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Sublethal effects of nicotinyl insecticides on bees


Posted 31 July 08

Dear friends

This is an important new development. The Sierra Club is the oldest and most influential and main stream environmental group in the United States.
They have put together a compelling case for suspending the approvals for neonicotinoids until the safety for honey bees has been reassessed.
While their letter is addressed to the US-EPA, the scientific evidence presented should be helpful to all of us, as we are making our case at the EU and the member state level.

Kind regards,

Wtitleer Haefeker


From Sierra Club
July 30, 2008

Anthony Britten
Registration Division Director
Office of Pesticide Programs
U.S. Environmental Protection Agency
Ariel Rios Building
1200 Pennsylvania Avenue, N.W., Mail code 7505P
Washington, D.C. 20460

Re: Request to suspend use of nicotinyl insecticides until EPA obtains scientific evidence that sublethal effects do not cause harm to America's honey bees.

Dear Mr. Britten:

The Sierra Club and its 1.3 million members and supporters is requesting that EPA's Office of Pesticide Programs (OPP) take urgent action to suspend use of the high volume pesticides known as the nicotinyl insecticides until the EPA possesses the scientific evidence to demonstrate that these pesticides do not cause or contribute to sublethal effects on the nation's honey bees. Serious questions need to be raised by EPA's OPP over the sublethal effects to honey bees occurring in the low parts per billion range (ppb) of 1.0 ppb to 20 ppb from these pesticides, which apparently the EPA has not evaluated to date, and the pesticide manufacturer's may not have adequately investigated or may have submitted incomplete findings to EPA. Synergistic effects may also be occurring. The EPA has clearly missed the unintended consequences of the nicotinyl (neonicotinoid) insecticides, including imidacloprid, thiamethoxam, clothianidin, and several others and now action is critical.

Without prompt EPA regulatory action to suspend use of the nicotinyl pesticides (also known as neonicotinoids), the mounting economic devastation to the nation's commercial honey bee operations and agriculture will reach into billions of dollars and will irreversibly harm beekeepers and farmers beyond their ability to make a recovery not to mention the huge losses in the fruits and vegetables available for consumers. The EPA's OPP surely is cognizant that federal agencies in France and Germany have already taken responsible regulatory actions to suspend use of these pesticides based on the best available scientific evidence since at least 2002-3. Preliminary evidence was available earlier in France, but EPA's OPP is moving too slowly to take action to suspend nicotinyl pesticides.

The public is seriously concerned that the EPA lacks the necessary scientific evidence to demonstrate the safety of sublethal doses of the neonicontinoids that honey bees are being routinely exposed to during their foraging activities in the US. Your Office of Pesticide Programs is charged with properly implementing the Federal Insecticide, Fungicide, and Rodenticide Act (FIFRA) for legal authorization to allow various pesticide applications and it appears that EPA's OPP is not diligently carrying out its duties under FIFRA to the public and agriculture. More than one hundred and sixty Section 18 FIFRA emergency exemptions have been approved by EPA's OPP since 1997 without evaluating sublethal effects.

As EPA knows, additional large losses of honey bee colonies continue to be widely reported by beekeepers in the United States into 2008 in approximately forty agricultural producing states where fruit and vegetable crops rely on honey bees for pollination and major crop production. Fruit and vegetable losses have been reported by American farmers as a growing agricultural crisis because honey bee colonies have been collapsing in those regions.

EPA's OPP has either inadequately evaluated or totally failed to evaluate the risks from sublethal effects due to low ppb range exposures of the neonicotinoids on honey bees. Following is information primarily from Germany and France where federal agencies have taken responsible regulatory actions to suspend use of neonicontinoids due to the growing scientific evidence of sublethal effects on honey bees. The EPA should be acting responsibly to collect as much scientific evidence as possible considering that the information is publicly available from scientists in Germany and France who have already conducted the research and collected the evidence to warrant suspending neonicotinoids.

