Photo of Doug at workDr. Doug Yanega is the Senior Museum Scientist at the University of California, Riverside, and an acting Commissioner of the International Commission on Zoological Nomenclature. His undergraduate and graduate degrees were under the tutelage of George Eickwort (Cornell University) and Charles D. Michener (University of Kansas), respectively, two of the world’s foremost bee authorities. Dr. Yanega has a broad background, and many of his publications deal with the natural history, pollination ecology, and taxonomy of bees.  

Doug published this on Facebook, and I wanted this to get a broader audience, so invited him here for a guest post.

Back in 2006, a team of bee researchers put out a report regarding a phenomenon affecting honey bees commonly called “Fall Dwindle Disease”, in which they decided that this name was misleading, and suggested a new name for this syndrome – the name they suggested as a replacement was “Colony Collapse Disorder” (CCD). It’s worth reading it (at, not only to get some perspective on things, but because – amazingly enough – even though this is the document that first used and defined the term, virtually no one who has published on CCD has ever cited this document… not even the people who wrote it.

To anyone acquainted with scientific research or journalism, the idea of using a term that was recently defined and NOT citing (or at least reading) the original definition goes completely against what anyone would consider to be proper research. Basically, not doing one’s homework.  Yet, this is precisely what has happened with this document. It can’t even be retrieved from the website on which it originally appeared, but if you’ve read it, you’re now better educated on the history of CCD than many of the scientists and journalists and beekeepers who have published on CCD in the past 7 years.

Why do I stress this so much? It’s quite straightforward: most of the scientists and journalists and beekeepers who have published on CCD in the past 7 years have either stated or implied that CCD is something that had never existed prior to 2006. And yet, the original paper defining CCD spelled out that it was an existing condition that they were simply coining a new name for, in the hope that the new name would be less misleading. Oh, the irony. Even more baffling is that it’s not like this information was totally lost or hidden – it’s been visible in the Wikipedia article (, with a citation, for all this time, so anyone in the world who simply Googled “Colony Collapse Disorder” could find this reference, since the WikiP article is the first link shown.

It gets even better: in both 2007 and 2009 another paper pointed out that there were at least 18 historical episodes of similar large-scale losses of honey bees dating back to 1869, at least several of which had symptoms similar enough that they cannot be ruled out as being the exact same ailment. Yet, how often have you seen any of the scientists and journalists and beekeepers acknowledging that any theories about the cause of CCD need to accommodate the evidence for similar bee crashes that pre-date neonicotinoid pesticides, high-fructose corn syrup (HFCS), migratory beekeeping, cell phones, genetically modified crops, or any of the other human-made “causes” that have been run up the proverbial flagpole?

Once again, there are an awful lot of people who are not doing their homework (admittedly, it is a big body of literature, but we’re talking about papers *central* to the issue). That 2009 paper also included the following statement, and I’ll quote it because it’s so important:

“Of the more than 200 variables we quantified in this study, 61 were found with enough frequency to permit meaningful comparisons between populations. None of these measures on its own could distinguish CCD from control colonies.”

Of the 61 variables quantified (including adult bee physiology, pathogen loads, and pesticide levels), no single factor was found with enough consistency to suggest one causal agent. Bees in CCD colonies had higher pathogen loads and were co-infected with more pathogens than control populations, suggesting either greater pathogen exposure or reduced defenses in CCD bees.” Yes, this study did actually look for connections to pesticides, Varroa mites, beekeeping practices, and other things, and no such connections held up to scientific scrutiny.

Here’s the thing about this: if you look at a lot of what you see these days, be it in the scientific literature or in the media, people are running around looking for things that kill honey bees, and when they find something that does so, they often make this GARGANTUAN leap to claim that since X kills honey bees, and since CCD kills honey bees, then X must cause CCD. Logic fail, anyone?

Does anyone seriously dispute that neonicotinoid pesticides are capable of killing honey bees? No. Does anyone dispute that Varroa mites can kill honey bees? No. Does anyone dispute that Nosema (a microsporidian fungus) kills honey bees? No. Sure, there are some ridiculous claims that no one in the scientific community WOULD stand behind (e.g., cell phones or chemtrails), but, by and large, most of the things that any one team of researchers or another puts forward as THE cause of CCD are things that, in and of themselves, are perfectly plausible as significant sources of bee mortality. But that DOES NOT mean that any of them is causally linked to CCD.

beesWhy not? Go back and read the papers I linked; (1) there’s a list of symptoms that characterize CCD, which are not universally present in these various “smoking gun” studies, and (2) they’re talking about something dating back to the 1800s. Did they have neonicotinoids or HFCS back in 1869? In 1969? If not, then those studies fail to do what ANY genuinely scientific hypothesis needs to do: offer an explanation consistent with ALL of the evidence (Occam’s Razor, anyone?).

