Progress 03/01/08 to 08/31/11
Outputs
OUTPUTS: Significant outputs included identifying functions of multiple pesticide-detoxifying enzymes in honey bees, providing an alternative explanation for the cause of colony collapse disorder via microarray analysis (viral overload and ribosome fragmentation), and characterizing components of honey and propolis that may improve bee resistance to pesticides. Findings have been disseminated in scholarly and popular publications as well as both academic and popular lectures and presentations. Popular presentations include: State Beekeepers Association, Wadsworth, IL, June 12, 2010 ("Bees and pesticides," "UI Pollinatarium"); Keynote lecture, Association of Education and Research Greenhouse Curators, July 27, 2010; Pollinator Conservation short course, Xerces Society, Cooperative Extension, July 29, 2010; C-U Sunrise Rotary, Business of bees, September 3, 2010; St. Louis SciFest, Colony Collapse Disorder, St. Louis, MO, October 16, 2010; USA Science and Engineering Festival, National Mall, National Academy of Sciences, "The Buzz on Bees," October 24, 2010; Lunch break segment, WGN News, "Cooking with honey," December 16, 2010; NPR Science Friday with Ira Flatow, "Bee Bonanza: From Beekeeping to Big Business," December 24, 2011; "CCD update" and "Honey and health" at Buzz into Beekeeping workshop, Kankakee River Valley Beekeeping Association, Bourbonnais, IL, March 12, 2011; March 29, 2011 Treehugger online interview; March 31, 2011 Interview, Savvy Soumya Misra Assistant Coordinator Food Safety and Toxins Centre for Science and Environment, Tughlakabad Institutional Area New Delhi, India; Interview MongaBay.Com April 3, 2011; Phone-in show, "Bees in crisis," KPCC Public Radio, Pasadena, CA April 14, 2011; Champaign Exchange Club, "The buzz on bees," Champaign, IL, April 25, 2011; "Honey I'm Homemade," Illinois State Beekeepers Association, Champaign, IL, June 25, 2011. Scholarly presentations include; Keynote, Michigan Entomological Society, June 26, 2010; Keynote lecture, International Conference on Pollinators, State College, PA, July 24, 2010; Keynote, Status of Pollinators; Past, Present, Future, North American Pollinator Protection Campaign, Washington, DC, October 20, 2010; Seminar in Ecology and Evolution, University of Amsterdam, The Netherlands, September 23, 2010; Department of Entomology seminar, Virginia Tech, Blacksburg, VA, October 7, 2010; Entomological Society of America L.L. Langstroth symposium, December 12, 2010; Environmental Protection Agency webinar, "Bees and pesticides," January 13, 2011. In addition, over 2000 visitors to the UI Pollinatarium received information on honey bee biology and honey and the PI organized a symposium for the 2010 Entomological Society of America annual meeting celebrating the bicentennial of the birth of Lorenzo Langstroth and the impact of his career on contemporary apicultural practices. PARTICIPANTS: May Berenbaum (Dept. Entomology) has served as principal investigator and Mary Schuler (Dept. Cell and Developmental Biology) as co-PI of this project. The doctoral dissertation of Reed M. Johnson was based on his work on this project; he graduated with a PhD December 2008, joined the laboratory of Marion Ellis at University of Nebraska as a postdoctoral associate studying pesticide synergism in bees and started as an assistant professor of bee biology at Ohio State University in August 2011. Guodong Niu devoted part of his doctoral work to this project; he received his PhD in August 2010 and is now a postdoctoral associate at Pennsylvania State University. Ling-Hsiu Liao and Katherine Noble are doctoral students who worked on this project during its last year of funding and learned basic techniques of bee research and beekeeping practices. Wenfu Mao has been a postdoctoral associate working on this project since its inception and has published several papers based on this work. Henry Pollock was an undergraduate associated with this project who is now enrolled as a graduate student at UIUC. Gene Robinson directs the UIUC Bee Research Facility and has provided valuable advice as well as bees throughout the duration of this project. TARGET AUDIENCES: Target audiences for this work include the scientific community, beekeepers, and the general public. Within the scientific community, our work has expanded knowledge of the function of cytochrome P450 monoozygenases in insects and provided a novel hypothesis to account for the causes of colony collapse disorder. Results of our work may have practical significance in determining beekeeping practices in that there is evidence that constituents of honey influence the ability of bees to detoxify pesticides, suggesting that honey alternatives (sucrose and high fructose corn syrup) have hitherto unsuspected implications for honey bee health. Our work also provides a potential method for determining whether pesticide exposure has occurred in-hive or as a consequence of foraging in treated agricultural fields. For the general public, our work has increased public awareness of threats to honey bee health and has increased public appreciation of the value of honey as a food not only for bees but for humans as well. PROJECT MODIFICATIONS: Not relevant to this project.
