by Greg Hunt and Christian Krupke, Purdue University
CAP Updates: 28
In the last 10-15 years, the EPA has gradually eliminated many uses of several “older” classes of pesticides. These include the widely used organophosphates, a staple of many agricultural systems. This left farmers and chemical companies looking for alternatives. A new class of pesticides called neonicotinoids, or neonics for short, were initially developed in the 1970’s. The chemical structure of these is derived from nicotine (also an insecticide, keeps tobacco plants safe from caterpillars) and they are relatively non-toxic to most vertebrates. Most are water-soluble and break down slowly in the environment, so they can be taken up by the plant and provide protection from insects as the plant grows and develops. During the late 1990’s this class of pesticides became widely used (primarily as imidacloprid, trade names include Gaucho, Provado, Merit). Beginning in the early 2000’s, two other neonics began to see wide use to treat corn and other field crop seeds. These compounds are clothianidin (trade name Poncho) and thiamethoxam (trade name Cruiser), the latter rapidly breaks down into clothianidin in living organisms. Currently, virtually every corn seed that is planted in the Midwest is treated with one of these two compounds, along with a cocktail of fungicides. In addition, most soybean seeds are also treated with neonics (usually thiamethoxam). Clothianidin is one of the most toxic substances we know of for honey bees. The lethal oral dose to give a 50% chance of death (the LD50) among an exposed group of adult honeybees is about 3 nanograms per bee. That’s 3 billionths of a gram, a tiny fraction of the weight of the bee (1/10 of a gram). Of course, toxicity by itself is not informative without exposure data. How often do honey bees encounter these pesticides? Where does this issue rank among the challenges facing honey bee health? These are some of the questions that the beekeeping and agricultural communities are trying to answer. Here we describe the current situation as we see it, and the status of our own investigations into health threats from neonicotinoids. These studies were funded by the North American Pollinator Protection Campaign and the Bee Health Coordinated Agricultural Project (CAP).
Some beekeepers saw this issue coming before we did. In the spring of 2010 we became aware of it when we saw dead bees in front of most of the Purdue bee hives during the week that corn was being planted nearby. Conditions were hot (85°F), dry and windy and clouds of dust were kicked up by the planters – a common sight throughout the Midwest in early spring. We tested bees that were dying in front of hives near agricultural fields and also healthy hives. The dead bees had clothianidin and several other seed treatment chemicals in or on their bodies. Most of the bees that were dying were actually the nurse bees that may have consumed pollen that was being collected from dandelions and other flowering plants in the area. We saw the characteristic color of dandelion pollen on most of the foragers. Pollen collected by returning foragers and pollen sampled from the cells of those hives had about 10 times the level of clothianidin and thiamethoxam as compared to that detected in the dead bees. In 2011, we conducted further studies and found that the talc that is put into seed hoppers to keep seeds flowing properly during planting contained an extremely high concentration of clothianidin and thiamethoxam (about 1 to 1.5%). A gram of talc containing 1.0% clothianidin could theoretically kill a million bees if they ingested it and could threaten about half as many bees if the dust contacted them (Laurino et al. 2011; Tremolada et al. 2010). Later in the season, pollen collected by bees when corn was shedding pollen in the area had up to 88 parts per billion (ppb) of clothianidin in it. These results suggest that there are many potential routes for exposure, but does not identify the key factor. We hypothesize that corn being planted nearby acts as a source of talc which may have contaminated flowers that bees were foraging on. Corn pollen from plants grown from treated seed had much less clothianidin, about 4 parts per billion. This is not enough to kill bees outright, but about 45% of the pollen our bees were collecting at that time was corn pollen. We do not know what effect this level of pesticide has on nurse bees that consume the pollen, or on the larvae they are feeding it to. Clothianidin is fairly stable in the soil with a documented half-life (the amount of time until half of the material is broken down in soil) of up to three years (EPA – 2003). After testing soil from various fields, we found that levels were just as high (about 9 ppb) in a field that had not had treated seed of any kind planted in it for the previous two growing seasons. Our overall conclusion was that the greatest danger occurs at planting time (due to the waste talc from planters), but that bees are exposed to sublethal levels of pesticide throughout the growing season. Our research paper is published online and is freely available (http://www.plosone.org/article/info:doi%2F10.1371%2Fjournal.pone.0029268).
Figure 1. Bees can be exposed to neonicotinoids at low concentrations from corn pollen and windblown soil that lands on other flowers. They are exposed to much higher concentrations from contaminated talc that escapes from seed hoppers for a short period around planting time (photo courtesy of Purdue entomology extension).
