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Sick Bees – Part 18F4: Colony Collapse Revisited – Environmental Toxins

First published in: American Bee Journal April 2013

Sick Bees Part 18f4: Colony Collapse Revisited

Environmental Toxins

First published in ABJ April 2013

Randy Oliver


New Chemicals in the Environment

Fear of Chemicals – It Ain’t Just Pesticides

Irrational Fear of “Chemicals”

Manmade Chemicals

General Environmental Pollutants

Natural Elements

Those Danged Bees!

Poor Colony Survival

Reality Check


References and Notes

Randy Oliver


I left off last month with the analogy of the bee colony being akin to a leaky boat needing to “bail out” (detoxify) numerous plant alleleochemicals.  Generally, they do a pretty good job at this.  But what if we now add more “leaks” in the form of manmade chemicals?


New Chemicals in the Environment

The modern era of chemical pest control began around the time of World War II, when the synthetic organic chemical industry began to develop. The first synthetic organic pesticides were organochlorine compounds, such as DDT.  At that time, DDT was considered to be a wonder of modern chemistry. It was cheap, knocked the snot out of insect pests, and appeared (at that time) to be relatively safe to humans. DDT and other organochlorine insecticides were widely used until scientists noticed that they were persisting in the environment (they did not readily degrade) and, more seriously, could bioaccumulate in birds, humans, and other animals. In 1962 Rachel Carson, in her book Silent Spring, introduced the term “ecosystem” to the general public, and kick started the environmental movement. As a result, the EPA was created in 1970 [1], which subsequently banned most of the organochlorine pesticides [2].

Up until Silent Spring, “chemicals” had a good name, synonymous with “progress” (Fig. 1).  The heyday of modern chemistry ran from WWII through the 1980’s, during which time the number of newly-created chemicals grew exponentially [3].

Figure 1.  Americans have gone from embracing “chemicals” to now being fearful of them.  Although I certainly wish to see chemical pollution of our air, water, and landscapes cleaned up, and am cautiously concerned about any manmade chemicals in my diet, I feel that public sentiment may have swung too far, based upon ignorance and unwarranted fear.

Chemists today have gone full circle, and now are at the forefront of analyzing and explaining how any pesticide or pollutant can affect health or ecosystems [4].  Unfortunately, the public confuses our newfound ability to detect chemicals in the parts per trillion with increased risk– a major misunderstanding which frustrates both toxicologists and the EPA risk assessors [5].

Scientific note: one thing that bugs me about studies on the sublethal effects of synthetic pesticides is that we have no perspective as to the degree of impact due the pesticide relative to the adverse effects of common plant alleleochemicals.  I’d like to see some benchmarking of a few common plant phytotoxins that could then be run as “positive controls.”

Fear of Chemicals—it ain’t just pesticides

We live in a society obsessed with fear.  These days you can’t even find a merry-go-round or jungle gym on a playground any more for fear that some child might get hurt while playing outdoors!  And in my chemical-phobic home state of California, every McDonalds and Starbucks are required by law to post warnings that French fries and coffee contain acrylamide–a lethal neurotoxin, carcinogen, and reproductive toxicant [6].  At the lumber yard, my receipt now warns me that:

 WARNING: Drilling, sawing, sanding or machining wood products generate wood dust, a substance known to the State of California to cause cancer.

For Pete’s sake, coffee, French fries, and sawdust are now considered to be “substances” that can cause cancer!  Heaven forbid that they ever get hold of my smoker!

Irrational Fear of “Chemicals”

The term “chemical” has become emotionally loaded.  In truth, there is nothing inherently good or bad about “chemicals”–everything that you can touch, taste, or smell is a chemical.  And as Paracelsus pointed out 500 years ago, “All things are poison, and nothing is without poison; only the dose permits something not to be poisonous.”

How about that proverbial grain (or teaspoon) of salt with which we should take the alarmists’ warnings?  Salt is an effective and nonspecific poison–1 tsp of salt is about 1/10 the lethal human dose [7]; salt is also mutagenic, can cause reproductive problems and muscular dysfunction.  Even water or oxygen can kill you if you consume too much.  It is all about the dose!

And don’t let multi-syllable names scare you.  Consider beta-dextro-fructofuranosyl-alpha-dextro-glucopyranoside.  This chemical is arguably the leading cause of preventable death in the U.S.–strongly linked to heart disease (the #1 cause of death), Type 2 diabetes, obesity, hypertension, colon cancer, and tooth decay [8], yet there are people who feed it to their children!  I’m sure that you’ve figured out its common name by now—table sugar.

Manmade Chemicals

I’m going to get back to pesticides soon, but first we should realize that our ecosystem is full of plenty of manmade chemicals other than pesticides—a number of which should be considered when we are looking at the background level of toxins that the bees must deal with (as per my leaky boat analogy).

General Environmental Pollutants

Long-time bee researcher and toxicologist Dr. Jerry Bromenshenk points out that our focus on agricultural pesticides overlooks plenty of other toxic substances to which bees are exposed (which got plenty of attention from beekeepers prior to the distraction of synthetic pesticides).  His research suggests that we could consider bees as “flying dust mops,” and hives to be “air sampling devices.”

Bromenshenk, funded at the time by the EPA, developed methods for using beehives as monitors of environmental pollution.  In 1989, based on his studies, EPA approved honey bees in their guidance reference manual for establishing and conducting ecological assessments of hazardous waste sites [9].  I’ve condensed his findings (from the book Honey Bee:  Estimating the Environmental Impact of Chemicals [10] and personal communications):

A colony of honey bees is an effective environmental sampling device for volatile and semi-volatile organic compounds.   Beehives located in uncontaminated environments contain compounds released by the bees themselves, from hive stores, and from the materials from which the beehives are constructed.  In all areas they also contain compounds from vehicles, farms, industries, and households in the hive vicinity.  Some of these are pesticides, but we also identified  on average more than 200 other (volatile and semi-volatile) chemical compounds  that occur simultaneously inside each and every beehive,  as well as trace elements,  heavy metals, and even radioactive materials, sometimes at levels that caused bee toxicity or queen mortality.  Thus, these chemicals should be included in any discussion of honey bee health.

To our credit, we have cleaned up pollution significantly since the ‘70’s, but there are still plenty of dusts, solvents, and volatile emissions that can be carried back to the hive by foragers (Fig. 2).

Figure 2.  The EPA tracks the levels of 177 air pollutants such as acetaldehyde, arsenic, mercury, benzene, carbon tetrachloride, formaldehyde, methyl chloride, toluene, and several pesticides [11].  Dusts stick to bees due to electrostatic charge, and are carried back to the hive, where they are inadvertently mixed with the pollen in the beebread.  Volatiles accumulate and may even bioconcentrate inside the bodies of bees and may be absorbed by the beeswax as bees ventilate the hive.

Bromenshenk pioneered using bee hives to track the distribution of trace element pollution downwind from smokestacks.  Oddly, his seminal paper [12] is widely cited in environmental studies, but rarely in the bee literature!  He also demonstrated that such heavy metal pollution could show up in hives even decades after a smokestack was shut down, and that such pollution could cause colonies to decline in strength [13]

Again, although we have made progress in reducing smokestack emissions, there is still plenty of heavy metal pollution going on (Fig. 3).   Keep in mind that unlike pesticides, heavy metals never degrade, remaining in the soil forever, possibly being concentrated in the pollen of plants growing there.  For example, lead-arsenate insecticides were widely used on cotton until they were banned in the ‘80’s.  But they’ve come back to haunt us when rice is then planted on previous cotton land [14].

Figure 3.  Heavy metal pollution is invisible.  The above map shows the amount of lead in the air in 2010 (in μg/m3; maximum 3-month averages).  Some plants exhibit the nasty habit of bioaccumulating heavy metals in their pollen [15].  Source EPA [16].


Update March 2015  One  natural trace mineral in pollen is manganese (which may be elevated in areas of high manganese content of the soil).  Manganese is also an air pollutant released by vehicle emissions, industry, and iron smelters.  A team of researchers found   “that manganese exposure negatively affects foraging behaviour in the honeybee…we found that honeybees treated with 50 mM Mn2+ showed a precocious transition from in-hive behaviours to foraging … Surprisingly, precocious foragers completed significantly fewer foraging trips over their lifetime …, which suggests that long-term exposure of beehives to Mn2+ could negatively affect colony fitness.

Søvik, E, et al (2015) Negative impact of manganese on honeybee foraging.  Biology Letters http://rsbl.royalsocietypublishing.org/content/11/3/20140989

For releases of manganese in your state, see http://www.atsdr.cdc.gov/toxprofiles/tp151-c6.pdf


And now I wonder about the volatiles being released by the fracking of shale formations—common in many beekeeping areas (Fig. 4).

Figure 4.  Fracking releases a number of potentially toxic petroleum hydrocarbons into the air, including benzene, ethylbenzene, toluene and xylene [17].  Do you place any hives near oil or gas wells?  Source [18].

Bromenshenk points out that when looking for the causes of bee health issues, we should keep in mind the background levels of environmental pollutants, which to my knowledge, are rarely tested for.

Practical application:  Do you know the history of heavy metal pollution where you place your bees?  If there was ever mining, a factory, a smokestack, or use of lead-arsenate insecticides, the soils and plants in that area may be quietly poisoning your bees and you’d never know!

Scientific application: Densely populated urban areas tend to have high exposures to a vast array of pollutants as evidenced by the preceding maps.  This fact should be taken into account in any trial of pesticide effects performed in such areas.

Natural Elements

So far, I’ve been speaking of manmade pollutants.  But some plants concentrate natural soil elements to high concentrations in nectar and pollen [19].  Beekeepers should be aware of a couple of recent studies on selenium and bees.  Quinn [20] found that some plants concentrate selenium in nectar and pollen to levels that could be toxic to bees, and that surprisingly, bees do not avoid those flowers!  Hladun [21] then demonstrated that such naturally-occurring levels of selenium can cause the same sorts of behavioral and mortality effects upon bees as one would see in the standard testing of insecticides!

Practical application (?): commercial beekeepers often summer bees in areas of high soil selenium (Fig. 5).  Some native plants in those areas concentrate selenium to toxic levels.  Of special concern is that alfalfa and canola can also concentrate selenium.

Figure 5.  Map of selenium concentration in soils.  Bees kept in the reddish areas stand the risk of being exposed to toxic levels of this metal via nectar and pollen, especially in drought years. Source [22].  You may wish to view a similar map for the arsenic content of soils [23]!

And if unavoidable environmental pollutants weren’t enough, bees have the annoying habit of getting “into things.”

Those Danged Bees!

Not only do bees get into soda cans and any other source of potentially harmful sweets (like cracked fruit, molasses, or ant or fly bait), but they are programmed to seek out toxic plant resins to use as propolis (Fig. 6).

Figure 6.  I’ve heard from two different friends that when they pull into certain trailer parks, that bees come and scrape the caulking out of the seams of their travel trailers (note the caulking in the pollen baskets).  In both cases the bees found the caulking of only one particular brand of trailer in the entire park to be attractive!  I have no idea as to the toxicity of the caulking once back in the hive.  Photo courtesy Kerry McDonald.

Poor Colony Survival

It’s easy to blame poor colony performance at the end of the season on pesticides, but are they always truly to blame?  I took the photo below (Fig. 7) in late July—about a month after the main honey flow ended.

Figure 7.  This colony appears to be well fed—notice the distended abdomens full of nectar and the abundant beebread.  However, if you look closely at the young larvae, you’ll notice that they are only being given a minimum amount of jelly, and the brood pattern is shot (indicating poor larval survival). Despite the presence of pollen and honey, the signs are that this colony is under serious stress!

If you inspected the above colony in late summer, you’d see pollen stores, well-fed adults, and active broodrearing—yet it is clearly under severe stress.  If the colony had previously been exposed to ag chemicals, the beekeeper might suspect that they were to blame.

However, the colony was one of mine, and I feel that I can safely assume that it had not been exposed to any pesticides (no crops or commercial landscapes within flight range).  I have no idea as to whether the stressed brood was due to an inadequate nutritional profile of the late-season pollen, plant alleleochemicals, or something else.  In my experience, this stressed colony (which is typical for my area at this time of year), without nutritional intervention by the beekeeper, would dwindle in strength, be unable to produce a healthy winter cluster, and likely not make it through winter, eventually succumbing to viruses or nosema.  The question then would be to what the beekeeper attributed that loss.  In this case, something sure wasn’t right, but it certainly wasn’t pesticides or miticide residues!

Practical application: colonies require high-quality pollen to prepare for winter.  Those suffering from poor nutrition may not be able to rear a healthy crop of “winter bees” [24, 25].  Such nutritional stress can not only cause the population to dwindle, but such dwindling could be exacerbated by the effects of any toxins, natural or manmade.  And an exposure to a dose of agricultural pesticides that a healthy colony might simply shrug off could be the kiss of death for such a nutritionally-stressed one!

Reality Check

Let me be clear that I’m not suggesting that pollution and plant alleleochemicals are the cause of most colony mortality, nor that pesticides aren’t involved.  Rather, the point of the discussion is that the local background levels of environmental pollutants and plant allelochemicals may help to explain why study after study has been unable to find a statistical relationship between colony mortality and pesticide residues [26]—it’s hard to figure things out when you’re working half blind!  The problem may be that there were additional variables that were not measured (each analyis adds to costs).  I have yet to see a study in which colony mortality was investigated in the full context of the sum total of all toxins (including those from plants, pollutants, air, and dust) to which the colony was exposed—these additional toxins are often present at levels that rival the toxicity of pesticides!  Such additional variables could easily confound attempts to link [27] colony mortality to pesticide residues.

Practical application: It is relatively straightforward to nail the cause of an acute pesticide kill.  It is much more difficult to separate any sublethal effects due to pesticides from those of the stew of natural and manmade toxins to which bees are exposed in the real world.  Unless we take into account all the leaks in the boat, we really don’t know how hard the colony is bailing to stay afloat.  Colonies may be able to shrug off an exposure to an agricultural pesticide in one location or under certain conditions, yet suffer serious mortality in another location or under other conditions.  Such variability makes it devilishly difficult to tease out the actual relationships between pesticide residues and colony health.

NEXT—on to (finally) manmade pesticides!


As always, I’m indebted to Peter Borst for his assistance in research, and to Drs. Jerry Bromenshenk and James Frazier for their helpful reviews and comments.

References and Notes

[2] Borek, V (2012) History of pesticides. (Broken Link!) http://www.chemistryexplained.com/Ny-Pi/Pesticides.html#ixzz2EzTpmYPS

[3] Pimentel, GC (1985) Opportunities in chemistry. http://www.nap.edu/openbook.php?record_id=606&page=4

[4] Laszlo, P (2006) On the self-image of chemists, 1950-2000.  HYLE–International Journal for Philosophy of Chemistry 12(1): 99-130. http://www.hyle.org/journal/issues/12-1/laszlo.htm

[5] Gold, LS, et al (2001) Pesticide residues in food and cancer risk: a critical analysis. In: Handbook of Pesticide Toxicology, Second Edition (R. Krieger, ed.), San Diego, CA: Academic Press, pp. 799-843 (2001).  http://potency.berkeley.edu/text/handbook.pesticide.toxicology.pdf I highly recommend this read!

[8] http://www.cdc.gov/PDF/Frequently_Asked_Questions_About_Calculating_Obesity-Related_risk.pdf

[9] Warren-Hicks, W, et al (1989) Ecological assessment of hazardous waste sites:  A field and laboratory reference. EPA/600/3-89/013.  A free download.

[10] Smith GC, GH Alnasser, DC Jones , and JJ Bromenshenk (2002) Volatile and semi-volatile organic compounds in beehive atmospheres.  In, Devillers and Pham-Delègue, eds.,  Honey Bees: Estimating the Environmental Impact of Chemicals, CRC Press.

[11] http://www.epa.gov/ttn/atw/nata2005/05pdf/2005polls.pdf

[12] Bromenshenk JJ, et al (1985) Pollution monitoring of Puget Sound with honey bees.  Science 227(4687): 632-634.

[13] Bromenshenk, JJ, et at (1991) Population dynamics of honey bee nucleus colonies exposed to industrial pollutants.  Apidologie 22 (4) 359-369.

[15] Roman, A (2009) Concentration of chosen trace elements of toxic properties in bee pollen loads.  Polish Journal of Environmental Studies 18(2): 265.

[18] Energy Information Administration.

[19] Terry, N, et al (200) Selenium in higher plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 51:401–32. http://www.plantstress.com/articles/toxicity_i/selenium.pdf

[20] Quinn CF, et al. (2011) Selenium accumulation in flowers and its effects on pollination. New Phytol 192: 727–737. http://rydberg.biology.colostate.edu/epsmitslab/Quinn%20et%20al%202011%20New%20Phytol%20proofs.pdf

[21] Hladun KR, et al (2012) Selenium Toxicity to Honey Bee (Apis mellifera L.) Pollinators: Effects on Behaviors and Survival. PLoS ONE 7(4): e34137. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0034137

[24] N. Höcherl, N, et al (2010) Effects of a pure maize pollen diet on the honeybee.  Apidologie 41: 676–694.  Free download.

[27] The other unknown variables (pollutants, alleleochemicals, nutrition, temperature) can bedevil the statistician when he tries to separate out the “effect” due solely to the pesticides.  The researcher is trying to determine whether the “independent variable” (pesticide level) correlates with the “dependent variable” (whatever aspect of bee or colony health being measured.  If there is a great deal of additional variation due to unmeasured factors such as pollution or plant allelochemicals, any sublethal effects due to pesticides may get buried in the “noise.”

Category: Pesticide Issues
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Sick Bees – Part 18F3: Colony Collapse Revisited – Keeping A Leaky Boat Afloat

First published in: American Bee Journal March 2013

Sick Bees Part 18f3: Colony Collapse Revisited

Keeping A Leaky Boat Afloat

First published in ABJ March 2013

Randy Oliver



the leaky boat analogy. 1

Why would bees collect toxic pollen?. 2

Almond pollen. 4

colony-to-colony variation. 5

bee genetics or gut endosymbionts?. 5

summary (so far). 6




The Leaky Boat Analogy

One way to put pesticide impacts upon bee health into perspective would be to think of a bee colony as a wooden boat, with exposure to each individual toxin representing a leak, or in the case of insecticide dust or sprays, a wave over the bow.  The colony “boat” must work at “bailing out” the allelochemicals in nectar and pollen (by detoxification or elimination); the more phytotoxins coming in, the less safe freeboard remaining.  In some cases a phytotoxin load may overwhelm the bailing crew and sink the boat.

In the above analogy, you can see that exposure to manmade pesticides is not a black or white situation—we must always keep in mind how much freeboard the boat had left prior to being exposed to the additional toxin.

Practical application:  so when we think of bee colonies and toxins of any sort, we must always keep in mind the amount of “bailing” that the colony is already doing to keep up with the leaks prior to its exposure to any new toxin.  And anything that adds to colony stress will likely make that colony more susceptible to damage by the addition of yet another toxicant.

On the other hand, the exposure of bees to some allelochemicals may prepare the crew for “bad weather”—by consuming plant toxins, the bees may upregulate their detoxification enzymes, kind of like the crew getting stronger by “practicing.”  May Berenbaum found that bees that consumed propolis extracts exhibited an enhanced capacity to detoxify mycotoxins [1].

Why Would Bees Collect Toxic Pollen?

There are two foods that foragers bring back to the colony—nectar and pollen.  However, the evaluation of the “safety” of these two food sources is entirely different.  In the case of nectar, there is a multi-step “homeland security” type of screening process to minimize the intake of toxins into the hive.  First, the individual forager samples the nectar, and may reject it should it find the taste repellent, since many phytotoxins are bitter or irritating.  Then on the flight home, should the forager become sickened by its nectar load, it may die in the field, or intentionally sacrifice itself by committing “altruistic self removal.”  Once back in the hive, the forager must then find a mid-aged receiver bee to take its nectar load, which provides yet another checkpoint against toxic nectar, since the receivers would likely be averse to taking any nectar that had previously bothered them.   So the colony appears have effective mechanisms in place to protect it from poisonous nectar.

Surprisingly, no such sort of screening appears to happen in the case of pollen!  Bees are well known to collect pollens toxic enough to kill the colony (as with California Buckeye in my area).  Since pollen foragers do not ingest the pollen that they gather, they have no way of knowing whether it is toxic or not.  Excellent studies by Pernal and Currie [2] demonstrated that foragers do not appear to discriminate between pollens due to nutritional content, but rather by particle size and aroma.  My own experimentation supports the importance of odor.

Since it would be non adaptive for bees to collect toxic pollen, one would suspect that natural populations of honey bees would evolutionarily  “learn” to avoid any toxic pollens in the local habitat based upon their odor, or to inherit the genes that caused them to favor pollens that were on the “proper odor list.”

So what happens when we move bees outside of their natural range, such as to the Americas, Australia, or New Zealand?  There they would be exposed to completely novel pollens, such as those from corn (maize), soybeans, melons and squash, sunflowers, cotton, blueberries, and cranberries (all of New World origin).  The European honey bee may not be well adapted to either the nutritional composition of these pollens, nor their allelochemicals.

Not surprisingly, when researchers inspect the actual pollen loads of foragers from hives placed adjacent to these New World crops, they often find that the bees eschew those pollens in favor of those from plants of Old World origin growing within flight range (either weeds or crop plants).  I suspect that the bees may simply not be “wired” to recognize the New World pollens as food.  Perhaps not surprisingly, some of them are also of notably poor quality as bee feed.

Consider corn pollen.   In a number of studies, corn (maize) is often found to be one of the major pollen sources used by honey bees [3, 4], and in the U.S., bees eagerly gather the pollen of sweet corn.  Yet U.S. beekeepers have told me that bees winter poorly on corn pollen.

These anecdotal reports are supported by recent research by Höcherl [5], who found that bees experimentally fed maize pollen produced less brood and had shorter longevity as adults than those fed mixed pollens.  Maize pollen is generally high in protein, but when I compared its amino acid composition to the ideal of deGroot [6], its nutritive value was limited by its low ratio of tryptophan.  However, that does not explain why bees so eschew the pollen of field corn.  Bromenshenk [7], who recently surveyed 116 colonies across the Corn Belt during the tasseling period, found that foragers preferentially seek out any other sort of pollen than that of field corn–a substantial proportion of colonies collected no corn pollen, and overall, the median percentage of corn in trapped pollen was only about 10%.  This finding means that foragers will fly over fields of field corn in full tassel in order to find weeds in flower.  So what’s up with that?

What could possibly make bees so dislike field corn pollen that the foragers would avoid gathering such an easily available and abundant food source?  Hungry foragers will gather sawdust (Fig. 1), so it can’t just be the lack of nutritional value.

Figure 1.  Bees collecting sawdust at my home yard on a sunny morning in January, when there was little natural pollen to be had.  There was far more activity at a feeder of dry pollen supplement that I had set out.

Could it be that allelochemicals in field corn pollen is repellent to foragers?  When I searched, I was surprised to find that the pollen of some varieties of corn “burns” the leaves of plants that it falls upon [8], perhaps due to its high content of phenylacetic acid (PAA).  I couldn’t find toxicity data of PAA [9] to bees, but it makes me wonder whether some of our cultivars of field corn are somewhat toxic to bees?

Almond pollen

One demonstrably toxic pollen of great interest to me is that of the almond tree (Fig. 2), which contains high concentrations of amygdalin (normally metabolically degraded to benzaldehyde and cyanide—also both toxic).  Yet bees thrive on almond pollen, despite the fact that in some cultivars the concentration of amygdalin approaches that of acute bee toxicity [10].  What concerns me is that no one has studied whether the necessary detoxification of amygdalin hampers the bees’ ability to simultaneously detoxify other pesticides.

Figure 2.  Almond pollen and nectar is loaded with the toxic and bitter cyanogenic glycoside amygdalin, yet honey bees thrive on it.  The bee is apparently preadapted to detoxify this class of chemicals since they are commonly produced by a number of European fruit trees in the rose family.

Despite its apparent toxicity, bees thrive on almond pollen, presumably because of their coevolutionary adaptation in the Mediterranean region to the even more toxic ancestor of the cultivated almond.

Colony-to-Colony Variation

One can easily observe the colony-to-colony difference in response to the toxic organic acids and essential oils used for varroa control.  The exact same dose applied to a number of hives will elicit vastly different responses.  Some colonies appear to barely notice the chemical, whereas others may pour out of the entrance, suffer serious mortality, or even abandon the hive.  This fact makes it difficult to define the “toxic dose”!

We must also keep in mind that not every colony in an apiary is foraging on the same plants.  All one need do is to put pollen traps on each hive to observe that each colony can be foraging on completely different flowers, and perhaps in totally separate areas.  The exposure of two side-by-side colonies to toxins, whether natural or synthetic, may be 100% different!

We tend to breed generic, highly productive bee stocks.  In natural settings, though, honey bees were much more locally adapted, fine-tuned to the toxins of the local flora.  On that subject, I found a fascinating and thought-provoking paper by Després [11], from which I’ll share some excerpts:

Over 400 million years of coevolution with plants, phytophagous [plant-eating] insects have developed diverse resistance mechanisms to cope with plant chemical defences.  Because insects face a geographical mosaic of chemical environments, from non-toxic to highly toxic plants, the costs associated with resistance traits vary with the probability of encountering a toxin…

I’ve heard anecdotally that in certain areas, locally-adapted bee stocks can better survive exposure to the local toxic flora (such as Buckeye in the Sierra foothills) or the dark fall honey that can cause winter losses in nonadapted stock.  Atkins [12] also pointed out that “Some hybrid strains of bees are more resistant to certain plant poisons than purer strains.”  This subject certainly deserves further investigation!

Bee Genetics or Gut Endosymbionts?

But is it actually the genetics of the bees that makes the difference, or the genetics of their symbiotic fungi and bacteria?  Honey bees harbor a distinctive microflora in both their guts and in the beebread [13].  In the beebread, the symbiotic fungi may be the more important for producing detoxification enzymes [14].  This hypothesis is supported by the finding by vanEngelsdorp [15] that pollen containing high levels of a fungicide apparently goes “toxic,” whereupon the bees seal it off.

I mentioned in my last article that pesticide detoxification appears to take place largely in the Malpighian tubules and ileum of the gut.  A recent study by Martinson [16] found that these organs appear to be specifically constructed to provide a home for symbiotic bacteria—perhaps those critical for the detoxification process.  These bee endosymbionts may be more important than we’ve realized:

Insect fungal symbionts (as well as bacterial symbionts) are well recognized as providers of nutrients for their insect hosts. The rationale behind this is that the insects are feeding on nutrient-poor resources, and need the microbial symbionts to provide a balanced diet. The effects of the presence of toxins in these food materials has been relatively overlooked, yet in many cases there is just as much need for detoxification as there is for nutrient provision [17] (emphasis mine).

It could be that a colony’s ability to handle pesticides is dependent upon the health and species composition of this gut community.  And what do we beekeepers often do?  We treat our colonies with antibiotics to kill bacteria!  Now I’m not about to claim that antibiotics are “bad” for bees—many beekeepers report that Terramycin (oxytetracycline) works like a “tonic,” similar to the manner in which poultry seem to benefit from antibiotics.  Indeed, the Moran lab [18] found that terramycin-resistant bacteria were common in the guts of commercial bees, but rare in colonies in which there was no history of antibiotic use.

But what happens if we introduce a novel antibiotic?  The authors noted that tylosin was registered for use by beekeepers starting in 2005 (and is widely applied applied in excess), just as CCD reared its ugly head.  Vásquez [19] found that the beneficial gut flora that they tested were more susceptible to tylosin than to tetracycline.  I had checked with Dr. Jerry Bromenshenk at the time of his first survey of potentials factors in CCD, asking whether there was any correlation with the use of tylosin—but none stood out.

But there is more to the story.  Nectar contains not only plant allelochemicals, but also bacteria and fungi which can grow in the sugar-rich solutions and produce toxic metabolites.  Once bees consume nectar, their symbiotic gut bacteria suppress the growth of these potentially harmful nectar microorganisms.  Vásquez [20] collected some 55 bacteria and 5 fungi from flowers, and found that the most common bee endosymbiotic bacterium was also the most potent in inhibiting the growth of all the flower microorganisms.  Her findings suggest that the typical feeding of Tylosin in fall by commercial beekeepers may suppress these important gut endosymbionts, with unknown consequences.

Practical application:  I’m not going to try to make a case against antibiotics–I use them myself when called for.  However, I will suggest that it would be wise to save them for when we really need them, rather than using them prophylactically across the operation.

Summary (so far)

Confused?  Me too!  We are still very much on the learning curve about bee responses to toxins!  Let’s review some points to keep in mind:

  • When we use the word “pesticides” or “toxins” we should realize that those terms include the plethora of natural plant allelochemicals to which bees are exposed via nectar, pollen, and propolis, and toxic bacterial and fungal metabolites in nectar and pollen.
  • At extremely low doses (parts per trillion), most plant allelochemicals and synthetic toxicants are likely merely “background noise” of little or no biological relevance.
  • At very low doses many toxins clearly have beneficial hormetic effects, perhaps by initiating certain immune response cascades; or stimulatory effects (as do the natural alkaloids caffeine and nicotine).
  • I’ll spare you the math [21], but when I calculated out the amount of plant alkaloids that would be consumed by an individual bee in pollen or nectar, and compared it to the oral lethal dose as determined by Detzel, bees appear to be commonly exposed to what should be lethal levels of plant alkaloids.
  • It is typically only under certain environmental conditions that colonies show signs of poisoning from natural flora (I don’t normally notice Buckeye poisoning to any great extent).  Oh duh! [22] However, any sort of stress on those plants, or lack of dilution by “safe” nectar or pollen, could suddenly shift the balance and allow for the natural “poisoning” of colonies.
  • We have virtually no idea as to how important bee breeding and colony endosymbionts are in relationship to the bees’ ability to detoxify allelochemicals or synthetic toxicants.

To return to my leaky boat analogy, colonies foraging on toxic pollen or nectar may not have much freeboard left.  Add to that environmental pollutants, poor nutrition, or parasite load and such colonies will be unable to tolerate any additional manmade toxicants.  On the other hand, a colony enjoying good nutrition and maintaining a robust broodnest may be able to recover from a pesticide spray.

Practical applications: 

  • Learn if you have known toxic flora in your vicinity
  • Keep locally-adapted bees
  • Don’t count on corn, sunflowers, vine crops, blueberries or cranberries for nutrition
  • Mitigate the effects of toxins by supplemental feeding to promote broodrearing
  • Use antibiotics with caution


Next I’ll add the contribution of manmade pollutants and pesticides to the picture.


As always, I am indebted to Peter Borst, and to my wife Stephanie for her forgiveness for my long hours, and her help with the final edit.


[2] Pernal SF, Currie RW (2002) Discrimination and preferences for pollen-based factors by foraging honey bees (Apis mellifera L.). Anim Behav 63(2): 369-390.

Pernal SF, Currie RW (2001) The influence of pollen quality on foraging behavior in honeybees (Apis mellifera L.).  Behavioral Ecology and Sociobiology 51(1): 53-68.

[3] Keller I, et al (2005) Pollen nutrition and colony development in honey bees – Part II. Bee World 86: 27–34.

[4] Malerbo-Souza, DT (2011) The corn pollen as a food source for honeybees. Maringá, 33(4): 701-704. http://www.scielo.br/pdf/asagr/v33n4/20.pdf

[5] Nicole Höcherl, N, et al (2012) Evaluation of the nutritive value of maize for honey bees.  Journal of Insect Physiology 58: 278–285.

[6] deGroot, AP (1953). Protein and amino acid requirements of the honeybee Apis mellifera. Physiologia Comparata et d’Ecogia. 3: 195-285.

[7] Bromenshenk, JJ and C Henderson (2012) In press.

[8] Anaya, AL, et al (1992) Phenylacetic acid as a phytotoxic compound of corn pollen.  Journal of Chemical Ecology 18(6): 897-905.

[10] London-Shafir, I, et al (2003) Amygdalin in almond nectar and pollen – facts and possible roles. Plant Syst. Evol. 238: 87–95.

[11] Després (2007) Op. cit.

[12] Atkins, EL (1975) Injury to honey bees by poisoning.  In The Hive and the Honey Bee, Dadant.

[13] Martinson, VG, et al (2011) A simple and distinctive microbiota associated with honey bees and bumble bees. Molecular Ecology 20: 619–628. (Broken Link!) http://www.danforthlab.entomology.cornell.edu/files/all/martinson_etal_2011.pdf

[14] Gibson, CM and MS Hunter (2010) Extraordinarily widespread and fantastically complex: comparative biology of endosymbiotic bacterial and fungal mutualists of insects.  Ecology Letters 13: 223–234. http://ag.arizona.edu/ento/faculty/hunter/PAPERS/Gibson_Hunter_10.pdf

[15] vanEngelsdorp, D, et al (2009) ‘‘Entombed Pollen”: A new condition in honey bee colonies associated with increased risk of colony mortality. J of Invert Pathology 101: 147–149. http://ento.psu.edu/pollinators/publications/Entombed

[16] Martinson, VG, et al (2012) Establishment of characteristic gut bacteria during development of the honeybee worker. Appl Environ Microbiol. 78(8): 2830–2840. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3318792/

[17] Dowd, PF (1992) Insect fungal symbionts: a promising source of detoxifying enzymes. Journal of Industrial Microbiology. 9: 149-161.  http://naldc.nal.usda.gov/download/24916/PDF

[18] Tian, B, et al (2012) Long-term exposure to antibiotics has caused accumulation of resistance determinants in the gut microbiota of honeybees.  mBio 3(6): http://mbio.asm.org/content/3/6/e00377-12.full.pdf+html

[19] Vásquez A, Forsgren E, Fries I, Paxton RJ, Flaberg E, et al. (2012) Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS ONE 7(3): http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0033188

[20] Vásquez, A, et al. (2012) Symbionts as major modulators of insect health: lactic acid bacteria and honeybees. PLoS ONE 7(3): http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0033188

[21] Typical food consumption by a nurse bee is about 10mg  of pollen per day.  Detzel quantified the alkaloids in lupine pollen at  about 50µg/g, so a bee consuming 10mg of pollen would be exposed to 0.5µg of alkaloids.  The LD50 for typical alkaloids (in syrup) was about 1/10th that amount.

[22]  As I’m reading these words to Stephanie for review, it occurs to me that this likely happened to my own colonies this year when the blackberry bloom failed to materialize!  We didn’t notice severe Buckeye poisoning, but the colonies sure didn’t do well.  It’s amazing to us that I can write an article, but have to read it aloud to realize that it may apply to me!