Impacts
Outcomes of this project include identification of a group of cytochrome P450 monooxygenases, in the subfamily CYP6AS, expressed in honey bee midguts that metabolize quercetin, a flavonoid that is abundant in nectar and honey, as well as identification of another group of midgut P450s, in the subfamily CYP9Q, that are principally responsible for detoxifying tau-fluvalinate and coumaphos, the two acaricides registered for use in-hive to control varroa mites. Earlier work on this project demonstrated that these two pesticides synergize each other; our finding that they are both metabolized by the same enzymes suggests a mechanism underlying that synergism. We have also demonstrated that both sets of genes encoding detoxification enzymes are upregulated by honey but not sucrose, high-fructose corn syrup, phenobarbital or other typical P450 inducers. We have identified coumaric and caffeic acid as responsible constituents for upregulation, along with propolis constituents including pinocembrin. Propolis also upregulates these detoxification enzymes and aids bees in detoxifying aflatoxin, a product of pathogenic Aspergillus fungi. The fact that the agricultural pesticide bifenthrin and tau-fluvalinate upregulate CYP9Q genes differentially suggests that patterns of induction can be used by beekeepers to ascertain whether exposure to pyrethroids occurred in-hive or while bees were foraging in agricultural fields.
Publications
- Niu, G., Johnson, R.M. and Berenbaum, M.R. 2010. Toxicity of mycotoxins to honeybees and its amelioration by propolis. Apidologie: 10.1051/apido/2010039.
- Johnson R.M., Evans, J., Robinson, G.E. and Berenbaum, M.R. 2009. Changes in transcript expression relating to colony collapse disorder in Apis mellifera. Proc. Nat Acad Sci USA 106: 14790-14795.
- Mao, W., Johnson, R.M., Rupasinghe, S., Schuler, M.A. and Berenbaum, M.R. 2009. Quercetin-metabolizing CYP6AS enzymes of the pollinator Apis mellifera (Hymenoptera: Apidae). Comp Biochem Physiol C: Toxicology and Pharmacology 154: 427-434.
- Johnson, R.M., Huang, Z.Y. and Berenbaum, M.R. 2010. Role of detoxification in Varroa destructor (Acari: Parasitidae) tolerance of the miticide tau-fluvalinate. Int. J.Acarol. 36: 1-6.
- Nasonia Genome Sequencing Consortium (Werren, J.H., Richards, S., Desjardins, C.A. et al.) 2010. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327: 343-348.
- Oakeshott, J., Johnson, R.M., Berenbaum, M.R., Ranson, H., Cristino, A.S. and Claudianos, C. 2010. Metabolic enzymes associated with xenobiotic and chemosensory responses in Nasonia vitripennis. Insect Molecular Biology 19(S): 147-164.
- Berenbaum, M.R. 2009. Colony collapse disorder: Apis-pocalypse now Atti Accademia Nazionale Entomologia (In Press).
- Mao, W., Schuler, M.A. and Berenbaum, M.R. 2011. CYP9Q-mediated detoxification of acaricides in the honey bee (Apis mellifera). Proc. Natl. Acad. Sci. USA 31: 12657-12662.
