Insecticides and CCD, Part II

Bee Culture (July) Vol. 136 (7): 17-18




Dr. Malcolm T. Sanford


Last month I discussed the rationale for pesticides being implicated in colony collapse disorder (CCD), specifically a new class of chemicals that is being implemented widely by applicators called neonicotinoids.  The lead compound for this class is imidacloprid.  It and its derivatives are extremely effective on insects, attacking specific nerve targets (nAChR), but relatively benign on mammals (humans, dogs and cats). 


Because they are so specific for insects, however, means that honey bees could be readily affected by neonicotinoids.  The first indication of this was in France, when beekeepers noticed an extreme decline in their colonies in sunflower fields.  The Syndicat National d'Apiculture. Syndicat des Producteurs de Miel de France, and Union Nationale d'Apiculture Française issued a joint statement in Paris,18th. December 2000, which contained the following preamble:


“A press communication dated 16th. December 1998, produced by the Minister of Agriculture and Fisheries, announced that: The commission (Commission de toxiques) charged to evaluate the impact of Pesticides have studied the dossier ‘GAUCHO’ (Imidacloprid - BAYER). Following these studies, it has published the following advisory comment

‘Taking into account recent studies evaluating the impact that Imidacloprid could have on the activity of bees when used as a seed treatment for sunflowers ‘, the Commission des Toxiques during its meeting held on the 16th. December 1998 considered that:  


The examined data does not allow for a conclusion of indisputable effect of imidacloprid or its metabolites on bees and the production of honey.


‘Inversely, it is not possible to totally exclude the effect of imidacloprid and its metabolites, taking into account the toxic effects of minute doses, doses that are in keeping with those concentrations potentially present in the plants during the period of harvest.


‘That complementary study should be undertaken to clarify the following points:


1.  The metabolism of the product in parts of the plant accessible to bees.

2.  The limit of the toxicity of the product and its metabolites for bees and the quantities present.

3.  The persistence of imidacloprid in the soil and the presence in crops that have not been treated.’”1  A demonstration in Paris by beekeepers associated with the above statement led to the pulling of the label for Gaucho®, the first and only time this has occurred to my knowledge.


This and other reports and investigations have led to numerous reflections on imidacloprid and its relatives.  Graham White in the United Kingdom provides a rather complete synopsis of his analysis with many good references via the British Beekeepers Assocation Web Site:2


My concerns are threefold:


“As a beekeeper I am concerned that we are beginning to see evidence of unusual collapse of bee colonies in the UK.


“As a conservationist I am concerned that the large scale use of this highly toxic, systemic and persistent insecticide in the UK is effectively sterilising fields of all soil-invertebrate life including: earthworms, beetles, ladybirds, butterflies, moths etc. This has profound ecological implications, especially for insectivorous birds and mammals.


Imidacloprid is highly persistent in the environment and is absorbed into all parts of the crop-plant: pollen, nectar and seeds. If collected by bees it is progressively concentrated in honey as the nectar is evaporated. It seems likely that it will be present in sunflower and rape-seed oil, - even if in small quantities. As a neuro-toxin this may have implications for the food chain and human health.”


He concludes: “Currently there is growing concern in the UK about the unexpected collapse of bee colonies in summer (a time when they normally thrive) and a sporadic incidence of failure of queen bees to mate or prosper.  As yet the evidence is anecdotal and a national survey/ study is urgently needed but if the pattern follows that observed in Sweden, France and Canada, it seems a reasonable hypothesis that imidacloprid may be a causal factor.  Imidacloprid is a systemic insecticide which attacks the nervous system of all invertebrates; the target pests are flea beetles and wireworms etc but beneficial species such as bees, earthworms and beetles are also killed. The pesticide is dusted onto seeds before they are planted and is used on a worldwide scale on crops including: sunflowers, oilseed rape, potatoes, wheat etc.”


Unfortunately, the evidence is mixed on imidacloprid’s presence in plants honey bees might use for forage.  In one Canadian study:3


Kentville, N.S., March 8, 2002. A collaborative research project recently found that imidacloprid (Admire®) was not found in pollen and nectar of wild flowers and clover flowers in years following an in-furrow application of the product.


“The research project was undertaken as a result of a question raised by beekeepers whether imidacloprid or its plant metabolites was the cause of the dwindling bee populations reported by beekeepers in Prince Edward Island and other areas.  Admire® is a popular insecticide for control of Colorado potato beetle and other insect pests in potatoes.


“Results of the Imidacloprid Residue Study were presented to the Canadian Honey Council and the Canadian Association of Professional Apiculturists in Banff on January 30, 2002.”  The principal investigators were Jim Kemp and Dick Rogers.


