Stung By Dead Bees

For about two weeks in the early spring, the San Joaquin Valley is a vast confection of pink and white, and the air is heavy with a magnolia-like scent. To some, the odor may seem overpowering, almost cloying. But to Jeff Anderson, a beekeeper in the small Stanislaus County town of Oakdale, it is the smell of money.

Oakdale is near the center of California's almond belt, and the pastel froth across the valley floor consists of hundreds of millions - maybe billions - of almond tree blooms. Each little blossom can produce a highly valuable nut - the 2012 crop was worth $4.8 billion. But the blossoms can't pollinate themselves.

That's where Anderson's bees come in. He sells honey, but he gets most of his income by providing pollination services to Central Valley growers. Some 35 percent of the world's food crops - including almonds, plums, kidney beans, okra, coffee, and watermelons - must be pollinated by insects to produce edible fruits, vegetables, and nuts, not to mention the seeds to sustain ensuing generations. Among all the insect pollinators, honeybees do most of the work.

In early spring, the California almond industry requires approximately 1.4 million hives, or 60 percent of the nation's managed colonies. With so much demand, you would think that Anderson's migratory pollination business would be secure. But his bees are dying, and his income is shriveling in direct proportion to their decline.

On this day in March, Anderson sits at the dining room table in his home, a prefabricated structure in a large, well-stocked compound filled with heavy equipment and stacks of bee boxes. "I had 3,200 colonies last spring," he says. "Now I'm at about 600 colonies, and they're not in great shape. At the peak of the pollination season, a typical colony will have 50,000 [worker] bees. Now, we're down to about 30,000 bees per colony."

To show me the problem, Anderson drives to a nearby almond orchard where his sons - Jeremy, Kyle, and Mitchell - and daughter, Alyssa, manage a number of colonies in boxes tucked under the trees. The day is sunny and warm - perfect pollinating weather - and the bees are out and about. Except it doesn't sound that busy. In a typical almond grove at the peak of bloom, the air positively vibrates with the susurrus of working bees everywhere. Here, you have to scan the tree canopy carefully to spot bees: one here, another over there. Most of the blossoms are vacant.

Anderson dons his beekeeper's protective suit, helmet, and veil to take a closer look at the bee boxes. He fires up his smoker - a bellows-like device beekeepers use to puff smoke into colonies they are inspecting. The smoke dulls the bees' receptors, preventing them from detecting pheromones that stimulate the hive occupants to attack an intruder.

After directing a couple of puffs to the bottom of a hive, Anderson pops off the lid and peers into a "super," a box containing hanging frames of wax sheets where the bees build comb to brood larvae and store honey. Even to my untrained eye, the super seems deficient of bees.

"Weak," mutters Anderson. "A really weak colony." He points to a windrow of dead bees outside the hive. "Sick or dying bees are immediately removed [by worker bees]," he says. "You always see some dead bees outside a colony. But that's a lot here. I'd say much more than normal. Unfortunately, that's the new 'normal.' "

Moribund beehives aren't confined to orchards in the San Joaquin Valley. Colony collapse disorder (CCD), as the phenomenon is known, has plagued honeybee populations across the developed world. The syndrome is defined by the USDA as a dead colony with neither adults nor dead bee bodies, but with a live queen and usually honey and immature bees still present. No cause has been scientifically proven.

Although colony losses directly attributable to CCD have declined, reports of honey bee colony losses are increasing. In an annual survey released in May by the Bee Informed Partnership, a consortium of universities and research laboratories, thousands of beekeepers reported losing 42 percent of their colonies in the past year. That is well above the 34 percent loss reported for the same period in 2013 and 2014, and it is the second-highest loss recorded since year-round surveys began in 2010.

A devout Seventh Day Adventist, Anderson puts great stock in scripture and in the Adventist ethos, which emphasizes a vegetarian diet and reverent stewardship of the natural world. He - and many other beekeepers in North America and Europe - are confident they've determined the cause of colony collapse: a new generation of pesticides known as neonicotinoids - "neonics" for short.

"We are losing huge numbers of bees where neonics are applied," says Anderson. "And the only areas where there isn't massive pollinator decline have little or no agriculture, like the remote parts of Montana. It is clear that neonicotinoids are driving this thing."

