Field-Level Sublethal Effects of Approved Bee Hive Chemicals on Honey Bees (Apis mellifera L)

Jennifer A Berry,Stéphane Pietravalle,W Michael Hood,Keith S Delaplane,Guy Smagghe

doi:10.1371/journal.pone.0076536

Jennifer A Berry, Stéphane Pietravalle + Show 3 more

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https://doi.org/10.1371/journal.pone.0076536

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Abstract

In a study replicated across two states and two years, we tested the sublethal effects on honey bees of the miticides Apistan (tau fluvalinate) and Check Mite+ (coumaphos) and the wood preservative copper naphthenate applied at label rates in field conditions. A continuous covariate, a colony Varroa mite index, helped us disambiguate the effects of the chemicals on bees while adjusting for a presumed benefit of controlling mites. Mite levels in colonies treated with Apistan or Check Mite+ were not different from levels in non-treated controls. Experimental chemicals significantly decreased 3-day brood survivorship and increased construction of queen supercedure cells compared to non-treated controls. Bees exposed to Check Mite+ as immatures had higher legacy mortality as adults relative to non-treated controls, whereas bees exposed to Apistan had improved legacy mortality relative to non-treated controls. Relative to non-treated controls, Check Mite+ increased adult emergence weight. Although there was a treatment effect on a test of associative learning, it was not possible to statistically separate the treatment means, but bees treated with Apistan performed comparatively well. And finally, there were no detected effects of bee hive chemical on colony bee population, amount of brood, amount of honey, foraging rate, time required for marked released bees to return to their nest, percentage of released bees that return to the nest, and colony Nosema spore loads. To our knowledge, this is the first study to examine sublethal effects of bee hive chemicals applied at label rates under field conditions while disambiguating the results from mite control benefits realized from the chemicals. Given the poor performance of the miticides at reducing mites and their inconsistent effects on the host, these results defend the use of bee health management practices that minimize use of exotic hive chemicals.

Highlights

The parasitic honey bee mite, Varroa destructor Anderson and Trueman has been responsible for transitioning beekeeping from one of the world’s most chemical-averse agricultural industries to one of its most chemical-dependent
In this paper we report a two-year (2008, 2009) study replicated across two states (Georgia, South Carolina) looking for sublethal effects on bees at labeled rates of compounds registered for use by beekeepers in the United States: the synthetic acaricides taufluvalinate (ApistanTM) and coumaphos (Check Mite+TM) used to control Varroa mites and, in Georgia only, copper naphthenate (JascoTM) used to protect wooden hive parts from termites and decay fungi
Each colony was randomly selected to receive one of the following treatments at labeled rates: (1) two strips of Apistan inserted one between frames 3 and 4 and one between frames 5 and 6 for 42 days, (2) two strips of Check Mite+ inserted one between frames 3 and 4 and one between frames 5 and 6 for 42 days or (3) no treatment, and in Georgia only (4) a 37.5645.760.3-cm sheet of wood laminate board impregnated with 2% copper naphthenate solution and placed on the hive floor for 42 days to simulate bee exposure to treated woodenware

Summary

Introduction

The parasitic honey bee mite, Varroa destructor Anderson and Trueman has been responsible for transitioning beekeeping from one of the world’s most chemical-averse agricultural industries to one of its most chemical-dependent. It is generally believed that Varroa-related losses would be unacceptably high without these inputs. These products have low acute toxicity (high LD50s) to honey bees, there is growing evidence that they are not entirely benign. Haarmann et al [3] showed that queens have reduced body weight if reared in the presence of elevated levels of fluvalinate. Coumaphos has been shown to alter honey bee gene expression for detoxification pathways and may down-regulate gene products associated with cellular or humoral immunity [6]. There is evidence that acaricides alter physiological functions, immune responses, and detoxification functions in the host bees rendering them more susceptible to pathogens and pesticides []. The active ingredients fluvalinate and coumaphos have been shown to synergize in the company of each other, elevating the honey bee toxicity of each to potentially injurious levels [8,9]

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