Worldwide Status and Distribution
Ceranae vs. apis
What if You’re Dealing with N. apis?
In my last article, I described how to quickly sample for nosema. So what do the spore counts actually mean as far as colony health is concerned? I wrote an article a little over two years ago with the tongue in cheek title “Nosema ceranae: Kiss of Death, or Much Ado about Nothing.” Well, N. ceranae is still an enigma, but it appears that the answer lies somewhere in between.
Dr. Mariano Higes (2005, 2006) was the first to raise the flag to alert beekeepers worldwide that a new species of nosema had invaded Europe, and appeared to be the cause of the unusual colony collapses that plagued Spain (a major beekeeping country) in 2003 and 2004. Then in 2007, just as Colony Collapse Disorder was rampaging through our own bee operations, we found out that Nosema ceranae had somehow spread throughout the U.S. right under our eyes!
Drs. Diana Cox-Foster and Ian Lipkin (2007) then published a paper suggesting that a newly-described virus was involved in CCD, but later research indicated that IAPV wasn’t the only culprit, leaving N. ceranae as a leading suspect.
Shortly afterward, Higes (2008) described in great detail the progression of N. ceranae infection (in his Spanish apiaries) through four stages: Asymptomatic, Replacement, False Recovery, and finally the dreaded Depopulation. The logic, the numbers, and the devastating final result were all clear and compelling. The specter of N. ceranae ravaging our hives resulted in unnerved beekeepers boosting the sales of fumagillin to the point that supplies ran short.
I had never previously worried about nosema, but I pulled out a microscope and found out that N. ceranae was indeed widespread in my operation. I ran trials, and found out that the danged parasite could flourish despite being drowned in fumagillin (Oliver 2008a), but more surprisingly, that colonies here at Comedy of Errors Apiaries thrived despite exhibiting spore counts in the millions. To try to reconcile the differences between the very different outcomes of N. ceranae infection in my operation with those reported for Spain, I began an ongoing correspondence with Dr. Higes, which continues to this day.
To be frank, some other Spanish researchers dispute Higes’ conclusions (debate leads to better science), so I have often questioned and challenged him on details of methodology and interpretation, which he and his team of collaborators have generally clarified with additional research. In this series of articles I will be citing a number of the Higes team’s papers, since they have clearly led the pack in N. ceranae research, meticulously investigating nearly every aspect of this pathogen’s effects upon bees.
I’ve previously written at length about N. ceranae in my “Nosema Twins” series (all available at ScientificBeekeeping.com), but feel that there has been so much recent research completed that it would benefit the reader for me to write a digest of our current state of knowledge. I’ve scoured the literature for every relevant research paper (including a number still in press), and have discussed as well current findings with many of the world’s nosema researchers. I wish that at this time I could say that I have the answers to all your questions about Nosema ceranae, but unfortunately, in many aspects this parasite still remains an enigma.
Worldwide Status and Distribution
Nosema ceranae has now spread into the European honey bee populations of most areas of the world, roughly concurrent with the spread of varroa (and its altering of virus dynamics), which greatly confuses analysis of the effect of these two novel parasites upon bee health. It is difficult to tell in which countries N. ceranae has already reached equilibrium, and in which it is still invading.
Since the first invasive wave of a novel parasite into naïve hosts is generally that most damaging, it would be helpful to know when ceranae actually arrived in various countries. For example, we know from analysis of archived bee samples that N. ceranae has been present on the East Coast for at least two decades (Chen 2008). Unfortunately, any initial effects of its invasion may have been masked by our focus upon the massive impact of the arrival of varroa at about the same time.
Since no one was looking for N. ceranae in the U.S. until 2007, we obviously didn’t start studying it until long after it was well established and likely homogenized throughout the bee population via migratory beekeeping practices. And it is also likely that by the time we started studying the impact of N. ceranae upon the health of colonies, natural selection may have already weeded out the bees least tolerant of the emergent pathogen.
In Europe, however, N. ceranae only recently invaded bee populations already suffering from varroa and viruses, miticide failure and comb contamination, extreme weather events, plus changes in agricultural practices and pesticide use—the combination of which likely factor into colony losses in that region.
In a fresh study (Botías 2011), the Higes team analyzed archived Spanish honey samples (frozen) and adult bee samples (in alcohol) dating back to 1998. They found that N. ceranae first appeared beginning in 2000 and increased in prevalence through 2009 (the latest samples analyzed), concurrent with a decrease in the prevalence of N. apis. It is noteworthy that Spain concurrently suffered from devastating drought during much of that period, which led to serious colony stress.
