The Effects of Neonicotinoid Insectcides on Bee Pollinators

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Table of Contents

Abstract

I. Introduction

II. Background

A. Neonicotinoid Insecticides

1. Systemic Nature.

2. Use on Insect Pests.

B. Methods of Neonicotinoid Application

C. Routes of Exposure

D. Levels of Exposure

1. Lethal toxicity.

2. Sublethal Effects.

III. Effects of Neonicotinoids on Bee Pollinators

A. Immunity and Colony Collapse Disorder.

B. Learning and Memory.

C. Foraging and Homing Flights.

D. Reproduction.

IV. Policies to Protect Pollinators

A. California Pesticide Regulation

B. Policy Recommendations

V. Conclusion

VI. References

Abstract

Neonicotinoids, a class of insecticides, are widely used around the world to protect against crop pests. Over the past two decades, the negative effects of neonicotinoids on pollinator pollinations, most notably on bees such as the economically important western honeybee species (Apis mellifera), have been a growing public concern. Neonicotinoids target the central nervous system of insects, demonstrating impaired behavioral and physiological traits on bees. This paper briefly explains neonicotinoids, discusses their prevalent insecticide use, and reviews literature examining the risks that neonicotinoids pose to pollinators at the individual and colony level. International, federal, and state approaches are then examined to determine policy actions and recommendations to reduce the harmful exposure of neonicotinoids to bee populations.

I.       Introduction

Flowering or seed-producing plants, otherwise known as angiosperms, perform a critical role in natural and agricultural ecosystems by supplying food, fiber, and shelter for wildlife and humankind (Calderone, 2012). For hundreds of thousands of angiosperms, pollination is a vital step in the reproductive process. Without adequate pollination, a plant will produce flowers with decreased fitness, hold fewer seeds, and produce fruit at a lower market value (Calderone, 2012). While pollination can result from abiotic factors, such as wind and water, or animal activity, most angiosperms rely primarily on insects for pollination (Calderone, 2012). For this reason, insect pollination is critical for the survival of fruitful angiosperms and ultimately results in healthy ecosystems and global food security.

Recent findings propose that bee pollination increases crop yields and the quality of agricultural products by improving shelf life, nutrient content, and appearance (Björn K. Klatt, 2016). Unfortunately, ongoing anthropogenic impacts on the environment threaten biodiversity and critical ecosystem services, such as bee pollination (Vanbergen & Initiative, 2013). For example, industrial development and intensive modern agricultural practices impact insect pollinators. In fact, the increasing use of pesticides in modern agriculture has been a concern since the 1970s (Vanbergen & Initiative, 2013).

Recently, research and public policies focus on the effects of neonicotinoid insecticides on bees, a non-target species. While pollinating insects and bees are beneficial to modern agriculture, the presence of neonicotinoids in agricultural fields increasingly threaten the populations of pollinating insects through various routes of exposure (Kessler et al., 2015). Currently, both managed and native pollinator populations are declining worldwide, while agricultural demands for insect pollination surpass available capacity (Sandrock, Tanadini, Tanadini, et al., 2014). Thus, it is critical to analyze the effects of neonicotinoid insecticides have on pollinators.

Honeybees, bumblebees, and solitary bees—the most widespread and economically valuable group of pollinators—provide approximately 35% of food crop production in the world (Blacquiere, Smagghe, van Gestel, & Mommaerts, 2012). The honeybee, Apis mellifera, is the dominant managed pollinator, providing at least 90% of commercial pollination worldwide (Budge et al., 2015). In addition to honeybees, wild pollinators are important to biodiversity in natural ecosystems, but unfortunately are also threatened by various stressors, including pesticide use (Barbosa, Smagghe, & Guedes, 2015). Although the public focuses on honeybees and their importance to the economy, wild pollinators can perform just as well, if not better than the honeybee (Sandrock, Tanadini, Pettis, et al., 2014). In fact, the response to honeybee losses have resulted in some species of wild pollinators being used for managed pollination services (Sandrock, Tanadini, Pettis, et al., 2014). Despite the importance of other bee species, including wild bees and solitary bees, most studies focus specifically on the effects of neonicotinoids on honeybee populations. For this reason, this review is centered mostly on honeybees, while also highlighting recent studies on other species.

