In the winter of 2007, panic spread among beekeepers across the globe. Their honeybees were dying at a rate never seen before. Beekeepers were stunned; where colonies were formerly plentiful with bees, there was now nothing – not even traces of their bodies. The bees were simply missing. In their 2009 Scientific American article, “Saving the Honeybee,” Diana Cox-Foster and Dennis vanEngelsdorp wrote that the crisis hit both commercial and small-scale beekeepers, although apiaries in the Northeastern United States were hit the hardest. One beekeeper from Florida, Dave Hackenberg, described the shock he felt as his colonies, which had been “boiling over” with bees the previous fall, became like “ghost towns” in the following spring. While it is common to observe losses of about 10% per year, beekeepers were reporting 30-90% losses, according to the Environmental Protection Agency.
Researchers named the phenomenon “colony collapse disorder,” or CCD. Susan Milius wrote in Science News that as the news spread, “amateur entomologists” sprung up among the general public as the media, environmentalists, and federal regulators speculated relentlessly about potential causes of CCD. The public assigned blame to climate change, fungi, viruses, poor nutrition, and even radiation from cell towers. Regardless of the cause, many people worldwide were concerned, and for good reason: in a 2018 review, a group from Shandong Agricultural University in China, led by researcher Guilin Li, said that without honeybees, worldwide crop production would drop by 90%. In particular, the European honeybee, Apis mellifera, is responsible for pollinating one-third of the world’s food crops.
However, as mysteriously and suddenly as the 2006-2007 CCD crisis occurred, it disappeared. According to Milius, very few, if any credible cases of CCD have been observed since then, although bee populations have been steadily declining. That doesn’t mean that speculation has ended, though. If anything, scientists are even more hard-pressed to solve the mystery of why CCD emerged that fateful winter – and whether it could happen again.
Unfortunately, very little consensus has emerged as to how colony collapse disorder started and why it stopped. There are many theories for honeybee decline. For example, Li’s group points to wide scientific agreement that parasites, including Varroa mites (Varroa destructor), contribute to bee decline and colony collapse disorder. These mites cause damage to honeybees by feeding on the hemolymph, the bee equivalent of blood, and transmit harmful bacteria into the bees’ bodies, leading to increased risk of infection. Furthermore, fungi, which proliferate in humidity and unstable temperatures, can cause chalkbrood and aspergillosis, diseases which have both been shown to damage honeybee hives and colonies.
As early as 2007, a study led by Diana Cox-Foster, an entomologist at Pennsylvania State University, found a variety of viruses, including Israeli acute paralysis virus (IAPV), Chinese sacbrood virus (CSBV), and deformed wing virus (DWV) in collapsed hives. According to the Shandong University team, such viruses have long been known to cause physical harm to honeybees, as well as to impair their growth and ability to learn. While DWV does not usually kill individual honeybees, it causes deformed wings and small body size in adult bees. In addition, it suppresses honeybees’ immune systems and decreases their lifespans, especially when disease-carrying, parasitic Varroa mites are present. CSBV also hurts honeybee populations by severely limiting larval development and reducing their capacity to produce antioxidants. According to Cox-Foster’s group, while many viruses were present in collapsed hives, IAPV appears to play a key role in CCD in the United States. The presence of IAPV is also closely correlated with the presence of Varroa mites, so Cox-Foster suggests that the mites act as a vector for the virus, spreading the disease among honeybees wherever they go. IAPV impairs critical biological processes such as cell division and energy production in honeybees, which can lead to death, according to Li’s group.
The Shandong University team also writes that multiple studies have shown that various environmental stressors, such as temperature or poor nutrition, cause declines in honeybee populations. While humidity less directly affects colony survival, studies show that honeybees lose the ability to cope with too-high or -low temperatures over long periods of time. Temperature stress can trigger re-allocation of labor within the hive; for example, when the outside temperature is too warm, some bees evacuate the hive in order to clear extra space for honeybees who are working to cool the hive. Furthermore, poor honeybee nutrition can exacerbate their sensitivity to disease. Honeybees fed diverse, pollen-based diets (as opposed to monocultures and sugar-based diets) have been shown to have stronger immune systems and higher body fat content.
Entomologists have many theories as to why bee populations are declining, according to Li’s group. Some scientists put more emphasis on biological factors such as fungi, mites, and viral diseases. Others put more stock in environmental causes, such as pesticides, increased temperature stress, or poor nutrition. Most studies on honeybee population acknowledge that it is a combination of all of these factors, both biological and environmental, that has caused a gradual decrease. However, as Li’s group writes, the mechanisms behind rapid collapse events – that is, CCD – are not very well understood.
