Carl Hayden Bee Research Center
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)
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) key factors (nutrients, biochemical pathways, semiochemical cues, colony microbes, and behaviors) that regulate food processing and the nutritional state of honey bee colonies, and 4) 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" (hormones, stress markers, pheromones, nutrient reserves, etc.) of honey bees during stress events, such as malnutrition and starvation
- the effects of stress and nutrition on pheromone production and perception (queen pheromones)
- 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
- contributions of beneficial microbes to honey bee nutrition and health
- 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) 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
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
PEER REVIEWED PUBLICATIONS
The publication of my research on honey bee chemical ecology (2007-2010, 4 to 6 publications) is on hold pending approval of a patent covering Varroa attractants isolated from bee brood.
Carroll, M. J., Duehl, A., and P. E. A. Teal. 2010. Methods for attracting or repelling Varroa mites. U.S. Patent (pending).
Graham, J., Ellis, J., Carroll, M., and P. Teal. 2010. Aethina tumida Murray (Coleoptera: Nitidulidae) attraction to volatiles produced by Apis mellifera L. (Hymenoptera: Apidae) and Bombus impatiens Cresson (Hymenoptera: Apidae) colonies. Apidologie, in press.
Sammataro, D., Finley, J., LeBlance, B., Wardell, G., Ahumada-Segura, F., and M. J. Carroll. 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. Journal of Apicultural Research 48: 256-262.
Carroll, M. J., Schmelz, E. A., and P. E. A. Teal. 2008. The attraction of Spodoptera frugiperda neonates to cowpea seedlings is mediated by volatiles induced by conspecific herbivory and the elicitor inceptin. Journal of Chemical Ecology 34: 291-300.
Carroll, M. J., Lampert, E. C., Berenbaum, M. R., Noyes, J. S., and P. J. Ode. 2007. New records of Copidosoma sosares (Walker) (Hymenoptera: Encyrtidae), a parasitoid of the parsnip webworm (Depressaria pastinacella (Duponchel)) (Lepidoptera: Elachistidae), in western North America. Journal of the Kansas Entomological Society 80: 309-318.
Schmelz, E. A., LeClere, S., Carroll, M. J., Alborn, H. T., and P. E. A. Teal. 2007. Cowpea chloroplastic ATP synthase is the source of multiple plant defense elicitors during insect herbivory. Plant Physiology 144: 793-805.
Carroll, M. J., Schmelz, E. A., Meagher, R. L., and P. E. A. Teal. 2006. Attraction of Spodoptera frugiperda larvae to volatiles from herbivore-damaged maize seedlings. Journal of Chemical Ecology 32: 1911-1924.
Schmelz, E. A., Carroll, M. J., LeClere, S., Phipps, S. M., Meredith, J., Chourey, P. S., Alborn, H. T., and P. E. A. Teal. 2006. Fragments of ATP synthase mediate plant perception of insect attack. PNAS 103: 8864-8899.
Carroll, M. J. and M. R. Berenbaum. 2006. Lutein sequestration and furanocoumarin metabolism in parsnip webworms under different ultraviolet light regimes in the montane west. Journal of Chemical Ecology 32: 277-305.
Carroll, M. J. and M. R. Berenbaum. 2002. Behavioral responses of the parsnip webworm to hostplant volatiles. Journal of Chemical Ecology 28: 2191-2201.
Zangerl, A. R., McKenna, D., Wraight, C. L., Carroll, M., Ficarello, P., Warner, R., and M. R. Berenbaum. 2001. Effects of exposure to event 176 Bacillus thuringiensis corn pollen on monarch and black swallowtail caterpillars under field conditions. PNAS 98: 11908-11912.
Carroll, M. J., Zangerl, A. R., and M. R. Berenbaum. 2000. Heritability estimates for octyl acetate and octyl butyrate in the mature fruit of the wild parsnip, Pastinaca sativa (Apiaceae). Journal of Heredity 91: 68-71.
Wraight, C. L., Zangerl, A. R., Carroll, M. J., and M. R. Berenbaum. 2000. Absence of toxicity of Bacillus thuringiensis pollen to black swallowtails under field conditions. PNAS 97: 7700-7703.
Carroll, M., Hanlon, A., Hanlon, T., Zangerl, A., and M. R. Berenbaum. 1997. Behavioral effects of carotenoid sequestration by the parsnip webworm, Depressaria pastinacella. Journal of Chemical Ecology 23: 2707-2719.