Research Entomologist
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Carl Hayden Bee Research Center |
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EDUCATION
Ph.D., Entomology (2003)
University of Illinois at Urbana-Champaign
M.S., Entomology (1997)
University of Illinois at Urbana-Champaign
B.A., Natural Sciences (1993)
New College of the University of South Florida (Sarasota, FL)
RESEARCH
My research focuses on the effects of stressors, such as poor nutrition, parasites, pathogens, poor queen quality, chemical treatments, and environmental extremes, on the nutrition, function and health of honey bee colonies. Specifically, this includes: 1) the effects of stressors on colony cohesion, communication, and performance, 2) mechanisms of individual and colony responses to colony stressors, 3) the effects of honey bee microbes (i.e. core, dysbiotic, and pathogenic bacteria) on critical colony interactions and functions, 4) key factors (nutrients, biochemical pathways, semiochemical cues, colony microbes, and behaviors) that regulate food processing and the nutritional state of honey bee colonies, and 5) novel chemically-mediated interactions that impact honey bees, both within the colony and between bees and their natural enemies.
As a social unit, honey bees show remarkable adaptation to colony stressors under adverse conditions. Changes in behavior and physiology allow bees to maintain colony functions and cohesiveness under a wide variety of challenges. Likewise, colony decline and death often represents a failure to fully adjust to stressors, whether through natural decline (aging queens, degraded colony infrastructure, pathogens), limitations on the efficacy of responses (starvation during poor forage, hygienic behaviors), or novel challenges (Varroa mites, chemical treatments). A key challenge is to understand how the internal state and perception of the stressed individual translates into effective colony-wide responses to stress. Bees readily adjust as a unit through individual responses to stressor cues and effective communication among colony members. To this end, my collaborators and I employ a highly-integrated, multidisciplinary approach that uses chemical ecology, behavior, biochemistry, microbiology, and functional genomics to understand how honey bees maintain a complex society in a constantly changing environment.
My primary focus is on nutritional ecology and physiology, since nutrition is a critical arbiter of health and stress responses in honey bees. Our understanding of how these honey bee social systems work includes consideration of the residential microbial communities associated with the colony. Beneficial microbes are intimately involved in nutritional processing and digestion, as well as the preservation of food stores and hive materials against other microbes. Given that honey bee colonies represent one of the most dense and microbially-vulnerable aggregations of animals on earth, inclusion of the beneficial microbial community in honey bee stress ecology is paramount.
Current research interests include:
- changes in the "internal state" (stress markers, pheromones, nutrient reserves, etc.) and responses of honey bees during stress events, such as malnutrition and starvation
- the effects of seasonal stress and nutrition on pheromone production and perception (queen pheromones)
- how beneficial and dysbiotic microbiomes affect worker-queen and worker-larva interactions
- novel chemical cues (nutrients, pheromones and semiochemicals) that regulate colony functions and nutritional outcomes, especially food processing, food storage, food sharing (trophallaxis), brood rearing (workers and reproductives), and larval-worker feeding interactions
- key nutrient and semiochemical cues used by workers to maintain colony hygiene, food stores, and beneficial microbial communities
- nutrient and biochemical changes in colony food stores (honey and bee bread (stored pollen)) during formation (food processing), storage, and eventual long-term degradation
- chemical cues that mediate interactions between honey bees and their natural enemies (Varroa mite attractants, hygienic cues from pathogens)
- effects of agricultural and apicultural practices (chemical treatments and pesticides) on colony stress, communication, food stores, and microbial balances
Two key technical approaches that I use to better assess the chemical world of bees are:
- the development of less intrusive techniques that allow for repeated sampling and chemical manipulation of the colony environment
- innovation of more sensitive, accurate, and applicable analytical techniques to evaluate honey bee chemistry and nutrition
PROFESSIONAL EXPERIENCE
October 2009 to present: Research Entomologist, Carl Hayden Bee Research Center, USDA-ARS Pacific West Area, Tucson, AZ
May 2008 to October 2009: Visiting Scientist (Postdoctoral Associate), Department of Entomology and Nematology, University of Florida, Gainesville, FL
May 2004 to May 2008: Research Entomologist (Postdoctoral Associate), Center for Medical, Agricultural, and Veterinary Entomology (CMAVE), Chemistry Unit, USDA-ARS, Gainesville, FL
August 1993 to May 2003: Graduate Teaching Assistant/Research Assistant, University of Illinois at Urbana-Champaign, Urbana, IL
August 1992 to July 1993: Department of Entomology Graduate Fellow, University of Illinois at Urbana-Champaign, Urbana, IL
HONEY BEE PUBLICATIONS
Carroll MJ, Brown NJ, Reitz D (2024) Sublethal effects of imidacloprid-contaminated honey stores on colony performance, queens, and worker activities in fall and early winter colonies. PLoS ONE 19(1):e0292376. https://doi.org/10.1371/journal.pone.0292376.