N. ceranae is still in the process of extending its range worldwide, and appears to be most successful in warmer climates. It is of interest that in varroa-free Australia, its invasion does not appear to be causing significant colony losses. Interestingly, although it is well-established in Canada, it is not yet common in some northern European countries, but this may be due to restrictions upon bee imports (Fries 2010).
N. ceranae is widely distributed throughout the U.S., but surprisingly, there were great differences in the percent of colonies infected in a recent state-by-state survey (Fig. 1).
Figure 1. Prevalence (percent of samples infected) of N. ceranae in various states as determined by PCR analysis (more sensitive than spore counts) of aggregate samples collected from 8 randomly selected colonies per apiary, 4 apiaries per state. Note that in some states over 70% of samples were infected! From Rennich, K, et al (2011) 2010-2011 National Honey Bee Pests and Diseases Survey Report.
Ceranae vs. apis
In a widely cited paper by Martín-Hernández (2007), her arresting graph of nosema positive samples over time clearly shows a definite shift over the period from 1999 to 2005—there initially were only spikes in spring and fall (ostensibly from apis), transitioning to nearly 100% of samples being positive every month of the year (due to ceranae). Of note is that her data has an inherent bias, in that the samples were voluntarily sent to the lab by beekeepers for diagnosis of problems, suggesting that the data may reflect the change in nosema loads in sick hives. Also of note, is that despite this graph being widely cited, it is often misunderstood—it did not plot spore levels, but rather only the yes/no detection of nosema spores.
What the graph did strongly indicate was that N. ceranae rapidly and thoroughly invaded Spain over a period of only a few years! This initial finding has now been confirmed by Botías (2011). Likely, a similar phenomenon occurred in the U.S., since Chen (2008) found N. ceranae to already be widespread in archived U.S. bee samples dating back to 1995.
The general trend appears to be that N. ceranae now predominates in warmer countries, whereas N. apis is better adapted to colder areas. It has been often stated that N. ceranae has displaced N. apis, but more careful analysis suggests that that may not actually be the case!
When Dr. Robb Cramer asked me in 2007 to send him infected bees so that he could culture pure N. ceranae, he found that the samples often contained some N. apis as a “contaminant.” In Dr. Diana Cox-Foster’s (2007) analysis of CCD colonies, they also found both species of nosema. Later studies by Bourgeois (2010) and Runckel (2011) of commercial operations in the U.S. also found N. apis, but in far fewer hives than its cousin, only in spring and/or fall, and notably, at much lower spore levels than N. ceranae.
The differences between the detectability of the two nosema species (N. apis typically produces much lower spore counts and is generally only seen in spring and fall) may lead “to an increased chance of detecting N. ceranae over N. apis, which could have biased the impression that N. apis has been displaced” (Higes 2010).
So, has ceranae actually displaced apis, or have we merely been overlooking its cousin? In order to answer that question, Dr. Raquel Martín-Hernández (2011) carefully analyzed over 2000 bee samples from all across Spain. She found ceranae and apis coexisting throughout country, with ceranae clearly predominant (in roughly 40% of hives), apis hanging in there (in up to 15%), and occasional mixed infections (below 7%). She also found that infection by ceranae was favored in hotter areas of the country, whereas apis succeeded better where winters are colder.
I’m seeing similar indications from other countries (e.g., Gisder 2010), which are appearing to confirm that apis is the more cold-adapted species. As far as seasonality, Martín-Hernández found apis only in the spring and fall, whereas ceranae could be found all year, and notably, once ceranae infects a colony, it almost always persists (detectable with PCR, even if not obvious via spore counts).
Practical note: these studies indicate that N. ceranae remains present as an infection in a colony throughout the year, even if it is not detectable by microscopy. But we don’t know whether these inapparent infections affect colony health.
I found one last study to be of special interest: Dr. Judy Chen (2009) looked at nosema invasion from the other direction—in a turn of the tables, N. apis appears to have been introduced from the Western honey bee (Apis mellifera) into the Eastern honey bee (Apis cerana) in Asia, and is now an emergent parasite in that species, which had historically been infected only by N. ceranae! She analyzed bee samples from China, Taiwan, and Japan. Her findings:
“N. apis was detected in 31% of examined bees and N. ceranae was detected in 71% of examined bees and that the copy number of N. ceranae was 100-fold higher than that of N. apis in co-infected bees, showing that N. ceranae is the more abundant of two Nosema species in the Eastern honey bees.”
