Bee Health: The Role of Pesticides
Released: 2015-02-17T00:00:00

There is increasing concern both in the United States and globally about whether a "pollinator crisis" has been occurring in recent decades. Reports worldwide indicate that populations of managed honey bees, wild bees, and native bees have been declining, with colony losses in some cases described as severe or unusual. Other reports indicate that many insect pollinator species may be becoming rarer, which some say may be a sign of an overall global biodiversity decline.

Many reasons are cited for bee population declines, including bee pests and diseases, diet and nutrition, genetics, habitat loss, agricultural pesticides, and beekeeping management. Because pesticides have been the focus of concerns in Europe and in the United States, this CRS report briefly describes recent scientific research and analysis regarding the potential role of pesticides among the factors affecting the health and well-being of bees. The report concludes with a summary of recent regulatory activity regarding neonicotinoids, a type of pesticide, and also provides the statutory authority and regulatory activities related to pesticide use at the U.S. Environmental Protection Agency (EPA), the federal agency charged with assessing risks and regulating U.S. sale and use of pesticides.

The focus of this report on bee exposure to pesticides is not intended to imply that pesticides are any more or less important in influencing the health and wellness of bees than any of the other identified factors influencing bee health.

Background and Introduction

In the United States, honey bee colony losses due to bee pests, parasites, pathogens, and disease are not uncommon. However, in late 2006, concerns about honey bees gained heightened attention when commercial beekeepers along the East Coast began reporting sharp declines in their bee colonies. Because of the severity and unusual circumstances of these colony declines, scientists named this phenomenon colony collapse disorder (CCD). This issue was legislatively active in the 110 th Congress and resulted in increased funding for honey bee research, among other types of farm program support to protect pollinators, as part of the 2008 farm bill (Food, Conservation, and Energy Act of 2008, P.L. 110-246 ). The 2014 farm bill ( P.L. 113-79 ) reauthorized and expanded upon many of these provisions.

The U.S. Department of Agriculture (USDA) reports that U.S. beekeepers continue to lose colonies each year. Since 2006, USDA estimates that overwinter bee colony losses have averaged nearly 30% annually. However, USDA reports that in 2012/2013, "there were more colonies that dwindled away" rather than suffering from CCD, which is characterized by a sudden loss in bee colony populations and the absence of dead bees. USDA also claims that "beekeepers did not report CCD as a major cause of colony loss" for overwinter losses reported in its 2012-2013 and 2011-2012 surveys. These data are tracked for managed honey bees only.

Comparable data and information is not collected available for native or wild bee species. Such data collection is complicated by sheer number and solitary nature of native and wild bee species.

To date, the precise reasons for honey bee colony losses are still unknown. USDA and most scientists working on the subject seem to agree that none of the research conclusively points to one single cause for the large-scale number of honey bee deaths. This general conclusion was reconfirmed in a May 2013 report by USDA and the U.S. Environmental Protection Agency (EPA), National Stakeholders Conference on Honey Bee Health (commonly referred to as the "USDA-EPA joint report"). A 2007 study by the National Research Council (NRC) of the National Academy of Sciences, Status of Pollinators in North America (referred to here as the 2007 NRC study), also provides a detailed scientific context for bee health. A series of other reports documenting the findings of USDA's ongoing research also describes the many factors affecting honey bees. See Figure 1 .

Reasons cited for bee population declines include a wide range of possible factors. Potential identified causes include bee pests and diseases, diet and nutrition, genetics, habitat loss and other environmental stressors, agricultural pesticides, and beekeeping management issues, as well as the possibility that bees are being harmed by cumulative, multiple exposures and/or the interactive effects of each of these factors.

One issue widely reported in the media is the potential role that pesticides—in particular, neonicotinoid pesticides—might play in overall bee health. As one of the potential causes of honey bee colony declines, this report addresses what role, if any, pesticides play in influencing the health and wellness of bees. Regarding honey bee health, the current state of knowledge of pesticides was summarized in a 2013 report by USDA and EPA:

There is broad consensus among all stakeholders that pesticide use should not affect honey bees in such a way that (1) honey production is reduced or (2) pollination services provided by bees are threatened.... However, it is not clear, based on current research, whether pesticide exposure is a major factor associated with U.S. honey bee health declines in general, or specifically affects production of honey or delivery of pollination services. It is clear, however, that in some instances honey bee colonies can be severely harmed by exposure to high doses of insecticides when these compounds are used on crops, or via drift onto flowers in areas adjacent to crops that are attractive to bees.

This report examines in greater detail the role of pesticides, providing a summary of selected scientific literature. The relative importance of pesticides in U.S. or global bee health is a subject of numerous research projects, some of which are discussed in this report.

Some groups have expressed concern about the assessment of most experts that the causes of pollinator health concerns are multifaceted and may involve the interaction of multiple factors, since this may deflect attention from the potential role of exposure to pesticides. On the other hand, some groups appear unwilling to acknowledge that pesticide exposure may play an important role in pollinator health concerns, especially if this acknowledgment leads to restrictions or reductions in the use of certain pesticides or related crop pest controls.

This report provides information regarding the potential role of pesticides in the health of bee colonies, and also the importance of pesticides relative to other influences on bee health. The report provides general information about the nature of pesticides, pesticide uses, and pesticide regulation in the United States, as well as more specific information about the registration status of a class of pesticides known as neonicotinoids, which have been implicated in some studies concerning honey bee colony declines. This report also describes a range of options to address pesticide exposure by bees, including implementing crop- and/or product-specific best management practices (BMPs) regarding pesticide use and applications. Some U.S. cities as well as some other countries, including Canada and those in Europe, have opted to institute restrictions on the use of certain pesticides. Congress has introduced similar legislation, but has also considered alternative policy options to address this issue.

U.S. Pesticide Laws and Regulation

Pesticide Laws and Statutory Framework

Pesticides are broadly defined in U.S. law as chemicals and other products used to kill, repel, or control pests. Familiar examples include pesticides used to kill insects (insecticides) and weeds (herbicides) that can reduce the yield, and sometimes harm the quality, of agricultural crops, ornamental plants, forests, and pastures, or wooden structures (e.g., through termite damage). But the broad legal definition of "pesticide" also applies to products with less familiar "pesticidal uses." For example, substances are pesticides when used to control mites, mold, mildew, and other nuisance growths in hives or on equipment. The term also applies to disinfectants and sterilizing agents, animal repellents, rat poison, and many other substances. An estimated 18,000 pesticide products are currently in use in the United States. Pesticides vary greatly in toxicity, persistence in the environment, and ability to bioaccumulate up the food chain, as well as in the range of plants and animals that are likely to be affected in the event of exposure. Some are nearly nontoxic to some species but exquisitely toxic to other species.

All pesticides are regulated by EPA under the authority of the Federal Insecticide, Fungicide, and Rodenticide Act (FIFRA), and approximately 5,800 pesticide products used in food production also are regulated under the Federal Food, Drug, and Cosmetic Act (FFDCA). FIFRA requires EPA to regulate the sale and use of pesticides in the United States through product registration and labeling so as to prevent unreasonable adverse effects on people and the environment, taking into account the costs and benefits of various pesticide uses. FIFRA prohibits the sale of any pesticide in the United States unless it is registered (licensed) and labeled to indicate approved uses and restrictions. It is a violation of the law to use a pesticide in a manner that is inconsistent with the label instructions. EPA registers each pesticide product for each approved use. For example, a product may be registered for use on bee hives to control mites or as a seed treatment for corn. In addition, FIFRA requires EPA to reregister pesticides first registered prior to 1984 and to review all registered pesticides periodically on a 15-year cycle, based on new data that meet current regulatory and scientific standards.

For the 600 or more active ingredients in pesticide products that are registered for use in food production, Section 408 of the FFDCA authorizes EPA to establish maximum allowable residue levels (also known as "tolerances") to ensure that human exposure to the pesticide ingredients in food and animal feed will be "safe." A "safe" tolerance is defined in the law as a level at which there is "a reasonable certainty of no harm" from the exposure, even when considering total cumulative and aggregate pesticide exposure of children. Under the FFDCA, foods (or animal feeds) with a residue of a pesticide ingredient for which there is no tolerance established, or with a residue level exceeding an established tolerance limit, are declared "unsafe" and "adulterated"; such foods cannot be sold in interstate commerce or imported to the United States. Pesticides may not be registered under FIFRA for use on food crops unless tolerances (or exemptions) have been established under the FFDCA.