Carroll MJ, Brown NJ, Ruetz Z, Ricigliano VA, Anderson KE (2023) Honey bee retinue workers respond similarly to queens despite seasonal differences in Queen Mandibular Pheromone (QMP) signaling. PLoS ONE 18(9):e0291710. https://doi.org/10.1371/journal.pone.0291710.
Bennett MM, Welchert AC, Carroll M, Shafir S, Smith BH, Corby-Harris V (2022) Unbalanced fatty acid diets impair discrimination ability of honey bee workers to damaged and healthy brood odors. J Exp Biol 225(7):jeb244103. https://doi.org/10.1242/jeb.244103.
Carroll MJ, Corby-Harris V, Brown NB, Snyder L, Reitz DC (2022) Methoxyfenozide has minimal effects on replacement queens but may negatively affect sperm storage. Apidologie 53(3):33. https://doi.org/10.1007/s13592-022-00940-7.
Corby-Harris V, Snyder L, Meador C, Watkins-DeJong E, Obernesser BT, Brown N, Carroll MJ (2022) Diet and pheromones interact to shape honey bee (Apis mellifera) worker physiology. J Insect Physiol 143(2):104442. https://doi.org/10.1016/j.jinsphys.2022.104442.
Corby-Harris V, Bennett MM, Deeter ME, Snyder L, Meador C, Welchert AC, Hoffman A, Obernesser BT, Carroll MJ (2021) Fatty acid homeostasis in honey bees (Apis mellifera) fed commercial diet supplements. Apidologie 52(6):1195-1209. https://doi.org/10.1007/s13592-021-00896-0.
DeGrandi-Hoffman G, Corby-Harris V, Carroll M, Toth AL, Gage S, Watkins deJong E, Graham H, Chambers M, Meador C, Obernesser B (2021) The importance of time and place: nutrient composition and utilization of seasonal pollens by European honey bees (Apis mellifera L.). Insects 12(3):235. https://doi.org/10.3390/insects12030235.
Gage SL, Calle SN, Jacobson NN, Carroll MJ, Hoffman GD (2020) Pollen alters amino acid levels in the honey bee brain and this relationship changes with age and parasitic stress. Front Neurosci-Switz 14:231. https://doi.org/10.3389/fnins.2020.00231.
Meikle WG, Corby-Harris V, Carroll MJ, Weiss M, Snyder LA, Meador CAD, Beren E, Brown N (2019) Exposure to sublethal concentrations of methoxyfenozide disrupts honey bee colony activity and thermoregulation. PLoS ONE 14(3):e0204635. https://doi.org/10.1371/journal.pone.0204635.
Carroll MJ, Meikle WG, McFrederick QS, Rothman JA, Brown NJ, Weiss M, Ruetz ZJ, Chang EW (2018) Pre-almond supplemental forage improves colony survival and alters queen pheromone signaling in overwintering honey bee colonies. Apidologie 49(6):827-837. https://doi.org/10.1007/s13592-018-0607-x.
DeGrandi-Hoffman G, Gage SL, Corby-Harris V, Carroll MJ, Chambers ML, Graham RH, Watkins de Jong E, Hidalgo G, Calle SN, Azzouz-Olden F, Meador CA, Snyder LA, Ziolkowski N (2018) Connecting the nutrient composition of seasonal pollens with changing nutritional needs of honey bee (Apis mellifera L.) colonies. J Insect Physiol 109:114-124. https://doi.org/10.1016/j.jinsphys.2018.07.002
Gage SL, Kramer C, Calle SN, Carroll MJ, Heien M, DeGrandi-Hoffman G (2018) Nosema ceranae parasitism impacts olfactory learning and memory and neurochemistry in honey bees (Apis mellifera). J Exp Biol 221:jeb161489. https://doi.org/10.1242/jcb161489.