This study suggests that N. apis can not only hold its own against N. ceranae, but can actually invade into ceranae’s turf! Interestingly, in the Eastern honey bee, despite its long coevolution with N. ceranae, ceranae still produces higher spore counts than its invading cousin.
This brings up the question of what happens when bees are infected simultaneously by both species of nosema? Dr. Zachary Huang (pers comm) found that in both cage trials and field observations that longevity was substantially shorter for coinfected bees as opposed to those infected by either species of nosema alone (unpublished data).
Note that in Cox-Foster’s (2007) CCD study that they found “a trend for increased CCD risk in samples positive for N. apis” (100% of CCD colonies tested positive for ceranae and 90% for apis, but remember that apis is easy to miss when samples consist of house bees). As Jim Fischer noted in a post to Bee-L, “What was striking was that every hive showing CCD symptoms tested positive for BOTH Nosema apis and Nosema ceranae, and this correlation was better than the correlation between CCD and IAPV that was the focus of the paper.”
These findings leave me very curious about the impact of coinfection by two nosema species upon colony health!
Spore counts of N. ceranae generally reach a peak in May, then drop spontaneously during summer, and may spike sporadically in fall and winter. But there is more to the picture than this. Dr. Ingemar Fries (2010), who has studied nosema for decades, explains thusly:
“The typical pattern for N. apis infections in temperate climates is low prevalence or hardly detectable levels during the summer with a small peak in the fall. During the winter there is a slight increased prevalence with a large peak in the spring before the winter bees are replaced by young bees… The pattern is similar both in the southern and northern hemisphere… Unfortunately, very few data exist for N. apis on the seasonal prevalence from tropical or subtropical conditions. The only published year round sampling under conditions where bees could fly all year round, revealed detectable levels of N. apis with no seasonal pattern of prevalence.”
Along that line, Dr. Denis Anderson in Australia (pers comm) tells me that, “there are also many unseasonal occurrences of N. apis — I get many samples sent in in the mid summer here that are loaded with N. apis.” This could well be happening in the U.S., where, as far as I can tell, there have been few studies on N. apis in warmer areas, other than the fact that it was commonly found in package bees produced in the southern states.
Practical application: we need to learn more about the prevalence and seasonality of N. apis in the warmer parts of our country!
I’ve now seen data and presentations on N. ceranae seasonal prevalence from researchers from all over the world. Since a picture is worth a thousand words, I’ve summarized them in a crude graph below (Fig. 2).
Figure 2. A generic graph of typical N. ceranae spore counts over the course of the year in my operation. Important note: Counts of house bees would follow the same trend, but at much lower levels. The late-season spikes are often sporadic flare ups that spontaneously “go away.”
Practical application: It is not unusual to see high nosema spore counts in April and May. Counts will typically drop in summer whether you treat or not. I’ll cover treatments in a subsequent article.
But new technology is showing something surprising about nosema sampling—that spore counts do not necessarily reflect degree of actual nosema infection (Meana 2010)! Look at the following graph (Fig. 3), from a recent nationwide study of pathogens in U.S. bees—instead of measuring spore counts, the blue bars indicate the percentage of colonies infected by N. ceranae as determined by DNA analysis (PCR).
Figure 3. The blue bars indicate the percentage prevalence of N. ceranae in sampled colonies (e.g., 0.7 = present in 70% of hives). Note that even though spore counts suggest that N. ceranae disappears for much of the year (previous graph), a substantial proportion of colonies actually remain infected to some degree by the parasite. Also note how closely the coinfection with another intestinal parasite (the presumably opportunistic trypanosomes) tracks nosema infection. No one is sure whether there is a causal relationship, or whether the simple explanation is that both parasites flourish in stressed bees. Graph from Rennich, K, et al (2011) 2010-2011 National Honey Bee Pests and Diseases Survey Report.
As opposed to the above graph, Runckel (2011) also measured the amount of nosema DNA in samples, which presumably correlates with the intensity of the infection. They found high levels of N. ceranae transcripts in midsummer, at a time when spore counts are generally quite low (Fig. 5)! Their data indicated that N. apis was only present in spring and fall (which does correspond to spore counts). Go figure!
