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The Future: Pesticides and Fungicides

Randy Oliver

Dave Hackenberg once quipped that “”Beekeepers have become the ugly stepchild of agriculture.” Despite their general disregard for us, perhaps there are lessons that we can learn from our agricultural stepparents.

Pest Resistance Management

Beekeepers worldwide, in their exuberant use of every miticide available, have accelerated the development of mites resistant to (surprise) every synthetic miticide to hit the market. Luckily, U.S. beekeepers have been thrown a lifeline at the last moment in the form of the latest “silver bullet”– Hivastan®. However, lest I sound critical, I’m not blaming them—varroa has been the worst thing ever to hit beekeepers—it just won’t go away! To their credit, every commercial beekeeper I’ve spoken to is concerned about the sublethal effects of miticides upon his bees, and most have experimented with alternative treatments.

The problem of varroa resistance to targeted poisons is hardly unique to beekeepers—this is a common phenomenon in modern agriculture. Allow me to quote from the pesticide industry’s own pest resistance management website (IRAC 2009):

“General insecticide use is no longer the answer to pest control. Insects have developed widespread, insecticide-defeating resistance to many traditional treatments, and the industry may not have enough resources to continually develop and supply the market with new products precisely when needed to replace old ones. Growers with resistance problems do not have enough time to wait for new chemistry. It is imperative that the effectiveness of available insecticides be conserved by growers through adoption of these management principles. By working together, insecticide resistance can be managed!” [emphasis mine]

Folks, the above statement comes from the very companies that sell pesticides! They are telling us that we’d better learn to use Pesticide Resistance Management (PRM) for our own bee pests—mites, bacteria, and fungi. PRM strategy uses three main tactics of pest control–cultural, biological, and as a last resort, chemical. In the case of varroa management, “cultural” would include such techniques as the making of splits and other biotechnical methods. “Biological” would involve mite-resistant bees or biocontrols such as fungi or viruses specific to mites (unfortunately, we don’t yet have the latter at our disposal). We should no longer consider miticides to be the first mode of defense.

A key aspect of pesticide resistance management to extend the effective life of a pesticide is the concept of “refuge strategy”—that is, to make sure that a large “refuge” of untreated pests remains outside of the managed fields. These untreated (and therefore susceptible) pests are expected to move in after treatment, and to outbreed the few resistant pests that survive the treatment, thereby delaying the development of pesticide resistance.

Unfortunately, the refuge strategy is problematic with varroa for two main reasons: (1) varroa normally mate brother to sister, so resistance alleles are difficult to breed out (shy of completely exterminating any colonies with resistant mites), and (2) because any miticide with a long residual life in the combs will maintain a constant selective pressure against “wild type” susceptible mites.

These facts suggest that long-term control of varroa with miticides will become more and more difficult with time (in case you hadn’t noticed).

The “New” Antibiotic

Since I’m on the subject of resistance management, let’s talk about tylosin. This antibiotic was registered for use against active cases of AFB. It was registered only after the AFB bacterium evolved resistance to the long-successful antibiotic Terramycin (oxytetracycline, or OTC). OTC has the desirable characteristic of degrading fairly rapidly in moist environments (as in a bee hive). Therefore, it fit the bill of allowing refuges of susceptible bacteria (and beneficial competing bacteria) to survive.

Tylosin, on the other hand has a very long life in the hive—on the order of several months or years (Kochansky 2004). That is why it is currently such an effective antibiotic against AFB—it just keeps killing and killing the bacteria. This persistence was noted in the process of its registration for bee hive use, so the label specifically prohibits its use as a prophylactic measure, or its application in sugar syrup.

Of course, many commercial beekeepers now routinely (and illegally, at least in my state) feed tylosin in sugar syrup as a prophylactic measure against AFB! It is a “box movers’” dream—no need to inspect for foulbrood, nor loss of AFB-tainted equipment—just treat ‘em all with tylosin. I strongly question this practice! We do not know the long-term effects of a persistent antibiotic upon symbiotic honey bee gut flora or those in the bee bread. Of even more concern is the imprudence of such practice—tylosin is an incredibly effective tool for the control of AFB. The routine use of it will predictably soon render it ineffective as tylosin-resistant bacteria evolve. Those misusing the product will ruin it for the rest of us! This is not a matter of “laughing with the sinners or crying with the saints”—it is rather a shortsighted folly.

First-World agriculture has reveled in the achievements of the Green Revolution and factory farms, the success of which unfortunately depend upon energy-gulping fertilizer and transportation, massive pesticide and herbicide use, dousing animals in “Concentrated Animal Feeding Operations” with antibiotics, and government subsidies. We’ve become infatuated with the beauty of our weapons* against pests, weeds, and diseases. Although this system has been highly effective for the short term, there are good arguments that it is unsustainable in the long run.