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Sick Bees – Part 18F2: Colony Collapse Revisited – Plant Allelochemicals

First published in: American Bee Journal February 2013

Sick Bees Part 18f2: Colony Collapse Revisited

Plant Allelochemicals

First published in ABJ February 2013

Randy Oliver


Nature Is Not Nice

Toxic Pollen and Nectar


Have You Ever Noticed Plant Toxic Effects?

What Doesn’t Kill You Makes You Stronger

An Unintended Effect on Varroa?

Self Medication

Tritrophic Interactions

Bee Detoxification of Allelochemicals



Plant Allelochemicals

How do pesticides relate to colony collapse?  That sounds like a simple question, but as I said in the last installment, it’s complicated (there are rarely simple answers in biology).  In order to begin to understand the effects of manmade pesticides upon bee health, we must first back up and understand some of the complex biology involved in natural bee/plant/toxin interactions.

Nature Is Not Nice

Every form of life on Earth is a “survivor” in an unbroken lineage that traces back roughly four billion years.  In some of those years, conditions were certainly not favorable, and each and every organism by necessity needed to have the ability to detoxify the numerous natural chemicals and toxic byproducts of volcanoes, natural radiation, ultraviolet light, and the free radicals created by exposure to oxygen.  Things got even tougher as bacteria and fungi began to engage in chemical warfare—creating a slew of nasty toxins in order to kill off their hosts or competition.  And once plants and their predators evolved, they developed an entire pharmacopeia of phytotoxins to repel, irritate, sicken, or kill anything that tried to eat them.

We humans tend to forget that plants are naturally full of toxic substances, but all one need do is to simply go outside and start randomly consuming wild plant leaves, fruit, and seeds to confirm that this is indeed the case!  (Kids, do not try this experiment!).  Plant breeders have intentionally bred some of the natural toxins out of our crops (or at least from the edible portions—e.g., breeding out the bitter alkaloids from potato tubers, while leaving them in the leaves to repel pests). One unfortunate effect of this sort of breeding is that it makes our crops more susceptible to herbivorous insects, which then forces farmers to spray synthetic insecticides to protect the crop [1].

Practical application: in order to reduce farmers’ reliance upon pesticides, plant scientists can breed for naturally insect-resistant plants.  The tradeoff is in repelling insects without making the plant too toxic for humans.

Toxic Pollen and Nectar

My point is that both humans and honey bees evolved in a world awash in poisons, and both eat diets brimming with natural toxins.  As Gold [2] points out, the vast bulk of toxins consumed by humans are the natural poisons in our food.  Honey bees also consume substantial quantities of natural phytotoxins—flower nectars and pollens contain a vast array of poisons (Fig. 1).


Figure 1. It helps to understand the vernacular used by toxicologists.

Although analysis of the bee genome indicates that for some reason honey bees appear to possess fewer detoxification genes than other insects, they are apparently adept at detoxifying or eliminating the plant toxins commonly found in nectar and pollen (Fig. 2).

Figure 2.  A bee foraging on a species of Senecio.  The pollen from this and a number of other related plants (comfrey, ragworts, and common groundsel) contain toxic pyrrolizidine alkaloids [[i]]—enough to raise concern by European health agencies about their levels in honey [[ii]].  Honey bees must metabolically detoxify these alkaloids [[iii]]. Photo courtesy Kathy Keatley Garvey.

[i] http://toxicology.usu.edu/endnote/Pyrrolizidine-alkaloids-in-food.pdf

[ii] http://www.efsa.europa.eu/en/efsajournal/pub/2406.htm

[iii] Reinhard, A, et al (2009)  Feeding deterrence and detrimental effects of pyrrolizidine alkaloids fed to honey bees (Apis mellifera). J Chem Ecol. 35(9):1086-95.

The pollen and nectar from many bee-pollinated plant species contains toxic “allelochemicals” (alkaloids, cardenolides, essential oils, anthraquinones, flavonoids, saponins, coumarins, etc.).    Some plants accumulate certain metals (e.g., selenium, manganese, copper) to levels that are toxic to plant-feeding insects [6], and onion flowers may concentrate enough potassium in the nectar that it discourages bee visitation [7].

In order to allow us to avoid excessive amounts of plant toxins, humans have extremely sensitive taste buds to detect the “bitterness” of typical allelochemicals.  All you need do is to taste almond nectar to find that it is surprisingly bitter, or bee collected pollen (one color pellet at a time) to notice the bitter chemicals.  Yet bees (and humans) readily consume, either by choice or necessity, such clearly toxic plant products.   German researchers Detzel and Wink [8] tested 63 different plant allelochemicals for attractiveness, deterrence, and toxicity to adult bees. Nearly 40 showed some degree of feeding deterrence.

Surprisingly, they found that several were toxic at levels that didn’t cause feeding deterrence, meaning that bees might unwittingly consume a toxic dose!  And remember that there is little chance for dilution of toxic nectar, since any individual nectar forager sticks to only one species of flower–which may be a good thing for the colony if an intoxicated bee is unable to return!  But then those toxins are concentrated when bees process the nectar into honey.

And just how toxic were those natural allelochemicals?  By my math, more than half of the tested compounds were acutely toxic to bees in the parts per million range–they would all have made Atkins’ [9] ranking as “highly toxic”—some of them approaching the toxicity of imidacloprid [10]!

Practical consideration: if one were to be admitted to the emergency room suffering from poisoning, the first thing that the doctor would ask would be, “What other drugs (toxins) had you taken?”  Yet if a beekeeper submits a sample of beebread to the lab for the standard pesticide analysis of 170 toxicants, no one’s looking at the plant allelochemicals!  When taken out of context of the bees’ total exposure to toxins both natural and synthetic, the typical pesticide analysis would give only part of the picture.

Beekeepers have long noticed that particular nectar flows may affect their bees—some nectar flows are said to make bees “pissy;” and the Australians refer to “hot” or “cold” honeyflows [11].  And bees may fare poorly if they get too much of a single nectar.  For example, linden nectar (Tilia) contains the bee-toxic sugar mannose (as well as a bit of nicotine).

It makes one wonder why plants that depend upon insects to pollinate them would produce toxic pollen and nectar?  Well, in the first place, pollen is precious to plants, and they only begrudgingly allow bees to eat it.  Another theory is that toxins produced to deter herbivores from grazing on the foliage simply “wind up” in the flower products [12].  But it appears to be more complicated than that–in many plants the allelochemicals are either concentrated or diluted in the nectar and pollen (relative to the amount in the sap), or of different composition than in the leaves.  So plants appear to be able to regulate their toxicity to pollinators.

Plants would then need to perform an evolutionary balancing act in being toxic enough to deter herbivores, yet keeping their nectar and pollen palatable to pollinators [13].  But nature abhors uniformity.  The phytotoxins in plants differ in both mixture and concentration not only from species to species, but even from individual plant to plant (this is a common energy-saving strategy used by prey species to “train” predators).  Linhart [14] studied wild thyme plants in the south of France, and found that individual plants varied in which of the six dominant monoterpenes that they produced. Thus, each individual plant exhibited a specific “chemotype.” Foraging bees may thus face a bewildering smorgasbord of plant chemotypes, even in a field of the same species of flowers!  When given a choice, they may avoid those that are too potent (or maybe not!).

Practical application: during nectar dearth, or the failure of a particular bloom, foraging bees may find their choices to be limited, and be forced to bring back plant products that they normally would have avoided.

Other hypotheses [15] propose that plants toxify their nectar to favor specialized pollinators, or to deter “nectar thieves” such as ants, or generalists such as honey bees.  One intriguing hypothesis is that plants serve up stimulants in their nectar to “hook” bees—bees apparently prefer a little caffeine or nicotine in their juice [16].  Such stimulants may also cause the bees to become more efficient pollinators by inducing them to move more rapidly from plant to plant, or not grooming the pollen off their bodies as efficiently.  Nature is not constrained by any ethical rules of “fair play.”

Something of interest is that Baker [17] found that the nectar of flowers pollinated by butterflies (which don’t eat pollen) tended to have a higher content of amino acids than did that from plants normally pollinated by bees.  This certainly implies that the nectar of some plants may be more nutritious to bees than that of others.  Of even greater interest is that when he surveyed plants from tropical lowlands up to alpine tundra, he found that the lower in elevation (or further south), the greater the concentrations of alkaloids or phenolics in the nectar (presumably due to the greater intensity of insect pressure)!  As we will see later, this has implications as to the differences in tolerance to manmade insecticides by honey bees as compared to bumblebees.

It is energetically costly to plants (meaning that it slows their growth) to produce these allelochemicals, so many annuals and biennials hold back until they start to flower (presumably to protect their future “offspring”).  Anyone who has tasted lettuce after it has started to bolt has surely noticed the sudden increase in bitter allelochemicals!  Plants may also upregulate the production of toxins when stressed by drought or by insect predation, or if neighboring plants communicate a chemical signal [18].

Practical application: floral toxicity may vary from plant to plant, region to region, or year to year, and increase in time of plant stress due to heat, drought, or insect attack.

At the colony level, incoming toxic nectar and pollen may be diluted or mixed with other pollens.  Foragers intentionally seek out a diverse mixture of pollens, which may help to keep them from poisoning the broodnest, since some nectars and pollens are quite toxic (Table 1):

Some Plants Acutely Toxic to Honey Bees

Largely from Atkins (1975), and Pellet (1920)

Black Nightshade

California Buckeye

Corn Lily

Death Camas



Horse Chestnut


Mountain Laurel



Seaside Arrowgrass

Summer Titi

Western False Hellebore

Whorled Milkweed

Yellow Jessamine

Table 1.  The above plants are not in any sort of class by themselves—they are simply those that beekeepers in North America have reported under some conditions to cause serious adult or larval bee mortality.  Most other plants produce a continuum of phytotoxins which may cause sublethal or beneficial effects that go unnoticed by beekeepers.

For example, in California, bees readily gather nectar from Buckeye (Aesculus californica) (Fig. 3):

Symptoms of buckeye poisoning usually appear about a week after bees begin working the blossoms. Many young larvae die, giving the brood pattern an irregular appearance. The queen’s egg-laying rate decreases or stops, or she may lay only drone eggs; after a few weeks, an increasing number of eggs fail to hatch or a majority of young larvae die before they are 3 days old. Some adults emerge with crippled wings or malformed legs and bodies. Foraging bees feeding on buckeye blossoms may have dark, shiny bodies and paralysis-like symptoms.  Affected colonies may be seriously weakened or may die [19].

Figure 3.  Pretty, but deadly. This is the toxic plant with which I have the most experience—California Buckeye.  In “normal” years my bees work it heavily for nectar, but I don’t see them collecting much pollen; the nectar is diluted by the concurrent nectar flow from wild blackberries.  But in years in which the blooms are out of synch, Buckeye can really hammer an apiary!

Although researchers have shown that the larvae of various species of bees vary in their ability to handle different pollens [20], and that some pollens are toxic to honey bee larvae [21], I’m not quite sure as to exactly what happens during buckeye poisoning, since incoming pollen is generally fermented into beebread, then eaten and digested by nurse bees, and finally converted into jelly for feeding the larvae and queen (actual pollen normally only constitutes a tiny portion of a larva’s diet).   So I’m unclear as to how the Buckeye nectar or pollen kills the brood (perhaps the toxin is passed via the jelly?).

Have You Ever Noticed Plant Toxic Effects?

The legendary bee toxicologist Larry Atkins [22] described the symptoms of natural plant toxicity to honey bees:

The substances in poisonous plants which are toxic to bees are specific in action and may be in both pollen and nectar or may be confined to the nectar or simply to the pollen.  Symptoms of plant poisoning are sometimes difficult to recognize or to be substantiated by chemical or microscopical diagnosis…The presence of symptoms usually is limited to the blooming period of the plant if the nectar is poisonous…However, if the toxic substance is in the pollen, the symptoms may linger as long as the supply of pollen remains in the combs…When only the adult bees are affected, piles of them may be found dead in front of the hive entrance, and there may not be enough adults to care for the brood or cover the combs.

And this is not to mention bees simply getting drunk on fermenting nectar [23].  The nectar in flowers readily ferments into alcohol, and beekeepers have long noticed drunken foragers.  Surprisingly, the alcohol in nectar appears to be the necessary substrate from which forager bees produce the primer pheromone ethyl oleate [24], by which the colony regulates the proportion of foragers to mid-aged bees [25].  So the presence of some amount of the toxin ethanol may be critical for the normal colony division of labor!

Bees show clear preferences when offered various pollens [26], and produce more brood when fed some pollens compared to others [27].  Even when placed in fields of some popular row crops, foragers seek out other sources of pollen, sometimes to the near exclusion of the crop that they are supposed to be pollinating!  But when we speak of the poor nutritional value of some pollen sources, we’re really not sure whether it is due to lack of nutrients, or to the presence of excessive toxins, or to some combination thereof.

Practical application: we really don’t know just how often bee colonies may be living on the “toxic edge.”  We know that colonies build up (or maintain) better on some flows than others, but is the lack of buildup sometimes perhaps due to the bees being at the limit of their ability to detoxify the natural nectars and pollens that they are bringing in? 

What Doesn’t Kill You Makes You Stronger

Paracelsus, regarded by many as the father of toxicology stated that, “All things are poison and not poison; only the dose makes a thing not a poison.”  He recognized that something that can be toxic at a higher dose can be stimulatory or medicinal at a lower dose.

Early physicians carried strychnine in their bags and prescribed it as a tonic to their elderly patients—only in high doses was it considered to be harmful.  Similarly, nicotine, caffeine, aspirin, and alcohol may be useful stimulants or have health benefits at low doses.  The term for this effect is “hormesis” (from Greek hórmēsis ” to set in motion”) and is well described by Bniecki [28]:

If you haven’t yet heard of “hormesis” you probably soon will.  A revolution is taking place in toxicology which will eventually change perspectives radically about the hazards or otherwise of pesticide traces in food.  Hormesis is described as the paradoxical effect of toxins at low concentrations. The paradox is that although most chemicals are toxic at high concentrations (or dose), the majority are likely beneficial at low concentrations (or dose).  The common regulatory assumption is that if a chemical is toxic at high dose it continues to be toxic but with diminishing toxicity as the dose is lowered.  In contrast, hormesis indicates that many chemicals have the opposite effect at low doses to those at high doses.

The above words were written in 2003.  You might have noticed that “hormesis” (or its implications) has not yet become part of the common lexicon.  Baldwin [29] explains:

The hormetic perspective also turns upside down the strategies and tactics used for risk communication of toxic substances for the public. For the past 30 years, regulatory and/or public-health agencies in many countries have ‘educated’ — and in the process frightened — the public to expect that there may be no safe exposure level to many toxic agents… If the hormetic perspective were accepted, the risk-assessment message would have to change completely. Changing a dominant risk-communication paradigm is not as simple as flicking on a light switch. It changes beliefs, attitudes, and assumptions… It would certainly be resisted by many regulatory and public-health agencies…

Although the public has not yet resonated with hormesis, entomologists (who also refer to it as “hormogliosis”) are well aware of the effect [30, 31, 32].  Such hormetic effects would certainly be expected to apply to honey bees and plant alleleochemicals:

As with all toxins, carefully conducted dose response studies with allelochemicals generally results in the finding of hormetic responses [33].

So, in general it appears that sublethal doses of many toxins, instead of being harmful, may actually promote health!  This concept is certainly contrary to what we’ve been led to believe, despite Paracelsus pointing out the obvious some 500 years ago.  It’s funny that we haven’t made the connection when we speak of “chemicals” in the environment, since, if you think about it, hormesis is the basis of modern medicine, in which doctors prescribe toxins at low doses to cure our ills (Fig. 4).

Figure 4.  There is no difference between a medicine or a toxin, other than the dosage.  More than half of the world’s population still relies entirely on plants for medicines, and plants supply the active ingredients of most traditional medical products. Plants have also served as the starting point for countless drugs on the market today [[i]].  Photo credit [[ii]].

[i] http://publications.nigms.nih.gov/medbydesign/chapter3.html

[ii] http://www.cliparttop100.com/

I found a fascinating article on the problem of consumer acceptance of bitter fruits and vegetables, despite the healthful benefits of those bitter plant allelochemicals [36].  The authors point out that plant breeders and our cooking methods deliberately “debitter” our food, with the unintended effect of perhaps removing the most healthful (especially anti-cancer) components!  The authors point out that, “When it comes to bitter phytonutrients, the demands of good taste and good health may be wholly incompatible.”

Perhaps the bees’ predilection toward bitter plant products may be telling us humans something important!

An Unintended Effect On Varroa?

In researching hormesis, I came across an item of interest—that low doses of some insecticides have the hormetic effect of increasing the fecundity of the insect that the chemical was intended to kill [37, 38]!  What especially piqued my interest was a study that found that the same applies to mites [39].  Could it be that miticide or insecticide residues in brood combs might increase varroa fecundity?

Self Medication

We humans (at least some of us) intentionally eat plants rich in potentially toxic phytochemicals for their beneficial hormetic effects—think of the aromatic flavors of herbs, the tingling burn of spices, strongly flavored fruits,  and “healthful” bitter salad greens.  Bees may well do the same in seeking out allelochemical-laced pollen and nectar for its healthful benefits.

Some plant toxins help bees to fight parasites—Laurentz [40] found that despite the fact that it was metabolically costly to detoxify plant toxins, it may be of benefit to the insect in that those toxins help to defend it from parasites!  Amazingly, there is even evidence that insects may actually self medicate with plant products when they are sick—Singer [41] found that parasitized caterpillars consume plant toxins to excess in order to kill their parasites.  And how about the toxic antimicrobial, ant-repelling, and mite-killing tree resins that we call “propolis”?  Mike Simone-Finstrom [42] recently found that honey bee colonies experimentally challenged with chalkbrood went out of their way to collect extra propolis.

But it gets even more complex than that…

Tritrophic Interactions

Just in case you’re not yet overwhelmed by the complexity of nature, let’s now move on to on “tritrophic interactions” (taking place at three levels):

Many insects live in close association with microorganisms (e.g., bacterial endosymbionts). Given the many enzymatic activities known to occur in bacteria and fungi, their role in detoxifying secondary plant compounds has been suspected but not yet clearly demonstrated. Further research will involve evaluating the role of endosymbionts in the detoxification of plant toxins [43].

Unfortunately, we don’t know squat about how important the honey bee gut- or beebread symbiotic bacteria and fungi are in detoxifying harmful chemicals!  But it’s not just in detoxification that we have tritrophic interactions.  In addition, bees are generally infected by one or more parasites (bacteria, fungi, viruses, mites, or nosema).  There is evidence that any or all of these parasites may be affected by both the plant allelochemicals that bees consume, as well as any synthetic pesticides (or beekeeper-applied miticides) that they are exposed to.

So what’s a “tritrophic interaction”?  Let’s say that a plant is preyed upon by grasshoppers, and that the grasshopper population is largely controlled by the presence of a gut parasite (say Nosema locustae).  All that the plant need do is to produce allelochemicals that favor the gut parasite (perhaps by suppressing the grasshopper immune response), so that any grasshoppers that eat that particular plant would suffer greater parasitism.  This is a common strategy in biocontrol using insect parasites—the parasite spores are introduced along with a synthetic insecticide that weakens the insects’ defenses.

It also works the other way—a plant can favor a pollinator or animal that distributes its seeds by producing healthful allelochemicals.  Can this phenomenon occur in bees?  You bet!

Diet has a significant effect on pathogen infections in animals and the consumption of secondary metabolites can either enhance or mitigate infection intensity. Secondary metabolites, which are commonly associated with herbivore defense, are also frequently found in floral nectar. One hypothesized function of this so-called toxic nectar is that it has antimicrobial properties, which may benefit insect pollinators by reducing the intensity of pathogen infections. We tested whether gelsemine, a nectar alkaloid of the bee-pollinated plant Gelsemium sempervirens, could reduce pathogen loads in bumble bees infected with the gut protozoan Crithidia bombi…Gelsemine significantly reduced the fecal intensity of C. bombi 7 days after infection when it was consumed continuously by infected bees…Lighter pathogen loads may relieve bees from the behavioral impairments associated with the infection, thereby improving their foraging efficiency. If the collection of nectar secondary metabolites by pollinators is done as a means of self-medication, pollinators may selectively maintain secondary metabolites in the nectar of plants in natural populations [44].

Just as humans eat certain strongly-flavored plants to ward off disease, could plant allelochemicals protect bees from viruses and nosema?  Cory, in the best paper on tritrophic interactions that I’ve seen [45], states that, “Thus far, only the tip of the pyramid of complex multitrophic interactions has been exposed.”  But she explains several mechanisms by which plant allelochemicals can protect bees from pathogens:

  • The lining of the bee gut (the peritrophic matrix) is a key barrier to viruses and nosema.  Phytochemicals can affect its structure, permeability, and physiology.
  • Plant allelochemicals can damage midgut cells so that they are sloughed off before viruses or nosema can replicate in them.
  • Plant-derived chemicals can cross the midgut and initiate signaling cascades to bring about cellular immune responses (hormesis).
  • By improving the nutritional benefit of the bee diet, phytochemicals could indirectly reduce bee mortality due to infection by pathogens.
  • Many phytochemicals, especially allelochemicals and nutrients, can modify the physiology and growth of the bee, affecting its susceptibility to infection.

Practical application: a number of researchers have found that sublethal doses of pesticides may make bees more susceptible to nosema or other pathogens.  On the other hand, some may actually help to protect them.  Perhaps the reason that bees do better on certain forage is because the phytochemicals in those plants help the bees to fight pathogens!  I am especially excited by the prospect that there are likely natural plant products that we could supplementally feed to colonies to help protect them from viruses and nosema (I currently have several at hand that I plan to test against nosema).

Bee Detoxification of Allelochemicals

In the first place, bees may not need to detoxify allelochemicals if they simply don’t absorb them in the first place–the bee gut is pretty efficient at simply shepherding some toxins straight through.  Suchail [46] found that only a small percentage of ingested radioactively-tagged imidacloprid (an alkaloid) ever makes it in any form into the bees’ haemolymph or thoracic muscles.

If absorbed, insects then depend largely upon three groups of detoxification enzymes to metabolize the toxins: the cytochrome P450 monooxygenases (P450s), the carboxylesterases (COEs), and the glutathione S-transferases (GSTs) [47].  The production of these enzymes is normally up- or down-regulated by the presence of allelochemicals in the diet.  Bees use the same enzymes to metabolize synthetic pesticides.

Older texts gave credit to the insect fat bodies as being the site of that enzymatic detoxification, but  recent research [48] suggests that even more important are the Malpighian tubules (Fig. 5), which play a major role in metabolism and detoxification of insecticides, as well as secreting antimicrobial peptides in response to infection [49].

Figure 5. Left to right, the bee midgut (or intestine), where most digestion takes place;  the ileum (narrower tube) in the middle; and the head of the rectum  to the right. The slender Malpighian tubules are attached at the junction of the midgut  and the ileum.  The Malpighian tubules and ileum perform detoxification, immune, and excretory functions analogous to the human liver and kidney.  (I took this photo with a pocket digital camera held to the scope, illuminated by a flashlight clamped between my teeth).

Something of interest is that some toxins or toxicants only affect either the adult bees or the larvae.  For example, bee larvae are apparently completely immune to neonicotinoids [[i]]; yet the nectar of summer titi appears to only poison the brood [[ii]].

Another oddity is that there may be instances of a “paradoxical effect,” in which it may take a sufficiently high dose of a chemical to initiate the detoxification response [[iii]], at which point the organism starts to exhibit “immunity” to that toxin.  However, I have yet to come across any instances where this has been demonstrated in bees.


  • Nectar, pollen, and propolis are chock full of plant allelochemicals, many of which may be toxic to bees at the levels found in natural settings.
  • When other forage is unavailable, bees may be forced to work toxic plants that they would normally avoid.
  • Sublethal doses of those allelochemicals may have beneficial hormetic effects upon bees.
  • Some plant allelochemicals may help bees to fight parasites, and bees may self medicate.
  • The coevolution of plants and bees involves complex chemical interactions that we are only beginning to understand.
  • Bees must first detoxify any plant allelochemicals in their diet before they can begin to deal with any additional manmade chemicals.
  • We cannot fully understand the impact of synthetic pesticides upon bee health unless we also take into consideration the above fact.

To be continued

In the next installment, I will explore the interactions between natural allelochemicals and synthetic pesticides.


As always, I’m indebted to Peter Borst for his assistance in research.


Atkins, EL (1975) Injury to honey bees by poisoning.  In The Hive and the Honey Bee, Dadant.

Pellet, FC (1920) American Honey Plants. http://archive.org/stream/americanhoneypla00pell/americanhoneypla00pell_djvu.txt

[1] Wink, M (1991) Plant Breeding: High or low alkaloid levels?  Proc. 6. Intl. Lupin Conf. Temuco, ILA, 326-334. http://www.uni-heidelberg.de/institute/fak14/ipmb/phazb/pubwink/1991/11.%201991.pdf

[2] Gold 2002 Misconceptions about the causes of cancer http://potency.berkeley.edu/pdfs/Gold_Misconceptions.pdf I highly recommend!

[3] http://toxicology.usu.edu/endnote/Pyrrolizidine-alkaloids-in-food.pdf

[4] http://www.efsa.europa.eu/en/efsajournal/pub/2406.htm

[5] Reinhard, A, et al (2009)  Feeding deterrence and detrimental effects of pyrrolizidine alkaloids fed to honey bees (Apis mellifera). J Chem Ecol. 35(9):1086-95.

[6] Trumble, J and M Sorensen (2008) Selenium and the elemental defense hypothesis. New Phytologist 177: 569–572.

[7] Baker , H.G . ( 1977 ) Non-sugar chemical constituents of nectar . Apidologie, 8 , 349 – 356.

[8] Detzel, A and M Wink (1993) Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicals. Chemoecology 4(1): 8-18.

[9] Atkins, EL, et al (1981) Reducing pesticide hazards to honey bees: Mortality prediction and integrated management strategies. Univ. Calif. Div. Agric. Sci. Leafl. 2883.

[10] In Detzel’s experiments, he fed the allelochemicals to the bees in 1:1 sugar syrup.  The midrange of toxicity was at about 0.3%.  Since a caged bee typically consumes about 30µL of syrup a day, that works out to be about 0.1µg of alleleochemical consumed.  Atkins ranked any toxicant with an LD50 of less than 1.0 μg a.i./bee as highly toxic.  Some of the allelochemicals were 100x more toxic than that average.

[11] Sommerville, D (2005) Fat bees, skinny bees. RIRDC Publication No 05/054.

[12] Adler, LS and RE Irwin. 2005. Ecological costs and benefits of defenses in nectar. Ecology 86(11): 2968-2978. http://people.umass.edu/lsadler/adlersite/adler/Adler%20and%20Irwin%202005%20Ecology.pdf

[13] Strauss, SY (1999) Ecological costs of plant resistance to herbivores in the currency of pollination. Evolution 53(4):1105-1113

[14] Linhart, et al (2005) A chemical polymorphism in a multitrophic setting: thyme monoterpene composition and food web structure.  The American Naturalist 166(4): 517-529.

[15] Adler, L. S. 2001. The ecological significance of toxic nectar  Oikos 91: 409-420. http://people.umass.edu/lsadler/adlersite/adler/Oikos00.pdf. Dr. Adler has a substantial body of research on this subject: [http://www.bio.umass.edu/biology/about/directories/faculty/lynn-adler; http://people.umass.edu/lsadler/adlersite/adler/adlerpublications.html]

[16] Singaravelan, N, et al (2005) Feeding responses of free-flying honeybees to secondary compounds mimicking floral nectar. J. Chem. Ecol. 31:2791–2804. http://web.oranim.ac.il/teachers/ido/My%20reprints/Journal%20of%20Chemical%20Ecology%2031%20(2005).pdf

[17] Baker, HG (1977) Non-sugar chemical constituents of nectar.  Apidologie 8(4): 349-356. Free access.

[18] Karban, R, et al (2000) Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia 125: 66-71.

[19] Mussen, EC, et al (1987) Beekeeping in California.  http://www.beeguild.org

[20] Sedivy, C, et al (2011) Closely related pollen generalist bees differ in their ability to develop on the same pollen diet: evidence for physiological adaptations to digest pollen. Functional Ecology 25: 718–725.

[21] Hendriksma HP, et al (2011) Testing pollen of single and stacked insect-resistant Bt-maize on in vitro reared honey bee larvae. PLoS ONE 6(12): e28174

[22] Ibid.

[23] Bozic J., et al (2006) Reduced ability of ethanol drinkers for social communication in honeybees (Apis mellifera carnica Poll.)”. Alcohol 38(3): 179–183.

[24] Castillo, C, et al (2012) Biosynthesis of ethyl oleate, a primer pheromone, in the honey bee (Apis mellifera L.). Insect Biochemistry and Molecular Biology 42: 404-416.

[25] http://scientificbeekeeping.com/the-primer-pheromones-and-managing-the-labor-pool-part-3/

[26] Schmidt, JO and BE Johnson (1984) Pollen feeding preference of Apis mellifera, a polylectic bee.  The Southwestern Entomologist 9(1): 41-47.

[27] Campana, BJ and FE Moeller (1977) Honey bees: preference for and nutritive value of pollen from five plant sources.  J Econ Ent 70(1): 39-41.

[28] Baniecki, JF (2003) Changes in toxicological dogma. http://www.wvu.edu/~agexten/lookwhat/lwot203.pdf

[29] Calabrese, EJ and  LA Baldwin (2003) Toxicology rethinks its central belief. Nature 421: 691-692.

[30] Joseph G Morse (1998) Agricultural implications of pesticide-induced hormesis of insects and mites.  Hum Exp Toxicol  17(5): 266-269.

[31] Guedes, RNC, et al (2009) Stimulatory sublethal response of a generalist predator to permethrin: hormesis, hormoligosis, or homeostatic regulation? Journal of Econ Ent 102(1): 170-176.

[32] Guedes, NMP, et al (2010), Insecticide-induced hormesis in an insecticide-resistant strain of the maize weevil, Sitophilus zeamais. J of Appl Ent 134: 142–148.

[33] Duke, SO (2011) Phytotchemical phytotoxins and hormesis – a commentary.  Dose Response 9(1): 76–78.

[34] http://publications.nigms.nih.gov/medbydesign/chapter3.html

[35] http://www.cliparttop100.com/

[36] Drewnowski, A and C Gomez-Carneros (2000) Bitter taste, phytonutrients, and the consumer: a review.  Am J Clin Nutr 72:1424–35. http://ajcn.nutrition.org/content/72/6/1424.full.pdf

[37] Dutcher, JD (2003) A Review of resurgence and replacement causing pest outbreaks in IPM.  In A. Ciancio and K. G. Mukerji, eds. General Concepts In Integrated Pest And Disease Management. Springer.

[38] Guedes (2009) Op. cit.

[39] James, DG and TS Price (2002) Fecundity in twospotted spider mite (Acari: Tetranychidae) is increased by direct and systemic exposure to imidacloprid.  J. Econ. Entomol. 95(4): 729-732.

[40] Laurentz, M , et al (2012) Diet quality can play a critical role in defense efficacy against parasitoids and pathogens in the Glanville Fritillary (Melitaea cinxia), J Chem Ecol  38:116–125

[41] Singer MS, et al (2009) Self-medication as adaptive plasticity: increased ingestion of plant toxins by parasitized caterpillars. PLoS ONE 4(3): e4796.

[42] Simone-Finstrom, MD, and M Spivak (2012) Increased resin collection after parasite challenge: a case of self-medication in honey bees? PLoS ONE 7(3): e34601.

[43] Després, L., et al (2007) The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol. Evol. 22: 298-307. http://www-leca.ujf-grenoble.fr/membres/fichiersPdf/despres/despresDavidGallet2007.pdf

[44] Manson, JS, et al (2009) Consumption of a nectar alkaloid reduces pathogen load in bumble bees.  Oecologia 162(1): 81-89. http://labs.eeb.utoronto.ca/thomson/publications/Manson%20et%20al.%20nectar%20alkaloid%20reduces%20pathogen%20load%202009%20Oecologia.pdf

[45] Cory JS, Hoover K. (2006)  Plant-mediated effects in insect-pathogen interactions.  Trends Ecol Evol. 21(5):278-86.  http://cals.arizona.edu/ento/courses/ento446_546/readings/Cory_2006.pdf I highly recommend!

[46] Suchail, S, et al (2004) In vivo distribution and metabolisation of 14C-imidacloprid in different compartments of Apis mellifera L.  Pest Manag Sci 60:1056–1062.

[47] Johnson, RM, et al. (2006) Mediation of pyrethroid insecticide toxicity to honey bees (Hymenoptera: Apidae) by cytochrome P450 monooxygenases. J Econ Entomol. 99(4):1046-50.

[48] Yang, J, et al (2007) A Drosophila systems approach to xenobiotic metabolism.  Physiol. Genomics 30(3): 223-231. http://physiolgenomics.physiology.org/content/30/3/223.full.pdf+html

[49] Dow, JAT and SA Davies (2006) The Malpighian tubule: Rapid insights from post-genomic biology. Journal of Insect Physiology  52(4):  365-378.

[50] Lodesani, Marco, pers comm

[51] Atkins, EL (1992) Injury to honey bees by poisoning.  In Graham, JM, ed, The Hive and the Honey Bee.

[52] Stevens, DA, et al (2004) Paradoxical effect of caspofungin: Reduced activity against Candida albicans at high drug concentrations. Antimicrob. Agents Chemother. 48(9): 3407-3411.

Category: Pesticide Issues
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Zombie bees

A parasitic fly was recently discovered to be infesting honey bees– the press wildly extrapolated it into being the cause of CCD.  I’ve kept in touch with the researchers in San Francisco, and with beekeepers in the affected areas.  The study is ongoing.

The fly is a native parasite that normally parasitizes bumblebees and paper wasps.  It is not the species of fly introduced to control the fire ant!

The authors write:
“It is possible that A. borealis expanded its host range to include the non-native honey bee many years ago and has gone unnoticed because infected bees abandon their hive and flies occurred undetected in low densities. We believe it is more likely that the phenomenon we report represents a recent host shift and an emerging problem for honey bees.”
If this is indeed a host shift, that would be bad news. But it could simply be that we’ve just never noticed it. I’ve spoken with the large commercial beekeeper in whose operation the fly was discovered, and he hasn’t even noticed it.
In the Bay Area hives that the researchers studied, it only appeared to be a significant problem in Sept/Oct, and even then only at very low levels–only a few percent of the foragers were infected.
Local beekeepers can test for the parasite’s presence by putting an overhead light near hives at night and collecting any bees that are drawn to it. Put the bees into a jar with ventilation (coffee filter rubberbanded over the top) and allow them to die naturally (I’m using that term very loosely in this case).
Keep the jar at room temperature for a week, and check to see if fruitfly-sized flies emerge. Please let me know if you find any!