A group of three researchers from eastern Massachusetts believe in a simple explanation: that neonicotinoids, a type of pesticide, are a sure cause of CCD. In 2013, Scott Helman, a science writer for the Boston Globe, profiled a Harvard researcher named Dr. Chensheng “Alex” Lu, who specialized in tracking the spread of pesticides in food, homes, and workplaces. Helman wrote that soon after the 2006-2007 collapse event, Dr. Lu became intensely interested in colony collapse disorder, and whether pesticides may have had a role in causing it.
Neonicotinoids, or “neonics,” have been in widespread use since the 1990s, and are among the most popular agricultural pesticides in the world, according to a March 2018 article in Chemistry World by Anthony King. They are systemic pesticides, which means that they are coated onto plant seeds, causing plants to then incorporate the chemical into their body tissue as shown in Figure 1. Neonics mimic acetylcholine, a neurotransmitter which normally triggers muscle movement in insects. At very high concentrations, neonics over-stimulate muscle movement, resulting in cell death and deactivation of nerve cells, which handily kills pests that damage crops.
Neonicotinoids are primarily used on agricultural crops like corn, which are pollinated by the wind. The wind blows corn pollen, which is laced with high concentrations of neonicotinoids, onto nearby flowers and crops. Honeybees and wild bees collect nectar from these flowers and crops, thus consuming neonicotinoids at sub-lethal concentrations. Alex Lu suspected that it was this low-level, long-term exposure to neonicotinoids that was the culprit for colony collapse.
Helman writes that in 2009, Lu approached Kenneth Warchol, a middle school social studies teacher and sixth-generation beekeeper, in the hopes of testing his hypothesis. Warchol’s expertise as a beekeeper was a family affair; the tradition of beekeeping extended all the way back to his ancestral roots in Poland in the 1840s. Warchol, highly regarded in local and national beekeeping associations, was passionate about protecting bee health. Also working with them on the project was Richard Callahan, an entomologist who was a past student of Mr. Warchol and had been working with bees for the past fifteen years.
As detailed in the paper they later published, the three researchers decided to test Lu’s hypothesis by setting up three apiaries with six colonies in each – eighteen colonies in total. They separated each group of six colonies into two sugar sources – three fed with normal sucrose, and three fed with high fructose corn syrup. Of each sugar group, two colonies were given neonicotinoids (either imidacloprid or clothianidin, two of the most widely used neonics) in their diet, and one colony served as the control, consuming a diet free of neonicotinoids.
In the fall, as Lu, Warchol, and Callahan tracked the progress of their colonies, their results showed no differences between treatments – all of the colonies were thriving, a discouraging result for the hopeful researchers. “At that time, I thought my hypothesis was wrong,” Lu told Helman. However, as soon as winter came, the beekeepers watching the three apiaries began to report alarming results – the bees were disappearing, and fast.
According to the review written by Li’s group at Shandong University, honeybee colonies normally survive the cold-temperature stress of winter by consuming the sugar provided by beekeepers, congregating together in solid masses, and performing rapid contractions of their wings to vibrate their thoracic (abdominal) muscles. However, when winter came, Lu, Warchol, and Callahan observed that in the colonies treated with trace levels of neonicotinoids, bees began to leave the hive in the middle of winter – in essence, committing suicide. By the end of the winter, all colonies treated with neonicotinoids had shown statistically significant decline compared to the control colonies. Six of the twelve neonic-treated colonies had been lost altogether, and showed symptoms analogous to that of CCD; there was virtually no activity inside the hives, and the bees had all disappeared. On the other hand, all of the control colonies had survived, except one, which the researchers attributed to an infection from Nosema ceranae, a fungus-like parasite known to be connected to colony collapse disorder as well.
These results were groundbreaking. Figure 2, which illustrates the findings of the experiment, shows that populations fed trace amounts of imidacloprid and clothianidin, shown in blue and red, declined continuously throughout the winter, while the control populations, shown in green, remained mostly unharmed through the winter. According to the results of this study, there was no question that trace amounts of neonicotinoids, consumed by bees over many months, caused colony collapse disorder. No researcher had ever made such a bold claim before, and there was no question that the symptoms they had induced were identical to those of colony collapse disorder. They had solved the mystery of the missing bodies: the neonicotinoid exposures in the study had caused the bees to flee their hives before they died, leaving empty hives just like the ones found by Dave Hackenberg in 2007. In addition, previous observations had shown that CCD most often occurred during the winter, which Lu’s team’s experiment corroborated.
