, G.E. 2015. Genomic signatures of evolutionary transitions from solitary to group living. Science. 348(6239):1139-1143.
  • Hoffman, G.D., Chen, Y., Rivera, R., Carroll, M.J., Chambers, M.L., Hidalgo, G., Watkins De Jong, E.E. 2015. Honey bee colonies provided with natural forage have lower pathogen loads and higher overwinter survival than those fed protein supplements. Apidologie. doi: 10.1007/s13592-015- 0386-6.
  • Peng, W., Zhao, Y., Chen, Y., Li, J., Zeng, Z. 2015. A descriptive study of the prevalence of parasites and pathogens in Chinese black honey bees, Apis mellifera mellifera. PLoS One. 142: 1364�1374.
  • Ziska, L.H., Pettis, J.S., Tomecek, M.B., Clark, A., Dukes, J.S., Loladze, I., Polley, H.W. 2016. Rising atmospheric CO2 is reducing the protein concentration of a floral pollen source essential for North American bees. Proceedings of the Royal Society B. 283(1828):20160414.
  • De Miranda, J., Cornman, R.S., Evans, J.D., Haddad, N., Neumann, P., Gauthier, L. 2015. Genome characterization, prevalence and distribution of a Macula-like virus from Apis mellifera and Varroa destructor. Viruses. 7:3586-3602.
  • Gauthier, L., Cornman, R.S., Hartmann, U., Cousserans, F., Evans, J.D., De Miranda, J., Neumann, P. 2015. The Apis mellifera filamentous virus genome. Viruses. 7:3798-3815.
  • Guo, J., Wu, J., Chen, Y., Evans, J.D., Dai, R., Luo, W., Li, J. 2015. Characterization of gut bacteria at different developmental stages of Asian honey bees, Apis cerana. Journal of Invertebrate Pathology. 127: 110- 114.
  • Poelchau, M.F., Coates, B.S., Childers, C., Evans, J.D., Hackett, K.J., Shoemaker, D.D. 2016. Agricultural applications of insect ecological genomics. Current Opinion in Insect Science. 13:61-69. doi:10.1016/j.cois. 2015.12.002.
  • Coates, B.S., Poelchau, M.F., Childers, C., Evans, J.D., Handler, A.M., Guerrero, F., Skoda, S.R., Hopper, K.R., Wintermantel, W.M., Ling, K., Hunter, W.B., Oppert, B.S., Perez De Leon, A.A., Hackett, K.J., Shoemaker, D.D. 2015. Arthropod genomics research in the United States Department of Agriculture-Agricultural Research Service: Current impacts and future prospects. Trends in Entomology. 11(1):1-27.
  • Pettis, J.S., Rice, N.D., Joselow, K., Vanengelsdorp, D., Chaimanee, V. 2016. Colony failure linked to low sperm viability in honey bee (Apis mellifera) queens and an exploration of potential causative factors. PLoS One. doi: 10.1371/journal.pone.0147220.
  • Dively, G.P., Embrey, M.S., Kamel, A., Hawthorne, D.J., Pettis, J.S. 2015. Assessment of chronic sublethal effects of imidacloprid on honey bee colony health. PLoS One. doi: 10.1371/journal.pone.0118748.
  • Mustafa, S.G., Spooner-Hart, R., Duncan, M., Pettis, J.S., Rosendranz, P., Steidle, J. 2015. Age and aggregation trigger mating behavior in the small hive beetle, Aethina tumida. Naturwissenschaften. doi: 10.1007/s00114-015- 1300-9.
  • Li, J., Powell, J., Guo, J., Evans, J.D., Wu, J., Williams, P., Lin, Q., Moran, N.A., Zhang, Z. 2015. Two gut community enterotypes recur in diverse bumblebee species. Current Biology. 25:R652-R653.
  • Tozkar, O.C., Kence, M., Kence, A., Huang, Q., Evans, J.D. 2015. Metatranscriptomic analyses of honey bee colonies. Frontiers in Genetics. doi: 10.3389/fgene.2015.00100.