Update 5 April 2018–Get involved!  A new citizen science 4-H organization in Minnesota is now tracking reports from beekeepers who have found A. borealis in their operations.  Please contact them at ZomBeeWatch.org

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The Harvard Study on Neonicotinoids and CCD

A recent press release by the prestigious Harvard School of Public Health claims that one of their researchers has found that Colony Collapse Disorder was caused by a common insecticide used on corn.  As an informed beekeeper and environmentalist, I feel that this study calls for standard scientific scrutiny to see whether their claims actually have merit.

At first glance, the study indeed appears to support the hypothesis that chronic exposure to field realistic doses of imidacloprid during summer and fall can lead to late winter collapse of the treated colonies.   But the devil is in the details…

The study got off to a good start—several colonies were fed different “field realistic” doses of imidacloprid in syrup, and colony populations and brood area were measured.   Had the authors stuck to this original design (which has already been performed numerous times in several countries) the results would have been meaningful.  Indeed,after a month of feeding such syrup, the investigators did not observe any adverse effects upon the colonies due to the insecticide!

But then, since the lead investigator seemed to be eager to “prove” that CCD is caused by imidacloprid, he dreamed up the fantastic scenario that in the winter of 2006/2007 that for some inexplicable reason the nation’s supply of HFCS was contaminated with high levels of imidacloprid.  My reading of the paper suggests that the author knows little about bees, little about pesticides, nothing about HFCS, had no understanding of the distribution of systemic pesticides in plants.  This paper is an example of authors so bent on “proving” that imidacloprid is the cause of CCD, that they strain credulity with some of their assumptions and reasoning, and even by changing the experimental protocol midstream!

When the investigators failed to prove their case after a month of feeding spiked syrup—they changed the protocol, and ramped up the doses of insecticide in the syrup to sky high and overtly toxic levels, and then made a series of compounding mistakes, notably by not performing the sort of necessary parasite management required for colonies to survive the winter.  And then, even though the symptoms of the colonies when they died did not match the symptoms of CCD, yet the Harvard press agent claimed that they did!

Unfortunately, there are also a great number of factual misrepresentations and quite a bit of fuzzy thinking in the paper, which obviously was not peer reviewed by any bee biologist nor toxicologist.   I realize, in retrospect, that some of my comments may sound a bit snarky, and I apologize to the authors, whom I’m sure were earnest in their quest to prove their anti-neonic agenda.  Back to the paper, allow me to discuss some of the problems.  The author stated in an interview:

“When other conditions cause hive collapse—such as disease or pests—many dead bees are typically found inside and outside the affected hives.”

Could someone please refresh my memory?  Other than in the case of tracheal mite, which diseases or pests leave many dead bees in a hive?  (Note that starvation or acute pesticide toxicity would not fall into the category of “disease or pest”).  The point is, that the natural behavior of sick or old bees is to abandon the hive—one normally does not find dead bees in hives that have died from parasites, including viruses.

Let’s look at a few more sentences from the paper:

“We hypothesized that the first occurrence of CCD in 2006/2007 resulted from the presence of imidacloprid … in high-fructose corn syrup (HFCS), fed to honey bees as an alternative to sucrose-based food. There are three facts to support this hypothesis. First, since most of the suspected but creditable causes for CCD were not new to apiculture, there must have been an additional new stressor introduced to honey bee hives contemporaneous with the first occurrence of CCD during the winter months of 2006 and early 2007.”

In fact, beekeepers who had never fed HFCS experienced plenty of cases of CCD.  Plus, new stressors such as Nosema ceranae and novel strains of viruses have been strongly associated with colony mortality.

The authors give no justification for their assumption that there was any change in HFCS in 2006.  And as Bob Harrison and others have pointed out, CCD actually started occurring in 2004-2005, prior to the authors’ assumption that tainted syrup hit the market beginning in 2006.  Any HFCS produced from such treated corn would have necessarily have been produced following the season of harvest.

The authors then cite a few studies that show that systemic insecticides are translocated, as they are intended, throughout the plants.  But then they stretch by stating:

“ These study results lend credence to our hypothesis that the systemic property of imidacloprid is capable of being translocated from treated seeds to the whole plant, including corn kernels and therefore likely into HFCS.”

My gosh, this is one helluva assumption!  Without taking the time to simply confirm that imidacloprid winds up in the kernels, the authors assume that it is concentrated there at high levels!  All they had to do was to look at the freely-available results of USDA annual testing of foods for pesticide residues—they would have found that of the 655 samples of corn grain tested, absolutely none showed residues of either imidacloprid or clothianidin!

And then they further go out on a limb by assuming that their imaginary residue of imidacloprid was then somehow concentrated when the corn was used to produce HFCS (ignoring the fact that the vast majority of corn is treated with clothianidin, rather than imidacloprid).  As if that weren’t enough, the authors go into la-la land with some even wilder creative assumptions:

“Since there is no tolerance level for imidacloprid in HFCS, we applied a 10-fold concentrating factor, or 0.5 ppm (500 μg/kg) of imidacloprid in HFCS, by taking into account the uptake by corn plants from seeds that are treated with imidacloprid.”

They simply created this “concentrating factor” out of thin air!  They give absolutely no justification for it.  In the actual process of making HFCS, pesticides are largely removed.  As I stated before, all that the authors had to do would have been to ask Roger Simonds at the USDA Gastonia pesticide testing lab as to the actual measured levels of imidacloprid in HFCS, and thus would not have brought embarrassment to Harvard School of Public Health by such a ludicrous assumption.


The paper turns into farce when the author states:

“we used food-grade HFCS fortified with different levels of imidacloprid, mimicking the levels that are assumed to have been present in the older HFCS.”

Why in the world would the authors “assume” that imidacloprid was present in the older HFCS, but not present in the HFCS that he used in the current study to feed the control colonies?  But then they go on to state:

“ The range of dosages used in this study from 20 to 400 μg/kg were not only environmentally relevant…”

Since when has 400 ppb ever been been considered to be “environmentally relevant”?  Levels of 1-4 ppb are environmentally relevant; levels above 40 ppb are usually considered to be overtly toxic.  So the 400 ppb level is 100 – 400 times as strong as the normal measured levels in the field due to seed treatment! 

“Therefore, we are confident that the imidacloprid dosages applied in this study would be comparable, if not lower to those encountered by honey bees inside and outside of their hives.”

Unfortunately, the authors’ confidence is not supported by any actual field measurements  by numerous other researchers across the world!

The authors state: “There are several questions that remain unanswered as a result of this study. First, the systematic loss of sealed brood in the imidacloprid-treated and control hives may indicate a common stress factor that was present across all 4 apiaries.”

Like, maybe the feeding of 71 (yes, seventy-one) pounds of HFCS was not the best nutrition for the colonies!  The authors neither gave the source of their corn syrup, nor whether it was a brand that has been tested by beekeepers as suitable feed (some brands cause bee health issues).  Since all the colonies in the trial (test and control) started going downhill (and since a quarter of the control colonies also died), it is difficult not to ignore that something was seriously wrong with the entire experimental design!

More to the point, the field investigators should have taken a few nosema or varroa counts, rather than simply assuming that these common parasites weren’t killing the colonies!  For all we know, all the hives could have beeb crawling with varroa or badly infected with nosema.  One statement suggests that varroa was evident: “nor a large number of Varroa mites was observed in hives during the summer and fall seasons,” which suggests to me that the investigators are admitting that mites were indeed observed!

Let’s look at varroa:  the study states that 3-lb packages were installed on March 28.  Surprisingly,  “By May 21st, 2010 all twenty frames in each of 20 hives were drawn out into comb and contained at least 14 frames of capped brood.”  These colonies really took off, meaning that they were virtual varroa breeding grounds.  By late July they averaged about 25,000 cells of sealed brood.

Strange and Calderone (2009) found Eastern package bees to contain about 3 mites per hundred bees, which would work out to about 300 mites in a 3-lb package.  When colonies are rapidly expanding, mite populations double each month.  So from late March through late July, we’d expect the mite populations in these hives to reach 4,800 by late July.  This is a very serious mite infestation level!  Yet, the researchers waited until October 5 to treat with Apistan strips (which are ineffective against mites in many areas of the U.S.)!  Any experienced beekeeper would suggest that these colonies died from a varroa/Deformed Wing Virus epidemic, which leaves deadouts, as the authors observed, “remarkably empty except for stores of food and some pollen left on the frames.”  Unfortunately, the authors only included a photo of a honey frame, rather than a brood frame, which might have been helpful in diagnosing the actual cause of death!  The dosing with high levels of an insecticide would be expected to cause the treated colonies to suffer more from varroa than the untreated controls.

The description of the dead colonies does not match the definitive signs of CCD at all—there was a dwindling of population, rather than a sudden collapse, and no abandoned brood.  Rather the descriptions of the deadouts more closely matched dwindling collapse due to varroa/virus or nosema.

The authors, on a roll, simply do not know when to stop: “If imidacloprid exposure is truly the sole cause of CCD, it might also explain the scenario in which CCD occurred in honey bee hives not fed with HFCS.  Considering the sensitivity of honey bees to imidacloprid as demonstrated in this study and the widespread uses of imidacloprid and other neonicotinoid insecticides, pollen, nectar, and guttation drops produced from those plants would have contained sufficient amounts of neonicotinoid insecticide residues to induce CCD.”

What are they talking about when they say “considering the sensitivity“?  Even the lowest fed dosage (20 ppb) is about 5-20 times higher than that commonly found in nectar, and the other three doses were far higher–it is amazing to me that the colonies were not killed outright!

Speaking of which, I find it odd that the investigators didn’t give any explanation as to why they changed treatment dosages mid trial.  To their credit, they initially treated the colonies with “field realistic” doses of the insecticide: 0.1 – 10 ppb.   I suspect that after feeding the colonies for four straight weeks in July, and not noticing any adverse effects, that they then decided that they had better really hit the colonies hard if they wanted to “prove their case”–so they arbitrarily ramped up the lowest dose to 200 times stronger, and the highest dose to 40x stronger (that oughtta do it!).

When I do the math on their insecticide spiking, their three higher doses provided enough imidacloprid to theoretically kill every single bee in every hive!  I find it hard to understand how they can claim that the dosages were anywhere near “field relevant.”

I can only imagine their surprise and disappointment when after nine weekly feedings of a full half gallon of syrup intentionally spiked to overtly toxic levels, that they still noted virtually no adverse effects! Surprisingly,  the amount of broodrearing was unaffected at the 20, 40, and 200 ppb dosages, and only slightly depressed at the clearly toxic 400 ppb dose!  Note that all the colonies were still alive at midwinter, fully 3 months after the dosing ended!  If anything, this study clearly demonstrated that colonies of bees can survive prolonged poisoning by imidacloprid at excessively high levels!

So why did the colonies die?  Such insecticide exposure to hives in late summer has been previously demonstrated to greatly increase the chance of a colony later dying from nosema or varroa infection during the winter.  In this study, poisoning the colonies all through late summer and early fall likely hampered the ability of the colonies to prepare a healthy population for winter.

The investigators state that they also took biweekly measurements of the cluster sizes of the colonies, yet  oddly chose not to include the results in the paper.  This makes me wonder whether the authors simply decided to exclude any data that did not support their hypothesis?

So although this paper is surely going to be cited by anti-neonic advocates as some sort of supportive evidence, I find it to be a case in which an initially well-designed study (the dosing of hives with a series of four field realistic doses of imidacloprid) turned to farce when the investigators arbitrarily ramped up the doses, and blew it on parasite management.

In my assessment, it appears that the data from this study actually support an alternative hypothesis–that field realistic doses of imidacloprid had no measurable adverse effects upon the colonies.  And even patently toxic doses had little immediate effect.  I suspect that the apparent delayed effect was due to the impact of the insecticide upon late summer colony populations (which the authors inexplicably did not present), which led to later collapse due to parasite buildup.

In reality, the neonicotinoids fully appear to be “reduced risk” insecticides, which under field conditions, when properly applied (no dust issues) have never been associated with significant colony health issues.  Compared to alternative insecticides, the data to date (including that of this study) support the hypothesis that neonicotinoid, when used as seed treatments, are an improvement over the previous classes of insecticides (there are clearly some questions about dust issues, chemigation, foliar and landscape treatments, which I will discuss in an upcoming article).

I find it unfortunate that the press, including both of our national bee journals, gave publicity to this paper without any sort of critical analysis.  Such messages only confuse the public.  Pesticides are a major issue to the beekeeping community.  What we need are well designed and executed studies, (as well as better enforcement of pesticide law) in order to solve these problems.  Sadly, this study just confuses the issues.

UPDATE JUNE 13, 2013

I am occasionally asked to referee scientific publications.  So I contacted the authors of the paper, and asked them if they would answer the sort of questions that I would have asked about their manuscript had I been asked to review the paper prior to publication.

I also sent the questions to the editor of the Bulletin of Insectology in order that they could be published for scientific debate in the usual manner in the Letters page, but unfortunately his publication is not set up for that type of discussion.

Unfortunately, after seeing the questions, the authors chose not to defend their work, so the questions in the abbreviated list below remain unanswered.

The Questions

[I have also added a few comments italicized in brackets]

Readers will likely wish to have a copy of the study [] at hand.  It can be freely downloaded athttp://www.bulletinofinsectology.org/pdfarticles/vol65-2012-099-106lu.pdf.    Remember, these are the typical sort of questions that a peer reviewer would ask when a manuscript is submitted for publication—the referee is expected to go over the paper detail by detail, check the math, make sure that previous research is cited, a challenge the author’s interpretation of the data.

The authors’ experience

Q: Could you perhaps briefly state for the benefit of my readers, your experience as apiarists?

Your assumptions and background research

vanEngelsdorp (2009) reported that “Large-scale losses are not new to the beekeeping industry; since 1869, there have been at least 18 discrete episodes of unusually high colony mortality documented internationally. In some cases, the descriptions of colony losses were similar to those described above.”

In my own beekeeping career, losses due to the initial tracheal mite invasion often reached 70%, and for varroa, up to 90%.  Wilson (1979) reported losses in the ‘70s to “Dwindling Disease” that were nearly as extensive as those from CCD (and the reporting at the time was not fueled by media coverage).  His maps of DD distribution were nearly identical with those of the 2006/2007 CCD incidence.

Q:  Could you please provide supportive evidence to substantiate your claim that:  “never in the history of the beekeeping industry has the loss of honey bee hives occurred in such magnitude and over such a widely distributed geographic area”

[In the following paper, Wilson had a map of the widespread problem of “Disappearing Disease” in 1979.  Wilson, WT and DM Menapace (1979) Disappearing Disease of Honey Bees: A Survey of the United States.  ABJ March 1979: 184-217.]

You state: “First, since most of the suspected but creditable causes for CCD were not new to apiculture, there must have been an additional new stressor introduced to honey bee hives contemporaneous with the first occurrence of CCD during the winter months of 2006 and early 2007.”

Q: Could you please explain why do you not consider the recent invasion of Nosema ceranae, the novel ubiquitous presence of DWV, nor the apparent recent invasion of IAPV to be novel “stressors?

A very similar trial was performed by Faucon (2005), with substantially different results.  As you are well aware, it is standard practice in scientific papers to cite previous similar research.  Yet you do not cite Faucon, nor any other studies in which spiked syrup or pollen was fed to colonies in situ.  [It is a scientific obligation for any author to cite previous research on the subject when he publishes a paper].

Q:  Why did you not cite and discuss previous research, especially that in which the findings conflicted with yours?

Justification of the imidacloprid in HFCS hypothesis

The central tenet of your paper is your hypothesis that HFCS (high fructose corn syrup) in 2006 was tainted with residues of imidacloprid: “The widespread planting of genetically engineered corn seeds treated with elevated levels of neonicotinoid insecticides, such as imidacloprid since 2004 (Van Duyn, 2004), and their acute toxicity to honey bees led us hypothesize a link between CCD and feeding of HFCS containing neonicotinoid insecticides.”

In response, Bayer Crop Science claims that imidacloprid has never been used on more than about ½ of 1% of corn plantings in the U.S.

Q: Do you have evidence to the contrary, or evidence to suggest that the harvest of that 0.5% of corn seed would have been preferentially used to produce HFCS?

You state: “it was the timing of the introduction of neonicotinoid insecticides to the cornseed treatment program first occurring in 2004/2005 that coincides with CCD emergence”

Dr. Eric Mussen observes that several California beekeepers (including myself) experienced CCD in our operations beginning as early as the fall of 2004. This does not appear to fit with your introduction of seed treatment timing.  Nor did Dr. Bromenshenk’s CCD survey find any correlation between CCD and the feeding of HFCS.

Q: Do you have supportive evidence that apiaries fed HFCS were more at risk for CCD?

A major problem with your study, in the minds of many, is the lack of support for your core hypothesis that imidacloprid contamination of corn syrup indeed actually occurs.

Q:  Your hypothesis is that CCD was caused by residues of imidacloprid in HFCS fed by beekeepers to their bees.  Since CCD still occurs through the current time, it seems then that you should be able to find it in 2012 syrup.  Yet in your own testing, there was no trace of imidacloprid in your samples of HFCS.  Some reviewers feel that your own testing disproved your hypothesis!

Q:  Could you please give an explanation for this inconsistency?

Q: Could you please explain your reasoning as to what had changed in the process of HFCS manufacturing between 2007 and the time that you purchased your HFCS (2010?) that would have caused pesticide residues to disappear?

One would assume due diligence on your part to check to see whether the commercial corn seed from which HFCS is manufactured actually contained residues of imidacloprid.  As an “ad hoc panel member of the US EPA Federal Insecticide, Fungicide, and Rodenticide Act (FIFRA) Scientific Advisory Panel,” your lead author (Dr. Lu) would certainly be aware that any residues of pesticides in corn grain would have been published in the USDA’s readily available “Pesticide Data Program Annual Summary, Calendar Year 2007”  [].

In Appendix F of that document (Distribution of Residues by Pesticide in Corn Grain), one can easily find that in 2007 the USDA tested 655 samples of corn grain (from which HFCS is made) and found absolutely no detections whatsoever of either imidacloprid or clothianidin!  Is seems odd to base your entire study on a hypothesis which the main author had every reason to know was unsupported by simple facts!

Q:  Could you please explain why you did not mention the absence of residues in corn seed in USDA testing?

You state: “It should be noted here that the residue levels of imidacloprid, or other neonicotinoid insecticides, have not been routinely monitored in HFCS.”  You call for us to note this as a fact.

Q:  Do you have documentation HFCS is not tested by the USDA or the HFCS manufacturers?

A simple internet search [] reveals that the ARS Tucson Bee Lab tested HFCS for both bee toxicity and contaminants in 2008.

Q:  Why do you not mention this, nor cite their results in your paper?

You state: “One apparent deficiency, in addition to the small number of honey bee hives used in this study, is that we were not able to obtain HFCS manufactured in 2005/2006 for use in this experiment.”

Q:  In light of the fact that the HFCS manufacturers are livid over your accusation that their product was contaminated by a pesticide, implying that they threatened the U.S. populace with pesticide exposure in common food products, did you actually ask the manufacturers to supply archived samples for testing?

Q: And if not, have you yet done so?

Perhaps the most controversial aspect of your study is the statement: “Since there is no tolerance level for imidacloprid in HFCS, we applied a 10-fold concentrating factor, or 0.5 ppm (500 μg/kg) of imidacloprid in HFCS, by taking into account the uptake by corn plants from seeds that are treated with imidacloprid.”

This is a pretty strong assumption, and implies that the EPA, the USDA, the FDA, and the corn syrup manufacturers were all derelict in their duty to protect the public from exposure to high levels of an insecticide in a ubiquitously-used sweetener in the American diet!

Frankly, it appears that your 10-fold “concentrating factor” was simply dreamed up!

Q: What supporting evidence do you have that would suggest that the insecticide would be concentrated by a factor of 10 (as opposed to being removed) in the manufacturing process of HFCS from corn kernels?

Justification of the claim of “field relevance” of dosages

You state: “The range of dosages used in this study from 20 to 400 μg/kg were not only environmentally relevant to those reported imidacloprid levels by studies that are cited previous…”

In a recent review, Cresswell (2011, whom you also oddly do not cite in your references) suggests that “the field-realistic range of imidacloprid concentrations is assumed to be 0.7–10 μg L-1.” [forbenefit of the reader, μg/kg  is equivalent to ppb (parts per billion); μg L-1 is similar, but by volume, rather than weight].

I commend you on your initial range of doses (0.1, 1, 5, and 10 ppb), which do indeed reflect typical levels found in nectar, with 10 ppb being at the far high end.

But after four weeks of feeding these field realistic doses, without explanation in the paper, you switched to much higher concentrations of the insecticide (20, 40, 200, and 400 ppb)—levels which would be considered to be overtly toxic to honey bees!  This is a key question, and a major criticism of the study.  

Q: Could you please elaborate as to why you changed the dosages mid study, and why you apparently changed your minds as to what constituted “environmentally relevant” levels.

In an excellent recent review  on the ecotoxicity of neonicotinoid insecticides to bees (which you also inexplicably failed to cite), Decourtye and Devillers (2010) note that “acute exposure [100 ppb] cannot probably occur in the realistic conditions since the concentrations of imidacloprid and its metabolites, to which honey bees are exposed always have been measured lower than 10 [ppb].”

Q:  Could you please explain how you arrived at the range of high doses that you used, since they appear to be far above (up to 40 times higher than) field-realistic doses?

Q:  Could you please specifically cite studies that have found 400 ppm of imidacloprid in nectar to which bees would normally be exposed to the extent that it could be associated with widespread CCD?

You state: “Considering that honey bees were diluting the concentrations of imidacloprid fed to the hives with natural nectars foraged during the HFCS feeding months (July to September)…”  Yet earlier in the same paper you state that the colonies experienced a nectar dirth [sic] during this period of time. These two statements appear to be contradictory!

Q: Do you have any daily weight gain data to support your contention that the treated syrup was indeed diluted by nectar during the feeding period?

You state: “Therefore, we are confident that the imidacloprid dosages applied in this study would be comparable, if not lower to those encountered by honey bees inside and outside of their hives.”

I find it difficult to believe, by any stretch of the imagination, that nine weekly feedings of  half gallons of 67% sugar solution (for a total of 51 pounds per colony) spiked at 400 ppb (or even 20 ppb) imidacloprid, during the nectar dearth, could be construed to mimic any field-realistic exposure of colonies to the insecticide! 

Q: Would you care to comment?

Questions on parasite monitoring and management

You state that: “Hives were monitored weekly, and managed using standard beekeeping techniques.”

As I’m sure you know, there are few observable signs for varroa infestation, and there are no field signs of Nosema ceranae infection.  Standard beekeeping management these days involves the monitoring of varroa mite levels, typically by natural mite fall, either roll, or alcohol wash [3].

[Since all the colonies in the trial (test and control) started going downhill (and since a quarter of the control colonies also died), it is difficult not to ignore that something was seriously wrong with the entire experimental design!

More to the point, the field investigators should have taken a few nosema or varroa counts, rather than simply assuming that these common parasites weren’t killing the colonies!  For all we know, all the hives could have been crawling with varroa or badly infected with nosema.  One statement suggests that varroa was evident: “nor a large number of Varroa mites was observed in hives during the summer and fall seasons,” which suggests to me that the investigators are admitting that mites were indeed observed!  

Let’s look at varroa:  the study states that 3-lb packages were installed on March 28.  Surprisingly,  “By May 21st, 2010 all twenty frames in each of 20 hives were drawn out into comb and contained at least 14 frames of capped brood.”  These colonies really took off, meaning that they were virtual varroa breeding factories.  By late July they averaged about 25,000 cells of sealed brood.

Strange and Calderone (2009) found Eastern package bees to contain about 3 mites per hundred bees, which would work out to about 300 mites in a 3-lb package.  When colonies are rapidly expanding, mite populations double each month.  So from late March through late July, we’d expect the mite populations in these hives to reach 4,800 by late July.  This is a very serious mite infestation level!  Yet, the researchers waited until October 5 to treat with Apistan strips (which are ineffective against mites in many areas of the U.S.)!  Any experienced beekeeper would suspect that these colonies died from a varroa/Deformed Wing Virus epidemic, which leaves deadouts, as the authors observed, “remarkably empty except for stores of food and some pollen left on the frames.”  Unfortunately, the authors only included a photo of a honey frame, rather than a brood frame, which might have been helpful in diagnosing the actual cause of death!  Note also that the dosing with high levels of an insecticide would be expected to cause the treated colonies to suffer more from varroa than the untreated controls.]

Q: Did you monitor mite levels during the trial?  If so, could you please elaborate on your testing method and share the results?

Nosema is a common pathogen, currently infecting about 50% of colonies, and can be deadly to colonies during winters such as yours.

Q:  Did you take any samples of bees from the colonies to monitor for nosema levels?  If so, could you please share the results?

You state: “Since all hives were considered healthy as they went into fall season, those pathogens posed very little threat to the health of honey bee hives.”

Q: Could you please elaborate on how you determined that the colonies (hives are the wooden boxes) “were considered healthy,” especially in light of the “systematic loss of sealed brood” that you report in your Discussion?

I am surprised that the investigators waited until October 5 to treat for varroa.  This is a much later date than recommended by most authorities (most successful beekeepers strive to treat by mid-August), as viruses can go epidemic in colonies with high mite levels in late summer, leading to midwinter collapse, as occurred in your colonies.

Q: Could you please explain why you waited so late to treat for varroa?

Your choice of Apistan strips as a mite treatment is of interest, since the mites in your colonies would be expected to be descended from those present in the original package bees.  Mites in most commercial operations exhibit high resistance to the active ingredient of Apistan.

Q: Do you have any data on what the actual mite levels were in the colonies in October, and whether the strips were actually effective at reducing the mite infestations to below economic thresholds?

Questions on unpublished data on colony strength

You mention that “notes were also made of the number of frames of adult bees observed.”

Those data would be of great interest, and allow the reader to track any treatment effects upon the colony size over time.  Unfortunately, the results are not included in the paper.  All the treated colonies survived for at least three months after treatments were completed.  I’m curious as to when adverse effects due to treatment became apparent.

[In the study, poisoning the colonies all through late summer and early fall likely hampered the ability of the colonies to prepare a healthy population for winter.]

Q: Could you share your data on cluster size?  I’m especially interested in how colony cluster size was affected during the initial four weeks of treatment at true “field relevant” dosages of imidacloprid.  Of note is that the initial field-relevant doses of imidacloprid appeared to stimulate broodrearing in proportion to the dose!

Q:  Do you have any comments about this surprising finding?

Questions on stored honey

In the trial, you fed a large amount of HFCS to the colonies (approximately 71 lbs).  I’m very curious about the apparent delayed effect due to the feeding of treated syrup.

Q: Did you test any of the stored honey in the dead colonies for the presence of imidacloprid?

In late December, you began feeding supplemental sugar in patty form.

Q:  If the colonies contained adequate stores, why was this necessary?

Q:  Do you have data on how much supplemental sugar was consumed by the various colonies during winter, and did this correlate with either treatment or mortality?

Could the HFCS that you used have been the cause of mortality?

You state: “the systematic loss of sealed brood in the imidacloprid-treated and control hives may indicate a common stress factor that was present across all 4 apiaries.”

I heartily agree, especially since one would expect nutritional and pathogen factors to vary from apiary to apiary!

I feel that it may be premature to reach the conclusion that imidacloprid-induced CCD occurred until you determine the cause of the reduced brood rearing, which you observed was “vastly different from that normally seen in honey bee hives” in your area.  Perhaps the reason was that the HFCS that you fed in the trial was a poor bee food, independent of any pesticide residue. 

In your trial, you fed an extraordinary amount of HFCS to the colonies (13 feedings of ½ gal at 11 lbs per gallon = 71.5 lbs of HFCS).  Few beekeepers that I know of have ever fed this amount of HFCS to colonies.

You cite a study by Dr. LeBlanc from the Tucson ARS lab, who found that storage of HFCS in warm conditions, especially in metal containers, could result in toxic levels of HMF formation.

Q  Could you please tell us how you stored your HFCS and whether you tested to confirm that HMF was not present in toxic levels in your syrup toward the end of the trial?

LeBlanc and his coworkers also determined that there were no imidacloprid residues in any of the several brands of HFCS that they tested! Of note though is that they found that some brands of HFCS caused increased mortality in caged bees.  You state that you used “food-grade HFCS.”

Q: Was it a brand that is normally fed to colonies by beekeepers in your area as winter feed, and do you have previous experience with feeding this brand to your colonies?   Could you please tell us which brand you used, as this is of great interest to beekeepers?

Q:  Did you perform any cage trials to see whether that brand of HFCS exhibited toxicity to bees?

Q: I’m curious as to why you did not feed sucrose syrup as a control group, to see whether the HFCS that you used caused colony morbidity for reasons other than your hypothesized insecticide contamination. Comments?

You state: “the delayed mortality in honey bees observed in late winter months remains puzzling.”  I agree that this is the key issue in your study.  The question is, was it due to the dosing with extremely high levels of the insecticide, the prolonged feeding of HFCS, or to nosema or varroa buildup in the colonies.  Without eliminating the other plausible causes, I feel that it is premature to place the blame for the observed colony mortality solely upon the insecticide.

Questions on dwindling of both test and control colonies

Regarding Figure 1 (brood area tracking), you mention that there were no significant differences in broodrearing due to treatment.  I find this point noteworthy, as well as surprising, given the high dosages of imidacloprid given!

Q: Any comments?

You state: “It should be noted that the steady decreasing trend of sealed brood during the summer months as observed in this study is vastly different from that normally seen in honey bee hives residing in the central Massachusetts area.”

It appears that all the colonies, including the controls, were suffering from some sort of morbidity.  The most likely suspects would be the poor nutrition of the HFCS (independent of the added insecticide), nosema, or the varroa/virus complex. 

Although you were monitoring brood areas weekly, and clearly noted that something was apparently wrong in all colonies, you waited until October 5 to begin any standard parasite treatments.

Q: Could you please explain why?

Figure 2 (the chart of colony survival) is striking, and clearly shows that colonies fed very high dosages a pesticide died sooner than those not fed pesticide.  I do not find the results surprising.  What would be of interest is the starting cluster sizes of the colonies going into winter cluster.  Smaller colonies are well known to exhibit poorer winter survival than strong colonies.

Q:  Did the treated colonies enter the winter with smaller cluster sizes, and could this be the reason for their early mortality?

Did you actually observe CCD, or mere dwindling

You state: “The magnitude and the pattern of honey bee hive loss during the winter months in this study resemble the reported symptoms of CCD.”

Frankly, this is where the CCD researchers that I’ve spoken with have questions.  They do not find the “symptoms” that you reported to be consistent with the markers for CCD!

Q: Did any of the members of your team have any actual previous experience with observing CCD in the field?

The CCD Working Group deliberately named CCD colony collapse to distinguish it from colony dwindle.  vanEngelsdorp (2009) suggests an operational case definition of CCD “characterized post hoc by a common set of specific symptoms: (1) the rapid loss of adult worker bees from affected colonies as evidenced by weak or dead colonies with excess brood populations relative to adult bee populations; (2) a noticeable lack of dead worker bees both within and surrounding the affected hives…”

To the contrary, you describe the dwindling of the treated colonies in your study as: “the strength of hives treated with the highest imidacloprid dose appeared to be weakening as observed by smaller clusters and frozen dead honey bees scattering (on snow) in front of the hives.”  You also show in Figure 3 a lack of sealed brood in a dead treated hive.

Since the “symptoms” that you report do not appear to match those that distinguish CCD, I cannot fathom how you can conclude: “Data from this in situ study provide convincing evidence that exposure to sub-lethal levels of imidacloprid causes honey bees to exhibit symptoms consistent to CCD months after imidacloprid exposure.”

Q: Could you please explain how you can state that the signs that you observed were “consistent” with those of CCD, rather than being typical signs of dwindling due to parasites or poor quality feed?

You state: “Snow usually fell between weekly hive examinations making the observation of scattered dead honey bees in front of individual hives noticeable. Although this observation is not quite reminiscent of the reported CCD symptoms…”

“Not quite reminiscent” is certainly an understatement—either you observed the signs of CCD or you didn’t!  In my personal beekeeping experience in a cold winter area, scattered dead bees on snow in front of hives during winter are normal, due to aging bees flying out to die, and is indeed not at all “reminiscent” of CCD symptoms.

Q: Why do you bring up this observation—is it not normal in your area to see dead bees in the snow following flight days during winter?

It appears that you consider the lack of dead bees in the hive to be unusual.  When I check the weather history for Worcester for the winter of 2010, it appears that there were an adequate number of days warm enough for bee flight through early December to allow virus- or nosema-infected bees to fly off to die.

So I’m not clear as to whether the dwindling of clusters reflected the normal self removal of sick, aged, or infected bees, or was due to unusual flight behavior in cold weather due to imidacloprid exposure (which your discussion hints at).

Q: Do you have any observations that could help clarify when the bees flew off?

Your definition of “sub-lethal”

You state: “Data from this in situ study provide convincing evidence that exposure to sub-lethal levels of imidacloprid in HFCS causes honey bees to exhibit symptoms consistent to CCD”

I think that everyone would be in agreement that the doses used during the first 4 weeks of feeding would be considered to be “sub-lethal.”  You did not report any adverse effects from those dosages, as expected.

But then, without explanation, your team ramped up the doses considerably.  Yet you still claimed that they were “sub-lethal.”  I must question whether the dosages that you used in 9 weeks of late-summer feeding would be considered to be “sub-lethal.” 


Your team added to the syrup for each weekly feeding doses of imidacloprid ranging from 51.9 μg to1038 μg.

You report that each colony covered about 20 frames.  There are typically about 1750 bees per covered frame, so that would suggest colony populations in the range of 35,000 bees.

You do not report how quickly the colonies emptied their feeders, but in my practical beekeeping experience, a half gallon of syrup is typically consumed in less than 24 hours, so unless you tell us otherwise, we can assume that the administration can be treated as 24-hr dosings.

Cresswell (2011) in his meta analysis of imidacloprid toxicity trials, found that observable toxic effects began to occur at doses exceeding about 2 ng per bee.  Bayer scientist Maus (2003) states that acute oral LD50 of imidacloprid to honey bees is as low as 40 ng/bee.

Let’s convert your four dosing regimines to ng/bee:

51.9 μg/colony =                    51,900 ng/colony = 1.5 ng/bee

103.8 μg/colony =               103,800 ng/colony = 3 ng/bee

519 μg/colony =                   519,000 ng/colony = 15 ng/bee

1038 μg/colony =              1,038,000 ng/colony = 30 ng/bee

So by my arithmetic (based upon previously published research), even your lowest rate of dosage gave a marginally toxic dose of imidacloprid to each and every bee in the hive, and your highest dose approached the LD50  for all the bees in the hive!