Meikle WG, Holst N, Colin T, Weiss M, Carroll MJ, McFrederick QS, Barron AB (2018) Using within-day hive weight changes to measure environmental effects on honey bee colonies. PLoS ONE 13(5):e0197589. https://doi.org/10.1371/journal.pone.0197589.
Ricigliano V, Mott BM, Floyd AS, Copeland DC, Carroll MJ, Anderson KE (2018) Honey bees overwintering in a southern climate: longitudinal effects of nutrition and queen age on colony-level molecular physiology and performance. Sci Rep-UK 8:10475. https://doi.org/10.1038/s41598-018-28732-z.
Rothman JA, Carroll MJ, Meikle WG, Anderson KE, McFrederick QS (2018) Longitudinal effects of supplemental forage on the honey bee (Apis mellifera) microbiota and inter- and intra-colony variability. Microb Ecol 76(3):814-824. https://doi.org/10.1007/s 00248-018-1151-y.
Carroll MJ, Brown N, Goodall C, Downs AM, Sheenan TM, Anderson KE (2017) Honey bees preferentially consume freshly-stored pollen. PLOS ONE 12:e0175933. https://doi.org/10.1371/journal.pone.0175933.
DeGrandi-Hoffman G, Chen Y, Rivera R, Carroll M, Chambers M, Hidalgo G, Watkins de Jong E. (2016) Honey bee colonies provided with natural forage have lower pathogen loads and higher overwinter survival than those fed protein supplements. Apidologie 47(2):186-196. https://doi.org/10.1007/s13592-015-0386-6.
Meikle WG, Adamczyk JJ, Weiss M, Gregorc A, Johnson DR, Stewart SD, Zawislak J, Carroll, MJ, Lorenz GM (2016) Sublethal effects of imidacloprid on honey bee colony growth and activity at three sites in the U.S. PLOS ONE 11(12):e0168603. https://doi.org/10.1371/journal.pone.0168603.
Anderson KE, Carroll MJ, Sheehan T, Mott BM, Maes P, Corby-Harris V (2014) Hive-stored pollen of honey bees: Many lines of evidence are consistent with pollen preservation, not nutrient conversion. Mol Ecol 23:5904-5917. https://doi.org/10.1111/mec.12966.
Teal PEA, Duehl AJ, Carroll MJ (2014) United States patent US 8647615-B1. Methods for attracting honey bee parasitic mites. Feb 11, 2014.
Graham JR, Carroll MJ, Teal PEA, Ellis JD (2013) A scientific note on the comparison of airborne volatiles produced by commercial bumble bee (Bombus impatiens) and honey bee (Apis mellifera) colonies. Apidologie 44(1):110-112. https://doi.org/10.1007/s13592-012-0162-9.
Torto B, Carroll MJ, Duehl A, Fombong AT, Katzav-Gozansky T, Nazzi F, Soroker V, Teal PEA (2013) Standard methods for chemical ecology research in Apis mellifera. J Apic Res 52:1-34. https://doi.org/10.3896/IBRA.1.52.4.06.
Carroll MJ, Duehl AJ (2012) Collection of volatiles from honey bee larvae and adults enclosed on brood frames. Apidologie 43:715-730. https://doi.org/10.1007/s13592-012-0153-x.
Graham J, Ellis J, Carroll M, Teal P (2011) Aethina tumida Murray (Coleoptera: Nitidulidae) attraction to volatiles produced by Apis mellifera L. (Hymenoptera: Apidae) and Bombus impatiens Cresson (Hymenoptera: Apidae) colonies. Apidologie 42(3):326-336. https://doi.org/10.1007/s13592-011-0017-9.
Sammataro D, LeBlanc BW, Carroll MJ, Finley-Short J, Torabi MT (2010) Antioxidants in wax cappings of honey bee brood. J Apicult Res 49(4):293-301.
Sammataro D, Finley J, LeBlance B, Wardell G, Ahumada-Segura F, Carroll MJ (2009) Feeding essential oils and 2-heptanone in sugar syrup and liquid protein diets to honey bees (Apis mellifera L.) as potential Varroa mite (Varroa destructor) controls. J Apicult Res 48(4):256-262.