In effect, what is happening is that researchers are studying one possible factor at a time, and seeing only a tiny part of the whole picture. It’s the parable of “The Blind Men and the Elephant”, where each one describes only that which is in their range of perception, instead of examining ALL of the evidence (including reading ALL of the literature) and coming up with a theory which explains all of it. We’ve got a pile of incomplete theories all competing for the media spotlight, each with its own proponents, and sometimes with a non-scientific agenda.

They’re using a single name, CCD, but may be using it to describe a pile of entirely different ailments. Even worse, there are fringe theories and fuzzy thinking and red herrings abounding, and the public can get easily confused – for example, not realizing that there are some 20,000 species of bees in the world, and only ONE of them is affected by CCD (yes, some other species of bees are dying off, but it’s a different set of things that are responsible).

What may well be a complete and sensible theory is out there, however, and it is referred to above, and hinted at elsewhere (mostly by folks who were involved with the original CCD work) though it has not yet been fully explored or elucidated to everyone’s satisfaction; I’ll highlight again the phrase “reduced defenses in CCD bees.” Way back when this whole thing came to everyone’s attention, Diana Cox-Foster and the other researchers made observations suggesting that CCD might be the result of bees with a compromised immune system.

For those of us who remember when AIDS first came to public attention, there are some striking parallels, and it wouldn’t be all that surprising to ultimately find out that CCD is something that works in much the same way. That is, if you have bees with a compromised immune system, then they could become vulnerable in such a way that a whole range of things that normally might NOT be lethal, are suddenly lethal.

Honey bees are exposed to all sorts of pathogens, chemicals (including not just pesticides, but HFCS, and mite-killing agents used by beekeepers), and other stress-inducing factors on a routine basis, and the levels of exposure to these factors are normally not enough to kill off healthy colonies. But if they are NOT actually healthy, and instead are immuno-compromised, then those same levels of exposure might trigger something catastrophic. Recall that the HIV virus does not itself kill people; the causes of death in AIDS victims are a variety of other diseases that would ordinarily have been fought off by the immune system. If no one had ever discovered the HIV virus, we would be seeing evidence of people dying from all sorts of other things, and likely pointing blame at each factor independently, while missing that there was something connecting them all.

Sound familiar? There is (and has been, all along) evidence that CCD is contagious, yet how often is that discussed? That evidence needs to be accounted for, along with all of the other patterns we’re seeing. There are people looking for viruses and other pathogens that could be at the root of CCD, and some tantalizing results have appeared – though such announcements haven’t been definitive, and (perhaps more importantly) haven’t gotten more attention than the incomplete (but more sensational) theories have gotten.

Not only would it be nice if more of the people who reviewed papers trying to link various things to CCD asked pointed questions like “How well can this theory explain similar bee dieoffs in the previous century?” or “How well can this theory explain the patterns of contagious pathology seen in CCD-affected apiaries?”, but it would also be far more professional and appropriate to do so, given that the scientific method is not based on cherry-picking of evidence, or sensationalism. I’m prepared to find out that I’m wrong, but I want to see some real evidence, for which there is an unambiguous and coherent explanation.

A reasonable question you could ask is “Well, even if we accept the idea that there’s an underlying pathogen, why is this all happening now, and to this degree, and over this length of time? If this is the same disease we’ve seen outbreaks of spanning several decades, why does this seem so much worse this time around?” I can offer two observations: (1) the way the modern news media network seeks out and reports on stories is VERY different, as is the level of environmental concern among the general public, and even if the exact same thing DID happen in the 1960s, it would not have made international news headlines; and (2) there are, quite simply, MORE potentially harmful things that honey bees are exposed to now than they were in the past – meaning that if the diefoffs are more widespread, more severe, and more prolonged, it should not be all that surprising.