II.    Background

A.    Neonicotinoid Insecticides

Neonicotinoids, first introduced in the early 1900s, are the most widely-used class of insecticides in the world (Jeschke, Nauen, Schindler, & Elbert, 2011). Neonicotinoid insecticides represent several subclasses of neonicotinoid: (1) imidacloprid, (2) acetamiprid, (3) clothianidin, (4) thiamethoxam, (5) thiacloprid, (6) dinotefuran, and (7) nitenpyram (Elbert, Haas, Springer, Thielert, & Nauen, 2008). By 2008, neonicotinoids made up nearly a quarter of the global insecticide market (Simon-Delso et al., 2015), with over 120 countries registering the use of neonicotinoids for the management of insect pests (Bonmatin et al., 2015).

The rate of neonicotinoid use is steadily increasing alongside an increasing demand for pollination (Furlan & Kreutzweiser, 2015). Though studies assert that neonicotinoids provide a valuable mechanism for managing some of the most damaging crops, especially the order Hemiptera (aphids, whiteflies, and planthoppers) and Coleoptera (beetles) (Nauen & Denholm, 2005), other studies claim that neonicotinoid use is not superior to other insecticides and methods. For example, the U.S. Environmental Protection Agency (U.S. EPA) concluded that there is little to no benefit of neonicotinoid seed treatments on soybean production (United States Environmental Protection Agency, 2014). While other insecticides share the public spotlight due to their negative effects on pollinators (e.g., organophosphates, pyrethroids, and fipronil), neonicotinoids remains on the forefront of public concern due to their widespread use and systemic nature (Bonmatin et al., 2015).

1.      Systemic Nature.

Unlike other currently popular insecticides, a distinguishing characteristic of neonicotinoids is their systemic nature. Neonicotinoids are small molecules and highly water soluble, which allows the compounds and their metabolites to circulate throughout the plant tissues (Elbert et al., 2008). The circulation of neonicotinoid compounds occurs via xylem transport, which carries sap fluid (water and nutrients) throughout the plant (Elbert et al., 2008). As a result, systemic transportation protects the plant against sap-feeding arthropods and allows for a wide variety of application methods. However, there is a downside to the systemic nature of neonicotinoids. Their systemic nature allows neonicotinoids to infiltrate a flowering plant’s pollen, nectar, and guttation fluids (xylem sap) through translocation (Elbert et al., 2008). Thus, forager bees that come into contact with affected plants are exposed to neonicotinoids and may transport contaminated pollen and nectar back to the hive where neonicotinoid insecticides are often detected in honey and bee bread (Brandt, Gorenflo, Siede, Meixner, & Buchler, 2016).

2.      Use on Insect Pests.

An additional feature of neonicotinoids is their ability to act specifically on insect pests, while having a relatively low toxicity to vertebrates compared to other currently used classes of insecticides (Nauen & Denholm, 2005). As agonists of nicotinic acetylcholine receptors (nAChRs), neonicotinoids act like nicotine and attack the central nervous system (CNS) of invertebrates. However, unlike nicotine, neonicotinoids are selective towards invertebrates and do not pose a risk to mammals (Nauen & Denholm, 2005). Although these properties are advantageous for crop protection and the protection of many vertebrates, they also increase the probability for environmental contamination and exposure to non-target organisms, such as pollinators (Bonmatin et al., 2015).

The development of neonicotinoid insecticides has provided

growers with invaluable new tools for managing some of the world’s most destructive crop pests, primarily those of the order

Hemiptera (aphids, whiteflies, and planthoppers) and Coleoptera (beetles), including species with a long history of resistance

to earlier-used products.