Introduced in the 1990s, neonics are a class of neuroactive nicotine-analog insecticides that may be applied at the plant root, sprayed onto foliage, or used as seed coating. By the early 2000s they were in wide use in Europe, Canada, and the United States. These systemic insecticides have largely replaced organophospate and pyrethroid pesticides, which had supplanted organochlorine pesticides such as DDT and Aldrin. Chemical companies developed each group to counter the deficiencies of its predecessor. For instance, although the organochlorines themselves weren't acutely toxic to mammals, they were highly stable, accumulating in the soil and in ecosystem food webs potentially for hundreds of years.

Enter the neonics, which act on the central nervous system of insects in ways similar to the natural insecticide nicotine. They cause paralysis that leads to death, often within a few hours. Although they do not appear to cause long-term harm to fish, mammals, or birds, they do persist in the environment and have been found as residues in many foods.

Unlike earlier families of pesticide, neonics are water soluble and enter a plant's vascular tissue directly. This means a treated plant's leaves, woody tissue, blooms, pollen, and nectar can become toxic to insects, and for long periods of time - good news for crops that must be defended against ravenous bugs, but devastating for bees.

"When bees forage on plants treated with neonicotinoids, they bring contaminated pollen and nectar back to the colony," Anderson says. "With neonics, the exposure is constant, never ending."

Usually the pesticide isn't applied at levels high enough to kill foraging bees outright. But bees eat pollen, and over time the neonicotinoids can sicken and kill them. Worse, most of the nectar they collect is converted to honey and fed to the colony's larvae - with potentially disastrous results.

In 2010 Bayer CropScience voluntarily changed its product labels to remove almonds from the list of uses for imidacloprid, the most widely used neonicotinoid, registered in more than 120 countries. Direct application of neonics on almond trees is now minimal. But bees - including those brought directly into the orchards at pollinating season - forage widely on surrounding weeds and wildflowers, picking up insecticide residues that accumulate in their bodies but aren't immediately lethal.

"It can wipe out an entire colony, or it can just weaken it - slashing the number of working bees - as we're seeing in these almond orchards," Anderson says, fitting the lid back on the hive.

His conviction that neonics are a cause of declining colonies is shared by many other beekeepers. One longtime friend, Steve Ellis, brings his hives to the Central Valley each year from Minnesota, where Anderson, too, maintains a home. Ellis says incidences of colony collapse disorder accelerated dramatically when the application of neonicotinoids became widespread.

Neonicotinoids are now used on nearly all corn and canola crops, and about half of all soybeans. "They're used in seed coatings and on nursery stock," Ellis says. "It is not a coincidence that incidents of colony collapse have tracked the expansion of neonicotinoid use. They are directly correlated."

Pesticide manufacturers insist that evidence suggests honeybee declines and incidences of colony collapse are caused by multiple factors, including mites and diseases that affect honeybees. By 2006, seven different neonicotinoid-active ingredients had been approved by federal and state regulators and were being widely marketed.

Despite data collected since then implicating neonics in colony decline, commercial beekeepers and honey producers say they got nowhere with administrative complaints to the U.S. Environmental Protection Agency (EPA) and state regulators. "Unfortunately, everybody circles the wagons when you bring up the subject of agricultural chemical usage," Ellis says. "That's especially the case with neonics."

"The problem is, [big agriculture] has gone from a pest-eradication policy to a pest-prevention policy," Anderson says. "Unfortunately, these poisons are not selective, and they're wiping out beneficial insects as well. The threat isn't just to beekeepers. The entire food-production system is at risk."

So Ellis and Anderson went to court.

The two migratory beekeepers first brought suit in Minnesota, where Ellis operates a honey farm. After pesticide overspray from neighboring land killed bees in their hives, they joined a third beekeeper to sue state regulators for negligence. The case was summarily dismissed by the trial court, but in 2005 the Minnesota Supreme Court reversed in part and remanded. (Anderson v. State Dept. of Nat. Res., 693 N.W. 2d 181 (Minn. 2005).)

Later, when their hives in California began to fail, Ellis became lead plaintiff in a case brought in 2013 by beekeepers and public interest groups against the EPA. The complaint alleges the agency lacked proper procedural frameworks and risk assessments when it authorized expanded use (2 million pounds applied annually on about 100 million acres) of clothianidin and thiamethoxam, two potent neonicotinoids.

