A Review of Dr. Lu’s paper on neonics in Massachusetts
A Review of Dr. Lu’s paper on neonics in Massachusetts
By Randy Oliver ScientificBeekeeping.com
August 18, 2015
I was recently asked by a couple of extension horticulturalists to comment on Dr. Alex Lu’s most recent publication on the neonicotinoid insecticides. I hesitated to do so, since Dr. Lu feels that I’ve picked on him. But since his papers carry the prestige of the Harvard name (and will thus grant him unwarranted attention from the media), I felt compelled to give it an honest review. But first let me explain why I go to the effort.
I’ve been an environmental activist since my teens, and am happy to see the progress that we’ve made since then. Our air and water are cleaner, and society’s environmental consciousness is at an all time high. That said, there is still much work to be done in reducing humanity’s negative impact upon the Earth’s environment. We still need watchdogs and activists to monitor our business and personal activities that may be contributing to environmental and health problems, and I applaud such watchdogs and activists for doing so.
But doing so also confers a responsibility not to exaggerate the facts, nor to unduly alarm the public, mislead the media, or to foment fear for fundraising purposes. Unfortunately, when I became involved in the politics of beekeeping I quickly learned how the media, in their quest for sensational stories, pander to activists and advocacy groups that are guilty of all the above. The public, which is unfortunately largely scientifically illiterate, then swallows these compelling false narratives hook, line, and sinker, leading well-intentioned folk to make poor judgments (such as going on low-fat diets, not vaccinating their kids, or worrying about the wrong things). Even worse, their misdirected activism subsequently leads to protests and public pressure on our representatives to “do something” about a problem that may be greatly exaggerated, and directs our energies away from more important environmental concerns.
Practical application: each of us can only devote a limited amount of our time towards constructive environmental activism. Such activism should thus be based upon sound science and rational discussion. To that end, I’ve attempted to objectively review the neonics in such a manner [].
Fear of Pesticides
Prior to World War II, farmers commonly used truly dangerous insecticides such as lead arsenate and nicotine to control pests. Then when the first synthetic insecticides were introduced, they were heralded as miracles—DDT was nearly nontoxic to humans, but wiped out mosquitoes, lice, and many other insect pests. But then Rachel Carson brought to our attention that we had not foreseen that the organochlorines not only did not degrade in the environment, but actually bioaccumulated, culminating in the devastation of some raptor and pelican populations.
Important fact: the neonics are not DDT. They don’t bioaccumulate, nor do they appear to build up in the soil to any appreciable extent despite repeated use [].
This, and the Big Tobacco debacle, left the public with the impression that our regulators are not to be trusted. In reality, the newly-founded EPA did indeed take those lessons to heart, and now does a great job of following its mandate to use the best science to carefully regulate pesticides to avoid “unreasonable risk to man or the environment.” What we need to keep in mind is that the EPA must attempt to find that difficult balance between our society’s demand for cheap, cosmetically-perfect food, versus the obvious negative effects of pesticides upon the environment (while worrying that a Republican-controlled Congress may cut its budget).
The problem is that for the foreseeable future, agriculture (conventional or organic) is going to require some use of pesticides in order to produce enough food for our burgeoning human population. The question then, is to figure out which pesticides should be allowed, and which restricted. These decisions are best based upon sound science, not misinformed activism.
Riding on Harvard’s Name
In recent years, the bee research community was surprised to see publications by a Dr. Alex Lu, an Associate Professor of Environmental Exposure Biology at Harvard Medical School. Why in the world, we wondered, was a medical researcher without any background with bees attempting to perform bee research? His biography may give us a clue: “Alex’s research focuses on understanding how ecological and human health are being affected by the pervasive presence of chemicals in the environment [].”
I applaud Dr. Lu on his bringing his concern to our attention, since human health is his field of expertise. Unfortunately, bee biology is not. Yet Dr. Lu seems determined to convince us that the neonicotinoid insecticides are both the cause of elevated honey bee colony mortality, as well as being a threat to human health, which due to the sensationalism of the subject, has made him a darling of the media. But for anyone with a good understanding of bee biology and the running of field trials, his papers tend to be sadly amusing; unfortunately, the press loves to trumpet his widely discredited “findings” as fact.
To his credit, Lu’s papers have improved over the years (perhaps in response to my critical reviews). But his latest paper, Distributions of neonicotinoid insecticides in the Commonwealth of Massachusetts: a temporal and spatial variation analysis for pollen and honey samples [], still follows his pattern. Dr. Lu is a man on a mission—to get us to fear the neonicotinoid insecticides—which comes as a surprise to the EPA, whose risk assessors consider them to be “reduced risk” products to both man and the environment, replacing the more harmful organochlorines and carbamates, and the failing pyrethroids.