This is a key question.  It appears to me that the high doses of imidacloprid that you used hardly be considered to be “sub-lethal.” 

Could you please explain how your team can consider such concentrations to be “sub-lethal”?

Your hypothesis and conclusions

Quite a number of trials worldwide have been performed to apply Koch’s third postulate in an attempt to create disease in healthy bee colonies by the feeding of field-relevant doses of neonicotinoid insecticides.  To date, that goal has eluded all other research teams other than yours!

For example, in a similar but more thorough study (Faucon 2005) the conclusion was that “In any case, during the whole study, mortality was very low in all groups, with no difference between imidacloprid-fed and control colonies.”

Q: Could you please elaborate as to why you feel that your results were different than all other trials to date? [this is normally done in the Discussion section of a scientific paper].

You suggest that: “The survival of the control hives managed alongside with the pesticide-treated hives unequivocally augments this conclusion.”

“Unequivocally” is a pretty strong statement!  In actuality, your Figures 1, 2, and 4 suggest that the control hives were suffering from serious morbidity, and on the same path to mortality as the treated hives, only to be rescued by the infusion of pollen in spring!  Note that the control group suffered 25% mortality (which hardly constitutes “survival”), which raises serious questions about any conclusions to be drawn.

Q: Could you please provide your cluster size observations to help the reader to determine the degree of morbidity in the control colonies relative to that of the treated colonies?

Q: Did you inspect the brood combs of the deadouts for guanine deposits, which would indicate that varroa was present at high levels as the colonies dwindled?

Q: Did you sample any of the dead bees in the snow for nosema?

Since all colonies in your trial suffered from unusual morbidity, the question is raised whether such morbidity was due to the unnatural feeding of the particular brand of HFCS that you fed to the colonies.

You state: “It is likely that CCD was caused by feeding honey bees with low levels of imidacloprid in HFCS throughout their lifecycle in which toxicity occurred during the larval/pupal stages and was later manifested in the adult honey bees.”

I find a paucity of published data on the toxicity of imidacloprid to bee larvae, or whether residues in syrup even make it into the larval food.  [The neonicotinoids are apparently virtually nontoxic to larvae (Lodesani 2009); Piotr Medrzycki, pers comm]

Q:  Could you please cite research to support your claim that “it is likely” that “toxicity occurred during the larval/pupal stages”?

Q: Similarly, could you please cite research to support your claim that “it is likely” that any such toxicity would be “later manifested in adult honey bees”?

SciTech Daily’s article [4] on the paper says, “Strikingly, said Lu, it took only low levels of imidacloprid to cause hive collapse — less than what is typically used in crops or in areas where bees forage.”

In actuality, it appears to me that the initial, field-realistic, levels of imidacloprid that you feed the first four weeks did not cause observable adverse effects. 

Q: How can you state that “it took only low levels of imidacloprid to cause hive collapse” when in your own paper you refer to it as “high imidacloprid dosing”?

Then even after feeding clearly lethal levels of the insecticide for an additional nine consecutive weeks, you still did not observe colony mortality!

It was only three full months after you ceased feeding the insecticide that you observed the first mortality, following a period in which the “systematic loss of sealed brood [in all] hives may indicate a common stress factor that was present across all 4 apiaries.”

[The authors state: “Considering the sensitivity of honey bees to imidacloprid as demonstrated in this study.”  Actually, no such “sensitivity” was demonstrated at all!  Even the lowest fed dosage (20 ppb) is about 5-20 times higher than that commonly found in nectar, and the other three doses were far higher–it is amazing to me that the colonies were not killed outright!  Yet no treated colony apparently showed any ill effects even after 13 weeks of continuous feeding with insecticide-spiked syrup!]

An alternative explanation for the results

Your proffered hypothesis is that: “Data from this in situ study provide convincing evidence that exposure to sub-lethal levels of imidacloprid in HFCS causes honey bees to exhibit symptoms consistent to CCD 23 weeks post imidacloprid dosing.”

To many, your evidence is actually less than convincing.

I suggest an alternate hypothesis that all the colonies were on a downhill track by late summer, and dwindled due to either HFCS toxicity or parasite loads, and that the feeding of unrealistically high doses of an insecticide merely accelerated the decline of the treated colonies.

Q: Do you have any evidence that would help to falsify this alternative hypothesis?

Feel free to make any additional comments at this point.  Thank you in advance for taking the time to answer these questions for the benefit of the beekeeping community!

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The Birds and the Bees

I was greatly concerned when I read that news item that the neonicotinoid seed treatments might be causing the decline of bird populations.  I don’t know whether you read the referred paper (http://www.abcbirds.org/abcprograms/policy/toxins/Neonic_FINAL.pdf), which was earnest and detailed.  Unfortunately, it was mostly speculative, as opposed to being based upon field evidence.  The authors themselves, in the section “Incidents [of observed bird poisoning]”, state:

“The monitoring and reporting of bird kills in the US has been very limited in recent years … There have been relatively few reports involving neonicotinoids. This is in part because the acute toxicity of these insecticides is lower than that of the organophosphorous and carbamate insecticides that they replaced.”

That is exactly why the EPA favors neonics, since they kill so fewer birds than previous classes of insecticides!  

Odd, I thought!  Does the American Bird Conservatory know something that the EPA is unaware of?  So as a reality check, I went to the heart of the Corn Belt, where there is the most intense use of neonic-treated seed.   I then determined which species of birds would be most affected by treated seeds.  Obviously, it would be seed-eating species that forage in the bare corn or soy fields as they are being planted (planting generally occurs only once each spring).  These would be large birds such as quail, pheasant, and partridge (the seeds are too large for small birds, and many small birds eat insects, not seed).  I lucked out and found a 2010 report by the Upland Game Bird Study Advisory Committee.  In it, they only mentioned pesticides in passing, suggesting that the use of herbicides suppressed quail populations:

“Fewer weeds in association with cropland are detrimental to the quail population.”

This is the same thing with honey bees and other wildlife—the current fencepost to fencepost monoculture planting of corn and soy has eliminated most of the food sources of pollinators and other wildlife.  And any plant or animal that has the audacity to actually compete with, or to eat any of those cultivated plants is labeled as a “pest,” and killed with pesticides (herbicides or insecticides).  And any bird or beneficial insect (such as honey bees) that depends upon the weed species or benign insects for nourishment thus has its food source eliminated in the process.  Understand that this is an indirect effect due to lack of forage, not due to poisoning from those pesticides.

This is exactly the situation with the Iowa game birds.  You can download the report athttp://www.iowadnr.gov/portals/idnr/uploads/Hunting/upland_report.pdf.  The Committee has tracked the populations of these grain-eating species since 1960, and produced graphs that demonstrate how populations of these birds are closely linked to the amount of farmland dedicated to bird-friendly wheat and oats (which have largely been replaced by corn and soy), and to weather events (partridge benefit from drought, other species are killed by cold winters).  There is no evidence that the declines of these bird populations are due to insecticides!

The same correlations apply to honey bees—the bee population is closely linked to the availability of forage and weather conditions (drought or cold winters are rough on bees).

As for the insect-eating birds, of course their populations will suffer if there are no insects to eat.  But the fact is that the seed treatments are targeted against only those sucking and chewing insects that attack the newly-emerged plants, and have virtually no effect upon insect populations other than those on the individual plants growing from the treated seed—due to the precise targeting, there is no overspray effect, so insects can continue to thrive in any weeds and field borders.  Understand, that farmers will always control insect pest populations—the use of seed treatments replaces far more environmentally-damaging spraying of insecticides (the vast majority of which goes into the environment without ever hitting the actual target insect).

As a second reality check, I figured that the corpses of birds as large as pheasant, quail, and partridge would be quite noticeable if they were to die from pesticide poisoning (they would likely be lying in bare fields immediately after planting, and since there are 160,000 licensed Iowa hunters, those 160,000 pairs of eyes would likely notice).

If you go to the American Bird Conservatory’s website, there is a portal for looking up all incident reports of bird kills.  For many common insecticides, there are reports of thousands of birds being killed.  However, for clothianidin (the most common neonic seed treatment) there is not a single report of a bird kill (check it yourself)!  The reality is that animals are cautious about eating new foods (such as the brightly-dyed treated seeds that may occasionally show up behind the planter once a year).  The strong stimulant effect of the neonicotinoids is unpleasant to birds, and they appear to quickly learn to avoid eating any more of the seed. 

So my two reality checks of the arguments that the neonic seed treatments are actually causing bird deaths or population decline both fail to hold water.  The same for the references to Dr. Tenneke’s studies in the Netherlands, in which bird populations have declined in wildlife preserves as well as in farmland (I’ve corresponded with Dr. Tennekes at length).

So this is what confounds me—here is a group of well-meaning advocates for birds (who doesn’t love birds?) calling for an immediate ban on an insecticide that has had zero on-the-ground reports of bird poisoning, and has replaced the use of insecticides that previously caused many documented bird kills (the situation is nearly identical with honey bees)!  They are calling for a ban based solely upon supposition, without any direct evidence.  And this despite the fact that the seed treatments are considered to be “reduced risk” insecticides because they are designed to be more bird (and bee) friendly than the alternatives!

Ah, the alternatives!  If the farmers were not to use seed-treatment insecticides, they would still need to control the rootworms, cutworms, flea beetles, and aphids.  The insecticides that they would then spray are well documented at causing bird deaths—be careful what you ask for!

Now don’t get me wrong—all pesticides are greatly overused in the U.S., generally applied as crop insurance, rather than in integrated pest management.  Our system needs great improvement, and organic farming shows viable alternative methods.  But I’m talking about immediate reality—the banning of the seed treatments would be devastating to both the birds and the bees in the short term!

I approach this subject through the Big-Picture eyes of a biologist, ecologist, and environmentalist, as opposed to the more tunnel vision view of some activists.  Here is the bottom line:

Every human being on Earth is in competition with all other species for the limited supply of “biologically productive” land upon which we grow our food, fiber, and biofuel crops.  When such land is converted to farmland, the entire ecosystem of that tilled acreage is utterly destroyed (even in organic agriculture)—every herb, shrub, and tree eliminated, and every burrow, log, or other hiding place removed,  and replaced by an artificial ecosystem  of exotic plants grown in monoculture, and again destroyed prior to planting the next season.  The only native species that we do not deny the right to exist are those that do not compete in any way with our crops, and that do not require the habitats or shelter that we destroyed by tilling the land!

As an ecologist/environmentalist, our most pressing problem at the planetary scale is the loss of species (extinction is forever).  The main cause of extinction is habitat conversion into farmland (as well as climate change).  Human demands upon the Earth’s finite ecosystem are growing.  There are only about 4.5 acres of biologically productive land on the surface of the Earth available for each current human inhabitant.  Depending upon the culture’s lifestyle, we use anywhere from 25 acres (U.S.) to as little as 1 acre (Bangladesh) to feed and clothe each person.  Unfortunately for the bee (and many other species), due to human population growth there are over 200,000 additional human mouths to feed every single day—each requiring the conversion of another couple of acres of natural habitat into farmland! 

The obvious problem is human population growth, which is due to two main technologies—the conversion of natural habitat to farmland and reduced infant mortality due to health care.  We are not going to backtrack on either of these—no one wants to go back to hunter-gathering or high infant mortality rates.  Technology got us into this mess, and we must embrace technology to get us out.  Our goal should be to use the most ecologically-friendly technologies.

The practice or organic farming was a great start, with its biodiversity, crop rotation, and independence from synthetic fertilizers and use of integrated pest management.  But its rigid and arbitrary orthodoxy has outlived its usefulness as a large-scale model (plus the concept of “organic farming” has been perverted by corporate agriculture; “certified organic” agribusiness bears little semblance to the ideals of organic farming).

Our goal should be to move ahead by adopting the concept of “agroecology”:

Agroecology is both a science and a set of practices. It was created by the convergence of two scientific disciplines: agronomy and ecology. As a science, agroecology is the “application of ecological science to the study, design and management of sustainable agroecosystems.”   As a set of agricultural practices, agroecology seeks ways to enhance agricultural systems by mimicking natural processes, thus creating beneficial biological interactions and synergies among the components of the agroecosystem. It provides the most favourable soil conditions for plant growth, particularly by managing organic matter and by raising soil biotic activity. The core principles of agroecology include recycling nutrients and energy on the farm, rather than introducing external inputs; integrating crops and livestock; diversifying species and genetic resources in agroecosystems over time and space; and focusing on interactions and productivity across the agricultural system, rather than focusing on individual species. Agroecology is highly knowledge-intensive, based on techniques that are not delivered top-down but developed on the basis of farmers’ knowledge and experimentation.

The above quote was taken from a must-read document for anyone interested in the future of agriculture:http://www2.ohchr.org/english/issues/food/docs/A-HRC-16-49.pdf

The practices of agroecology allow more latitude than the arbitrary restrictions of “organic” farming, and are much more likely to be embraced by the agricultural community as a whole.  These practices greatly reduce the amounts of pesticides or off-source fertilizers, but do not categorically exclude them.  Nor would agroecology prohibit the use of genetic engineering in the development of, for example, drought- or saline-resistant crops.  Agroecology adopts the best of all worlds, with sustainability and the maximizing of ecological biodiversity as its goals.  Agroecology is especially targeted to help small farmers, but can also be adopted by agribusiness.

Now don’t get me wrong—I’m all for organic farming, and practice it myself in my garden and orchard (although, hard as we try, it is nearly impossible for most beekeepers to qualify for “organic” certification due to unrealistic restrictions).  However, the “all or nothing” restrictive hurdles of meeting organic certification limit its overall environmental impact in agriculture as a whole–less than 1% of U.S. cropland is certified organic.  That means that there would be far greater overall positive environmental impact if the other 99% made even tiny changes towards agroecology (without needed to meet every single detail of “organic” certification).  I’m a Big Picture kind of guy, and am looking for what is best for the environment overall.

I wholeheartedly support organic farming, the American Bird Conservatory, and beekeepers.  But their misinformed calls for the banning of all neonicotinoids or genetically engineered crops is at odds with the larger environmental perspective of lessening the impact of the human population upon the other species on this wondrous planet.

Category: Topics
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Simple Early Treatment of Nucs Against Varroa

First published in: American Bee Journal, April 2013

Simple Early Treatment of Nucs Against Varroa

Randy Oliver


First published in ABJ April 2013

Starting the season with a low level of varroa allows a colony to get a jump on the mite and its associated viruses.  I tested a simple method for incorporating varroa management into nuc production.


When I try to understand something about beekeeping, I seek out examples from the extreme ends of the spectrum.  For that reason, I often look to the experience of our Canadian brethren, due to their long, cold winters and bounteous honey crops.  We can take advantage of those huge honey yields to allow us to discern even small effects upon honey production from the impact of the varroa mite, eh?  Dr. Rob Currie found that surprisingly low mite levels can affect yield [1], recommending that the late spring varroa infestation rate not exceed 1 mite per 100 bees.  At this year’s ABF convention, Dr. Medhat Nasr described how beekeepers in Alberta, Canada find that they get best results with very early season mite control.

I’ve previously described how one can reduce mite levels by using queen cells to make up spring nucs [2]; but we can go a step further if we hit the nucs with a miticide at the same time!  The question then, is which miticides are gentle enough so as not to adversely affect the newly-mated queen or the buildup of the nuc?

Several studies have found that the synthetic miticides may have adverse effects upon queens, so I hesitate to use them.  That leaves the essential oils and organic acids.  I know from experience that the most effective essential oil—thymol–is disruptive to broodrearing, so I’d rather not apply it to small nucleus colonies (there are also temperature issues with thymol).

As far as formic acid is concerned, the manufacturer of Mite-Away Quick Strips™ recommends that they be applied only to colonies exceeding 6 frames in strength [3], and anecdotal reports from a number of beekeepers suggest that formic acid, under some circumstances, may be risky to queens–an observation supported by research by Dr. Pierre Giovenazzo [4].

So that leaves us with only two proven miticides–the recently-registered product HopGuard® (hops beta acids) and the unregistered oxalic acid.  The manufacturer of Hopguard states that the product is safe for queens [5], so it sounded promising.  The oxalic acid dribble was a likely candidate as well, since it also does not appear to negatively affect queens [6,7].  Giovenazzo [8] had also tested oxalic acid with good results.

However, both Hopguard and oxalic have one drawback—since they only kill phoretic (hitchhiking) mites, and since either product is only active for a few days in the hive, they don’t hit the reservoir of mites in the brood.  Both of these miticides are most effective in broodless colonies, such as in fall, or during a period of induced broodlessness, as demonstrated by Wagnitz and Ellis [9]–who caged the queen in late summer, replaced her in a few days with a queen cell, and then later applied oxalic acid after all the brood had emerged.

I normally start nucs with queen cells.  It occurred to me that in such nucs, a window of opportunity exists for the effective use of short-term natural treatments against varroa.  It’s all about the timing.  A nuc is made up with frames of brood from an established colony.  That brood will contain mites.  Some of the unsealed brood will continue to be invaded by mites for up to 9 days after the nuc is made up (bottom colored bar).  But any and all brood from the parent queen will have emerged by Day 21 after the making of the nuc (Fig. 1).

Figure 1.  The theory behind the early treatment of nucs—it’s all about timing!  There is a brief window of opportunity from Day 19 to Day 21 after make up in which every mite in the nuc is forced out of the safety of the sealed brood.  A short-term treatment applied at that precise time could result in a very effective kill of the now-exposed mites!

I insert 10-day* queen cells into the nucs on the day after I make them up.  That means that the new queen won’t emerge until Day 2 or 3 after make up (middle colored bar), and not begin laying eggs until around Day 11 after make up (sometimes a bit sooner).

But the mites cannot yet enter the new brood, since varroa doesn’t invade a cell until about 8 days after the egg is laid [10].  That means that the first opportunity for the mite to hide in new brood generally occurs around Day 19 post make up of the nuc (upper colored bar).  So from Day 19 through Day 21, virtually every mite would be exposed to the treatment!

OK, this sounds good in theory.  So I ran two trials to see just how well it actually worked in practice.

* I no longer use cells any more ripe than that, because since I started selecting for mite resistance, the occasional batch of cells will emerge on Day 11, rather than on Day 12 after grafting.

Trial #1

Materials and Methods

The unusually warm winter of 2011-2012 was a good opportunity to test the method, since mite levels were unacceptably high by early April.  We used a batch of nucs grafted from two queen mothers (the majority from one mother) on April 12.  On May 1 (Day 19 after make up) we equalized them to 48 queenright nucs each containing 5 full frames of bees by adding frames from the unmated nucs to the mated ones, and by shaking bees, which helped to randomize the original mite infestation rates.  At this point (again apparently due to warm weather), some larvae from the new queens were already being sealed, meaning that some mites may have already infested those cells prior to treatment.

Since the nucs were scatted in a rough line in the order of make up, every 4-5 in the row would have come from the same parent colony, so we marked them sequentially down the line for treatments in order to avoid any effect from the original brood sources.  After allowing 2 hours for them to settle down, we took samples of ½ cup of bees (~320 bees) from each nuc, preserved them in alcohol for later washing for mites, and then applied treatments as below (Table 1).

Treatment Application
Control Open and smoke alone
Hopguard® 1 strip in center of nuc
Hive Clean®* 1- 15mL packet dribbled evenly over seams of bees
Oxalic acid dribble 5mL per seam of bees  3.2% w:v oxalic acid solution in 1:1 syrup**
* Bee-Vital Hive Clean® is a widely-used product from Austria, containing water, sugar, oxalic acid, citric acid, formic acid, and propolis.


Table 1. Treatments used on nucs, 12 colonies in each group.

After a week, we moved the nucs to another yard, placing them in groups of 4 facing out 90 degrees to each other, and rotated to equalize the directions of the entrances for the various treatments.  Shortly afterward, we worked each nuc into a single, adding 5 frames of foundation.  We fed 1:1 sucrose syrup equally as necessary to augment the natural honey flow.

We took mite samples again at Day 37, Day 51, and Day 87 post treatment.

Results and Discussion

The mite infestation rates of the groups are shown in Figure 2 (Day 0 is now reset from the treatment date).

Figure 2.  Changes in mite infestation rates over 87 days (approximately 5 to 6 mite reproductive cycles). Note that the infestation rates at Day 0 were exaggeratedly high due to there being no brood in which mites could hide.  Standard errors of the means indicated.

The differences between the first two bars are the most indicative of the efficacy of the treatments, with the greatest reduction being from the oxalic treatment.  Mite infestation rates climbed at a fairly steady rate after treatments.  My treatment threshold is 2 mites per 100 bees.  This level was exceeded in the control group (which began with the lowest mite level) by the first time point.  By contrast, the mite level in the oxalic group (which began at nearly twice the mite infestation rate of the controls) was still well below threshold at three months!

To more easily compare the effects of treatment, I normalized the mite population growth curves for all groups to start at 100% (Fig. 3).

Figure 3.  Normalized curves of mite population growth.  The mite infestation rate nearly tripled in the control group over the course of the trial.  The mite rate of the oxalic group even three months after treatment was only slightly higher than half the starting rate!

The mite count data need to be taken with a bit of caution, as they were only single samples from each colony at each time point, and thus have a built in degree of potential error, especially in the low ranges, which give disproportionate influence to any single mite in (or not in) the sample.  However, I’ve carefully inspected the raw data, and feel that the results are meaningful, despite the variability in counts.

The intermediate performance of Hopguard and Hive Clean (applied at manufacturer’s recommended rates) suggests that their efficacy was less than that of the oxalic dribble.  The registrants may need to adjust the suggested treatment rate for nucs.

Note also that each colony had received a new queen, who may have passed on mite resistance to her offspring.  Indeed, in 3 of the 10 colonies in the control group which made it to the end of the trial, the mite counts were lower at the end of the trial than they were in the beginning.  But compare this to the oxalic group, in which mite counts went down in 9 out of 11!

Colony Survival and Productivity

We removed 9 colonies during the course of the trial due to failure or disease (EFB), roughly spread among groups.  The oxalic group had the lowest rate of failure, with only one removal.

Measuring the productivity of the nucs was problematic, since the main honey flow essentially failed.  On July 27 (Day 87 post treatment) I opened every hive in the test apiary, excluding (censuring) any that had superseded, or with abnormally small populations.  I recorded which colonies fell into one of two extremes from the norm (which had roughly filled a third to a half of the second deep with honey)—as “productive” (having nearly filled the second deep with honey) or as “nonproductive” (having barely touched the foundation).  The results were unexpected:

  • · Of the 13 “productive” colonies, only 3 had received an acid treatment (oxalic or Hive Clean).
  • · Of the 7 “nonproductive” colonies, 6 had received some form of acid treatment.
  • · The Hopguard group contained the highest proportion (6 of 10) of productive colonies
  • · Of the 13 “productive” colonies, 4 had high mite counts (4.7-13 mites/100 bees).

I don’t know whether the apparent lack of production of the acid-treated colonies was a fluke, or whether the acid treatment had some sort of long-term effect upon productivity–the lack of normal honey flow may have confounded the results.  Giovenazzo [11] also observed a nonsignificant 13% reduction in honey yield after oxalic treatment, but he applied twice the dosage of oxalic acid as I did.    This potential effect certainly demands further investigation!  On the other hand, compare this result to the grading for colony strength in Trial 2.

Trial #2

Materials and Methods

We ran a second trial with oxalic dribble alone to see whether we would obtain similar results as from Trial 1.  Grafting (all from the same queen mother) took place May 3, and we made up 4-frame nucs 9 days later.  In this trial, the weather was warm, and the queens started laying unusually early, with mature larvae at Day 15 after nuc make up.  We equalized 36 queenright colonies to 5 frames of bees on that date.

We alternately treated the hives the next day (May 28), with either oxalic dribble or sham opening, but did not take initial mite counts.  This treatment timing was earlier than optimum, since workers from the parent queen would still be emerging for 5 more days after treatment, possibly compromising the efficacy of the treatment.

After a week, we moved the hives to another yard and worked them into singles, adding 5 frames of foundation.  The honeyflow failed to materialize in June (but pollen was abundant), so we fed the colonies equally with 1:1 sucrose syrup.  The strongest colonies were just filling the 10th frame at grading on Day 69 after making the nucs (Fig. 4).

Figure 4.  Timeline of Trial #2.Results and Discussion

All colonies in the oxalic group survived to the end of the trial; three failed in the control group.  Again, the oxalic dribble substantially suppressed mite infestation rates.  I present the results differently here, showing the distribution of mite rates across the treatment groups (Fig. 5).  The green bars represent the control group, which had a median value of 4 mites per 100 bees at Day 53 post treatment, compared to a median of 1 mite per 100 bees for the oxalic-dribbled group.

Figure 5.  The mite count of the control group was distributed around 4/100 bees, with 2 colonies having excessive counts.  On the other hand, 12 of the 18 OA-treated colonies had counts of 1/100 bees or less.

I observed no negative effects due to treatment of the nucs with oxalic dribble.  Only two colonies in the entire yard went queenless—both were in the untreated group.  Overall, the oxalic-dribbled colonies were substantially stronger at 53 days (2.5 brood cycles) after treatment (Fig. 6).  This result reflects those of Giovenazzo [12], who also observed stronger colonies after oxalic treatment (although not statistically significant).  One plausible explanation for this result is that the knockback of mites just prior to the first round of brood being sealed is enough to break the virus infection cycle of the first generation of bees, allowing for greater longevity of those bees.

Figure 6.  Distribution of colony strength at the end of the trial.  The median strength of the control group was 7 seams of bees; of the oxalic-dribbled group, 9 seams.  This result suggests that any negative effect of the oxalic dribble was more than compensated for by the benefit of mite reduction.

I was curious as to whether differences in strength of the colonies was related to nosema infection, so I checked a 20 house-bee sample from each of the three weakest, and three strongest colonies, with representatives included from each treatment group.  None of the strongest colonies showed nosema spores, but two of the weakest did—one of which showed 30 spores per field of view (1 mL/bee dilution).  I squashed an additional 10-bee sample from that colony one bee at a time—only 1 of the 10 was moderately infected.

So, did colony strength reflect the mite infestation rate?  I plotted colony strength vs. final mite count (Fig. 7).

Figure 7.  There was a distinct trend that those colonies with higher mite counts tended to be weaker, although the correlation was weak, perhaps due to the lack of precision in single-sample mite washes.

Overall Discussion

Despite the fact that in both trials some brood had already been sealed by the time I applied treatment, the method was not only very effective at reducing mite levels (to 1 per 100 bees in most colonies), but also inexpensive (pennies) and quick.

Based upon the early results, we treated several hundred nucs this spring with oxalic dribble at Day 19, and did not notice any difference in queen failure over our normal low rate.

Practical application:  following only two mite treatments in the past 9 months (one oxalic dribble in November, and the oxalic dribble over the nucs in May)  our mite counts across the board in late July were still gratifyingly low—averaging a bit less than 2 mites per 100 bees (some of this was also due to breeding for resistant stock).

But how in the world, you say, will I be able to keep track of treatment window dates during the hectic spring season?  That was also a major concern to me, since during our spring nuc making frenzy I often wouldn’t be able to tell you the day of the week!  I solved the problem by printing up a simple spreadsheet (Fig. 8) that I could check each morning.  For the cells grafted on any day, it shows the two critical dates in red—the last day that we can make nucs for that batch, and the 19th day for queen check and treatment.

Table X.  A portion of my queen rearing spreadsheet for 2012, which helped me to keep my dates straight.  The two critical dates are in red.  In order to avoid weekend commitment as much as possible, I don’t graft on Wednesdays or Thursdays.  I fill in the grafting details and yard in which the nucs are placed.

The above spreadsheet made it really easy to pull off the timing of treatments despite my perpetual disorganization (and actually made me feel somewhat professional)!  The method only required one slight change in our regular production of nucs.  We normally check for queen rightness two weeks after putting in the cells (good mating weather permitting), but in order to save trips to the nuc yards, we now wait 19 days, so that we can do three things on the same visit:

  1. Check for laying queens.  On Day 19, any queens from the grafted cells should normally have a good pattern of open brood, and it is just before the date that any emergency queens or laying workers would have started laying.
  2. We combine the frames of bees from the unmated nucs with the queenright ones to boost them all to 5 frames of bees.
  3. We then dribble them with oxalic acid before putting the lids back on.

By this method, the added oxalic dribble only adds a few seconds per nuc to our normal routine, plus by waiting a few more days to check for laying queens, we weed out the early failures or poor layers.

Possible Improvements On The Method

In warm weather, there may be brood from the new queens being sealed a few days earlier than Day 19, so you should check to see whether you need to treat earlier.  If you find this to be the case, it may be of benefit to make the nucs up a few days before the cells are ripe, to allow the original brood (and mites) enough time to emerge.

The efficacy could also be improved by treating the parent colonies of the nucs with formic acid a few days prior to splitting them.  If one makes up nucs by the “yard trashing” method (the complete breakdown of the parent colonies into nucs), any queen loss due to the formic treatment would make little difference.

Since mites continue to enter brood in a nuc for 8 days after make up, efficacy could potentially be improved by applying an additional oxalic dribble or Hopguard strip at make up.  Let me also make clear that I have not given up on Hopguard or Hive Alive (should it be registered in the U.S.)—both show potential.


This method uses precise timing, combined with making normal colony increase, to gain the most advantage of residue-free “natural” mite treatments.  The oxalic dribble costs pennies and takes seconds to apply.  We already love it for early winter treatment at cessation of broodrearing, and now can also use it in spring.  Our findings also call for more research on the possible effect of oxalic dribble on productivity, and whether treatment with two Hopguard strips would give better results.

Practical consideration:  this project was funded by donations from beekeepers, performed by beekeepers, for the benefit of beekeepers.  You can support such research with your donations to ScientificBeekeeping.com.


I greatly appreciate the help in running this trial from my sons Eric and Ian, whose labor was covered by your generous donations to ScientificBeekeeping.com. I especially wish to thank volunteer Brion Dunbar for his unstinting assistance throughout the trial.  The Hive Clean was generously donated by BeeVital, Seeham, Austria.


[1] Currie, RW and P Gatien (2006) Timing acaricide treatments to prevent Varroa destructor (Acari: Varroidae) from causing economic damage to honey bee colonies. Can. Entomol. 138: 238–252.

[3] (Broken Link!) http://www.miteaway.com/uploads/3/0/7/9/3079637/_maqs_application_brochure.pdf

[4] Giovenazzo, P and P Dubreuil (2011) Evaluation of spring organic treatments against Varroa destructor (Acari: Varroidae) in honey bee Apis mellifera (Hymenoptera: Apidae) colonies in eastern Canada.  Experimental and Applied Acarology 55(1 ): 65-76.

[6] Cornelissen, B, et al (2012) Queen survival and oxalic acid residues in sugar stores after summer application against Varroa destructor in honey bees (Apis mellifera).  Journal of Apicultural Research 51(3): 271-276.

[7] Wagnitz, JJ and MD Ellis (2010) The effect of oxalic acid on honey bee queens. Science of Bee Culture 2(2) (Supplement to Bee Culture magazine 138(12): 8-11. http://www.beeculture.com/content/ScienceJournalDec2010.pdf

[8] Giovenazzo (2011) Op. cit.

[9] Wagnitz, JJ and MD Ellis (2010) Combining an artificial break in brood rearing with oxalic acid treatment to reduce varroa mite levels. Science of Bee Culture 2(2) (Supplement to Bee Culture magazine 138(12): 8-11. http://www.beeculture.com/content/ScienceJournalDec2010.pdf

[11] Giovenazzo (2011) Op. cit.

[12] Giovenazzo (2011) Op. cit.

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Sick Bees – Part 18F1: Colony Collapse Revisited – Pesticides

First published in: American Bee Journal January 2013

Sick Bees Part 18f1: Colony Collapse Revisited


Randy Oliver


A Bit of History

Nailing Down the Guilty Party

Keep ’em Honest!

Pesticides and CCD

Making the Link



As long as I’ve been keeping bees, one of our worst fears has been that we might suffer a serious pesticide kill.  Pesticides (especially insecticides) have always been, and will continue to be, a problem for bees and beekeepers. 

Jim Doan of New York hadn’t experienced a serious pesticide kill in 25 years of keeping bees in corn/soy/alfalfa farmland.  But when he approached one of his yards last spring, he smelled the stench of dead bees.  What he saw made him sick to the stomach—piles of dead and rotting bees in front of every hive!

Jim related to me that he called his state’s Department of Conservation to investigate the kill, to no avail.  So he contacted his State Apiarist, who sent out an inspector a couple of days later to take samples, which then languished in a refrigerator until at Jim’s request they were sent to Dr. Maryann Frazier, who in turn sent them to the USDA lab for analysis.

Although pesticide residues were found, no investigation was done.  No applicator was reprimanded, and no fine imposed.  And Jim’s losses weren’t covered by either his insurance policy or by ELAP [1].

Jim’s disaster was hardly an isolated case.  I’ve spoken with a number of beekeepers who have suffered recent pesticide kills.    Dave Shenefield’s bees were working white clover in Indiana at corn planting time.  A farmer drilled treated corn seed directly into a field of flowering clover without first burning the weeds off with herbicide.  The planting dust fell directly onto the blossoms being worked by the bees, poisoning his colonies as the foragers returned covered with toxic dust.

Darren Cox’s bees in Utah get hit regularly by applications of pyrethroids or carbamates onto flowering alfalfa hay.  These applications done are despite label restrictions that clearly state:

“This product is highly toxic to bees exposed to direct treatment or residues on blooming crops or weeds. Do not apply this product or allow it to drift to blooming crops or weeds if bees are visiting the treatment area.”

Darren related to me a scenario: an aerial applicator, under a contract arranged perhaps two weeks earlier, loads up with insecticide, and flies 50 miles to treat the field.  But when he gets there, he’s surprised to see that the alfalfa is purple with bloom.  What’s he to do—turn around and unload, or just go ahead and spray anyway, knowing that such an action would be in violation of the label.  But this is Utah, where the local primacy partner tends to turn its head to pesticide violations (Fig.1).  You can guess the rest–such unnecessary and preventable bee kills frustrate Darren to no end!

Figure 1.  A typical insecticide kill in Utah.  Simple timely communication between the grower and the applicator as to the stage of bloom could prevent many such kills, as the applicator could then make more appropriate product application choices.  Photo courtesy Jared Taylor.

