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Neonicotinoids and pollinators
Prof. Dr Jeroen P. van der Sluijs @Jeroen_vdSluijsUniversity of
Bergen & Utrecht University
Numbers for Policy, Castelldefels, 31 Aug 2018
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The trend of world wide pollinator loss is a major threat to
biodiversity
Causes include: new pesticides, land use change and climate
change
European Research project ALARM:
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http://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0185809&type=printable
http://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0185809&type=printable
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“The impact on wildlife of changes in farming practice (and the
expansion of the farmed area) is so rapid and severe that it is
hard to get your head round the scale of what is happening. A study
published this week in the journal Plos One reveals that flying
insects surveyed on nature reserves in Germany have declined by 76%
in 27 years. The most likely cause of this Insectageddon is that
the land surrounding those reserves has become hostile to them: the
volume of pesticides and the destruction of habitat have turned
farmland into a wildlife desert.”
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The importance of pollinators• 90 major crops (35% world food
production volume)
depend on pollinators• Key nutrients: 90-100% from pollinator
mediated crops (vit
C, antioxidants, lycopene, β-tocopherol, vit A and folic acid)•
Value in Europe: 14.2 billion Euro / yr• 87% of all flowering
plants on earth depends on 25000 bee
species for reproduction and evolution
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World wide: 25000 bee speciesIn NL about 350 bee species, 181 of
them are on the Red List / at risk of extinction
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2011
2011
20062013
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Mean winter losses of bee hives 2009-10 Europe, Turkey &
Israel (Van der Zee e.a., 2012;
Coloss)http://dx.doi.org/10.3896/IBRA.1.51.1.12
http://dx.doi.org/10.3896/IBRA.1.51.1.12
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The work of the honeybee
• Colony 10,000 to 80,000 bees• Empty honeybee 80 to 100 mg•
Maximum “freight”: 70 mg/honeybee.• Water “freight” up to 40
microliter per bee• One colony visits 21 million flowers / day• 700
flowers visited per honeybee per day • 1 liter nectar requires
20,000 to 100,000 flights• Worker honeybee lives ca. 20 - 42 days,
winterbees
170 days and more.
Modified from:
http://www.unaf-apiculture.info/presse/DOSSIER_DE_PRESSE_2009_L_ABEILLE_SENTINELLE_DE_L_ENVIRONNEMENT.pdf
http://www.unaf-apiculture.info/presse/DOSSIER_DE_PRESSE_2009_L_ABEILLE_SENTINELLE_DE_L_ENVIRONNEMENT.pdf
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New pollinator emerging in China
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Pollinator decline: interaction of mutually reinforcing
causes
PPPP• Pollen• Pathogens• Pesticides• Places (for nesting)
monoculture
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Professor Shinzo Kagabu received the 2010 American Chemical
Society International Award for Research in Agrochemicals in
recognition of his discovery of imidacloprid (IMI) and thiacloprid,
which opened the neonicotinoid era of systemic pest management.
(Tomizawa & Casida, 2010, DOI:10.1021/jf103856c)
Systemic insecticides: revolution in plant protection
Systemic = crop takes it up into its plantsap:chemical makes
plant toxic from inside
http://dx.doi.org/10.1021/jf103856c
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1962
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Imidacloprid + Thiamethoxam+ Clothianidin in EU:>200
products>1000 allowed applications
Nicotine
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http://www.bijensterfte.nl/sites/default/files/Neonicotinoid_e.pdf
http://www.bijensterfte.nl/sites/default/files/Neonicotinoid_e.pdf
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Toxicity of neonicotinoidsPesticide ® Use LD50 (ng/honeybee)
Toxicity indexrelative to DDT
DDT Dinocide insecticide 27000 1
Amitraz Apivar insecticide / acaricide 12000 2
Coumaphos Perizin insecticide / acaricide 3000 9
Tau-fluvalinate Apistan insecticide / acaricide 2000 13.5
Methiocarb Mesurol insecticide 230 117
Carbofuran Curater insecticide 160 169
λ-cyhalothrin Karate insecticide 38 711
Deltamethrine Decis insecticide 10 2700
Thiamethoxam Cruise insecticide 5 5400
Fipronil Regent Insecticide 4.2 6475
Clothianidine Poncho Insecticide 4.0 6750
Imidacloprid Gaucho Insecticide 3.7 7297Toxicity of insecticides
to honeybees compared to DDT. The final column expresses the
toxicity relative to DDT. (Source: Bonmatin, 2009)
http://www.bijensterfte.nl/images/Bonmatin-conclusions-sentinelle-gb-2009.pdf
http://www.bijensterfte.nl/images/Bonmatin-conclusions-sentinelle-gb-2009.pdf
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Systemic insecticides• Systemic: Contamination of nectar and
pollen• Very high toxicity for honeybees• A long persistence in
soils (t½ = 9 months) and
water (160 days)• Main metabolites as toxic as imidacloprid for
bees• Acute effects (overdosing, sowing…)• Subletal effects and
chronic exposure• Risks in fields : PEC/PNEC >> 1• Synergies
with other pesticides• Synergies with other pathogens (Nosema,
Wing
Deform Virus)• Major weakening factor of bee colonies
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Imidacloprid 2010World production:20,000 tonnes
(DDT peak-use 80,000 tonnes in 1959)
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Spray uses in Europe (70%)
Uses: spray, seed treatment, other
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Seed treatment uses in Europe (20%)
Other uses in Europe
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Since 2004,Netherlandssurfacewater is heavilypolluted
withImidacloprid
www.bestrijdingsmiddelenatlas.nl
Only 1.6 to 20% of applied neonicotinoid is absorbed by the
growing crop (Sur & Stork 2003)80 to 98.4% leaches to soil
& water!