We have also communicated with beekeepers on how they can report beekills to state agencies and the EPA (email@example.com). This report has generated some discussion and of course, and more questions. It is not a “smoking gun” that points to neonicotinoids as the cause of CCD. What the work does show is that there is significant room for improvement in how we plant field crops in North America. Although problems with bee kills and clothianidin had been seen in Germany in 2008, there are many differences in planting practices, land use, and equipment that mean the European experience does not readily translate to questions here. For example, the virtually ubiquitous pneumatic planters that use forced air to plant seeds (and exhaust used talc in the process), are not widely used in the E.U., nor is talc widely used as a seed lubricant. It is also important to note that the acreages (both in total and individual fields) here in North America dwarf European production. At some 95 million acres planted this year, corn alone accounts for almost a quarter of the harvested acres in the United States. It is the largest use of US agricultural land and virtually every seed is coated with neonicotinoid insecticides. The United States accounts for over 40% of worldwide production, over 20 times more than the highest ranking country in the E.U. (France, ranking 7th worldwide).
What does all this mean? Is this a tempest in a teapot, or will our agricultural practices spell the end of honey bees in North America? It is tempting in the era of “thumbs up/thumbs down” and instant judgements to label every scientific finding as one or the other – but of course the truth lies in the middle. Only more data will reveal the extent of the problem and possible solutions. For example, this spring we have observed more dead and twitching bees in front of colonies during the corn planting here in Indiana. The Indiana Office of the State Chemist worked on a handful of incident reports and all of the dead bee samples tested positive for clothianidin and other seed treatment chemicals. Similar reports have been coming from Ohio, Minnesota and the provinces of Ontario and Quebec. In Ontario, more than 100 samples from this year’s spring bee kills are being analyzed and regulation of neonicotinoids is being re-evaluated because of threats to pollinators (http://www.hc-sc.gc.ca/cps-spc/pubs/pest/_decisions/rev2012-02/index-eng…). It is certainly true as Randy Oliver recently pointed out that many people are still successfully keeping bees in the corn belt (Oliver 2012). If growing treated seed led directly to drastic reductions in honey bee health, we would not need research (or researchers!) at all. The results would be apparent to beekeepers and field crop producers alike. This story is like the layers of an onion, that unfortunately require time to peel. There is no question that other potential causes of these bee kills should be considered as well. However, when we see kills that are synchronized with each other and with corn planting over a wide area, and the pesticide is found in dead bees near agricultural fields, the weight of the evidence points in just one direction.
Some of the problems associated with planting can likely be solved with some effort to change planting practices. The neonics are effective pesticides that are relatively non-toxic for many life forms (most notably humans), but (of course) are highly toxic to insects. Like all pesticides, they should be used judiciously – where there is a demonstrated need. This is a principle of pest management that has largely gone by the wayside in some large acreage cropping systems. The bee story is one indication that perhaps it is time to re-evaluate whether it is necessary to use up to 1.25 milligrams of neonicotinoids on virtually every single corn kernel that is planted in the country. Planting corn is the largest use of arable land in the US, and each corn seed theoretically has enough pesticide to kill well over 100,000 bees.
The EPA is currently in the process of re-evaluating the registration of clothianidin. This includes convening a scientific advisory panel to weigh the published information, data packages from the registrants of these chemicals, and input from stakeholders. This is the time to make your voice heard. The public docket can be found online under the docket number EPA–HQ–OPP–2011– 0865. Remember that in these cases, the most useful input is factual, science-based, and presents an argument that is not based on emotion, feelings or perceptions but data.
Let’s try to put the seed treatment issue into perspective with what is going on with our bees. We are all still hearing the words “colony collapse disorder” and it is synonymous in the media with the major bee health problem. Yet it is not clear how common these symptoms (rapid dwindling of colony population, leaving untended brood and food stores, but no dead bees) occurred in the past or are happening now. Symptoms of CCD were noticed during 2006 and 2007, perhaps less often since then. Since that time, there has been a comprehensive tallying of the nation’s winter bee kills, and there is a general belief that losses have increased – we are averaging about 30% winter die-offs each year. But prior to that time, losses were recorded from regional surveys that exceeded 30% after the spread of parasitic mites (occurring about 1990). For example, a survey of beekeepers in Indiana during the winter of 1995-1996 showed that about 57% of the state’s bee colonies died, and that not treating for Varroa resulted in much higher losses (Hunt 1998). In Pennsylvania, 53% of all bee colonies died that year, and losses were much higher for colonies not treated for Varroa [Finley et al. 1996]. Recent surveys and studies around the world still put Varroa at the top of the list among factors causing winter losses (Guzman-Novoa et al. 2010; Le Conte et al. 2010; Peterson et al. 2010; Ratnieks and Carrick 2010). What is clear is that bees in many areas of the world (including areas far from neonicotinoid treated seed use) are in trouble. However, since we perform agriculture on a massive scale in this country, it makes sense to consider the factors that are stressing our bees in and near the modern agricultural setting. Neonicotinoids are a key player and a good place to start. Their effects are beginning to be better characterized, but they don’t occur in a vacuum – we need to also consider interactions with other stressors of honey bees (mites, other pesticides, viruses and poor nutrition).