Before I go any further, allow me to clearly state that I have no beef with Dr. Lu, I’m sure that he is a fine scientist and human being, and thank him for investigating any adverse effects of neonics upon humans. My problem is not with him personally, but rather with any scientific publications based upon sloppy science, or that play loose with facts and interpretation; and especially those that are announced at press conferences prior to publication in order to promote the authors’ agenda in the media.
Alarmism vs. Good Science
Lu makes the claims that neonic residues are causing honey bee colony collapse, killing birds and other wildlife, and possibly causing neurotoxicity in developing mammalian brains []. The above claims are cause for serious concern, and call for deeper investigation, which I’ve done. What I found was that each of the claims was speculative and only weakly substantiated.
- No credible evidence has ever been found to support the hypothesis that neonics are the cause of CCD; plenty of researchers have tried to do so, but none have been successful. On the other hand, plenty of beekeepers report good colony health in regions of high-neonic use [].
- And there is scant evidence that they are of harm to birds [], and actually appear to be a major improvement over previously-used insecticides [].
At this point allow me to make clear that I believe that our agricultural system is far too dependent upon pesticides, and that no insecticide is without fault. Neonic planting dust from corn seeding is sometimes a serious problem for pollinators. Neonics also appear to be more of an issue for some pollinators (such as bumblebees and mason bees) than to honey bees. And there is suggestive evidence that neonics may be involved in premature queen failure and immune suppression. I’d be the last person to argue that neonics are harmless. Insecticides by definition kill insects. Ideally, any registered use of an insecticide will provide the most targeted impact on the pest(s), with the least collateral damage to other species.
That said, let’s look into Lu’s claim that that neonics might cause neurotoxicity in the developing brains of humans. Again, I’d sincerely like to thank Dr. Lu for being a watchdog for our health. In another paper [], he states:
In light of new reports of toxicological effects in mammals, the results strengthen the importance of assessing dietary neonicotinoid intakes and the potential human health effects.
The mention of these “new reports” got my attention, so I read further. He actually cites only a single in vitro (test tube) study [] on the action of neonics on human neurons (which did not even mention toxicity); this is a good example of how Dr. Lu creatively extrapolates others’ findings.
Lu, as a toxicologist, fully understands that risk is the product of hazard (toxicity) times exposure. In order for a neonic to be a risk to the developing brain, the person must first consume in excess of a defined amount of the chemical via residues in food, the chemical must then pass through the blood-brain barrier, and then it must actually cause a negative effect in the brain itself.
So let’s then look into each of these conditions in turn, in order to see whether there is data to back up Lu’s dogma.
EXPOSURE THROUGH FOOD
Our first question should be, is it realistic for a person to consume enough residues of neonics to be of concern? In order to answer that question, we first need to know the NOAEL (No Observable Adverse Effects Level) of the chemical, as determined from long-term feeding studies of surrogate animals [,,]. For imidacloprid in rats, mice, rabbits, and dogs, this was found to be around 10 mg/kg/day. The EPA, heeding the precautionary principle, then goes much further, and sets the chronic dietary reference dose for humans nearly 200x lower–at 0.057 mg/kg/day.
I understand that the above figures are gobbledygook to most readers, so let me put them into understandable (and personal) terms. I love apples, and eat at least two a day. Could I be poisoning myself with neonics? As luck would have it, Lu himself conveniently supplies us with analyses of seven different apple cultivars [], for which residues of imidacloprid averaged less than 1 ppb.
So how many neonic-tainted apples would I need to consume in a day in order to approach the extremely conservative “safe” level of exposure as determined by the EPA? I of course did the math []. Result? I’d need to eat nearly 10,000 pounds of apples a day to approach any level of concern.
GETTING THROUGH THE BLOOD-BRAIN BARRIER
OK, so let’s say that I was really craving apples, and managed to consume 10,000 pounds today. Some of the imidacloprid residues would be absorbed through my gut; but could they then make it through my blood-brain barrier (which our body uses to protect ourselves from dietary neurotoxins)? Lu sounds the alarm that:
Neonicotinoids and some of their metabolites are also shown to be able to pass through the blood-brain barrier in mouse, and some metabolites having enhanced potency to nAChR are even more toxic than their parent compounds [].
This surprised me, so I checked his reference. As Lu has a habit of doing, he distorted the findings of others. For example, he ignored the authors’ finding that:
Brain levels of 3–16 ppm can be achieved without obvious poisoning signs.
Now keep in mind that 3-16 ppm is equivalent to 3000-16,000 ppb directly in the brain, yet still no obvious toxicity! Lu also neglected to say that these levels were only obtained by the researchers intentionally adding a second solvent (DMSO) in order to help the insecticide to pass through the blood-brain barrier. In fact, one of the attractions of the neonics is that they only penetrate the mammalian blood brain barrier to a very limited extent.