I could go on and on, beekeeper after beekeeper.  What I hear is that some states are better at others at enforcing pesticide regulations—it’s tough to be a beekeeper in those states that aren’t doing their job!  To make things worse, beekeepers are often justifiably hesitant to pursue investigation, since in a number of states, complaining beekeepers have been fined for having illegal miticide residues in their hives!  And if a beekeeper raises too much of a stink he could become persona non grata to the local landowners and lose his locations.

Farmers and applicators could often easily prevent bee kills by simply making sure that they spray before or after a crop comes into bloom, or by spraying after dusk with a product having a short residual toxicity, or by using a less bee-toxic product that is labeled for application during bloom.  Such practices would eliminate a large proportion of bee kills, yet some farmers and applicators just don’t give a damn, and worst of all, get away with illegal applications (scofflaw applicators may consider any fines levied for pesticide misapplication as a minor business cost)!

What bothers beekeepers most is the unfairness of it.  Ranchers (even of alpacas, reindeer, or emus) receive government benefits for livestock losses due to fire or severe weather [2], and beekeepers may be eligible for benefits for colony losses if they jump through the hoops of ELAP [3].  But neither of those programs cover losses due to pesticide application–either legal or in violation of the law.

Think about it–if someone poisoned a herd of cattle with pesticide overspray, it would make the news!  You could damn well bet that the incident would be investigated and the applicator fined, and the cattleman would sue for damages via civil action.  But this is generally not the case if your livestock are honey bees.  Few damaged beekeepers receive any compensation at all for their losses.

Now I don’t want to give the impression that the pesticide situation is dire for all beekeepers.  As I pointed out in a previous article [4], many beekeepers in agricultural areas have little or no problem with pesticides.  And many commercial beekeepers simply shrug off the occasional bee kill as a cost of getting good locations in agricultural areas.  However, in some areas of intensive agriculture, those commercial beekeepers who provide the bulk of pollination services tell me that pesticide issues are their major problem.

A Bit of History

In order to understand the run up to our current situation, it is helpful to read the engaging “Report on the Beekeeper Indemnity Payment Program” (which was in effect from 1967-1980) [5].  I’ll share a few excerpts:

During the mid-1940’s, [pesticide] damage subsided as farmers shifted from the use of arsenicals to DDT which is less toxic to bees.  However, by the late 1960’s, use of DDT was decreased sharply because of insect tolerance to the poison.  Finally, use of DDT and other chlorinated hydrocarbons was banned because of environmental concerns.  In most cases, the highly toxic [organo] phosphates and carbamates were used in place of the banned sprays.  This increased the problem of bee loss to the point of disaster for many beekeepers…

Partial colony losses are not always easy to detect…pesticides may weaken colonies to such a point that they do not survive the winter.  This type of loss is often ascribed to winterkill rather than pesticides.  Further, this loss may be extended to the replacement bees placed in contaminated equipment the next season.  Often, not all losses are discovered soon enough after the chemical application to determine the exact cause of death.

Investigatory clue: these records of the field experiences of beekeepers prior to varroa are important to keep in mind, notably that there were “sublethal effects” from the pesticides that caused later winter mortality.  I hear the exact same complaints from beekeepers in agricultural areas today.  Clearly, varroa and beekeeper-applied miticides have added to the stress upon bee colonies, but elevated winter mortality due to pesticide exposure was the norm prior to the introduction of varroa. 

Colony losses due to pesticides were severe in several states during the 1960’s.  There was a “sharp decline in pesticide losses” in California during the early ‘70’s due to the state imposing “strict control of spray application”—only 54,000 colonies were killed in 1974, compared to 89,000 in 1970 (an improvement, but hardly cause for celebration).  But then in the mid 1970’s, encapsulated insecticides (Penncap-M) were brought to market, again causing devastating losses when foragers dusted with the time-release particles returned to the hive and stored them in the beebread.

During June 1976, selected beekeepers in California and Washington were contacted to discuss the pesticide situation…Beekeepers in Washington report that there are no safe locations for bee yards.  One beekeeper said, “No matter where I place my bees in the Yakima Valley, they will be sprayed at least once within ten days.”  A beekeeper in the San Joaquin Valley of California described his efforts to protect his apiaries as “playing musical chairs with 40 loads of bees….”  Several beekeepers said that even if they did move their colonies to another location, it could be sprayed the next day.

Practical application: I hear exactly the same words today from commercial operators.  We have made great progress with pesticides since the 1960’s, but still not enough!

Beekeepers in Arizona, California, and Washington accounted for a large proportion of claims because they lacked access to “safe” forage areas (these were the early days of using forklifts in bee operations, and moving bees was hard work).  It was not unusual for large beekeepers to suffer serious pesticide damage to half their hives each year, and they would likely have been unable to stay in business without governmental help (Fig. 2).

Figure 2.  Back when the Agricultural Stabilization and Conservation Service kept records of reported bee kills for indemnification purposes (not all kills were reported), it was easy to see in which states pesticide applications were a serious problem.  In recent years bee kills have not been tracked by any agency.  Map from Erickson & Erickson 1983 [[i]].

[i] Erickson, EH, and BJ Erickson (1983) Honey bees and pesticides.  ABJ 123(10): 724-730.

For nearly a decade, the Indemnity Program compensated beekeepers for pesticide losses.  Those in only eight states filed the bulk of claims.  As today, a small percentage of commercial beekeepers control the vast majority of colonies, and provide most pollination services.  Well less than 1% of beekeepers in the country filed claims in any one year.  By contrast, over 90% of the Arizona beekeepers in the program filed claims— not surprising due to the frequent spraying of the vast acreage of cotton suffering from a serious infestation by pink bollworm in the mid 1960’s [7], and the lack of alternative non-agricultural forage in that dry state.

The largest payment to a single beekeeper (name and state not specified) was $225,400 in 1972 (that would be $1 million in today’s dollars), and he filed for $228,000 two years later.  You can imagine how this might not have set well with some budget-conscious congressmen!

And of course some crafty beekeepers learned to work the system:

On the other hand, some commercial beekeepers contend the indemnity payments have permitted, and in some cases encouraged, the survival of marginal beekeeping operations.  The “marginal manager,” in this context, was characterized as any beekeeper who had become dependent upon indemnity payments as a source of income.

Those alleged “marginal beekeepers” reportedly left their hives in areas that they knew would be sprayed, and managed their colonies only enough to keep them barely alive so as to be able to collect more payments the next year (or kept collecting payments on deadouts).  These fraudulent practices also did not play well to the program overseers.

The study also looked at the profitability of beekeeping; I found one of the tables to be of particular interest (Fig. 3):

Figure 3.  You can roughly adjust these figures into today’s dollars by multiplying them by five.  What surprises me is that despite it being painfully costly to maintain colonies today in California (the annual expense being about $190) [[i]], the profit margin is substantially higher now than it was back then–not because of honey (since honey prices have only kept pace with inflation [[ii]]), but rather due to much higher pollination rates in almonds.  Also of interest is that in those days beekeepers spent next to nothing on feeding syrup, and pollen supplement isn’t even mentioned!

[i] Mussen, E (2009) How much does it cost to keep commercial honey bee colonies going in California?  http://projectapism.org/content/view/83/27/

[ii] http://www.nass.usda.gov/Statistics_by_State/California/Historical_Data/Bees.pdf

It is instructive that the analysts were aware of the cost to the beekeeper of pesticides:

This analysis shows that beekeeping income is affected most by severely damaged and destroyed colonies.  Severely damaged colonies may require 6-8 weeks to recover colony strength.  If the damage occurs during a major honey flow, the field force will be greatly reduced and honey yields could be lowered 60 percent or more.  Severe damage in late summer may weaken a colony preparing for winter and increase the chances for significant winter kill…Beekeepers estimate it takes about one year for a destroyed colony to regain its income earning potential.

The authors conclude that without the indemnity payments, “farmers seeking pollination services would have to pay substantially higher rental fees to obtain bees.”  Congress decided to pass that cost onto the farmers anyway, and terminated the indemnity program in 1980 (leaving some beekeepers with still-unpaid IOU’s).  Today the almond growers bear the brunt of those higher rental fees; the huge number of colonies produced to meet the demand for high-paying almond pollination  ensures that there are plenty of strong hives available for other crops afterwards.

Colonies generally come out of almonds in better shape then when they went in.  This is not true for a number of other crops.  The combination of poor forage and pesticides in several crops  can weaken colonies to the extent that they don’t survive the season.

Allow me to close with some prescient conclusions from the report:

Unless Federal and State governments act ot regulate and caution applicators of toxic pesticides, colony damage will continue to be a major problem for beekeepers. However, most government officials emphasize that farmers and spray applicators are already confronted with enough regulations…the current development of stronger and longer-lasting pesticides…is creating an environment entirely unsuitable for honey bees in many parts of the U.S.  These areas will find it harder to maintain the present level of bee population regardless of an Indemnity Program or higher honey and pollination prices.

Remember that the above words were written prior to the invasion of the tracheal mite, the varroa mite, Nosema ceranae, or the Small Hive Beetle—beekeeping hasn’t gotten any easier since their arrival!

Practical application: beekeeping in agricultural settings has always been a tough way to make a living.  Fortunately, many beekeepers tell me that things have gotten better in their regions.  But in some areas of intensive pesticide application, it’s hard to keep a hive alive from one year to the next.

Nailing Down the Guilty Party

This spring my bee operation suffered from a case of Sudden Forklift Collapse (Figure 4).

Figure 4.  Early this spring I suffered from a case of Sudden Forklift Collapse.  This was no “sublethal effect” and did not go unnoticed!  In a forklift kill like this, it didn’t take Sherlock Holmes to determine that the cause of death was due to a falling oak tree.  If only the causes of pesticide kills were so easy to pin down!

In my case of Sudden Forklift Collapse, the cause was evident.  Such is often not the case with pesticide kills.  You may not even see any dead bees if the field force is poisoned in the field and never makes it back to the hive.  Perhaps (as in the case of planting dust) you only see a handful of young bees and drones dying at the landing board.  Or maybe the brood turns spotty.  If the pesticide disorients the foragers, you may wonder why you didn’t get the normal honey crop.  Or maybe there is some sublethal effect from which the colony simply “slows down” for a few months, or doesn’t make it through the winter.

In any of those cases, it may be difficult, if not impossible, to nail down the culprit.  You don’t know where your bees were foraging, and any pesticide application within a 3-mile radius is suspect.  You may not immediately recognize that there was a pesticide problem at all, so any residues could be degraded or washed off by rain by the time you think to have the dead bees or beebread tested.  And even if you happen to visit the yard immediately after the kill, good luck in getting an understaffed and untrained state or county agency to quickly come out and properly collect and freeze a good fresh sample.  And even then the analytical tests cost so darned much!

Action item: aggrieved beekeepers often have VERY STRONG FEELINGS!  However, in order to change pesticide regulations, the EPA needs incontrovertible evidence that a certain pesticide used according to label restrictions caused adverse effects to honey bees.  We need any and all beekeepers who suffer from substantial pesticide kills to file an “incident report.”  Such a report is most effective if it contains a photographic record, documentation that rules out other plausible causes for the dead bees (e.g., tracheal mites or starvation due to unusual weather or forage conditions), and chemical analysis of samples of bees and beebread, properly taken by a state agent.  If your local primacy partner is unable or unwilling to help, you may report directly to http://www.npic.orst.edu/eco or beekill@epa.gov.

One would think that solving Jim Doan’s kill would have been straightforward, since there were fresh piles of dead bees in front of the hives.  He hadn’t previously experienced serious kills in those yards, so something different had happened.  There was no apparent change in plantings this year, but with commodity prices at an all-time high, a farmer might have felt that it was worthwhile to apply more or different insecticides as precautionary “risk management.” Surely it would be easy to find incriminatingly-high levels of the offending pesticide in the dead bees or combs.

According to Jim, due to unfamiliarity with the investigation of pesticide kills, the state inspector collected less than an optimal amount of bees for pesticide analysis. Two samples were later sent off to the USDA lab (the cost of analysis was split between Jim and Project Apism)—results below (Fig. 5).

Figure 5.  Analysis report of the two samples from Jim Doan’s spring bee kill (column headings added).

Figure 5. Analysis report of the two samples from Jim Doan’s spring bee kill (column headings added).OK, so now Jim had a report.  But what did it tell him?  As for the dead bees, the 1.6 ppb* of clothianidin insecticide is far too low to have caused bee mortality (1.6 ppb = 0.16 ng/bee; the LD50 for clothianidin lies in the range of 22-44 ng/bee).

* To help with the math, LD50 = median lethal dose; 1 ppb = 1 part per billion = 1 μg/kg = 1 ng/g; μg = microgram (one millionth); ng = nanogram (one billionth); a bee weighs about a tenth of a gram, so for every 10 ppb of residues in a sample of dead bees, any bee on average would contain 1 ng/bee .

So how about the high dose of Captan fungicide?  As best I can tell from the literature, “Studies on the honeybee using technical Captan fungicide indicate that the LD50 is greater than 10 μg a.i./bee, and that there is 9.8% mortality at 215 μg a.i./bee.”  So let’s do the math: 1290 ppb = 129 ng/bee, or 0.129 μg/bee—so again, it would be hard to make a case that this chemical was responsible for the obvious pile of dead bees.

Maybe the analysis of the pollen sample from the comb might help.  I have no idea as to how it was taken, which can make a huge difference (Fig. 6).

Figure 6.  These are plugs of beebread that I pulled from a brood frame.  Note the layering of the different species of pollen.  If a colony suffers from a pesticide kill, any traces of the responsible pesticide residue may only be in the topmost layer of pollen.  If the state agent who takes the beebread sample scoops all the way to the midrib, he may dilute the offending pesticide by a factor of 10 or more.

The one pollen sample from the one comb from one colony (get my point?) in Jim’s affected apiary contained 399 ppb of the organophosphate insecticide Phosmet.  The contact LD50 for this compound is listed as 0.0001 mg per bee (= 0.1 μg/bee = 100 ng/bee).  Surprisingly, there doesn’t appear to be any published oral LD50 for Phosmet to honey bees!    By my math, the concentration of Phosmet in Jim’s pollen sample would not be expected to have killed his bees either, although since it is a violation of the label to spray the insecticide on flowering crops, one is left wondering how it appeared in the pollen.

So this is how it can be for a beekeeper and his innocent bees—the suddenly-appearing piles of rotting corpses in front of every one of his hives certainly suggest that his bees were killed by a pesticide application.  Unfortunately, due to a lackluster investigation by the primacy partner, and lack of implicating chemical evidence, Jim will never know what or who was responsible for the kill, nor be compensated for his losses, if justified.  And he has no idea whether the same thing will happen again next season!

To make matters worse, Jim’s bees apparently got hit again in July, resulting in piles of greasy-looking dead and twitching dying bees in front of the entrances.  And as I write these words in November, Jim sent me yet another photo of hundreds of freshly-dead bees once again in front of the hives (despite him confirming low levels of varroa and nosema).  Jim is now a justifiably frustrated and angry beekeeper–not only did he suffer considerable financial loss (not to mention the ugly death of his beloved bees), but no one learned anything from the experience!  The unwitting farmer(s) have no idea whether their pesticide applications caused the problem, Jim’s state agencies aren’t making any particular effort to prevent the same thing from happening again next year, and EPA didn’t receive any useful adverse effects report.  Yes, frustrating!

It is disturbing for me to present these facts.  Our managed honey bees function as a conspicuous and charismatic indicator species for the effects of pesticides upon “non target organisms.”  Yet some agricultural areas are a “no bees land” due to either inadequate label restrictions or flagrant violation of those restrictions.  And keep in mind that the honey bee colony has the capacity to absorb pesticide kills that would exterminate solitary pollinators, such as native bees, butterflies, and beneficial insects.

Practical application: if honey bee colonies are being killed, we can safely assume that the situation is even worse for more sensitive species!

Keep ‘em Honest!

Let me share another quote from the Indemnity Report:

The Beekeeper Indemnity Program itself discourages civil court action…Greater use of the civil court system by beekeepers to seek compensation for pesticide losses could reduce applicator negligence.

There you have it!  The sad truth is that it will take the push of lawsuits to ensure that our pesticide laws are actually enforced.   Accordingly I’ve studied the judgments for some beekeeper lawsuits.  Be forewarned that a successful lawsuit requires unimpeachable evidence and impeccable argumentation—so one should not enter into an expensive lawsuit lightly!

The AHPA has started a legal defense fund to pursue test cases against egregious violations of pesticide law, with the hope of setting legal precedent, as did Jeff Anderson’s successful lawsuit against the state of Minnesota  in 2005 [10].  I’m hesitant to step into politics, but I feel that this is probably a good course of action that could help the cause of advancing pesticide regulation.  We beekeepers must tread carefully here to avoid pissing off the farmers who allow us to place bees upon their land.  In truth, I’d like to see Xerces or some other environmental groups filing such lawsuits, so that they, rather than beekeepers, would take the heat.  However, action is preferable to inaction.

Action item:  you may join me in contributing to the National Pollinator Defense Fund at http://pollinatordefense.org/site/?page_id=11

I wish that I could present a simple solution to this problem, but there isn’t one—especially since the U.S. is currently locked into the high-input large-scale monoculture agribusiness model.    The good news is that EPA is on the side of the beekeepers and the environment [11], and that things are clearly getting better—the worst pesticides are being phased out, new “reduced risk” pesticides and “biological” are put on the EPA fast track in order to get them into the market, plus a new generation of “smart” robotic application systems are being developed.  There has never been more public awareness of the plight of the honey bee, and beekeepers are awkwardly basking in the spotlight of being considered as environmental stewards.  The bad news is that the process of reducing the damage by pesticides to non target species is hampered by, among other things, ignorance (and lack of enough good scientific data), politics, property rights, consumer demand, and Money (intentionally spelled with a capital M).

OK, that’s enough griping for now–let’s get back to an investigation into any connections between pesticides CCD.

Pesticides and CCD

Biological plausibility:  pesticides can weaken the colony by killing or otherwise affecting the foragers, reducing adult bee longevity, having adverse effects upon the queen, brood, or nurse bees, or by affecting bee behavior.  In addition, they could react with other toxins, beekeeper-applied miticides, or suppress the bee immune response to pathogens.  Any of the aforementioned could conceivably result in colony dwindling, mortality, or collapse.

Residues in the Combs

Let’s narrow down our focus.  CCD by definition is not the result of the sorts of acute pesticide kills detailed above.  So what we are interested in is colony mortality or morbidity due to sublethal effects that hadn’t already killed bees outright!  In the case of winter mortality, since few pesticides are applied at that time of year, and since colonies normally purge any remaining field bees during the “fall turnover” [12], we’d expect any contribution by pesticides to be from residues in the combs, where they should be detectable by analysis.

Making the Link

One would think that it would be a simple matter to make the connection between pesticide residues and winter mortality—simply analyze pollen and beeswax samples from the combs, and determine whether there is a correlation between residues of specific pesticides and colony mortality.

The above sounds so straightforward and easy, but in actuality this is where it gets complicated.  My point of going into detail on the analysis of Jim Doan’s apparently obvious bee kill was that if it’s that hard to figure out exactly what caused an acute pesticide kill, imagine how difficult it would be to definitively link colony mortality to any sublethal effects from a specific pesticide!

In fact, I took artistic license in greatly simplifying Jim’s story.  In doing my usual fact checking, I found out that the actuality was complicated by personalities, politics, weather (Fig. 7), and a history of indemnity payments.  To add further confusion, another beekeeper on the same farm did not observe any dead bees in front of his hives (but did notice that his nucs on that farm did not build up as well as those at other nearby locations).

Figure 7.  Western New York experienced extraordinarily warm weather (followed by cold) in May.  I find that such weather anomalies can result in piles of dead bees in front of hives due to short-term starvation events.  Weather graph from www.weatherunderground.com.

However, I’m appreciative of Jim for sharing his observations and analysis report, and feel that it was a good example of the problems that researchers and regulators encounter as they try to figure out exactly how pesticides are affecting colony health.

These complicating factors may be why no scientific study has yet been able to firmly link colony mortality to pesticides.  Here are the conclusions of all monitoring and analytical studies that I’ve seen to date:

  • Germany: “As expected, the results show that pollen [from 210 hives sampled over 3 years] is contaminated with a plethora of chemical substances originating from the agricultural practice of using pesticides but also from the apicultural necessity of using acaricides… Accordingly, no relation between contamination of pollen and colony development or winter losses could be demonstrated in the course of the project although special emphasis was put into this aspect” [13].
  • France: “Several cases of mortality of honey bee colonies (varying from 38 to 100%) were observed in France during the winter of 2005-6. In order to explain the causes of these mortalities, a case control study was conducted on a limited area, together with a larger survey in 18 other apiaries located in 13 sites over the entire country…No pesticide residues of agricultural origin were found in the samples of beebread, beeswax, honey and dead honey bees, with the exception of imidacloprid…found in one apiary [and] not considered to be able to cause honey bee acute mortality” [14].
  • France: “A 3-yr field survey was carried out in France, from 2002 to 2005, to study honey bee … colony health in relation to pesticide residues found in the colonies… No statistical relationship was found between colony mortality and pesticide residues” [15].
  • Italy: “The data obtained from the winter 2009-2010 inspections were used as the basis for chemical analyses on bee and wax samples, to test for residues of organophosphate, organochlorurate, carbamate and neonicotinoid pesticides, but no significant presence of these substances was detected” [16].
  • Spain: “The present data [beebread samples from 12 apiaries] are in agreement with studies showing no negative effects of seed-treated crops. Some pesticide residues were found here, in particular several varroacides and insecticides, but no significant differences were observed between the different sunflower crop samples and those from the sites of wild vegetation. This fact not only implies environmental contamination but also supports the theory that, most of the time, inadequate [read that “unapproved”] treatments are the main source of residues that might weaken bee colonies and make them more sensitive to other factors” [17].
  • Spain: “This study was set out to evaluate the pesticide residues in stored pollen from honey bee colonies and their possible impact on honey bee losses in Spain. In total, 1,021 professional apiaries were randomly selected… A direct relation between pesticide residues found in stored pollen samples and colony losses was not evident accordingly to the obtained results” [18].
  • Europe (thorough review): “Currently there is no clear evidence from field based studies that exposure of colonies to pesticides results in increased susceptibility to disease or that there is a link between colony loss due to disease and pesticide residues in monitoring studies” [19].
  • USA (CCD Descriptive Study): “This study found no evidence that the presence or amount of any individual pesticide occurred more frequently or abundantly in affected apiaries or colonies” [20].
  • USA (2012 CCD Progress Report): “When pesticides are viewed in aggregate on a national scale, residues of pyrethroids …pose a threefold greater hazard to bee colonies than neonicotinoids, based on mean and frequency of detection in pollen samples and relative acute toxicity. The synthetic pyrethroid detected in the highest quantity and frequency in honey bee colonies that is used by beekeepers to control Varroa mite is tau fluvalinate” [21].
  • USA (Stationary Hive Project) : “We did not find any relationship with any of our measures of pesticide contamination and colony loss rate at the apiary level for either 2009 or 2010” [22].

OK, I’m as puzzled as you are!  It defies both common sense and a long history of beekeeper experience that researchers haven’t yet nailed down any link between pesticide residues in the combs and colony mortality!  The above were not industry-funded studies, and several of the researchers started with a strong anti-pesticide bias (nearly all researchers suspect that pesticides are involved to some extent).  And I’m certainly not about to tell you that pesticides/miticides and winter mortality are unrelated–it’s just, like I said, complicated.

I found that in order to begin to understand the effects of manmade pesticides upon bee health that I first needed to back up and examine some of the complex biology involved in natural bee/plant/toxin interactions.  We’ll start in on that next month…


I’d like to thank the editor of this journal, Joe Graham, for giving me the latitude, support, and encouragement to write this series of articles.  And a special thanks to Dianne Behnke of the publishing department for digging up and scanning archived issues of ABJ for my research.


[1] http://www.fsa.usda.gov/Internet/FSA_File/elap_honeybee_11.pdf

[2] http://www.fsa.usda.gov/Internet/FSA_File/lip2011_158c020211.pdf

[3] http://www.fsa.usda.gov/Internet/FSA_File/elap_honeybee_11.pdf

[4] http://scientificbeekeeping.com/the-extinction-of-the-honey-bee/

[5] ERS (1976) Report on the beekeeper indemnity payment program. http://babel.hathitrust.org/cgi/pt?id=coo.31924001799307;seq=8;view=1up

[6] Erickson, EH, and BJ Erickson (1983) Honey bees and pesticides.  ABJ 123(10): 724-730.

[7] http://naldc.nal.usda.gov/download/48077/PDF

[8] Mussen, E (2009) How much does it cost to keep commercial honey bee colonies going in California?  http://projectapism.org/content/view/83/27/

[9] http://www.nass.usda.gov/Statistics_by_State/California/Historical_Data/Bees.pdf

[10] Anderson v. State Department of Natural Resources Minnesotahttp://www.animallaw.info/cases/causmn693nw2d181.htm

[11] http://www.epa.gov/opp00001/ecosystem/pollinator/then-now.html

[12] Mattila HR, Otis GW (2007) Dwindling pollen resources trigger the transition to broodless populations of long lived honeybee each autumn. Ecol Entomol 32:496–505.

[13] Genersch E, et al (2010) The German bee monitoring project, a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41:  332-352.

[14] 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: 40-51.

[15] Chauzat MP, et al (2009) Influence of pesticide residues on honey bee (Hymenoptera, Apidae) colony health in France. Environmental Entomology 38: 514-523.

[16] Mutinelli, F, and C Porrini (2010) Report based on results obtained from the second year (2010) activity of the APENET project. http://ebookbrowse.com/apenet-2010-report-en-6-11-pdf-d189566755

[17] Bernal J, et al (2011) An exposure study to assess the potential impact of fipronil in treated sunflower seeds on honey bee colony losses in Spain. Pest Management Science 67: 1320-1331.

[18] Bernal J, et al (2010). overview of pesticide residues in stored pollen and their potential effect on bee colony (Apis mellifera) losses in Spain. Journal of Economic Entomology 103: 1964-1971.

[19] Thompson, HM (2012) Interaction between pesticides and other factors in effects on bees. http://www.efsa.europa.eu/en/supporting/doc/340e.pdf

[20] vanEngelsdorp D, et al. (2009) Colony Collapse Disorder: A Descriptive Study. PLoS ONE 4(8): e6481.

[21] http://www.ars.usda.gov/is/br/ccd/ccdprogressreport2012.pdf

[22] Drummond, F, et al (2012) The first two years of the stationary hive project: Abiotic site effects.  http://www.extension.org/pages/63773/the-first-two-years-of-the-stationary-hive-project:-abiotic-site-effects

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“Fried Eggs” Identified!

“Fried Eggs” Identified!

Randy Oliver

First Published in ABJ in Feb 2012

I mentioned in my previous article that I’ve been seeing an unidentified organism that looked like “fried eggs”  in the guts of bees from my operation in the California foothills (Figure 1).  I sent out requests to a number of researchers for ideas as to what it was.  Thanks to Antonio Gómez Pajuelo of Consultores Apícolas in Spain for identifying them as rust fungus spores.

Figure 1.  These “fried eggs” have a distinctive pattern of tiny spikes on their outer shell, which helped to identify them as some sort of rust fungus spore.  What appeared to be the process of cell division in this photo may have actually been the process of digestion!  Photo by the author.

Upon further research, I found that beekeepers have long reported bees gathering rust spores and packing them into their pollen baskets, and that a number of scientific papers had been written on the subject (it always pays to dig into the older literature).  The rusts are a large group of parasitic fungi with complicated life cycles.  They infect quite a number of different plants, often forming reddish spore masses on the undersides of leaves. Bees have been observed collecting spores from a number of genera of rusts, including Uromyces, Puccinia, Caeoma, and Melampsora (Fig. 2),

Figure 2.  Spores of the Poplar Rust Melampsora, which is commonly collected by bees.  It’s not clear whether rust spores in general are harmful to bees.  Photo courtesy www.bioimages.org.uk, © Malcolm Storey.

A.J. Cook reported in 1885 that bees in New York were gathering spores from blackberry rust “with great apparent greed.”  Of interest is that the last two seasons, I had noticed unusual infestations of fluorescent orange rust on our invasive Himalaya blackberries in the foothills.  I hadn’t put it together previously, but I had also noticed bees bringing in loads of a brilliant orange  “pollen” that I’d never noticed before (by the time I got the dang things ID’d, I could no longer find that orange “pollen” to check under the ‘scope).  Blackberry rust is generally attributed to Caeoma, but I found that UC Davis extension (Bolda 2011) reported we have a new invasion of orange rust of blackberries caused by  two other fungi—Arthuriomyces and Gymnoconia (Fig. 3).

Figure 3.  An orange rust on blackberry.  This looks like the same thing that I saw around my apiaries.  Photo courtesy Mark Boulda.

Something that I find intriguing is that some rust fungi produce sugary secretions for the purpose of attracting insects in order to help disperse their spores (Wäckers 2005).  Even more fascinating is a potential explanation for the day-glow orange spore masses of blackberry rust.  Shaw (1980), studying the collection of rust spores by honey bees, found that the spore masses reflected ultraviolet light of a wavelength to which bees are highly sensitive.  So the fungus may be “intentionally” using bees to its advantage!

Bees consume rust spores readily; during our fall pollen dearth I often find bee guts packed with them.  Schmidt (1984) found that bees in cages consumed Uromyces rust spores as readily as they did dandelion pollen, despite it being low in protein.  The question then is whether rust spores are of any nutritional value to bees, or, since I often find them associated with sick colonies, whether they cause actual harm to the bees (my sampling is admittedly biased towards colonies in poor health).

Above is a photo of a typical comb filled with beebread consisting of rust fungus spores.  Note the lousy brood pattern and the dying brood.  When the colony is feeding upon this beebread, it goes downhill quickly.  However, if we feed the hive several pounds of high-quality pollen sub, it will turn around immediately and grow again.

Antonio Pajuelo (pers comm) also reports a correlation between the consumption of poplar rust spores and colony mortality, but doesn’t know whether it is due to spore toxicity or lack of better nutrition.  It may be that the collection of rust spores is due to the lack of more attractive and nutritious floral pollen, and as such would simply be a generic indicator of poor colony nutritional status.

On the other hand, Schmidt (1987) found that caged bees fed Uromyces spores as a sole protein source actually had their lifespan reduced compared to those fed sugar syrup only—strongly suggesting that the spores were toxic.  The spore-fed bees  lived about 20 days less than those fed the most nutritious pollens!

Practical application: it may be wise to feed pollen supplement if you observe your bees collecting rust spores.


Thanks to Antonio Pajuelo and all the other researchers who helped with trying to put a name to these organisms.  And a big thanks to Peter Borst and Juanse Barros for plying through Google Images in the search for the identity of these spores, and Dr. Jose Villa for digging up the old literature.


Bolda, M (2011) Orange rust emerging again in blackberry.  http://cesantacruz.ucdavis.edu/?blogpost=4660&blogasset=16664

Cooke, AJ (1885) Fungus spores for bee bread: A new kind of pollen. Gleanings in Bee Culture July 1885 pp. 455-456.

Schmidt, JO and BE Johnson (1984) Pollen feeding preference of Apis mellifera, a polylectic bee.  The Southwestern Entomologist. 9(1).

Schmidt, JO, SC Thoenes and MD Levin (1987) Survival of honey bees, Apis mellifera (Hymenoptera: apidae), fed various pollen sources.   Annals of the Entomological Society of America 80(2): 176-183.

Shaw, DE (1980) Collection of neurospora by honeybees.  Trans. British Mycol Soc. 74 (3): 459-464.

Wäckers, FL, J Bruin (2005) Plant-provided food for carnivorous insects: a protective mutualism. Cambridge Univ. Press.

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Nosema Ceranae and Honey Production in Healthy Colonies

Randy Oliver and Brion Dunbar

There is considerable scientific and practical debate about the degree of impact that Nosema ceranae infection has upon the honey bee colony.  It is reasonable to assume that there would be noticeable impairment, since infection by its cousin, Nosema apis, is well documented to adversely affect bee metabolism, protein levels, longevity, and most noticeably,  honey production [1].  Studies on the new parasite have found similar metabolic harm [2], [3].  And Dr. Frank Eischen’s data from Louisiana [4] suggests that infection by N. ceranae also suppresses honey yields.  In this study, we wished to see whether infection by Nosema ceranae was related to poor honey production in colonies of roughly the same strength, as opposed to colonies simply weakened in strength by nosema infection.

One of the problems with trying to document any correlation between N. ceranae and colony production is that that the typical method of monitoring the parasite consists of determining the average spore count from a small sample of bees.  This method is demonstrably unreliable, depending upon factors such as from where in the hive the sample is taken, the time of day, the presence in the sample of a single highly-infected bee, or the number of bees sampled [5].  Furthermore, mean spore counts may not correlate well with the actual degree of infection [6].

To overcome the problems inherent with mean spore counts, I’ve been revisiting Dr. G.F. White’s original method of assessing the degree of nosema infection in the colony by squashing bee guts one at a time [7].  In my first study, I took samples from the two strongest and two weakest colonies in several apiaries in December, and compared the percentage of bees showing infection (Fig. 1).

Figure 1.  Distribution of nosema prevalence in the weakest and strongest hives in my apiaries in early December, based upon 10-bee samples taken from under the lid or outside combs.  In none of the strong hives were more than 1 bee out of 10 infected; whereas the majority of the weak hives scored at least 1 or more infected bees out of 10, and 40% scored 2 or more positives.  Chart reprinted from Sick Bees 15.

There was a clear relationship in December between colony strength and the proportion of infected bees in a hive.  By February, nosema prevalence in some dwindling colonies had risen to 8-10 bees out of 10!  By changing my assessment method to gut squashes rather than mean spore counts, for the first time I could see a relationship between infection by Nosema ceranae and poor colony performance!

Skip forward to spring.  My hives returned from almonds looking great, whereupon I split and requeened them all.  The splits grew rapidly during the best spring in years, and gained weight on the early flows in April.  But then during our main flow in June, things came to a screeching halt— despite looking strong and healthy, most hives did not even make adequate winter stores.  The normal variation in colony-to-colony honey production was arrestingly apparent—a number of hungry colonies pulled early honey down out of the second brood chamber, yet others cried for additional supers, and filled them!

I couldn’t help but suspect that the poor producers might be suffering from a nosema infection (there are no overt symptoms of infection by N. ceranae).  Intrigued by my findings above, I decided to see if the same held true for honey production–that is, whether I could detect a difference in infection levels between the best and worst producing healthy colonies in each yard.