As EPA's OPP is aware, the German federal government Office for Consumer Protection and Food Safety (BVL) ordered the immediate suspension of the approval for eight seed treatment products due to the mass death of bees in Germany's Baden-Wuerttemberg state. The suspended pesticide products are mainly neonicotinoids:

According to the German Research Centre for Cultivated Plants, they reported that 29 out of 30 dead bees it had examined had been killed by contact with the neonicotinoid clothianidin. Wild bees and other insects are also suffering from a significant loss of population. In communications with German beekeepers, Manfred Hederer, president of the German Professional Beekeeper's Association reported that 50 to 60 percent of the bees have died on average, and some beekeepers have lost all their hives. Beekeepers and agricultural officials in Italy, France and Holland all noticed similar phenomena in their fields when planting began in April and May.

In France most applications of imidacloprid were already banned in 1999. In 2003 the federal government science committee called Comit' Scientifique et Technique, convened by the French government, declared that the treatment of seeds with the neonicotinoid imidacloprid produces a significant risk for bees. Only a few months ago Bayer's application for the pesticide clothianidin was rejected by French authorities. French research teams have published scientific evidence that they identified several of these neonicotinoid pesticides in low parts per billion concentrations throughout the plant tissues and organs well beyond the root system, and they also identified the same pesticides in the honey bees which forage on the same crop species. By applying a sophisticated analytical technique using High Performance Liquid Chromatography (HPLC) coupled to tandem Mass Spectrometry (atmospheric pressure chemical ionization-mass spectrometry or APCI-MS/MS), French scientists were able to precisely measure low amounts of imidacloprid in the soils, plants (leaves and flowers), and pollens. Extraction, separation, and detection were performed according to quality assurance criteria.

It's obvious that EPA-OPP should be quite concerned with the fact that neonicotinoid compounds share specific characteristics under the following categories that combine to increase their sublethal effects in honey bees and EPA-OPP has failed to perform a comprehensive evaluation of these combined characteristics that have been devastating American honey bee colonies in recent years:

1. These neonicotinoid substances and their metabolites are systemic pesticides. Systemic neonicotinoid treatments, which target the entire plant, are probably contaminating all its parts (French team reported average levels 5-6 ppb), including the flower (reported average levels 5-6 ppb) through translocation from the root system and seeds (Bonmatin et al., 2003 and 2005). Corn had a reported tassel average of 4 ppb and the ear averaged 10 ppb. Sunflower and corn pollen contained about 5 ppb imidacloprid after pesticide treatment. Additional French scientists observed imidacloprid in even higher levels in young fast-growing plants where they measured 10-20 ppb in upper leaves, reaching 100-200 ppb in other leaves, 2-3 ppb in pollen, and less than 1.5 ppb in the nectar. It is confirmed today by repeated laboratory analyses, and the pesticide manufacturer's no longer deny it, that the specific active substances are present in the nectar and the pollen of plants coming from neonicotinoid treated seeds and residues in the soils. Besides, this fact is not ignored in the research on imidacloprid and fipronil. These substances are thus found in the food of bees and their brood. See two studies by Bonmatin et al., 2003 and 2005, and two studies by Chauzat et al., 2002 and 2006.

Entomologist Dr. Maryann Frazier's June 26, 2008 testimony at a Congressional hearing on honey bee colony losses stated: "We are becoming increasingly concerned that pesticides may affect bees at sublethal levels, not killing them outright, but rather impairing their behaviours and their abilities to fight off infections." Pesticides and metabolites are being identified in pollen she added, a disturbing finding! In fact, she testified that 46 different pesticides including six of their metabolites were identified out of 108 pollen samples analyzed. Up to 17 different pesticides were found in a single sample. Samples contained an average of 5 different pesticide residues each. One of the most striking points in Dr. Frazier's testimony is that 97.2% of pollen samples had pesticides and only three (2.8%) of the 108 pollen samples had no detectable pesticides [perhaps using a lower detection limit may have found pesticides at lower trace concentrations]. In 88 wax samples analyzed, 20 different pesticides including two of their metabolites were identified. As identified in pollen, the most commonly detected pesticides were fluvalinate, coumaphos, chlorpyrifos, and the fungicide chlorthalonil, with fluvalinate and coumaphos detected in 100% of the samples. Extraordinary levels of fluvalinate were measured up to 204 parts per million in the brood nest wax and pollen.

