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2016 ; 11
(6
): e0156886
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Honeybees Produce Millimolar Concentrations of Non-Neuronal Acetylcholine for
Breeding: Possible Adverse Effects of Neonicotinoids
#MMPMID27285384
Wessler I
; Gärtner HA
; Michel-Schmidt R
; Brochhausen C
; Schmitz L
; Anspach L
; Grünewald B
; Kirkpatrick CJ
PLoS One
2016[]; 11
(6
): e0156886
PMID27285384
show ga
The worldwide use of neonicotinoid pesticides has caused concern on account of
their involvement in the decline of bee populations, which are key pollinators in
most ecosystems. Here we describe a role of non-neuronal acetylcholine (ACh) for
breeding of Apis mellifera carnica and a so far unknown effect of neonicotinoids
on non-target insects. Royal jelly or larval food are produced by the
hypopharyngeal gland of nursing bees and contain unusually high ACh
concentrations (4-8 mM). ACh is extremely well conserved in royal jelly or brood
food because of the acidic pH of 4.0. This condition protects ACh from
degradation thus ensuring delivery of intact ACh to larvae. Raising the pH to
?5.5 and applying cholinesterase reduced the content of ACh substantially (by
75-90%) in larval food. When this manipulated brood was tested in artificial
larval breeding experiments, the survival rate was higher with food supplemented
by 100% with ACh (6 mM) than with food not supplemented with ACh. ACh release
from the hypopharyngeal gland and its content in brood food declined by 80%, when
honeybee colonies were exposed for 4 weeks to high concentrations of the
neonicotinoids clothianidin (100 parts per billion [ppb]) or thiacloprid (8,800
ppb). Under these conditions the secretory cells of the gland were markedly
damaged and brood development was severely compromised. Even field-relevant low
concentrations of thiacloprid (200 ppb) or clothianidin (1 and 10 ppb) reduced
ACh level in the brood food and showed initial adverse effects on brood
development. Our findings indicate a hitherto unknown target of neonicotinoids to
induce adverse effects on non-neuronal ACh which should be considered when
re-assessing the environmental risks of these compounds. To our knowledge this is
a new biological mechanism, and we suggest that, in addition to their well
documented neurotoxic effects, neonicotinoids may contribute to honeybee colony
losses consecutive to a reduction of the ACh content in the brood food.