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Understanding the Science: the Impact of Imidacloprid on Bees
Imidacloprid is the largest-selling pesticide on earth. It has been widely implicated as an important cause in honeybee death worldwide, and the Colony Collapse Disorder (CCD) problem. The following describes some of the important toxic characteristics of imidacloprid.
Units and Measurement:
- ug - microgram, or one-millionth of a gram
- ng - nanogram, or one-billionth of a gram
- ppb - parts per billion
- kg - kilogram
- half-life - time required for half of a substance to break down
- LD50 - the Lethal Dose required to kill 50% of bees (or anything) - a standard often used by the US Environmental Protection Agency
- metabolite - breakdown products of a chemical, often very toxic
- NOAEC - "No Adverse Effects Concentration" acronym for a term used by the US Environmental Protection Agency to refer to a chemical concentration where no adverse effects are reported
Imidacloprid is a nicotine-based insecticide, belonging to a class of chemicals called the "neonicotinoids." Functioning as a neurotoxin, imidacloprid and its metabolites interfere with the transmission of nerve impulses in insects by binding to one or more of the nicotinic acetylcholine receptors. Because imidacloprid is a systemic insecticide, it has the ability to readily move within the plant from the soil into the leaves, flowers, fruiting bodies, pollen and nectar of plants. As such, the entire plant becomes toxic - this is referred to as a 'systemic' pesticide - and it forms a shield inside the plants that effectively kills insects and other invertebrate organisms. Imidacloprid is the most widely used insecticide in the world, and in the United States it can be applied as a seed treatment, soil drench, foliar spray, and as a tree injection to a large variety of crop and non-crop plants. It is also common as a pet treatment.
Environmental fate studies have shown that imidacloprid is very persistent in soil and water with half-lives of up to three years in soil, and one year in water. Field studies have shown that residues in soil can bioaccumulate for several years from successive applications of imidacloprid. Imidacloprid is metabolized in plants and in bees, but the breakdown products can be as toxic and in some cases more toxic than the parent to bees and other insects. One of its metabolites desnitroimidacloprid has been shown to be toxic to mammals, but these effects have not been well studied (http://www.ncbi.nlm.nih.gov/pubmed/12460746).
In 2001, the French Minister of Agriculture established a Technical and Scientific Committee of expert scientists to explore the factors causing the massive die-off of bees in France. One of the factors this Committee explored was Gaucho or imidacloprid and its impact on bees. The Committee of experts was tasked with evaluating all the research studies conducted by independent researchers and by the pesticide industry on imidacloprid and bees. In 2003, the Committee released a report summarizing their findings. (www.agriculture.gouv.fr/IMG/pdf/rapportfin.pdf).
Based on validated exposure studies, the Committee concluded that imidacloprid levels in pollen of sunflowers and corn averaged 3.3 -3.5 ug/kg (ppb), respectively, and 1.9 ug/kg (ppb) in sunflower nectar. Soil residues averaged 10.25 ppb. Residues in corn plant leaves, stems, and flowers varied from 3 – 7.5 ppb, while sunflower plant samples averaged 4.6 ppb. Higher residue levels in plants (> 4 ppm) have been reported to EPA and the California Department of Pesticide Regulation by the pesticide registrant http://www.cdpr.ca.gov/docs/registration/canot/2009/ca2009-02.pdf). In addition, recent unpublished studies conducted at the University of Maryland have found high levels of imidacloprid in pollen of pumpkin plants. According to the French Technical and Scientific Committee, the calculated total amount of imidacloprid that could be brought back to the hive as sunflower pollen range from 0.84 to 50 ug and from 0.17 to 66 ug for imidacloprid in corn pollen. The total amount of imidacloprid brought back to the hive in nectar range from 133 to 266 ug based on hives from which 20 kg and 40 kg of honey were harvested.
Many acute mortality studies have been conducted to examine the short-term effects of imidacloprid to bees. All of these studies show that imidacloprid is highly toxic to bees when applied topically or ingested by bees on an acute basis (24 – 48 hours). The French Technical and Scientific Committee found that acute mortality by oral ingestion ranged from an LD50 of 4 to 71 ng of imidacloprid per bee, while the topical LD50 ranged from 6.7-242 ng imidacloprid per bee. U.S. EPA uses acute mortality values of 3.8 ng imidacloprid/bee for oral ingestion and 7.8 ng imidacloprid/bee for contact toxicity.