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Progress 03/01/10 to 02/28/11
Outputs
OUTPUTS: Most significant outputs include identifying functions of multiple pesticide-detoxifying enzymes in honey bees, providing an alternative explanation for the cause of colony collapse disorder, and characterizing components of honey and propolis that may improve bee resistance to pesticides. Findings have been disseminated in scholarly and popular publications as well as both academic and popular lectures and presentations. Popular presentations include: State Beekeepers Association, Wadsworth, IL, June 12, 2010 ("Bees and Ppesticides," "UI Pollinatarium"); Keynote lecture, Association of Education and Research Greenhouse Curators, July 27, 2010; Pollinator Conservation short course, Xerces Society, Cooperative Extension, July 29, 2010; C-U Sunrise Rotary, "Business of Bees," September 3, 2010; St. Louis SciFest, Colony Collapse Disorder, St. Louis, MO, October 16, 2010; USA Science and Engineering Festival, National Mall, National Academy of Sciences, "The Buzz on Bees," October 24, 2010; Lunch break segment, WGN News, "Cooking with Honey," December 16, 2010; NPR Science Friday with Ira Flatow, "Bee Bonanza: From Beekeeping to Big Business," December 24, 2011; "CCD update" and "Honey and Health" at Buzz into Beekeeping workshop, Kankakee River Valley Beekeeping Association, Bourbonnais, IL, March 12, 2011; March 29, 2011 Treehugger online interview; March 31, 2011 Interview, Savvy Soumya Misra Assistant Coordinator Food Safety and Toxins Centre for Science and Environment Tughlakabad Institutional Area New Delhi, India; Interview MongaBay.Com April 3, 2011; Phone-in show, "Bees in Crisis," KPCC Public Radio, Pasadena, CA April 14, 2011; Champaign Exchange Club, "The buzz on bees," Champaign, IL, April 25, 2011; "Honey I'm Homemade," Illinois State Beekeepers Association, Champaign, IL, June 25, 2011. Scholarly presentations include; Keynote, Michigan Entomological Society, June 26, 2010; Keynote lecture, International Conference on Pollinators, State College, PA, July 24, 2010; Keynote, Status of Pollinators: Past, Present, Future, North American Pollinator Protection Campaign, Washington, DC, October 20, 2010; Seminar in Ecology and Evolution, University of Amsterdam, The Netherlands, September 23, 2010; Department of Entomology seminar, Virginia Tech, Blacksburg, VA, October 7, 2010; Entomological Society of America L. L. Langstroth symposium, December 12, 2010; Environmental Protection Agency webinar, "Bees and pesticides," January 13, 2011. In addition, over 2000 visitors to the UI Pollinatarium received information on honey bee biology and honey. PARTICIPANTS: May Berenbaum (Dept. Entomology) has served as principal investigator and Mary Schuler (Dept. Cell and Developmental Biology) as co-PI of this project. The doctoral dissertation of Reed M. Johnson was based on his work on this projectp; he graduated with a PhD December 2008 and joined the laboratory of Marion Ellis at University of Nebraska as a postdoctoral associate studying pesticide synergism in bees and will start as an assistant professor of bee biology at Ohio State University in August 2011. Guodong Niu devoted part of his doctoral work to this project; he received his PhD in August 2010 and is now a postdoctoral associate at Johns Hopkins University. Ling-Hsiu Liao and Katherine Noble are doctoral students who worked on this project during its last year of funding and learned basic techniques of bee research and beekeeping practices. Wenfu Mao has been a postdoctoral associate working on this project since its inception and has published several papers based on this work. Henry Pollock was an undergraduate associated with this project who is now enrolled as a graduate student at UIUC. Gene Robinson directs the UIUC Bee Research Facility and has provided valuable advice as well as bees throughout the duration of this project. TARGET AUDIENCES: Target audiences for this work include the scientific community, beekeepers, and the general public. Within the scientific community, our work has expanded knowledge of the function of cytochrome P450 monoozygenases in insects and provided a novel hypothesis to account for the causes of colony collapse disorder. Results of our work may have practical significance in determining beekeeping practices in that there is evidence that constituents of honey influence the ability of bees to detoxify pesticides, suggesting that honey alternatives (sucrose, high fructose corn syrup) have hitherto unsuspected implications for honey bee health. Our work also provides a potential method for determining whether pesticide exposure has occurred in-hive or as a consequence of foraging in treated agricultural fields. For the general public, our work has increased public awareness of threats to honey bee health and as well has increased public appreciation of the value of honey as a food not only for bees but for humans as well. PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
Outcomes of this project include identification of a group of cytochrome P450 monooxygenases, in the subfamily CYP6AS, expressed in honey bee midguts that metabolize quercetin, a flavonoid that is abundant in nectar and honey, as well as identification of another group of midgut P450s, in the subfamily CYP9Q, that are principally responsible for detoxifying tau-fluvalinate and coumaphos, the two acaricides registered for use in-hive to control varroa mites. Earlier work on this project demonstrated that these two pesticides synergize each other; our finding that they are both metabolized by the same enzymes suggests a mechanism underlying that synergism. We have also demonstrated that both sets of genes encoding detoxification enzymes are upregulated by honey but not sucrose, high-fructose corn syrup, phenobarbital or other typical P450 inducers. We have identified coumaric and caffeic acid as responsible constituents for upregulation, along with propolis constituents including pinocembrin. Propolis also upregulates these detoxification enzymes and aids bees in detoxifying aflatoxin, a product of pathogenic Aspergillus fungi. The fact that the agricultural pesticide bifenthrin and tau-fluvalinate upregulate CYP9Q genes differentially suggests that patterns of induction can be used by beekeepers to ascertain whether exposure to pyrethroids occurred in-hive or while bees were foraging in agricultural fields.