http://www.bestrijdingsmiddelenatlas.nl/
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Effects on honeybees• Acute intoxication• Chronic intoxication•
Sublethal effects• Synergy effects
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Corn coated with Gaucho® (imidacloprid)
75 gram imidacloprid / ha corn100000 seeds / ha
0.00075 gram imidacloprid / seed
3.7 nanogram = LD50 Honeybees
202702 LD50 / corn seed
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Pomurje, Slovenia April 2011, sowing period clothianidin
corn
Damage2500 colonies lost
> 100 million bees
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Field test in PaduaDeadly dust cloud< 30 seconds 10m away:300
to 4000 ng imidaclopridper bee
http://www.bijensterfte.nl/en/node/507
http://www.bijensterfte.nl/en/node/507
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What are exposure pathways?• Treated crops
– Contact– Pollen (delayed consumption!, Bee bread etc.)– Nectar
(delayed consumption!, honey)– Extrafloral nectar– Honey-dew (from
aphids)– Guttation (plant sap excreted by the plant)– Dew/rain
(waterdrops from the atmosphere)– Sweet remains of e.g. sugarbeets,
etc.
• Systemic uptake by untreated wild plants and trees on same
soil• Systemic uptake of contaminated water by wild plants and
trees• Spray drift / dust drift to flowering fields• Direct contact
with dust (flying through the dust cloud)• Foraging on polluted
surface water (for drinking and COOLING!)• Residues in sugar used
for sugar syrup supplementary feeding• Residues in water used by
beekeepers to make sugar syrup (violation
of drinkingwater norm in NL > 100 ng/liter)• Can it travel
trough the air? On PM2.5? On diessel soot/black carbon?
On airosol-water?• Brabant, NL scandal 2011: Waste-sand from
treated Lilly bulbs used for
trails in protected nature area • Etc……..
Example: bees collect honeydew excreted by aphids
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Krupke e.a. 2012 study
Krupke e.a. 2012. Multiple Routes of Pesticide Exposure for
Honey Bees Living Near Agricultural Fields.
http://dx.doi.org/10.1371/journal.pone.0029268
http://dx.doi.org/10.1371/journal.pone.0029268
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Do trees translocate imidacloprid from surface water into pollen
& nectar?In NL we took samples from willow trees (Salix) in
polluted areas
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T. Seeley, The wisdom of the hiveChapter 9 regulation of water
collection
Exposurevia guttation?
Via waterfor drinkingand cooling?
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Chronic toxicity imidaclopridfor bumblebeesMicro colonies fed
with imidacloprid at • 200 ppm 100% mortality few hours• 20 ppm
100% mortality 14 days• 2 ppm 100% mortality 28 days• 0.2 ppm 100%
mortality 49 days, • 20 ppb 15% mortality (77 days)• 10 ppb 0%
mortality (77 days)NOEC reproduction
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Relationship between neonicotinoid concentration and time to 50%
effect (ET50) in the organisms exposed follows a hyperbolic curve
asymptotic on the y axis; in reality, this asymptote is determined
by the no-effect concentration (NEC), while the upper limit of the
curve is determined by the life span of the organism.