  • Corona, M.V., Libbrecht, R., Wheeler, D.E. 2016. Molecular mechanisms of phenotypic plasticity in social insects. Current Opinion in Insect Science. 13:55-60. doi: 10.1016/j.cois.2015.12.003.
  • Jiang, H., Dobesh, S., Donghun, K., Evans, J.D., Nachman, R.J., Krzysztof, K., Janusz, Z., Park, Y. 2016. Ligand selectivity in tachykinin and natalisin neuropeptidergic systems of the honey bee parasitic mite Varroa destructor. Scientific Reports. 6:19547. doi: 10.1038/srep19547.
  • Straub, L., Williams, G.R., Pettis, J.S., Fries, I., Neumann, P. 2015. Superorganism resilience: Eusociality and susceptibility of ecosystem service providing insects to stressors. Current Opinion in Insect Science. 12:109.
  • Smart, M.D., Pettis, J.S., Rice, N., Browning, Z., Spivak, M. 2016. Assessing the health of colonies and individual honey bees (Apis mellifera L.) in a commercial beekeeping operation. PLoS One. e0152685. doi:10.1371/ journal.pone.0152685.
  • Guseman, A.J., Miller, K., Kunkle, G., Dively, G.P., Pettis, J.S., Evans, J.D., Vanengelsdorp, D., Hawthorne, D.J. 2016. Multi-drug resistance transporters and a mechanism-based strategy for assessing risks of pesticide combinations to honey bees. PLoS One. doi: 10.1371/journal.pone. 0148242.
  • Cook, S.C., Eubanks, M.D., Gold, R.E., Behmer, S.T. 2016. Seasonal effects of food macronutrient content on ants: Colony and individual responses. Journal of Insect Physiology. 87(2016):35-44.
  • Chaimanee, V., Evans, J.D., Chen, Y., Jackson, C., Pettis, J.S. 2016. Sperm viability and gene expression in honey bee queens (Apis mellifera) following exposure to the neonicotinoid insecticide Imidacloprid and the organophosphate Acaricide Coumaphos. Journal of Insect Physiology. 89:1-8. doi: 10.1016/j.jinsphys.2016.03.004.
  • Abbo, P.M., Kawasaki, J.K., Hamilton, M.C., Cook, S.C., Hoffman, G.D., Li, W., Lie, J., Chen, Y. 2016. The effects of Imidacloprid and Varroa destructor on the survival and health of European honey bees, Apis mellifera. Insect Science. doi: 10.1111/1744-7917.12335.
  • Grozinger, C.M., Evans, J.D. 2015. Social insects: from the lab to the landscape - translational approaches to pollinator health. Current Opinion in Insect Science. doi:10.1016/j.cois.2015.06.001.
  • Huang, Q., Chen, Y., Wang, R., Schwarz, R., Evans, J.D. 2015. MicroRNAs of host honey bees, Apis mellifera respond to the infection of Microsporidian parasite Nosema ceranae. Scientific Reports. doi: 10.1038/srep 17494 2.