Publications
- Mao, W., Schuler, M.A. and Berenbaum, M.R. 2011. CYP9Q-mediated detoxification of the miticide tau-fluvalinate in the honey bee (Apis mellifera). Published online before print PNAS July 20, 2011, doi: 10.1073/pnas.1109535108.
- Johnson, R.M., Mao, W., Pollock, H.S., Niu, G., Schuler, M.A. and Berenbaum, M.R. 2011. Ecologically appropriate xenobiotics induce cytochrome P450s in Apis mellifera. Submitted to PLoS ONE.
- Johnson, R.M., Pollock, H. and Berenbaum, M.R. 2009. Synergistic interactions between in-hive miticides in Apis mellifera. Journal of Economic Entomology 102(2):474-479.
- Oakeshott J., Johnson, R.M., Berenbaum, M.R., Ranson, H., Cristino, A.S. and Claudianos, C. 2010. Metabolic enzymes associated with xenobiotic and chemosensory responses in Nasonia vitripennis. Insect Molecular Biology 19(S): 147-164.
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Progress 03/01/09 to 02/28/10
Outputs
OUTPUTS: Annotating the detoxification genes of the wasp Nasonia vitripennis permitted the use of a comparative approach to identify the CYP6AS subfamily, which underwent expansion in Apis mellifera relative to N vitripennis, as candidate genes encoding enzymes that metabolize hive products unique to A. mellifera. Induction studies showed that CYP6AS1, CYP6AS3, and CYP6AS4 are inducible by honey, pollen and propolis. Molecular models indicated quercetin, a flavonoid in honey and pollen, as a shared substrate for CYP6AS1, CYP6AS3, CYP6AS4, and CYP6AS10 and in vitro biochemical assays with heterologously expressed enzymes confirmed activity. The availability of the honey bee genome sequence facilitated identifying genes encoding enzymes effecting pesticide metabolism. Expression of 6 P450 cDNAs revealed CYP9Q1, CYP9Q2, and CYP9Q3 all metabolize tau-fluvalinate (Apistan). Work is ongoing to characterize the hydroxylated metabolite. Toxicity of aflatoxin B1 and ochratoxin A, products of Aspergillus species found in hives (and the causative agent of stonebrood) was evaluated. Workers tolerate a range of concentrations of both mycotoxins. Enhancement of AB1 toxicity by piperonyl butoxide, a P450 inhibitor, indicates a role for P450s in AB1 detoxification. Extracts of propolis also reduced AB1 toxicity and delayed mortality consistent with P450-mediated detoxification. Propolis may serve a role in bee health by inducing activity of P450s involved in mycotoxin detoxification. Bees consuming honey also showed greater AB1 tolerance; moreover, bees fed quercetin display enhanced tolerance of fluvalinate, indicating P450 regulation is tuned to chemicals that occur naturally in the hive environment. Thus, toxicologically, sucrose diets are not equivalent to honey; aflatoxin toxicity increases on diets of sucrose and HFCS. We examined molecular regulation of detoxification using phenobarbital as a general inducer, monitoring transcript variation on a custom microarray with probes specific for 45 P450s, 10 carboxylesterases, 7 glutathione-S-transferases, 206 chemosensory genes, 17 tetraspanins, and houskeeping genes and controls. Only one gene, tetraspanin 16, was differentially expressed in response to phenobarbital. No P450s or other detoxificative genes were differentially expressed (NCBI-GEO). We used whole-genome microarrays to compare gene expression in guts of bees from CCD colonies from the East and West Coasts and guts of bees from healthy colonies collected before the appearance of CCD. We identified a consensus list of 65 transcripts as potentially diagnostic for CCD status. Elevated expression of detoxification genes was not seen in any populations and genes associated with immunity showed no trend in expression despite increased prevalence of viruses in CCD colonies. Unusual ribosomal RNA fragments, however, were substantially more abundant in CCD bee guts. These fragments may result from picorna-like viruses and arrested translation due to viral hijacking of the ribosome. Ribosomal fragment abundance and multiple viruses are promising diagnostic markers for CCD. PARTICIPANTS: Graduate students Reed Johnson, Guodong Niu, Postdoctoral Associate Wenfu Mao and Undergraduate Henry Pollock. TARGET AUDIENCES: The scientific community, the general public, and the apiculture community. PROJECT MODIFICATIONS: Not relevant to this project.