Pesticide Registration Process

When pesticide manufacturers apply to register an active ingredient for a pesticide, a commercial pesticide product, or a new use of a pesticide registered under FIFRA Section 3, EPA requires them to submit scientific data on toxicity and behavior in the environment. In evaluating a pesticide registration application, EPA assesses a range of potential human health and environmental effects associated with use of the product. EPA's process of registering a pesticide comprises a scientific, legal, and administrative procedure involving the ingredients of the pesticide; the particular site or crop where it is to be used; the amount, frequency, and timing of its use; and storage and disposal practices. EPA may require data from any combination of more than 100 different tests, depending on the potential toxicity of active and inert ingredients and degree of exposure.

To register a pesticide for use on food, EPA also requires applicants to determine the amount of residue that could remain on crops, as well as on (or in) food products (such as corn syrup), assuming that the pesticide product is applied according to the manufacturers' recommended rates and methods. Based on the data submitted, EPA determines whether and under what conditions a proposed pesticide use would present an unreasonable risk to human health or the environment, and, for a food or residential use, whether its use would be safe. Some features of pesticides that might affect registration decisions include the specificity of the pesticide for the targeted pest, its toxicity to people who apply it, its tendency to persist in the environment over time, and its ability to bioaccumulate in animals higher in the food chain.

EPA specifically takes into account unintended harm to bees and available information for other nontargeted insects in its registration decisions. EPA requires studies to determine acute (short-term) toxicity of a pesticide on individual bees when they come into body contact with pesticide residue. EPA also collects reports on bee-kill incidents. If a pesticide appears to be very toxic to bees, EPA may require long-term studies of its effects.

If the risk is determined to be unreasonable or unsafe, EPA attempts to mitigate the risk by adjusting requirements on the label (for example, requiring a buffer zone around lakes and streams or requiring personal protective equipment for pesticide handlers). If the risk remains unreasonable or unsafe, EPA will refuse to register the pesticide. If the risk is determined to be reasonable and safe, registration is granted, and the agency specifies the approved uses and conditions of use, including safe methods of pesticide storage and disposal, which the registrant must explain on the product label. EPA can and often does require specific application methods to be printed on the product label to minimize environmental damage. For example, the label sometimes requires that application of certain pesticides occur only when bees are not foraging, when there is little wind, or in a granular form or as a seed coating rather than aerially, in order to minimize spray drift off property. Pesticide registrations are reviewed at least once every 15 years to consider new scientific information and may be reviewed at any time in response to reports of adverse effects and possible unreasonable risks from use of particular pesticides.

Neonicotinoid Pesticides

Neonicotinoids are a relatively new major class of insecticides and among the fastest-growing class of insecticides in modern crop protection. Developed in the 1980s, some products such as imidacloprid were first introduced in the early to mid-1990s, but not widely marketed until the mid-2000s. Neonicotinoids are systemic pesticides that, regardless of application method (spray, drip irrigation, granular spreading, or seed coating), once taken into the plant, migrate into all parts, including flowers, pollen, and nectar. Neonicotinoids are related to nicotine and were developed as an alternative to highly toxic (to humans) organophosphate insecticides such as methyl parathion. Active ingredients of some of the most commonly applied neonicotinoids include imidacloprid, clothianidin, and thiamethoxam. Others include acetamiprid, dinotefuran, nitenpyram, and thiacloprid. (See text box below.)

Neonicotinoids are generally considered to be reduced-risk compared to some other types of pesticides, and have low toxicity to mammals, birds, and fish compared to some other types of pesticides. However, as their use has increased, so have concerns about their potential harm to birds, earthworms, aquatic insects, and insect pollinators, including bees. They comprise a class of active ingredients that have come under considerable scrutiny with respect to their potential effects on bee health. The attention is partly due to an incident of misuse (that is, use not in accord with the pesticide label) of one neonicotinoid, imidacloprid, in Germany that resulted in a large bee kill, as well as widespread beekeeper concerns about use of another neonicotinoid, clothianidin, and its impact on bees in France.

Neonicotinoids are insect neurotoxins that vary in strength of their effect on honey bees. The scientific evidence to date indicates that although neonicotinoids are highly toxic to bees exposed to relatively high levels, individual pesticides in this class are not the only cause of declining bee health, and pyrethroid exposures may be more significant. Although neonicotinoids have been a focus of scientific, public, and political interest, they have not been proven to be the primary cause of declines in bee health. Some experts, however, emphasize that research studies support the hypothesis that "total pesticide load" is an important influence on honey bee health, probably in combination with mite infestation, poor nutrition, viruses, and perhaps other stressors.

Possible Role of Pesticides in Bee Health

Bees can be exposed to numerous different types of pesticides applied to field crops and other types of plants in areas where they forage or maintain their hive. In addition, beekeepers may also use pesticides registered for the control of bacteria, fungi, mites, and other bee pests. These pesticides are applied within and in the vicinity of hives. Besides the active ingredients, pesticide products include other ingredients, such as "inerts" or adjuvants that are intended to improve delivery of the active ingredient to the target pest. Others are used to increase the toxicity of a pesticide, for example, by inhibiting breakdown of a pesticide by insets.

Studies have shown that bees are exposed to pesticides in many ways throughout the foraging period: from planter exhaust material produced during the planting of treated seed; from the soil of both planted and unplanted fields; in flowers growing near these fields; as well as applications in or near bee hives. Bees also sometimes are exposed to pesticides accidentally, either when pesticides are misused or misapplied or when they are used according to label directions to control pests in areas frequented by bees—for example, alongside roads or rights of way for the control of weeds, trees, or other pests; on or near commercial farm crops; or on or near fields, lawns, and gardens to control fleas, ticks, weeds, grubs, mosquitos, or other adult insects.

Figure 2 illustrates some significant paths of bee exposure to pesticides applied as a spray or as a soil or seed treatment (systemic). If bees happen to fly through a newly treated field or dust clouds from planting of seeds coated with pesticide or are orally exposed to pesticide in food or water, and if exposure is high enough, bees may be sickened or die from pesticide exposure. With respect to the role of pesticides in honey bee health, "[t]he most pressing research questions lie in determining the true pesticide exposure that bees receive and the effect, if any, that pervasive exposure to multiple pesticides have [sic] on the health and productivity of whole honey bee colonies."

Pesticides are reported to have adverse local impacts on honey bees and some native bees. Widespread use of herbicides reduces habitat available to bees; many pesticides are known to be lethal to bees, given sufficient levels of exposure; and some reports of local bee kill incidents have been well documented. Effects on individual bees may be lethal or sublethal depending on dose and other conditions of exposure. A summary of the types of sublethal effects reported in bees exposed to pesticides includes

decreased navigation, orientation, and communication abilities; altered foraging behavior and motor activity; short- and long-term memory loss; impaired learning behavior and sensory detection; compromised immune functioning; increased susceptibility to diseases and pests; reduced fecundity (fertility and reproduction); and impaired reproduction and development.

Although pesticides have been shown to damage bee health, it is unclear whether the level of harm is sufficient to attribute pesticides as the single or as the major cause of honey bee population declines.

The Appendix provides a summary of selected scientific literature based largely on publications in peer-reviewed journals. In addition, a number of industry and advocacy groups have compiled literature reviews regarding pesticide effects on bees, not all of which are specifically discussed in this report. In general, studies looking at impacts of pesticides on other animal species, such as birds, are also not addressed.

Best Management Practices to Protect Pollinators

Best management practices (BMPs) are available for beekeepers, crop producers, and pesticide applicators and include environmentally responsible pest management practices to reduce risk and minimize pesticide exposure in bees. A number of states have also developed guidance to protect pollinators. Some of these resources are listed on the Pesticide Environmental Stewardship (PES) website and on EPA's website.

For beekeepers, guidance by apiculturists and university extension services emphasizes the importance of reducing the exposure of bees to insecticides with high toxicity, recommending that if such chemicals are used in an area where bees are foraging, steps may be necessary to reduce risk of poisoning. This involves both selecting a site for an apiary in an area with low pesticide risk and notifying "growers and applicators in the area, the county agent, and the State Apiary Inspector of the location of your hives.... If the insecticide to be used has a long residual life and is being applied to a plant where bees are foraging, it may be best to move your bees out of the area."

