My program focuses on understanding the relationship between pollinators and their environment, with an emphasis on the effects of pesticides and understanding the physiological basis of pesticide toxicity.
Research Area:
Insect pollinators are vital for the production of many fruits, nuts and vegetables, including apples, blueberries, almonds, tomatoes and pumpkins. These crops are also vulnerable to pests and diseases, which are often controlled through the use of pesticides. However, pesticides may be toxic to insect pollinators, setting up a conflict between the need for pollination and the need for pest and disease control. In our lab we are seeking to understand how to protect pollinators from the pesticides and other toxins they encounter. The managed European honey bee, Apis mellifera, serves as a model pollinator for toxicological testing. While the honey bee is the most economically important pollinator in the U.S. and serves as an excellent model species, we are also interested in understanding pesticide toxicity in other pollinating insects as well.
Current research projects include:
1. Using sequencing to determine the floral origin of bee-collected pollen
2. Determining the impact of corn seed treatment insecticides on honey bee colonies in Ohio
3. Comparative toxicogenomics between pollinating bee species: honey bees (Apis mellifera), bumble bees (Bombus impatiens), alfalfa leafcutter bees (Megachile rotundata) and squash bees (Peponapis pruinosa)
4. Assessment of honey bee immature survival using a photographic method and analysis by volunteers at http://broodmapper.com
5. Comparing the success of managed honey bee colonies in urban and rural environments in Ohio
Teaching
Beekeeping (ENTMLGY 2200) Spring Semesters
Pesticide Science (ENTMLGY 5800) Fall Semesters (co-taught with Celeste Welty)
Graduate Students
Lilly Johnson, (Advisor), Entomology M.S. Student 2023-present
Adam Foster, (Advisor), Entomology M.S. Student 2022-present
Brandon Shannon, (Advisor), Environmental Sciences Graduate Program, M.S. 2023; Ph.D. Student. AU2023-present
Karlan Forrester (Advisor), Entomology M.S. 2022
Dylan Ricke (Advisor), Entomology M.S. 2022
Emily Walker (Advisor), Environmental Sciences Graduate Program M.S. Student. 2019-2021
Harper McMinn-Sauder (Advisor), Entomology Ph.D. Student. 2018-present
Stephanie Murray (Advisor), Entomology M.S. Graduated Dec. 2019
Rodney Richardson (Advisor), Entomology Ph.D. Graduated Dec. 2018
Natalia Riusech (Advisor), Environmental Sciences Graduate Program M.S. Graduated Dec. 2017
Douglas Sponsler (Advisor), Entomology Ph.D. Student. Graduated Dec. 2016
Baini Li (Advisor), Entomology M.S. Student. 2012-2013
Fariba Kanga (Co-advisor), Entomology M.S. Student. 2014-2015
Recent Journal Articles, past three years
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Lin, C-H.; Sponsler, D.B.; Richardson, R.T.; Watters, H.D.; Glinski, D.A.; Henderson, W.M. Johnson, R.M. 2020. Honey bees and neonicotinoid-treated corn seed: contamination, exposure, and effects. Environmental Toxicology and Chemistry 10.1002/etc.4957
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Richardson, R.T.; Eaton, T.D.; Lin, C-H.; Cherry, G.; Johnson, R.M.; Sponsler, D.B. 2020. Application of plant metabarcoding to identify diverse honeybee pollen forage along an urban-agricultural gradient. Mol Ecol, 10.1111/mec.15704
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McMinn-Sauder, H.; Richardson, R.; Eaton, T.; Smith, M.; Johnson, R. 2020. Flowers in Conservation Reserve Program (CRP) Pollinator Plantings and the Upper Midwest Agricultural Landscape Supporting Honey Bees. Insects, 11 (7), 10.3390/insects11070405
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Richardson, R.T.; Sponsler, D.B.; McMinn-Sauder, H.; Johnson, R.M. 2019. MetaCurator: A hidden Markov model-based toolkit for extracting and curating sequences from taxonomically-informative genetic markers. Methods in Ecology and Evolution, 11 (1), 181-186. 10.1111/2041-210X.13314
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Wade, A., C.-H. Lin, C. Kurkul, E. R. Regan, and R. M. Johnson. 2019 Combined Toxicity of Insecticides and Fungicides Applied to California Almond Orchards to Honey Bee Larvae and Adults Insects 10:10010020.
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Richardson, R. T., H. R. Curtis, E. G. Matcham, C. Hua Lin, S. Suresh, D. B. Sponsler, L. E. Hearon, and R. M. Johnson. 2019. Quantitative multi-locus metabarcoding and waggle dance interpretation reveal honey bee spring foraging patterns in Midwest agroecosystems. Mol. Ecol. 28(3):686-697.
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Richardson, R. T., M. N. Ballinger, F. Qian, J. W. Christman, and R. M. Johnson. 2018. Morphological and functional characterization of honey bee, Apis mellifera, hemocyte cell communities. Apidologie. 49: 397–410.
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Johnson, R. M., B. A. Harpur, K. A. Dogantzis, A. Zayed, and M. R. Berenbaum. 2018. Genomic footprint of evolution of eusociality in bees: floral food use and CYPome “blooms.” Insectes Soc. 65: 445–454.