So what’s up with high levels of N. ceranae DNA transcripts without correspondingly high spore counts? No one to my knowledge has answered that important question. What we do know is that N. ceranae can exist in the vegetative stage for a while before it produces spores (Martín-Hernández 2009). But we’re not clear on to what extent N. ceranae produces “autoinfective spores,” as opposed to the “environmental” spores that are discharged into the gut contents (Cali 1999), and whether such autoinfective spores show up under microscopy. What is clear, however, is that N. ceranae appears to be able to reproduce within a bee without producing spores that are observable by microscopy.
Practical note: although N. ceranae spore counts may disappear in summer, DNA analysis indicates that the bees may still be infected. This is something of a mystery, as the bee population turns over rapidly during the summer, suggesting that N. ceranae is somehow infecting new bees without spores being evident!
So the next question is, is an infection by N. ceranae more pathogenic than one by N. apis? Although some initial cage trials indicated extreme virulence for the new nosema, trials in which bees were allowed to feed upon natural pollen generally found that both species affect bee longevity about the same (Forsgren 2010, Porrini 2011, Huang pers comm) despite the fact that spore levels get much higher with N. ceranae.
Take home: We clearly still have lots to learn about N. ceranae! It does not appear to cause rapid death of well-fed bees. The inapparent summer infections are puzzling.
So what’s the cause of the seasonality of nosema spore counts? With N. apis it is presumed to be due to the requisites of transmission via dysentery by infected bees in the hive during the winter and colony nutritional stress, and limited by its sensitivity to high temperature. Martín-Hernández (2009, 2010) demonstrated that N. apis can only grow in a narrow range of temperature (about 33°C). N. ceranae, on the other hand, grows readily over a range from 25°C to 37°C. However, N. ceranae spores are surprisingly susceptible to chilling (Fries 2010), which may limit their infectivity at lower temperatures.
Studies from a number of countries coinfected with both of the nosema cousins suggest that N. apis will continue to be the historical problem during winter and spring, with typical fall and spring spikes, whereas ceranae will be more prevalent in warmer climes, present throughout much of the year, spiking in late spring (perhaps tracking pollen flows), and then again sporadically in fall through winter.
Take home: if Nosema apis was a problem in your area prior to the invasion of N. ceranae, it may still contribute to colony health issues during the fall and spring!
It would sure be easier if there were a simple sampling protocol that everyone could follow, and if there were clear treatment (or worry) thresholds based upon nosema spore counts, as there are for varroa (Fig. 4), but alas, I’m sorry to say that there aren’t.
Figure 4. Average varroa infestation rates from 2700 colonies in 13 states (many of which received mite treatments). Sampling for varroa infestation level is relatively straightforward and simple to interpret. Typical treatment thresholds are below 5 mites per 100 bees. Graph from Rennich, K, et al (2011) 2010-2011 National Honey Bee Pests and Diseases Survey Report.
Unlike sampling for varroa, which are easily seen with the naked eye, sampling for nosema requires either a microscope or laboratory apparatus that can perform PCR. However, a number of researchers (Meana 2010, Bourgeouis 2010, Traver 2010) have demonstrated that spore counts alone do not give an accurate picture of the actual degree of infection. Unfortunately, as far as assessment methods available to Joe Beekeeper, spore counts will have to suffice as a surrogate measure of the actual degree of infection (Fig 5).
Figure 5. Average nosema spore counts from the same 2700 hives. Note the typical huge spike in spore counts (predominantly from N. ceranae) in spring, and then again lesser spikes in fall and winter. Important note: these spore counts were from samples of bees from brood frames—counts from entrance bees would likely be several times higher (compare to Figure 2). Graph from Rennich, K, et al (2011) 2010-2011 National Honey Bee Pests and Diseases Survey Report.
That said, let’s return to sampling for a bit. If you want to find spores, then sample older bees, such as foragers at the entrance (Meana 2010)—spore counts will typically be about 10 times higher in older bees, since it takes a while for the infection to build up in a bee (Smart 2011). He found that in infected colonies with a background spore count of 0.5-1M in bees from under the inner cover, almost no bees younger than 12 days old contained spores (at least detectable by microscopy).
This is not at all surprising, since El-Shemy (1989) found the same to be true for N. apis—spore counts were an order of magnitude higher in bees from the entrance. Indeed, he suggested that it was best to sample exiting bees at the entrance, since returning bees have likely defecated. The magnitude of the spore counts from an infected colony generally increases in samples (in order from lowest to highest), of bees from the broodnest, outer areas of the cluster, entrance bees, exiting foragers, returning foragers.
