Large-scale monitoring of effects of clothianidin-dressed oilseed rape seeds on pollinating insects in Northern Germany: effects on honey bees (Apis mellifera)

Ecotoxicology, Sep 2016

Possible effects of clothianidin seed-treated oilseed rape on honey bee colonies were investigated in a large-scale monitoring project in Northern Germany, where oilseed rape usually comprises 25–33 % of the arable land. For both reference and test sites, six study locations were selected and eight honey bee hives were placed at each location. At each site, three locations were directly adjacent to oilseed rape fields and three locations were situated 400 m away from the nearest oilseed rape field. Thus, 96 hives were exposed to fully flowering oilseed rape crops. Colony sizes and weights, the amount of honey harvested, and infection with parasites and diseases were monitored between April and September 2014. The percentage of oilseed rape pollen was determined in pollen and honey samples. After oilseed rape flowering, the hives were transferred to an extensive isolated area for post-exposure monitoring. Total numbers of adult bees and brood cells showed seasonal fluctuations, and there were no significant differences between the sites. The honey, which was extracted at the end of the exposure phase, contained 62.0–83.5 % oilseed rape pollen. Varroa destructor infestation was low during most of the course of the study but increased at the end of the study due to flumethrin resistance in the mite populations. In summary, honey bee colonies foraging in clothianidin seed-treated oilseed rape did not show any detrimental symptoms as compared to colonies foraging in clothianidin-free oilseed rape. Development of colony strength, brood success as well as honey yield and pathogen infection were not significantly affected by clothianidin seed-treatment during this study.

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Large-scale monitoring of effects of clothianidin-dressed oilseed rape seeds on pollinating insects in Northern Germany: effects on honey bees (Apis mellifera)

Ecotoxicology Large-scale monitoring of effects of clothianidin-dressed oilseed rape seeds on pollinating insects in Northern Germany: effects on honey bees (Apis mellifera) Daniel Rolke 1 2 ● Stefan Fuchs 1 2 ● Bernd Grünewald 1 2 ● Zhenglei Gao 0 2 ● Wolfgang Blenau 2 0 tier3 solutions GmbH , Leverkusen , Germany 1 Institut für Bienenkunde (Polytechnische Gesellschaft), Goethe University Frankfurt , Oberursel , Germany 2 Current address: Zoological Institute, Cologne Biocenter, University of Cologne , Cologne , Germany Possible effects of clothianidin seed-treated oilseed rape on honey bee colonies were investigated in a large-scale monitoring project in Northern Germany, where oilseed rape usually comprises 25-33 % of the arable land. For both reference and test sites, six study locations were selected and eight honey bee hives were placed at each location. At each site, three locations were directly adjacent to oilseed rape fields and three locations were situated 400 m away from the nearest oilseed rape field. Thus, 96 hives were exposed to fully flowering oilseed rape crops. Colony sizes and weights, the amount of honey harvested, and infection with parasites and diseases were monitored between April and September 2014. The percentage of oilseed rape pollen was determined in pollen and honey samples. After oilseed rape flowering, the hives were transferred to an extensive isolated area for post-exposure monitoring. Total numbers of adult bees and brood cells showed seasonal fluctuations, and there were no significant differences between the sites. The honey, which was extracted at the end of the exposure phase, contained 62.0-83.5 % oilseed rape pollen. Varroa destructor infestation was low during most of the course of the study but increased at the end of the study due to flumethrin resistance in the mite populations. In summary, honey bee colonies foraging in clothianidin seed-treated oilseed rape did not show any detrimental symptoms as compared to colonies foraging in clothianidin-free oilseed rape. Development of colony strength, brood success as well as honey yield and pathogen infection were not significantly affected by clothianidin seed-treatment during this study. Colony development ● Field study ●; Neonicotinoid ● Plant protection product ● Pollinator ●; Seed-treatment - The Western honey bee, Apis mellifera, is economically the most valuable pollinator of crop monocultures worldwide and yields of some fruit, seed and nut crops are estimated to decrease by more than 90 % without these pollinators (Klein et al. 2007). As abundance of wild bees in agricultural fields is often insufficient, managed honey bee hives are indispensable to ensure sufficient crop pollination. Furthermore, the global stock of domesticated honey bees is growing more slowly than agricultural demand for pollination (Aizen and Harder 2009). In recent years, honey bees have suffered from high colony mortality, including colony collapse disorder, overwinter or seasonal colony losses (vanEngelsdorp et al. 2008; Neumann and Carreck 2010; Smith et al. 2013). Honey bee colonies are exposed to multiple and varying stressors (Potts et al. 2010) including habitat loss, malnutrition, parasites and pathogens, and plant protection products (PPPs). In particular, systemically acting PPPs of the neonicotinoid class of compounds are often held responsible for honey bee colony losses (Sánchez-Bayo 2014; Goulson et al. 2015; Pisa et al. 2015). Like the botanical insecticide nicotine, neonicotinoids act as agonists at nicotinic acetylcholine receptors in the insect central nervous system (for reviews, see, Tomizawa and Casida 2005; Jeschke et al. 2013). Neuroactive neonicotinoids are commonly used as seed dressings in a variety of crops including oilseed rape (OSR) and are taken up systemically by the growing plant and distributed to all tissues (Elbert et al. 2008). The systemic activity of neonicotinoids makes them effective as a seed dressing, providing protection to crops in their more vulnerable early stages of growth. This reduces the number of foliar insecticide applications required, which are often applied at much higher application rates and generally result in an increased exposure of nontarget organisms (Cutler et al. 2014; Pisa et al. 2015). Due to the concerns about the impact of neonicotinoids on honey bees and other pollinators, the use of the three neonicotinoids imidacloprid, clothianidin, and thiamethoxam has been temporarily suspended in the European Union as seed treatment, soil application, and foliar treatment in crops attractive to bees (European Commission 2013). Various laboratory and semi-field studies that link poor overall condition of bee colonies to widespread use of neonicotinoid PPPs have been criticized (Cresswell and Thompson 2012; Guez 2012; Carreck and Ratnieks 2014; Godfray et al. 2014) for not using field realistic doses or for subjecting bees in the laboratory exclusively to food spiked with (...truncated)


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Daniel Rolke, Stefan Fuchs, Bernd Grünewald, Zhenglei Gao, Wolfgang Blenau. Large-scale monitoring of effects of clothianidin-dressed oilseed rape seeds on pollinating insects in Northern Germany: effects on honey bees (Apis mellifera), Ecotoxicology, 2016, pp. 1648-1665, Volume 25, Issue 9, DOI: 10.1007/s10646-016-1725-8