The plaintiffs maintain that by permitting new uses for the chemicals without affording notice in the public register or allowing for sufficient public comment, the agency is violating the Federal Insecticide, Fungicide and Rodenticide Act (FIFRA) (7 U.S.C. §§ 136-136y), the Endangered Species Act (16 U.S.C. § 1531-1544), and the Administrative Procedure Act (APA) (5 U.S.C. § 501-706). They seek to have the EPA vacate its registrations and conditional-use approvals of the two chemicals, and consult with the U.S. Fish and Wildlife Service to insure that any agency action "is not likely to jeopardize the continued existence of any endangered species or threatened species." (See 16 U.S.C. § 1536(a)(2). (Ellis v. Bradbury, No. 13-CV-1266 (N.D. Cal. filed Mar. 21, 2013).)

The EPA and defendant - intervenors Bayer CropScience, Syngenta Crop Protection, CropLife America, and Valent U.S.A. challenged the suit based on lack of subject matter jurisdiction, failure to state a claim, ripeness, standing grounds, and failure to exhaust administrative remedies. Last year U.S. District Judge Maxine M. Chesney dismissed several of the plaintiffs' claims, but granted leave to amend the complaint. She permitted claims against more than a dozen products under the Endangered Species Act to survive. (Ellis v. Bradbury, 2014 WL 1569271 (N.D. Cal.).) Plaintiffs filed a second amended complaint in May 2014.

"This is a national lawsuit on extremely serious misregistration [of chemicals], but the problem is that the legal system moves very slowly," Ellis says. "While our case works its way through the courts, the injuries continue in the field."

Around the same time Ellis was filed, Jeff Anderson joined a coalition of commercial beekeepers and honey producers to petition the Ninth U.S. Circuit Court of Appeals for review of the EPA's registration of a new insecticide, sulfoxaflor, which is related to neonicotinoids. In 2013 the EPA approved three formulations produced by Dow AgroSciences, mitigated by reduced application rates, increased minimum application intervals, and product labels to protect pollinators. The agency acknowledged the potential risks to bees, but concluded the benefits of sulfoxaflor - including its unique mode of action and strong potential to replace older and more toxic pesticides - outweighed the risks. Petitioners allege the EPA skewed its analysis of sulfoxaflor's risks and benefits by discounting its adverse effects on the beekeeping industry and on crops that depend on bees for pollination. (Pollinator Stewardship Council v. EPA, No. 13-72346 (9th Cir. petitioner's opening brief filed Dec. 6, 2013).)

Greg C. Loarie is a staff attorney with Earthjustice in San Francisco and lead petitioners' counsel in the case. "Ellis attempts to reopen the discussion on older neonics," he explains. "Pollinator is perhaps more clear-cut, in that we contend the EPA did not follow its own guidelines when it registered sulfoxaflor under FIFRA."

Loarie notes that the EPA typically requires acute-toxicity tests on adult bees to determine the safety of neonicotinoids. But he asserts, "Any attempts to look into sublethal effects of sulfoxaflor were halfhearted at best. And sublethal effects are really the critical issue: The bees are bringing back contaminated nectar and pollen to the colonies - they feed that to the brood, the brood dies, and the colony collapses."

Robert G. Dreher, then an acting assistant attorney general, responded in the EPA's answering brief that "petitioners' argument is based on a flawed, overly restrictive view of how EPA evaluates risk to pollinators." The agency noted, Dreher wrote, "that for migratory beekeepers, it is extremely difficult to characterize risk since free roaming bees cannot be confined and there is no way to quantify their exposure to all sources of risk."

The petitioners in Pollinator hope to put the EPA on notice that it must evaluate all possible colony impacts - not just the effects on adult bees - before registering a pesticide. "Under FIFRA, a cost-benefit standard applies to pesticides," Loarie says, "so you could have a risky pesticide approved if the benefits are considered substantial [as with sulfoxaflor]. We say, if you want to do that, you have to do a genuine assessment of all the risks."

In a third California suit, Earthjustice represents a coalition of public interest groups that allege that the state's Department of Pesticide Regulation (DPR) is dragging its feet on a 2009 requirement to reevaluate pollinator impacts caused by four neonicotinoids. The plaintiffs say the department is simultaneously allowing the pesticides' expanded use, in violation of the California Environmental Quality Act (CEQA). (Pesticide Action Network North America (PANNA) v. Calif. Dep't of Pesticide Regulation, No. RG14731906 (Alameda Super. Ct. filed Jul. 8, 2014).)

"The PANNA case is a little wonky," Loarie says. "It really boils down to a fundamental disagreement over CEQA: DPR says CEQA doesn't apply because there is a list of issues and activities - including pesticide regulation and timber harvesting - that is exempt from a mandated environmental impact report. But it's clear the law does demand an impact analysis of these programs equivalent in scope to a formal EIR. DPR, however, is translating this list as a free ride - it's claiming no meaningful review is required."