*Apologies to Leonard Cohen

Commercial beekeeping has become a microcosm of the larger agricultural system. Let me note that I make my living as part of that system—renting bees for pollination, and selling honey by the drum. I enjoy as well plentiful, and what appears to be “cheap,” food (if one ignores the hidden costs). Be assured that I’m not criticizing the system nor the farmers or beekeepers who feed the nation. Neither am I disparaging the use of miticides and antibiotics—they are valuable and necessary tools. However, I feel that it may be wise to pay attention to the evolution of the larger system, as beekeeping will likely reflect similar changes and challenges.

Big Agriculture is moving toward fewer (and safer) pesticides and antibiotics, more biotechnical methods of pest control, such as crop rotation and interplanting, better breeding for pest and disease resistance, and better animal nutrition. The parallels with beekeeping are hard to ignore.

New Pesticides

The market for agricultural pesticides is huge, so there is a constantly evolving arsenal of new pest control products—this year look for imaginative new names like Belay, Endigo, Zeal, Movento, Synapse, and Coragen (all ®) (Roberson 2009). The good news is that the newer classes of insecticides are generally designed to be more environmentally friendly, which is good news for bees.

However, with the release of each new pesticide, beekeepers wonder if there will be unforeseen ill effects upon their bees. When colonies die for no apparent reason, it is easy to blame said losses on the unfamiliar new product.

This has certainly been the case for the neonicotinoids. The good news is that the systemic neonics are replacing the nasty organochlorines and organophosphates (WHO Class 1–“extremely hazardous”), and can be used in much smaller amounts, since they are applied directly to the seed prior to planting, rather than spread or sprayed over the soil or crops.

However, many beekeepers in Europe, and some in the U.S., feel strongly that neonics can cause detrimental effects to their colonies. Numerous field trials (by Bayer, government labs, and independent researchers) generally fail to support this supposition (the continuing reports in the press are generally recycled old research). There is no doubt that some bees are harmed by some neonic applications, but in general, monitored test colonies appear to thrive when placed adjacent to neonic-treated crops in which the chemical has been properly applied. Indeed, I’ve spoken to some large commercial beekeepers who profess their love the neonics, as their use has reduced the typical historical kills by the older generation of pesticides.

This is certainly not the final word on the neonics—I’m sure that the labels will need to be modified as we find specific cases where their use (such as in potatoes followed by clover, in melons, when applied by chemigation, etc.) appears to be harming bees and other nontarget organisms.

Guttation “water”

O.K., by the time you read this article, you may have heard the buzz about “guttation droplets” and neonicotinoids in young corn (maize) plants. Dr. Vincenzo Girolami in Italy released a video last year of bees dying rapidly after drinking droplets of sap exuded by clothianidin-treated corn seedlings. The twitching deaths were gruesome to watch, and fired up justifiable emotional outrage in beekeepers. Had the culprit for colony losses finally been pegged?

Well, there’s a bit more to the story. In the first place, the knowledge about systemic pesticides in guttation fluid (a natural phenomenon in young plants in the grass family) was well known. The whole reason for seed treatment is to make the sap of seedlings toxic to root- and leaf-eating insects. Then as the plant matures, the concentration of pesticide naturally decreases, plus guttation normally ceases.

Beekeepers have complained about bee losses at the time of sunflower or corn flowering—but this occurs months after guttation in the seedlings. But some beekeepers also complained about losses just after planting. These losses could be explained by contaminated dust from the seeds as they are planted (as in the well-publicized clothianidin kill in Germany last year, in which the pesticide was not glued properly to the seed). Or, as Dr. Girolami (2009) points out in his recent paper, perhaps bees might be poisoned by drinking guttation droplets. His laboratory studies indicate that the droplets can indeed be toxic, but alas, he did not perform any “real-life” field tests, and stated “it is still not possible to draw a judgment on a possible correlation between neonicotinoid translocation into guttation drops and CCD.”

Luckily, others have performed such field tests. I’ve been able to preview Bayer-funded studies that were performed in corn fields this spring at six sites in Austria and France, under different climatic conditions (some specifically chosen to have access to water restricted, and little alternative attractive flora), and involving 38 fields and about 100 colonies. Guttation on the corn seedlings was commonly present during foraging hours.

The results were that bees were observed foraging only at the field margins, and “only very occasionally” were individual bees observed exhibiting symptoms of intoxication. I’ve looked at the graphs of the numbers of dead bees caught in hive traps or fallen on linen sheets placed before the hives—there didn’t appear to be any significant effect of seed treatment compared to control colonies on untreated fields.

The researchers found that the placement of gravel-filled watering trays decreased bee foraging for guttation water. However, colony development for three months appeared to be identical (and normal) whether alternate water was provided or not.

