First published in: American Bee Journal, August, 2012
Trying to Make Sense of It All
Look and You Shall Find It
Looking at Both Sides of the Issue
The Regulatory Gauntlet
A Balancing Act
Who Does the Testing?
Academic versus Field Applicable
Problems in Methodology and Interpretation
Science is all about trying to understand things. When a scientist gets a hunch about why is it that something happens, he puts his hypothesis to the test in an experiment. He may then publish the results, including his own interpretation of the data—at which point other scientists are duty bound to question every aspect of the study, as well as to attempt to replicate the original results. In the end, we hope to learn what is actually true.
And this is my intent, to get to the truths of the neonicotinoid issue. In this series of articles, I am essentially “thinking out loud.” I find that the neonic issue is so emotionally charged that folk try to pigeonhole you as holding a black or white position, and then try to paint you as defending that position. Please let me be clear—I hold no position, and am not trying to defend anything! I’m simply asking that we stick to the facts, rather than playing to irrational fears and supposition. To that end I am intentionally taking on the role of “mythbuster,” which is predictably rubbing some folk the wrong way. But if I can get people actually thinking, rather than merely parroting, then I feel that my efforts have been successful!
So how do we reconcile the conflicting reports on the neonics? Last month I reported from Ground Zero of neonicotinoid use, and found the majority of beekeepers to be doing just fine. On the other hand, there was a rash of reports this spring of apiaries suffering serious mortality from planting dust. And to further confuse the issue, several recent scientific studies have been interpreted as having demonstrated that neonics are going to be the death of bees.
Trying to Make Sense of It All
As I reported in my last article, many beekeepers feel strongly that the widespread use of the neonicotinoid insecticides has been a good thing—there are far fewer spray kills nowadays than back in the bad old days (in 1968 an estimated 83,000 colonies were lost to pesticides in California alone ). However, there remain several unresolved issues and unanswered questions about these insecticides:
- There are occasional, but intolerable bee kills due to seed planting dust (especially so this year), from which individual beekeepers may suffer serious financial losses. This issue must be resolved!
- Although there is a substantial amount of good field data indicating that neonic residues in pollen and nectar are generally at tolerable levels, in some instances higher concentrations have been found. These situations need to be clearly identified.
- The long-term potential buildup of residues in soil must be carefully monitored.
- The sky-high application rates of neonics for landscape uses (turf, ornamentals, homeowner use) and on flowering trees, and the resulting runoff into surface waters, is of legitimate concern.
- The sublethal effects upon bee behaviors, such as memory, navigation, and age-related task allocation need to be further studied.
- The interactions between these insecticides and the bee immune response to parasites such as mites, nosema, and viruses need to be thoroughly investigated.
- Neonics have been shown to synergize with one particular class of fungicides. Other synergies should be explored, although there is no particular reason to suspect that neonics are unique in this matter.
All the above are things to be suspicious of, but to date there is no overwhelming evidence that any of them, save for the planting dust issue , generally cause serious problems. To date, no independent investigatory body has been able to confirm that the neonics are responsible for large-scale colony mortality .
Practical application: the scientific community and the regulatory bodies are well aware of the potential adverse effects of the neonicotinoids, are actively researching the issues above, and are in the process of reassessing their risks.
There is a growing public demand for more environmentally-friendly pesticides, which must be balanced against the real-world needs of agriculture for effective pest control products in order to feed a hungry world. Unfortunately, there are constraints due to cost and the expiration of patents that limit the actual amount of testing that can be done before regulators must make decisions as to whether a pesticide appears to be safe enough to be registered for use. Accordingly, the EPA often grants “conditional registration,” which allows it to ask for continued testing under actual field conditions. This is a good thing, since approved uses of a conditionally-registered pesticide can be quickly revoked should problems appear.
This is where independent scientists take over from those of the pesticide industry, and follow their hunches to test for any suspected negative effects that the pesticide might cause to “off target” organisms, such as humans and honey bees. The confusing part to the public is that…
Look and You Shall Find It
As with anything, the more you look, the more you will find potential risks (just Google the words “dangers of” followed by any food, medicine, or household chemical). You can drive yourself crazy with “what ifs.” The trick is to try to put all the findings into perspective.
Looking at Both Sides of the Issue
What I find, is that to be objective one must go out of one’s way to investigate all of the evidence, and to listen carefully to the interpretations by all parties. I already had a thorough grounding in distrust of pesticides, having come of age shortly after the publication of Rachel Carson’s seminal book, Silent Spring (which jumpstarted the environmental movement). I have a background in aquatic biology, and have clearly seen the devastating effects of pesticides and pollutants on downstream organisms. I’m deeply concerned about our overreliance upon pesticides and the resultant environmental consequences, well summarized by Dr. David Pimentel .
What I have also done, however, is to take a look at the issue through the eyes of the other stakeholders—the farmers and the companies that supply them with the plant protection products that they clamor for. I find that it often helps to play “Devil’s Advocate” and argue the “other side’s” position. I must admit that my doing so has gotten me into hot water with a number of beekeepers, but if our side can’t rebut the other side’s arguments, then we don’t really have a good case, do we?
What I found was that there are dedicated people already trying to objectively sort out the evidence. These are the regulatory agencies, such as the EPA, which are assigned the difficult responsibility of deciding how best to balance environmental safety with the demands of agriculture—a difficult task to say the least!
The Regulatory Gauntlet
Manufacturers screen each newly-developed chemical for any potential uses, including that as a pesticide. For a chemical (whether natural or synthetic) to be registered as a pesticide, the registrant must demonstrate both its efficacy against one or more pests, as well as its relative safety to both humans and to the environment as a whole. To do so it must run a gauntlet of tiered levels of “risk assessment.”
In general, a product is evaluated in a stepwise fashion, first (in the case of honey bees) to determine the degree of exposure (e.g., honey bees wouldn’t be expected to get into cockroach bait), and then to quantify the toxicity of the product by both contact (spray or contamination of leaves) and orally (as in nectar, pollen, or water). Risk assessment has been updated to take into account exposure to residues from systemic pesticides (such as the neonicotinoids), which are absorbed by plants and distributed in plant tissues, rather than simply sitting on the surface (Fig. 1).
Figure 1. Routes of exposure to systemic insecticides and potential effects upon honey bee colonies. Diagram © SETAC (2011) Pesticide Risk Assessment for Pollinators: Summary of a SETAC Pellston Workshop.
After determining whether there is a risk of bees being exposed to the product, the next tier of risk assessment is to determine the LD50 (median lethal dose) and the NOEL (no observed effects level) of the pesticide, for both oral and contact routes, and acute and chronic exposure, for adult bees as well as brood. Safety margins are then applied to decide whether the risks to either adult bees or brood indicate that additional testing is necessary to quantify sublethal effects. Testing is done first in the lab, then “semi field” (in enclosed screened tunnels over crop plants), and then under full field conditions (hives next to planted fields) (Fig. 2).
Figure 2. A simplified flow chart for the risk assessment of plant protection products. This diagram has since been updated to reflect the use of systemic insecticides (EPPO 2010, SETAC 2011). IGR means “insect growth regulator.” The EPPO, EPA, and SETAC documents are freely available on the web—I suggest that interested beekeepers read them! Chart © European and Mediterranean Plant Protection Organization (EPPO 2003), by permission.
Not all countries use exactly the same testing requirements, most notably that in the EU and Canada, the formulated product, as opposed to solely the active ingredient, must be tested (a position that I strongly support). I’ve sat with some of the principals and discussed the state of the art of testing. All parties (including Bayer) would like to improve the risk assessment protocols, and develop a standardized set which all countries (and manufacturers) alike could use. I suggest that interested readers download two recent (and free) documents on pesticide risk assessment for honey bees:
- The 2008 International Symposium on Hazards of Pesticides To Bees , and
- Pesticide Risk Assessment for Pollinators: Summary of a SETAC Pellston Workshop 
You may be surprised by how thoroughly every aspect of pesticide testing with regard to bees is being discussed!
Practical application: the regulatory process for risk assessment of pesticides is constantly improving, and is adjusting specifically for the case of systemic insecticides. The regulators are looking long and hard at the neonics , but objectively rather than emotionally.
A Balancing Act
Roughly 15% of agricultural crop losses are due to insects, 13% to fungus. Growers call for industry to provide plant protection products to keep them from losing their crops (just as beekeepers call for products to protect our bees from varroa). The plant protection product (PPP) industry tests perhaps 200,000 compounds for any one that it actually brings to market, at a typical cost of some $200 million for each new product . The manufacturers need clear sets of rules in order to maintain the incentive to develop more ecologically-friendly pesticides.
The difficult balancing act between providing the PPP industry with rules, and the well-deserved scientific scrutiny of the effects of manmade pesticides in the environment are handled by regulatory agencies such as EPA and EPPO, with guidance from SETAC and The International Commission for Plant–Bee Relationships.