Progress 10/01/14 to 09/30/15

Outputs
Progress Report Objectives (from AD-416): The overarching goal of the Bee Research Laboratory (BRL) is to provide beekeepers and regulators practical advice for maintaining sustainable honey bee populations for pollination and hive products. BRL will use integrated laboratory and field approaches to develop novel management strategies for 1) diagnosing and mitigating disease, 2) reducing the impacts on bees of pesticides and other environmental chemicals, and 3) improving bee health through better nutrition. Objective 1: Exploit genetic analyses of parasites, pathogens and bee immunity (including gut microbe interactions) to improve diagnosis and management of bee diseases. [NP305, Component 2, Problem Statement 2B] Subobjective 1.A: Manipulate honey bee immune responses toward disease. Subobjective 1.B: Conduct metagenomic analyses to identify novel pathogens and pathogen webs important for bee disease. Subobjective 1.C: Exploit bacterial gut symbionts to defend honey bees against disease. Objective 2: Use genomic information to develop novel controls for mites and other parasites, e.g., controls based on RNAi strategies or that target parasite vulnerabilities. [NP305, Component 2, Problem Statement 2B] Subobjective 2.A: Produce genome-led control strategies against Varroa mites. Subobjective 2.B: Develop gene-based control strategies for the gut parasite Nosema ceranae. Subobjective 2.C: Reduce the impacts of mite-transmitted viruses on bee health. Objective 3: Determine the impacts of physiological stress on worker and queen development and longevity, including that caused by overwintering and unbalanced diets. [NP305, Component 2, Problem Statement 2A] Subobjective 3.A: Determine the impacts of nutritional components on behavioral development, immune response and susceptibility to disease. Subobjective 3.B: Determine the effects of dietary fatty acids (FAs) on honey bee colony survival. Subobjective 3.C: Improve queen fecundity and longevity through better nutrition. Objective 4: Identify key impacts of in-hive and environmental pesticides on bee health, including sub-lethal effects and interactions with bee pathogens. [NP305, Component 2, Problem Statement 2B] Subobjective 4.A: Define synergisms between chemical exposure and disease. Subobjective 4.B: Determine whether pesticide exposure increases oxidative stress in honey bees, and if so, develop means to reduce the potential negative effects of oxidative damage to honey bees. Subobjective 4.C: Determine the effects of pesticides on honey bee basal metabolic rate (BMR). Objective 5: Develop and test hive-level treatments against mites and other bee threats. [NP305, Component 2, Problem Statement 2B] Subobjective 5.A: Develop best practices for resource availability, mite control, and colony health for migratory commercial beekeepers. Subobjective 5.B: Develop colony management strategies for improved queen health. Approach (from AD-416): Research at the Bee Research Laboratory (BRL) focuses on using microbiological, genomic, physiological, and toxicological approaches to improve the management of bee diseases and parasites, with a mission to develop innovative tools that can be used by beekeepers to build and maintain healthy bee populations. Integrated laboratory and field approaches will be used to develop novel management strategies for 1) diagnosing and mitigating disease, 2) reducing the impacts on bees of pesticides and other environmental chemicals, and 3) improving bee health through better nutrition. This project made several important advances relative to relevant to National Program 305 (Crop Production), Action Plan Component II (Bees and Pollination), Problem Area A (Honey bees) this year. Several genome- based studies reached publication this year, describing traits and weaknesses of honey bee parasites (e.g., Nosema apis), and describing the genomes and stress responses of two additional honey bee species, two bumble bee species, and several additional pollinators. BRL scientists produced high profile papers describing the correlates with colony decline and experimental efforts to determine the impacts of pesticides on queen and colony health. They also described the impacts of disease on queen health. ARS scientists in Beltsville, MD presented these findings to stakeholders, policy leaders and fellow researchers in a timely fashion, and the key results were widely reported in local and national media as well as the scientific literature. Accomplishments 01 Reducing pesticide stress on honey bee colonies. Bee colonies were shown to accumulate diverse agricultural chemicals in wax, honey, and bee bodies, enabling an improved resolution of pesticide stress on bee health. In addition, analyses showed that honey bee colonies exposed to the insecticide imidacloprid have higher rates of mortality. Doses in the field were low, however, generally below the experimental level that induced colony health impact. This information can be used by beekeepers and growers to limit exposure of bees to damaging chemicals, ensuring that farming practices will be compatible with pollinator health. 