With the assistance of beekeeper Brion Dunbar, I took samples from 10 apiaries on June 15 and 16, as the main honey flow was ending.  Each apiary had been started from nucs in early April, mostly with sister queens (different for each yard).  In each apiary we identified the two colonies that had produced the most honey, and the two that had produced the least, inspecting each colony to exclude those showing any signs of disease, queen problems, or lack of cluster size (not surprisingly, we excluded a number of nonproductive colonies for the above reasons).  In other words, we wanted to compare only strong, apparently healthy colonies to determine whether their differences in honey production were due solely to the degree of nosema infection.

We took bee samples from under the lid or from an outside comb.  Brion took on the Herculean task of individually squashing and viewing the gut contents of 10 bees from each hive (for a total of 410 bees), scoring each bee as being either positive or negative for nosema infection.


The results surprised us—there was no striking difference in the prevalence of infected bees between the productive and nonproductive hives!   On the average, 7% of the sampled bees were infected in the productive colonies, compared to 10.5% in the nonproductive (not statistically significant).  The distribution of the degree of infection was similar for both groups of hives (Fig. 2), with one notable exception—an apparently badly-infected colony in the nonproductive group.

Figure 2.  Distribution of nosema prevalence at the end of the honey flow in June.  Although a larger percentage (55%) of the productive hives scored negative for nosema infection (as opposed to 38% of the nonproductive), that relationship did not necessarily hold for lightly infected colonies.  Overall, both groups had similar distributions of infection prevalence.


It is easy to understand how colonies weakened in population due to nosema infection would produce less honey.  We suspected that even in strong colonies, nosema, due to its metabolic drag on the bees, would suppress honey production.  So in this study we compared the prevalence of infection between apparently healthy colonies at the extreme ends of weight gain in each yard (most productive vs. least productive).

Since we had earlier found a marked difference in nosema infection between strong and weak hives the previous fall, we fully expected to find more nosema in the nonproductive hives.  To our surprise, there was no striking trend in that direction.  Such a relationship might have been more evident had we sampled more hives, or taken more bees in each sample.

It’s likely that by excluding any sick or weak colonies that we also omitted any badly-infected hives from analysis–in our sporadic sampling of weak hives in the operation (data not shown) we often found nosema to be prevalent.  Note that of the 41 colonies selected, in only 3 were more than 20% of the bees in the samples infected.  Returning to Dr. White’s detailed studies on Nosema apis, he [8] concluded:

As a rule colonies which in the spring of the year show less than 10 per cent Nosema-infected bees gain in strength and the losses are not detected.  This is often true also in cases where the infection is somewhat greater than 10 per cent.  When the number of infected bees approaches 50 per cent the colonies become noticeably weakened and in many cases death takes place.

So perhaps colonies can still be productive despite having up to 20% of their bees infected by Nosema cerana, so long as they remain strongBut that may be the exception– keep in mind that 16 of the 20 productive colonies had less than that rate of infection, and only 1 had more than 20% infected.  On the other hand, in the nonproductive hives, 13 of 21 had at least 10% of the bees infected.  So these data suggest that the “tip point” at which nosema noticeably affects honey production occurs when more than about 10-20% of the bees are infected.

Nosema ceranae was certainly present in my operation in June—we found infected bees in over half the colonies, productive or nonproductive.  Keep in mind that our samples of only 10 bees would certainly underestimate whether infection was present—it’s likely that every single colony in my operation contained at least a few infected bees.  But by early August, nosema was hard to find when I sampled for it, despite the fact that I had not applied any treatments.  This relative disappearance of nosema in late summer appears to be common [9].

In conclusion, it did not appear that infection by nosema was the main cause for the differences in honey production between my strong colonies—other factors must have been involved.  It also appears that if a colony is able to maintain its strength despite being infected with nosema at a low level, then it can still make honey.  And finally, our results perhaps support Dr. White’s conclusion that colonies are less likely to be productive when more than 10% of the bees are infected by nosema.


Thanks to Brion Dunbar for completing the tedious task of squashing and scoring bees.  And thanks to the donors to ScientificBeekeeping.com for supporting this sort of practical research.


[1] Fries, I (1993) Nosema apis – a parasite in the honey bee colony.  Bee World 74 (1): 5-19

[2] Mayack, C and D Naug (2010) Parasitic infection leads to decline in hemolymph sugar levels in honeybee foragers. Journal of Insect Physiology 56(11):1572-1575

[3] http://scientificbeekeeping.com/sick-bees-part-17-nosema-the-smoldering-epidemic/

[4] Eischen, FA, et al (2011) Impact of nutrition, Varroa destructor and Nosema ceranae on colonies in southern Louisiana.  Proceedings of the American Bee Research Conference 2011

[5] http://scientificbeekeeping.com/sick-bees-part-16-the-quick-squash-method/

[6] Traver, BE and RD Fell (2011) Prevalence and infection intensity of nosema in honey bee (Apis mellifera L.) colonies in Virginia. Journal of Invertebrate Pathology 107(1):43-49.

[7] http://scientificbeekeeping.com/sick-bees-part-15-an-improved-method-for-nosema-sampling/

[8] White, GF (1919) Nosema-Disease.  USDA Bulletin No. 780. A free download from Google Books.

[9] Rennich, K, et al (2012) 2011-2012 National Honey Bee Pests and Diseases Survey Report. http://www.aphis.usda.gov/plant_health/plant_pest_info/honey_bees/downloads/2011_National_Survey_Report.pdf

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Sick Bees – Part 18E: Colony Collapse Revisited – Genetically Modified Plants

First published in: ABJ December 2012

Genetically Modified Plants

What Is Genetic Modification?

There’s Nothing New About Transgenics


An Odd Series of Connections

The Vilifying of Monsanto

What Are They Up To?

Practicality Overrides Principle

Hold the Hate Mail

The Changing Face of Agriculture

Bt Crops

Roundup Ready

Direct Effects of Roundup Use

Indirect Effects of Roundup Use

The Future of Roundup

Reality Check

Looking Ahead: The Chemical Treadmill & Pest Resistance

Additional Discussion

The Back Story on Plant Breeding and GM Crops

The Profit Motive

Enter GM Crops

The Second “Green Revolution”

Cautions About GM

Perspectives on GM

So What’s The Problem?



Sick Bees – Part 18E:

Colony Collapse Revisited – Genetically Modified Plants

Randy Oliver

First Published in ABJ in Dec 2012

Genetically modified (or GM) plants have attracted a large amount of media attention in recent years and continue to do so. Despite this, the general public remains largely unaware of what a GM plant actually is or what advantages and disadvantages the technology has to offer, particularly with regard to the range of applications for which they can be used [1].

The above quote is certainly an understatement!  Genetically Modified Organisms (GMO’s) are a highly contentious topic these days, and blamed by some for the demise of bees.  In researching the subject, I found the public discussion to be highly polarized—plant breeders and farmers are largely enthusiastic (with appropriate reservations) about the benefits of genetic engineering, whereas health and environmental advocacy groups tend to be fearful of the new technology [2].  I will largely save my review of the history and pros and cons of GM crops for my website, and focus this article upon how GMO’s relate to honey bee health.

What is genetic modification?

The knowledge of genetics was not applied to plant breeding until the 1920’s; up ‘til then breeders would blindly cross promising cultivars and hope for the best.  With today’s genetic engineering, breeders can now take a gene from one plant (or animal, fungus, or bacterium) and splice it into the DNA of another plant.  If they get it just right, the new gene can confer resistance to frost, drought, pests, salinity, or disease.  Or it could make the crop more nutritious, more flavorful, etc.  Such genetically modified crops are also called “transgenic,” “recombinant,”  “genetically engineered,” or “bioengineered.”

There’s nothing new about transgenics

There is nothing new about transgenic organisms, in fact you (yes you) are one.  Viruses regularly swap genes among unrelated organisms via a process called “horizontal gene transfer” [3].  For example, the gene which is responsible for the formation of the mammalian placenta was not originally a mammal gene—it was inserted into our distant ancestors by a virus.  If a gene introduced by a virus confers a fitness advantage to the recipient, then that gene may eventually be propagated throughout that species’ population.   Until recently, we didn’t even know that this process has occurred throughout the evolution of life, and didn’t know or care whether a crop was “naturally” transgenic!


Both the scientific community and industry have done a terrible job at explaining genetic engineering to a distrustful public.  There are clearly potential issues with genetic engineering, but they are being carefully addressed by independent scientists [4] and regulatory agencies, especially in Europe:

From the first generation of GM crops, two main areas of concern have emerged, namely risk to the environment and risk to human health.… Although it is now commonplace for the press to adopt ‘health campaigns’, the information they publish is often unreliable and unrepresentative of the available scientific evidence [5].

Jeffrey Smith, in his book “Seeds of Deception” [6] details a number of legitimate issues and early missteps in bioengineering, as well as pointing out the substantial political influence firms such as Monsanto have upon researchers, regulators, and legislators. We should be cautious to take their assurances with a grain of salt.  On the other hand, I’ve checked the claims of other anti-GMO crusaders for factual accuracy, and found that many simply don’t hold water.  For example, two headlined studies of late, one on rats fed GE corn and Roundup herbicide, and another on the purported increased use of herbicides due to GE crops simply do not stand up to objective scrutiny [7].   It bothers me that the public is being misled by myths and exaggeration from both sides.

From my point of view, GE holds incredible promise and should be pursued in earnest, yet must also be very carefully monitored and regulated.  In any case, GE crops have been widely adopted in U.S. agriculture (Table 1), and thus are now a part of beekeeping.

Table 1.  The genetically engineered traits available to farmers have evolved rapidly as technology improves and as such crops become more widely adopted.  Table from http://www.census.gov/compendia/statab/2012/tables/12s0834.pdf.

An Odd Series of Connections

In 1972, the dean of biological sciences at my university hired me to set up a “world class insectary” (which I did).  I raised mass quantities of insects for hormone extraction, in the hope that we might develop a new generation of eco-friendly insecticides [8].  Several years later I was shocked when Monsanto–a widely-despised chemical company with a sordid history– then hired him to create “a world-class molecular biology company” (which he apparently did).   In 2002, Monsanto was spun off as an independent agricultural company.

Jump forward to 2010, when I had the good fortune to work with an Israeli startup—Beeologics—and witnessed the efficacy of their eco-friendly dsRNA antiviral product for honey bees.  But to bring the product to market, they needed more backing.  To my utter astonishment, they recently sold themselves to Monsanto!

The Vilifying of Monsanto

These days one can simply mention the name “Monsanto” in many circles, and immediately hear a kneejerk chorus of hisses and boos.  Sure, it had been easy for me to enjoy the camaraderie of riding the anti-Monsanto bandwagon; but I realized that that I shouldn’t allow that sort of fun to substitute for the responsibility of doing my homework and getting to the actual facts of the matter!  When I did so, I found that some of Monsanto’s actions did indeed deserve opprobrium; but that much of the criticism directed at the current company is undeserved (Monsanto suffers from an ingenerate inability to practice effective PR).  Concurrent with the purchase of Beeologics, Monsanto hired well-respected apiarist (and columnist) Jerry Hayes to head up a new honey bee health division, and appointed some prominent beekeepers (not me) to its advisory board.  It dismays me that some beekeepers then immediately jump to the erroneous conclusion that Jerry has sold his soul to the Devil—nothing could be further from the truth!

What are they up to?

Some beekeepers imaginatively feared that Monsanto was about to create a GM bee or was up to some other nefarious plot.  But in reality, Monsanto’s vision of its future direction is anything but evil—I suggest that you peruse their website for your own edification [9], [10].  Of course I was curious as to why they had purchased Beeologics, since the market for bee medicine is far too tiny to draw the interest of a giant corporation.  But one needn’t be some sort of psychic in order to figure out a corporation’s plans—all you need do is to read its recent patents, which are a virtual crystal ball for seeing ten years into the future.  So I searched out any patents containing the words “Monsanto” and “RNAi.”

To my great relief, I found that Monsanto was not up to some evil plot—far from it!  I suggest you read two of the patents yourself [11]:

Chemical pesticidal agents are not selective and exert their effects on non-target fauna as well…Some chemical pesticidal agents have been shown to accumulate in food, and to exhibit adverse effects on workers that manufacture and apply such chemical agents. Thus there has been a long felt need for methods for controlling or eradicating… pest infestation on or in plants, i.e., methods which are selective, environmentally inert, non-persistent, biodegradable, and that fit well into pest resistance management schemes. Plant biotechnology provides a means to control pest infestations by providing plants that express one or more pest control agents. Recombinant pest control agents have generally been reported to be proteins selectively toxic to a target pest that are expressed by the cells of a recombinant plant.

What the patents tell us is that Monsanto clearly sees that the public is sick of pesticides.  Genetic RNAi technology would allow plant breeders to develop crop cultivars that control insect pests in the same manner that the plants naturally control viruses.  All that the breeder need do would be to identify a unique target protein in a particular pest, and then splice a gene into the plant to produce a “blocking” dsRNA molecule that would prevent the pest from building that specific protein.  The beauty is that dsRNA molecules are already naturally found in plant tissues, the blocking molecule would be entirely specific for that pest alone, completely nontoxic to humans or other non target species, and be rapidly biodegradable.  It would be a win all around (except for the pest)—crop protection, no toxic pesticides, and a sustainable farming technology (as well as a market for Monsanto’s products, since they would need to continually develop slightly different cultivars in order to avoid pest resistance).  Who’d have guessed that Monsanto would be leading the way toward developing eco-friendly pest control?  Life is full of surprises!

Practicality overrides principle

Some folk make GM crops out to be some sort of abomination of nature, and shun them with religious fervor.  I’m not sure that this is the best course for environmentalists to take, and that perhaps, in the face of an expanding human population and a warming climate, we should leave all the possible plant breeding solutions on the table.  The organic farming community wholeheartedly endorses the biotechnology of “marker assisted selection” [12], yet arbitrarily draws the line at the directed insertion of desirable genes.  This may sound like heresy, but as an environmentalist, I suggest that GE holds great promise for developing more nutritious plants that don’t require pesticides, fertilizer, or irrigation—all of which would be wins for organic farming.

From a biological standpoint, I simply don’t see GM crops as being any more inherently dangerous than conventionally bred crops.  Our domestic plants today are often far from “natural”—you wouldn’t recognize the ancestors of many.  Be aware that even conventionally bred cultivars of several crops (beans, potatoes, celery, etc.) often turn out to be too toxic for humans.

This is not by any means a fluff piece for Monsanto or agribusiness.  Farming is not what it used to be.  In the U.S., 85% of farm sales are produced by less than 10% of farms, which hold 44% of farm acreage [13].  A mere six companies collectively con­trol around half of the proprietary seed market, and three quarters of the global agrochemical market [14].  I abhor such corporate domination; neither do I see today’s high-input agricultural practices as being either sustainable or ecologically wise.

That said, human demands upon the Earth’s finite ecosystem are growing.  There are only about 4.5 acres of biologically productive land on the surface of the Earth available for each current human inhabitant.  Depending upon the culture’s lifestyle, we use anywhere from 25 acres (U.S.) to as little as 1 acre (Bangladesh) to feed and clothe each person.  Unfortunately for the bee (and many other species), due to human population growth there are over 200,000 additional human mouths to feed every single day—each requiring the conversion of another couple of acres of natural habitat into farmland!

It doesn’t take a mathematician to figure out that if we wish to conserve natural ecosystems that we need to get more yield out of existing cropland!  And one of the best ways to do that is to breed crops that are more productive and pest-resistant.  The plant scientists in the corporate labs are making huge strides in developing such cultivars, both by GM and conventional breeding.  If they manage to file a patent [15], so what?—other breeders can easily “steal” the germplasm away from the patented genes, and in any case, the patents expire after 20 years!

Monsanto has seen the writing on the wall—farmers and consumers are demanding not only more food production, but also more eco-friendly agricultural practices.  Monsanto research is heading in that direction with their conventional breeding programs, the development of “biological” insecticides [16], and the goal of producing pesticide-free dsRNA crops. Add to that that the company could actually bring to market dsRNA medications against bee viruses, nosema, and perhaps varroa.  All would be huge wins for the honey bee and beekeepers!

Hold the hate mail

Full disclosure: so despite my innate aversion to corporate dominance and corporate agriculture, I feel that we beekeepers should work with Monsanto to develop products for the beekeeping industry, as well as bee-friendly cultivars of crop plants, and have thus personally decided to be a cooperator in their initial bee research trial.  Is this some sort of Faustian bargain?  I don’t know, but as a condition of my cooperation, I asked, and Monsanto agreed, to allow me to share the data collected with the beekeeping community—which could be a big win for us, since Monsanto has some of the best analytic labs in the world!  I feel that it is far better to have Monsanto working on the side of beekeepers, rather than perhaps against us.  At this point, I’d like to leave the GM debate behind, and address the facts of the matter as to any relationship between GM crops and CCD.

The Changing face of agriculture

Genetic engineering has clearly changed the face of agriculture in the U.S. (Fig. 1).

Figure 1.  These three crops account for over half of all U.S. acreage planted to principal crops, and all are worked to some extent by bees.  Data from http://www.ers.usda.gov/data-products/adoption-of-genetically-engineered-crops-in-the-us.aspx

As can be seen from the figure above, any bees near corn, soy, or cotton are going to be exposed to pollen and nectar from GM plants, as well as to indirect effects due to the technology.  So could GM crops be the cause of CCD?

Bt Crops

Biological plausibility: the insecticidal Bt toxins in GM corn and cotton pollen could harm adult or larval bees.

Organic farmers have long used the spores of the bacterium Bacillus thuringiensis (Bt) to kill caterpillars.  Bt spores germinate in the caterpillar gut, and the bacterium produces insecticidal crystalline proteins (Cry proteins) that bind to specific receptors on the insect intestinal wall.  Since different insect species have different receptors on their gut cells, different strains of Bt have evolved to specifically kill various caterpillars, beetles, mosquitoes, etc. [17].  The proteins are so species specific that wax moths can be controlled on combs by Bt aizawai, which produces Cry proteins that are toxic to moth larvae, but not to bees.

Molecular biologists tweak these Cry proteins to make them even more species specific, and then insert them into plant DNA, so that the plant then produces the proteins itself, thus making its tissues toxic to the target species.  In order to delay the inevitable evolution of Cry-resistant pests, growers plant a percentage of “refuge” crop not containing the Cry genes. Even so, any particular Cry gene will only be effective for some number of years until resistant pests show up.

People have expressed concern about a poisonous substance being introduced into plant tissues, and to them I highly recommend the paper “Misconceptions about the Causes of Cancer” [18].  The reality is that plant tissues are naturally awash in poisonous substances.  Plants have needed to repel herbivores throughout their evolution, and since plants can’t run, hide, or bite back, they do it chemically.  Many of our most popular fruits, nuts, grains, and vegetables (and especially herbs and spices) contain powerful phytotoxins.  Their wild ancestors required cooking or leaching before the plant was edible to humans.  Plant breeders systematically select for cultivars with lower levels of (the often strongly flavored) toxins.

Plants that are naturally resistant to pests contain more phytotoxins, often produced in response to damage from insects.  For example, the sprouts of wheat, corn, and rye produce potent mutagens (enjoy that cup of wheatgrass juice!) [19].  And some plants naturally contain symbiotic bacteria and fungi in their tissues, which produce non-plant chemicals [20].  There is absolutely nothing biologically novel about insecticidal toxins in plant tissues.

The toxicity (or lack thereof) of Cry proteins to non-target organisms, especially upon two “charismatic” species—the honey bee and the monarch butterfly—has been well studied [21], [22], [23].  A recent and very well-designed experiment on the effect of GM Bt corn pollen upon the growth and survival of honey bee larvae was recently performed by a team of independently-funded German researchers [24].  They added pollen from four different sources to a standard semi-artificial larval diet.

Results: surprisingly, the larvae fed the pollen from the “stacked” GM corn containing a combination of three different Cry proteins exhibited a higher survival rate (100%), than those fed non-GM corn pollen!  To me, a big plus for this study was that they also included a positive control of pollen from a wild plant said to be harmful to bees—only about 30% of those larvae survived!  This finding confirmed that even some natural pollens are quite toxic, and that we should compare any toxicity trials of pesticides with those of the natural phytotoxins in nature.

Analysis: CCD and colony mortality occur even in the absence of GM Bt crops; feeding GM Bt pollen to adult bees or larvae does not cause observable adverse effects.

Verdict on Bt crops:  The specific Bt cry proteins used in GM crops were intentionally chosen to not cause harm to bees.  There is no evidence to date that they do.   On the other hand, Bt crops require less use of insecticides that are clearly toxic to bees [25].

Roundup Ready

Monsanto’s pitch is that Roundup Ready® (RR) crops allow farmers to practice weed-free “no till” farming, which saves both topsoil and money.  The catch is that farmers must then douse their fields with Monsanto’s flagship product, Roundup (ensuring sales of that herbicide—a great marketing strategy).  Bayer CropScience has followed suit by introducing crops resistant to its Liberty herbicide, which has a different mode of action.

Herbicide-resistant crops do indeed address several major environmental problems:

  1. No till farming does in fact require less labor and reduces soil compaction.
  2. Farmers get greater production due to less competition from weeds.
  3. No till also reduces the amount of petrochemical fuel involved in tillage.
  4. No till greatly reduces soil erosion, which has long been a major environmental concern.
  5. No till may help to sequester carbon in the soil, and to rebuild soil.

So what’s not to love about Roundup Ready?  There are a few main complaints—(1) the massive spraying of the active ingredient, glyphosate, for which there is questionable evidence that it may be an endocrine disruptor [26], (2) claims of intimidation by Monsanto of farmers who choose not to plant RR seed, and (3) the environmental impact and sustainability of the sort of weed-free monoculture possible with RR crops.

So how do Roundup and RR crops relate to honey bees?

Direct Effects of Roundup Use

Biological plausibility: either the active ingredient (glyphosate), or the adjuvants could cause bee toxicity.

The EPA has thoroughly reviewed the research and found glyphosate to be practically nontoxic to bees (and humans).  They have found the same for Roundup’s adjuvant polyoxyethylene-alkylamine.  However, some beekeepers tell me that they see increased bee mortality following the spraying of glyphosate (Fig. 3), but are not sure whether it was a generic product, or perhaps contained additional ingredients (surfactants, fungicides, or insecticides) added to the tank mix.

Figure 3.  A farmer spraying glyphosate herbicide over Roundup Ready corn seedlings.  Photo courtesy of beekeeper Larry Garrett.

Analysis: there is no strong evidence that the spraying of Roundup or generic glyphosate herbicide is directly causing significant bee mortality.  However, Drs. Jim and Maryann Frazier have legitimate concerns about the effect of some adjuvants—especially the organosilicones [27], [28].

Indirect Effects of Roundup Use

Biological plausibility: the elimination of weeds reduces bee forage.

The success of Roundup Ready technology has allowed farmers to largely eliminate weeds from their fields (at least until the inevitable resistant weeds take over).  But they don’t stop there—nowadays they practice “clean farming” and use herbicides to burn off every weed along the fencerows and in the ditches—the very places that bees formerly had their best foraging.  This elimination of flowering weeds severely reduces the amount of available of bee forage, plus kills off the host plants of native pollinators (such as monarch butterflies) and beneficial insects.

European honey bees evolved in Europe (hence the name), and are adapted to the nutrition provided by Old World flowering plants.  Many of the weeds in North America are old friends of the honey bee.  On the other hand, honey bees were never exposed to corn, soybeans, sunflowers, or squashes until recently; neither corn nor sunflowers supply complete amino acid profiles in their respective pollens.  Until the advent of Roundup Ready, the weeds in an around crops provided alternative nectar and pollen sources for bees; today there is often nary a bee-nutritious weed to be seen in or around a field of corn or soybeans (Fig. 4).

Figure 4.  I took this photo of a no-till herbicide-resistant corn field, prior to the shading canopy of the crop closing over.  Note the total lack of any sort of bee forage (or any species of anything other than corn).  The soil surface is a far cry from the original densely vegetated prairie sod.  Prior to RR, there was more weedy forage for bees, and especially from the traditional weed-controlling crop rotation into legumes or pasture.

Some intriguing (but controversial) research by Dr. Don Huber [29] concerns the fact that glyphosate was originally developed as a chelating agent (a chemical that binds to metal ions; from chela = claw).  Roundup does not kill weeds directly; rather it ties up certain trace metals (notably manganese), which then stresses the plant to the extent that soil fungi and other pathogens eventually kill it.  Huber’s research found that plants following in rotation after Roundup applications the previous year could be lacking in trace elements due to the residual glyphosate in the soil!  Lack of trace elements causes serious stress and disease in other livestock, and it’s possible that honey bees may also be affected.  The above susceptibility to fungi due to the use of Roundup may then lead to increased application of fungicides, a number of which are demonstrably toxic to bee brood.

But nothing in nature is simple.  Eliminating the competition of weeds and insects may allow plants to hold back from the production of natural toxins.  And a surprising piece of research found corn kernels from plants sprayed with either of two different herbicides actually contain more of the healthful carotenoids [30]!

The Future of Roundup

It took Monsanto several years to genetically engineer Roundup-resistant crops, yet took farmers only slightly longer to inadvertently produce Roundup-resistant weeds by the conventional breeding technique of applying a strong selective pressure–the continuous application of Roundup!

Weed management scientists consider glyphosate to be a once-in-a-100-year discovery—it works on 140 species of weeds, and is relatively environmentally friendly.  However, its overuse has led to the creation of several “driver weeds” that could soon lead to its redundancy in corn, soy, and cotton acreage [31].  This will drive farmers to turn to other herbicides (which will also in time fail).  We can only hope that someday they will be forced back into practicing crop rotation into legumes and pasture.

Reality Check

In order to clarify cause and effect, I often seek out extreme cases.  Such would be the situation in the Corn Belt, where I could compare the USDA’s hive and honey data from the old days to those under today’s intense planting of GM crops (Fig. 5)!

Figure 5.  The most intense planting of GM crops is in Iowa and Illinois (the dark green areas of the map above).  U.S. farmers planted nearly 100 million acres of corn this year, and 76 million of soy.  That is enough acreage to cover the entire state of Texas with GM crops!.   Source: http://www.nass.usda.gov/Charts_and_Maps/Crops_County/pdf/CR-PL10-RGBChor.pdf

So I went through the tedious process of downloading and transcribing the NASS agricultural census figures for Iowa.  I entered the amount of corn acreage, the total number of colonies in the state, and what I consider to be the best measure of colony health—honey yield per hive (which of course is largely weather dependent, but should show any trends).  I plotted the data below (Fig. 6):

Figure 6.  Bee and corn data from Iowa, and the dates of introduction of corn pest control technologies.  The dotted line is median honey yield per colony.  No factor appears to have affected honey production, but colony numbers have decreased since the arrival of varroa.  Gaps are missing data.  Source NASS.

Note: for non beekeepers, varroa is a parasitic mite that arrived in the U.S. around 1990 and quickly became, and still remains, the Number One problem in bee health–far more than any other factor.

Over the years, corn acreage increased by 18%.  Other than the prodigious crop of 1988, honey production has averaged around 67 lbs per hive.  The thing that stands out is the plot of number of colonies.  Hive numbers jumped up in the late 1980’s, likely due to federal honey price support payments, which peaked in 1988, and were cut off in 1994 [[i]].  Colony numbers peaked in 1990, the same year that varroa arrived in Ohio, and went down from there, leveling off to about half the number of hives present in the 1970’s.

I fully expected honey yields to decrease concurrent with the adoption of Roundup Ready varieties, but they didn’t!  Colonies still produce as much honey today as they did in the past, but this might be partially due to having fewer bees working the same amount of land, or to increased soybean nectar (which saved a number of Midwestern beekeepers from disaster during this year’s droughts).

Perhaps even more surprising is the fact that in a state covered in corn and soy, colony productivity did not appear to be affected by the introductions of either Bt or Roundup Ready corn, nor by the universal use of neonicotinoid seed treatments (between corn and soy, on over roughly two thirds of the entire state land area).  Note that honey yields actually increased for a few years following the introduction of clothianidin seed treatment!

Tellingly, hive numbers started to decrease after the arrival of varroa, and plummeted in the late 1990’s as fluvalinate failed as a miticide, and many beekeepers simply threw up their hands and quit the business.

Verdict on herbicide tolerant crops: from a nutritional standpoint, the increased use of herbicides, and the associated weed free “clean farming” has certainly not helped the bees in corn/soy areas, but it is hard to make a case for them causing colony collapse.

Verdict on GM crops in general:  Allow me to quote from the USDA:

…there is no correlation between where GM crops are planted and the pattern of CCD incidents. Also, GM crops have been widely planted since the late 1990s, but CCD did not appear until 2006. In addition, CCD has been reported in countries that do not allow GM crops to be planted, such as

Switzerland [33].

Looking Ahead:  The Chemical Treadmill & Pest Resistance

It is interesting to observe the evolution of agriculture from the perspective of a biologist.  Simple systems in nature are inherently less stable than complex systems.  The current agricultural model in the U.S. exemplifies simplicity to the extreme—plant a single species into bare soil year after year, killing any competitive weeds or insects with pesticides (either sprayed, systemic, or engineered into the plants), and attempt to maintain fertility by adding energy-costly fertilizer.  From a biological perspective, such a strategy is little more than an intense selective breeding program for the most resistant pests, and doomed to escalating chemical and energy inputs until the system collapses under its own weight.

I’m anything but a salesman for either Bt nor RR crops.  Both are mere short-term solutions—resistant bugs and weeds are already starting to spread.  I also have questions about the benefits of herbicide-intense no till planting [34], and hope that farmers return to alternative methods of weed control [35].  Luckily, the system will likely be self correcting, eventually forcing humanity to practice more sustainable methods of farming the land.  However, I suggest that those methods may well include the wise use of biotechnology.

Additional Discussion

The Back Story on Plant Breeding and GM Crops

Traditionally, farmers simply replanted with the seeds from the most desirable individual plants year after year; this is the simplest form of “selective breeding.”  For example, all the various cole crops (cabbage, kale, broccoli, cauliflower, kohlrabi, Brussels sprouts) were developed by intentionally selecting for unusual forms of the species (resulting from random recombination of the natural allelic diversity, spontaneous mutants, or natural hybrids).  This sort of selective breeding tends to result in a diverse assembly of locally-adapted cultivars.  In Oaxaca, Mexico– the birthplace of corn–some 150 traditional varieties of maize are grown without pesticides or herbicides, thereby maintaining an invaluable reservoir of genetically-diversity “germplasm,” which breeders can then cross and backcross in order to develop new cultivars (e.g., for pest or drought resistance).

In the early years of the U.S., seeds from desirable cultivars were distributed to farmers by the government, and plant breeding was performed at universities and at the USDA [36].  But since every strain breeds true, a farmer could save the seed and replant, leaving little opportunity for seed companies to make a buck.  So in 1883, they formed the American Seed Trade Association and began to lobby for the cessation of the government programs.

The Profit Motive

In the early part of the 20th century, the companies began to promote hybrids— crosses of two (or more) different strains or species that exhibited some sort of “hybrid vigor”—offering greater production, tastier fruit, or some other desirable characteristic.  Hybrids were a godsend to the companies, since they are often sterile or don’t breed true, meaning that farmers needed to purchase (rather than save) seed each season.

The seed lobby eventually shifted public funding away from the free distribution of selected seedstocks to instead encouraging the USDA and universities to develop inbred parental lines and breeding stock that the seed trade could then use to create proprietary hybrid varieties.  By 1960, farmers planted less than 5% of corn from saved seed; and less than 10% of soybeans by 2001.  As on-farm familiarity with the saving of seed was forgotten, farmers became willing consumers of produced seed.

Enter GM Crops

Then in 1980, the Supreme Court decided that seed companies could patent new varieties if they contained distinct and novel genetic markers.  This meant that farmers (in some countries) could now be required to sign licensing agreements to allow them to use the patented seed each season [37] (there is a hodge-podge of international patent laws in this regard [38]).

The Second “Green Revolution”

The first “green revolution” was based upon fertilizer, pesticides, and hybrid seed (and also resulted in forcing farmers onto “agricultural treadmills”–making them less self sufficient and sustainable, and more reliant upon purchased seed, pesticide and fertilizer use, and upon borrowed money).

In 1950 the Secretary of Agriculture Ezra Benson said to farmers, “Get big or get out.” His 1970s successor, Earl Butts, repeated that message, and exhorted farmers to “plant fence row to fence row” and to “adapt or die.”  Politicians who understood that a well-fed electorate is a happy electorate promoted policies that resulted in the destruction of the small family farm.  Our policy of price supports and favorable treatment of agribusiness has changed the face of the American farm and the composition of the American diet [39].

Today’s “second green revolution” is based upon technological advances in plant genetics (including GM) and the (at least partial) replacement of nasty pesticides with “biologicals.”  As an environmentalist, I find the new revolution to be more promising for ecological sustainability, but it is not without its downside—the current consolidation of agribusiness.    As I mentioned before, farms, seed companies, and chemical companies are all being bought up by a few main players.  Philip Howard details this consolidation in a free download [40], from which I quote:

This consolidation is associated with a number of impacts that constrain the opportunities for renewable agriculture. Some of these include declining rates of saving and replanting seeds, as firms successfully convince a growing percentage of farmers to purchase their products year after year; a shift in both public and private research toward the most profitable proprietary crops and varieties, but away from the improvement of varieties that farmers can easily replant; and a reduction in seed diversity, as remaining firms eliminate less profitable lines from newly acquired subsidiaries.

He then speaks of the concept of the “treadmill”:

For the majority of farmers, however, the result is that they must constantly increase yields in order to simply maintain the same revenue. [Monsanto’s sales pitch is that economic success in farming is driven by yield per acre [41].  Those that are unable to keep up with this treadmill will fall off,” or exit farming altogether. Their land ends up being cannibalized” by remaining farmers who seek to increase scale of production as another means of keeping up with the treadmill, leading to the increasing centralization of agriculture. Farmers who have managed to stay in business have adapted to this process, and are typically on the leading edge of the adoption of new technologies. As a result, they have a high degree of confidence in science and technological innovations.

However, this problem has nothing to do with GMO’s, but is rather due to the public’s unknowing acceptance of the practice.  Capitalism inevitably leads to consolidation unless consumers stop supporting corporate agribusiness with their pocketbooks and their votes, and start demanding that their government enforce antitrust efforts and better support small farmers.

But we are allowing economics and politics to distract us from the topic at hand—the technology of genetic engineering in plant breeding.