For growers, recommendations involve reducing the hazards associated with insecticides, including avoiding the use of dusts, such as those from treated seeds, and using chemicals with reduced risk to bees whenever possible. Other recommendations include applying insecticides "in the late evening, night, or early morning when fewer bees will be foraging, and when spray drift and volatilization due to extreme heat are at a minimum"; not spraying "when winds favor drifting, and us[ing] ground applications instead of air where possible"; and avoiding "spraying when the crop or other plants in the field or nearby (including weeds) are in bloom." Some agricultural groups provide such guidance to their growers. For example, the Almond Board of California recommends that growers avoid applying insecticides when plants are in bloom or when pollen is available and honey bees are feeding. Additional grower BMPs are listed in the text box below.

Pesticide applicator BMPs recommend avoiding pesticide use when crops are blooming and applying pesticides to blooming crops only after bees are done foraging for the day and preferably at night. Bayer Crop Science notes the importance of following pesticide label recommendations as "naturally beneficial to bees' safety," as well as cooperation between farmers and beekeepers "to optimize spray times and minimize exposure to foraging bees."

Such BMP guidance is generally voluntary. Several studies suggest, in general, adoption of voluntary BMPs is characterized by both slow adoption rates (i.e., long lead times) and long lag times between BMP adoption and observed effects; also BMP implementation tends to be mostly self-funded. Some claim therefore that reliance on voluntary agricultural BMPs regarding pesticide use and potential pollinator impacts is unlikely to produce timely behavioral changes and BMP adoption, even with a broad outreach and education program.

In response to recent bee die-offs in Canada, federal agencies there have instituted additional protective requirements when using treated seed in corn and soybean production. These include required use of safer dust-reducing seed flow lubricants; adherence to safer seed planting practices; pesticide and seed package labels with enhanced warnings; and evaluation of the need for neonicotinoid treatment on certain commercial crops. (More information on Canada's requirements is discussed in " Restrictions in Canada .")

Agro-chemical industry representatives maintain that unwanted pesticide exposure is best addressed through "effective product labeling and the implementation of meaningful stewardship actions that help minimize harmful interactions," along with "crop- and product-specific integrated pest management (IPM) practices and messaging to improve bee and pollinator safety." However, some claim that because the use of systemic insecticides applied via seed coatings is mostly "prophylactic" (i.e., applied regardless of actual pest pressure) the use of such insecticides violates basic IPM principles, which recommend minimizing use of chemical pesticides through pest monitoring, maximizing the use of biological and cultural controls, applying chemical pesticides only when needed, and avoiding broad-spectrum, persistent compounds. The text box below provides additional information on IPM practices.

Other guidance by apiculturists and university extension focuses on providing recommendations to private landowners and homeowners for proper use of pest control products on ornamental plants. One recommendation is to avoid applying any pesticides, including insecticides and fungicides, during bloom of ornamental plants that attract bees (e.g., heather, lavender, linden, rhododendron, and rose). It is also recommended that any pesticides be applied "only after flower petals have fallen, when ornamental plants are less attractive to bees," and that all specific requirements to protect bees on the pesticide label be strictly followed. If pesticides are used when plants are in bloom, those that are less toxic to bees are recommended. Some recommend using certain pesticides—including products containing clothianidin, dinotefuran, imidacloprid, and thiamethoxam—only after flower petals have fallen, and avoiding soil drench or tree injection methods when using these products for plants known to attract bees because "these methods may contaminate nectar and pollen for up to several years after the insecticide is applied," or, alternatively, recommend against buying plants treated with insecticides containing these ingredients.

Consumer campaigns have been initiated to encourage businesses and home gardening centers to stop selling certain pesticides or plants treated with these products because of concerns about the effects on bees and other pollinators. A consumer campaign initiated by the Center for Food Safety highlights that more than 60 commonly used home and garden products contain neonicotinoid pesticides and recommends that homeowners avoid certain commonly used pesticide products. In addition, concerns have been raised about the use of mosquito control services by some homeowners, because of potential adverse effects to bees and other beneficial insects that might feed on plants or be exposed to pesticides within the sprayed areas, as well as effects to species on adjacent or nearby property due to drift.

Federal Agency Efforts

National Pollinator Health Strategy ("Presidential Memorandum")

In June 2014, the Obama Administration issued its Presidential Memorandum, "Creating a Federal Strategy to Promote the Health of Honey Bees and Other Pollinators," directing federal agencies to take steps to protect and restore domestic populations of pollinators. It established a "Pollinator Health Task Force," co-chaired by USDA and EPA, with representatives of the Departments of State, Defense, the Interior, Housing and Urban Development, Transportation, Energy, and Education; among other agencies and offices.

The task force is directed to develop a National Pollinator Health Strategy, which is to include a Pollinator Research Action Plan to "focus federal efforts on understanding, preventing, and recovering from pollinator losses." Among the many activities expected to inform the action plan is "identification of existing and new methods and best practices to reduce pollinator exposure to pesticides, and new cost-effective ways to control bee pests and diseases." Task force member agencies will develop plans to increase and improve pollinator habitat. These plans may include "use of integrated vegetation and pest management," among other actions. Member agencies will also "make any necessary and appropriate changes to enhance pollinator habitat on federal lands through the use of integrated vegetation and pest management and pollinator-friendly best management practices." The task force is expected to release its National Pollinator Health Strategy in spring 2015.

In November 2014, USDA and EPA held a number of public listening sessions to inform the task force members. Concerns about pesticide use were among the major discussion points. Commercial beekeepers, environmental groups, and some food businesses continue to push for restrictions on pesticide use and question whether other factors, such as parasitic mites, are the primary driver behind bee declines. Most pesticide industry groups and commercial growers continue to encourage broader consideration beyond pesticides and claim that some alternative pesticides are more toxic than neonicotinoids.

Currently, at EPA, the agency's pollinator strategic plan outlines efforts to advance scientific knowledge and assessment of pesticide risks to pollinators; improve management tools for mitigating risks to pollinators; and increase and broaden communication and public outreach.

USDA-EPA Joint Report

In 2013, USDA and EPA published a joint report, National Stakeholders Conference on Honey Bee Health . Among the goals of the conference were to "synthesize the current state of knowledge regarding CCD, bee pests, pathogens, and nutrition, potential pesticide effects on bees, and bee biology, genetics and breeding." The report's key findings include recommendations to address risks to honey bees from parasites and disease; increase the genetic diversity in bee colonies; and improve nutrition for honey bees. In addition, regarding pesticides, the report acknowledged the following needs:

Collaboration and Information Sharing. Best management practices (BMPs) associated with pesticide use and bees are known but are not widely or systematically followed by U.S. crop producers. "Informed and coordinated communication between growers and beekeepers" is needed, along with "effective collaboration between stakeholders on practices to protect bees from pesticides." Beekeepers have identified the need for "accurate and timely bee kill incident reporting, monitoring, and enforcement." Additional Pesticide Research. According to EPA, "[t]he most pressing pesticide research questions relate to determining actual pesticide exposures and effects of pesticides on bees in the field and the potential for impacts on bee health and productivity of whole honey bee colonies."

The National Honey Bee Health Stakeholder Conference Steering Committee is made up of representatives from Pennsylvania State University; from USDA's Office of Pest Management Policy (OPMP), National Institute of Food and Agriculture (NIFA), Agricultural Research Service (ARS), Animal and Plant Health Inspection Service (APHIS), Natural Resources Conservation Service (NRCS), and National Agricultural Statistics Service (NASS); and from EPA's Office of Pesticide Programs (OPP). Much of the current research on bee health is being conducted by scientists at USDA and its Beltsville bee laboratory, by the USDA-supported Bee Informed Partnership, and by scientists at many of the land-grant universities nationwide.

Environmental Protection Agency

EPA's Pesticide Registration Review of Neonicotinoid Pesticides

Neonicotinoid pesticide registrations are being reviewed by EPA. According to EPA:

Some uncertainties have been identified since their initial registration regarding the potential environmental fate and effects of neonicotinoid pesticides, particularly as they relate to pollinators. Data suggest that neonicotinic residues can accumulate in pollen and nectar of treated plants and may represent a potential exposure to pollinators.