Practical application: I find it surprising that some advocates keep repeating that the regulatory agencies or the PPP industry are being negligent in looking out for the well being of honey bees—it only takes the slightest bit of homework to see that this claim is entirely untrue!
Who Does the Testing?
In general, after initial in-house testing, a manufacturer will generally shop out “core studies” to an independent lab or university researcher. Some will say that when an independent researcher is paid by the manufacturer to run a trial to test a product, that he is then hopelessly biased. I’ve spoken to a number of researchers, who take great offense at that suggestion! Or manufacturer may hire an independent company to run the trial. At the 2012 Eastern Apicultural Society conference, entomologist Jessica Lawrence from such a company (Eurofin) gave an impressive presentation on the nitpicky details that such a lab must follow in order to meet the highest standards of scientific testing .
The EPA even then does not take study conclusions at face value, but has its own reviewers go over them with a fine-toothed comb (for an example see ). They then thoroughly analyze all the available data prior to making a registration decision (see the 137-page document for the registration of clothianidin for some crops ).
Practical application: The point that I’m trying to get across is that, although the system is not perfect, I tend to trust the EPA’s thorough evaluation of a pesticide more than that of some blogger who has simply read a few abstracts.
Academic versus Field Applicable
Something that confuses the issue is that many of the published studies are academic—of scientific interest, but not necessarily relevant to “real life” situations. The problem with extrapolating from lab tests is that doses which cause adverse effects to individual bees under laboratory conditions may not cause any measurable effect when given to normal free-flying colonies. A number of researchers have told me that there appears to be some sort of colony-level mitigation of the effects of the neonicotinoid insecticides.
EPPO (2012) “adopts the assumption that the most reliable risk assessment is based on data collected under conditions which most resemble normal practice, i.e. by field tests or by monitoring the product in use. Such studies are relatively expensive and difficult to conduct, but the results should be considered as decisive if there is any conflict with results from lower-tier testing (laboratory and semi-field testing)”.
From my point of view, the best perspective is to not get distracted by the hypothetical, but rather to focus upon the two final arbiters of the effects of a pesticide upon colony health—the ability to maintain its population, and the ability to put on surplus honey. These two metrics (cluster size and weight gain) reflect the final calculus of all the potential effects of the pesticide, and are easily measured in the field.
Practical application: this is why I give such weight to the on-the-ground assessment of the effects of seed treatments upon bees by the beekeepers in the Corn Belt and on Canadian canola, who report good colony survival and honey production despite their bees foraging in landscapes with high neonicotinoid use.
The actual measured amounts of neonic residues found in the nectar or pollen of treated plants are typically in the range of 0-3 ppb (rarely above 5 ppb) (EFSA 2012). However, researchers routinely test bees fed at levels of 25 – 400 ppb, in order to find out what kind of negative effects may occur. The problem is that in many cases, the researchers do not make clear that they are testing at residue levels that would not normally occur under “field relevant” conditions.
The thing to keep in mind is that the neonics are, like nicotine, stimulants. Their effect is similar to that of other stimulants such as the toxic alkaloid caffeine, with which 90% of U.S. adults intentionally dose themselves with on a daily basis.
As an analogy, suppose that you wanted to perform an experiment to determine the effects of the stimulant caffeine on the ability of downhill bicycle racers to negotiate a tricky course. A cup or two of coffee would likely enhance their performance; but imagine if you forced them to drink 10 or 40 cups (still “sublethal doses”) before the race! Would you consider the results to be relevant to everyday real life?
Dr. James Cresswell  recently performed a meta-analysis of published research on the effects of neonicotinoids upon bees, in both laboratory and field trials. He then fitted dose-response curves to the data (Fig. 3), which suggested that there would be little expected bee mortality at field relevant doses (the paper is a free download, and worth reading).
Figure 3. Neonicotinoids are typically tested at doses higher than those to which bees would be normally exposed in the field via nectar or pollen. This is a legitimate method for identifying potential negative effects, but the results may not necessarily be relevant under field conditions. Graph roughly after Cresswell 2010.
On the other hand, Cresswell found that “Dietary imidacloprid at measured levels in nectar from two widespread crops is expected to reduce performance [e.g., navigation] in honey bees by between 6 and 11% (oilseed rape) and between 14 and 16% (sunflower). These findings raise renewed concern about the impact of systemic neonicotinoids on honey bees that forage in agriculturally intensive landscapes.”
However, we must again compare those hypothetical performance reductions with reality—colonies in Canada make great honey crops on treated canola, as can bees in areas of treated corn and soy. The problem in reconciling these disparate reports is that several factors come into play in the field:
- The dose makes the poison—field doses from seed treatments are typically (except in the case of planting dust) very low. They are intentionally designed to be so.
- Bees metabolize neonicotinoids quickly , similar to the manner in which humans quickly metabolize nicotine, so that they appear to tolerate small doses well.
- Bees appear to find neonicotinoid residues distasteful , and avoid drinking highly contaminated nectar. However, they may well bring home highly contaminated pollen or dust.
- Just because an insecticide goes systemic in a plant, that doesn’t mean that bees are constantly exposed to that product. Treated plants only produce contaminated nectar or pollen for a relatively short period of time each season. The rest of the season the bees would ignore those plants.
- Several surveys of trapped pollen found that bees in agricultural areas often mainly collect pollen from plant species other than the treated crops. These findings suggest that bees may be avoiding the treated crops, and that nectar and pollen from the untreated plants would tend to dilute the insecticide residues. However, if the treated crop is the only plant in bloom, then the colony would be exposed to a greater degree (note, however, that colonies foraging on virtually undiluted treated canola appear to do fine).
- The above factors would lead to the dilution of the insecticide within the hive.
- Then there is the “colony effect.” Even when fed extremely high doses of imidacloprid over a period of weeks or months, colonies may continue to thrive (Pettis 2012; Lu 2012; Galen Dively, pers comm).
- This is not to say that exposure to high levels of planting dust can’t result in sudden loss of a large portion of a colony’s adult population!
Practical application: Just as drinking a couple of cups of coffee a day won’t hurt you, a little bit of neonics in the diet don’t appear to harm bees. The question then is always, “How great was the dose?” With modern analytical equipment, that is an easy question to answer by sampling the nectar, pollen, dust, or bees themselves. It is not hard to pin the problem on a specific pesticide if there is actual evidence, which is why it is so important for beekeepers to report adverse effects, and to make sure that samples are taken for analysis!
Problems in Methodology and Interpretation
To be frank, I find many studies on the neonics to exhibit obvious bias—those from the registrant tend to play down any adverse effects; to the contrary, some other labs are clearly on a mission to prove that neonics are the scourge of bees. Therefore, I find myself reading papers on this subject with an extremely critical eye. As an example of a well-designed and objectively interpreted study, I’ve included an arbitrarily-chosen free download in the references: (Aliouane 2009).
The first tier of testing for adverse effects involves laboratory trials with caged bees. One must keep in mind that the results of these studies must be qualified, in that it is difficult to duplicate the natural hive environment and social milieu with a handful of queenless, broodless bees in an incubator, so the results may not really apply to bees in real life. Dr. Geoff Williams has compiled a list of suggestions for the standardization of cage trials, soon to be published.
There are also inherent problems with tunnel and field trials, since it then becomes much more difficult to control extraneous variables, such as the impact of confined flight, weather, alternative forage, disease, and the finding of matching control plots. Often, unforeseen problems (Murphy’s Law applies in scientific research) crop up during a study and the study is junked; in other cases, the researcher openly discusses the problems; but sometimes obvious problems are simply ignored in the write up. Here are a few of the typical questionable details that I see in studies:
- I’ve already mentioned excessive dosing. Exaggerated dosing may help to point us toward avenues for further research, but should not necessarily be interpreted as having any field relevance. I suggest that you take a look at the dosing level in any study. Anything over 5 ppb in feed is likely not relevant to normal field exposure.
- Decourtye  found that there were substantial differences in susceptibility between winter and summer bees. There may well also be race and patriline differences to be accounted for.
- Lack of a “positive control”–that is, a dose of a known toxicant (typically the insecticide dimethoate) for comparison. Without a positive control, you really don’t know how the effects of the tested product compare to those from a generic chemical stressor (such as a hive miticide or a natural plant toxin). Amusingly, I’ve spoken with researchers who included a 100 ppb dose of imidacloprid expecting it to be a positive control that would kill most of the bees, but found to their surprise that there was actually little effect at the colony leve!.
- Additional solvents–some labs routinely use the solvent DMSO to first dissolve the neonicotinoid. When I checked with a toxicologist, he said that DMSO is dangerous to even have in a lab, since it greatly increases absorption of chemicals across membranes. Since the bee gut membrane is an effective barrier to neonicotinoids , I find such use of DMSO, which is not found in commercial neonic formulations, to be potentially problematic.
- Test bees are often knocked out with CO2 or chilled on ice for easier handling. Both stresses can affect be behavior and survivability [15, 16].
- Lack of control of stress due to parasites. Bees stressed by nosema or virus infection may be more susceptible to pesticide toxicity , indicating that in any testing of pesticides, the parasite load of the subject bees should be controlled for.