02 Determination of the impacts of parasite interactions on bee health. Honey bees, especially in situations of colony decline, often battle two or more parasites at the same time. Controlled experiments showed which parasites interact with each other to impact bee disease and colony health, information that can be used by beekeepers as they monitor and treat their colonies. This work also includes symbiotic bacteria of honey bees, and these results pave the way for probiotics or beekeeper-driven changes in bee nutrition that can bolster bee health. 03 Improved understanding of honey bee and pollinator immunity through genomics. Through collaborative work, ARS researchers at Beltsville, Maryland, carried out full genome sequencing on two Asian honey bee species, the North American bumble bee species used most for commercial pollination, as well as the Alfalfa leaf cutting bee. These projects helped identify the behavioral and disease-related traits of these species, and gave insights into social behavior and their key biology traits. Researchers can now target immune proteins that are especially responsive to disease agents. This information can be used for the management of pollinator species in croplands, and to help improve efforts of honey bee breeders. 04 Rates and causes of queen and colony failure for honey bees. ARS scientists in Beltsville, Maryland, presented evidence for continued high colony losses in the United States. They worked jointly with USDA- APHIS and the University of Maryland to conduct the most extensive survey of U.S. honey bee health and disease agents to date. They presented evidence for continued high colony losses in the U.S., helped identify predominant viruses in FY15 and determined specific causes through experimentation. Results indicate that queen health, disease, and genetic traits have a strong bearing on colony losses. By expanding this multiyear project to include 34 states, ARS will generate substantial baseline data for bee colony health, and will be better able to catch emergent signs of Colony Collapse Disorder (CCD) and disease outbreaks. 05 Characterization of a widespread gut parasite of honey bees. Beltsville scientists determined in 2015 that the primary trypanosomatid parasite of honey bees was misidentified, leading to confusion in the understanding of bee disease. Using extensive collections as well as genetic and microscopic insights, a new genus and species were named in order to improve the understanding of this parasite and its biology. This result has enabled worldwide studies of this parasite, pointing to an unappreciated role in bee declines. The new species has been recognized by the entire beekeeping and regulatory community and has led to renewed analyses of disease collections to determine its impact on bee health worldwide.

Impacts
(N/A)

Publications

  • Elsik, C.G., Worley, K.C., Bennett, A.K., Beye, M., Camara, F.C., Childers, C.P., De Graaf, D.C., Debyser, G., Deng, J., Devreese, B., Elhaik, E., Evans, J.D., Foster, L.J., Graur, D., Guigo, R., Hoff, K.J., Holder, M.E., Hudson, M.E., Hunt, G.J., Jiang, H., Josh, V., Khetani, R.S., Kosarev, P., Kovar, C.L., Ma, J., Maleszka, R., Moritz, R.F., Munoz-Torres, M.C., Murphy, T.D., Muzny, D.M., Newsham, I.F., Reese, J.T., Robertson, H.M., Robinson, G.E., Rueppell, O., Solovyev, V., Stanke, M., Stolle, E., Tsuruda, J.M., Vaerenbergh, M., Waterhouse, R.M., Weaver, D.B., Whitfield, C.W., Wu, Y., Zdobnov, E.M., Zhang, L., Zhu, D., Gibbs, R.A. 2014. Finding the missing honey bee genes: lessons learned from a genome upgrade. Biomed Central (BMC) Genomics. 15:86.
  • Barribeau, S.M., Sadd, B.M., Du Plessis, L., Brown, M.J., Buechel, S.D., Carolan, J.C., Christiaens, O., Colgan, T.J., Erler, S., Evans, J.D., Helbing, S., Karaus, E., Lattorff, M.G., Marxer, M., Meeus, I., Napflin, K. , Schmid-Hempel, R., Smagghe, G., Waterhouse, R.M., Yu, N., Zdobnov, E.M., Schmid-Hempel, P. 2015. A depauperate immune repertoire precedes evolution of sociality in bees. Genome Biology. 16:83.
  • Wheeler, D.E., Buck, N., Evans, J.D. 2014. Expression of insulin/insulin- like signalling and TOR pathway genes in honey bee caste determination. Insect Molecular Biology. 23(1):113-21.
  • Schwarz, R.S., Bauchan, G.R., Murphy, C.A., Ravoet, J., De Graaf, D.C., Evans, J.D. 2015. Genetic and ultrastructure characterization of a known and a new species of trypanosomatidae from the honey bee Apis mellifera: Crithidia mellificae Langridge and McGhee, 1967 and Leptomonas passim sp. n. Protist. 1:1-17.
  • Chaimanee, V., Chantawannakul, P., Chen, Y., Evans, J.D., Pettis, J.S. 2014. Effects of host age on susceptibility to infection and immune-gene expression in honey bee queens (Apis mellifera) inoculated with Nosema ceranae. Apidologie. 45(4): 451-463.