Indeed, the DPR and manufacturers cite a recent appellate opinion stating, "The Legislature found certification warranted, in part, because the 'preparation of environmental impact reports and negative declarations for pesticide permits would be an unreasonable and expensive burden on California agriculture and health protection agencies.' " (Californians for Alternatives to Toxics v. Calif. Dept. of Pesticide Regulation, 136 Cal. App. 4th 1049, 1059 (2006) (citing Cal. Code Regs., tit. 3, § 6100, sub. (a)(6).)

Although the DPR does conduct reevaluations of previously approved pesticides, Loarie contends the reviews are perfunctory and typically have no moderating effect on pesticide use. "Even though these [four] neonicotinoids are still being reevaluated, they're still being applied because use can continue during the review process," Loarie says. "[R]eevaluation is a black hole for pesticides - it can take years."

In April, Judge George C. Hernandez Jr. issued a tentative ruling directing the DPR to set aside and vacate registration of two neonicotinoids - Venom and Dinotefuran 20SG - pending the agency's reevaluation. Noting that the DPR hadn't amended its regulatory certification program in 35 years, Hernandez held that the law requires the department to apply current CEQA analysis in deciding whether to register pesticides. He concluded, "By skipping the alternatives analysis and jumping straight to the implied finding that for economic reasons farmers need access to new compounds to address insect resistance management, the document provided inadequate public disclosure." (Pesticide Action Network North America (PANNA) v. California Dep't of Pesticide Regulation, No. RG14731906 (Alameda Super. Ct. order Apr. 10, 2015).)

Last year the Legislature passed AB 1789, which requires the DPR to complete its reevaluation of neonicotinoids by 2018, and to institute new review practices by 2020. (See Cal. Food and Agric. Code § 12838.) But Loarie isn't mollified, noting that the statute permits the agency to extend that deadline if it needs more time. Even though DPR admits there may be a problem with neonics, he says, "it allows expanded use during the reevaluation period. That's only incremental expansion, but the results are devastating."

When oral argument in Pollinator was presented to a Ninth Circuit panel in April, Loarie's concerns about neonicotinoids' toxicity seemed to carry weight. The judges alluded to "significant limitations" in the EPA's evaluation of toxicity studies prior to its approval of sulfoxaflor.

Judge N. Randy Smith said the agency seemed to be applying a flexible set of standards. "[The EPA studies] don't meet OECD [Organization for Economic Co-operation and Development] guidelines, they don't test the effect of the poison on brood development, [or] test long-term colony health," Smith said. "And yet you are going to rely on [the studies]? That's my problem."

EPA attorney John T. Do responded that the agency's mitigation measures for sulfoxaflor were "not necessarily reliant" on studies that tested its effects on hive health.

Judge Mary M. Schroeder quickly countered, "They're not reliant on anything."

"They're reliant on common sense," Do replied, eliciting smiles from the judges.

In response to requests for comment on the federal neonics litigation, the Department of Justice's Environmental Defense Section referred to their court briefs. But in regard to the PANNA case, California Department of Pesticide Regulation spokesperson Charlotte Fadipe says the correlation between neonicotinoids and colony collapse disorder is not as clear-cut as the plaintiffs claim.

"DPR is at the forefront of examining the role [neonicotinoids] play and how to mitigate for them," Fadipe says. "But the truth is, we're facing a multifaceted agricultural problem."

Fadipe cited research by the U.S. Department of Agriculture indicating that a parasite known as the Varroa mite is a primary culprit in U.S. incidents of colony collapse disorder. She also notes that research in Australia, where neonicotinoids are used, suggests malnutrition may play a major role in degrading the health of bee colonies.

Still, Fadipe says, DPR is considering all the possible impacts of neonicotinoids, including sublethal effects on hives. And she distinguishes between the department's "conditional registration" status for pesticides and its reevaluation process.

Conditional registration means that DPR has received enough data to determine that no significant adverse effects to humans or the environment are expected, but additional data is still required. Reevaluation, Fadipe says, occurs when there is some indication that the pesticide "may have caused or is likely to cause an adverse effect to people or the environment." The process "allows DPR to require [pesticide] companies to conduct tests and submit additional data." Reevaluation of the four pesticides targeted in the PANNA case, for example, has been underway since 2009.

Fadipe says DPR is being thorough - not dilatory. "We are always worried if we are doing enough," she says. "The science is getting sharper. We're finding things we would have missed 20 years ago - and that sometimes leads to more restrictions than some people care to see."

