POLLINATORS POLLINATION AND FOOD PRODUCTION

THE ASSESSMENT REPORT ON POLLINATORS, POLLINATION AND FOOD PRODUCTION
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2. DRIVERS OF CHANGE OF POLLINATORS,
POLLINATION NETWORKS AND POLLINATION
2.3.1.4 Sublethal effects of pesticides on
bees
2.3.1.4.1 Importance of sublethal effects
In addition to the traditional measurements of lethal
effects happening during acute exposure to pesticides,
an increasing number of studies have focused on the
sublethal effects of pesticides on pollinators, since the
1970’s. Sublethal effects are defined as the effects on
individuals that survive exposure (Desneux et al., 2007).
They mainly follow chronic exposure to pesticides, but can
also be a consequence of acute exposure. A pioneering
study by Schricker and Stephen (1970) showed that when
honey bees were exposed to a sublethal dose of parathion,
an organophosphate insecticide, they were unable to
communicate the direction of a food source to other bees.
Using a variety of methods, many studies have shown
the effects of newer classes of insecticides, for instance
pyrethroids (Vandame et al., 1995) and neonicotinoids (Henry
et al., 2012), causing alterations in the navigation of bees
and their orientation to food resources and colony location,
resulting in bee losses. After reviewing the documented
sublethal effects of pesticides on bees, we examine the
Class
Acetylcholinesterase
(AChE) inhibitors
GABA-gated
chloride channel
antagonists
Sodium channel
modulators
Nicotinic
acetylcholine
receptor (nAChR)
agonists
Nicotinic
acetylcholine
receptor (nAChR)
allosteric modulators
Chloride channel
activators
Modulators of
chlordotonal organs
Examples (chemical
subgroup or exemplifying
active ingredient
Organophosphates,
carbamates
Cyclodiene
organochlorines;
phenylpyrazoles
Pyrethroids, pyrethrins;
DDT/methoxychlor
Neonicotinoids; nicotine;
sulfoxaflor; butenolides
Spinosyns
Avermectins, milbemectins
Pymetrozine; flonicamid
Mode of action
Inhibits enzyme which terminates the
action of the excitatory neurotransmitter
acetylcholine at nerve synapses.
Acetylcholine is the major excitatory
neurotransmitter in insects.
Blocks GABA-activated chloride
channel; GABA is the major inhibitory
neurotransmitter in insects
Keep sodium channels open causing
hyperexcitation and in some cases nerve
block. Sodium channels are involved in
the propagation of action potentials along
nerve axons.
Mimic the agonist action of acetylcholine
at nAChR causing hyperexcitation.
Acetylcholine is the major excitatory
neurotransmitter in insects.
Allosterically activate nAChRs causing
hyperexcitation. Acetylcholine is the major
excitatory neurotransmitter in insects.
Allosterically activate glutamate-gated
chloride channels causing paralysis.
Glutamate is an important inhibitory
neurotransmitter in insects
conclusions of the principal reviews on this topic with respect
to the role of sublethal effects of these pesticides in the
decline of bees, and the pollination they provide.
2.3.1.4.2 Range of sublethal effects
An extensive variety of sublethal effects has been
studied, and can be classified into effects at the individual
(physiological and behavioral) and colony levels. We provide
several examples of each detected effect, based on the
principal reviews (Thompson, 2003; Desneux et al., 2007;
Belzunces et al., 2012; Van der Sluijs et al., 2013; Godfray
et al., 2014; Pisa et al., 2014) (see Table 2.3.3).
As shown in Table 2.3.3, there exist a broad variety of
sublethal effects, including individual physiological and
behavioral effects as well as colony-level effects. Most of
these effects have been shown with the honey bee, and
most of the recent studies look at neonicotinoid insecticides
effects. Despite this research, important gaps of knowledge
remain; for example: 1) most studies have been carried
out with honey bees, a few with the bumble bee, Bombus
terrestris, but very few with other social or solitary bee
species (Sandrock et al., 2014) (Table 2.3.3, Figure 2.3.6).
TABLE 2.3.2
Examples of classes. Mode of action and toxicity of insecticides acting on nerve/muscle targets (from IRAC MoA Classification
v7.3 February 2014 http://www.irac-online.org/documents/moa-classification/?ext=pdf)
Stimulate chlordotonal proprioceptors
by an unknown mechanism; impairs fine
motor control, resulting in disruption
of feeding and other behaviours of
Hemiptera and certain other insects
application rate
+ 10’s g ai/ha
++ 100’s of g ai/ha
Example honeybee
LD50 µg a.i. (active
ingredient)/bee*
++ Dimethoate 0.1
+ Fipronil 0.004
(oral lowest)
+ Deltamethrin 0.0015
(contact lowest)
+ Thiacloprid 17.3
(oral lowest)
Imidacloprid 0.0037
(oral lowest)
+ Spinosad 0.0036
(contact lowest)
+ Abamectin 0.002
(contact)
+ Pymetrozine >117
(oral lowest)
* toxicity data from http://www.agritox.anses.fr/php/fiches.php