Cautions About GM

The most vocal critic of genetic modification is Jeffrey Smith, fear-mongering author of Seeds of Deception, producer of the film Genetic Roulette, and executive director of the inappropriately-named Institute for Responsible Technology. Smith is a gifted and effective communicator, as well as being a practitioner of “yogic flying” [42].  I will be the first to say that Smith’s anti-GMO claims [43] would scare the pants off of anyone, and make for compelling story!  The problem is that he plays loose with the facts—most of his claims simply do not stand up to any sort of scientific scrutiny.  I suggest that for an objective analysis of the facts, that you visit AcademicsReviewed.org, a website that tests popular claims against peer-reviewed science.  They address each of Smith’s alarming “facts” one by one [44].  It is a thrilling ride to open the two web pages side by side, first being shocked by Smith’s wild and scary claims, and then reading the factual rebuttal to each!  The thing that most bothers me about Smith’s writing is that he treats GM cultivars generically, rather than specifically addressing the merits or concerns for them individually.  This makes little sense, since any conventional crop has cultivars that cause human allergy or contain excessive levels of natural toxins, yet no one calls for the testing of each of them!

Perspectives On GM Crops

As you may have guessed by now, to me, the GM debate should not be about being pro or con, rather it should be about the intelligent discussion of reconciling its promise with its problems.  The GE genie is out of the bottle, and I can’t see that anyone is going to put it back in–so we might as well work with it!  So let’s cut through the hype and hysteria, the fears and judgments, and try to objectively look at the facts of the matter:

  1. From a plant breeder standpoint, genetic engineering holds incredible promise for the development of crops that could be tremendously beneficial to humans or the environment.  For example, “Transgenic cotton has reduced the need for conventional insecticides used against lepidopteran [pests] an average in the USA about 59.4% [and] Texas 74.7%…an average number of pesticide applications in conventional cotton has fallen from 4.3 in 1995 to 2.1 in the USA… with benefits to human health and the environment” [45].
  2. GM is only a part of plant breeding—most advances continue to be in conventional breeding, now assisted by “marker assisted selection,” which is embraced by environmentalists [46].
  3. However, someone needs to pay for the research, and the taxpayer is not doing it!  For a thoughtful discussion of the benefits of gene patents, see [47].
  4. Novel genetic markers can be patented, and a licensing fee can be charged, despite the fact that they are not GM!
  5. From a consumer standpoint, advanced breeding techniques can result in cheaper and more nutritious food, and less environmental impact from farming.
  6. Consumers have erroneously been led to believe that GM crops are dangerous to their health, and call for application of the precautionary principle.  My gosh, please read “Misconceptions about the causes of cancer” [48].  Few foods are entirely “safe”!  And “safety” can never be proven—it can only be disproven.  And no studies have ever disproven the safety of GM crops, nor have doctors noticed anyone ever getting sick from them, despite our eating them for 15 years!
  7. In truth, some scientists argue that plants produced by classical breeding methods should undergo the same safety testing regime as genetically modified plants. There have been plenty of instances where plants bred using classical techniques have been unsuitable for human consumption, causing toxicity or allergic reactions.
  8. Those that speak of applying the “precautionary principle” should read Jon Entine’s trenchant analysis of the fallacy of overapplication of that principle [49].  In truth, our regulators (EPA and FDA) vigorously apply the precautionary principle in the form “reasonable certainty of no harm.”
  9. The benefits of seed biotechnology cannot be realized without good seed germplasm to start with.  So a few large seed companies started buying up their competitors to acquire the most productive and desirable varieties.
  10. The downside of the above practice is that by 2008, 85% of GM maize patents and 70% of non-maize GM plant patents in the U.S. were owned by the top three seed companies: Monsanto, DuPont, and Syngenta [50].  Note that economists figure that when four firms control 40% of a market, it is no longer competitive; in the case of GE crops, the top four seed firms control 56% of the global proprietary seed market!
  11. On the flip side, these profits are an incentive for the large corporations to invest in innovative plant breeding research—Monsanto spends about $2 million a day on this.  This is important to keep in mind in an increasingly hungry world.
  12. On the dark side, Monsanto’s nearly $12 billion in annual sales allows the company to lobby regulators, influence universities, and spin the news.  These are standard business practices for any large corporation, but hardly make Monsanto uniquely evil.
  13. Be aware that patented genes are of use only if inserted into high-producing cultivars–which are developed by conventional breeding (which constitutes nearly half of Monsanto’s plant breeding budget).  These desirable cultivars have no patent protection.  Monsanto uses a non GE technology called SMART = Selection with Markers and Advanced Reproductive Technologies.  SMART technology is warmly embraced by environmental groups [51].
  14. Adding a genetic marker allows a company to identify its proprietary strains, like putting a nametag on a dog.  But clever breeders can back engineer the desirable germplasm out from patent protection.
  15. And remember that patents expire after 20 years.  The patents for Roundup Ready soybeans expire in 2014—at which time farmers, universities, and seed companies will then be free to propagate and sell the variety [52].  Patents are granted in order to spur innovation; by filing for patent protection, a company must make its discoveries public knowledge.  This is a good thing.
  16. Monsanto  invests 44% of its R&D on conventional (as opposed to GM breeding).
  17. Monsanto has also given rights to some of their patented crops to poorer countries, and recently donated a database of some 4000 genetic markers from cotton to Texas A&M [53].  The university plant breeders are excited in that the information will assist them in their conventional (non-GM) breeding of cotton, to the benefit of the environment [54 ].
  18. From the farmer’s standpoint, he has the choice of purchasing GE varieties that may be more productive, reduce insecticide use, or reduce tillage costs [55].  Keep in mind that there is nothing keeping him from purchasing “conventional” non-GM seed—it is available (I checked, and it sells at about half the cost of GM seed).  In our free enterprise system there is nothing to keep non-GM seed companies from selling an alternative product if there is a demand.  Farmers who are unimpressed by GM varieties freely switch back to conventional seed.
  19. From an agricultural standpoint, the widespread adoption of a few favored crop varieties (GM or not) can result in the irreplaceable loss of crop genetic diversity—this is of great concern to plant breeders.  If you haven’t yet seen the graphic of our loss of crop genetic diversity from National Geographic magazine, you should! [56].  Luckily, this does not appear to be occurring yet with maize in Oaxaca [57], but there is a legitimate concern that economics will force traditional farmers out of business, leading to the loss of heirloom varieties.  However, this is not a GM issue, but rather an effect of consolidation.
  20. From a sustainability standpoint, there is nothing to prevent constant breeding innovation to keep pace with pest evolution.  Genetically engineered crops can play a role in sustainable farming as our agricultural practices begin to shift to more ecologically sustainable methods.
  21. One should keep in mind how the simple splicing of a virus gene into the papaya saved the Hawaiian papaya growers from the ravages of ringspot virus—the GE papaya is the mainstay of the industry, and by virtue of keeping the virus in check actually allows nearby organic papayas to thrive.  Yet ecoterrorists recently hacked down thousands of GM trees [58].  It’s interesting to read the history of “Golden Rice” [59] to see how the anti-GMO lobby is specifically scared that the success of such a lifesaving crop might open the door for acceptance of other GM plants!

Update Jan 2013

News item: Leading Environmental Activist’s Blunt Confession: I Was Completely Wrong To Oppose GMOs. Blog in Slate Magazine

“If you fear genetically modified food, you may have Mark Lynas to thank. By his own reckoning, British environmentalist helped spur the anti-GMO movement in the mid-‘90s, arguing as recently at 2008 that big corporations’ selfish greed would threaten the health of both people and the Earth. Thanks to the efforts of Lynas and people like him, governments around the world—especially in Western Europe, Asia, and Africa—have hobbled GM research, and NGOs like Greenpeace have spurned donations of genetically modified foods.

But Lynas has changed his mind—and he’s not being quiet about it. On Thursday at the Oxford Farming Conference, Lynas delivered a blunt address: He got GMOs wrong.”

Anyone opposed to GMO’s should read Mr. Lynas’ well thought out address: http://www.marklynas.org/2013/01/lecture-to-oxford-farming-conference-3-january-2013/

Update May 2014

I’ve compiled a list of recent worthwhile reading on the “other side” of the GMO debate at http://scientificbeekeeping.com/gmo-updates/

So What’s The Problem?

The problem is that anti-GMO advocacy groups are determined to put a stop to all GE technology.  They targeted California with Prop 37, which applied only to packaged foods and produce.  A more cynical take on Prop 37 was that it was all about marketing: “If your produce is no different in terms of taste, safety and nutrition from a competitor, and costs more, apparently the only marketing option is to create a negative image of your competitor’s product” [60].

If Prop 37 had been successful, the promoters would then have targeted restaurants, the meat and dairy industry, and the beverage industry.  I personally feel that this is an extreme position, what with the human population growing hungrier every day, and climate change threatening agriculture worldwide with heat, drought, pestilence, and salinity problems.  Not only that, but GM crops hold promise for cheap omega-3 fatty acids (so that we don’t have to harvest fish for them), cost-effective biofuels, and less expensive pharmaceuticals.

A good blog on the problem with the anti-GMO fear campaign can be found at [61], from which I quote:

It would be bad enough if something like the Seralini study simply contributed to the unnecessary angst amongst consumers around the world.  It also has very real political, economic and practical effects.  For instance brand conscious food companies have used their leverage to prevent the development of GMO versions of potatoes, bananas, coffee and other crops because they fear controversy.  Apple growers worried about the market response are opposing the introduction of a non-browning apple even though it was developed by one of their own fruit companies.  French activists destroyed a government-run field trial of a virus-resistant root stock which could have made it possible to produce good wine on sites that have become useless because of contamination with sting nematodes and the virus they vector.  California voters have the potential to pass a seriously flawed “GMO labeling” initiative next month that could only serve the purposes of the lawyers and “natural products” marketers who created it.  More importantly, European and Japanese importers of wheat essentially blackmailed the North American wheat producers into blocking biotech wheat development because those companies were nervous about consumer response in countries where GMO angst is so high.  This has delayed by decades not only specific desirable trait development, but also what might have been an enormous private investment in a crop that is critically important for feeding a lot more people than just those in those rich countries.  There is a huge cost of “precaution” based on poor science.

I believe that people should be well informed before taking a stance on important issues.  I’d like to suggest one last excellent blog by an independent U.C. Berkeley evolutionary biologist and medical researcher:“How Bt Corn and Roundup Ready Soy Work – And Why They Should Not Scare You [62].


As always, thanks to my friend and collaborator in research Peter Loring Borst, and to anyone who still reads my articles after finding out that I’ve collaborated with Monsanto!


[1]  Key S, et al (2008) Genetically modified plants and human health. J R Soc Med.101(6):290-298. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2408621/

[2] For example: Antoniou, M, et al (2012) GMO myths and truths.

(Broken Link!) http://earthopensource.org/files/pdfs/GMO_Myths_and_Truths/GMO_Myths_and_Truths_1.3.pdf

[3] Chiba S, et al. (2011) Widespread endogenization of genome sequences of non-retroviral RNA viruses into plant genomes. PLoS Pathog 7(7): e1002146.

[4]  Domingo, JL and JG Bordonaba (2011) A literature review on the safety assessment of genetically modified plants. Environment International 37: 734–742.

[5] Key (2008) op. cit.

[6] Smith, JM (2003) Seeds of Deception.  Yes! Books

[7] Séralini, GE, et al  (2012)  Long term toxicity of a Roundup herbicide and a Roundup-tolerant genetically modified maize. Food and Chemical Toxicology (2012) http://foodpoisoningbulletin.com/wp-content/uploads/Toxicity-of-Roundup-Ready-Maize.pdf;



http://www.efsa.europa.eu/en/faqs/faqseralini.htm#9, http://www.emilywillinghamphd.com/2012/09/was-it-gmos-or-bpa-that-did-in-those.html,

(Broken Link!) http://www.ask-force.org/web/Seralini/Anonymous-Rat-List-Spaying-2003.pdfs, http://storify.com/vJayByrne/was-seralini-gmo-study-designed-to-generate-negati;

Benbrook, CM (2012) Impacts of genetically engineered crops on pesticide use in the U.S. — the first sixteen years.  Environmental Sciences Europe 24:24 http://www.enveurope.com/content/pdf/2190-4715-24-24.pdf,

Review http://weedcontrolfreaks.com/2012/10/do-genetically-engineered-crops-really-increase-herbicide-use/#more-432

[8]  http://journals.tubitak.gov.tr/agriculture/issues/tar-04-28-6/tar-28-6-1-0309-5.pdf

[9] http://www.monsanto.com/whoweare/Pages/monsanto-history.aspx

[10]  http://www.businessweek.com/stories/2010-01-10/monsanto-v-dot-food-inc-dot-over-how-to-feed-the-world

[11]  Methods for genetic control of plant pest infestation and compositions thereof



[12]  http://www.greenpeace.org/australia/PageFiles/348427/smart-breeding.pdf

[13] 2007 figures http://www.census.gov/compendia/statab/2012/tables/12s0835.pdf

[14] ETC Group (2008) Who owns nature? Corporate power and the final frontier in the commodification of life. http://www.etcgroup.org/sites/www.etcgroup.org/files/publication/707/01/etc_won_report_final_color.pdf

[15]  Blakeney, M (2011) Trends in intellectual property rights relating to genetic resources for food and agriculture. http://www.fao.org/docrep/meeting/022/mb684e.pdf This document covers the hodge-podge of international patent laws regarding plants and animals.

[16] http://www.monsanto.com/products/Pages/biodirect-ag-biologicals.aspx

[17] History of Bt  http://www.bt.ucsd.edu/bt_history.html

Mode of action http://www.bt.ucsd.edu/how_bt_work.html

[18] Gold 2002 Misconceptions about the causes of cancer http://potency.berkeley.edu/pdfs/Gold_Misconceptions.pdf A “MUST READ”!

[19]  Buchmann CA, et al (2007) Dihydroxy-7-methoxy-1,4-benzoxazin-3-one (DIMBOA) and 2,4-dihydroxy-1,4-benzoxazin-3-one (DIBOA), two naturally occurring benzoxazinones contained in sprouts of Gramineae are potent aneugens in human-derived liver cells (HepG2).  Cancer Lett. 246 (1-2):290-9.

[20]  http://en.wikipedia.org/wiki/Endophyte

[21] Duan JJ, et al (2008) A meta-analysis of effects of Bt crops on honey bees (Hymenoptera: Apidae). PLoS ONE 3(1): e1415.

[22]  Center for Environmental Risk Assessment (2011) A review of the environmental safety of the Cry1Ab protein. http://cera-gmc.org/docs/cera_publications/cry1ab_en.pdf

[23] Han, P, et al (2012) Does transgenic Cry1Ac + CpTI cotton pollen affect hypopharyngeal gland development and midgut proteolytic enzyme activity in the honey bee Apis mellifera L. (Hymenoptera, Apidae)?  Ecotoxicology. 2012 Aug 7. [Epub ahead of print]

[24]  Hendriksma HP, et al (2011) Testing pollen of single and stacked insect-resistant bt-maize on in vitro reared honey bee larvae. PLoS ONE 6(12): e28174.

[25] Benbrook, CM (2012) op. cit.

[26] Reviewed in http://www.sourcewatch.org/index.php/Glyphosate

[27] Mullin, C.A., J.L. Frazier, M.T. Frazier & T.J. Ciarlo – A primer on pesticide formulation ‘inerts’ and honey bees.  http://www.extension.org/pages/58650/proceedings-of-the-american-bee-research-conference-2011

[28] Ciarlo TJ, CA Mullin, JL Frazier, DR Schmehl (2012) Learning impairment in honey bees caused by agricultural spray adjuvants. PLoS ONE 7(7): e40848.

[29] Johal, GS and DM Huber (2009)  Glyphosate effects on diseases of plants.  Europ. J. Agronomy 31: 144–152.  http://www.organicconsumers.org/documents/huber-glyphosates-2009.pdf

Huber, DM (2010) Ag chemical and crop nutrient interactions – current update.  http://www.calciumproducts.com/dealer_resources/Huber.pdf

Reviewed in (Broken Link!) http://www.weeds.iastate.edu/mgmt/2010/glyMndisease.pdf

[30] Kopsell et al. (2009) increase in nutritionally important sweet corn kernel carotenoids following mesotrione and atrazine applications.  Journal of Agricultural and Food Chemistry 090619124509017 DOI: 10.1021/jf9013313

[31]  Laws, F (2010) http://cornandsoybeandigest.com/issues/will-glyphosate-fall-wayside-resistance-grows

[32]  http://www.nationalaglawcenter.org/assets/crs/RS20759.pdf

[33]  http://www.ars.usda.gov/is/AR/archive/jul12/July2012.pdf

[34]  http://www.misereor.org/fileadmin/redaktion/MISEREOR_no%20till.pdf

[35]  http://www.acresusa.com/toolbox/reprints/Organic%20weed%20control_aug02.pdf

[36] http://www.seedalliance.org/Seed_News/SeminisMonsanto/

[37] (Broken Link!) http://earthopensource.org/files/pdfs/GMO_Myths_and_Truths/GMO_Myths_and_Truths_1.3a.pdf

[38]  Blakeney, M (2011) Trends in intellectual property rights relating to genetic resources for food and agriculture. http://www.fao.org/docrep/meeting/022/mb684e.pdf This document covers the debate involved in international patent law regarding plants and animals.

[39] Philpott, T (2008) A reflection on the lasting legacy of 1970s USDA Secretary Earl Butz. http://grist.org/article/the-butz-stops-here/; but for a contrary view by an actual corn farmer, read Hurst, B (2010) No Butz About It. (Broken Link!) http://www.american.com/archive/2010/july/no-butz-about-it

[40] Howard, Philip H. 2009. Visualizing consolidation in the global seed industry: 1996–2008. Sustainability, 1(4), 1266-1287. http://www.mdpi.com/2071-1050/1/4/1266/pdf

[41] http://www.monsanto.com/investors/Documents/Whistle%20Stop%20Tour%20VI%20-%20Aug%202012/WST-Fraley_RD_Update.pdf

[42] http://academicsreview.org/reviewed-individuals/jeffrey-smith/

[43] http://responsibletechnology.org/docs/145.pdf

[44] http://academicsreview.org/reviewed-content/genetic-roulette/

[45] Greenberg, S, et al (2012) Economic and Environmental Impact Transgenically Modified Cotton Comparative with Synthetic Chemicals for Insect Control. Journal of Agricultural Science and Technology B 2 750-757.

[46] Greenpeace (2009) Smart Breeding.  Marker-Assisted Selection: A non-invasive biotechnology alternative to genetic engineering of plant varieties.  http://www.greenpeace.org/australia/PageFiles/348427/smart-breeding.pdf

[47] http://www.genengnews.com/gen-articles/in-defense-of-gene-patenting/2052/

[48]  Gold 2002 Misconceptions about the causes of cancer http://potency.berkeley.edu/pdfs/Gold_Misconceptions.pdf

[49] Entine, J (2010) Crop Chemophobia: Will Precaution Kill the Green Revolution? http://www.jonentine.com/pdf/CROPCHEMOPHOBIApre-orderform.pdf

[50] Howard, Philip H. 2009. Visualizing consolidation in the global seed industry: 1996–2008. Sustainability, 1(4), 1266-1287. http://www.mdpi.com/2071-1050/1/4/1266/pdf

[51] http://www.greenpeace.org/australia/PageFiles/348427/smart-breeding.pdf

[52] http://www.monsanto.com/newsviews/Pages/roundup-ready-patent-expiration.aspx;

[53] http://www.cotton247.com/article/3401/monsanto-donates-marker-technology

[54] http://www.youtube.com/watch?v=dcZyFH_eITQ

[55] http://www.biofortified.org/2012/05/the-frustrating-lot-of-the-american-sweet-corn-grower/#more-8670

[56] http://ngm.nationalgeographic.com/2011/07/food-ark/food-variety-graphic If you didn’t see this graphic in National Geographic, you should!

[57] (Broken Link!) http://researchnews.osu.edu/archive/mexmaize.htm

[58] http://www.huffingtonpost.com/2011/08/20/genetically-modified-papayas-attacked_n_932152.html

[59]  http://en.wikipedia.org/wiki/Golden_rice

[60] http://westernfarmpress.com/blog/proposition-37-gone-probably-not-forgotten?

[61]  http://appliedmythology.blogspot.com/2012/10/can-damage-from-agenda-driven-junk.html?utm_source=feedburner&utm_medium=email&utm_campaign=Feed%3A+AppliedMythology+%28Applied+Mythology%29

[62] http://www.science20.com/michael_eisen/how_bt_corn_and_roundup_ready_soy_work_and_why_they_should_not_scare_you

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Sick Bees – Part 18D: Colony Collapse Revisited

First published in: ABJ November 2012


Geomagnetic Flux


Back to the Suspects for CCD

Ag Exposure

A Pesticide-Free Control Group

CRP Lands

Good News



Sick Bees Part 18: Colony Collapse Revisited

Randy Oliver

Originally published in ABJ November 2012

“It’s what you know for sure that keeps you from learning.”

And I’m all about learning.  I’d like to make it perfectly clear that I do not consider myself to be the final arbiter on any matter!  In investigating many of these controversial subjects, my brain feels like a GPS unit, repeatedly saying, “Recalculating” and sometimes even “Turn around when possible.”   This is why I take care to hold no positions, and appreciate being intelligently challenged on any point.   If something comes to my attention that makes me rethink or correct anything I’ve written, I am more than happy to rebut myself on these pages.


Geomagnetic Flux

In my last article I dismissed geomagnetic flux as the cause of CCD, but also said that I was corresponding with proponent Dr. Tom Ferrari.  A point that he recently made is that the timing of a flux event is critical—it must occur during, or immediately before flight hours.  Although I still have a healthy skepticism about solar flares causing colony collapse, I am keeping an open mind that they may indeed affect bee homing ability, and could plausibly contribute to forager loss.


In a recent article, I put in a good word for Purdue’s Driftwatch program [1], based upon the positive feedback that I had gotten from some beekeepers.  However, I wish to thank beekeeper Jeff Anderson for bringing to my attention legitimate concerns about its uncritical promotion by state agencies.

First, some background on pesticide regulation.  Pesticides are registered and labeled at the federal level by the EPA.  States must follow those labels–they may impose further restrictions, but not fewer.  In general, the state has primary authority for monitoring pesticide applicators to ensure that they comply with label restrictions, and is charged with the responsibility to take enforcement action in the case of violations (as in those resulting in bee kills).  The EPA refers to the states as “primacy partners”; each of which may use a “state lead agency” (such as its department of pesticide regulation, agriculture, or environment to enforce the law [2].

A problem may occur when a state writes pesticide use guidelines for the protection of honey bees (and other pollinators).  Pesticide applicators may put pressure on the local primacy partner to shift the responsibility of pollinator protection from the EPA and the applicator onto the shoulders of the beekeepers.  If guidelines are written to suggest that beekeepers should register their apiary locations, and that applicators about to spray should then notify those beekeepers, the applicators may get the misimpression that such notification absolves them from their responsibility to carefully adhere to label restrictions, especially if there is any wording about the beekeeper moving or covering his hives.  Commercial beekeepers strongly object to any suggestion that they be forced to “duck and cover”!  And, a beekeeper may be adverse about putting his prime locations into a public database, which might result in some unscrupulous beekeeper moving in right on top of him!

In many places, conscientious applicators do indeed work constructively with beekeepers, and I’ve had them give me courtesy calls to discuss potential spray issues.  As much as I appreciate that sort of cooperation, a large commercial beekeeper simply has too many locations, and not enough time to negotiate with every applicator who might be spraying within flight range of every one of his yards.  It’s not the beekeeper’s job to be a pesticide expert–that’s the responsibility of the applicator!

The fact is that the EPA label restrictions are designed to protect pollinators, and if the restrictions are carefully followed, the beekeeper theoretically should need not ride herd on every pesticide applicator (Fig.1).

Figure 1.  A grower spraying fungicide onto almond trees, and the understory weeds, each in full bloom.  This sort of application is permitted by the label, and generally has only minor impact upon bees.  However, EPA is closely following recent research on adverse effects of both fungicides and their adjuvants upon colony health.

Practical application: voluntary programs in which beekeepers may register their apiary locations to be notified by applicators can be of benefit (it works for me in my county), and a beekeeper may well wish to negotiate with an applicator about to make a lawful application.  But beekeepers must be careful about allowing any “hot button” words involving the moving or covering of hives to be institutionalized in state guidelines, lest applicators get the misimpression that they can then ignore restrictions such as “Do not use on flowering crops or weeds” if they have notified the beekeeper, or that it is then the beekeeper’s responsibility to protect his hives from pesticide misapplication.

Back to the Suspects for CCD

Ag Exposure

Biological plausibility: plausible due to nutritional or pesticide issues.

Honey bees and farming have one major aspect in common—they both prosper on fertile, moist land.  Prime bee forage land and prime agricultural land are one and the same.   As it is, much of the world’s best acreage for bee forage has been converted to intensive agriculture, often dedicated to the cultivation of a single species of plant.

I’ve had beekeeper after beekeeper tell me how colonies summered on agricultural cropland often go downhill, or don’t make it through the winter.  These anecdotal reports are supported by data from at least two studies:

  1. I mentioned a couple of months ago Dr. Erickson’s demonstration that colonies exposed to permethrin-sprayed corn died during the following winter.
  2. The Coordinated Action Project’s data for 2009-2012 [3] found that the proportion of land in intensive agriculture within 2 miles of the apiaries correlated with colony mortality.  Although pesticides were obvious suspects, the study surprisingly did not find any particular correlations between pesticide levels in trapped pollen and amount of ag exposure, nor any correlations between pesticide exposure and colony mortality!

Curious as to whether recent colony losses (Fig. 2) correlate with the degree of exposure to commercial agriculture (Fig. 3), I checked the National Agricultural Statistics to find which states had the greatest percentages of their land areas in various crops.

Figure 2. Recent colony mortality rates for surveyed states.  Compare the apparent correlation between those areas with high loss rates (dark states) with the types of cropland in the following map.  Copyright the International Bee Research Association. Reproduced from [[i]] the Journal of Apicultural Research (2011) Issue 50(1): 1-10 by the permission of the Editors.

[[i]]  vanEngelsdorp, D, et al (2011) A survey of managed honey bee colony losses in the USA, fall 2009 to winter 2010. Journal of Apicultural Research 50(1): 1-10.

Figure 3.  The scope of the impact of farming practices is staggering–roughly 2/3rds of the land area in the entire states of Iowa and Illinois, and half the footage of Indiana and North Dakota, are planted to principal crops (a small amount is pasture). Source http://www.nass.usda.gov/research/Cropland/cdl09_l.jpg

It’s hard to compare the two maps above directly, since beekeepers move hives, and the colony mortality data is very crude by comparison (only to the state level) to the cropland map.  However, one can’t help but see that colony mortality appears to be higher in corn, soy, and cotton areas.

As an aside, in researching this subject, I found that even more detailed interactive maps are available from the NASS (Fig. 4):

Figure 4.  I created the above map to scout for alfalfa locations (in pink) in a small area of Nevada.  The detail of these maps is amazing!    Check it out at http://nassgeodata.gmu.edu/CropScape/.


The first thing about agricultural land and bees that generally comes to mind is the impact of pesticides, which I will return to later in this series.  However, one must not ignore another important effect of crop monoculture—its impact upon bee nutrition:

“One impact of large-scale agriculture with extended expanses of a single cultivated crop species to honey bees is the availability of pollen, which is the only source of proteins and lipids in the bee diet and thus crucial for their survival and development.  Agricultural trends toward larger monoculture farming systems can place pollinating honey bees in situations where they have a restricted choice of dietary pollen” [5].

So what is wrong with a “restricted choice” of pollen?  Some “monolectic” species of solitary bees are specialized to feed solely on a single type of pollen (mono = single; lect = to gather).  Honey bees, on the other hand, need to collect pollen throughout the season, so must by necessity be “polyletic” since no single plant species blooms for that long.  Some pollens (almond, mustards, apples, red gum, etc.) are plentiful and nutritionally complete, but a number (corn, sunflower, blueberry, citrus, pumpkin) are not.  If you’ve ever trapped pollen, you’ve noticed that pollen foragers bring home a medley of pollen types, thus increasing their chance of obtaining all necessary nutrients.

In agricultural areas, despite there being vast fields of single species of plants in bloom, bees still go out of their way to collect a diversity of pollens.  Dr. Jerry Bromenshenk (in prep) has surveyed pollen loads in agricultural areas for the past few years.  In corn country during tassling, he found that on average,  corn pollen still constituted less than 25 percent of pollen loads.  This is not surprising if you think about it, since if the bees in those areas are producing honey, they sure aren’t getting it from corn, so must have located other forage!  When I visited apiaries in the Midwest, I surveyed their surroundings from the ground and via Google satellite maps–it appears that bees are remarkably efficient in finding little patches of good forage scattered among vast seas of corn and soybeans!

Another aspect of commercial crops is that plant breeders select for yield per acre, not for plants that produce nectar or nutritious pollen.  Beekeepers report vast differences in bee response to different cultivars of several crops.

Practical application: Colonies may go downhill on certain crops due to poor pollen nutrition; they then need better forage in order to recover.  Recent research found that colonies subsisting solely on corn pollen rear less brood, and have shorter worker lifespans [6].  Such colonies cannot be expected to winter well.

However, so long as alternative forage is available, bees may fare well in agricultural areas, provided that they don’t take a hit from pesticides.

A Pesticide-Free Control Group

I will return in a subsequent article to the impact of pesticides, but for now let me say that the few studies that have looked at pesticide levels in beebread do not clinch the case for pesticides being the only problem for bees in ag areas [7].

My apiaries often serve as a “control group” with regard to pesticides, since I avoid (other than in almonds) areas in which pesticides are used.  Yet I still experience, in some locations, poor buildup, late summer dwindling, and poor winter survival.  A case in point is a pumpkin pollination contract that I had for several recent years in an area of Nevada surrounded by desert (Fig. 5).

Figure 5.  I pollinated 40 acres of pumpkins grown in this irrigated oasis in the middle of the desert.  The only other “green” is a sod farm (most of the rectangular checks) and some center pivot alfalfa.  No pesticides were used in this valley, yet colonies still fared poorly.  Imagery from Google maps, ©DigitalGlobe, GeoEye, USDA Farm Service Agency, TerraMetrics.

The only forage available was 40 weedy acres of pumpkins, quite a bit of irrigated alfalfa, and natural Rabbitbrush in fall.   Pesticides were not used anywhere in the valley.  I’d move strong colonies in each July, heavy with stores, treated for mites, and with a 3-lb chunk of pollen supplement.  The poor bees experienced boom and bust situations (mostly bust).  The colonies simply starved on the forage provided by the pumpkins and weeds between alfalfa blooms (typically two blooms), and I generally had to resort to emergency open drum feeding and pollen supplement to keep them alive.  Depending upon how much alfalfa was under irrigation that year, they might be able to rally and fill the combs with honey, or not.  Some years they would rebound somewhat when Rabbitbrush came into bloom, but generally not enough to build up for winter.

In the above example, my 40 colonies were the only ones on about two square miles of irrigated green cropland.  But there is no way that they could have survived on their own.  There simply wasn’t enough consistent mixed forage to support them.

Living at the Edge and on the Edge

Unlike in natural areas, in which pollen and nectar flows transition fairly gradually, on agricultural lands they can be cut off in a matter of hours (just watch how fast a modern swather takes down a field of alfalfa in full bloom—breaks your heart).  A flow can suddenly end when fields are tilled, when flowering weeds are mowed or burned off with an herbicide, or when every plant in a crop finishes blooming all at the same time.  The bees are then forced to forage at the edges of the fields (Fig. 6).

Such a sudden cessation of food intake can also quickly bring a colony to the edge of serious protein deficit (not to mention the lack of nectar).  The nurse bees in such a stressed colony must immediately deal with all the protein-hungry brood and foragers, and the colony must shift to survival mode.

The more I study bees, the more it appears to me that colonies are often living right on the edge of disaster.  As I pointed out with my growth rate graphs [8], normal colony growth requires phenomenal production of brood, with a complete turnover of the summer population about every 5 weeks.  Colonies can go from boom to bust in a matter of days if nutritious pollen and nectar become unavailable.  Colony immunocompetence falters and broodrearing is curtailed, setting up conditions for varroa, nosema, or viruses to explode.

Practical tip:  Here at Samemistaketwiceagain Apiaries, we find that as with many management issues involving bees, being proactive is much more cost effective than being reactive—it’s easier to maintain colony momentum than to restart them after they’ve come to a halt!  A little supplemental feeding during dearth can go a long way towards healthier colonies.

Figure 6.  The bee in the center of this photo is foraging at the edge of a cornfield that is weed-free after being sprayed with Roundup.  The clover on the margins, and whatever grows in the patches of woods, is the only forage between here and the horizon.  Modern farming practices greatly reduce the amount and diversity of bee forage.  Photo courtesy of beekeeper Larry Garret.

Now add the pesticide component

When the forager force suffers attrition due to pesticides—although perhaps not enough to cause piles of dead bees in front of the hives—this will both reduce incoming nectar and pollen, plus force younger bees to take the places of the poisoned foragers.   A strong colony full of sealed brood may be able to rebound from one hit to the foragers, but not from repeated hits, or from a hit late in the season.

Or, pesticide residues in stored pollen or nectar might negatively affect brood survival, harm the nurse bees (due to their eating so much pollen), decrease resistance to parasites, or shorten winter bee longevity.  This may be especially true with the cocktail of insecticides, fungicides, and surfactants sometimes found in beebread.

During dearths (and in fall), a colony that shuts down into survival mode due to lack of pollen can generally stick it out until it can rebound when another nectar and pollen flow starts.  However, the beekeeper should be aware that when a colony cuts back its population, the relative rate of infestation by varroa can quickly skyrocket!  And if a colony in such a condition is then exposed to what would normally be a minor hit by pesticides, the negative effects can be greatly exacerbated.

Practical application:  if, due to lack of alternative flora, bees are forced to forage solely on agricultural crops, then they may be exposed to pesticide residues that they would normally avoid, or store larger proportions of nutritionally-incomplete pollens (such as from field corn).  Extension apiculturists have long pointed out that feeding colonies pollen supplement may help to mitigate the above problems.  This is especially true in late summer as colonies suffer from the triple whammy of normal downsizing, poor nutrition, and rapidly rising varroa infestation rates.

CRP lands

Beekeeper Zac Browning explains that large-scale commercial beekeepers are having a tough time finding safe places to park their hives during the summer: “We’re limited to the fringes of rural America, where we can stay away from pesticides, where we can find wildflowers.”

One of the most popular places to look for locations has been on Conservation Reserve Program lands, for which farmers are paid by the government to convert cropland to long-term vegetative cover for the benefit of the environment.  These lands in the northern states are often planted to clover or legumes, thus providing excellent forage for pollinators.  As a result, commercial migratory beekeepers flock there during summer (Fig. 7).

Figure 7.  CRP lands often provide good bee forage.  Over a third of commercial hives spend the summer in just three states—Montana and North and South Dakota [[i]].  Map from USDA [[ii]].