A reasonable course of action, to my mind, is acknowledging that we aren’t likely to find that any man-made factors are the true cause of CCD, devoting energy to looking for contagious pathogenic agents, and taking a closer look at genetic diversity in honey bees themselves (e.g., are there strains that are resistant to CCD?), while at the same time working towards reducing the exposure and impacts of man-made factors that are capable of harming bees (but without BLAMING them in the process, or overreacting). Does every potentially harmful thing need to be banned outright, or just used more prudently? Is there a level of exposure to neonicotinoids that is not harmful? Can beekeepers simply use less HFCS, or less or different acaricides, or make other changes to their practices that will result in fewer bee deaths? Answers may not be simple, nor black-and-white, but real science rarely is.

bees[P.S. from Doug – the day after I first posted this on Facebook, the USDA released this PDF, in which the pre-2006 existence of CCD is once again not mentioned, despite having nearly all of the original co-authors among the 175 conference attendees. This is remarkable, and makes me wonder if people are intentionally trying to distance themselves from the original definition of CCD. It’s almost like someone publishing a paper coining the term “lung cancer” and then other people coming along and using that same term for every other known form of cancer, to the point where the original concept has been forgotten entirely.

The report states explicitly that honey bees are suffering from multiple different things, which I can’t dispute, and “CCD” is (at this point) being used as a blanket term for things that may have genuinely separate causes – but this is a practice I don’t like. If we KNOW there are multiple causes and multiple effects, then it confuses the issue to lump them all under a single name, and you’re going to have serious problems coming to solid conclusions about treatment, prevention, and epidemiology, not to mention communicating with the public. I’ll give just one example to make my point: several studies show that parasitic Varroa mites are strongly linked to CCD, and several other perfectly valid studies show that CCD can kill bees that have no Varroa mites. The net effect is that all we can say is “Beekeepers should prevent their bees from getting Varroa mites” – which is something everyone has known for decades. But if it turns out that some of the chemicals used to kill Varroa mites also weaken the bees, then by failing to tease apart the different contributing factors, we’ve made a vague recommendation that might have negative consequences. I’m not saying teasing these things apart is easy – experimental research on honey bee pathology is incredibly difficult, because it’s nearly impossible to get large numbers of replicates, or establish proper controls for all variables – but I still think that we should TRY to keep the different causes separate, and maybe we can some day figure out what the original CCD was.

Other things you might want to read about pesticides and bees:

Posted by Gwen Pearson

Entomologist. Educator. Writer. NERD.


  1. Thanks for this! It is important that this kind of commentary be heard in this soundbite-addicted world.

  2. Yes, a lot of people didn’t want to got to Facebook to read the original.

  3. Why does the “original” definition of CCD matter? As long as the new studies are clear about the phenomena that the researchers are studying and the scope of the study, I don’t see a problem with using CCD as a shorthand for the not well understood phenomena. I haven’t looked back at the old 1800s and 1960s information, but is there enough information about the problems then to tell what was going on? My guess is that there isn’t, and speculating about what was going on then isn’t going to be productive.

  4. Glenn Scriven May 3, 2013 at 2:49 pm

    Several years ago, bees were falling out of the air and landing on my driveway. They were severely disabled, unable to fly or walk. They then died. This behavior lasted for several years and then stopped. Bees, in my area, are now healthy and abundant. The disability seems to have coincided with the appearance of Africanized bees in the area. Just wondering if the Africanized bees may have brought in a pathogen that affected susceptible domestic bees. Over time the domestic bees have developed resistance or tolerance to the new pathogen. Movement of bee colonies around the country could have easily spread the new pathogen to areas where African bees are absent. Just a thought.
    I am a retired Entomologist and former beekeeper.

  5. This is an excellent, very readable article, which I could readily understand. (And I’m an engineer, not a biologist !) Thank you for bringing it to us.
    The simplistic view presented by the mainstream media can be very misleading, but that’s all that most of us see and base our judgements upon. But then the media are only interested in engaging an audience, not in pursuing truth. For them, science is just another form of sport, and it doesn’t matter which side wins as long as there is someone to watch the game.

  6. Refreshing attitude and article, but “the scientific method is not based on cherry-picking of evidence, or sensationalism” seems a bit retro. Most of the ‘science’ I see being hyped by the media (including university ‘news’ pages and press releases) is very much cherry-picked for sensationalism.

  7. Interesting. I agree with this part – “If we KNOW there are multiple causes and multiple effects, then it confuses the issue to lump them all under a single name, and you’re going to have serious problems coming to solid conclusions about treatment, prevention, and epidemiology, not to mention communicating with the public.” I think sometimes beekeepers may be using the blanket term ‘CCD’ to explain their hive losses, when actually if they delved a bit deeper other explanations could be found – for instance colonies have been known to abscond due to high varroa infestations.