- Improper incubation temperature of bees or brood. Bee behavior and longevity can be strongly influenced by incubation temperature [18, 19], yet in some studies, the test bees have been severely chilled.
- Running tests solely on very young adult bees, rather than mixed age workers.
- Lack of proper nutrition for caged, newly-emerged bees. Many trials start with bees that are emerged into a near-sterile environment. These “teneral adults” are generally deprived of the normal meal of jelly from a nurse bee (and the included inoculum of the critical endosymbiotic gut bacteria), nor are they fed beebread, or any other protein source. DeGrandi-Hoffman  demonstrated that young bees deprived of protein get hammered by DWV. DWV can strongly affect bee brain function.
- In one widely-cited study, it appears that the researcher unknowingly starved the bees for sugar, yet claimed that their mortality was due to the insecticides .
- Caged bees are generally not exposed to the normal queen and brood pheromones of the broodnest. We have no idea how such deprivation affects their behavior, physiology, or resistance to insecticides.
Imagine that if we wished to determine the effects of a pesticide on humans, but that we used as test subjects young children that had been ripped away from their families, chilled, starved, and held in isolation, then knocked out and revived, dosed with a stimulant and then watched to see how well they performed some arbitrary test. Would we feel that the results of such a test were applicable to the human community in the real world? Again, the question on any scientific study on bees is whether the results are field relevant.
Practical application: when I carefully scrutinize scientific papers, I find that a number suffer from (often inadvertent) flaws in methodology, or from overreaching interpretation of the results. Luckily, the majority of researchers are meticulous and methodical, and I am greatly impressed by their diligent work! Unfortunately, most beekeepers can’t take the time to sort the good from the questionable.
There have been several widely cited studies released in the last couple of years—I’ve indicated in the references those that are free downloads. For those few of you who still trust my judgment and objectivity, I’ll give short summaries. Please note that I’ve often corresponded with the authors to get further details of their studies—in general, the researchers are happy to discuss their methodology and findings.
Nosema: Alaux (2009); Vidau (2011); Pettis (2012)—There is every reason to expect a synergy between insecticide stress and nosema infection; neonic treatment may either increase or decrease spore production, but appears to increase mortality in infected bees. However, such results may not be apparent at the colony level. In the Pettis study, after 10 weeks of feeding colonies pollen patties spiked at 5 or 20 ppb imidacloprid, “there was surprisingly no relationship between Nosema infection and imidacloprid treatment which would have been predicted by the lab study.”
Chronic toxicity: Tennekes (2010a, b)—I discussed the paper and his alarming book at length with Dr. Tennekes. He points out legitimate concerns about high levels of residues in surface waters; however, the applicability of the Druckrey–Küpfmüller equation does not stand up to scrutiny, nor does his bird data.
Guttation fluid: Hoffmann (2012) found the guttation fluid droplets on treated melons could contain high levels of neonics. I corresponded with the author about his three studies in Arizona—alternate water sources were available, and he did not observe bees taking up the guttation droplets.
Imidacloprid and CCD: Lu (2012). I don’t wish to belabor this paper’s shortcomings (see ScientificBeekeeping.com for detailed questions). Scott Black, executive director of the Xerces Society for Invertebrate Conservation, called the study “fatally flawed,” both in its design and its conclusions . However, there were two clear conclusions that could be drawn from the study—(1) feeding colonies for four straight weeks with a half gallon of HFCS spiked with imidacloprid at field-realistic levels did not have any negative effects, and (2) then feeding the colonies with sky-high levels of the insecticide for another nine weeks straight still did not harm them enough to cause mortality during treatment or for three months afterward.
Planting dust: Krupke (2012) contained little new information–planting dust can cause bee mortality; the test colonies recovered (Greg Hunt, pers comm). Points out potential synergies with fungicides—there are also other pesticides in the dust. There is a large body of research already published on this issue—see Krupke’s or Marzaro’s (2011) references sections.
Bumblebees: Whitehorn (2012) found that bumblebee colonies fed realistic doses of imidacloprid gained less weight and produced fewer queens. This finding is of great interest, since solitary- and bumblebee colonies are more likely to be affected by pesticides than would be honey bees (due to the population reserve in the honey bee colony). This is of special concern, since native pollinators are already suffering greatly from habitat disturbance and introduced pathogens. “However, it is uncertain as to what extent the exposure situation in the study is representative to field conditions since bumblebees would need to forage for two weeks exclusively on imidacloprid-treated crops in order to be exposed to the same extent as in the study” EFSA (2012).
Homing ability: Henry (2012) glued RFID chips to foragers, fed them a substantial dose of thiamethoxam, released them up to a km away from their hives and recorded whether they made their way home. They then calculated that colonies should crash due to loss of foragers—a result not substantiated in, say, canola fields. Schneider (2012), using similar tracking chips, found that field-realistic doses of imidacloprid or clothianidin had no effect the number of foraging trips from the hive to the feeder, the duration of these foraging trips, and the time interval a bee spent inside the hive between foraging trips, but that much higher doses, as expected, did cause negative effects. The EFSA review (2012) states that “it should be noted that there are several uncertainties regarding these results, therefore, they should be considered with caution. In particular, in the studies from Henry et al and Schneider et al. bees consumed the total amount of active substance within a relatively short period and not administered over a longer period (i.e. a day). Depending on the substance properties and how fast the substance can be metabolised by the bees, this method of exposure could have led to more severe effects than what may occur when bees are foraging.”
Sucrose responsiveness and waggle dancing: Eiri (2012) found that foragers treated with imidacloprid were less responsive to low sugar concentrations in offered droplets of syrup (intoxicated bees “liked” sweeter syrup). They also found that if bees were fed a 24 ppb (about 10x field realistic) dose of imidacloprid, the next day they performed fewer waggle dances (were they “hung over”?). Again, I must question the relevance of such high doses.
Other studies: I could fill the pages of this magazine several times over with my notes on hundreds of studies and my correspondence with various researchers, as I’ve really been trying to make sense of the neonicotinoids. I wish that I could give you cut and dried answers, but the science is not yet there. I’ll continue my analysis in the next issue…
 Swift (1969), cited in McGregor (1976) Insect Pollination Of Cultivated Crop Plants. http://www.ars.usda.gov/SP2UserFiles/Place/53420300/OnlinePollinationHandbook.pdf]
 AFSSA (2009) Mortalités, effondrements et affaiblissements des colonies d’abeilles (Weakening, collapse and mortality of bee colonies). http://www.afssa.fr/Documents/SANT-Ra-MortaliteAbeilles.pdf. This free download, translated into English, is an excellent overall review of colony mortality in Europe by the French Food Safety Agency.
 Pimentel, D. (2001) Environmental effects of pesticides on public health, birds and other organisms. Rachel Carson and the Conservation Movement: Past Present and Future. Conference presented 10–12 August 2001, Shepherdstown, W.V. http://rachels-carson-of-today.blogspot.com/2011/02/environmental-effects-of-pesticides-on.html
 Oomen, PA and HM Thompson (Editors) (2009) Hazards of Pesticides to Bees: International Commission for Plant-Bee Relationships, Bee Protection Group, 10th International Symposium. http://www.jki.bund.de/fileadmin/dam_uploads/_veroeff/JKI_Archiv/JKI_Archiv_423.pdf. This document is a “must read” for anyone seriously interested in pesticide risk assessment for honey bees.
 Pesticide Risk Assessment for Pollinators: Summary of a SETAC Pellston Workshop http://www.setac.org/sites/default/files/executivesummarypollinators_20sep2011.pdf
 Whitford, F, et al (nd) The Pesticide Marketplace, Discovering and developing new product. http://www.ppp.purdue.edu/Pubs/PPP-71.pdf]
 EPA (2003) Data evaluation record honey bee – Acute oral LD50 test http://www.epa.gov/pesticides/chem_search/cleared_reviews/csr_PC-044309_20-Mar-03_d.pdf
 EPA (2005) EFED Registration Chapter for Clothianidin for use on Potatoes and Grapes as a spray treatment and as a Seed Treatment for Sorghum and Cotton. http://www.epa.gov/pesticides/chem_search/cleared_reviews/csr_PC-044309_28-Sep-05_a.pdf
 Cresswell, JE (2011) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20(1):149-57. Epub 2010 Nov 16.
 Suchail, S, et al (2004) Metabolism of imidacloprid in Apis mellifera. Pest Manag Sci 60:291-296.
 DEFRA (2007) Assessment of the Risk Posed to Honeybees by Systemic Pesticides, PS2322. Central Science Laboratory, (GB). http://randd.defra.gov.uk/Default.aspx?Menu=Menu&Module=More&Location=None&Completed=0&ProjectID=13502 This is a long download, but full of good data.
 Decourtye, A (2003) Learning performances of honeybees (Apis mellifera L) are differentially affected by imidacloprid according to the season. Pest Manag Sci 59: 269-278.