  • Poelchau, M.F., Childers, C., Moore, G.G., Tsavvatapalli, V., Evans, J.D., Lee, C., Lin, H., Lin, J., Hackett, K.J. 2015. The i5k Workspace@NAL � enabling genomic data access, visualization, and curation for the i5k community . Nucleic Acids Research. 43:D714-719.
  • Sadd, B.M., Bambeau, S.M., Bloch, G., Bourke, A.F., Collins, D., Dearden, P.K., Flores, K.B., Degraaf, D.C., Elsik, C.G., Gadau, J., Grimmelikhuijzen, C.J., Klasberg, S., Hasselmann, M., Lozier, J.D., Robertson, H., Robinson, G.E., Amdam,, G.V., Brown, M.J., Chittka, L., Erler, S., Evans, J.D., Gibbs, R., Hartfelder, K., Hasselmann, M., Hauser, F., Hudson, M., Johnson, R.M., Moritz, R., Murphy, T., Richards, S., Rueppell, O., Salzberg, S.L., Zdobnov, E.M., Schmid-Hempel, P., Smagghe, G. , Stolle, E., Van Vaerenbergh, M., Waterhouse, R., Worley, K. 2015. Two bumblebee genomes illuminate the route to advanced social living. Genome Biology. 16:76.
  • Chen, Y., Pettis, J.S., Zhao, Y., Cornman, R.S., Tallon, L.L., Sadzewicz, L.L., Ye, J., Li, R., Zhang, X., Hamilton, M.C., Pernal, S., Melathopoulos, A., Yan, X., Evans, J.D. 2013. Sequencing and genome annotation of honey bee microsporidia parasite, Nosema apis and comparative genome analysis with its sympatric congener, N. ceranae. Biomed Central (BMC) Genomics. 14:451. DOI: 10.1186/1471-2164-14-451.
  • Chen, Y., Pettis, J.S., Corona, M.V., Chen, W., Spivak, M., Visscher, K.P., Hoffman, G.D., Boncristiani, H., Zhao, Y., Vanengelsdorp, D., Delaplane, K., Solter, L., Drummond, F., Kramer, M.H., Lipkin, I.W., Palacios, G., Hamilton, M.C., Smith Jr, I.B., Huang, S., Zheng, H., Li, J., Zhang, X., Zhou, A., Wu, L., Zhou, J., Lee, M.L., Teixeira, E.W., Li, Z., Evans, J.D., Li, C. 2014. Israeli acute paralysis virus: epidemiology, pathogenesis and implications for honey bee health and Colony Collapse Disorder (CCD). PLoS Pathogens. 10 (7):e1004261. DOI: 10.1371/journal.ppat.1004261.
  • Li, J., Cornman, R., Evans, J.D., Pettis, J.S., Zhao, Y., Murphy, C.F., Hammond, J., Peng, W., Wu, J., Boncristiani, H., Zhou, L., Chen, Y. 2014. Systemic spread and propagation of a plant pathogenic virus in European honey bees, Apis mellifera. mBio. 5(1):e00898-13. DOI: 10.1128/mBio.00898- 13.
  • Tarpy, D.R., Pettis, J.S., Vanengelsdorp, D. 2013. Genetic diversity affects colony survivorship in commercial honey bee colonies. Naturwissenschaften. 100(8): 723-728.