Where do these compounds and other pesticides rank as players in the CCD debate? Again, there is no definitive answer – but for a bee, it probably depends on where you live! Another CAP-funded study that surveyed levels of pesticides in colony wax, pollen and bees found that levels of neonicotinoids, when present, were usually low in wax and pollen and they were absent in bees. The study did not report any detections for clothianidin but it is important to note that the survey also did not include many samples from the corn belt (Mullin et al. 2010). Another study showed that bees reared in comb from commercial beekeeping operations that had relatively high levels of pesticides (including neonics) took longer to develop into adults and had their adult life span reduced by four days (Wu et al. 2011). These two studies highlight the complexity of teasing out how hive contamination with pesticides may have sublethal effects on bees. The real conundrum is that to design informative experiments we usually have to work with one compound at a time to uncover mechanisms – whereas the bees in the field are exposed to many compounds (and other stressors) simultaneously!
What we can say at this point, is that the use of neonicotinoid seed treatments over hundreds of millions of acres annually, coupled with their extremely high toxicity to honey bees, and their persistence in plants (including nectar and pollen that bees eat) combine to create an environment where it is very difficult for bees to avoid exposure to these highly toxic chemicals. That in itself makes this topic worthy of further investigation. Another thought that gives us pause is that if we are seeing bee kills in honey bees that have a colony to rely on, what is happening to the many species of native bees in North America that have to go it alone?
- Dainat B, Evans JD, Chen YP, Gauthier L, Neumann P (2012) Predictive markers of honey bee colony collapse. PLoS ONE 7(2): e32151. doi:10.1371/journal.pone.0032151.
- EPA (United States Environmental Protection Agency). 2003 Pesticide Fact Sheet: Clothianidin. Available at: http://www.epa.gov/opp00001/chem_search/reg_actions/registration/fs_PC-044309_30-May-03.pdf.
- Finley J, Camazine S, Frazier M (1996) The epidemic of honey bee colony losses during the 1995-1996 season. Am Bee J 136: 805-808.
- Food and Agriculture Organization of the United Nations, Statistics Division (2009). “Maize, rice and wheat : area harvested, production quantity, yield”. http://faostat.fao.org/site/567/DesktopDefault.aspx?PageID=567.
- Guzmán-Novoa E, Eccles L, Calvete Y, McGowan J, Kelly PG, et al. (2010) Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie 41: 443-450.
- Hunt GJ (1998) The war against Varroa: How are we doing? Am Bee J 138: 372-374.
- Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K. 2012. Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS ONE 7(1):e29268. doi:10.1371/journal.pone.0029268.
- Laurino D, Porporato M, Patetta A, Manino A (2011) Toxicity of neonicotinoid insecticides to honey bees: laboratory tests. Bull Insectology 64:107-113.
- Le Conte Y, Ellis M, Ritter W (2010) Varroa mites and honey bee health: can Varroa explain part of the colony losses? Apidologie DOI: 10.1051/apido/2010017.
- Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, vanEngelsdorp D, Pettis JS (2010) High levels of miticides and agrochemicals in North American apiaries: Implications for honey bee health. PLoS ONE 5(3): e9754. doi:10.1371/journal.pone.0009754.
- Oliver R (2012) The extinction of the honey bee? Am. Bee J. 152(7):697-704.
- Peterson M, Gray A, Teale A (2010) Colony losses in Scotland in 2004-2006 from a sample survey. J. Apic. Res. 48: 145-146.
- Ratnieks FLW, Carreck NL (2010) Clarity on bee colony collapse? Science 327: 152-153.
- Tapparo A, Marton D, Giorio C, Zanella A, Solda L, Marzaro M, Vivan L, Girolami V (2012) Assessment of the environmental exposure of honeybees to particulate matter containing neonicotinoid insecticides coming from corn coated seeds. Environ. Sci. Technol. 46: 2592-2599.
- Tremolada P, Mazzoleni M, Saliu F, Colombo M, Vighi M (2010) Field trial for evaluating the effects on honeybees of corn sown using Cruiser and Celest xl treated seeds. Bull Environ Contam Toxicol 85:229-234.
- Wu JY, Anelli CM, Sheppard W (2010) Sub-lethal effects of pesticide residues in brood comb on worker honey bee (Apis mellifera) development and longevity. PLoS ONE 6(2): e14720. doi:10.1371/journal.pone.0014720.