 Suchail, S, et al (2004) In vivo distribution and metabolisation of 14C-imidacloprid in different compartments of Apis mellifera L. Pest Manag Sci 60(11):1056-62.
 Ebadi, R, et al (1980) Effects of carbon dioxide and low temperature narcosis on honey bees Apis mellifera. Environmental Entomology 9: 144–147.
 Frost, E (2011) Effects of cold immobilization and recovery period on honeybee learning, memory, and responsiveness to sucrose. Journal of Insect Physiology 57: 1385–1390.
 Vidau C, et al. (2011) Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. PLoS ONE 6(6): e21550. doi:10.1371/journal.pone.0021550
 Tautz, J, et al (2003) Behavioral performance in adult honey bees is influenced by the temperature experienced during their pupal development. Proc Natl Acad Sci 100(12): 7343–7347.
 Medrzycki, P, et al (2010) Influence of brood rearing temperature on honey bee development and susceptibility to poisoning by pesticides. Journal of Apicultural Research 49(1): 52-59
 DeGrandi-Hoffman, G, et al (2010) The effect of diet on protein concentration, hypopharyngeal gland development and virus load in worker honey bees (Apis mellifera L.). Journal of Insect Physiology 56: 1184–1191.
 Schmuck, R (2004) Effects of a chronic dietary exposure of the honeybee Apis mellifera (Hymenoptera: Apidae) to imidacloprid. Arch. Environ. Contam. Toxicol. 47: 471–478.
 Nordhaus, H (2012) The honeybees are still dying. http://boingboing.net/2012/05/07/the-honeybees-are-still-dying.html
Alaux C, et al (2010) Interactions between Nosema microspores and a neonicotinoid weaken honeybees (Apis mellifera). Environ Microbiol 12:774–782. http://www.prodinra.inra.fr/prodinra/pinra/data/2011/03/PROD20116cf9b1b_20110315103742504.pdf
Aliouane, Y, et al (2009) Subchronic exposure of honeybees to sublethal doses of pesticides: effects on behavior. Environmental Toxicology and Chemistry 28 91): 113–122. This is a free download, and an excellent example of a rigorous and meticulous investigation into the sublethal effects of some insecticides, in which they freely admit to some surprising and unexplained negative results for thiamethoxam. http://cognition.ups-tlse.fr/productscientific/documents/papers/Aliouane%20ET&C%2008.pdf
EFSA (2012) Statement on the findings in recent studies investigating sub-lethal effects in bees of some neonicotinoids in consideration of the uses currently authorised in Europe. http://www.efsa.europa.eu/fr/efsajournal/doc/2752.pdf
Eiri, D and JC Nieh (2012) A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing. The Journal of Experimental Biology 215: 2022-2029.
EPPO (2003) EPPO Standards: Environmental risk assessment scheme for plant protection products, Chapter 10, Honeybees. OEPP/EPPO Bulletin 33: 99–101. http://archives.eppo.int/EPPOStandards/PP3_ERA/pp3-10(2).pdf?utm_source=archives.eppo.org&utm_medium=int_redirect
EPPO (2010) Environmental risk assessment scheme for plant protection products. Chapter 10: honeybees. http://onlinelibrary.wiley.com/doi/10.1111/j.1365-2338.2010.02419.x/pdf
Henry, M, et al (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336 (6079): 348-350.
Hoffmann, EJ and SJ Castle (2012) Imidacloprid in melon guttation fluid: a potential mode of exposure for pest and beneficial organisms. J. Econ. Entomol. 105(1): 67-71.
Krupke CH, et al (2012) Multiple routes of pesticide exposure for honey bees living near agricultural fields. http://www.plosone.org/article/info:doi%2F10.1371%2Fjournal.pone.0029268
Marzaro, M, et al (2011) Lethal aerial powdering of honey bees with neonicotinoids from fragments of maize seed coat. Bulletin of Insectology 64 (1): 119-126. http://www.bulletinofinsectology.org/pdfarticles/vol64-2011-119-126marzaro.pdf
Pettis, JS, et al (2012) Pesticide exposure in honey bees results in increased levels of the gut pathogen Nosema. Naturwissenschaften 99(2):153-8. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3264871/?tool=pubmed
Schneider CW, et al (2012) RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0030023
Tennekes, H (2010a) The significance of the Druckrey–Küpfmüller equation for risk assessment—The toxicity of neonicotinoid insecticides to arthropods is reinforced by exposure time. Toxicology 276(1):1-4.
Tennekes, HA (2010b) The systemic insecticides: a disaster in the making. Weevers Walburg Communicatie.
Vidau C, et al (2011) Exposure to sublethal doses of fipronil and thiacloprid highly increases mortality of honeybees previously infected by Nosema ceranae. http://www.plosone.org/article/info:doi%2F10.1371%2Fjournal.pone.0021550
Whitehorn, P, et al (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336 (6079): 351-352.
First published in: American Bee Journal, September, 2012
“Scientists have largely remained silent when the public discussion turns to the trade-off of benefits and risks from chemicals. They are often unwilling to engage controversial issues that could endanger their funding and research…The public interprets the unwillingness of scientists to engage those who campaign against chemicals as an implicit validation of their dangers. Those who do speak out are often…branded as industry apologists. Maybe the best we can hope for is that brave scientists, scientifically literate journalists and government officials who are responsible for translating science into regulatory policy will take the public’s best interest into account…[and] resist the irrational and often regressive impulse stirred by the scare tactics that are so common today.” 1
Thanks for the Feedback!
Following the publication of my article “The Extinction of the Honey Bee?” 2 in which I pointed out that honey bees were thriving at Ground Zero of neonicotinoid use, I fully expected to be excoriated by the anti-neonicotinoid True Believers. But to my great surprise, I was instead deluged by letters of support from beekeepers and researchers worldwide! A few examples:
- “I’m an amateur beekeeper in France and I want to tell you that I strongly believe that CCD is not caused by pesticides. Like you, I’d like to find the culprit but so far it remains a mystery.”
- “I liked your article because here in Germany we are facing a hard discussion with bee keepers and other organizations regarding neonicotinoids and feel similar as you that often any scientific idea is missing and that it is a political mission,” from a researcher at the major agricultural science institute.
- “Likewise in USA, in Europe the discussion is more and more polarized, and in the hands of activists rather than scientists,” a bee researcher from the Netherlands.
- Thanks, Randy, for acting as a mythbuster,” from a beekeeper from the Corn Belt.
Fortified by your vote of support, allow me to return to what I hope is an objective analysis of the neonicotinoid debate.
Innate Distrust of Chemicals
I came of age in the ‘60’s, and was profoundly influenced by Rachel Carson’s book Silent Spring, which detailed how humans were poisoning the environment with pesticides. I have always had an innate distrust of manmade chemicals. I became an environmental activist, subscribed to Mother Earth News and Organic Gardening, moved to the woods, and began a lifelong quest to “walk the walk”—going solar, avoiding pesticides and manmade toxins in my personal environment, creating an organic garden and orchard. I’m a lifelong member of the Sierra Club and The Nature Conservancy, and am considered in my community to be about as green as you can get.
When I first heard reports from France that some new insecticides—the neonicotinoids—were causing massive bee mortality, I of course assumed, “Here we go again—the corporate recklessness of the chemical industry, coupled with government regulators asleep at the switch, has created yet another environmental catastrophe.” 3 So, having a background in biology and chemistry, in my usual manner I began to investigate the subject deeply.
Boy, was I in for an education! I read the literature from both sides of the pesticide debate, and got to know the principal players—the beekeeper anti-neonic advocates (who I fully respect), bee researchers, ecotoxicologists, farmers, and scientists from the chemical companies and the EPA. I soon found out who I could trust for accurate information, and who was so biased that I had to take anything they said with a grain of salt. I had thought that I knew something about pesticides; but in reality, how little I knew!
“Until the mid-20th century, pest insect control in agriculture relied on largely inorganic and botanical insecticides, which were inadequate. Then, the remarkable insecticidal properties of several organochlorines, organophosphates, methylcarbamates, and pyrethroids were discovered, leading to an arsenal of synthetic organics. The effectiveness of these insecticides, however, diminished over time due to the emergence of resistant insect strains with less sensitive molecular targets in their nervous systems. This created a critical need for a new type of neuroactive insecticide with a different yet highly sensitive target. Nicotine in tobacco extract was for centuries the best available agent to prevent sucking insects from damaging crops, although this alkaloid was hazardous to people and not very effective. The search for unusual structures and optimization revealed a new class of potent insecticides, known as neonicotinoids, which are similar to nicotine in their structure and action.” 4
The neonicotinoids had three other distinct advantages:
- They are far more toxic to insects than to mammals, making them much safer for humans.
- They are absorbed by plants and translocated via the vascular system, giving effective control of sap sucking and boring insects which other sprayed insecticides might not contact.