They concluded:  "Our answers to the question are based on determining the residue levels in parts per billion after imidacloprid was applied in-furrow.  Measurements were taken in the current year and the first and second year after application.  Imidacloprid and its two main metabolites (hydroxy and olefin forms) were not found in clover flowers and wildflowers, bee collected pollen and nectar, and uncapped honey. Residues can be measured when they are at or above the detectable limit of 2 parts per billion.”


“The study took place during the summer of 2001 in PEI and New Brunswick. It included sampling and analysis of over 3,800 soil cores, over 8,000 clover leaves, over 2,000 clover flowers, over 480 grams of wildflowers and over 6,000 honeybees.


“The Imidacloprid Residue Study was funded in part by the governments of Prince Edward Island and New Brunswick, with major funding by Bayer Inc. Additional partners and collaborators in the study included the Agriculture and Agri-Food Canada Research Branch, Cavendish Farms Research division, Jasper Wyman & Son and the potato growers and beekeepers of the Maritimes.”


A study by a team of French scientists “describes a new approach to assess more specifically the risk posed by systemic insecticides to honey bees with the example of imidacloprid (Gaucho®).  This approach is based on the new and existing chemical substances Directive in which levels of exposure (PEC, Predicted Exposure Concentration) and toxicity (PNEC, Predicted No Effect Concentration) are compared. PECs are determined for different categories of honey bees in relation to the amounts of contaminated pollen and nectar they might consume.  PNECs are calculated from data on acute, chronic, and sublethal toxicities of imidacloprid to honey bees, to which selected assessment factors are applied.  Results highlight a risk for all categories of honey bees, in particular for hive bees.  These data are discussed in the light of field observations made on honey bee mortalities and disappearances.  New perspectives are given to better determine the risk posed by systemic insecticides to honey bees”.


In their discussion, the authors conclude: “The PEC/PNEC derived from the calculation of honey bees' exposure to which appropriate assessment factors were applied show that the risk posed by imidacloprid is alarming for all categories of honey bees. These ratios are all over 1, and greater in adult hive bees than in any other categories of bees. Whatever the validated toxicity data are, the determined PNECs are in a limited range of values (between 1.2 and 50 pg/bee). These estimates are in agreement with observations made in regions of extensive sunflower and maize cultures, which report a decrease in honey production since the launching of imidacloprid on sunflower plants in 1994.”


“At sublethal doses, pesticides are known to have profound impacts on the colony, in particular on the honey bees' longevity, the brood production, the development of hypopharyngeal glands, and the egg laying .  Imidacloprid is known to affect the honey bees' cognitive behaviors such as the proboscis extension reflex PER.  Learning and memorization in honey bees' tasks are very important.  For example, a forager that is disorientated might get lost and eventually die.  In the case of massive foragers' intoxications, the colony is likely to be greatly affected.  In an experiment under tunnels, Vandame et al. exposed honey bees to deltamethrin at a sublethal dose that is 20-fold lower than the registered dose at which foragers are expected to be exposed to in the environment.  They found that 54% of the treated bees were disoriented and took flight toward the sun.  The authors concluded that such sublethal effects may be the cause of the symptom called the ‘disappearance bee disease’ by beekeepers who observed colonies' weakening without finding dead bees close to the hives.  This hypothesis was formerly raised by other scientists.”4


Note that deltamethrin mentioned here is a pyrethroid5 in the same class as fluvalinate, considered one of the most benign pesticides used for Varroa control.  If one mixes this knowledge with the fact that organophosphates (coumaphos in CheckMite+®) may also be used inside beehives at very low levels, then the blame for disorientation and forager loss may not lie strictly with the neonicotinoids.  The bottom line is that we simply don’t know how much sublethal pesticide levels individual honey bees can take before their population becomes at risk of “disappearing” and/or “collapsing.” 


Several beekeepers I have talked to are convinced that neonicotinoids are implicated in CCD.  And David Hackenberg, one of the first beekeepers affected by the disorder, has written his pollination customers providing them a list of materials, asking them not to apply any of these substances, and to instead consider alternatives.6  Beekeepers might also consider this when planning their control measures for parasitic mites.  There seems little question that adding any pesticide to the honey bee’s environment puts it and the colony it inhabits at greater peril. 




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3.  Posted on Bee-L April 11, 2007:<>.

4.  Marie-Pierre Halm,, et. al. 2007.  “New Risk Assessment Approach for Systemic Insecticides: The Case of Honey Bees and Imidacloprid (Gaucho),” Environ. Sci. Technol., 40 (7).

5.  <>.