Practical application: it is actually difficult to intentionally poison oneself by drinking imidacloprid straight up []. This simple fact alone speaks volumes about how little we should be concerned about neonic toxicity to humans, relative to the alternatives [].
The other thing that Lu does is to raise our concern about the metabolites that are of increased toxicity, but as a toxicologist, he should also explain that overall toxicity of the metabolites would not exceed that of the parent compound as a whole. I find this sort of intentional omission to be both misleading and indefensible.
CITED EFFECT UPON THE BRAIN
Despite the evidence so far that I really didn’t need to worry about unintentionally poisoning myself with neonics, I was still concerned about Lu’s suggestion [] of the “possible neurotoxicity in developing mammalian brain.”
I certainly don’t want my grandkids to develop brain abnormalities from consuming neonic-tainted produce. So I dug a bit deeper into the cited study. What the researchers had actually demonstrated was that when neuronal cells in a petri dish were directly flooded with a 1μM solution of imidacloprid, that they fired similarly to those exposed to the same concentration of nicotine, but took a bit longer to recover. The authors didn’t even mention neurotoxicity.
And just how strong is a 1μM concentration? It works out to 256 ppb actual exposure to the neurons. Compare this to the typical concentration of imidacloprid residues in apples of less than 1 ppb [], and the tiny amount that would ever make it through the blood-brain barrier. Why the researchers used such an unrealistically high concentration of imidacloprid is beyond me. It would have been scientifically prudent for them to continue to reduce the dose to determine the NOAEL at which the neurons no longer exhibited any excitation.
Practical application: scientists perform in vitro (“test tube”) experiments to screen for potential health effects; real life application can only be determined by in vivo testing on live animals (generally lab rats as surrogates for humans), testing on human volunteers, or from the effects of accidental (or intentional) poisonings.
So I continued my literature search for such in vivo studies (which are also what the EPA focuses upon). What I found distressing is that the titles of scientific papers again tend to sensationalize their findings. For example, Duzguner [] showed “acute oxidant and inflammatory effects of imidacloprid on the mammalian central nervous system.” But he did so by injecting ¾ of the lethal dose (26,000 ppb by my calcs, along with DMSO penetrant) into rats. I question the relevance of such studies to the sort of actual exposure to humans that humans would get from eating produce with residues of insecticides.
Practical application: if you are a young scientist wanting to get your paper widely cited in order to improve your advancement and funding, all you need to do is to include the word “neonicotinoid” in the title, and then speculate in the abstract that there could conceivably be some effect upon human health, and the media will trumpet your name across the globe.
Due to Lu’s association with the name “Harvard,” his efforts at scientific research gain far more attention than they deserve. Indeed, he comes off more as a showman than a scientist (as evidenced by his latest publicity stunt of analyzing the food served to Congress in order to claim that the traces of neonics found in their produce were cause for concern). His “research” so far may be politically provocative, but unfortunately, for all practical purposes, irrelevant to meaningful discussion of the neonics.
Perhaps we can better put things into perspective by returning to our neonic-poisoned congresspersons, many of whom smoke cigarettes (if not something else). The nicotine in cigarettes is roughly 100 times as toxic to mammals as is imidacloprid. When a congressperson smokes a cigarette, their blood concentration of nicotine goes to about 12 ppb []. To match that toxicity by the consumption of apples, a congressperson would need to consume at least 1200 times his/her body weight in apples in one sitting (and repeat that performance for the next cigarette). It seems to me that the members of Congress should be more concerned about secondhand smoke than with the produce on their table.
At this point in my research, and being a nontoxicologist, I was getting frustrated by trying to get at the truth of the matter. So I searched for the most conservative opinion by actual toxicologists that I could think of. The most precautionary assessment would likely be that from the European Union’s EFSA (analogous to our EPA), the members of which go out of their way to cover their butts to appease the European anti-neonic activists. These learned toxicologists concluded that []:
As the current ARfD and AOEL [] for imidacloprid may not be protective enough for potential developmental neurotoxicity of this active substance, the Panel also recommends to conservatively lower these reference values to the same level as the ADI (0.06 mg/kg bw per day) [emphasis mine].
In case your brain is already fogging over with numbers, that’s the same figure used by the EPA (and that which I used to calculate the 10,000-pound dose of apples that you’d need to consume a day).
I’m as concerned as anyone about being exposed to pesticides, and especially about unforeseen effects upon my health, or the developing brains of my grandkids (or our congressmen). However, contrary to Lu’s alarmism about the neonics, any objective review of research to date would suggest little cause for fear. All the evidence that I’ve seen to date concur with the EPA’s assessment that neonics are indeed reduced risk insecticides, so far as humans are concerned, and it appears highly unlikely that the amount in produce is likely to harm you in any way.