- They can be applied as seed treatments (Fig. 1), thus being a solution to the longstanding problem that roughly 99% of sprayed treatments never actually hit a target pest, and thus are unnecessarily dumped into the environment. 5
Figure 1. Treated seed, dyed for identification. The purple ones on the left are canola. Seed treatment has a very long history , and has been popular in the U.S. for about 40 years. Treatment can consist of any number of fungicides or insecticides, often in “cocktails.” The neonicotinoids, since they are transported by the plant vascular system, lend themselves well to this application. The treatments are diluted as the plants grow—in canola, they no longer kill aphids or flea beetles by the time the plants have grown for a month, and by bloom time, are nontoxic to bees.
The neonicotinoid insecticides have become widely popular with farmers, and when used as seed treatments, drenches, or attentively applied foliar sprays, appear to indeed be more environmentally friendly than the alternatives. However, the problem lies in the delicate balance between applying them in a manner that targets the pests, without harming “off target” species, such as bees and native pollinators. So let’s look at some of the questioned adverse effects.
I can’t think of any researcher who has more thoroughly investigated the effects of the neonicotinoids upon honey bee behavior than Dr. Axel Decourtye in France. In an extensive and excellent recent review, 7 he summarizes research on behavior:
Learning performance: Field-relevant doses do not appear to negatively affect learning, but higher doses may. “In general, results from these studies cannot be extrapolated to natural conditions. Moreover, imidacloprid can also have facilitatory effects on learning performances that complicate the interpretation at an ecological level.” Yes, you understood him–a low dose of neonic may help bees to learn!
Orientation: “The lowest observed effect concentration on the frequentation of feeding site was 50 [ppb]” (normal field-realistic doses are usually less than 5 ppb).
Foraging: “Although these studies showed the absence of effect of neonicotinoids on foraging of treated plants, perturbations of the foraging behavior on artificial feeder were revealed in other experiments. Thus, for example, it was found a quick decrease in the foraging activity in honey bee colonies at about 20 ppb of imidacloprid. This is probably due to the anti-feedant character of the compound.” This is a key point—bees appear to avoid nectar with high concentrations of neonicotinoids. Decourtye does mention that doses at the high end of field relevance may affect bee communication within the hive.
Stress due to exposure to any insecticide could plausibly affect bee immune response to pathogens. I find the research along this line less than compelling. What struck me was the lack of dose response, inconsistency of effect upon nosema replication, and lack of effect in field colonies. I’m sure that we will see further research on this subject.
Some beekeepers have been confused by the action of imidacloprid against termites, thinking that it suppressed the general termite immune function. This does not appear to be the case, as explained by Ramakrishnan (1999) 8: “Collectively, this evidence indicates that imidacloprid did not disrupt termite cellular defense mechanisms, and further suggests that social behaviors are the primary defense against pathogen infection.” The social behavior he refers to is grooming, by which termites clean fungal spores off their bodies to prevent infection. Since grooming does not appear to be critical for bee defense against the most common pathogens, I find it difficult to extrapolate the action of imidacloprid against termites to bees.
Social interactions and task allocation:
It is plausible that intoxication by neonics could affect bee social behavior or alter the normal progression of age-related tasks (as proposed by Dr. James Frazier). However, if this were the case, it should affect overall colony performance, which hasn’t been observed.
Putting sublethal effects into perspective:
People get hung up on the word “toxin.” Perhaps it would help to consider the neonics as “stimulants.” As I type these words, I’m enjoying the effects of a sublethal dose of the toxic alkaloid caffeine (plants produce caffeine to poison herbivores). Two cups of coffee supplies about 1/40th of the human LD50 (median lethal dose). 9 The way I brew my java, I’m at the high end of a sublethal dose! And I’ll dose myself again late this afternoon.
So why don’t I die from caffeine toxicity? Because my body quickly degrades the toxin. The same thing happens with nicotine, and with the neonicotinoids in bees. Suchail 10, 11 found that ingested imidacloprid is rapidly passed to the bee’s rectum and excreted or degraded within hours. Very little makes it into the blood or rest of the body. Only about 5% is absorbed into the brain or flight muscles, where it is converted to the more toxic olefin metabolite, which then disappears within a day. Although the metabolite is more toxic on a dosage basis, understand that little of it actually formed.
This is the main problem with the hypothesis of Dr. Henk Tennekes 12, whose widely-cited publications attempt to make a case for the application the Druckrey–Küpfmüller equation for chronic toxicity to the neonics. I’ve corresponded at length with Dr. Tennekes, and asked him to explain why the neonics, which are also rapidly degraded by the bee, would have any more chronic toxicity than nicotine would to a human smoker. There is enough nicotine in a pack of cigarettes to easily kill a human, yet no one dies from nicotine toxicity (I watched in perverse horror as my high school biology teacher injected a rat with nicotine—its death was not a pretty sight). The point is, that nicotine and neonics appear to be so rapidly metabolized, that there is no buildup in the body (as there is in the case of DDT), the binding to the nerve receptors is reversible and insects recover fully, 13 and there is generally no increased mortality due to low-level chronic exposure.
Indeed, a number of studies have found that exposure to low doses of imidacloprid resulted in foragers being more active and carrying more pollen! 14 Some plants secrete nicotine or caffeine in their nectar; recent research 15 suggests that bees prefer a bit of stimulant “buzz” and are able to accurately self dose—avoiding syrup spiked to toxic levels.
Bottom line: Any number of scientists have diligently tried to find any sorts of sublethal effects of neonics on bees, but have failed to demonstrate adverse effects at the colony level at doses produced by seed treatments.
Effect Upon Brood
The surprising thing here is that bee larvae appear to be essentially immune to the effects of neonics! In fact no one’s been able to come up with LD50’s because you simply can’t dissolve enough of the insecticide in syrup to cause 50% of the larvae to die! 16, 17
However, there could be indirect effects, should the nurse bees—the main consumers of pollen in the hive—be affected by neonics residues. It is plausible that the nurses may exhibit reduced brood feeding. Hatjina 18 found in a lab study that nurse bees fed field-realistic doses of imidacloprid had reduced hypopharyngeal glands (that produce jelly).
On the other hand, perhaps nurses amped up on stimulants work harder—Lu 19 found that field-realistic doses of imidacloprid actually increased broodrearing, and that even extremely high doses had no significant effect upon brood area.
Bottom line: if there were an effect on brood, we would expect to see it in field studies. Such studies do not show negative effects at realistic doses.
Vine Crops—squashes and melons
Colonies fare poorly on vine crops (cucurbits) unless they have alternate forage (pers obs). Exposure to pesticides likely exacerbates this problem. Two recent studies found that foliar, soil, or irrigation-applied imidacloprid may result in residues in squash or pumpkin nectar and pollen to levels at which some behavioral effects on bees may occur.
Dively 20 found that seed treatment of pumpkins was safe for bees, but that if neonics are applied close to bloom (as by chemigation or foliar application) that they may contaminate the pollen to the extent that one might expect some effects on the “pollen hogs” in the colony, that is, newly emerged workers and drones, or nurse bees.
Stoner 21 found that at allowed label rates for squash, neonic residues in nectar or pollen could push into the low range of observable behavioral effects. Such effects would likely only be serious to honey bees should lack of alternative forage be available. However, this would be different for the specialized native squash bees: “squash bees are specialists on Cucurbita, feeding their larvae exclusively on Cucurbita pollen, and also build their nests in soil, often directly beneath squash and pumpkin vines, so they could have much more exposure to the soil-applied insecticides used on these crops.” 22
Beekeepers in France emphatically blamed Gaucho seed treatment of sunflowers for colony losses. Bonmatin 23 (clearly on a mission against imidacloprid) found that sunflowers could recover imidacloprid from the soil following crops treated the previous year, and that the plants concentrated the residues in the flower head tissue (although he did not analyze nectar). Even so, he did not find residues that should have caused intoxication, even with seed treated at a much higher rate than on the U.S. label.
In Argentina, Stadler 24 placed hives in the center of large fields of flowering sunflowers from seed treated again at a higher rate than the U.S. label, and confirmed that at least 20% of the pollen in the combs was sunflower, and that the colonies had stored sunflower honey. They could not detect residues of imidacloprid in the pollen, and found that the colonies in the treated field actually performed better than in the untreated! They then moved the hives to natural pasture, and checked them again after 7 months, and found no differences between the groups.
So I don’t understand the videos I’ve seen of trembling or lethargic bees on sunflower blossoms in France. If any U.S. beekeepers have had trouble with bees on seed-treated sunflowers, I’d like to hear!
Buildup in Soil
In some clay soils residues of the neonicotinoids bond tightly to soil particles and may degrade slowly. However, the question is whether the roots of subsequently planted crops are able to absorb them (a Bayer rep pointed out to me that if they did, the farmer wouldn’t need to pay for seed treatment the next year). Data from canola fields in Canada (Fig. 2), in which treated seed has been planted year after year, do not support that residues escalate in the bloom, and a study is currently being run in California.