The development of neonicotinoid insecticides has provided

growers with invaluable new tools for managing some of the world’s most destructive crop pests, primarily those of the order

Hemiptera (aphids, whiteflies, and planthoppers) and Coleoptera (beetles), including species with a long history of resistance

to earlier-used products.

The development of neonicotinoid insecticides has provided

growers with invaluable new tools for managing some of the world’s most destructive crop pests, primarily those of the order

Hemiptera (aphids, whiteflies, and planthoppers) and Coleoptera (beetles), including species with a long history of resistance

to earlier-used products.

The development of neonicotinoid insecticides has provided

growers with invaluable new tools for managing some of the world’s most destructive crop pests, primarily those of the order

Hemiptera (aphids, whiteflies, and planthoppers) and Coleoptera (beetles), including species with a long history of resistance

to earlier-used products.

B.     Methods of Neonicotinoid Application

Neonicotinoids may be applied in several ways. A few examples of neonicotinoid application include foliar sprays, soil drenches, trunk injections to trees, and seed treatments. The dominant methods of application are seed and soil treatments, attributing to approximately 60% of all neonicotinoid applications globally (Bonmatin et al., 2015). Such applications are considered a “safer” option because seed and soil treatment reduces pesticide drift, therefore minimizing impacts to non-target organisms. However, in the process of planting the seeds, honeybees are at the greatest risk of exposure. Specifically, honeybee exposure to neonicotinoids has been linked with the sowing of treated seeds, and there has been concern regarding the potential routes of exposure during and shortly after the planting period (Bonmatin et al., 2015).

C.    Routes of Exposure

Pollinators are directly and indirectly exposed to pesticides by many of the methods of neonicotinoid application. For example, exposure can occur from the dispersion of drift droplets during the foliar spraying of crops, inhalation of pesticides during or after application, drinking from field waters contaminated with pesticides, dust from seed sowing during or after planting, and residues present in pollen, wax, nectar, honey, and guttation drops. In honeybees specifically, direct contamination can occur during treatment of the combs (Sanchez-Bayo & Goka, 2014).

Neonicotinoids have been detected in samples of wild flowers gathered shortly after the planting of commercial fields, which suggests contamination of planter dust (Stewart et al., 2014). One research study reports chronic levels of exposure on agricultural maize fields, which suggests exposure is greatest during the planting period when exceptionally high neonicotinoid concentrations in waste talc are released during and after planting. In the process of planting, talc is added to seed boxes to lessen the stickiness of seeds during planting so that they can evenly be placed. Most of the talc is released into the environment as waste, with minimal pieces of the seeds themselves, becoming contaminated with pesticides (Krupke, Hunt, Eitzer, Andino, & Given, 2012). As a result, the “talc waste” dust cloud around the sowing machines exposes bees to severe intoxication during their foraging flights to nearby forests or flowering fields. Studies report high levels of seed treatment of neonicotinoids present on or in the dead bodies of foraging bees and the presence of toxic particles transported back to the hive (Pisa et al., 2015). Interactions with the sowing of seeds is reported to contribute to mass colony losses that have been recorded in several countries including Italy, Germany, Austria, Slovenia, the USA, and Canada (Pisa et al., 2015).

Apart from organic production (0.2% of total acreage), neonicotinoid seed treatments comprise of nearly all maize planted in North America and maize production is expected to increase. Current application rates for the major compounds used in maize seed treatments are at a range that is highly toxic to honeybees. With a range from 0.25 to 1.25 mg/kernel, a single kernel contains an active ingredient amount significantly more than the LD50 values for honeybees (Krupke et al., 2012).