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Bengtsson-Palme, J., R. T. Richardson, M. Meola, C. Wurzbacher, É. D. Tremblay, K. Thorell, K. Kanger, K. M. Eriksson, G. J. Bilodeau, R. M. Johnson, M. Hartmann, and R. H. Nilsson. 2018. Metaxa2 Database Builder: enabling taxonomic identification from metagenomic or metabarcoding data using any genetic marker. Bioinformatics. 34: 4027–4033.
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Richardson, R. T., J. Bengtsson-Palme, M. M. Gardiner, and R. M. Johnson. 2018. A reference cytochrome c oxidase subunit I database curated for hierarchical classification of arthropod metabarcoding data. PeerJ. 6: e5126.
Selected Past Papers
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Sponsler DB, Matcham EG, Lin CH, Lanterman JL, Johnson RM. 2017. Spatial and taxonomic patterns of honey bee foraging: A choice test between urban and agricultural landscapes. Journal of Urban Ecology. 3(1). http://dx.doi.org/10.1093/jue/juw008
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Richardson RT, Bengtsson-Palme J, Johnson RM. 2016. Evaluating and optimizing the performance of software commonly used for the taxonomic classification of DNA metabarcoding sequence data. Molecular Ecology Resources http://dx.doi.org/10.1111/1755-0998.12628
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Sponsler DB, Johnson RM. 2017. Mechanistic modeling of pesticide exposure: The missing keystone of honey bee toxicology. Environ. Toxicol. Chem. 36: 871–881. http://dx.doi.org/10.1002/etc.3661
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Richardson RT, Lin C-H, Quijia JO, Riusech NS, Goodell K, Johnson RM. 2015. Rank-based characterization of pollen assemblages collected by honey bees using a multi-locus metabarcoding approach. Applications in Plant Sciences. 3 (3): 1500043.http://dx.doi.org/10.3732/apps.1500043
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Berenbaum MR, Johnson RM. 2015. Xenobiotic detoxification pathways in honey bees. Current Opinion in Insect Science. 10: 51–58. http://dx.doi.org/10.1016/j.cois.2015.03.005
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Johnson RM. 2015. Honey bee toxicology. Annual Review of Entomology. 60:415-34. http://arjournals.annualreviews.org/eprint/JNCiwDc63RIR3bDDRRqi/full/10.1146/annurev-ento-011613-162005
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Richardson RT., Lin C-H, Quijia Pillajo JO, Sponsler DB, Goodell K, Johnson RM. 2015. Application of ITS2 metabarcoding to determine the provenance of pollen collected by honey bees in a field-crop dominated agroecosystem. Applications in Plant Sciences. 3 (1): 1400066 http://dx.doi.org/10.3732/apps.1400066
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Johnson RM & Percel EG. 2013. Pristine effects on queen rearing success in honey bees. Journal of Economic Entomology. 106: 1952-1957. http://dx.doi.org/10.1603/EC13199
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Johnson RM, Dahlgren L, Siegfried BD & Ellis MD. 2013. Acaricide, fungicide and drug interactions in honey bees (Apis mellifera). PLoS ONE. 8(1): e54092. http://dx.doi.org/10.1371/journal.pone.0054092
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Dahlgren L, Johnson RM, Siegfried BD & Ellis MD. 2012. Comparative toxicity of acaricides to honey bee (Hymenoptera: Apidae) workers and queens. Journal of Economic Entomology. 105: 1895-1902. http://dx.doi.org/10.1603/EC12175
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Teeters BS, Johnson RM, Ellis MD & Siegfried BD. 2012. Video-tracking honey bee behavior after pesticide exposure. Environmental Toxicology and Chemistry. 31: 1349-1354.http://dx.doi.org/10.1002/etc.1830
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Johnson RM, Mao W, Pollock HS, Niu G, Schuler MS & Berenbaum MR. 2012. Ecologically appropriate xenobiotics induce cytochrome P450s in Apis mellifera. PLoS ONE. 7: e31051. http://dx.doi.org/10.1371/journal.pone.0031051
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Johnson RM, Ellis MD, Mullin CA & Frazier M. 2010. Pesticides and honey bee toxicity – USA. Apidologie 41: 312-331. http://dx.doi.org/10.1051/apido/2010018
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Johnson RM, Evans JD, Robinson GE &Berenbaum MR. 2009. Changes in transcript abundance relating to colony collapse disorder in honey bees (Apis mellifera). Proceedings of the National Academy of Sciences of the United States of America 106: 14790-14795. http://dx.doi.org/10.1073/pnas.0906970106
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Johnson RM, Pollock HS &Berenbaum MR. 2009. Synergistic interactions between in-hive miticides in Apis mellifera.Journal of Economic Entomology 102: 474-479. http://dx.doi.org/10.1603/029.102.0202
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Johnson RM, Wen Z, Schuler MA, & Berenbaum MR. 2006. Mediation of pyrethroid insecticide toxicity to honey bees (Hymenoptera :Apidae) by cytochrome P450 monooxygenases. Journal of Economic Entomology 99:1046-1050. http://dx.doi.org/10.1603/0022-0493-99.4.1046