Figure 2. Some of Canadian beekeeper Cory Bacon’s hives working canola this July. Lab studies aside, Canadian bees appear to do quite well on seed-treated canola year after year, and I don’t hear the beekeepers complaining.
There are many other insects that feed on nectar and pollen. Native bees (Fig. 3) would be especially susceptible to systemic insecticides, since they do not fly far to forage, their larvae consume pollen directly, and due to their solitary nature, if the behavior of any female bee is disrupted, she may be unable to leave offspring. However, should native bee larvae have as high a tolerance of neonicotinoids as do honey bee larvae, the concern for larvae may be unfounded.
Figure 3. A sweat bee, Agapostemon virescens, on chicory flowering alongside an Indiana corn field. It is likely that solitary bees, such as this species, would be more negatively affected by neonicotinoids than would a honey bee colony. Photo by Larry Garrett, ID thanks to Dr. Robbin Thorpe.
Solitary native bees are an excellent bioindicator of whether systemic insecticides are causing problems, since they do not have a “reserve” as does a honey bee colony. As far as I can tell from the research, the decline in native bee populations appears to be mostly from habitat loss due to wall-to-wall tillage, not to mention spraying with old-school pesticides. There is scant evidence that field-relevant doses of neonics harm native pollinators, but this is an area that cries for additional research. Two good species to investigate would be our native squash and sunflower bees, since both forage predominately on the nectar and pollen of those plants, and since neonicotinoids are applied to both those crops.
Other Species of Life
There is legitimate concern about the effects of seed treatments upon earthworms. Dittbrenner 25 found that some species moved less soil in response to imidacloprid. Other researchers 26 have found that some predatory species of insects or spiders may be negatively affected in treated fields, likely due to the suppression of aphid populations–seed treatment only suppresses aphids while plants are young. As plants grow, the insecticide becomes too diluted to affect either sap-sucking insects or (ideally) pollen- or nectar-feeding insects.
The seed treatments appear to be more environmentally friendly to birds (who learn to avoid the seeds) and mammals than the insecticides that they replace
I’ve got a background in aquatic biology, and I agree with Dr. Henk Tennekes that levels of imidacloprid in surface waters in areas of heavy applications on non food crops (such as in the Netherlands) are of concern for aquatic ecosystems. Jody Johnson 27 found 7-30 ppb in some urban/suburban water, and up to 130 ppb in nursery puddles, and low levels in some streams. Neonics are relatively nontoxic to fish, but could affect the populations of the invertebrates upon which they feed.
Dr. Vera Krischik 28 has pointed out the potential dangers of landscape or ornamental uses of imidacloprid due to the possibility of extremely high doses making it into the nectar. Residues that would not be allowed in field crops are possible with landscape and nursery applications, and there are reports of bees dying from nectar from treated nursery plants. I concur with Dr. Krishik’s concerns.
In order to kill certain tree pests (lerp psyllids on eucalypts, borers in elm or ash) imidacloprid is registered for root or tree treatment. There is reason for concern about some of these registrations, as there is unpublished data of scary high concentrations in nectar.
Clearly the best uses for neonicotinoids are for seed application or soil drench. Foliar applications open a new can of worms, due to irregularity of application, translocation to bloom or extrafloral nectaries, or to adjacent flowering weeds. Foliar applications of neonicotinoids can clearly cause bee kills, and are much more subject to vagaries in application timing and other details than are seed treatments.
The registered uses as foliar applications should be safe for bees if label directions are followed exactly, but I simply haven’t seen enough data to make an assessment. Beekeepers should file incident reports if there are problems.
Dr. Jim Frazier points out that the unrotated use of the same seed treatments is contrary to good pesticide resistance management. Already we are seeing calls to expand the refuge plantings of non Bt corn; 29 it would likely be wise to do the same with neonic treatments. My concern is that if the pests develop resistance, then farmers will have to use additional sprays.
The Absence of any “Smoking Gun”
If neonics were actually causing colony mortality, it should be child’s play to demonstrate—just feed a colony syrup or pollen spiked with the insecticide and see how long it takes to kill it. The fact is, that try as they might, no research team has ever been able to induce colony mortality by exposing the bees to field-relevant doses of any neonicotinoid (although one can get a significant kill from corn planting dust). Nor has any investigation ever been able to link neonic residues in the hive to colony mortality. Every claim that neonics are causing serious bee mortality is unsupported supposition, not backed by any concrete evidence.
The Ignoring of Negative Findings
What is interesting about the neonics and honey bees is that the adverse effects that one may see when testing individual bees in the lab don’t necessarily translate into effects at the colony level in the field. I’ve spoken with several researchers who have tried to demonstrate harm to colonies by feeding them large amounts of imidacloprid, and found that it is hard to see any effect. 30
Such “negative findings” are rarely published—after all, who, other than the registrant or the EPA, would be interested in studies in which investigators expose bees to the chemical, and find that nothing happens? So the majority of such findings would only be published by the registrant, and of course no one trusts their research (damned if they do, damned if they don’t)!
Reviews of the Evidence
There has been a mountain of research done on the neonics, but most folk don’t have time to review it all (even if they could get their hands on the papers), so they must depend upon a trusted other to do so. Please don’t take my word for it–here are some (mostly) recent reviews; most are free downloads:
Reviews with a pro neonic bias:
I find that documents coming from the chemical industry typically have a reassuring slant, but invariably get their facts straight (it would be foolish for them to get caught in a lie).
Maus, C, G Cure, R Schmuck (2003) Safety of imidacloprid seed dressings to honey bees: a comprehensive overview and compilation of the current state of knowledge. Written by Bayer scientists, but the facts are sound. http://www.bulletinofinsectology.org/pdfarticles/vol56-2003-051-057maus.pdf
Reviews with an anti neonic bias:
Anti-neonic reviewers tend to cherry pick out several questionable studies, embellish the implications, and ignore on-the-ground beekeeper experience.
Small Blue Marble. Free downloads of a number of neonic papers. http://smallbluemarble.org.uk/research/
Pilatic, H (2012) Pesticides and Honey Bees: State of the Science. Decent summaries of many studies. http://www.panna.org/sites/default/files/Bees&Pesticides_SOS_FINAL_May2012.pdf
Relatively objective reviews:
- Xerces Society (who advocate on behalf of native pollinators)–Are Neonicotinoids Killing Bees? http://www.xerces.org/neonicotinoids-and-bees/]—did not find any strong evidence that neonics are harming pollinators, but recommend caution with use and further study.
- AFSSA (2010) Weakening, collapse and mortality of bee colonies The French Food Safety Agency conducted a thorough review of all suspected causes of colony mortality in Europe. They arrived at the politically unpopular finding that “The investigations and field work conducted to date do not lead to any conclusion that pesticides are a major cause of die-off of bee colonies in France.” http://www.uoguelph.ca/canpolin/Publications/AFSSA%20Report%20SANT-Ra-MortaliteAbeillesEN.pdf
- The European Food Safety Authority in their Statement on the findings in recent studies investigating sub-lethal effects in bees of some neonicotinoids in consideration of the uses currently authorised in Europe http://www.efsa.europa.eu/fr/efsajournal/pub/2752.htm, concluded that “Further data would be necessary before drawing a definite conclusion on the behavioural effects regarding sub-lethal exposure of foragers exposed to actual doses of neonicotinoids.”
- Blacquière, et al (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment http://www.gesundebiene.at/wp-content/uploads/2012/02/Neonicotinoide-in-bees.pdf This is a very thorough review of 15 year’s worth of research (over 100 studies).
- Cresswell (2011) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. http://www.springerlink.com/content/j7v320r55510tr54/fulltext.pdf in reviewing 14 studies, estimated that “dietary imidacloprid at field-realistic levels in nectar will have no lethal effects, but will reduce expected performance in honey bees by between 6 and 20%.”
- Creswell, Desneux, and vanEngelsdorp (2012) Dietary traces of neonicotinoid pesticides as a cause of population declines in honey bees: an evaluation by Hill’s epidemiological criteria. (Note the coauthor Dennis vanEngelsdprp, who has studied CCD as closely as anyone) “We conclude that dietary neonicotinoids cannot be implicated in honey bee declines, but this position is provisional because important gaps remain in current knowledge. We therefore identify avenues for further investigations to resolve this longstanding uncertainty.”
Of course, all researchers cover their butts and qualify their statements by suggesting that additional research needs to be done. These insecticides have been on the market for about a decade, and we are still learning about them. We definitely want to learn more about their effects upon other non target species, interactions with parasites, synergies with other pesticides, and sublethal behavioral effects.
I would prefer that you read the studies yourself, and then form your own opinions, but in reality I don’t expect you to read the hundreds of studies that I’ve read. It’s likely that most of you won’t even bother to read the reviews above!
Summary: The consensus opinion of the comprehensive reviews above, as well as of the vast majority of bee researchers that I’ve spoken with, mirrors Blacquière’s conclusion: “Many lethal and sublethal effects of neonicotinoid insecticides on bees have been described in laboratory studies, however, no effects were observed in field studies with field-realistic dosages.”