Neonicotinoids contaminate soils, water sources, and non-target plants in agricultural systems as well as nearby areas. Consequently, these numerous pathways contribute to severe, prolonged exposure of non-target organisms (Bonmatin et al., 2015). Neonicotinoid concentrations are frequently present in both urban and agricultural surface water, causing concern for pollinator declines. Due to their water solubility, neonicotinoids are easily transportable, resulting in extensive offsite movement to nearby water sources. In a national study conducted across the United States, at least one neonicotinoid was found in 63% of the 48 streams sampled (Hladik & Kolpin, 2016). The neonicotinoid, imidacloprid, was detected most often, and their presence was linked to urban land-use. Meanwhile, the presence of clothianidin and thiamethoxam were both linked to the number of cultivated crops in the sample area. Furthermore, transportation of neonicotinoids to streams in agricultural basins were revealed to be correlated with use and precipitation (Hladik & Kolpin, 2016).

Neonicotinoids have not only been detected in surface water in the United States but they have also been detected in soil and groundwater. Neonicotinoid detections are usually coincided with areas of intensive irrigated agricultural production (Huseth & Groves, 2014). Between the years 2008 and 2012, neonicotinoid insecticides were found at 23 well monitoring locations maintained by the Wisconsin Department of Agriculture, Trade, and Consumer Protection-Environmental Quality Section (WI DATCP-EQ) (Huseth & Groves, 2014).

D.    Levels of Exposure

In the United States, guidelines to evaluate the potential risks of insecticides are regulated by the U.S. EPA and directed by the Federal Insecticide, Fungicide and Rodenticide Act (FIFRA). Under FIFRA, measurements of lethal toxicity consist of counting the numbers of dead bees after 24 to 48 hours. Then, the corresponding median lethal dose is calculated (LD50) on the individual (organism) level. Studies have suggested that the level of toxicity is dependent on the route of exposure and that physical contact was more toxic than oral, yet there was a large variability in studies on the effects of toxicity on oral exposure (Blacquiere et al., 2012). The U.S. EPA has established “levels of concern” for honeybee exposure to pesticides and acute levels of concern were defined as 40% of the LD50 value (Stewart et al., 2014).

1.      Lethal toxicity.

Recently, it has been estimated that a level of 0.25 μg kg−1 of the neonicotinoid imidacloprid in honey would be lethal to a large population of honeybees over 150 days (A. Jones & Turnbull, 2016). United Kingdom (UK) studies demonstrate that concentration levels of the neonicotinoids imidacloprid, clothianidin, and thiamethoxam in honey were less than the limit of detection (LOD), with LOD being the lowest quantity that can be reliably detected in a sample. As a result, it is possible that lethal concentrations of neonicotinoids in honey are nonexistent in the UK. As an example, a study was conducted in several UK apiaries located 2 miles from oilseed rape (OSR), a crop that is the only widely grown in the UK that is attractive to pollinators and grown from neonicotinoid coated seed. The results of this study were like other studies conducted in the UK. Imidacloprid was not detected in any of the samples and two neonicotinoids, clothianidin and thiamethoxam, were less than the LODs in other studies (A. T. Jones, G. , 2016). The absence of imidacloprid could be due to the decrease of its use in the UK compared to clothianidin and thiamethoxam. No detections in any imidacloprid samples were at the level estimated to be lethal to honeybees over 150 days.

While the toxicity of imidacloprid in honey has been analyzed, the long term lethal toxicity of other neonicotinoids such as clothianidin and thiamethoxam, have not been estimated (A. Jones & Turnbull, 2016). Despite the large variability in some studies, overall evidence suggests that direct lethal effects of neonicotinoids from unintentional exposure of severe toxic concentrations rarely occurs (Brandt et al., 2016).