Both El-Shemy and Higes (2008) found that the best indicator of degree of infection was to squash bees from an entrance sample one at a time in order to determine the percentage of bees infected. My own sampling of sick colonies supports this recommendation. But in reality, few of us have time to squash dozens of bees one at a time for each sample—so I won’t even suggest that you go there!
The next best method may be to do a spore count for a pooled sample of 50 bees from the entrance (but don’t forget that even one or two highly-infected bees can greatly skew the count). In practice, however, it is often danged difficult and time consuming to collect 50 entrance bees, even if you use a special vacuum (Oliver 2008b), especially in cool weather or from sick colonies with few foragers.
For this reason, many researchers simply take standardized samples of bees from under the cover, or from an outside comb. There is support for this, as Gajda (2009) found that although spore counts were much higher in entrance bees, the relative proportion of infected bees was similar in samples taken from an outside comb.
Practical application: If you want to find out whether N. ceranae is present to any significant extent in your operation, sample bees from the entrance. If you want to know if the infection is serious, sample house bees from under the cover.
If you are curious as to whether you have gotten old or young bees in your sample, here is an easy general observation that I’ve made: since only nurse bees normally eat pollen, they are the only ones that will have it in their guts (duh). But my point is, that this is really easy to use that pollen as an indicator of bee age if you use the ziplock bag method for processing samples (see my previous article, and Fig. 6).
Figure 6. How to tell if your sample contains young or old bees. (Left photo) when you crush samples of nurse bees in a ziplock bag, and then mush them in water, the fluid will typically turn opaque yellow (since the guts of nurse bees are full of pollen). (Right photo) on the other hand, the fluid from the guts of entrance bees will typically be a tan/gray color (since foragers and guards don’t eat pollen).
What if You’re Dealing with N. apis?
Oh, that it were only so simple as dealing with only one nosema, but the previously cited studies suggest that many of us actually may still have N. apis popping up in fall and early spring. To make things even harder, spore counts of N. apis, on a per bee, or per pooled sample basis, are generally only a fraction (about 1/10th, as best I can tell from previous studies) of what we see with N. ceranae. But it also appears that an infection by N. apis at that low level can be as serious as an infection by N. ceranae at a much higher spore count!
Important note: Martín-Hernández (2011) easily found N. ceranae in samples of either foragers or house bees, whereas she only found N. apis in foragers and drones. So if N. apis is your concern, then you should take entrance samples! N. apis infection may be serious at a much lower spore level!
The other consideration is that you must put any spore count into the context of time of year, the climate that your bees are in, the nutritional status of the colonies, and especially the load of other pathogens. I will discuss these points in the next article.
In cold climates, nosema management may have other considerations. Hedtke (2011) performed a detailed 6-year study of 220 hives in Germany, and (surprisingly) found that “No statistical relation between N. ceranae detection in autumn and the following spring could be demonstrated, meaning that colonies found to be infected in autumn did not necessarily still carry a detectable infection in spring, and colonies which developed a detectable infection over winter had not been detectably infected in autumn.” So much for careful sampling!
Heck, I’d be crazy to stick my neck out and give any recommendations! So let’s look at what sort of nosema levels are involved in crashing colonies. The CCD colonies analyzed by Cox-Foster (2007) had mean spore counts in the range of tens to hundreds of millions from broodnest samples! Is it really any surprise that those colonies collapsed? The house bees in Higes’ (2008) winter-collapsing colonies hit 20M before they went down (field bees hit 50M), but those that collapsed in summer only hit 3M.
But note that in the U.S. survey graph above, that 2M was the average spore count across the U.S. in April and May of this year, yet I’m not hearing of massive colony collapses, despite very poor conditions in many states.
In my own California foothill operation (we get snow during the winter, and move to almonds in February), it is not unusual to see entrance spore counts in May in the millions or tens of millions, but they generally drop during summer, provided that colonies are not stressed by other factors. Entrance counts during summer and fall are typically in the zero to 5M range (25 spores per field of view if you follow the protocol in my previous article—I’ll call these FOV counts (Oliver 2008c)). I have not looked at near as many samples of house bees, but counts are generally zero to a fraction of a million, even in colonies running at 10M at the entrance.