[[i]]  http://usda01.library.cornell.edu/usda/current/Hone/Hone-03-30-2012.pdf

[[ii]]  http://www.fsa.usda.gov/Internet/FSA_File/crpenrolloct11dot.pdf

But with the high prices currently being offered for agricultural commodities, farmers are converting bee-friendly CRP land to monoculture cropland, putting the hurt on beekeepers.  I don’t expect this situation to improve.

Good news

Press release: August 29, 2012

Portland, Ore.— Last Friday Agriculture Secretary Tom Vilsack announced that the Xerces Society for Invertebrate Conservation, along with collaborating bee researchers, will receive a $997,815 USDA Natural Resource Conservation Service Conservation Innovation Grant to improve pollinator habitat on farms and ranches across the U.S.

Through this project the researchers and conservationists hope to answer questions such as how to best manage wildflower meadows on the edge of farms as long term pollinator habitat, how to control weeds in such pollinator meadows using organic techniques, and how to quantify the effectiveness of various types of flowers in supporting crop-pollinating wild bees and honey bees.  Another part of the project will work with native plant nurseries to mass-produce wildflower seed for plants with high pollen and nectar value that are not currently available among the nursery industry.

OK, the above sounds pretty idealistic, but beekeepers can certainly encourage these sorts of efforts to increase pollinator habitat on agricultural lands.  Europe has a leg up on us in this direction, and can serve as an example [11].  Many landowners are willing to manage their lands for the benefit of wildlife, including pollinators.  There is currently great support for such efforts across the political spectrum; beekeepers should certainly get on board the bandwagon!

Ag Exposure and CCD Conclusion

Colonies in agricultural lands often do not fare as well as those in favorable natural settings.  It is not yet clear how much of the problem is due to pesticides or other factors, but the lack of diverse nutritional sources is a prime suspect.

Small-scale beekeepers may have thriving hives in agricultural areas in which large-scale beekeepers report problems.  This observation suggests that hobbyists may have better luck in finding good apiary locations, perhaps since they don’t need to unload truckloads of hives.

Agricultural exposure does not fulfill Koch’s postulates as being the cause of CCD, but may well be a contributory factor in colony mortality and collapse.

To be continued…dare I broach the subject of GMO’s?


As always, I am immensely indebted to my partner in research, Peter Loring Borst.  I wish to thank the hardworking members of our national associations (the National Honey Bee Advisory Board and the AHPA/ABF/EPA beekeeper pollinator protection work group members) who are representing beekeepers’ interests in Washington and at the state level.  Darren Cox, Jeff Anderson, Dave Mendes, Steven Coy, and Rick Smith have been especially generous with their time in explaining the politics to me.


[1]  http://www.driftwatch.org/

[2]  http://www.epa.gov/opp00001/enforcement/monitoring.htm

[3]  Drummund, F, et al (2012) The First Two Years of the Stationary Hive Project: Abiotic Site Effects. http://www.extension.org/pages/63773/the-first-two-years-of-the-stationary-hive-project:-abiotic-site-effects

[4]  vanEngelsdorp, D, et al (2011) A survey of managed honey bee colony losses in the USA, fall 2009 to winter 2010. Journal of Apicultural Research 50(1): 1-10.

[5] Chauzat, M-P, et al (2009) Influence of pesticide residues on honey bee (Hymenoptera: Apidae) colony health in France. Environ. Entomol. 38(3): 514-523.

[6]  Höcherl, N, et al (2012) Evaluation of the nutritive value of maize for honey bees. Journal of Insect Physiology 58(2): 278–285.

[7] Thompson, HM (2012) Interaction between pesticides and other factors in effects on bees. http://www.efsa.europa.eu/en/supporting/doc/340e.pdf

[8]  http://scientificbeekeeping.com/sick-bees-part-17-nosema-the-smoldering-epidemic/

[9]  http://usda01.library.cornell.edu/usda/current/Hone/Hone-03-30-2012.pdf

[10]  http://www.fsa.usda.gov/Internet/FSA_File/crpenrolloct11dot.pdf

[11] Wratten, SD, et al (2012) Pollinator habitat enhancement: Benefits to other ecosystem services. Agriculture, Ecosystems & Environment 159: 112–122.  Good bibliography of research papers on the subject.

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Sick Bees – Part 18C: Colony Collapse Revisited

First published in: ABJ October 2012

Sick Bees Part 18c:

Colony Collapse Revisited

Randy Oliver


Originally published in ABJ October 2012

Beekeeper Management Practices

Environmental Factors

Ozone and Air Pollution

HAARP (The High Frequency Active Auroral Research Program)

Cell Phones/Electromagnetic Radiation (EMR)

Geomagnetic Flux




Summary So Far


Further Reading


Sorry for my recent diversion from this series while I addressed the neonicotinoid insecticides. Please allow me to continue with my retrospective analysis of the suspects suspected or implicated, rightly or wrongly, to be the cause of CCD.

In the previous article of this series, it seems that I hurt the feelers of some beekeepers by irreverently dismissing some of their pet suspects for Colony Collapse.  Unlike during the peak of CCD, when researchers were desperately following up every possible lead, I have the advantage of retrospection, as well as now having had the opportunity to observe and study sudden colony depopulation again and again.

However, before I get to the real meat of CCD, I feel that it would be to the benefit of the reader to cut through the muddle of all the various things that have been blamed for being the cause of the disorder by evaluating each of them using scientific logic.

Although most named suspects are biologically plausible, a number can be quickly ruled out by the application of Koch’s postulates—either that suspect isn’t always present during collapse events, or doesn’t always cause the problem when it is present.    I’ll address the suspects in the following order (spoiler: I’m saving the best for last).

  1. Beekeeper management practices
  2. Environmental factors
  3. Chemical exposure
  4. Biological agents

Although my focus will be upon determining the “proximate causative agents” of sudden colony collapse, I’ll also examine how the various suspects may contribute to colony mortality or morbidity in general.  In order to pick up the thread of this series, and to review the terms that I’ll be using, you may wish to reread the previous installment (available at my website1.

Beekeeper Management Practices

Due to his being a government employee, Colony Collapse researcher Dr. Jeff Pettis, unlike me, must be careful that his public statements are politically correct.  But in his presentations on CCD, he can’t help but candidly note that 25% percent of beekeeping operations accounted for fully 75% of total colony losses.  And any apiary inspector will tell you that it was usually the same beekeepers over and over.  This fact certainly suggests that beekeeper management practices may be related to the degree of colony mortality in an operation.

Let me be perfectly clear here—CCD can happen to anyone, and there is nothing funny about it.  If you’ve never watched the film “The Last Beekeeper,” you should.  In it, hard working beekeepers are brought to tears as they watch their operations collapse from CCD just prior to almond bloom—leading to their financial ruin.  I’ve experienced CCD myself, and wouldn’t wish it upon anyone!

That said, CCD also quickly became an excuse for absolving oneself of the consequences of PPB (Piss Poor Beekeeping).  I’ve heard many a beekeeper who knew damn well that his colonies died from varroa or some other form of neglect, later piously tell a reporter that they were hit by CCD!

Here’s the thing:  I’ve visited beekeepers all over the country.  Even in areas in which some “noisy” beekeepers blame their elevated colony losses upon pesticides, the weather, the alignment of the stars, or some other factor, there are always other “quiet” beekeepers who experience very low losses under the same conditions.  The difference could be luck, but more often appears to be due to better management.

Biological plausibility:  Allow me to quote from the original CCD report, back when it was still called “Fall Dwindle Disease”2:

“All [affected operations] experienced some form of extraordinary “Stress” at least 2 months prior to the first incidence of “die off” associated with “Fall dwindle disease”.  The nature of this stress was variable but included nutritional stress (apiary overcrowding, pollination of crops with little nutritional value), dramatic pollen and nectar dearth, or varroa mite pressure.”

Honey bee colonies can handle a lot of insults so long as they get enough high-quality forage (Fig. 1) to maintain vigorous broodrearing, and are not hamstrung by parasites.  Those beekeepers who make sure that their colonies are always well fed, especially with protein, and never allow varroa infestation to exceed a few percentage points, appear to have far fewer problems than others.  In some areas, treatment against nosema also appears to help.

Figure 1.  One common denominator for healthy colonies is that they have year ‘round access to high quality forage.  A profusion of pollen sources promotes strong broodrearing and a robust immune system.  In the arid West, patches of irrigated pasture such as this are precious, and you’d no more tell other beekeepers where you found them than you’d brag about where your favorite fishing hole was.


Transportation stresses from migratory beekeeping—non beekeeper bloggers love to blame CCD on our “unnatural” moving of bees from one location to the next.  In truth, bees, due to their innate ability to reorient to a new location after swarming, seem to take being moved in stride.  In my own operation, I follow the bloom up the mountains during the season, akin to moving other livestock to better pasture, and my colonies are the better for it.  Even colonies moved from the East Coast to California and back do not appear to suffer greatly from transportation.

Multiple pollination contracts—If bees are moved from one pollination contract to another, they may suffer from poor nutrition and exposure to pesticides.  This problem can generally be mitigated by supplemental feeding (Fig. 2) or by “resting” them on natural pasture to rebuild.

Figure 2.  One management practice that beekeepers learned from the CCD experience is the value of feeding supplemental protein.  There are several high quality pollen supplements now on the market.  Not only can good nutrition boost the bees’ immunocompetence, but the colony can convert this protein into replacement bees to take the place of those lost due to disease or pesticides.

Feeding of high-fructose corn syrup–HFCS has been blamed with little supportive evidence.  Granted, HFCS can become toxic to bees due to the formation of hydroxymethylfurfural if it is overheated or stored for long periods in metal containers, but most commercial beekeepers are now aware of this.  No correlation has been found between the feeding of HFCS and CCD.

Overcrowding of locations—just as other livestock cannot thrive if they are overstocked onto insufficient pasture, too many hives in one area compete for limited resources.  If a beekeeper places a hundred hives into an apiary that has adequate forage for only two dozen, he can expect those colonies to have problems.

Holding yards—the need to stockpile semi loads of hives at certain times of the year can create serious problems due to:

  1. The nutritional stress due to inadequate forage as mentioned above.
  2. The behavioral stress caused by the robbing pressure between overstocked colonies.
  3. The fact that crowded bees all “share spit” in nearby flowers and at water holes.  Need I explain the consequences?

Easy transmission of virulent strains of pathogens (especially the constantly-mutating viruses) that may spontaneously arise in one or more hives (the more hives, the more chance of the evolution of a new strain).  Drifting, robbing, and hitchhiking varroa mites can quickly spread that pathogen throughout the entire yard (Fig. 3)!  In a number of instances, beekeepers observed CCD spreading from one group of sick colonies to adjacent holding yards.

Figure 3.  Perfect conditions for the spread of an epidemic.  In this almond orchard, as with many monocultures, there is virtually no bee forage prior to, or immediately after the bloom, resulting in colony nutritional stress.  Even in good honey locations, beekeepers must keep in mind the forage conditions at times other than during the flow.

Other commercial beekeeping practices—some “natural beekeeping” advocates have blamed the use of antibiotics, synthetic miticides, or sugar feeding for CCD, but these practices were common prior to CCD, and are used in many operations that have not experienced CCD, so the charges simply don’t stick.

Verdict:  I’m not buying the notion that CCD can be blamed on commercial beekeeping practices per se, since no particular practice is always associated with colony collapse, nor does any particular practice always create it.  But poorly managed colonies–whether in a large commercial or small organic operation–appear to be more susceptible to mortality or collapse.  Good bee husbandry—including proper nutrition and parasite management—goes a long way toward keeping colonies healthy.  One need only note how commercial beekeepers were able to ramp up their colony numbers for almond pollination when the growers made it financially worthwhile for them to invest in good management practices!

Environmental Factors


Biological plausibility: Ozone is highly reactive chemically, and oxidizes organic molecules.  “The scent molecules produced by flowers in a less polluted environment, such as in the 1800s, could travel for roughly 1,000 to 1,200 meters; but in today’s polluted environment downwind of major cities, they may travel only 200 to 300 meters…This makes it increasingly difficult for pollinators to locate the flowers.”3

Analysis:  Although the negative effect of ozone upon bee foraging success is biologically plausible, neither the timing nor location fit the sporadic occurrence of CCD.  The timing is wrong, since ozone levels (and general air pollution) in the U.S. have actually been dropping since the early 1990’s and ozone levels showed a notable decline after 2002.4  Neither does location fit, since CCD occurred in rural areas with little ozone, and conversely is not normally a problem in my area of the Sierra foothills, which often (and unfortunately) has one of the highest ozone levels in the country due to the smog blowing up from Sacramento (easy to confirm, since the ozone quickly destroys anything made of rubber).

Verdict:  Although a high ozone levels certainly doesn’t make life any easier for bees (or beekeepers), it does not appear to be the cause of colony collapse.


HAARP is a favorite of conspiracy theorists, and one website5 presents a convincing case that the high frequency transmissions are the cause of CCD.  The hypothesis is that the transmissions are interfering with the bees’ navigational ability.  I’m not being frivolous here–some earnest beekeepers implored me to investigate the facts.

Biological plausibility: In brief, the HAARP antenna array in Alaska is a cooperative military/academic experimental station that shoots strong electromagnetic pulses into the ionosphere.  Either the resulting wavelengths of light produced in the ionosphere above the station, or the extra low frequency (ELF) radio waves transmitted around the globe could plausibly interfere with the bee navigation system.

Analysis: The emitted electromagnetic energy pulses from HAARP are dwarfed by the natural atmospheric electromagnetic radiation variation from the sun, and their strength drops off according to the inverse square law.  At only 150 ft away from the antennas, it already falls within human safety standards.   When I did the math, the strength of the signal by the time it finally reaches my apiaries in California would be less than a billionth of the intensity of that typically found near AM broadcast station antennas in many urban areas6.

Similar ELF waves are created by lightning bolts, which strike the Earth some 100 times per second.  A single bolt can produce far more electromagnetic radiation that the entire 3600kW output of HAARP.7  And as far as the timing, HAARP started intermittent testing in 1994, but did not actually begin transmitting at full power until 2007, long after CCD started to be reported.

Verdict:  The laws of physics and the timing appear to let HAARP off the hook as being the cause of CCD (the math doesn’t support it being the cause of earthquakes either).

The next two factors come under suspicion based upon the hypothesis that CCD is caused by bees being unable to find their way back to the hive, thus leading to sudden colony depopulation.

Cell Phones / Electromagnetic Radiation (EMR)

Biological plausibility: Bees produce tiny molecules of magnetite in their bodies, which they appear to use in navigation.[i]  Electromagnetic fields could plausibly disrupt their ability to find their way back to the hive.  Alternately, some bee tissues may resonate with certain wavelengths of EMR, leading to biological effects.

Analysis: The intermittent appearance of CCD does not match the steady proliferation of cell phone and other electromagnetic transmissions.  More importantly, CCD occurred in areas in which you couldn’t get cell reception; conversely, plenty of apiaries thrived immediately adjacent to cell phone and radio towers, and under electrical transmission lines.

Verdict:  Although the cell phone hypothesis certainly resonated with the public (and gave beekeepers fodder for a lot of jokes), there are more cell phone transmissions today than when CCD made the press, yet CCD has largely gone away.  One thing to keep in mind with any alleged cause of CCD is that it should also explain the historical appearances of colony depopulations in the older literature—cell phones were not around then.

Geomagnetic Flux

Natural solar flares cause “geomagnetic storms” on Earth.  Dr. Tom Ferrari8 has proposed that such storms may be the cause of CCD due to their effect upon bee magnetoreception, causing bees to lose the ability to find their way home.

Biological plausibility: The hypothesis that geomagnetic flux affects bee navigation is biologically plausible, and I have been corresponding with Dr. Ferrari, and have seen his supportive (unpublished) experimental data that forager return takes longer during solar flare events.  Solar storms have also occurred as long as the Earth has existed, so could possibly explain historical colony depopulation events.

Analysis: The question boils down to whether CCD is actually caused by the inability of foragers to find their way back to the hive.  If solar storms were indeed the cause of CCD, one would expect them to affect all colonies equally over a wide area in which the flux occurred during daylight hours, which does not happen.  And since I began correspondence with Dr. Ferrari, I’ve paid particular attention to any news reports of major solar storms to see whether I could observe the resulting geomagnetic flux causing any noticeable depopulations of my apiaries—I haven’t.

Verdict:  Although I find Dr. Ferrari’s experimental data to be of great interest, since it appears to indicate that bee navigation is indeed affected by aberrations in the geomagnetic flux, I do not find it to make a compelling case for being the cause of CCD.  I do look forward, however, to seeing more research on this aspect of bee navigation.


In many recent and historical instances of unusual colony mortality, an unexpected spring or fall chill preceded the event.

Biological plausibility: The unexpected chilling of a colony with brood requires the colony to ramp up its metabolism, which stresses bees already suffering from nosema or virus infections.  Such chilling may also suppress the bee antiviral response.9  In addition, should the colony already have a low bee:brood ratio due to a virus or nosema infection, then a cold snap could result in the chilling of the brood, which can greatly shorten the subsequent life spans of those workers.10

Analysis:  Dr. Bill Wilson observed in 1979 how “Disappearing Disease” tended to be associated with chill events:

“In the case of [Disappearing Disease]… the colonies frequently have gone through a period of nectar and pollen collection with active brood rearing. Then the weather has turned unseasonably cool and damp and remained adverse for from about 3 to 14 days. Such a situation usually occurs in early spring. During the inclement weather, the bee populations dwindle because the worker bees disappear from the hive leaving a “handful” of bees and the queen.” 11

A similar correlation between chill events and the occurrence of sudden colony depopulation has been noted again and again in the historical record, as it was with the first reports of CCD.12  In my own experience, I have repeatedly observed unseasonable chills to precipitate the sudden collapse of colonies infected with either nosema or viruses. 13

Verdict:  There is a strong case to be made for unexpected chilling to contribute to colony collapse.  The chilling is not the proximate cause of the exodus of the bees from the hive, but tends to precipitate the chain of events leading to colony collapse (see Sick Bees, Part 2).14


Naysayers aside, the Earth’s climate appears to be warming, and such change is reflected in shifting weather patterns, which may affect bee forage.  Dr. Eric Mussen15 has noted that in some areas of the California foothills, previously common native plants no longer supply fall forage.

Biological plausibility:  The weather is well known to be a huge factor in colony survival, due to its indirect effect upon plant production of nectar and pollen, and the ability of bees to forage for them.  Temperature extremes (hot or cold) also stress colonies.  In addition, the weather appears to affect the levels of nosema and varroa.  Climate change affects plant communities, which may then have either positive or negative effects upon pollinator populations—a drier climate may eliminate bee forage, whereas a warming climate would expand favorable bee habitat northward.

Analysis: Dr. Gordon Wardell16 gave an excellent presentation shortly after the first reports of CCD, in which he used weather maps to show how unusual weather patterns appeared to correlate with subsequent increased colony mortality.  In certain areas, warm winter weather led to fruitless foraging and the using up of precious stores; in other areas, prolonged spring rains prevented necessary foraging for pollen.  On the other hand, this year’s warm January appeared to be very beneficial to bees.   

Verdict:  Weather and climate change may well be associated with pollinator decline in certain areas, directly affect colony survival, and could well be contributing factors to CCD.


Biological plausibility: The seasonal buildup of colonies, and their health over the rest of the season, is largely a function of the availability of good mixed forage, which is best provided by the diverse plant communities naturally present in areas with fertile soil and ample water.

Analysis:  Unfortunately, honey bees are in direct competition with humans for such habitats, as people convert fertile lands into cropland and towns.  Habitat loss directly and clearly affects many species, including honey bees.  This fact sets it apart from bee-specific factors such as varroa or beekeeper management practices.

It strikes me odd that when people think of the impact of farming upon bees that they focus upon pesticides.  In truth, the most destructive annihilator of natural ecosystems is the act of tillage—the mechanical preparation of land for the growing of crops (Fig. 4).

Figure 4.  Humans are the bees’ worst competitor, in that we destroy sustentative plant communities, and replace them with artificially-maintained monocultures that are virtual “bee deserts” for most or all of the year.  Note the absolute annihilation of the natural plant and animal communities in the tilled cropland behind the tractor (which takes place even in organic agriculture).

I keep bees on several organic farms, and they are lovely to look at.  But I choke when someone starts to wax poetic about organic agriculture being in harmony with nature.  Try to explain that illusionary harmony to the unfortunate former denizens of the diverse ecosystem that existed previous to the clearing and tillage of that fertile land!  In an acre of the former natural ecological community, there may have existed hundreds of species of plants and animals.  When converted to farmland, you may be able to count the number of reestablished species on your fingers and toes.  And those species of plants that are favorable to bees we generally refer to as weeds!

Habitat conversion to agriculture has changed the face of the most fertile lands on Earth.  Unfortunately for the honey bee, the flora of converted lands, rather than being replaced with bee-friendly plants, are largely planted to crops that offer scant nutrition for pollinators (Fig. 5).

Figure 5.  Land use in the United States.  The yellow pie slices indicate the proportion of each area allocated to cropland–the most biologically productive acreage.  Fully two thirds of that cropland is planted to only a handful of crops– corn, soy, hay, wheat, and cotton, which produce forage for bees for only brief periods, if ever.  Sources: USDA, Economic Research Service calculations based on data from Major Uses of Land in the United States, 2007; http://www.census.gov/compendia/statab/2012/tables/12s0858.pdf.

Only a tiny proportion of cropland actually requires pollination by bees, but even that fact hardly makes it good bee habitat.  Take almond orchards, for instance.  Over half of all managed hives in the country are transported to supply the pollination needs of this crop.  Why?  Because bees can’t survive on land converted to almond orchards when the trees are not in bloom!  The almond orchards represent over 1000 square miles of fertile California Central Valley land that becomes a “bee desert” for the 49 weeks of the year that the trees are not in bloom.

Farmers today are also moving away from their previous rotations of legume-rich (and bee friendly) pasture, upon which livestock were formerly put out to graze.  The new model is to keep beef and dairy cattle in feedlots, bringing their food—in the form of hay, silage, and corn—to them.  Compare the photos below that I took of two dairies in Indiana (Figs. 6 and 7).

Figure 6.  Dairies, such as this one in Indiana, traditionally allowed the cows to graze on legume-rich, bee friendly pasture, often rotated with corn or other crops.  Compare the bee forage potential of this ground to that of the dairy below

Figure 7.  At this “modern” dairy corn will be grown for silage, and brought to confined animals in the name of “efficiency.”  Note the distinct lack of bee forage in the foreground.

Newer beekeepers may not notice the effects of land use change due to the “shifting baseline syndrome”—in which we take for granted the current state of affairs, not knowing or remembering how it used to be.  In this matter, the old timers (once you get past the “the older I get, the better I was” part) are a valuable resource of historical knowledge to which we can compare the situation of today.  For example, I ran my hives to irrigated alfalfa for some 25 years, until the demand for high protein “dairy hay” caused the farmers to start cutting it at the slightest hint of bloom, greatly reducing the honey crop.  Even so, since summer bee pasture is at such a premium in the West, it got to the point that I could throw a rock and hit another beekeeper’s hives at any of my long-held locations.  So even though one would not see any particular change in land use in the area, those fields went from being my most productive locations to not being worth the effort to move bees to.

Verdict:    Although habitat conversion is not likely the proximate cause of colony mortality, colonies stressed by lack of good forage are less able to cope with parasites, pesticides, overcrowding, and other insults.  The conversion of meadows and other biologically productive lands to monocultures, the practice of fencepost-to-fencepost tillage and the elimination of hedgerows, “clean farming” requirements by food processors to remove extraneous animal habitat, the shift away from pasturing livestock, and the placing of fallow lands into cultivation, have all resulted in loss of bee forage.  Such habitat change is the scientific community’s number one suspect for pollinator decline in general.18  It doesn’t directly cause CCD, but colonies that suffered from CCD often came from areas of poor forage.  This physical elimination of food sources is likely a major cause in increased colony mortality worldwide, since malnourished colonies cannot thrive.

It will be difficult to reverse the trend, but land management practices can make farmland more pollinator friendly.  A number of organizations worldwide are promoting such practices, and public pressure will greatly help to promote the conservation of biodiversity.  See References for more information.

Summary So Far

None of the above discussion is revelatory, since this series is largely retrospective.  However, I felt it necessary to grant some myths a dignified death.  Next I’ll move onto some more contentious issues, such as agricultural exposure, GMO’s, and pesticides.


Thanks as ever to my friend and collaborator Peter Loring Borst for his untiring help in literature review.  And thanks to all the researchers who perform the tedious hard work of investigating colony mortality—it is only through their efforts and helpful correspondence that I could attempt my methodical analysis of this subject.

All would be academic if it were not for the smart and hardworking professional beekeepers who keep me informed.  My sons and I are continually learning how to better manage our own hives.  My articles are simply a reflection of what goes through my head each day as I try to digest all the scientific research, and then apply it in a practical manner to our own operation.

Most importantly, thanks for the appreciation and support that I get from beekeepers large and small worldwide.  We are all in this together.

Further Reading

OPERA (2011) Bee health in Europe – Facts and Figures http://www.pollinator.org/PDFs/OPERAReport.pdf  One of the best overall objective reports, from a European think tank called OPERA.  I highly recommend.

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.

Landscape enhancement for bees

Support beekeeper Kathy Kellison’s nonprofit Partners for Sustainable Pollination http://pfspbees.org/

Project Apism is working to get growers to plant bee forage in California http://projectapism.org/content/view/142/61/

Decourtye, A,  E Mader, N Desneux (2010) Landscape enhancement of floral resources for honey bees in agro-ecosystems.  Apidologie 41: 264–277.  Free download

Wrattena, SD, et al (2012) Pollinator habitat enhancement: Benefits to other ecosystem services.  Agriculture, Ecosystems and Environment 159: 112– 122.

An excellent download for increasing pollinator habitat on farmland can be found at ftp://ftp-fc.sc.egov.usda.gov/NH/WWW/New%20England_NRCS_Pollinator_Tech_Note_FINAL.pdf

And to their credit, Syngenta has a program! http://operationpollinator.com


1 http://scientificbeekeeping.com/sick-bees-part-18b-colony-collapse-revisited/

2 vanEngelsdorp, D, et al (2006) “Fall-Dwindle Disease”: Investigations into the causes of sudden and alarming colony losses experienced by beekeepers in the fall of 2006.  http://www.freshfromflorida.com/pi/plantinsp/apiary/fall_dwindle_report.pdf

3 McFrederick, Q.S., J.C. Kathilankal, and J.D. Fuentes (2008) Air pollution modifies floral scent trails. Atmospheric Environment 42:2336.


5 (Broken Link!) http://d1027732.mydomainwebhost.com/articles/articles/HAARP%20Jamming%20Bees%20= %20CCD.htm

6 http://www.haarp.alaska.edu/haarp/faq.html

7 Bianchi, C and A Meloni (n.d.) Terrestrial natural and man-made electromagnetic noise. http://www.progettomem.it/doc/MEM_Noise.pdf

8 Reviewed by Wajnberg, E, et al (2010) Magnetoreception in eusocial insects: an update. http://rsif.royalsocietypublishing.org/content/7/Suppl_2/S207.full.pdf+html?sid=4cea0921-cf0e-48df-80f8-fe2206db6976

9 Ferrari, T.E. & A.B. Cobb (2011) Correlations between geomagnetic storms and colony collapse disorder.  And Honey bees, magnetoreception and colony collapse disorder.  http://www.extension.org/pages/58650/proceedings-of-the-american-bee-research-conference-2011

10 Bailey, L (1969) The multiplication and spread of sacbrood virus of bees.  Ann. App. Biol. 63: 483-491.

11 Medrzycki, F, 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.

12 Wilson, WT, and DM Menapace (1979) Disappearing disease of honey bees: A survey of the United States.  ABJ March 1979: 184-186.

13 Dr. Jerry Bromenshenk, pers comm.

14 Oliver, R (2012) Sick Bees 18a—Colony Collapse Revisited http://scientificbeekeeping.com/sick-bees-part-18a-colony-collaspse-revisited/

15 Oliver, R (2010) Sick Bees – Part 2: A Model of Colony Collapse.  http://scientificbeekeeping.com/sick-bees-part-2-a-model-of-colony-collapse/

16 Dr. Eric Mussen, pers comm.

17 Presentation to Western Apicultural Society, Tucson, AZ, 2007.

18 Blacquière, T (2010) Care for bees: for many reasons and in many ways.  Proc. Neth. Entomol. Soc. Meet. 21: 35-41. http://edepot.wur.nl/185843

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Neonicotinoids: Trying To Make Sense of the Science – Part 2

First published in: American Bee Journal, September, 2012

Neonicotinoids: Trying to Make Sense of the Science

Part 2

Randy Oliver


First published in ABJ 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!

Why Neonicotinoids?

“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:

  1. They are far more toxic to insects than to mammals, making them much safer for humans.
  2. 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.
  3. 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[i], 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.

[i] Munkvold, G (2006) Seed Treatment http://www.extension.iastate.edu/Publications/CS16.pdf


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.

Sublethal 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.

Immune function:

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.

Native Pollinators

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

Water Pollution

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.

Landscape/Ornamental Uses

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.

Tree Injections

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.

Foliar Applications

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.

Simple Overuse

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 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.

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:

The Good

  • 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.

The Bad

  • 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.

The Ugly

  • 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

22 ibid

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.

29 http://www.sciencedaily.com/releases/2012/06/120605102846.htm)–it

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

35 http://www.panna.org/sites/default/files/BayerPullImidacloprid.pdf

36 Entine, op. cit.

37 http://www.cdpr.ca.gov/docs/pur/pur10rep/comrpt10.pdf

38 http://www.chcf.org/~/media/MEDIA%20LIBRARY%20Files/PDF/C/PDF%20CancerInCalifornia12.pdf

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

40 http://www.organicfarming101.com/organic-pesticides/

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

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Testing of Bee Feed Syrups for Neonicotinoid Residues

First published in: American Bee Journal, August, 2012

Eric Mussen1 and Randy Oliver2

The widespread adoption of the systemic neonicotinoid insecticides has led a number of beekeepers to question whether the commercially available corn, beet, or cane sugar syrups might be contaminated with residues of those insecticides.


Beekeepers often feed some form of sugar syrup to colonies for either buildup or winter stores.  The raw materials for sugar production come mainly from three cultivated crops–traditionally sugar cane or sugar beets, from which sucrose is extracted; or from corn (maize), from which high fructose corn syrup (HFCS) is produced.

In recent years, growers have widely adopted the practice of treating corn and sugar beet seed with systemic neonicotinoid insecticides [1, 2, 3], and clothianidin may be used on sugar cane in some areas [4].   The understanding that these insecticides are “systemic” (transported throughout the plant tissues) has led some beekeepers to question whether residues may make it into the final sugar product.

We submitted samples of the bee feed syrups offered by two major U.S. suppliers for independent testing.  Residues of neonicotinoid insecticides, as well as their degradation products, can be multiply-detected at as little as ppb levels by modern analytical instrumentation [5].

Materials and Methods

We solicited samples of syrups (Table 1) from Stuart Volby of Mann Lake Ltd. (Mann Lake, MN) and from Dadant (Chico, CA) branch manager John Gomez, which we reshipped for testing to Roger Simonds, Laboratory Manager of the USDA Agricultural Marketing Service lab.  We requested analyses for neonicotinoid insecticides and their principal degradates.

Supplier Manufacturer Syrup Type
Mann Lake Ltd. Cargill Type 55 HFCS

Type 42 HFCS

Liquid sucrose (beet)

Liquid sucrose (cane)

Dadant & Sons, Inc. (Chico branch) Archer Daniels Midland (ADM) California blend:

50% Type 42 HFCS

50% Liquid sucrose (cane)

Table 1. Bee feed syrups submitted for analysis.

1 Extension Apiculturist, University of California, Davis, CA 95616

2 Proprietor, Golden West Apiaries, Grass Valley, CA 95945


None of the tested samples contained detectable levels of either the neonicotinoid parent compounds or their degradates (Fig. 1).

Figure 1.  Typical test results.  The LOD is the “limit of detection,” i.e., the lowest concentration in parts per billion (ppb) that the instrument can detect.  The lab tested for both parent compounds (e.g., imidacloprid) as well as for the degradation products of the insecticides, which may also exhibit toxicity.


Although no residues were detected in the syrup samples submitted for testing, the possibility exists that there were residues below the limit of detection (1 ppb for most of the parent compounds).  However, levels below 1 ppb are generally accepted as being well below the no observable adverse effects concentration (NOAEC) [6].

These results are not surprising for HFCS, given that when the USDA tested 655 samples of corn grain in 2007 [7], no residues of neonicotinoid insecticides were detected.  Although the tolerance level for clothianidin in sugar beets is 20 ppb [8], there are often no detectable residues from beets in the field [9].  Similarly, there were no detectable residues in the sample of beet sugar that we submitted.

Although this was a very limited sampling, it gave no evidence that beekeepers need to be concerned about neonicotinoid insecticide residues in feed syrups from the major suppliers.


Thanks to the cooperation of Stuart Volby and John Gomez for supplying samples, Roger Simonds for expediting the analyses, and to the U.C. Davis Extension Apiculture Program for providing funds for sample analyses.


[1] Anon (2012) 2012 Corn Insect Control Recommendations. http://eppserver.ag.utk.edu/redbook/pdf/corninsects.pdf

[2] Valent (2011) Valent USA Announces NipsIt™ SUITE Sugar Beet Seed Treatment System. http://www.seedtoday.com/info/ST_articles.html?ID=113940

[3] Syngenta (2012) CRUISER FORCE sugar beet seed – the UK’s number one choice. http://www.syngenta-crop.co.uk/pdfs/products/CruiserSB_uk_technical_update.pdf#view=fit

[4] APVMA (2010) Trade Advice Notice on clothianidin in the product Sumitomo Shield systemic insecticide http://www.apvma.gov.au/registration/assessment/docs/tan_clothianidin_60689.pdf

[5] http://quechers.cvua-stuttgart.de/

[6] 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.

[7] USDA (2008) Pesticide Data Program Annual Summary, Calendar Year 2007, Appendix F Distribution of Residues by Pesticide in Corn Grain http://www.ams.usda.gov/AMSv1.0/getfile?dDocName=STELPRDC5074338

[8] Federal Register (2008) Clothianidin; Pesticide Tolerance.  https://www.federalregister.gov/articles/2008/02/06/E8-1784/clothianidin-pesticide-tolerance

[9] FAO (2005) Clothianidin, Table 103. http://www.fao.org/fileadmin/templates/agphome/documents/Pests_Pesticides/JMPR/Evaluation10/Chlotiahinidin.pdf