So let’s now return to Lu’s current paper, in which he sticks to neonic residues in pollen and honey, which are likely more relevant to the diet of bees than to humans. Unlike humans, some insects exhibit behavioral effects from neonics at concentrations as low as a few ppb. So this study had the potential to determine whether neonic residues in pollen affected colony health. Alas, Lu did not bother to do so; instead he used his state of the art equipment essentially to show off that he could detect residues of neonics in the vanishingly small parts per trillion—levels likely of biological irrelevance.
Lu’s Current Paper
In a typical scientific paper, the author proposes a testable hypothesis (in this case, that neonics are present in the environmental at a level that is causing health problems to bees and humans), then designs an experiment to test that hypothesis (in this case by measuring levels of neonic residues in honey and pollen), and then seeing whether the results of the experiment either support or refute his hypothesis (by seeing whether there was a correlation between neonic exposure and colony performance).
But Lu’s study was not a test of a hypothesis, but rather an extremely informal survey for neonic residues in bee-collected pollen (due to his anti-neonic tunnel vision, he didn’t bother to analyze for any other pesticides). The paper starts off on shaky ground by referring to an excellent paper by Mullin, and points out that neonics were previously found in beebread samples. But what he doesn’t mention was that no neonic was found in more than 5% of Mullin’s samples, refuting his next claim that:
Neonicotinoid insecticides, in particular imidacloprid and clothianidin, have long been implicated and recently shown complicit in honeybee colony collapse disorder (CCD).
Given the weight of evidence, chronic exposure to imidacloprid at the higher range of field doses (20 to 100 μg/kg) in pollen of certain treated crops could cause negative impacts on honey bee colony health and reduced overwintering success, but the most likely encountered high range of field doses relevant for seed-treated crops (5 μg/kg) had negligible effects on colony health and are unlikely a sole cause of colony declines.
Lu further goes on to claim that:
No study has yet been published that demonstrates the prevalence of neonicotinoids in the environment where bees are foraging to elucidate the temporal and spatial variations of neonicotinoids in pollen.
While perhaps technically true, numerous researchers have been tracking pesticide residues in pollen since the early 2000’s [].
Technicalities and Details
We all want scientific papers to be technically accurate. One expects any scientific paper to be thoroughly reviewed by other peer experts for accuracy in technical details, and reasonality in its conclusions. Don’t count on this for Lu’s work. For example, he includes flonicamid as a neonicotinoid, although its mode of action is completely different—it does not target the same nAChR neuronal receptors []. As explained by another researcher [],
Flonicamid has no effect on the nAChR and according to both the IRAC and the EPA, flonicamid is not a neonicotinoid by classification or mode of action.
the “rpf” of residues
Lu goes on to calculate the “relative potency factor” for combinations of neonic residues, but the information that he used to calculate those factors frustratingly cannot be found at the cited source, and he didn’t bother to state whether the toxicity values were calculated for rats or for bees (critical, since neonics are vastly more toxic to insects). Without such information, his RPFvalues are nearly meaningless. It appears, based upon the values, that he used mammalian toxicities, which would be misleading if applied to honey bees.
Why the Different Results?
One may wonder why Lu’s team manages to detect a greater prevalence of neonic residues than other researchers, such as the huge data sets for produce by the USDA [], or by bee researchers []. The reason appears to be that the Chen lab is comfortable with the accuracy of their “sensitive and modified LC-MS/MS method along with the QuEChERS procedure to simultaneously measure 8 neonicotinoid residues” [].
Unlike other labs, which detect neonics at the ppb level, Chen’s lab claims to set their level of quantification in the parts per trillion.
Lu’s methodology is explained in great detail in some areas, but to my untrained eye seemed to be lacking in other critical aspects; so I asked two experts in the field for their opinions. They pointed out that pesticide residue analysis is complicated and difficult–that’s why it costs so much. Lu described the easy part in the paper. What he didn’t detail were the difficult parts–his quantification and quality control of the mass spectrometry. This is critical, since there are many things that must be carefully controlled in order to maintain precision and accuracy in residue analysis. As one reviewer explained:
[Lu] describes the LC program well that was used for the analyte separations but doesn’t say what parent and product ions he screened for each compound or any information at all about standard reference materials that were used for identification and quantification. Did he use matrix matched standards? How many levels in his calibration curves? Is the method validated/verified? What were the analyte recoveries? Is his lab accredited? Does he participate in a third party proficiency sample program that would lend credibility to his residue analysis? Does his lab have a Quality Management System? There are a lot of ways for a lab to demonstrate competency and proficiency, but none were referenced in this paper.