I am by no means suggesting that you follow my lead, but I simply no longer worry about high spore counts in spring, as they generally spontaneously drop later in the season, and I haven’t experienced winter losses associated with N. ceranae (unless I’ve intentionally inoculated the hives with viruses). However, I do keep my mite levels down, and feed pollen supplement to maintain good nutrition if necessary. And I monitor nosema levels throughout the year so that I don’t get blindsided!
I’ve never treated for nosema (except in experiments), yet have not experienced colony collapses since 2006. But I’m not saying that you have no reason for concern—I will be writing about a trial in which I did compare survival of treated vs. untreated colonies that had virus issues, and fumagillin appeared to help.
I’d be concerned if counts for house bees got above 5 per FOV at any time, although I know several large commercial beekeepers who routinely ignore such counts with no dire consequences so far. I just checked a number of samples of house bees today (late October), and they ran from zero to 2 spores per FOV, despite there often being counts of 100-200 per FOV of entrance samples this spring.
In some operations where N. ceranae apparently got out of hand, treatment and comb sterilization seemed to help. However, in other operations with sky-high spore counts in spring, lack of treatment did not result in any noticeable problems. Due to these huge discrepancies, it is confoundingly difficult to come up with recommendations. However, the more beekeepers who start tracking spore counts, the more we will learn about appropriate treatment decisions.
If you are in an area with a long, cold winter which keeps the bees confined, you may be dealing with Nosema apis, for which the economic threshold of 1M (5 per FOV) for house bees has been well established.
Practical application: since spore counts for N. apis generally only reach levels about 1/10th of those for N. ceranae, you’d be wise to ask your local university determine which nosema species you’re dealing with, since it follows that the economic threshold for treatment for N. apis may be far less than that for N. ceranae.
I will continue this review of N. ceranae in the next issue, including treatments, and its relationship to colony mortality and honey production.
Thanks to you, my readers! It just occurred to me that I’ve recently passed the 5 year mark in writing for ABJ, and it’s been one wild ride! If I had any idea what I was getting into, I would probably have chickened out. But your feedback and appreciation keep me going—my motivation is simply the gratification that I get from sharing what I’ve learned with other beekeepers. Your donations also allow me to perform the sort of quick and dirty research necessary to answer burning questions. I am constantly on the learning curve, and greatly appreciate hearing information that is relevant to better bee management—feel free to contact me (no beginners questions please) firstname.lastname@example.org.
As always, Peter Loring Borst has helped me greatly with research. I thank Dr. Mariano Higes for his patience in discussing his research. Dr. Steve Pernal and Ingemar Fries have been gracious with their time. I also thank all the other nosema researchers who have patiently answered my questions.
Botías, C, et al (2011) The growing prevalence of Nosema ceranae in honey bees in Spain, an emerging problem for the last decade. Research in Veterinary Science (in press).
Bourgeois, AL (2010) Genetic detection and quantification of Nosema apis and N. ceranae in the honey bee. Journal of Invertebrate Pathology 103: 53–58.
Cali, A and PM Takvorian (1999) Developmental morphology and life cycles of the microsporidia. P. 121. in Wittner, M and LM Weiss, eds. The Microsporidia and Microsporidiosis.,American Society for Microbiology.
Chen, Y.P., et al (2008). Nosema ceranae is a long-present and widespread microsporidian infection of the European honeybee (Apis mellifera) in the United States. J Invertebr Pathol 582 97: 186–188.
Chen, YP, et al (2009) Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. Journal of Invertebrate Pathology 101 (2009) 204–209.
Cox-Foster, DL, et al. (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318(5848): 283-287.
El-Shemy, A.A.M. and RS Pickard (1989) Nosema apis Zander infection levels in honeybees of known age. J. Apic. Res. 28 (2), 101–106.
Forsgren, E, and I Fries (2010) Comparative virulence of Nosema ceranae and Nosema apis in individual European honey bees. Veterinary Parasitology 170: 212–217.
Fries, I (2010) Nosema ceranae in European honey bees (Apis mellifera). Journal of Invertebrate Pathology 103: S73–S79. https://bienenkunde.uni-hohenheim.de/uploads/media/Nosema_ceranae_in_European_honey_bees__Fries.PDF
Gajda, A (2009) The size of bee sample for investigation of Nosema sp. infection level in honey bee colony. http://www.coloss.org/publications/Nosema-Workshop-Proceedings.pdf
Gisder S, et al. (2010) Five-year cohort study of Nosema spp. in Germany: does climate shape virulence and assertiveness of Nosema ceranae? Appl Environ Microbiol 76: 3032–3038.