Progress 10/01/13 to 09/30/14

Outputs
Progress Report Objectives (from AD-416): The overarching goal of the Bee Research Laboratory (BRL) is to provide beekeepers and regulators practical advice for maintaining sustainable honey bee populations for pollination and hive products. BRL will use integrated laboratory and field approaches to develop novel management strategies for 1) diagnosing and mitigating disease, 2) reducing the impacts on bees of pesticides and other environmental chemicals, and 3) improving bee health through better nutrition. Objective 1: Exploit genetic analyses of parasites, pathogens and bee immunity (including gut microbe interactions) to improve diagnosis and management of bee diseases. [NP305, Component 2, Problem Statement 2B] Subobjective 1.A: Manipulate honey bee immune responses toward disease. Subobjective 1.B: Conduct metagenomic analyses to identify novel pathogens and pathogen webs important for bee disease. Subobjective 1.C: Exploit bacterial gut symbionts to defend honey bees against disease. Objective 2: Use genomic information to develop novel controls for mites and other parasites, e.g., controls based on RNAi strategies or that target parasite vulnerabilities. [NP305, Component 2, Problem Statement 2B] Subobjective 2.A: Produce genome-led control strategies against Varroa mites. Subobjective 2.B: Develop gene-based control strategies for the gut parasite Nosema ceranae. Subobjective 2.C: Reduce the impacts of mite-transmitted viruses on bee health. Objective 3: Determine the impacts of physiological stress on worker and queen development and longevity, including that caused by overwintering and unbalanced diets. [NP305, Component 2, Problem Statement 2A] Subobjective 3.A: Determine the impacts of nutritional components on behavioral development, immune response and susceptibility to disease. Subobjective 3.B: Determine the effects of dietary fatty acids (FAs) on honey bee colony survival. Subobjective 3.C: Improve queen fecundity and longevity through better nutrition. Objective 4: Identify key impacts of in-hive and environmental pesticides on bee health, including sub-lethal effects and interactions with bee pathogens. [NP305, Component 2, Problem Statement 2B] Subobjective 4.A: Define synergisms between chemical exposure and disease. Subobjective 4.B: Determine whether pesticide exposure increases oxidative stress in honey bees, and if so, develop means to reduce the potential negative effects of oxidative damage to honey bees. Subobjective 4.C: Determine the effects of pesticides on honey bee basal metabolic rate (BMR). Objective 5: Develop and test hive-level treatments against mites and other bee threats. [NP305, Component 2, Problem Statement 2B] Subobjective 5.A: Develop best practices for resource availability, mite control, and colony health for migratory commercial beekeepers. Subobjective 5.B: Develop colony management strategies for improved queen health. Approach (from AD-416): Research at the Bee Research Laboratory (BRL) focuses on using microbiological, genomic, physiological, and toxicological approaches to improve the management of bee diseases and parasites, with a mission to develop innovative tools that can be used by beekeepers to build and maintain healthy bee populations. Integrated laboratory and field approaches will be used to develop novel management strategies for 1) diagnosing and mitigating disease, 2) reducing the impacts on bees of pesticides and other environmental chemicals, and 3) improving bee health through better nutrition. This project made several important advances relevant to National Program 305 (Crop Production), Action Plan Component II (Bees and Pollination), Problem Area A (Honey bees) this year. The Bee Research Laboratory has a balanced focus on several aspects of bee management and health, with scientists focused on nutrition, chemical stress, and the effects of parasites and pathogens, the three major causes of honey bee declines. Work at the colony level revealed high levels of pesticides in production honey bee colonies across the country, and an impact of colony genetic diversity on persistence and health. Controlled experiments with important pathogens and parasites showed traits of resilience in bees that can be exploited by breeding or improved management. Genomic strategies showed the depth of the honey bee immune response, vulnerabilities in varroa mites, the key bee parasites, and possible virulence factors in honey bee viruses. Scientists presented these findings to stakeholders, policy leaders, and fellow researchers in a timely fashion, and the key results were widely reported in local and national media as well as the scientific literature. Accomplishments 01 Abundance of agricultural chemicals and impacts on bees. Bee colonies were shown to accumulate diverse agricultural chemicals in wax, honey, and bee bodies. Levels of one fungicide in particular were shown to be correlated with colony health and in particular with levels of the parasite Nosema ceranae. 02 Development of resources and protocols for bee research. BRL scientists played major roles in five chapters of the BeeBook compilation, a multi-year effort to document best practices in bee research that was published in book form in early 2014. They were also involved in organizing and enacting the efforts of the i5k (5000 arthropod genome) initiative, an effort that will improve bee and crop health through comparative genomics, and in a major analysis of protocols for controlled rearing of honey bees. 03 Immune responses toward bacterial pathogens. A complete transcriptome project was carried out to determine the effects of bacterial infection (the agent of American foulbrood disease) on honey bee larvae, the first such project focused on a bee pathogen. Disruptions to bee development were shown as well as changes in immune profiles, an aid to breeding more resistant bees.