Adverse effects data as well as beekill incidents have been reported, highlighting the potential direct and/or indirect effects of neonicotinic pesticides. Therefore, among other refinements to ecological risk assessment during registration review, we will consider potential effects of the neonicotinoids to honeybees and other pollinating insects.

Review of several neonicotinoid pesticide registrations began December 2011, with review of imidacloprid starting a few years earlier, in December 2008 ( Table 1 ). EPA aims to review all neonicotinoids as a group.

In July 2014, the Natural Resources Defense Council (NRDC) petitioned EPA to conduct an emergency review of the impacts of neonicotinoid pesticides on bees and to complete its review within one year. At an October 2014 meeting, an EPA official indicated that the agency would move up its dates for its review of neonicotinoid pesticides from 2018-2019 to 2016-2017.

Currently, among the neonicotinoid pesticides under review, some products are being used under a "conditional" registration, while some products are being used under an "unconditional" registration. FIFRA provides that EPA register a pesticide if, among other findings, it meets the statutory standard, namely: (1) the pesticide will perform its intended function without unreasonable adverse effects on human health and the environment, and (2) the pesticide will not generally cause unreasonable adverse effects on human health and the environment when used in accordance with widespread and commonly recognized practice. Under an unconditional registration, after reviewing the data and information submitted to support an applicant/registrant's pesticide product application under consideration, if EPA determines that the pesticide meets the statutory standard and there are no outstanding data requirements, the agency may approve an "unconditional" registration. If, however, EPA finds that the pesticide meets the standard for registration, but there are outstanding data requirements, the agency may, under certain circumstances, grant a "conditional" registration. Before granting a conditional registration, EPA must determine that, although an application lacks some of the necessary data, use of the pesticide would not significantly increase the risk of unreasonable adverse effects on the environment during the time needed to generate the necessary data. A product's "conditional" or "unconditional" status is determined on a product registration by product registration basis, and not for the pesticide's active ingredient as a whole. An indication of a product's current status can be found at EPA's searchable label database.

The U.S. Government Accountability Office (GAO) has conducted studies that are critical of EPA's pesticide registration process, particularly regarding the program's conditional registrations. Environmental and other groups argue that conditional registrations are a loophole in EPA's requirements, allowing pesticides onto the market that might not otherwise be allowed under a thorough agency review. These groups further claim that EPA has overused conditional registrations and that the agency does not have a reliable data-gathering system to track conditional registrations. GAO's 2013 report states that "the total number of conditional registrations granted is unclear" due to database inaccuracies and confusion in EPA's recordkeeping system for tracking pesticides.

In the process of reviewing registrations for neonicotinoids, EPA has revised its risk assessment process "to reflect advancements in the state of the science that underlie bee exposure and effects assessments." The draft risk assessment policy was released to the public, and materials were distributed and discussed at a FIFRA Scientific Advisory Panel (SAP) meeting in September 2012. The final risk assessment guidance was released in June 2014. The guidance is founded on EPA's ecological risk assessment framework, integrates an analysis of honey bees and other pollinators within the agency's broader components of ecological risk assessment, and was prepared in collaboration with Health Canada's Pesticide Management Regulatory Authority and California's Department of Pesticide Regulation. The guidance describes the basic framework of the risk assessment process and the data used to support risk management decisions, and includes a process to assess both foliar spray applications and soil/seed treatment applications.

Some groups argue that EPA does not take into account chronic, sub-lethal effects in its risk assessments, nor synergistic effects with other compounds used in real field settings, such as fungicides, adjuvants, and inerts. These groups also claim native and wild bee species are generally not addressed as part of EPA's risk assessment. Since most native bee species (about 70%) are ground nesting, these groups further claim that the use of systemic insecticides poses risks to native bees from exposure through their habitats in the ground. Native and wild bee species are also generally not addressed as part of EPA's pesticide labeling approach (discussed in " EPA's New "Bee Advisory" Labeling Requirements ").

As part of EPA's overall review, the agency has conducted a study of the benefits of neonicotinoid seed treatments for insect control in U.S. soybean production. EPA's analysis concluded: "these seed treatments provide little or no overall benefits to soybean production in most situations. Published data indicate that in most cases there is no difference in soybean yield when soybean seed was treated with neonicotinoids versus not receiving any insect control treatment." Reportedly, EPA also studied the potential benefits of neonicotinoid seed treatments to corn production but has not published those findings. In 2013, EPA and USDA conducted a summit with stakeholders on reducing exposure to dust from treated seed and potential acute exposure of honey bees and pollinators to pesticides. Information and stakeholder presentations from the summit are at EPA's website.

EPA's Consideration to Modify Thiamethoxam Tolerance Levels

In September 2014, EPA announced that it had received "several initial filings of pesticide petitions requesting the establishment or modification of regulations for residues of pesticide chemicals in or on various commodities," including a petition by Syngenta that EPA increase the allowable threshold for residues of thiamethoxam. Syngenta's petition would apply to alfalfa, barley, corn and wheat, both the crop itself and the straw and stover left over after cultivation. According to some reports, the petition seeks to increase the tolerance levels ranging from about 1.5 times current levels for stover from sweet corn to about 400 times current levels for hay from wheat. EPA's review of this request is still pending. Thiamethoxam is one of the neonicotinoid pesticides banned for use in the European Union.

EPA's New "Bee Advisory" Labeling Requirements

In August 2013, EPA announced that it had developed new pesticide labels that prohibit use of some neonicotinoid pesticide products where bees are present. The new requirements apply to foliar applications of products containing imidacloprid, dinotefuran, clothianidin, thiamethoxam, tolfenpyrad, and cyantraniliprole. Exceptions apply under certain conditions for agricultural crops and commercially grown ornamental plants. The new labels require a "Pollinator Protection Box" (or "bee advisory," Figure 3 ) and bee icon with information on routes of exposure and spray drift precautions, as well as new language added under "Directions for Use."

The bee advisory will, among other things, alert pesticide applicators to restrictions regarding certain pesticides when bees are present; clarify that pesticides cannot be applied until all petals have fallen; and emphasize the importance of avoiding pesticide drift (for example, due to wind) to other areas where bees may be present. The new bee icon will signal the pesticide's potential hazard to bees, and warns that direct contact and ingestion can harm pollinators. Information is at EPA's website.

EPA's new labeling requirements have received mixed reviews from beekeepers, who argue that the new labels are inadequate and include exceptions that may make them less protective for bees and other pollinators. Groups, such as the Pollinator Stewardship Council, have expressed concerns about EPA's label as well as concerns about the conditions under pesticide applications would be allowed. Figure 4 shows some of this group's concern with EPA's label, including concerns that none of the terms in the label is defined and many are ambiguous (which they claim makes the requirements unenforceable), as well as the concern that the label refers applicators to a pesticide industry website, among several other issues.

Some groups, including the Pollinator Stewardship Council, have voiced concerns about EPA's exceptions to the new labeling requirements, which would allow application under certain conditions. Exceptions to the labeling requirements are as follows.

For " Crops Grown Under Contracted Pollination Services ," the label for some neonicotinoid pesticide products states: "Do not apply this product while bees are foraging" or "until flowering is complete and all petals have fallen." Exceptions are allowed for in cases where "an application must be made when managed bees are at the treatment site, the beekeeper providing the pollination services must be notified no less than 48 hours prior to the time of the planned application so that the bees can be removed, covered or otherwise protected prior to spraying."

For " Food Crops and Commercially Grown Ornamentals not Under Contract for Pollination Services But Attractive to Pollinators ," the label for some products also states: "Do not apply this product while bees are foraging" or "until flowering is complete and all petals have fallen." Exceptions are allowed for in cases where:

The application is made to the target site after sunset. The application is made to the target site when temperatures are below 55˚F. The application is made in accordance with a government-initiated public health response. The application is made in accordance with an active state-administered apiary registry program where beekeepers are notified no less than 48 hours prior to the time of the planned application so that the bees can be removed, covered, or otherwise protected prior to spraying. The application is made due to an imminent threat of significant crop loss, and a documented determination consistent with an IPM plan or predetermined economic threshold is met. Every effort should be made to notify beekeepers no less than 48 hours prior to the time of the planned application so that the bees can be removed, covered, or otherwise protected prior to spraying.