Aha, you say, that research was funded by Bayer! I also found that the Swiss government independently performed their own tests (BLW 2008), in which they found that clothianidin indeed occurred at toxic levels in the droplets for about a month after sowing. Again, the toxic droplets appeared to be repellent to bees. The independent Swiss researchers found no mortality due to clothianidin of bees in colonies placed next to the fields during and after sowing, and observed no deterioration of the health of the colonies. They did suggest that it would be good beekeeping practice to provide clean water if such was not naturally available.

The above findings will likely apply to the U.S. However, we plant corn in huge expanses, and I wouldn’t be the least surprised if bees in such areas might be poisoned if drought occurs during the first month of seedling growth, should no clean alternative water sources be available. Again, please note that potential poisoning from guttation droplets would be an entirely different phenomenon from poisoning from the much later tasseling of corn.

In any case, I hope that the neonicotinoid question is resolved soon. Meanwhile, there is another class of plant protection products that keeps coming up on my radar…


Although beekeepers have long cursed pesticides, fungicides have generally been assumed to be safe for bees. We’ve recently learned otherwise. Some fungicides are demonstrably toxic to bee larvae. Exposure of larvae to pollen containing Captan®, Ziram®, or iprodione led to 100 percent mortality (Alarcón 2009).

Fungicides may also have synergistic effects when combined with other pesticides, or miticides applied by the beekeeper, making the either more toxic to the bees. This is a problem that we experience when our colonies are pollinating almond orchards—where fungicides are often sprayed on the bloom. Many almond pollinators (myself included) have had serious issues after certain fungicides (e.g., Rovral® or Pristine®) were sprayed, sometimes in the short term, sometimes killing brood weeks later (Mussen 2008). This is a serious concern to those producing queens from colonies returning from almond pollination.

A scary thing about fungicide contamination is that there may be a delayed effect—one may not notice problems until the bees dig back into stored pollen months after exposure! VanEngelsdorp (2009) coined the term “entombed pollen” to describe brick-red beebread sealed by the bees with a black capping, and often associated with the fungicide chlorothalonil (Bravo®). The authors state: “These results provide compelling evidence that entombed pollen indicates exposure to a risk factor that is detrimental to honey bee colony survival.” However, they did not find it to be directly responsible for either significant brood mortality or CCD.

Entombed pollen

Entombed pollen from the author’s apiary. Note the scattered entombed cells in the broodnest.

Cell opened with a hive tool

A cell opened with the hive tool (this pollen is not quite as red as that described by vanEngelsdorp. I have not tested it for fungicides.

In a recent series in this Journal, Dr. Gloria DeGrandi-Hoffman, et al (2009) reviewed the literature on beneficial microbes in bee hives. These microbes are mainly bacteria and fungi. Bees gather pollen, add nectar, saliva, and microbe inoculant from their mouths, and pack it into cells to undergo a lactic acid fermentation, similar to the making of silage, sauerkraut, or yogurt. After the initial fermentation, which preserves the beebread with acid, beneficial fungi then continue to digest the pollen, apparently making it more nutritious to the bees.

So let’s say that you were about to make cheese out of milk at home. Unless you take special care to make sure that the culture is properly inoculated with beneficial bacteria and fungi, you will end up with a putrid, and possibly toxic, product (due to the bacterial and fungal toxins produced by unwanted microbes).

When bees ferment pollen into beebread, they count on the right microbes to do the job. Honey bees have a long evolutionary involvement with beneficial symbiotic bacteria and fungi, and several of them appear to be associated with the health and nutrition of colonies. When a fungicide (or possibly an antibiotic) is inadvertently added to the pollen, we simply do not know whether the “normal” fermentation process will take place, or whether the chemicals will allow toxin-producing microbes to thrive. The entombment of pollen may simply be the way that bees deal with beebread “gone bad” so that the nurse bees don’t suffer from “food poisoning.”

Now I’ve saved what most interests me for last. Honey bees require sterols as essential dietary nutrients (meaning that they can’t create them themselves, similar to vitamins). The critical bee sterol is 24-methylenecholesterol (I’ll abbreviate it as 24-mCh). Luckily, this is often the main sterol found in pollen (Svoboda 1983). There is also a sterol precursor to 24-mCh called sitosterol, but Herbert ( 1980), in feeding trials of synthetic diets, found that bees were apparently unable to convert sitosterol (or other sterols) to 24-mCh.

Without 24-mCh in the diet, nurse bees apparently “steal” it from their own body reserves to produce the jelly which they then feed to the queen and larvae. Herbert (1980) found that in diets lacking 24-mCh, broodrearing is restricted, and drops off precipitously after two brood cycles (although they can use plain cholesterol in the short term).

Note that this drop off after two brood cycles is typical of pollen “substitutes,” including that used in a recent greenhouse trial at the Tucson lab. The colonies in that trial quickly recovered when they were given a small amount of beebread scraped from combs of free-flying colonies. No one has determined what the critical ingredient supplied by the beebread was.