But let’s give Dr. Lu the benefit of the doubt and accept his residue results at face value. What I’m more concerned about are his interpretations of the scientific literature as he attempts to put his results into perspective.
For example, one of Lu’s claims caught my attention:
A comparable study has demonstrated that bees living and foraging near cornfields in Indiana are being exposed to neonicotinoids…When maize plants reached anthesis [tasseling], maize pollen that was collected directly from bees using a pollen trap from treated seed was found to contain clothianidin and thiamethoxam, ranging from non-detectable to 88 [ppb] and non-detectable to 7.4 [ppb]respectively.
The 88 ppb level in the pollen of seed-treated corn was nearly 50x higher that any measurement that I’d previously seen. How could I have missed this? So I reread the study that he cited []. It seems that Dr. Lu has trouble in understanding scientific papers, since the 88 ppb figure was from bee-collected pollen from flowers on July 10, not from the pollen of seed-treated corn, which measured at only 3.9 ppb clothianidin. Dr. Lu’s misrepresentations of the scientific literature makes his work an embarrassment to other researchers.
Lu further stretches credibility by then stating:
In brief, honeybees exposed to imidacloprid or clothianidin at levels ranging from 0.5 to 30 ppb…could lead to CCD, a systematic disease still lingering in many countries after its first occurrence in the winter of 2005–2006.
In the first place, signs of CCD were already common in the winter of 2004-2005. In the second place, there is no such thing as a “systematic disease,” and CCD is a disorder, not a disease. You’d think that a researcher from the Harvard Medical School (or his reviewers) would understand disease terminology. And then Lu’s very own previous research [] contradicts his statement, since in his 2012 paper, it was obvious that there was no apparent effect from feeding colonies syrup spiked with up to 20 ppb of imidacloprid. So he has zero supporting evidence for his claim that a dose 40x lower could cause CCD. On a roll, Lu continues:
Sub-lethal exposure to acetamiprid, imidacloprid, clothianidin, dinotefuran, fipronil, thiacloprid or thiamethoxam could lead to developmental impairments, including poor colony growth at levels of 2–5 ppb.
I again have no idea as to how Lu could make this claim. The two citations that he uses to support the claim did not involve any neonic other than imidacloprid, so he can’t legitimately mention any others. And as far as claiming poor colony growth at 2-5 ppb, in the two cited studies, colony growth between the treated and control colonies was identical at up to 20 ppb in the first study, and identical at 135 ppb in the second. These sorts of contradictory and unsupported claims are simply unacceptable in a scientific paper.
To Lu’s credit, he was able to come to some coherent conclusions, for example:
Lastly, the use of the LOAEL as the basis of calculating imidaclopridRPF may be a reasonable approach for estimating the aggregate neonicotinoid exposure by pollen ingestion, but one should be cautious when interpreting the cumulative risks in bees.
Yes, a neonic RPF would be a reasonable approach, if one leaves chemicals with dissimilar modes of action (such as flonicamid) out of the equation (and uses values for bees, not mammals). And yes, one should be extremely cautious about interpreting the cumulative risk (especially if you screw up the basic assumptions in the first place). It would have been of far greater interest had Lu had taken the time to identify the pollens associated with the few unusually high detects of neonics in his samples. But then Lu returns to his deductive logic of putting the cart before the horse:
Considering various sublethal effects of neonicotinoids on bees, it is prudent to identify ways to reduce the uses of neonicotinoids in order to reverse the deteriorating trends in honeybee health and the declining numbers of honeybee colonies.
Yes, it would indeed be prudent to reduce the uses of all pesticides! But Lu ignores the plain fact that the trend for honey bee health has improved greatly in recent years (provided that beekeepers manage varroa), and that the numbers of colonies are hardly declining, but rather increasing [].
relevance of the results
If we give Lu the benefit of the doubt that his methodology was valid, his results indicate that traces of neonics can be commonly detected in pollen and honey samples from Massachusetts. This comes as no surprise to anyone who has checked the pest control product shelves in any hardware or garden store, and Lu rightly concludes that:
The ubiquity of neonicotinoids in states such as Massachusetts where the planting of neonicotinoid-treated crops only represents a very small fraction of overall agricultural activities suggests that non-agricultural uses of neonicotinoids is likely the main contribution to the levels found in pollen and honey that bees brought back to their hives.
Of interest is that in some honey samples, levels of dinetefuran or imidacloprid reached nearly 15 ppb (of no concern to humans, since few people consume honey by the gallon in a day). Such levels are not consistent with agricultural applications, suggesting that it is homeowner or landscape applications that are putting that much insecticide into the nectar—I agree that this is cause for concern regarding pollinators. Unfortunately, Lu didn’t take the obvious step of then performing pollen analysis of those honey samples, which may have indicated from which floral sources that tainted nectar came—data which would have been of interest to the EPA.