(Sanchez-Bayo, 2009)http://dx.doi.org/10.1080/03601230701229239
http://dx.doi.org/10.1080/03601230701229239
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Sublethal effects• Foraging behaviour / navigation• Task
differentiation in the hive• Grooming• Immune system• Brood• Larval
development• etc/.
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A: familiar location; B random location
http://dx.doi.org/10.1126/science.1215039
Dose per bee: 1.34 ng thiamethoxam in 20-μl sucrose solution
Henry ea. 2012Sciencestudie
Radio IDchips
http://dx.doi.org/10.1126/science.1215039
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Radar-tracking experiment Randolf Menzel:Bees exposed to
neonicotinoids loose orientation
Fischer J, Müller T, Spatz A-K, Greggers U, et al. (2014)
Neonicotinoids Interfere with Specific Components of Navigation in
Honeybees. PLoS ONE 9(3): e91364.
doi:10.1371/journal.pone.0091364http://www.plosone.org/article/info:doi/10.1371/journal.pone.0091364
Yellow-RedThiacloprid-bees
Green-BlueControl bees
http://www.plosone.org/article/info:doi/10.1371/journal.pone.0091364
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Using video-tracking to assess sublethal effects of pesticides
on honey bees
• Bees exposed to 0.05, 0.5, 5.0, 50, and 500 ppb imidacloprid
in a sugar agar cube
• significant reduction in distance moved at 50 and 500 ppb
imidacloprid (p
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Science, 29 Mar 2012
http://dx.doi.org/10.1126/science.1215025
http://dx.doi.org/10.1126/science.1215025
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http://dx.doi.org/10.1021/es405331c
Charpentier ea, 2014
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Lu e.a. 2012 Harvard University- 5 Apr 2012In situ replication
of honey bee
colony collapse disorder
http://goo.gl/1a0Aa
http://goo.gl/1a0Aa
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Yamada 2012 D= clothianidin 10, 50, 100x dilutedS= dinotefuran
10, 50, 100x dilutedCompered to recommended field rate
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Required dose of neonicotinoid per bee till colony
extinction
(Yamada, 2013)
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Problems with field studies• Some field studies have n=1
(Schmuck 2001)• Statistical power:
– 75 hives needed to detect 35% drop in colony performance–
>2000 hives to detect 5% drop in colony performance
• Many flaws in experimental set-up of field studies used for
authorization. Transport of nectar & pollen ≠ exposure!
• Many field studies turned out to have a hidden sponsor: Bayer
Cropscience – Flawed-by-design!
• Example: Cutler and Dupree 2007 study• In authorization
protocols field studies (even flawed
ones and n=1 ones) get more weight than lab studies, but from a
scientific point of view lab studies are more reliable!
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(bron: Robert Luttik, 2013)
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Plurality and uncertainty in risk assessment: lessons
learned
• Diversity of the knowledge base: – It must be based on the
full spectrum of available scientific
knowledge;• Robustness of the knowledge claims
– Include uncertainty, dissent and criticism in the analysis,
synthesis and assessments;
• Make thorough Knowledge Quality Assessment the key task in the
science policy interface and develop a joint language to
communicate limitations to our knowledge and understanding clearly
and transparently
• Make use of information of non-scientific sources (local
knowledge)– But scrutinize this information and be clear on its
status;
• Clarify values, stakes and vested interests that play a role
in research and in the political and socioeconomic context within
which the research is embedded.
(Maxim and van der Sluijs, 2007, 2012)
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If time allows…
A few more concerns …
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ECOSYSTEM FUNCTIONING
Impacts cascade through the ecosystem weakening its
stability
• Persistence & solubility led to large scale contamination
of:
• soils and sediments• ground and surface water• treated and
non-treated vegetation
• Multiple routes chronic & acute exposure non-target
species
• Toxicity increased by the duration of exposure• Effects lethal
& sublethal: behaviour, immune
suppression, reproduction• Levels resulting from authorized uses
frequently
exceed ‘lowest observed adverse effect concentrations’ for wide
range of non-target species.
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250000
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0 50000 100000 150000 200000 250000 300000
Series1
• Species abundance data: 7381 locations (left) • Imidacloprid
database: 801 locations (right)• Years 1998, 2003-2009 pooled•
18898 points with IMI data within 1 km radius & < 160 days•
4009 species from 92 orders included
250000
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0 50000 100000 150000 200000 250000 300000
Series1
Macro-invertebrate decline in Dutch surface waters polluted with
imidacloprid
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