Hedtke, K, et al (2011) Evidence for emerging parasites and pathogens influencing outbreaks of stress-related diseases like chalkbrood. Journal of Invertebrate Pathology 108:167–173.
Higes, M (2010) Nosema ceranae in Europe: an emergent type C nosemosis. Apidologie 14(3): 375 – 392.
Higes, M., et al (2005) El síndrome de despoblamiento de las colmenas en España. Consideraciones sobre su origen. Vida Apícola 133: 15–21.
Higes M, et al (2006) Nosema ceranae, a new microsporidian parasite in honeybees in Europe, Invertebr Pathol. 92(2):93-5.
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First published in: ABJ October 2012
Beekeeper Management Practices
Ozone and Air Pollution
HAARP (The High Frequency Active Auroral Research Program)
Cell Phones/Electromagnetic Radiation (EMR)
WEATHER AND CLIMATE CHANGE
Summary So Far
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).
- Beekeeper management practices
- Environmental factors
- Chemical exposure
- 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:
- The nutritional stress due to inadequate forage as mentioned above.
- The behavioral stress caused by the robbing pressure between overstocked colonies.
- 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!
OZONE AND AIR POLLUTION
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 (THE HIGH FREQUENCY ACTIVE AURORAL RESEARCH PROGRAM)
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.
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
WEATHER AND CLIMATE CHANGE
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;
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.
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
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 http://d1027732.mydomainwebhost.com/articles/articles/HAARP%20Jamming%20Bees%20= %20CCD.htm
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
First published in: ABJ November 2012
Back to the Suspects for CCD
A Pesticide-Free Control Group
“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.
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 , 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 .
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
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:
- I mentioned a couple of months ago Dr. Erickson’s demonstration that colonies exposed to permethrin-sprayed corn died during the following winter.
- The Coordinated Action Project’s data for 2009-2012  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  the Journal of Apicultural Research (2011) Issue 50(1): 1-10 by the permission of the Editors.
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).
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” .
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 . 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 .
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 , 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.
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 [9 ]. Map from USDA [10 ].
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.
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 . 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.
 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
 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.
 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.
 Höcherl, N, et al (2012) Evaluation of the nutritive value of maize for honey bees. Journal of Insect Physiology 58(2): 278–285.
 Thompson, HM (2012) Interaction between pesticides and other factors in effects on bees. http://www.efsa.europa.eu/en/supporting/doc/340e.pdf
 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.
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
Direct Effects of Roundup Use
Indirect Effects of Roundup Use
The Future of Roundup
Looking Ahead: The Chemical Treadmill & Pest Resistance
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?
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 .
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 . 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” . 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  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 .
Jeffrey Smith, in his book “Seeds of Deception”  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 . 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.
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 . 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 , . 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 :
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” , 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 . A mere six companies collectively control around half of the proprietary seed market, and three quarters of the global agrochemical market . 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 , 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 , 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).
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?
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. . 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” . 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!) . And some plants naturally contain symbiotic bacteria and fungi in their tissues, which produce non-plant chemicals . 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 , , . 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 . 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 .
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:
- No till farming does in fact require less labor and reduces soil compaction.
- Farmers get greater production due to less competition from weeds.
- No till also reduces the amount of petrochemical fuel involved in tillage.
- No till greatly reduces soil erosion, which has long been a major environmental concern.
- 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 , (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 , .
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  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 !
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 . 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.
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)!
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.
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
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 , and hope that farmers return to alternative methods of weed control . 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.
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 . 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  (there is a hodge-podge of international patent laws in this regard ).
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 .
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 , 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 . 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” . I will be the first to say that Smith’s anti-GMO claims  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 . 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:
- 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” .
- 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 .
- 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 .
- Novel genetic markers can be patented, and a licensing fee can be charged, despite the fact that they are not GM!
- From a consumer standpoint, advanced breeding techniques can result in cheaper and more nutritious food, and less environmental impact from farming.
- 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” . 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!
- 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.
- Those that speak of applying the “precautionary principle” should read Jon Entine’s trenchant analysis of the fallacy of overapplication of that principle . In truth, our regulators (EPA and FDA) vigorously apply the precautionary principle in the form “reasonable certainty of no harm.”
- 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.
- 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 . 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!