Impacts
1. Management suggestions made at several meetings of beekeeping groups (Garfield Park Conservatory, Illinois State Beekeepers Association). 2. Findings presented at public lectures, designed to raise pollinator awareness: NASA interview about citizen science and pollinators August 13, 2009; Executive Club Luncheon, "Queen (bee) for a day," Champaign Country Club, Champaign, IL, August 20, 2009: WILL AM Focus 580 August 25, 2009; week of August 25, 2009, BBC ScienceAction Now, BBC Material World, BBC Radio Five Live, Jop de Vrieze. Wetenschapsredactie, NRC Handelsblad, Popular Science Magazine, Times of London, New Scientist, The Scientist, Time Magazine, Fox News Channel, Bloomberg News; New York Times news forum, August 29-30, 2009; Campus Round Table, Pollinatarium, September 10, 2009; Girls Do Science, Flowers and Pollinators, Pollinatarium, Urbana IL, September 12, 2009; Bug Night, B.T. Washington Elementary School, Champaign, IL, May 12, 2010; WILL AM Focus 580 May 16, 2010; permanent exhibit constructed at UI Pollinatarium (public outreach science center devoted to pollinators). 3. Findings presented at scientific meetings (XXII Italian Congress of Entomology, Ancona, Italy, June 15, 2009; Karlsruhe Institute of Technology, Environment/Technology October 12, 2009;USDA AFRI workshop, March 24, 2010. 4. Graduate training--Reed Johnson, Guodong Niu; Postdoctoral training--Wenfu Mao
Publications
- Johnson R.M., Evans, J., Robinson, G.E. and Berenbaum, M.R. 2009. Changes in transcript expression relating to colony collapse disorder in Apis mellifera. Proc. Nat. Acad. Sci. USA 106: 14790-14795.
- Mao, W., Johnson, R.M., Rupasinghe, S., Schuler, M.A. and Berenbaum, M.R. 2009. Quercetin-metabolizing CYP6AS enzymes of the pollinator Apis mellifera (Hymenoptera: Apidae). Comp. Biochem. Physiol. C: Toxicology and Pharmacology 154: 427-434.
- Johnson, R.M., Huang, Z.Y. and Berenbaum, M.R. 2010. Role of detoxification in Varroa destructor (Acari: Parasitidae) tolerance of the miticide tau-fluvalinate. Int. J.Acarol. 36: 1-6.
- Nasonia Genome Sequencing Consortium (Werren, J.H., Richards, S., Desjardins, C.A. et al.). 2010. Functional and evolutionary insights from the genomes of three parasitoid Nasonia species. Science 327: 343-348.
- Oakeshott J, Johnson, R.M., Berenbaum, M.R., Ranson, H., Cristino, A.S. and Claudianos, C. 2010. Metabolic enzymes associated with xenobiotic and chemosensory responses in Nasonia vitripennis Insect Molecular Biology 19(S): 147-164
- Berenbaum, M.R. 2010. Colony collapse disorder: Apis-pocalypse now Atti Accademia Nazionale Entomologia (In Press).
- Niu, G., Johnson, R.M. and Berenbaum, M.R. 2010. Toxicity of mycotoxins to honeybees and its amelioration by propolis. Apidologie (In Press).
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Progress 03/01/08 to 02/28/09
Outputs
OUTPUTS: Outputs: 1. Completion of microarray analysis of honey bees with and without a diagnosis of colony collapse disorder. 2. Identification of substrates for CYP6AS3 (quercetin and other flavonoids). 3. Characterization of inducibility responses of CYP6AS genes in honey bees (responses to extracts of honey, propolis, and pollen but not to sucrose, phenobarbital, or xanthotoxin). 4. Identification of substrates for CYP4G11 (oleic acid and other related fatty acids). 5. Documentation of synergistic interactions between coumaphos and fluvalinate in honey bee adults. 6. Demonstration of nonenzymatic resistance to fluvalinate in varroa mites. 7. Completion of doctoral training of Reed Johnson. 8. Introduction of three undergraduates to honey bee research. 9. Outreach efforts through Beespotter and the University of Illinois Pollinatarium. PARTICIPANTS: Reed Johnson - Graduate Student: Now a postdoctoral associate with Blair Siegfried at the University of Nebraska at Lincoln. Wenfu Mao - Postdoctoral Associate. Gene Robinson - Collaborator and UIUC Faculty. Jay Evans - Collaborator from USDA-ARS, Beltsville, MD. Henry Pollock - Undergraduate, currently a senior at Washington University. Alan Yanahan and Allen Lawrance - UIUC Undergraduates involved in honey bee outreach efforts and toxicology studies. TARGET AUDIENCES: Target audiences include honey bee researchers (work on functional genomics of CYP genes and gene inducibility), beekeepers (work on CCD effects on gene expression, miticide toxicity, and effects of diet on detoxification), the insect genomics community (work on comparative hymenopteran genomics), and the general public (multiple public lectures to garden groups, beekeepers, and the general public on honey bee health and the results of this work). PROJECT MODIFICATIONS: Nothing significant to report during this reporting period.