The manufacturers of neonicotinoids maintain that the entire class of pesticides has been unjustly demonized. Jean-Charles Bocquet is the director general of the European Crop Protection Association, a Brussels-based trade group for EU producers of agricultural chemicals. (BASF, Bayer CropScience, Syngenta, Dow AgroSciences, Monsanto Europe, and DuPont de Nemeurs are members.)

Bocquet contends opponents of neonics oversimplify a complex problem. "I've been in this business since the late 1970s, and beekeepers get nervous every time there's a new pesticide," he says.

"In the early 1980s, pyrethroids were accused of causing acute mortality in bee colonies, so we did a lot of research on this, including on over-wintering populations." He says studies determined that the Varroa mite had been present in the hives with the highest mortality, and that a bacterial disease, Nosema, also played a role. He acknowledges that pesticides also are an area of concern, but denies they are the primary cause of colony collapse disorder. "It's a multifaceted issue, and we're working on all [fronts]," he says.

The industry's position enjoys some support in academia. Dennis vanEngelsdorp, an assistant professor of entomology at the University of Maryland who directs its Honey Bee Lab, doubts that neonicotinoids alone account for the widespread and accelerating diminution of honeybees.

"On the whole," vanEngelsdorp says, "my data suggests they are not a major driver. I think they're a contributing factor, but not the sole or major factor."

The Varroa mite, vanEngelsdorp says, probably is a bigger problem. Beekeepers have known about and managed the mites for decades, he says, "But the populations are different now, and the methods of controls typically used don't work as well as they did 30 or 40 years ago."

Commercial beekeepers and honey producers disparage that theory. "We've been controlling for the Varroa mite very successfully for a very long time," Ellis says. "Now we're supposed to believe that all the beekeepers in the nation suddenly forgot how to control for mites? And that it was just a coincidence that we started losing colonies just as neonics went into heavy use? It's ridiculous."

Furthermore, Ellis says, anecdotal evidence that neonicotinoids are the real culprit is coming from Europe, where the European Commission (EC) restricted the use of three neonics in May 2013 for a two-year period (Regulation (EU) No. 485/2013). Bayer CropScience and Syngenta later sued to overturn the proscription.

Ellis believes the EC ban has been effective. "We're seeing upticks in pollinator populations in Italy, Slovenia, France, and Germany [where bans have been in place for longer]," he says. This shows "that the environment can detoxify once neonic applications are stopped, and that pollinators will recover."

In April, the European Academies Science Advisory Council released a study linking the use of neonicotinoids to declining ecosystem health, including harm to pollinators. The report could influence the upcoming review of the European Commission's neonics ban.

In the United States, President Obama created an interagency Pollinator Health Task Force last year, co-chaired by the EPA and the Department of Agriculture. In April, the EPA placed a moratorium on approval of any new use permits for neonicotinoids.

Anderson was not impressed. "In the last year, EPA has approved registration for two new neonics, and expanded uses of these pesticides to additional blooming crops," he told PANNA. "Allowing increased toxic exposure to my bees and then announcing a moratorium? Very disingenuous."

In May, Obama's task force issued a National Strategy to Promote the Health of Honey Bees and other Pollinators. It announced accelerated EPA review of neonics, to be completed by 2018. And it acknowledged the particular risk pesticides pose to contracted pollination services, proposing "to prohibit the foliar application of acutely toxic products during bloom for sites with bees on-site under contract, unless the application is made in accordance with a government-declared public health response."

Earthjustice attorney Loarie lives in Sonoma County, where the EC-banned neonic imidacloprid, among other pesticides, is applied in the grape vineyards through drip irrigation systems. "So it affects everything in the vineyard, not just the vines. In the early spring, the vineyards are typically full of wild mustard - the whole county is blazing with bright yellow flowers," he says. "And not long ago, they were always full of bees and other pollinating insects. Now they're just empty and quiet."

Back in Oakdale, 22-year-old Alyssa Anderson - who has always helped her dad out with the hives - contemplates her future. Not too long ago, she planned to go into the business full time.

"My family has been keeping bees for 75 years, and I always figured I'd be part of that," she says. "But there's just no security in it now. What's happening to the bees is really tragic, and not just for us. People don't realize that one-third of their food supply depends on bees. Even the farmers are in denial. It's going to be a rude awakening for everybody when they finally understand the stakes."

Glen Martin is a contributing environmental writer based in Santa Rosa.

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