- 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.
- 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.
- 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 .
- 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.
- 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 . 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.
- Monsanto invests 44% of its R&D on conventional (as opposed to GM breeding).
- 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 . 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 ].
- 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 . 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.
- 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! . Luckily, this does not appear to be occurring yet with maize in Oaxaca , 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.
- 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.
- 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 . It’s interesting to read the history of “Golden Rice”  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. https://mail.google.com/mail/?ui=2&ik=c920d227a0&view=lg&msg=13c06f358e4dea8c
“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.
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” .
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 , 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 .
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!
 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/
 For example: Antoniou, M, et al (2012) GMO myths and truths.
 Chiba S, et al. (2011) Widespread endogenization of genome sequences of non-retroviral RNA viruses into plant genomes. PLoS Pathog 7(7): e1002146.
 Domingo, JL and JG Bordonaba (2011) A literature review on the safety assessment of genetically modified plants. Environment International 37: 734–742.
 Key (2008) op. cit.
 Smith, JM (2003) Seeds of Deception. Yes! Books
 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;
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,
 Methods for genetic control of plant pest infestation and compositions thereof
 2007 figures http://www.census.gov/compendia/statab/2012/tables/12s0835.pdf
 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
 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.
 History of Bt http://www.bt.ucsd.edu/bt_history.html
Mode of action http://www.bt.ucsd.edu/how_bt_work.html
 Gold 2002 Misconceptions about the causes of cancer http://potency.berkeley.edu/pdfs/Gold_Misconceptions.pdf A “MUST READ”!
 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.
 Duan JJ, et al (2008) A meta-analysis of effects of Bt crops on honey bees (Hymenoptera: Apidae). PLoS ONE 3(1): e1415.
 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
 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]
 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.
 Benbrook, CM (2012) op. cit.
 Reviewed in http://www.sourcewatch.org/index.php/Glyphosate
 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
 Ciarlo TJ, CA Mullin, JL Frazier, DR Schmehl (2012) Learning impairment in honey bees caused by agricultural spray adjuvants. PLoS ONE 7(7): e40848.
 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 http://www.weeds.iastate.edu/mgmt/2010/glyMndisease.pdf
 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
 Laws, F (2010) http://cornandsoybeandigest.com/issues/will-glyphosate-fall-wayside-resistance-grows
 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.
 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. http://www.american.com/archive/2010/july/no-butz-about-it
 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
 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.
 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
 Gold 2002 Misconceptions about the causes of cancer http://potency.berkeley.edu/pdfs/Gold_Misconceptions.pdf
 Entine, J (2010) Crop Chemophobia: Will Precaution Kill the Green Revolution? http://www.jonentine.com/pdf/CROPCHEMOPHOBIApre-orderform.pdf
 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
 http://ngm.nationalgeographic.com/2011/07/food-ark/food-variety-graphic If you didn’t see this graphic in National Geographic, you should!
First published in: American Bee Journal January 2013
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 .
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 , and beekeepers may be eligible for benefits for colony losses if they jump through the hoops of ELAP . 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 , 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) . 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 .
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 , 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) , 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 ), 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!
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 email@example.com.
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).
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 . 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 , 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” , 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” .
- 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” .
- 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” .
- 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” .
- 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” .
- 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” .
- 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” .
- 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” .
- 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” .
- 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” .
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.
 ERS (1976) Report on the beekeeper indemnity payment program. http://babel.hathitrust.org/cgi/pt?id=coo.31924001799307;seq=8;view=1up
 Erickson, EH, and BJ Erickson (1983) Honey bees and pesticides. ABJ 123(10): 724-730.
 Mussen, E (2009) How much does it cost to keep commercial honey bee colonies going in California? http://projectapism.org/content/view/83/27/
 Anderson v. State Department of Natural Resources Minnesotahttp://www.animallaw.info/cases/causmn693nw2d181.htm
 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.
 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.
 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.
 Chauzat MP, et al (2009) Influence of pesticide residues on honey bee (Hymenoptera, Apidae) colony health in France. Environmental Entomology 38: 514-523.
 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
 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.
 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.
 Thompson, HM (2012) Interaction between pesticides and other factors in effects on bees. http://www.efsa.europa.eu/en/supporting/doc/340e.pdf
 vanEngelsdorp D, et al. (2009) Colony Collapse Disorder: A Descriptive Study. PLoS ONE 4(8): e6481.
 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