    I notice that many of the beekeepers interviewed in the original CCD article at which you linked to were regularly reusing old brood comb from dead colonies and giving the bees antibiotics – not great beekeeping practices! With the bees having the stress of being moved around all the time on top of that, it’s hardly surprising they were losing colonies.

  8. Thanks for sharing this. I am especially interested in the historical evidence presented. But I’m not sure how you make the rather large leap to this conclusion: “A reasonable course of action, to my mind, is acknowledging that we aren’t likely to find that any man-made factors are the true cause of CCD . . . ” Humans have been managing/manipulating bees in increasingly aggressive ways over the last several hundred years. When I think of all the human interventions that are likely to cause stress to bee populations from the modest (provoking swarming to split hives, harvesting honey) to the more aggressive (shipping them across the nation and across climate zones, artificially importing and inseminating queens, spraying chemicals in hives to kill varroa mites, exposing them to a range of chemical pesticides, including neonic, saturating almond groves with so many bees that the work of each bee is made extraordinarily difficult because of all the competition for blooms) I reach the opposite conclusion–that it is LIKELY man-made factors are contributing to or causing the die-offs. Our industrial ag system places bee colonies under extraordinary stress. A virus could certainly be the cause–and would help explain how die-offs spread to feral colonies. But even in this case, it is reasonable to hypothesize that any such virus emerged and found the perfect environment for spreading in the industrial bee-keeping environment. I am inclined to see the causes of this latest crises–which was not a simple one-off collapse, but a more sustained one–as a result of multiple stressors, most related directly or indirectly to human management of bee colonies. And neonics are likely one of those. I also think no one should be surprised that the scientists who will be the last to recognize the harmful effects of neonics will be those who work directly or indirectly for the neonic industry.

  9. […] about the decline of bees and colony collapse disorder?  Read this –> an important message (thanks Bug Girl for posting […]

  10. Nice post.

    How often is the term “disorder” used in bee agriculture or entomology?

    Going with the idea that there is a thing we see (a syndrome would normally be the word used in ecology and also medicine) that we can describe reasonably well (so different instances of the syndrome can be collected together and pondered upon), is CCD a “syndrome?” It seems to me that this is in part what you are saying (though that conflicts with the insistence that the “thing” we are observing should be recognized as having been a thing with a set of (unknown) causes for long periods of time.

    In other words, I think it is a good idea, as you seem to be suggesting here, that CCD (though maybe it should have been called Colony Collapse Syndrome) be viewed as a set, though maybe a polythetic or fuzzy set, of similar outcomes for which we don’t presume a specific cause or set of causes.

    A bee colony is a complex thing and many different things have to work. The honey bees we are talking about, as far as I know, are semi domesticated or domesticated. (as a person who’s studied domestication I’m reluctant to use a very specific term there) which means that a) the colonies may exist outside of the “primordial” habitat (though we compensate for that) and b) there may be genetic issues. (Also, I suppose, this affects the pathogen problem as well; in the wild a particular species may actually go locally extinct, which has the incidental but useful effect that zoonotic pathogens can’t take hold or are reset.) Tiven these factors, it may actually be surprising that this whole domesticated honey be agriculture works as well as it does.

    One more question: Is there any research at all that addresses the question of this Disorder/Syndrome occurring in wild bees in their natural range? I know of now such work but maybe you’ve heard of something.

  11. […] We recently discussed news from the EU on banning neonicotinoid pesticides in order to stem the so called Colony Collapse Disorder (CCD) among honey bees. Bug Girl has an important guest post on the phenomenon of CCD by bee expert Doug Yanega. This is a must read not only for those interested in bees and CCD, but skepticism and science reporting in general, as Yanega places the current discussion in a strong historical context and provides a valuable critique of much of the reporting on CCD. Go read Honey bees, CCD, and the Elephant in the Room. […]

  12. Re: Greg Laden post.
    There is some evidence that domestic bees in some areas of eastern Europe are free of CCD symptom’s. Pers. com. Dr. Mike Parella, UC Davis.

  13. it’s Monsantos’ fault.

  14. chrismcmullen May 6, 2013 at 8:59 pm

    Exactly. Look for a patented bee..the savior of the world. Then you will have your explanation. Own and control everything. Food,knowledge,wealth. Everything.