2.      Sublethal Effects.

In contrast to rare lethal concentrations,pollinators are more commonly exposed to low concentrations of neonicotinoids, leading to sublethal effects including immunity-suppression and behavioral complications (Brandt et al., 2016). Behavioral effects often include impaired learning, foraging, homing, and reproduction. Sublethal effects contribute to a wide range of complications in individual bees, leading to the weakening of their colonies. While various studies demonstrate the impairment of learning, homing, reproduction, and other behaviors linked with neonicotinoid exposure, it is important to note that there are molecular effects underlying these impairments. Transcriptional changes in genes from neonicotinoid exposure cause substantial molecular effects in the brain of honey bees and expressional changes of immune system related genes suggested that negative effects were not only on brain function, but immunity defense as well (Christen, Mittner, & Fent, 2016).

III. Effects of Neonicotinoids on Bee Pollinators

A.    Immunity and Colony Collapse Disorder.

Immunocompetence is the ability of an organism to support an immune response. It is a critical part of pollinator health because the maintenance of the immunity in animals is one of the most taxing physiological systems (Alaux, Ducloz, Crauser, & Le Conte, 2010). For example, immune defense for honeybees is important because a weak defense makes them vulnerable to parasites and pathogens (Alaux et al., 2010). High levels of pathogens and parasites are correlated with colony losses, and thus “suggests a causal link between external stress factors and reduced immune function” (Brandt et al., 2016).

Immune defense depends on several factors such as the age or nutritional state of the pollinator, but more importantly, immune function may also be negatively impacted by pesticides. The effects of three neonicotinoids (thiacloprid, imidacloprid, clothianidin) on honeybee immune parameters demonstrate that immunity defense is affected by sublethal concentrations of neonicotinoids. Specific immune parameters include total hemocyte count (analogous to white blood cells in humans), encapsulation (wound healing response), and antimicrobial activity of the hemolymph (fluid in invertebrates analogous to blood in mammals) (Brandt et al., 2016). Due to sublethal neonicotinoid exposure, immunity suppression in bees can occur, making them susceptible to parasite infections and viral diseases. Consequently, these infections and viruses are spread at higher rates among individuals and colonies compared to those not exposed to neonicotinoids (Sanchez-Bayo et al., 2016).

Several factors can contribute to the weakening of the colony and eventually its collapse (Figure 1). When an individual bee interacts with pesticides, parasites, and pathogens, this creates a cycle of immunity suppression until the colony weakens. For instance, the widespread Varroa mites weakens immunity and maintains a viral infection, potentially facilitating infections by other pathogens including the prevalent Nosema ceranae in honeybees (Sanchez-Bayo et al., 2016). Neonicotinoid exposure exacerbates these parasitic and pathogenic interactions in honeybees. This cycle of immune suppression increases the toxicity of neonicotinoids and weakens the colony until it collapses.

As a result of such interactions affecting immunity, neonicotinoids have recently been linked to widespread colony failure, also known as colony collapse disorder (CCD) (Brandt et al., 2016). CCD is a phenomenon that occurs when there are large winter losses due to the sudden disappearance of worker bees and/or queen failure (Sanchez-Bayo et al., 2016). Since the first report of CCD in North American in 2006, large colony losses of managed Western honeybees have been reported in several European countries, parts of Canada, Middle East, and Japan (Farooqui, 2013). The consensus among the scientific community is that no single stressor is the cause of CCD and that it is caused by a complex set of factors. However, studies have shown that sub-lethal concentrations of neonicotinoids are potentially one of the main sources of CCD (Lu, Warchol, & Callahan, 2014). CCD differs from past colony losses in that it is rapid, more severe, and lack of dead bees of workers are found in and around the hive, indicating that death occurs in the field (Farooqui, 2013).

Sublethal concentrations of neonicotinoids reduce survival of bee colonies by impairing the behavior of bees. Bees exposed to sublethal concentrations of neonicotinoids resulted in various behavioral impairments to foraging, feeding, navigating, motor function, and the inability to detect floral traits. These behavioral impairments frequently result in colony failure (Kessler et al., 2015). While it has been suggested that bees can choose non-contaminated flowering plants, ultimately avoiding exposure to neonicotinoid concentrations, evidence reveals that both the bumblebee (Bombus terrestris) and honeybee (Apis mellifera) prefer foods containing the most commonly used neonicotinoids; imidacloprid, thiamethoxam, and clothianidin (Kessler et al., 2015).