Impacts
The honey bee genome encodes just 46 P450's. The paucity of P450 genes in the honey bee is not a trait common to the order Hymenoptera; the jewel wasp (Nasonia vitripennis) genome encodes 92 P450's, a number consistent with other insect genomes. Yet P450-mediated detoxification occurs in honey bees. P450's detoxify the pyrethroid pesticide tau-fluvalinate, which is commonly used as a miticide to control the honey bee parasite Varroa destructor. Varroa mites have developed resistance to tau-fluvalinate, likely through a non-detoxicative mechanism, causing beekeepers to switch to coumaphos, an organophosphate. However, both coumaphos and tau-fluvalinate are lipophilic and accumulate in the wax component of the hive, potentially exposing bees to both compounds simultaneously. Coumaphos is detoxified by P450's as well, and bees pretreated with either coumaphos or tau-fluvalinate were much less tolerant of the other miticide in bioassays, suggesting that bee mortality may occur as a result of interactions between these two widely used compounds. Phenobarbital failed to induce P450 activity in honey bees; other chemicals effective at inducing P450's in other insects, including xanthotoxin, salicylic acid, and indole-3-carbinol, also failed to induce P450 activity. Only quercetin, a component of pollen and honey, brought about increased tau-fluvalinate tolerance. Whereas a diet of "bee candy" alone caused no upregulation of P450's, feeding on a diet containing honey, pollen, or propolis extracts induced gene expression of three potentially detoxicative P450's. Thus, P450's in honey bees appear to be regulated largely or exclusively by compounds frequently encountered in the hive environment; this work calls into question the practice of feeding bees for an extended period of time on non-honey diets. Subsequent work documented that CYP6AS3 is responsible for detoxifying quercetin; this P450 is the first to be functionally characterized in honey bees. Pesticides were initially suspected as a contributing factor in colony collapse disorder (CCD), the mysterious disappearance of bees first noticed in late 2006. Gene expression of guts from bees diagnosed with CCD was compared with guts of healthy bees using whole genome micorarrays. One non-detoxicative P450 showed reduced expression in guts of CCD bees. Several genes with immune function were differentially expressed in healthy and afflicted bees but differences were not consistent with the state of colony health. Deformed wing virus was more prevalent in CCD bees, as were unusual ribosomal RNA fragments that may be related to the breakdown in ribosome function following picornavirus infection, one in particular may serve as a genetic diagnostic maker for CCD. These RNA fragments suggest that ribosome breakdown mat be a root cause of CCD. In general, this work demonstrates that deeper understanding of honey bee toxicology may contribute to improving management practices that enhance overall honey bee health.
Publications
- Johnson, R.M. and Berenbaum, M.R. 2009. Role of detoxification in Varroa destructor tolerance of the miticide tau-fluvalinate. Int. J. Arachnology [Submitted].
- Johnson, R.M. 2008. Toxicogenomics of Apis mellifera. Doctoral dissertation, University of Illinois Urbana Champaign.
- Johnson, R.M., Pollock, H. and Berenbaum, M.R. 2009. Synergistic interactions between in-hive miticides in Apis mellifera. Journal of Economic Entomology 102(2):474-479.
- Berenbaum, M.R. 2009. Colony collapse disorder: Apis-pocalypse now Atti. Accademia Nazionale Entomologia.
- Johnson, R.M., Evans, J.D., Robinson, G.E. and Berenbaum, M.R. 2009. Changes in gene expression relating to colony collapse disorder in Apis mellifera. Proceedings of the National Academy of Sciences [Under Review].
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