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
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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)