Among the expressed concerns regarding EPA's exceptions to its label advisory are:

harm caused by foliar application of the affected pesticides will be the responsibility of the beekeeper, including damage or die-off from applications allowed for under the labels exceptions; uncertainty about what constitutes notifying a beekeeper to move their bees, and concern that native bees will be harmed since they are not similarly managed; foliar application of adjacent or nearby sites may affect bees since they have a 3-mile to 7-mile forage range; exceptions to applications made when temperatures are below 55˚F may affect bees that forage at temperatures as low as 45˚F; and other labeling issues, including who decides when foliar treatments are needed, what are the criteria for determining whether treatment are needed, where should beekeepers transport bees during applications, and who determines what mitigation measures are appropriate.

Exceptions do not apply to non-agricultural crops, such as ornamental crops grown by homeowners, and the pesticide label requires that the product not be applied while bees are foraging or when plants are flowering.

EPA Support of State Pollinator Protection Plans

EPA is working with states to draft guidance on the development of EPA-approved, state-managed pollinator protection plans. Guidance is being developed by EPA's State FIFRA Research and Evaluation Group (SFIREG), and will outline a process for reviewing and accepting state pollinator protection plans as part of EPA's broader pollinator protection efforts related to pesticides. The draft guidance was presented at a December 2014 meeting of the Association of American Pesticide Control Officials (AAPCO), and contained information on the core elements for EPA-approved state pollinator plans, the process for EPA review and updating of state plans, how to reference state plans through labeling requirements, and how to access recommended best management practices. Pollinator protection plans are in place in several states, including California, Colorado, Florida, Mississippi, and North Dakota. Other states are considering similar initiatives.

EPA Development of Voluntary Controls for Pesticide Drift

In October 2014, EPA announced a new voluntary Drift Reduction Technology (DRT) program to encourage the use of verified, safer pesticide spray products to reduce exposure and pesticide movement, and also to reduce costs to farmers from pesticide loss. EPA defines pesticide spray drift as the "movement of pesticide dust or droplets through the air at the time of application or soon after, to any site other than the area intended." More information is at EPA's website. A similar effort—the DriftWatch Specialty Crop Site Registry—provides for a voluntary communication tool between crop producers, beekeepers, and pesticide applicators, and is intended to protect high-value, pesticide-sensitive crops and commodities before applying pesticides. The program is currently in use in many midwestern and mid-Atlantic states.

Fish and Wildlife Service Memorandum

In July 2014, the U.S. Fish and Wildlife Service (FWS) in the Department of the Interior announced that it would phase out the feeding of genetically engineered crops to wildlife and the use of neonicotinoid pesticides in all of its wildlife refuges by January 2016.

Initially this decision was meant to phase out the use of neonicotinoids in Region 1 only, which covers Oregon, Washington, Idaho, Hawaii, and the Pacific Islands. Under the guidelines, refuge managers will also need to comply with new mandatory requirements for all chemically treated seeds on refuge lands.

In early 2013, Representative Austin Scott, chairman of a House Agriculture subcommittee, indicated that the committee would direct FWS to undergo "a uniform risk assessment process ... when making decisions on products already approved" under FIFRA and/or the Plant Protection Act. To date, no such action has been untaken.

Other Ongoing Efforts

Restrictions in Some U.S. Cities and Counties

A number of cities and counties, among other local jurisdictions, have instituted restrictions on the use of neonicotinoid pesticides in an effort to protect pollinators. In March 2014, Eugene, Oregon, became the first U.S. city to restrict neonicotinoid use. (Despite the ban, a mass die-off of bees was reported in June 2014 at an apartment complex in northwest Eugene. It was attributed to insecticide sprayed on blooming linden trees.) Since then other cities have also instituted bans, including Seattle and Spokane in Washington; Shoreline, Minnesota; and Skagway, Alaska. Other cities and counties, such as Tucson and Pima County in Arizona, and Boulder County in Colorado, also are considering restrictions. Some state legislatures, including Alaska, California, Maryland, Minnesota, New York, New Jersey, Oregon, and Vermont, have considered legislation to further study and/or restrict neonicotinoid use. Some localities also have instituted other types of pesticide restrictions, such as with disclosure laws in the county of Kauaˋi in Hawaii. Other localities have implemented programs to encourage households and municipalities to pledge to create "pollinator-friendly, toxin-free ecosystem habitats," such as in the city and county of Denver, Colorado. Some state agencies are actively studying the issue.

In addition, several states—California, Colorado, Florida, Mississippi, and North Dakota—have state pollinator protection plans in place, and other states are considering similar initiatives. (For information, see " EPA Support of State Pollinator Protection Plans ")

Restrictions in the European Union

Like the rest of the world, the countries of the EU have experienced overwinter honey bee colony losses. As reported by the nonprofit honey bee research association, COLOSS, overwinter colony losses averaged 9% in 2013/2014, the lowest since the group began collecting such data in 2007. Across countries, losses ranged from 6% to 12%. This is lower than results reported for 2012/2013, when overwinter losses ranged from 6% to a high of 37% across all reporting countries. Another report commissioned by the European Commission and EU member states concluded honey bee colony mortalities were "better than previously expected" and "higher than normal in certain countries, with significant regional (and possibly temporal) differences."

In response to concerns about declining bee populations, in May 2013, the European Commission (EC) adopted Regulation No 485/2013 banning the use of certain neonicotinoid pesticides for a period of two years, among other proposed limits on the use of other pesticides. The regulation includes the following provisions:

use of three neonicotinoid pesticides—clothianidin, imidacloprid, and thiamethoxam—is restricted for seed treatment, soil application (granules), and foliar treatment on bee attractive plants and cereals; any authorized uses are available to professionals only; any exceptions to these restrictions are limited to treating bee-attractive crops in greenhouses or in open-air fields after flowering; and restrictions are to be maintained for two years, effective December 1, 2013.

As new information becomes available, the EC will review the approval conditions for these three pesticides and take into account relevant scientific and technical developments. Previous mitigation measures (EC Regulation No 1107/2009) restricted spraying of insecticides on bee-attractive flowering crops.

The EC's 2013 regulatory action was in response to the European Food Safety Authority's (EFSA) scientific assessment that identified "high risks for bees for some uses of three neonicotinoids (imidacloprid, clothianidin and thiamethoxam) and fipronil," such that "the approval criteria of these pesticides were no longer satisfied." Regarding the three restricted pesticides, EFSA identified "high acute risks" for bees from exposure to pesticides associated with the production of several crops such as corn, grains, and sunflower, as well as exposure to residue in pollen and nectar in certain crops.

The EU Commission has further proposed to restrict the use of fipronil, an insecticide which EFSA has identified as posing an acute risk to Europe's honey bees when they are exposed to seeds treated with the chemical.

Other reports, such as a study published by the United Kingdom's Department for Environment, Food and Rural Affairs (DEFRA), dispute some of the findings linking bee health and exposure to neonicotinoids. Other studies also highlight the likely multifaceted nature of possible factors contributing to pollinator declines. Researchers in Europe continue to study this issue and reportedly are in the process of completing a large-scale study reviewing the landscape-scale effects of neonicotinoid use on crops. Some member state officials are also questioning the ban and its possible effects on agricultural production.

Restrictions in Canada

In Canada, the Canadian Association of Professional Apiculturists (CAPA) reports that overwinter honey bee colony losses in 2013/2014 averaged 25% across Canada, but some provinces, such as Ontario, reported wintering losses of 58% . In addition, in 2012, Health Canada's Pest Management Regulatory Agency (PMRA) began reporting higher bee mortalities associated with pesticide applications in some areas as part of its pesticide incidents reporting.

In April 2012, PMRA reported a "significant number of honey bee mortality reports" in the provinces of Alberta, Manitoba, Saskatchewan, Nova Scotia, Quebec, and Ontario. Most reports were from southern Ontario, involving more than 40 beekeepers and 240 different locations, with also one report from Quebec involving eight bee yards. Health Canada concluded "an unusually high number of reports of honey bee mortalities were received from beekeepers in corn growing regions of Ontario and Quebec.... Timing and location of these honey bee mortalities appeared to coincide with planting corn seed treated with insecticides."

PMRA's preliminary findings conclude "there is an indication that pesticides used on treated corn seeds may have contributed to at least some of the 2012 spring bee losses that occurred in Ontario." The agency continued to "receive a significant number of pollinator mortality reports from both corn and soybean growing regions of Ontario and Quebec, as well as Manitoba" in spring 2013. A 2013 field study by researchers at the University of Guelph reported no link between bee health and pesticide applications.