A 10-day chronic oral toxicity study with honey bees, which was validated by the French Committee, indicate an LD50 of 0.12 ppb or 1.2 pg/bee/day for imidacloprid and its metabolites, including 5-hydroxyimidacloprid, olefin, 4,5-dihydroxyimidacloprid, 6-chloronicotinic acid, desnitroimidacloprid, and urea derivative (Suchail, 2001). In response to Suchail’s findings, the pesticide manufacturer conducted studies with two of the imidacloprid metabolites, but the results of these studies were contradictory and the studies had numerous deficiencies. Other oral chronic toxicity studies published in the literature and that measured mortality in honey bees after 10 or more days of ingesting imidacloprid have reported NOAEC values < 4 ppb (Moncharmont, 2003), NOAEC < 12 ppb (Decourtye, 2003), and NOAEC < 10 ppb for bumble bees (Mommaerts, 2010).
A large number of laboratory, tunnel, and field studies (> 40) conducted by independent researchers and the pesticide manufacturer have shown that low concentrations of imidacloprid and its metabolites produce sublethal or behavioral effects in bees. These studies have observed the following sublethal effects in bees from exposure to imidacloprid: disorientation, reduced learning performance, poor motor coordination, reduced foraging activity, knockdown effects, reduced consumption of food, biochemical effects, and other effects that weaken the colony and impair the bee’s ability to find its way back to the hive. Several of these studies have shown a number of sublethal effects to bees at concentrations less than 1 ppb. According to the French Technical and Scientific report, the LOECs (Lowest Observed Effect Concentrations) in these studies ranged from 0.1 – 40 ng/bee in laboratory studies; 0.07 – 7 ng/bee in tunnel studies; and 0.25 – 7 ng/bee in field studies.
Over 20 tunnel and field studies have been conducted to examine the effects of imidacloprid in more natural conditions, most of which were conducted by the pesticide manufacturer. Although these studies have numerous deficiencies, several of the studies demonstrated sublethal effects to bees and in some cases increased mortality when exposed to imidacloprid-treated crops.
The extent to which all of these studies show deficiencies point out the extreme difficulty in designing and interpreting data from field studies. Since bees can forage 6-7 kilometers from their hives, researchers must find at least two large fields (> 7 km) that do not have previous pesticide residues. The treated and control fields must be separated by a comparable distance to ensure that the bees do not cross into the other field. Another difficulty in implementing these studies is ensuring that the fields are comparable in flower and nectar production and in physical and climatic conditions. Since a large number of bees (at least 4,000) must be used in field experiments, sophisticated equipment and observers must be used to track a large number of bees to ensure that they are visiting the treated crop and not nearby crops.
After reviewing a large number of laboratory and field studies, the French Technical and Scientific Committee developed scenarios to evaluate risk of imidacloprid to bees. Based on validated studies, the Committee concluded that there was a significant risk to bees from exposure to Gaucho on sunflowers and maize, the only crops for which they had exposure data. Furthermore, development of exposure data for other crops could show similar risks. As a result of the Committee’s report, the French Agriculture Ministry suspended the use of imidacloprid on sunflower seed and maize. Italy and Slovenia have taken even more aggressive steps in suspending the use of the neonicotinoids on most crops.
A large amount of money is being spent on additional research to determine the causes of the massive bee die-offs around the world. Only a small percentage of this money is being spent on pesticide research, and of this small percentage, most of the money is directed to examining effects that have doubtful value. Although there is enough evidence to show high risks to bees from exposure to imidacloprid in the environment, if additional research is conducted, it should be focused on examining effects of imidacloprid on brood and larvae development, chronic dietary toxicity of parent and major metabolites, persistence of major metabolites, well-executed and designed tunnel/field studies that examine over-wintering success of the hive, and exposure data measuring residues of imidacloprid in pollen and nectar of major crops and in the hive. Given the complexity of these studies and the poor track record in conducting these studies, additional field or semi-field studies should be carefully planned and implemented with on-site visits by EPA to ensure that the results are valid.