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Goals and Objective: Goal 1
Objective 1.7

Obj 1.7: Determine sub-lethal effects of pesticide metabolites on physiological and behavioral systems


Rationale and significance
Studies on the effects of agrochemicals and their metabolites on pollinators have focused on acute effects (Atkins and Kellum 1986) at the expense of sub-lethal outcomes (Desneux et al. 2007). In the case of metabolites, there is little information at all. There is evidence that pyrethroids and neonicotinoids impair associative learning performance in bees (Decourtye et al. 2003, Desneux et al. 2007). Many agricultural pesticides are known to impair bee development, adult longevity, mobility, navigation, orientation, feeding behavior, and learning (Desneux et al. 2007). This may partly explain the common CCD observation that affected foragers fail to return to the nest. 

We will concentrate our efforts on insecticides (fluvalinate, coumaphos, etc.) and combinations that include potentially synergistic fungicides that are frequently detected, based on our current work, at high residue levels in beehive samples (pollen, wax, bees) associated with CCD or declining bee health. If we show that relevant doses of pesticides and their combinations, already documented in declining hive samples, impact food consumption, longevity and key motor behaviors of the bees in lab bioassays, a case for colony-level impact can then by hypothesized. Support for this will be further developed by using more discriminatory olfactory learning tests such as the proboscis extension response bioassay and through electrophysiological recordings to assess combinatory interactions at specific contact neuroreceptors. Identification of key pesticides and combinations at documented hive levels that reconstitute acute or sublethal symptoms in lab groups of bees that are consistent with colony decline can then be used in colony level experiments. Diagnostic pesticide blends incorporated into artificial pollens or nectars can then be fed to observational bee colonies for longer term studies. However, these latter studies, due to their expense and time constraints, need to occur after the prerequisite lab investigations designed to filter out the complexity of many potential chemical combinations and synergistic interactions with bee diseases. 

Expected outcomes
To determine:

  1. impact of chronic ingestion of pesticide metabolites on survivorship and immune system function,
  2. impact of chronic ingestion of pesticide metabolites on behavior changes and learning, and
  3. the distribution of pesticide metabolites within chronically exposed colonies (pollen, nectar, honey, brood, adult bees, wax and royal jelly) at different exposure levels. 

Pesticide sub-objectives

  • 1.6. Elucidate synergistic and sub-lethal effects of in-hive miticides on colony health
  • 1.7. Determine sub-lethal effects of pesticide metabolites on physiological and behavioral systems
  • 1.8. Determine sub-lethal effects of pesticides on bees exposed to pesticides and selected combinations of pesticides during larval development and the nurse bee stage

Workers across these objectives are aware of the need to coordinate with fellows in Objective 1.2E to provide optimum pesticides and dosages for studies on interactions of pathogens with toxins.

Summary Statement for Goal 1
This goal constitutes our attempts at understanding the most important morbidity factors at work in North American Apis mellifera. Work in this Goal is characterized by a high degree of interinstitutional linkages within CAP labs, resulting in four topical groups. The Nosema group is comprised of Lee Solter (Univ IL), Tom Webster (KY State Univ), Zach Huang (MI State), Christina Grozinger (Penn State), and Kate Aronstein (ARS Weslaco). The virus group is made up of Jay Evans and Judy Chen (ARS Beltsville) and Lee Solter. There have been cross-group linkages with Greg Hunt (Purdue) who is studying the genetic basis of bee resistance to N. ceranae and Israeli Acute Paralysis Virus (IAPV). A diagnostics group is comprised of Jay Evans, Judy Chen, and Kate Aronstein. The toxicology group is comprised of Marion Ellis (Univ NB), Maryann Frazier, Jim Frazier, and Chris Mullin (Penn State). A sentinel apiary monitoring group, led by Frank Drummond (Univ. of Maine), is comprised of Nancy Ostiguy (Penn State), Marla Spivak (Univ. of Minn.), Kate Aronstein (ARS Weslaco), Sheppard (Univ. of Wash.), Kirk Visscher (Univ. of CA - Riverside); analytic work by Anne Averill (Univ. of Mass.), Nancy Ostiguy (Penn State), and Brian Eitzer (CT Experiment Station) is collecting baseline data on field colonies and factors contributing to bee morbidity. And finally, an IPM adoption group is headed up by Keith Delaplane (Univ GA).


Methodology, data and analysis of results to date are shared in an annual report to USDA. Papers generated by team members during the time of the CAP are listed and periodically updated below. Beyond the citation of published papers, the consensus of the group is that it would otherwise be unhelpful or possibly misleading to state preliminary results within the context on this web site.


Publications of objective 1.7 principal investigator (Mullin) to date during the CAP

Ciarlo, T. and C. Mullin. 2011. Pesticide adjuvants and inert ingredients may impair
foraging behavior in honey bees (Apis mellifera). In: American Bee Research
Conference, Galveston, TX. American Bee Journal, 151(4) (Poster Abstract)

Cox-Foster, D. L., M. Frazier, J. Frazier and C. Mullin. 2011. Loss of honey bee colonies: Unraveling the interactions between pathogens and pesticides. In: North American Beekeeping Conference & Tradeshow, Galveston, TX. American Bee Journal, 151(4) (Abstract)

Frazier, J.L., M.T. Frazier, C.A. Mullin and W. Zhu. 2011. Does the reproductive ground
plan hypothesis offer a mechanistic basis for understanding honey bee health? In:
American Bee Research Conference, Galveston, TX. American Bee Journal,

Frazier, J., C. Mullin, M. Frazier, and S. Ashcraft. 2011. Pesticides and their involvement in Colony Collapse Disorder. American Bee Journal, 151(8):779-781.

Johnson, R.M. , M. Ellis, C.A. Mullin , M. Frazier. 2010. Pesticides and honey bee toxicity - USA. Apidologie 41:312–331 DOI: 10.1051/apido/2010018

Johnson, R.M., M.D. Ellis, C.A. Mullin, M. Frazier. (ed. Samataro) Book: ”Honey Bee Colony Health: Challenges and Sustainable solutions” Book chapter 14, Pesticides and Bee Toxicity - U.S.A Taylor and Francis, LLC, (accepted, 2011)

Mullin, C.A., J.L. Frazier, M.T. Frazier and T.J. Ciarlo. 2011. A primer on 'inerts' and honey bees. In: American Bee Research Conference, Galveston, TX. American Bee Journal, 151(4) (Abstract)

vanEngelsdorp,  D., N. Speybroeck, J.D. Evans, B.K. Nguyen, C. Mullin, M. Frazier, J. Frazier, D. Cox-Foster, Y.P. Chen, D.R. Tarpy, E. Haubruge, J.S. Pettis, C. Saegerman. 2010.  Identification of risk factors associated with bee Colony Collapse Disorder by classification and regression tree analysis. J. Econ Entomol, 103: 1517-1523

Further Background Information
Documentation of CAP progress in general, and of this objective in particular, is available through the following sources:

  1. Bee Health, an eXention initiative for peer-reviewed scientific recommendations
  2. Colony Collapse Disorder Progress Report for 2009
  3. When Varroacides Interact
  4. Pesticides Applied to Crops and Honey Bee Toxicity
  5. Wild Bee Status and Evidence for Pathogen 'Spillover' with Honey Bees
  6. Assessing the Risks of Honey Bee Exposure to Pesticides
  7. Pesticides and their involvement in Colony Collapse Disorder

Updated August 19, 2011.