Following this investigation, PMRA determined that "current agricultural practices related to the use of neonicotinoid treated corn and soybean seed are affecting the environment due to their impacts on bees and other pollinators." The agency implemented measures to reduce honey bee exposure to dust generated during planting of treated corn seed, including "communication of best practices to reduce the exposure of honey bees, labelling of treated seed, a treated seed dust standard, and development of technical solutions to reduce dust, including developments in the areas of seed coating quality, seed flow lubricants, planting equipment, and disposal of treated seed bags." For the 2014 planting season, PMRA issued additional protective measures for corn and soybean production. PMRA has continued to re-evaluate nitro-guanidine neonicotinoids to determine if further regulatory action was needed. PMRA is reportedly also planning to implement label changes similar to those being considered by EPA in the United States (see " EPA's New "Bee Advisory" Labeling Requirements ").

In November 2014, the province of Ontario announced a proposal to reduce the use of neonicotinoid-treated corn and soybean seed (based on acreage of treated seeds planted) by 80%. If approved, the new regulations would go into effect by July 1, 2015, prior to the 2016 planting season. Manufacturers of the chemicals claim the decision is not supported by science. The Canadian industry association, CropLife Canada, is also urging the Canadian government to broaden its examination of bee population declines beyond pesticides and neonicotinoids. The Canadian government continues to study this issue.

In September 2014, two large beekeeping operations filed a class-action lawsuit on behalf of Canadian beekeepers against several chemical manufacturers, claiming thiamethoxam (and its predecessor, imidacloprid) and its breakdown product clothianidin led to more than C$450 million (about US$410 million) in total damages from 2006 to 2013. The alleged chronic effects of the use of these pesticides include "bee deaths; impaired reproduction; immune suppression; behavioral abnormalities resulting in hive loss; reduced honey production; impacts on the quality of honey; contamination of hive equipment; loss of queen bees; breeding stock; and difficulties fulfilling honey product or pollination contracts." The lawsuit alleges that Bayer and Syngenta were "negligent in their design and development of the neonicotinoid pesticides," and were and continue to be "negligent in their distribution and sale of the neonicotinoid pesticides," as well as "negligent in permitting or failing to prevent the damages caused by the neonicotinoids to the beekeepers." The plaintiffs further claim that Bayer and Syngenta "knew or ought to have known that the neonicotinoids would cause damage to the property" of beekeepers, since they allege that the harm to the beekeepers was "reasonably foreseeable."

Legal and Other Actions by Some Interest Groups

Selected Actions by Environmental Groups

A number of environmental and food safety advocacy groups, along with individual beekeepers, have remained active in pressing federal and state authorities on policies and issues pertaining to the approval and use of neonicotinoid pesticides, among other agrochemicals. Among these are the Center for Food Safety (CFS); Earthjustice; Pesticide Action Network North America (PANNA); Beyond Pesticides; Friends of the Earth; Sierra Club; and the Center for Environmental Health. These groups have published a series of widely available reports supporting their policy positions and/or have posted literature reviews on their organization's websites, and also have undertaken a series of legal challenges in these matters.

In March 2013, CFS and a coalition of four beekeepers and five environmental and consumer groups filed a lawsuit against the EPA to stop the use of pesticides containing clothianidin and thiamethoxam, which beekeepers in the case claim is damaging the central nervous system of their bees. The lawsuit also challenges EPA's risk assessment framework for determining whether pesticides harm pollinators and questions EPA's approval of certain neonicotinoids. An opening brief was filed in December 2013 further challenging EPA's risk assessment framework and requesting that the court reverse EPA's decision to register sulfoxaflor. In July 2014, CFS, Earthjustice, PANNA, and Beyond Pesticides challenged California's approval of new agricultural uses for two neonicotinoid pesticides, Venom Insecticide and Dinotefuran 20SG.

Previously, in 2005, two beekeepers residing in Minnesota sued the state's Department of Natural Resources for losses incurred from spraying of a pesticide, carbaryl. In that case, the pesticide users reportedly offered to settle, and the state's Department of Natural Resources stopped using the pesticide.

These legal challenges follow previous requests for EPA to restrict the use of certain pesticides. In a March 2012 citizen petition, CFS and a coalition of beekeepers along with PANNA filed an "Emergency Petition" with EPA asking for a suspension of the use of clothianidin until it is proven safe to pollinators and the environment. EPA responded in part to the petition in July 2012. A few weeks later, EPA announced that it was denying the request to suspend registrations "to prevent imminent harm" because the petitioners did not meet the burden of proof for registration suspension. However, EPA received public comments on this decision and may revisit its decision as it reviews neonicotinoid registrations. Again, in July 2014, NRDC petitioned EPA to conduct an emergency review of the impacts of neonicotinoid pesticides on bees, and to complete its review within one year. For more information, see " EPA's Pesticide Registration Review of Neonicotinoid Pesticides ."

In June 2013, a coalition of advocacy groups, including CFS, sent a letter to President Obama asking him to order EPA to ban use of neonicotinoid insecticides for at least two years. The letter asserts that the registration process lacks consideration of pesticide effects on colonies and focuses exclusively on acute mortality, rather than on sublethal effects of repeated exposure. Another letter followed in January 2015 from commercial beekeepers, environmental groups, and some food businesses, who continue to push for restrictions on pesticide use.

Selected Actions by Agrochemical Companies

Some major agrochemical companies—in particular, Syngenta AG (a global Swiss agribusiness company) and Bayer AG (a global German company)—have been actively engaged in defending the use of neonicotinoid pesticides, among other agrochemicals, and claim there is no evidence to support a systematic correlation between honey bee colony mortality and the use of neonicotinoids. Bayer's bee care pamphlet claims "poor bee health is correlated with the presence of Varroa , a parasitic mite, viruses and many other factors, but not with the use of insecticides." These companies and other industry groups, as well as the trade association CropLife Amercia, have published commissioned reports supporting their policy positions, and have supported various pollinator health as well as lobbying efforts.

According to news reports, both Syngenta and Bayer are legally challenging the EU's neonicotinoid ban. Syngenta claims these pesticides are not responsible for the pollinator population declines, which they claim are instead the result of disease, viruses, habitat loss, and poor nutrition. According to reports, Syngenta wants to reverse the EU ban but also wants to be compensated for damages and "defend our reputation which has been significantly damaged." Syngenta claims the EU's decision to ban the pesticides is based on "a flawed process, an inaccurate and incomplete assessment by the European Food Safety Authority and without the full support of EU Member States."

Syngenta also has petitioned EPA to increase the allowable threshold for residues of thiamethoxam. EPA published its proposal in September 2014.

Congressional Consideration

Given continued concerns about the health and well-being of honey bees and other pollinators, this issue has continued to be legislatively active. The 2014 farm bill ( P.L. 113-79 ) reauthorized and expanded provisions supporting research on honey bees and other pollinators that were enacted in the 2008 farm bill. In previous Congresses, bills were introduced to promote and improve habitat for honey bees and wild bees, among other pollinators. Still other introduced legislation would address a range of pesticide issues affecting pollinators. Over the past few years, Congress has conducted hearings on this issue and hosted a series of congressional briefings to discuss these and related issues representing a broad range of interested groups.

For the 114 th Congress, Representative Rodney Davis, the incoming chairman of the House Agriculture Subcommittee on Biotechnology, Horticulture, and Research, is quoted as saying that bee health will be a top issue for his subcommittee.

Saving America's Pollinators Act

In the 113 th Congress, Representatives Earl Blumenauer and John Conyers Jr. introduced H.R. 2692 , the Saving America's Pollinators Act of 2013. The bill would have suspended registrations of neonicotinoids and banned new registrations of any pesticide for use on "bee attractive plants, trees, and cereals." This bill was initially introduced, in part, as a response to reports that 50,000 bees were found dead in a suburban shopping-center parking lot in Wilsonville, Oregon, in June 2013, reportedly due to exposure to pesticides used on trees near the parking lot to control aphids.

Specifically, the bill would have required EPA to "suspend the registration of imidacloprid, clothianidin, thiamethoxam, dinotafuran, and any other members of the nitro group of neonicotinoid insecticides to the extent such insecticide is registered, conditionally or otherwise," under FIFRA (7 U.S.C. 136 et seq.) "for use in seed treatment, soil application, or foliar treatment on bee attractive plants, trees, and cereals."