In 2012, after being rejected over and over again by various reputable journals, Lu, Warchol, and Callahan’s paper was accepted by an Italian journal, The Bulletin of Insectology. It was titled “Sub-lethal exposure to neonicotinoids impaired honeybees winterization before proceeding to colony collapse disorder.” According to Helman, the paper was not well-received by the scientific community. Following its publication, May Berenbaum, the head of the Entomology Department at the University of Illinois at Urbana-Champaign, argued that the sample size of Lu’s paper – just eighteen colonies – was too small, and that the findings were not significant enough to justify a complete ban on neonicotinoids. Helman wrote that other leading researchers also attacked the paper’s credibility, with one prominent bee researcher even saying that the findings were “embarrassing.”
Despite the controversy, most scientists do agree that neonicotinoids are at least part of the problem, if not the primary cause behind colony collapse disorder, according to Li’s review. In 2015, in an email to NBC News, Dr. Berenbaum acknowledged that current studies on the effects of neonics on honeybees “indicate that, at least with current technology, systemic use of pesticides is fraught with environmental problems.” Furthermore, a 2015 study by Sebastien Kessler’s team at the Institute of Neuroscience at Newcastle University even shows that bees prefer food sources containing neonicotinoid pesticides, which makes neonics’ deleterious effects on bee colonies even worse.
As a result of repeated findings condemning the use of neonicotinoids, many governments worldwide have taken steps to limit their use. In April 2018, NPR’s Bill Chappell reported that the European Union plans to “completely ban” outdoor use of neonicotinoids because they may harm bees. The head of the European Food Safety Administration’s pesticide unit, Jose Tarazona, said in February, “Some low risks have been identified, but overall the risk to the…types of bees we have assessed is confirmed” (Chappell).
Not all governments have adopted the same stance as the EU. For example, Reuters’ Laura Zuckerman writes that in August 2018, the Trump administration rescinded an Obama-era regulation that had prohibited the use of neonicotinoids in wildlife refuges where farming is permitted. In the United States, enacting legislation to bolster the fight against colony collapse disorder is complicated. In addition to the complexity of proposed causes of honeybee decline, upcoming legislation also faces the challenge of powerful pesticide company opposition. For example, Helman writes that Bayer, one of the largest pesticide manufacturers in the world, tries to downplay the effects of pesticides on honeybees, and instead touts other factors such as Varroa mites, whose causal link to CCD has been proven to be a weak one, according to Li’s group’s review. CropLife America, a lobby that represents Bayer and other influential pesticide companies, spent $11.2 million on lobbying between 2008 and 2013 according to a 2013 article in the Huffington Post by Christina Wilkie. They also put $643,000 into a PAC supporting congressional candidates who were sympathetic to the pesticide industry.
Lu, Warchol, and Callahan’s findings also pose a dilemma for growers. While many farmers depend on neonics to protect their crops from pests, some, not all farmers also rely on bees to pollinate their crops. As Elizabeth Grossman, an environmental journalist, wrote in 2013 for Yale Environment 360, neonicotinoids are used on 95% of corn plants and half of all soy plants in the US. However, since corn is pollinated by wind and soy is self-pollinating, these crops do not depend on honeybees to grow. Therefore, corn and soy farmers may be reluctant to consider the deleterious effects of their pesticides on honeybees and other types of crops. That’s not to say that American crops aren’t dependent on honeybees: Grossman also writes that other crops such as California almonds and various types of vegetables are heavily reliant on honeybee pollination.
Although large-scale colony collapse disorder has not occurred for over a decade, bee populations are still declining at concerning rates. Research points to neonicotinoids as a sure culprit behind honeybee population decline. However, Lu, Warchol, and Callahan’s findings do not explain why the mass CCD events of 2006-2007 occurred when they did, why there have been no mass die-offs in winters since then, and whether another mass CCD event could happen again. Furthermore, more research must be done to find additional methods to protect honeybees against threats like mites, viruses, and environmental stressors, which are still contributing to abnormally fast declines.
Terrestrial ecosystems have relied on bees for millions of years; they are some of our most valuable and overlooked natural resources. While scientists have made leaps and bounds in bee research since the mass die-offs of the fateful winter of 2007, there is still much more work to be done to protect our bees.
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