The Elephant in the Living Room
Let’s just put all scientific speculation aside, and look at the obvious—the survival and productivity of colonies actually exposed to neonics-treated crops. Not only is there no compelling evidence to date that exposure to seed-treated crops is causing harm to bees, but there are plenty of examples to the contrary, such as the thriving bee operations in the Corn Belt.
Neonicotinoid seed treatments actually appear to be living up to expectation as reduced-risk insecticides. When skeptical researchers have tested actual pollen and nectar from seed-treated crops, they invariably confirm that any neonicotinoid residues are indeed quite low. Bonmatin 32 sampled imidacloprid levels in corn pollen (Fig. 4) for three years running in France—they averaged 2.1 ppb. But contaminated pollen only made up about half of the pollen trapped at the entrances, so he revised his overall colony exposure via pollen to 0.6 ppb—a level at which no harmful effects have ever been observed.
Over the past two seasons Henderson and Bromenshenk (in press) sampled trapped nectar and/or pollen from hives in canola fields in Canada and corn across the Midwest; 95% contained less than 2.5 ppb of clothianidin residues.
Figure 4. By the time that a seed-treated plant is of any interest to bees—when it finally produces nectar or pollen—the concentrations of the neonicotinoid in those products are diluted to what appear to be easily detoxified levels. Larry Garrett took this photo of a bee gathering a load of corn pollen.
Colonies subsisting on corn pollen alone may indeed go downhill, but that would be due to its lack of certain amino acids. They do not appear to suffer from going into winter with a portion of their beebread consisting of pollen from seed-treated corn. No study (and there have been several) has been able to demonstrate that colonies suffer from foraging on seed-treated corn pollen, and some suggest that it was actually of benefit to them. 33
On the Canadian prairie, colonies build up and survive fine on a diet of canola nectar and pollen from treated fields. If neonicotinoid seed treatments were indeed causing the sort of colony mortality that some claim, the Midwestern and Canadian beekeepers should notice!
The Good, the Bad, and the Ugly
My personal assessment of our state of knowledge on the neonics:
- Neonics are unquestionably reduced-risk insecticides as far as humans and wildlife are concerned, and their use as seed treatments appears to be an environmentally-friendlier way to put the pesticide exactly where it is needed.
- Bees and other pollinators appear to be able to thrive on the pollen and nectar of seed-treated plants.
- There are clearly documented sublethal behavioral effects, but they do not appear to affect bees at field-relevant doses, and appear to be greatly mitigated at the colony level.
- Misapplication by homeowners and nurseries can result in unacceptably high residues in nectar or pollen, as can chemigation (as in vine crops).
- There is the possibility of residue buildup in soil, which should be monitored.
- Landscape and ornamental use can result in runoff into aquatic ecosystems, as documented by Henk Tennkes.
I suggest that beekeepers work closely with regulators on these issues.
- Foliar (spray) applications are less well studied than seed treatments, and have greater potential for inadvertent impact on pollinators. Applications to flowering (or soon to be flowering) plants could cause serious bee mortality, and should be carefully regulated.
- Injections of, or root application to, nectar-producing trees. For the sake of pollinators these applications must be closely investigated and monitored.
- Planting dust from sowing of corn. Although significant planting dust kills are rare, they are ugly. This issue is a bleeding wound to the beekeeping community, and needs to be addressed by the EPA and the registrants. Beekeepers should not be forced to suffer mortality to their livestock due to unregulated pneumatic planter dust. France and Germany have models that we can follow. Beekeepers rightfully feel strongly that the registrants should step forward and compensate beekeepers for their losses until the issue is resolved.
There is no conclusion. Neonics have only been on the market for about a decade, and we are learning how best to use and regulate them. There is plenty of current research and monitoring being done, and the world’s main regulatory agencies are currently carefully reviewing their registrations.
Separating Fact from Fiction
Up ‘til now this article has been my best shot at an objective review of the scientific data and on-the-ground assessments of the neonicotinoid insecticides. Now I am going to shift from statement of fact to my own personal opinions.
I don’t want to hammer on the anti-neonic crowd, nor do I want to sound condescending. One can indeed make a circumstantial case against the neonics, and I feel for beekeepers who have watched their hives fall apart—especially from pesticide issues. What I found, however, is that if one really does their homework, that the case against the neonics largely falls apart.
What bothers me is when advocates embellish the facts to suit their case. I choke on the amount of mis- or disinformation in many of their publications. For example, a recent issue of Britain’s The Beekeepers Quarterly 34 informs us that:
“in California [neonics] were applied to the entire almond crop for the last decade—which is why American bees collapsed so dramatically”
How easy it would have been to solve CCD if only that statement had any veracity! In truth, neonics were not used to any extent on almonds, a fact easy to check since California pesticide use reports are freely available. I find this sort of tossing about misinformation to be unethical.
The facts are that that when I checked the use reports for 2003, 2006, 2009, and 2010, there were zero neonic applications in the first two years, and only 96 and 1070 lbs of imidacloprid applied in 2009 and 2010 respectively (58 applications in 2010, and one app. of thiamethoxam of 0.17 lbs). To put those figures into perspective, about 20 million pounds of some 350 different pesticides are applied to almonds each season, predominately fungicides, which the growers spray liberally over the bees and bloom during wet springs. Yet colonies generally come out of almonds looking great!
It’s true that Bayer withdrew the registration for imidacloprid for almonds, but rather than being an admission of a problem, 35 it simply wasn’t worth it for Bayer to perform additional supportive studies for a product that not only wasn’t being used, but had gone off patent and would have been sold by copycat manufacturers using Bayer’s data (Dr. David Fischer, pers comm).
The problem with misinformation is that well-meaning folk then hop on the bandwagon to push their legislators to do something about an imagined problem. The more that I investigate pesticide issues, the more I find that policy has been driven by the politics of misinformation and fear, rather than by objective analysis of risks vs. benefits. I quoted the introduction to this article from a very readable book (a free download which I highly recommend) called “Scared to Death.” 36 The author gives examples in which well-meaning advocacy groups have fomented enough public pressure to force the withdrawal of this or that chemical from the market, despite a lack of evidence that the chemical was in truth harmful!
Caution: If you are a lifelong environmentalist, reading a decidedly pro-chemical book such as this will take you out of your comfort zone, and may force you to reevaluate your established views. However, it is impossible to dismiss the author’s analysis, since he does a pretty good job of backing up his claims with facts!
Overstepping the Bounds
I strongly support the pesticide watchdog groups, and frequently refer to their websites for information. However, I feel that they sometimes fall into Abraham Maslow’s trap of: “If the only tool you have is a hammer, you tend to treat everything as if it were a nail.” Some of these groups would have us believe that every health problem that humans or bees have can be blamed upon pesticides, a fear that I bought into in my younger days. But reality is not that simple.
For example, in researching the DPR database, I came across the figures for total pesticide use per county in California. 37 Aha, I thought, here’s a chance to nail a correlation between pesticide exposure and cancer! So I ran down a map for incidence of cancer by county to compare. 38 To my utter surprise, Fresno and Kern, agricultural counties using 30 and 25 million pounds of pesticides, respectively, in 2010 had lower cancer rates than did the pristine Northern California coastal counties such as Humboldt and Mendocino (0.03 and 1 million pounds). That bastion of environmental activism and organic everything, Marin county (0.06 million lbs), was in the highest tier of cancer incidence! Astoundingly, all six of the Calif counties with the highest pesticide usage were in the lowest tiers of cancer rates. Go figure!
The neonicotinoids (generally lumped together with GMO’s) have currently been pumped up to be a straw man that is responsible for the demise of the honey bee, and some advocacy groups are pulling out all stops in order to take them down. A problem happens when advocacy groups shift from merely informing our regulatory agencies, to the starting of public campaigns (that ignore actual evidence) to push lawmakers to overstep the regulators and ban a certain chemical anyway. This can result in unintended consequences to both humans and bees.
I have a vested interest in pesticides that are safer for humans, and the neonics fit that bill. In the case of bees, should seed treatment with clothianidin be banned, as PANNA is pushing, it’s not like farmers are all going to suddenly go organic—they will simply substitute other insecticides, which will then pollute the environment (and likely cause bee mortality) to a much greater degree–even some “organic” pesticides are more harmful to bees or other beneficials than some synthetics. 39, 40
Not only that, but when emotion trumps science, what are farmers and the Plant Protection Product industry supposed to do? It takes millions of dollars to bring a new product to market—including the newer generation “biopesticides” and reduced-risk pesticides. Why should industry invest if their hard work all goes up in smoke as the result of an irrationally fearful public campaign?
Practical application: my concern is that the beekeeping community should be cautious about allowing itself to be used as a poster child for the “neonicotinoids are the cause of CCD and the extinction of the bee” NGO’s. Some of these same advocates could well be campaigning next year against the natural toxins, or grains of GMO pollen, that are found in some honeys!