These suspensions on existing registrations and restrictions on new registrations would remain until more research is conducted and EPA determines that the insecticide will not cause "unreasonable adverse effects" on pollinators, including honey bees, native bees, and other pollinators. Such an assessment would be based on an evaluation of the published and peer-reviewed scientific evidence and a completed field study. The bill also would have required the Department of the Interior to coordinate with EPA in monitoring the health and populations of native bees, and annually report to Congress on their health and population status.

H.R. 2692 was similar to proposals being implemented or considered in the EU and Canada. In particular, the bill's language regarding "bee attractive plants, trees, and cereals" is similar to that under the EU's ban of the use of three neonicotinoid pesticides—clothianidin, imidacloprid and thiamethoxam—for "seed treatment, soil application (granules) and foliar treatment on bee attractive plants and cereals." However, the EU's restrictions provide for certain exceptions (such as greenhouses and open-air fields after flowering), which are not provided for in H.R. 2692 . (See " Restrictions in the European Union " for additional information on the EU's ban.)

In September 2014, the sponsors of H.R. 2692 , along with 58 other Members of the U.S. House of Representatives, sent a letter to EPA urging the agency to "restrict and/or suspend the use of neonicotinoids on bee-attractive crops and ornamental application," including restricting the "times, methods of application, and location" for use of these pesticides, as well as urging EPA to review its policies related to EPA's pesticide registration, among other recommendations. EPA received a similar letter from many environmental and sustainable agriculture organizations, including CFS, Friends of the Earth, Food and Water Watch, and other groups.

Groups opposed to restrictions on pesticide use contend that comprehensive studies "challenge unsubstantiated claims against pesticides as a significant cause of colony decline" and note that "infrequent accidental exposures are not indicative of the general health of honey bee colonies." Some further claim "there is no evidence linking neonicotinoids to bee declines" or to adverse health effects on bees. They generally challenge studies that target neonicotinoids as the sole factor contributing to pollinator declines, and further maintain that unwanted pesticide exposure may be best addressed through "effective product labeling and the implementation of meaningful stewardship actions that help minimize harmful interactions." Others question whether crop-applied pesticides pose a major risk to bees, given current approved uses and beekeeping practices.

Expedited Pesticide Registration for Managing Parasitic Pests

In the 113 th Congress, Representative Austin Scott introduced H.R. 5447 , which would have amended U.S. pesticide laws (FIFRA; 7 U.S.C. 136a(c)(10)) to provide for expedited registration of pesticides that "improve managed pollinator bee health, including managing resistance to parasitic pests" and for expedited review of a pesticide registration that is "reasonably expected to improve the health of managed pollinator bees, including managing resistance to parasitic pests of managed pollinator bees," such as miticides. H.R. 5447 would have also required reports to Congress from both USDA and EPA. The report required from USDA would address the "extent and scope of the threat to the health of managed pollinator bees" from pathological factors (such as the parasitic mite, Varroa destructor ; other arthropod pests; and fungal, microbial, and viral diseases) and from environmental factors (including habitat, forage, beekeeper practices and husbandry, and nutritional needs of managed bees). The report required by EPA would address the availability of pesticides to manage parasites and also EPA's efforts to expedite approvals of new products to control parasites of managed bees. The bill would have defined "managed pollinator bee" to mean "any bee that is raised and housed in a managed hive or other appropriate housing and used for honey production, managed pollination of crops, or breeding for commercial purposes." The bill was supported by some U.S. crop producers and other industry groups.

Some advocacy groups were opposed to H.R. 5447 and contend that "fast-tracking pesticide approvals" has contributed to current concerns involving bees and pesticides. They further complain that focusing attention on other factors contributing to bee declines (such as mites) tends to shift attention away from remedies that could address beekeeper concerns about pesticide exposure, such as instituting agricultural best management practices (BMPs) that might avoid application of insecticides during bloom, and minimize exposure to bees by avoiding applications when pollen is available and bees are feeding.

In February 2015, EPA announced its intentions to fast track approval of oxalic acid dihydrate for use as a miticide in beehives. Oxalic acid has been used against varroa mites and is generally considered more safe compared to other higher risk chemicals. It has been approved for use in Canada since 2010, where a government analysis there claims: "An evaluation of available scientific information found that under the approved conditions of use the product has value and does not present an unacceptable risk to human health or the environment."

Appendix. Review of the Scientific Literature169

Following is a summary of selected scientific literature based largely on publications in peer-reviewed journals.

Bee Exposure to Pesticides

Researchers at USDA and others found that "high levels" of fungicides were present in both crop and non-crop pollen collected by bees, and that "real world pollen-pesticide blends affect honey bee health." These scientists found very high levels of the fungicide chlorothalonil in pollen and wax, and found high levels of at least four insecticides, three other fungicides, and an herbicide. Chlorothalonil and the two miticides, fluvalinate and coumaphos, were most frequently detected in pollen and wax. A 2010 study tested samples of beebread, trapped pollen, brood nest wax, beeswax foundation, and adult bees and brood and found a broad range of pesticides, including acaricides (which kill arachnids like spiders, ticks, and mites), fungicides, insecticides, and herbicides.

Bees can be exposed to neonicotinoids in many ways. One study identified multiple routes of exposure to low levels of neonicotinoids for honey bees living and foraging near agricultural fields planted with corn or soybeans. The highest potential exposure to the pesticides appeared to occur during planting season, when bee mortality was also high. Clothianidin was found in about half the bee-collected pollen sampled, thiamethoxam (which is quickly metabolized to become clothianidin) in 3 of 20 samples, and fungicides in all pollen samples. Levels of clothianidin in some pollen were high enough to kill bees. Clothianidin was detected in all dead and dying bees but in no healthy bees. Although corn is not an insect-pollinated crop, this research demonstrated that bees forage for corn pollen and take it back to the hive. About half the hive pollen sampled came from corn in this study. In addition, the study documented high levels of pesticide in exhaust material from mechanical planters when pesticides and talc were used to coat seeds, and found clothianidin in soil samples from planted and unplanted fields.

Other studies have measured neonicotinoids in pollen and nectar of canola (rape seed), corn, and sunflowers grown from seed coated with pesticides. Levels found were below those known to be acutely toxic. Other studies have found that imidacloprid and thiamethoxam concentrations in nectar were greater in squash and pumpkin flowers when insecticide was applied to the soil than they were in canola and sunflowers grown from seed treated with neonicotinoids. Researchers also found metabolites of imidacloprid and thiamethoxam (clothianidin) in all parts of squash plants, along with the parent compound.

A 2012 study found levels of neonicotinoids in bee-collected corn pollen that were similar to levels of imidacloprid determined by other scientists to have sublethal effects potentially affecting colony health. Similarly, a subsequent study in 2013 found that imidacloprid levels in pollen gathered from bees in the field were high enough to cause sublethal effects on honey bees and bumble bees, based on laboratory research. A 2013 study by the European Food Safety Agency (EFSA) of three neonicotinoid pesticides—imidacloprid, clothianidin, and thiamethoxam—determined that bees faced several risks including exposure to pollen and nectar, dust, and guttation fluid from maize.

Another potential source of exposure was suggested by another 2012 study, showing that bees might be exposed to neonicotinoids in the corn syrup they are sometimes fed during the winter by beekeepers. However, the researchers did not sample corn syrup actually fed to bees, but rather showed that bees would consume sufficient imidacloprid to produce toxic sublethal effects if they were provided contaminated corn syrup in the hive. Other research found no pesticides in samples of high-fructose corn syrup obtained from three major suppliers.

Pesticide Effects on Bee Health

According to research cited in a 2007 study by the National Research Council (NRC), "the application of pesticides, especially insecticides used to control crop pests, kills or weakens thousands of honey bee colonies in the United States each year." Nevertheless, the study concluded that local bee kills "likely have not contributed significantly to the recent national decline in colony populations" [emphasis added].

Recent studies have begun to identify mechanisms by which some chemical interactions occur. For example, some fungicides may inhibit an enzyme that bees need to detoxify miticides. However, further research is needed since measurement difficulties continue to complicate study of this issue, including difficulty testing the in-field or field-realistic doses; effects at different life stages; how to account for cases of accidental exposure or exposure to multiple different types of pesticides; and how to account for species diversity (e.g., between honey bees and native bees), differences in nutritional needs/access and nesting sites, biological organization, and floral specialization.