Note also that due to bee colony population dynamics, a major drop in brood rearing wouldn’t be noticed by the beekeeper (unless he’s inspecting the broodnest) until about six weeks later, when the missing brood would have become foragers. A colony can quickly recover the field force if there is a lot of sealed brood, but not if there was a break in brood rearing several weeks previously.

Now here’s the part that catches my attention. Loper (1980) found that almond pollen, hand brushed from the blossoms, contains both sitosterol and 24-mCh, but that in the same pollen, trapped from bees’ legs in pollen traps that were emptied hourly, the sitosterol content dropped sharply (154 to 38 mg/kg), whereas the 24-mCh content rose substantially (428 to 544 mg/kg)!

So here’s my question: If bees are unable to convert dietary sitosterol into 24-mCh in cage trials lasting weeks, how the heck do they manage to do it in an hour in the pollen loads on their legs?

The answer may come from Gilliam (1997): “Our studies of floral and corbicular [collected on bees’ legs] pollen …demonstrated that pollen from a flower changes microbiologically and biochemically as soon as the honey bee collects it.” She found that bacteria and yeasts were very quickly replaced by molds (fungi). Certain fungi (such as Mortierella) are notable for producing 24-mCh (although Gilliam did not identify this genus in bees).

So, questions that I have for researchers are, (1) what is the mechanism for the conversion of sterols in the corbicular pollen, (2) do agricultural fungicides stop the process, and (3) since 24-mCh is critical in the royal jelly to produce queens, how are fungicides used in almonds affecting the queens produced afterwards? I’m very curious as to how fungicides, even those that aren’t overtly toxic to bees, are affecting the nutrition, health, and development of queens in our colonies.

Wrap Up

Modern agriculture has become heavily dependent upon pesticide use. Unfortunately, the pests are catching up. All forms of agriculture, including beekeeping, will be forced to move to smarter management, with fewer, and less hazardous, pest control products. Proactive beekeepers are currently shifting to such practices as IPM and natural treatments.

The incredibly effective antibiotic tylosin is unfortunately being misused, which will likely lead to resistant AFB bacteria, and possibly to unexpected problems with colony biotic balance.

Agriculture is generally moving toward more environmentally-friendly pesticides. The neonicotinoids appear to be one of these. However, some beekeepers feel that the neonics are causing serious problems. There is currently a lack of supporting scientific evidence in most cases (with noted exceptions), but research continues.

Fungicides, which have been generally considered to be harmless to bees, are being found to be anything but! Researchers are reinvigorating investigation of the roles that microflora play in colony health and nutrition, and the effects that fungicides and antibiotics may have when the microfloral “balance” is disrupted.


As always, I am deeply indebted to my collaborator Peter Loring Borst, without whom I could not conduct the research necessary to document these articles.


Alarcón, R and G DeGrandi-Hoffman (2009) Fungicides can reduce, hinder pollination potential of honey bees. Western Farm Press March 7, 2009.

BLW (2008) Bienen Monitoring in der Schweiz (available as pdf by Googling the title)

DeGrandi-Hoffman, G, et al (2009) The importance of microbes in nutrition and health of honey bee colonies. ABJ 149(6, 7, and 8).

Gilliam, M (1997) Identification and roles of non-pathogenic microflora associated with honey bees. FEMS Microbiology Letters 155: 1-10.

Girolami, V, et al (2009) Translocation of Neonicotinoid Insecticides From Coated Seeds to Seedling Guttation Drops: A Novel Way of Intoxication for Bees. J. Econ. Entomology 102(5): 1808-1815.

Herbert, EW Jr, et al (1980) Sterol utilization in honey bees fed a synthetic diet: effects on brood rearing. J. Insect Physiol. 26 287-289.

IRAC (2009) IRM The Facts. http://www.irac-online.org

Kochansky, J (2004) Degradation of tylosin residues in honey. JAR 43(2): 65–68.

Loper, GM, et al (1980) Biochemistry and microbiology of bee-collected almond (Prunus dulcis) pollen and bee bread. Apidologie 11(1): 63-73.

Mussen, E (2008) Fungicides toxic to bees? Apiculture Newsletter Nov/Dec 2008.

Roberson, R (2009) Vegetable insecticide arsenal expanding. Southeast Farm Press. March 26, 2009. http://southeastfarmpress.com/vegetables-tobacco/vegetable-production-0326/

Svoboda, J, et al (1983) Comparison of sterols of pollens, honeybee workers, and prepupae from field sites. Arch. Insect Biochem and Physiology 1983, pp. 25-31.

VanEngelsdorp, D, et al (2009) “Entombed Pollen”: A new condition in honey bee colonies associated with increased risk of colony mortality. Journal of Invertebrate Pathology 101: 147–149.

Category: Pesticide Issues