2. These neonicotinoid substances and metabolites are neurotoxic to insects including honey bees in low concentrations in the low parts per billion range. The neonicotinoid substances are powerful insecticides that irreversibly block the receptor sites for acetylcholine and neurotransmission in the adult insect or in the larval stage (J. Pest. Reform, 2001). In very small doses (approximately one part per billion - ppb) these compounds are able, without killing the insect, to cause behavioural disturbances (e.g. orientation errors) that could be deadly for the colony, whose survival relies on the integrity of the ability of its members. EPA knows that neonicotinoids are a new class of insecticides since 1992 that specifically act on the central nervous system of insects  (J. Pest. Reform, 2001).

One of imidacloprid's breakdown products, called the Olefine metabolite, is particularly troubling since it is known to be more toxic to insects than imidacloprid itself, according to a 1996 study (Rouchaud et al.). French researchers measured imidacloprid's metabolites in addition to imidacloprid in 69% of the pollen in concentrations as low as 1.1 ppb to 5.7 ppb. A serious concern is that imidacloprid's metabolites have powerful sublethal effects on honey bees and may act in combination with imidacloprid to induce additive toxic effects. However, EPA has failed to consider effects of such metabolites.

3. These neonicotinoid substances and metabolites have greater neurotoxic effects on honey bees due to genomic vulnerability. Research on mapping the honey bee genome discovered that its nicotinic acetylcholine receptor possesses eleven vulnerable subunit members in its nervous system (Jones et al., 2006). The honey bee possesses more nicotinic acetylcholine receptors than either the mosquito or the fruit fly, research has found. In short, the problem for honey bees is they possess more vulnerable acetylcholine receptors to be blocked by pesticides like imidacloprid compared to other insects, and from a theoretical perspective, the honey bee is made more sensitive to pesticides like imidacloprid and similar neurotoxins.

French scientists led by Dr. Marc Colin (Institut National de la Recherche Agronomique, INRA) in 1998 videotaped one set of their experiments on bees exposed to low ppb concentrations of imidacloprid to demonstrate that the honey bees became too groggy and intoxicated effectively impairing their short-term memory in smell and theoretically blocking normal foraging behaviour. After only a few days, the honey bees exposed to low ppb levels of imidacloprid stopped feeding and their numbers sharply dropped compared to the control groups. Dr. Colin compared videotapes of exposed bees and unaffected control bees to dramatically demonstrate the powerful sublethal effects of imidacloprid. If the bees stopped their feeding behaviour, they will quickly die.

4. These neonicotinoid substances are persistent in the environment. Evidence confirms the environmental persistence of imidacloprid and fipronil as well as for some of their metabolites. The same applies to clothianidin and thiamethoxam. Persistence was expected since the stability of these compounds is necessary for the systemic action supposed to last for the entire growing period of the plant over several months. An imidacloprid fact sheet (J. Pest. Reform, 2001) cited 1993 EPA information on a field test showing the concentration of this insecticide did not decrease for a year following treatment. As the pesticides are widely used and may be used on all cereals, maize, sugar beets, potatoes (as spray), as well as on beetroot, oilseed rapes or sunflower, for several consecutive years and in a systematic rotation, it is necessary to study the behavior of the substances in the soil after several successive years of treatment, and the possible contamination of untreated flowering crops that have been grown in a soil being treated for several consecutive years.

5. These neonicotinoid substances and metabolites may act synergistically with fungicides in complex combinations. Research at a North Carolina University laboratory found certain neonicotinoids when combined with specific fungicides acted synergistically to increase the toxicity to honey bees over 1,000 times (Iwasa et al., 2004). This presents a concern for honey bees because both neonicotinoids and fungicides (Terraguard and Procure) are used rather widely.

Due to the archaic science and theories being applied at the agency, the EPA Office of Pesticides does not even address or investigate the possible biological effects including sublethal effects of combinations of pesticides, but synergistic pesticidal effects can no longer be ignored when complex multiple combinations of toxic pesticides are being measured in bees wax and pollen without EPA having a clue as to what adverse effects they may be causing.

6. Honey bees may avoid higher concentrations of neonicotinoids in plants with pollen and nectar. Evidence suggests that honey bees have an innate ability to detect higher concentrations of neonicotinoids in plants and may avoid feeding on those plants to avoid chemical exposures, which lead Bayer scientists to conclude there were no effects below 20 ppb (Schmuk et al., 2001). But the Bayer's studies may not have considered that honey bees have an innate detection ability to sense the presence of neonicotinoids above 20 ppb.