Generalizations about the relative importance of pesticides for global bee health cannot be drawn from available data, given the disparate study designs and results. Moreover, research has been and continues to be conducted, with most scientists focusing on a single pesticide or pathogen at a time. Consideration of interactions has been minimal—whether exposure from different types of chemicals or exposure from chemicals in combination with other factors. One study explains:

Attempts to correlate global bee declines or CCD with increased pesticide exposures alone, have not been successful to date.… Pesticide interactions among various mixtures as well as with other stressors including Varroa and Nosema , IAPV, beneficial hive microbes, and impacts on bee immune systems all require further study. It seems to us that it is far too early to attempt to link or to dismiss pesticide impacts with CCD.

The study noted that the doses of individual pesticides found in bees were not concentrated enough to be lethal, but the authors remained concerned about possible chronic problems caused by long-term exposure and possible additive or synergistic effects of exposure to the combinations of pesticides found. For example, numerous pesticides classified as pyrethroids that were found in the field have been shown to cause disorientation in honey bees.

It is important to note that virtually all information about pesticide risks to bees derives from studies in cultivated fields or laboratories. There is little or no information about the possible impacts on bee populations of pesticides applied by homeowners (for example, to control mosquitos) or to ornamental plantings.

Nevertheless, a sizeable and growing body of scientific research presents compelling evidence suggesting that pesticide exposure may be harmful to bees and other animal species. For example, a 2014 meta-analysis covering 800 peer-reviewed reports over two decades examined the reported effects of systemic pesticides on ecosystems and a range of animal species—terrestrial invertebrates, including insect pollinators; aquatic invertebrates; and birds. The analysis, conducted by entomologists and ornithologists based in Europe, concluded that neonicotinoid pesticides "pose a serious risk to honeybees and other pollinators such as butterflies and to a wide range of other invertebrates such as earthworms and vertebrates including birds."

In response to reports that honey bees are disappearing and causing hives to collapse, recent studies of the impacts of exposure to imidacloprid and other neonicotinoids have focused more on their potential to affect complex behaviors in insects, including flight, navigation, olfactory memory, recruitment, foraging, and coordination. One study reported sublethal effects of neonicotinoid pesticides on honey bee foraging behavior that may impair the navigational and foraging abilities of honey bees. Another study found a reduction of foraging activity and homing behavior of honey bees exposed to treated crops at certain exposure levels of neonicotinoids.

Scientists at Bayer Crop Science argue with the findings of these and other studies, claiming that the dose of pesticide delivered to bees in some studies is not "field-relevant," resulting in findings obtained "under artificial conditions" and "in conflict with" earlier studies. Some of the statements made in the 2012 Bayer Crop Science review of the scientific literature have been rebutted by researchers at Purdue University and Pennsylvania State University, based on comments submitted by the Center for Food Safety as part of EPA's public rulemaking docket. Among a list of concerns regarding various statements in the Bayer Crop Science report, Professor Frazier from Pennsylvania State University states: "To object to a specific dose on the basis of an estimated level without giving the reader the actual basis for this neglects not only good science protocol, but also obfuscates any arguments." Among other comments, Professor Krupke from Purdue University further acknowledges: "These data suggest that there is a strong likelihood that the neonicotinoids thiamethoxam and/or clothianidin were responsible for the bee kills we investigated."

EPA has determined that clothianidin "has the potential to be highly toxic on both a contact and an oral basis" to honey bees. EPA also has reported that one honey bee field study submitted to the agency indicates that "mortality, pollen foraging activity, and honey yield were negatively affected by residues of clothianidin," but the residue levels causing the effect were not reported. Acute effects also have been demonstrated in another field study. It showed that honey bees can be killed by exposure to pesticide-contaminated talc if they fly through dust clouds associated with planting, but mortality appears to depend on high levels of humidity. Health Canada has concluded that corn planting also was implicated in bee mortalities in Ontario during the spring planting season in 2012.

Research has shown that honey bee exposure to sublethal levels of pesticides, including neonicotinoids, exhibit impaired brood development, impaired olfactory associative behavior, and impaired homing ability. Exposure to sublethal levels of neonicotinoid has also been associated with higher rates of Nosema infection, and also reduced immune functioning in those bees infected, making bees more susceptible to viral infections. In another study, responsiveness to sucrose and the bee's "waggle dancing" abilities were adversely affected when honey bees ingested imidacloprid. Another study alternatively fed honey bee hives corn syrup treated with imidacloprid, while other hives were fed untreated corn syrup. After 6 months, nearly all the treated hives collapsed, while the untreated control hives remained healthy. Another study showed that imidacloprid ingestion by larvae of the stingless bee ( Melipona quadrifasciata anthidioidides ) resulted in decreased survival rates, negatively affected development of a specific region of the bee brain, and impaired walking behavior of newly emerged adult worker bees.

A 2013 study found that exposure to a combination of an insecticide (imidacloprid) and a miticide (coumaphos) impaired learning and memory formation, important behaviors involved in foraging, in honey bees exposed under "field-realistic concentrations." A similar study also showed cognitive impairments from exposure to these same pesticides. Studies also have found increased honey bee susceptibility to and mortality from Nosema after exposure to sublethal concentrations of some pesticides (fipronil, amitraz, fluvalinate, chlorothalonil, pyraclostrobin, and imidacloprid). Another study concluded that high levels of the fungicide chlorothalonil in pollen and wax may be associated with entombing behavior, a sign that a hive has been poisoned. These and other pesticides commonly used to control mites have also been shown to have toxic effects on developing honey bee larvae at levels currently found in hives.

A 2014 study reported linkages between CCD and sublethal exposure of neonicotinoid pesticides—imidacloprid and clothianidin—which affected the winterization of the bees, comparing exposed bee colonies to a control of non-exposed bee colonies. In the study, one-half the bee colonies exposed to neonicotinoids exhibited symptoms resembling CCD and had abandoned their hives during the winter, whereas one-sixth of the control colonies were lost exhibiting Nosema ceranae symptoms. The control colonies did not abandon their hives but re-populated quickly; the surviving exposed colonies were small and either without queen bees or had no brood, according to the study. Some have criticized this study for its small sample size, lack of replication at each location, and the use of pesticide doses that may not reflect realistic field conditions.

Researchers at USDA and affiliated bee laboratories at land grant universities throughout the United States continue to study the effects of neonicotinoids and other pesticides, including the effects of interactions between pesticides and other stressors. Some of these studies demonstrate that exposure by bees to certain pesticides and/or combinations of insecticides (e.g., neonicotinoids with miticides) may affect the bee's overall energy budget, including its metabolism, physical activity, digestion, and immunity; cause other types of physiological effects; and affect different parts of the bee's nervous system, depending on the type or combination of insecticides studied among other variables, including diet and nutrition.

A few studies have examined the effects of pesticides on various species of bumble bees. One study found that bumble bee exposure to imidacloprid may affect bee brain functioning, as well as colony growth and nest conditions. Another study found that bumble bee colonies exposed in a laboratory to low levels of imidacloprid had a significantly reduced growth rate and an 85% reduction in queen production relative to untreated colonies. Other studies have found that exposure of neonicotinoids could adversely affect foraging behavior, reproductive success, and locomotor behavior. Another study showed effects following direct contact with a range of pesticides, including shortened life spans and inability to produce brood in worker bees; however, some pesticides and all fungicides tested reportedly did not result in sublethal effects. Yet another study reported no adverse impacts on brood production or other sublethal effects on bumble bees from exposure to the neonicotinoid thiamethoxam. One study showed that chronic exposure to two pesticides, one a neonicotinoid, at concentrations close to those found in fields "impairs natural foraging behavior and increases worker mortality leading to significant reductions in bumblebee brood development and colony success." Bayer Crop Science argues that the results of some of these studies were also obtained "under artificial conditions and are in conflict with" earlier studies.

A 2013 study examining the health of bumble bee colonies placed near crops treated with neonicotinoids were inconclusive due to weather and insufficient data, underlining the need to conduct further field studies that complement laboratory studies. Some cite this study as evidence against the need to impose restrictions on the use of neonicotinoid pesticides, while others criticize some of the study's published sources and research methodologies.