As far honey bees are concerned, I must take issue with Lu’s exaggerated claim that:
The levels of neonicotinoids that we measured in pollen samples have significant implications for honeybee health.
One should look at his Figure 4, which clearly shows just how negligible most of those residues were. In only 6 of 45 monthly samples did residues exceed 2 ppb, with the highest being roughly 5 ppb. Based upon numerous studies, and summarized by Dively, levels of neonics in the range of 5 ppb have negligible effect upon honey bee colonies (although other pollinators may be affected at that level).
What troubles me is that Lu’s agenda appears to be to circumvent the EPA, and instead use the media to put pressure on Congress to ban the neonics, despite the fact that EPA’s registration of neonic products has allowed us to greatly reduce our exposure to the more harmful organophosphate and carbamate insecticides. I’d much rather see Dr. Lu use his training and talents to help collect data that might be usable by the EPA.
The Need for Good Science
I appreciate that Dr. Lu is acting on his convictions, but I’d rather that he do so honestly and based upon sound science. He is exhibiting a classic case of deductive reasoning—prior to any research, he came to the conclusion that neonics are bad, so he deduces that there must be an effect on bees and human health. Such erroneous logic is anathema to science, which instead uses inductive reasoning—coming to conclusions only after careful observation, extensive testing of hypotheses, and the collection of supportive data. Lu’s data do not support his hypotheses, yet he continues to stick with his preconceived agenda.
Although I fault Dr. Lu for the above, the real responsibility lies with others. We trust the editors and referees of scientific papers to recognize errors and reject papers not suitable for publication. Every one of the egregious errors that I’ve pointed out in Lu’s papers should have been caught by his reviewers and been corrected, or been cause for the paper to be rejected for publication—this is their duty to the scientific community and the public. I’m appalled that a trusted institution such as Harvard allows its name to be associated with examples of science at its worst. And how about our media, who stoop to tabloid sensationalism by uncritically parroting this sort of unscientific nonsense upon an unsuspecting public?
Data vs. Dogma
We have a regulatory mechanism in place to assess the risks of pesticides. The EPA is tasked with a job that is guaranteed to never please everyone. However, I speak with its risk assessors regularly, and feel that they are indeed basing their decisions on the best available data.
The public debate about pesticides is a good thing. We need to keep pressure on industry and the regulators. But we need to do so with solid supporting evidence—good scientific data that tells us where there are truly issues that need to be addressed. Researchers such as Dr. Lu are in a position to test for adverse effects, and to supply such needed data to the EPA. Wild unsubstantiated claims only confuse the issue. Speaking of such, Dr. Lu showed his true colors by saving one for the press conference held for the release of his paper.
Risk to Humans via Pollen?
Although Lu’s findings confirmed that neonics were sometimes present in pollen at extremely low levels, in his press release [] he used the Harvard name to promote the preposterous claim that those minuscule residues “may pose health risks for people inhaling neonicotinoid-contaminated pollen.” Such knowing contortion of science is a deplorable use of the Harvard press office.
In the first place, Lu’s study had absolutely nothing to do with the airborne pollens that we inhale—he collected only the typically sticky pollens gathered by bees. But let’s do the math anyway. Worst-case exposure to pollen grains is in the order of less than 10,000 grains per day []. For neonic-treated corn, there are around 3000 pollen grains per milligram [], and median neonic residues of hand-collected pollen is about 2.8 ppb []. This works out a 170-lb person inhaling at worst 0.0000000001 mg/kg body weight/day of neonic residues. Compare that figure to the conservative safe intake of 0.06 mg/kg, which works out to you’d need to inhale tainted corn pollen every day for million years straight in order to meet even one day’s level of concern. As a medical researcher and “expert” on pesticides and toxicology, Dr. Lu knows full well how to do calculations such as the one above. I find it inexcusable for a Harvard scientist to promulgate clearly unwarranted fear in a trusting public.
Practical application: I’m as concerned about the impacts of pesticides upon the environment and human health as is anyone, and I submit formal comments (backed by good science) to the EPA detailing specific issues. On the other hand, I find the gratuitous fomenting of fear in a concerned public by a medical researcher of Dr. Lu’s stature to be reprehensible, and an embarrassment to the Harvard institution. Lu could benefit by the example of the Harvard students who recently published an excellent review on GMOs and our food [].
Practical Application to Beekeepers
You can decide for yourself, but if I were a resident of Massachusetts, I’d continue to eat commercial apples without undue fear (and inhale deeply as I do so). And as far as the bees, despite Lu’s unshakeable belief that the major bee problem is neonics, for some reason in this study he did not to attempt to link cause and effect. I cannot fathom why he did not ask his cooperating beekeepers to additionally record colony health, productivity, or survivorship, so that he could have told us whether there was any correlation between neonic exposure and colony performance []—data which would have been of far more interest than the colorful graphics in the paper.