  15. good for you! best writing I’ve seen on the topic. First time reader (via Boingboing) and I’ll be back. :)

  16. War to find THE cause of cancer and cure it, anyone?

  17. Jim The Pollen Wrangler May 6, 2013 at 10:53 pm

    Doug’s heart is in the right place, but he is (still) wasting his time, keeping a death-grip on his Wikipedia page on CCD, and unhappy that he will be unable to “complete” it with a profound conclusion. Everyone else has moved on and quietly admitted that the poster-children for CCD were each candidates for the title “Typhoid Mary of Beekeeping”, with massive over-use of off-label miticides and out-of-control chronic pest and disease problems in their operations, and that the early cases of CCD were most likely self-inflicted gunshot wounds to the foot of those beekeepers. “PPB” (Piss-Poor Beekeeping) was more of a factor in “CCD” than anything else. Other beekeepers joined in, mis-diagnosing more common problems as “CCD” in order to cash in on the expected government support that never came. Meanwhile, the number of pathogens from the other side of the planet suddenly appearing in the USA and Europe increased every year.

    The reason why certain papers are not cited, and the term “CCD” is avoided as much as possible is that no one really cares what CCD specifically is or was any more, as it turned out that “CCD” was a collection of pathogens we already knew about, except for IAPV (“Ian’s (Lipkin) Annoying Pet Virus”) which turned out to both mostly harmless in the USA strain, and widespread in the USA as far back as the mid-1980s, according to Jeff Pettis’ (of USDA) latest talks circa 2013.

    CCD also was embarrassing, as it attracted too much heat, and not enough light. It meant “Cash Cow Discovery” for too many groups who raised millions on the backs of bees and beekeepers, but gave none of that money to bee research. It far better for researchers to get down to work, and address the tangible problems at hand, the exotic invasive pathogens and pests that have come to our shores from the other side of the planet with all that “world trade” everyone thought was such a neat idea.

    What’s happened to beekeeping? The same exact “disorder” that has affected all of agriculture, planet wide. Un-Inspected and un-regulated trade in goods that should contain no living hitchhikers result in far too much spread of invasive species. Ask any farmer or beekeeper, the costs ducked by the free traders have been externalized onto all of agriculture, and the result is more expensive food, laced with ever-more complex pesticides.

    If anyone wanted to solve the problems, they could ask their representatives to fund the research with more than the current tiny crumbs allocated. There are both USDA and University efforts, even a multi-institution project or two, but the funding is very limited, which slows the work to a crawl, with grant writing and begging taking more time than the science.

    And the bees still die. Before varroa came to the USA, we beekeepers had “too many splits”, more hives than we knew what to do with. Now, we have 30% to 50% losses every year, even when using best practices and diligent monitoring.

    So, the price of honey is eternal vigilance.
    Worrying about semantics, labels, and names is mere etymology, and we need some serious entomology.

  18. Thanks for posting this here. It needed visibility beyond that of Facebook.
    I have been trying to call attention to two other related matters. One is the exaggerated claims heard everywhere; for instance bees approaching extinction or last year losses worse than ever before. The reality is quite different as this survey shows:
    The other is the unwillingness to get to the root of the problem, agricultural practices that include monoculture fields and huge numbers of bees trucked for pollination. These two practices stress bees and predispose them to illness:

  19. 3rd Scientist From The Left May 14, 2013 at 8:30 am

    Doug Yanega? Of ENTOMO-L@Listserv.UoGuelph.CA ? The esteemed EDITOR of the Wiki-page on CCD?

    When I see a critique of others from someone who has not published a thing himself since 2008, I read it with care.
    When the critique is from someone who has never published anything on Apis mellifera, (honey bees), I read it again.
    When the critique is published in the well-respected refereed science journal FACEBOOK, I read it yet again.

    When the critique, published on FACEBOOK is of peer-reviewed research published in legit journals that invite and publish letters and short notes, and even review papers, where the work of others is compared and contrasted, well I sit up and pay close attention!

    Doug is a valid justification for all those “Far Side” cartoons that feature entomologists.
    Doug should back to his air-conditioned bug collection, and leave the research of practical value to those willing to do the work.

  20. The different responses here are exactly why I wanted to have Doug’s rant published in a more accessible place than Facebook. I don’t agree with everything that Doug’s said, but I do think it’s an important part of the discussion about CCD, and bee health.

    My personal opinions are laid out in the 4 “other things you might want to read” posts linked here.

Comments are closed.