Impacts
(N/A)

Publications

  • Boncristiani, H., Evans, J.D., Chen, Y., Pettis, J.S., Murphy, C.A., Lopez, D.L., Simone-Finstrom, M., Strand, M., Tarpy, D., Rueppell, O. 2013. In- vitro infection of pupae with Israeli Acute Paralysis Virus suggests variation for susceptibility and disturbance of transcriptional homeostasis in honey bees (Apis mellifera). PLoS One. DOI: 10.1371/journal. pone.0073429.
  • Chaimanee, V., Chantawannakul, P., Chen, Y., Evans, J.D., Pettis, J.S. 2012. Differential expression of immune genes of adult honey bee (Apis mellifera) after inoculated by Nosema ceranae. Journal of Insect Physiology. 58(8):1090-1095.
  • Cornman, R.S., Boncristiani, H., Dainat, B., Chen, Y., Vanengelsdorp, D., Weaver, D., Evans, J.D. 2013. Population-genomic variation within RNA viruses of the Western honey bee, Apis mellifera, inferred from deep sequencin. Biomed Central (BMC) Genomics. 14:154.
  • Huang, S., Csaki, T., Double, V., Dussaubat, C., Evans, J.D., Gajda, A.M., Gregorc, A., Hamilton, M.C., Kamler, M., Lecocq, A., Muz, M.N., Neumann, P. , Ozkirim, A., Schiesser, A., Sohr, A.R., Tanner, G., Tozkar, C., Williams, G.R., Wu, L., Zheng, H., Chen, Y. 2014. International standardization of cage designs and feeding regimes for honey bee in vitro experiments. Journal of Economic Entomology. 107(1):54-62.
  • Evans, J.D., Brown, S.J., Hackett, K.J., Richards, S., Lawson, D., Elsik, C., Coddington, J., Edwards, O., Emrich, S., Gabaldon, T., Goldsmith, M., Hanes, G.W., Misof, B., Mu-Oz-Torres, M., Niehuis, O., Papanicolaou, A., Pfrender, M., Poelchau, M., Purcell, M.F., Robertson, H.M., Ryder, O., Tagu, D., Torres, T., Zdobnov, E., Zhang, G., Zhou, X. 2013. The i5K Initiative: Advancing arthropod genomics for knowledge, human health, agriculture, and the environment. Journal of Heredity. 104(5):595-600.
  • Neumann, P., Evans, J.D., Pettis, J.S., Pirk, C.W., Schafer, M.O., Tanner, G., Ellis, J.D. 2013. Standard methods for small hive beetle research. Journal of Apicultural Research. 52(4):1-32.
  • Cornman, R.S., Lopez, D.L., Evans, J.D. 2013. Transcriptional response of honey bee larvae infected with the bacterial pathogen Paenibacillus larvae. Developmental and Comparative Immunology. DOI: 10.1371/journal.pone. 0065424.
  • Cabrera, A.R., Shirk, P.D., Grozinger, C.M., Evans, J.D., Teal, P.E. 2013. Examining the role of foraging and malvolio in host-finding behavior in the honey bee parasite, Varroa destructor (Anderson & Trueman). Archives of Insect Biochemistry and Physiology. 85(2):61-75.
  • Pettis, J.S., Lichtenberg, E.M., Andree, M., Stitzinger, J., Rose, R., Vanengelsdorp, D. 2013. Crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS One. DOI: 10.1371/journal.pone.0070182.
  • Tarpy, D., Pettis, J.S., Vanengelsdorp, D. 2013. Genetic diversity affects colony survivorship in commercial honey bee colonies. Naturwissenschaften. DOI: 10.1007/s00114-013-1065-y.