Nor did he make the effort to determine the sources of neonic contamination in nectar or pollen, which he could have easily done by simple microscopic analysis, and which would have had great practical application. I implore Dr. Lu, should he continue his studies on neonics, to consult with experts who can help him to better design his experiments or surveys, so that his results will be meaningful to beekeepers, the public, and our regulators.
In conclusion, I’m no salesman for any pesticide, and am concerned about the general overuse, and some specific uses of the neonics. But I realize that growers are going to protect their crops. I’d like the products used to be regulated based upon good science, rather than showmanship. I urge the reader to review three recent well designed and executed studies on actual field exposure of bees to seed-treated canola or corn [], none of which found any effect from the neonic residues in the pollen and nectar upon foraging, orientation, colony performance, or survival.
In the spirit of my review, if any reader finds even a single error in fact or interpretation in this article, I will be glad to correct it here.
The full citation for the paper is: “Distributions of neonicotinoid insecticides in the Commonwealth of Massachusetts: a temporal and spatial variation analysis for pollen and honey samples,” Chensheng (Alex) Lu, Chi-Hsuan Chang, Lin Tao and Mei Chen, Journal of Environmental Chemistry, online July 23, 2015, doi: 10.1071/EN15064
One researcher points out that “CCD is, by definition, a new name for an old disorder,” and suggested that I cite the source for the term “CCD”: http://www.beekeeping.com/articles/us/ccd.pdf
Correction: Dr. Lu is an associate professor of environmental exposure biology in the Department of Environmental Health at the Harvard T.H. Chan School of Public Health.
Aug 28–I’ve now received a large amount of positive feedback for this review from other bee researchers; most of whom, out of professional courtesy, are hesitant to publicly criticize other scientists. I wrote the review as a call to action for scientists and editors to start cleaning up their act before the public loses all faith in the integrity of science. I hope that it makes a difference.
Notes and Citations
 Whiting, SA, et al (2014) A multi-year field study to evaluate the environmental fate and agronomic effects of insecticide mixtures. Science of the Total Environment 497–498: 534–542. (See Fig. 2).
Jones, A, et al (2014) Neonicotinoid concentrations in arable soils after seed treatment applications in preceding years. Pest Management Science 70(12): 1780–1784.
 Lu, C, et al (2015) in Environ. Chem. http://dx.doi.org/10.1071/EN15064
 citing Kimura-Kuroda J, et al (2012) Nicotine-like effects of the neonicotinoid insecticides acetamiprid and imidacloprid on cerebellar neurons from neonatal rats. PLoS ONE 7(2): e32432.
 Chen, M, L Tao, J McLean, C Lu (2014) Quantitative analysis of neonicotinoid insecticide residues in foods: implication for dietary exposure. J. Agric. Food Chem. 62: 6082. doi:10.1021/JF501397M
 Kimura-Kuroda (2012) op cit.
 A 2-year feeding study in rats fed up to 1,800 ppm resulted in a No Observable Effect Level (NOEL) of 100 ppm. A 1-year feeding study in dogs fed up to 2,500 ppm resulted in a NOEL of 1,250 ppm http://extoxnet.orst.edu/pips/imidaclo.htm
 Researchers estimated the NOAEL at 14 mg/kg/day for rats. The chronic dietary reference dose (RfD) has been set at 0.057 mg/kg/day based on chronic toxicity and carcinogenicity studies using rats. http://npic.orst.edu/factsheets/imidacloprid.pdf
 Chen (2014) op cit.
|175||lbs my weight|
|79.54545||kg my weight|
|0.057||mg/kg/day EPA safe exposure level|
|4.534091||mg/day number of mg of imidacloprid that I can safely consume|
|0.004534||mg/day converted to grams/day|
|9987||lbs apples at 1ppb/day|
 Chen (2014), citing: Ford Kevin A. Ford and John E. Casida (2006) Chloropyridinyl neonicotinoid insecticides: diverse molecular substituents contribute to facile metabolism in mice. Chem. Res. Toxicol 19 (7): 944–951.
 Mohamed, F, et al. (2009) Acute human self-poisoning with imidacloprid compound: a neonicotinoid insecticide. PLoS ONE 4(4): e5127.
 For those interested in comparing the toxicity of other insecticides to that of the neonics, I suggest reading this great online lecture by Dr. Allan Felsot (see Tables 3 and 4):
 In Chen (2014) op cit.
 Chen (2014) op cit.
