Review of field and monitoring studies investigating the role of nitro-substituted neonicotinoid insecticides in the reported losses of honey bee colonies (Apis mellifera)
Review of field and monitoring studies investigating the role of nitro-substituted neonicotinoid insecticides in the reported losses of honey bee colonies (Apis mellifera)
Richard Schmuck 1
● Gavin Lewis 0 1
0 JSC International Ltd. , Harrogate , UK
1 Bayer CropScience AG , Monheim am Rhein , Germany
The nitro-substituted neonicotinoid insecticides, which include imidacloprid, thiamethoxam and clothianidin, are widely used to control a range of important agricultural pests both by foliar applications and also as seed dressings and by soil application. Since they exhibit systemic properties, exposure of bees may occur as a result of residues present in the nectar and/or pollen of seed- or soiltreated crop plants and so they have been the subject of much debate about whether they cause adverse effects in pollinating insects under field conditions. Due to these perceived concerns, the use of the three neonicotinoids imidacloprid, clothianidin and thiamethoxam has been temporarily suspended in the European Union for seed treatment, soil application and foliar treatment in crops attractive to bees. Monitoring data from a number of countries are available to assess the presence of neonicotinoid residues in honey bee samples and possible impacts at the colony level and these are reviewed here together with a number of field studies which have looked at the impact of clothiandin on honey bees in relation to specific crop use and in particular with oilseed rape. Currently there is considerable uncertainty with regards to the regulatory testing requirements for field studies. Accordingly, a testing protocol was developed to address any acute and chronic risks from oilseed rape seeds containing a coating with 10 g clothianidin and 2 g beta-cyfluthrin per kg seeds (Elado®) for managed honey bee (Apis mellifera) colonies, commercially bred bumble bee (Bombus terrestris) colonies and red mason bees (Osmia bicornis) as a representative solitary bee species. This is described here together with a summary of the results obtained as an introduction to the study details given in the following papers in this issue.
Neonicotinoids ● Risk assessment ● Bee monitoring ● Honey bees ● Bumble bees ● Solitary bees
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The nitro-substituted neonicotinoid insecticides, which
include imidacloprid, thiamethoxam and clothianidin, are an
agronomically very important group of insecticides which
are widely used to control a range of important agricultural
pests both by foliar applications and also as seed dressings
and by soil application. They are agonists of insect nicotinic
acetylcholine receptors (nAChR) and, therefore, often
effectively control pest species which have evolved
resistance to other insecticide classes like acetylcholinesterase
inhibitors (organophosphates, carbamates) and sodium
channel agonists (pyrethroids). Since neonicotinoids show
systemic activity, exposure of bees may occur as a result of
residues present in the nectar and/or pollen of seed- or
soil-treated crop plants or when applied as a spray before
flowering. Due to their high intrinsic toxicity to honey bees,
nitro-substituted neonicotinoid insecticides have been
intensively examined worldwide by regulatory agencies for
their risks posed to honey bees. In Europe, the active
substance clothianidin whose impact to bees were further
investigated as outlined in the following chapters was
included in Annex I to Directive 91/414/EEC on 1 August
2006 by Commission Directive 2006/41/EC.
In spring 2008, a number of bee poisoning incidents
were reported during sowing of seed-treated maize in the
Upper Rhine valley and in parts of Bavaria in Germany
(Pistorius et al. 2009). The reason for the poisoning was the
abrasion of dust from maize seeds treated with the
insecticide Poncho Pro (a.s. clothianidin) and subsequently during
the sowing process with pneumatic sowing machines, the
blowing out of this dust containing the active substance into
the environment. Most probably, forager bees passively
collected these dust particles and returned a mix of dust and
pollen back to their hives. Due to this incident, the specific
provisions of the approval were amended by Commission
Directive 2010/21/EU, to permit use of clothianidin, and
other nitro-substituted neonicotinoids (thiamethoxam
and imidacloprid) as well as the insecticide fipronil
(an antagonist of GABA- and glutamate-gated chloride
channels that is also highly bee-toxic) as seed treatments
only where the seed coating is performed in professional
seed treatment facilities. These must apply the best available
techniques to ensure that the release of dust during
application to the seed, storage and transport can be minimised,
and where adequate drilling equipment is used to ensure a
high degree of incorporation in soil resulting in a
minimisation of dust emission.
In the years following the incident in the Upper Rhine
valley, a large number of scientific investigations were
published with a special emphasis on the sub- (...truncated)