7. These neonicotinoid substances carry acute toxicity that is extremely harmful to bees. EPA-OPP has identified imidacloprid and clothianidin as highly toxic to honey bees. According to the EPA Fact Sheet on Clothianidin, "Clothianidin is highly toxic to honey bees on an acute basis (LD50>0.439 mg/bee). It has the potential for toxic chronic exposure to honey bees, as well as other non-target pollinators through the translocation of clothianidin residues in nectar and pollen. In honey bees, the affects of this toxic chronic exposure may include lethal and sublethal effects in the larvae and reproductive effects on the queen." Seeds are treated with clothianidin in advance or sprayed with it in the field, and the insecticide can also be blown onto other crops. The chemical is often sprayed on corn fields during spring planting to create a protective film on cornfields.

Conclusion .... The EPA's Office of Pesticide Programs needs to promptly suspend use of the nicotinyl insecticides until EPA obtains scientific evidence that sublethal effects do not cause harm to America's honey bees.

Sincerely yours,

Laurel Hopwood
Chair, Sierra Club Genetic Engineering Committee
2459 Queenston Road
Cleveland Heights, Ohio 44118-4315

cc: members of the U.S. House of Representatives Committee on Oversight and Government Reform, and Committee on Agriculture Subcommittee on Horticulture and Organic Agriculture; Marcel Howard


1. Bonmatin, J. M., I. Moineau, R. Charvet, M. E. Colin, C. Fleche, E. R. Bengsch. 2003. Fate of imidacloprid in fields and toxicity for honeybees. Environmental Chemistry.
2. Bonmatin, J. M., P. A. Marchand, R. Charvet, I. Moineau, E. R. Bengsch and M. E. Colin. 2005. Quantification of Imidacloprid Uptake in Maize Crops. J. Agric. Food Chem. 53, 5336-5341.
3. Chauzat, M. P., J. P. Faucon, A. C. Martel, J. Lachaize, N. Cougoule and M. Aubert. 2002. A Survey of Pesticide Residues in Pollen Loads. Agence Francaise de Securidad Sanitaire des Aliments
4. Chauzat, M. P., J. P. Faucon, A. C. Martel, J. Lachaize, N. Cougoule and M. Aubert. 2006. A Survey of Pesticide Residues in Pollen Loads Collected by Honey Bees in France. J. Econ. Entomol. 99 (2):
5. Colin, M. E., J.M. Bonmantin, I. Moineau, C. Gaimon, S. Brun, J.P. Vermandere. 2004. A Method to  Quantify and Analyze the Foraging Activity of Honey Bees: Relevance to the Sublethal Effects Induced by Systemic Insecticides. Arch. Environ. Contamin. Toxicol. 47, 387-395.
6. Decourtye, A., C. Armengaud, M. Renou, J. Devillers, S. Cluzeau et al.. 2004. Imidacloprid impairsmemory and brain metabolism in the honeybee (Apis mellifera L.) Pestic. Biochem. Phys 78:83-92
7. Frazier, Maryann,  Department of Entomology, The Pennsylvania State University, Testimony  before the U.S. House of Representatives Committee on Agriculture Subcommittee on Horticulture and Organic
on Update on Colony Collapse Disorder in Honey Bee Colonies in the United States, June 26, 2008
8. Iwasa, T. N. Motoyama, J. T. Ambrose and R. M. Roe. 2004. Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Protection 23, 371-378
9. Jones, A.K., V. Raymond-Delpech, S.H. Thany, M. Gaulthier, and D.B. Sattelle. 2006. The nicotinic acetylcholine receptor gene family of the honey bees, Apis Mellifera.  Genome Res. 16(11). 1422-30.
10. Rouchaud, J., F. Gustin, and A. Wauters. 1996. Imidacloprid insecticide metabolism in sugar beet field crops. Bull. Environ. Contam. Toxic. 56:29-36.
11. Schmuk, R., R. Schoning, A. Stork, and O. Schramel. 2001. Risk posed to honey bees (Apis mellifera) L., Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Manag. Sci. 57(3), 225-38.
12. U.S. EPA Fact Sheet on Clothianidin
13. Imidacloprid Fact Sheet, Journal of Pesticide Reform, Spring 2001, Vol. 21(1), 15-21


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