 Duzguner, V & S Erdogan (2010) Acute oxidant and inflammatory effects of imidacloprid on the mammalian central nervous system and liver in rats. Pesticide Biochemistry and Physiology 97(1):13–18.
 Digard, H, et al (2012) Determination of nicotine absorption from multiple tobacco products and nicotine gum. Nicotine Tob Res doi: 10.1093/ntr/nts123.
 The ARfD of a chemical is the estimate of a substance in food or drinking water, expressed on body weight basis, that can be ingested over a short period of time, usually during one meal or one day, without appreciable health risk to the consumer on the basis of all known facts at the time of evaluation. The AOEL is the Acceptable Operator Exposure Level.
 Carreck, NL,et al (2014) The dose makes the poison: have “field realistic” rates of exposure of bees to neonicotinoid insecticides been overestimated in laboratory studies? Journal of Apicultural Research Vol. 53(5): 607-614.
Cutler et al. (2014), A large-scale field study examining effects of exposure to clothianidin seed-treated canola on honey bee colony health, development, and overwintering success. PeerJ 2:e652; DOI 10.7717/peerj.652
Dively GP, Embrey MS, Kamel A, Hawthorne DJ, Pettis JS (2015) assessment of chronic sublethal effects of imidacloprid on honey bee colony health. PLoS ONE 10(3): e0118748. doi:10.1371/journal.pone.0118748
 Dively (2015) op cit.
 For example, the heroic efforts of Marie-Pierre Chauzat in France, Helen Thompson in Great Britain, Jim and Maryann Frazier and Chris Mullin in Pennsylvania, and Jeff Pettis and Dennis vanEngelsdorp in the U.S. in general (not to mention several others).
Chauzat, MP, et al (2006) A survey on pesticide residues in pollen loads collected by honey-bees (Apis mellifera) in France. Journal of Economic Entomology 99: 253-262.
Pettis JS, et al (2013) crop pollination exposes honey bees to pesticides which alters their susceptibility to the gut pathogen Nosema ceranae. PLoS ONE 8(7): e70182. doi:10.1371/journal.pone.0070182
 Nicotinic acetylcholine receptors. Both nicotine and neonicotinoids bind to these receptors and allow sodium ions to flood through, initiating an “action potential.” In layman’s terms, they are stimulants, and kill insects by overstimulating them.
 Whipple, SD (2015) Letter to the Editor regarding “Simultaneous determination of residues in pollen and high-fructose corn syrup from eight neonicotinoid insecticides by liquid chromatography–tandem mass spectrometry”. Anal Bioanal Chem 407:1273.
 For example:
Mullin, CA, M Frazier, JL Frazier, S Ashcraft, R Simonds, D Vanengelsdorp, JSS Pettis (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS One 5, e9754. doi:10.1371/JOURNAL.PONE.0009754.
Rennich, K, et al (2015) 2013-2014 National Honey Bee Pests and Diseases Survey Report. http://beeinformed.org/wp-content/uploads/2015/07/2013-2014-NHBS-Report.pdf
 Chen (2014) op cit.
 Krupke, CH, et al (2012) Multiple routes of pesticide exposure for honey bees living near agricultural
fields. PLoS One 2012, 7, e29268.
 Lu, C, et al (2012) In situ replication of honey bee colony collapse disorder. Bulletin of Insectology 65 (1): 99-106. Refer to his Fig. 1.
 Rosenberg, GL, et al (1983) Inhalation challenge with ragweed pollen in ragweed-sensitive asthmatics. Journal of Allergy and Clinical Immunology Volume 71 (3): 302–310.
 Dr. Jerry Bromenshenk (in press)
 Typically, other researchers who have done so, conclude that, as did Chauzat, “No statistical relationship was found between colony mortality and pesticide residues.”
Chauzat, MP, et al (2009) The influence of pesticide residues on honey bee (Hymenoptera: Apidae) colony health in France. Environmental Entomology 38: 514-523.
Chauzat, MP, et al (2010) A case control study and a survey on mortalities of honey bee colonies (Apis mellifera) in France during the winter of 2005-6. Journal of Apicultural Research 49(1): 40-51.
 Cutler, GC, et al. (2014) A large-scale field study examining effects of exposure to clothianidin seed-treated canola on honey bee colony health, development, and overwintering success. PeerJ 2:e652; DOI 10.7717/peerj.652
Pilling E, et al (2013) A four-year field program investigating long-term effects of repeated exposure of honey bee colonies to flowering crops treated with thiamethoxam. PLoS ONE 8(10): e77193.
Thompson, H, et al (2015) Thiamethoxam: assessing flight activity of honeybees foraging on treated oilseed rape using rfid technology. Environ Toxicol Chem., Accepted Article • DOI: 10.1002/etc.3183