The EPA is actually doing a decent job. I’ve read their risk assessments for the neonics. They ask the right questions, and base their decisions on scientific evidence, not anecdote and emotion. I feel that when anti-chemical advocates or beekeepers bypass the system, that our society and the environment may suffer. The current focus on the neonicotinoids has drawn attention away from the incontrovertible damage caused to colonies every year by spray applications of other pesticides, as well as from important bee research which is finally elucidating the biological causes of colony mortality worldwide. To me, this misdirection of focus is a problem.
Folks, all regulatory agencies worldwide are fully aware of the questions regarding the neonicotinoid insecticides. The EPA is stuck between a hostile congress and farm lobby on one side, and the NGO advocacy groups and beekeepers on the other, and must stick to scientific evidence. There are plenty of watchdogs making sure that EPA does its job.
Let’s Redirect Our Energy
Instead of putting unwarranted lobbying effort against the single insecticide clothianidin, the bee industry would better benefit by going after (as Darren Cox says) “the low-hanging fruit”—the all-too-common bee kills due to spray applications of other pesticides. This is a labeling, educational, and enforcement issue.
- The EPA needs to better clarify its label requirements to prevent applicators from spraying onto flowering crops or allowing pesticide drift onto impact adjacent areas.
- The EPA needs to reassess the impact of fungicides, surfactants, other adjuvants, or tank mixes upon bees.
- Growers and applicators need to be better educated as to how to protect their crops without harming pollinators. Sometimes simply changing the timing of spraying can protect bees.
- EPA needs to push state agencies to cooperate with (rather than discourage) beekeepers when they suffer damages.
- State agencies need to take the lead in actually enforcing pesticide laws when violations occur.
The EPA has brought beekeepers to the regulatory table, and we are currently being well represented by the National Honey Bee Advisory Board, and by Darren Cox at the Pesticide Program Dialogue Committee. I’m greatly encouraged that the NHBAB currently includes beekeeper/growers—who see both sides of the issue of necessary plant protection vs. “acceptable damage” to bees. The commercial beekeepers are clearly letting the EPA know of the extent of their losses due to pesticides.
I want to also be clear that we should all be appreciative of the hard work done by the NGO’s (overzealous or not) and especially by those beekeepers who, at considerable personal expense, donate their time toward the benefit of our industry by lobbying the regulators to pay attention to our very real issues.
Last minute update:
As I was getting ready to send this article off to press, the EPA denied the recent petition requesting emergency suspension of clothianidin based on imminent hazard, stating in its response:
“Based on the data, literature, and incidents cited in the petition and otherwise available to the Office of Pesticide Programs, the EPA does not find there currently is evidence adequate to demonstrate an imminent and substantial likelihood of serious harm occurring to bees and other pollinators from the use of clothianidin.” 41
You can read the technical supporting documents yourself. 42 I do not for a moment doubt the earnestness of the petitioners, but I found that the EPA interpreted the research exactly as I have, and concur that there was simply not enough evidence (to date) that clothianidin poses a major threat to bees, beekeeping, or pollinators in general.
1 Entine, J (2011) Scared Death: How Chemophobia Threatens Public Health. http://www.acsh.org/include/docFormat_list.asp?docRecNo=1133&docType=0
2 July ABJ
3 Credit to Entine (2010) op. cit.
4 Tomizawa, M and JE Casida (2009) Molecular recognition of neonicotinoid insecticides: the determinants of life or death. Acc. Chem. Res. 42(2): 260–269.
5 Pimentel, D. 2001. Environmental effects of pesticides on public health, birds and other organisms. Rachel Carson and the Conservation Movement: Past Present and Future. Conference presented 10–12 August 2001, Shepherdstown, W.V. http://rachels-carson-of-today.blogspot.com/2011/02/environmental-effects-of-pesticides-on.html
6 Munkvold, G (2006) Seed Treatment http://www.extension.iastate.edu/Publications/CS16.pdf
7 Decourtye and Devillers (2010) Ecotoxicity of Neonicotinoid Insecticides to Bees. In, Insect Nicotinic Acetylcholine Receptors, Advances in Experimental Medicine and Biology 683: 85-95, DOI: 10.1007/978-1-4419-6445-8_8.
8 Ramakrishnan, R (1999) Imidacloprid-enhanced Reticulitermes flavipes (Kollar) (Isoptera: Rhinotermitidae) susceptibility to the entomopathogen Metarhizium anisopliae (Metsch.) Sorokin. J. Econ. Entomol 92:1125–1132.
9 Peters, J M (1967). Factors affecting caffeine toxicity: a review of the literature. The Journal of Clinical Pharmacology and the Journal of New Drugs (7): 131–141
10 Suchail, S, et al (2004a) Metabolism of imidacloprid in Apis mellifera. Pest Manag Sci 60:291-296
11 Suchail, S, et al (2004b) In vivo distribution and metabolisation of 14C-imidacloprid in different compartments of Apis mellifera L. Pest Manag Sci 60(11):1056-62 (2004b).
12 Tennekes HA. The significance of the Druckrey-Küpfmüller equation for risk assessment–the toxicity of neonicotinoid insecticides to arthropods is reinforced by exposure time. Toxicology 276(1):1-4.
13 Dr. John Casida, pers comm
14 Faucon, J-P, et al (2005) Experimental study on the toxicity of imidacloprid given in syrup to honey bee (Apis mellifera) colonies. Pest Manag Sci 61:111–125.
15 Are bees addicted to caffeine and nicotine?.ScienceDaily. Retrieved February 8, 2011, from http://www.sciencedaily.com/releases/2010/02/100210101504.htm
16 Lodesani, M, et al (2009) Effects of coated maize seed on honey bees: Effects on the brood. http://www.cra-api.it/online/immagini/Apenet_2009_eng.pdf
17 Lodesani, Marco, pers comm
18 Hatjina, F and T Dogaroglu (2010) Imidacloprid effect on honey bees under laboratory conditions using hoarding cages. http://www.coloss.org/publications/proceedings_workshop_bologna_2010
19 Lu,C, KM Warchol, RA Callahan (2012) In situ replication of honey bee colony collapse disorder. Bulletin of Insectology 65 (1): 99-106.
20 Dively, GP, Kamel A (2012) Insecticide residues in pollen and nectar of a cucurbit crop and their potential exposure to pollinators. J Agric Food Chem. 60: 4449–4456.
21 Stoner KA and BD Eitzer (2012) movement of soil-applied imidacloprid and thiamethoxam into nectar and pollen of squash (Cucurbita pepo). PLoS ONE 7(6): e39114. doi:10.1371/journal.pone.0039114
23 Bonmatin, JM, et al (2005) Quantification of imidacloprid uptake in maize crops. J. Agr. Food Chem. 53: 5336-5341.
24 Stadler T, et al (2003) Long-term toxicity assessment of imidacloprid to evaluate side effects on honey bees exposed to treated sunflower in Argentina, Bull Insect 2003; 56:77-81.
25 Dittbrenner, N, et al (2011) Assessment of short and long-term effects of imidacloprid on the burrowing behaviour of two earthworm species (Aporrectodea caliginosa and Lumbricus terrestris) by using 2D and 3D post-exposure techniques. Chemosphere 84(10): 1349–1355.
26 Albajes R, López C, Pons X (2003) Predatory fauna in cornfields and response to imidacloprid seed treatment. J Econ Entomol. 96(6):1805-13.
27 Jody Johnson (2011 ABRC)
28 Krischik,VA, AI Landmark, and GE. Heimpel (2007) Soil-Applied Imidacloprid Is Translocated to Nectar and Kills Nectar-Feeding Anagyrus pseudococci (Girault) (Hymenoptera: Encyrtidae). Environ. Entomol. 36(5): 1238-1245.
30 Dively, GP, et al (2010) Sublethal and synergistic effects of pesticides http://agresearch.umd.edu/recs/WREC/files/2010Programs/EASSubletha%20Effects2010.pdf
31 Creswell, Desneux, and vanEngelsdorp (2012) Dietary traces of neonicotinoid pesticides as a cause of population declines in honey bees: an evaluation by Hill’s epidemiological criteria. Pest Management Science 68(6): 819–827
32 Bonmatin (2005) Op. cit.
33 Nguyen BK, et al (2009) Does imidacloprid seed-treated maize have an impact on honey bee mortality? J Econ Entomol 102:616–623.
34 The Beekeepers Quarterly June 2012 (U.K.) Neonicotinoids—Our toxic countryside http://www.boerenlandvogels.nl/sites/default/files/BKQ%20108%20-%20Neonicotinoid%20Pesticides_0.pdf
36 Entine, op. cit.
39 Bahlai, CA, et al (2010) Choosing organic pesticides over synthetic pesticides may not effectively mitigate environmental risk in soybeans. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0011250
41 Response to petition http://www.regulations.gov/#!documentDetail;D=EPA-HQ-OPP-2012-0334-0006
42 Technical supporting documents http://www.regulations.gov/#!documentDetail;D=EPA-HQ-OPP-2012-0334-0012