To assess whether bees avoid nectar (sucrose solutions) containing neonicotinoids, an experiment was designed to identify the bee’s ability to taste capacity to nectar toxins. Using a two-choice test, individual adult worker bumblebees and honeybees were housed separately in plastic boxes for 24 hours and given two types of food: one with a sucrose solution and a sucrose solution containing concentrations of imidacloprid, thiamethoxam, or clothiandin. Concentration values were derived from specific concentrations reported from nectar and pollen. Preference was tested by checking whether the neonicotinoids constrained their feeding behavior through their proboscis extension reflex (PER), which is stimulated when a sucrose solution touches a bee’s antenna. PER was not affected by sucrose solutions containing imidacloprid, thiamethoxam, or clothiandin. Although the neonicotinoid concentrations reduced their survival, neither species of bee avoided the natural occurring concentrations and in fact, they both showed a preference for solutions containing imidacloprid and thiamethoxam over sucrose alone. In addition to preference for neonicotinoid-laced solutions, total food consumed in the 24 hour period was increased when neonicotinoids were present (Kessler et al., 2015).

B.     Learning and Memory.

Bee pollinators, such asthe honeybee, require a properly functioning nervous system to maintain the functioning of both the individual and colony. Sublethal exposure of neonicotinoids can alter the learning, memory, and orientation in honeybees (Pisa et al., 2015). In the honeybee brain, the neural bases for olfactory learning (sense of smell) circulate among several areas such as the antennal lobes (ALs) and mushroom bodies (MBs), implicating the involvement of different areas to carry out aspects of memory including learning, recall, and odor perception (Farooqui, 2013). Olfactory learning is crucial in many facets of honeybee behavior, including “recognition of nestmates, foraging, food preferences, hive location, and navigation” (Farooqui, 2013). Navigation of honeybees requires learning direction and distances between their travel to and from the nest as they forage. Additionally, their navigational decisions and routines are based on the origin of their flight path and recognition of associations between landmarks, implicating map-like organization and spatial memory (Farooqui, 2013). Due to their complex sensory systems, any interference with their olfactory learning and memory could lead to negative consequences on foraging performance (Farooqui, 2013).

C.    Foraging and Homing Flights.

The ability of pollinators to forage and return home plays a critical role in the survival of colonies. Neonicotinoid exposure interferes with honeybee foraging efficiency at the colony level by manipulating the psychological traits and cognitive abilities of individual bees (Sandrock, Tanadini, Tanadini, et al., 2014). When exposed to pollen containing chronic doses of thiamethoxam and clothianidin over 1.5 months, honeybees were found to have a strong reduction in their pollen collection and honey production (Sandrock, Tanadini, Tanadini, et al., 2014). In addition to foraging, direct topical exposure under field conditions of two neonicotinoids on individual bees resulted in the reduction of homing flights that were not significant at doses below one-twentieth of their LD50s (Matsumoto, 2013).

In bumblebees, exposure to field-realistic thiamethoxam concentrations caused unusual foraging patterns, resulting in less pollen collection and longer foraging bouts (Stanley, Russell, Morrison, Rogers, & Raine, 2016).

D.    Reproduction.

Although life-time reproductive success is a major determinant of fitness, this area has been somewhat neglected in pesticide assessment research. Nonetheless, the effect of neonicotinoids on life-time reproductive success is important to understanding the long-term impacts of systemic insecticides on pollinator populations (Sandrock, Tanadini, Pettis, et al., 2014). Though honeybees are the most studied bee species, they act as poor representatives for pesticide evaluations because of their complex perennial life cycle, making it difficult to quantify reproductive success. On the other hand, bumblebees have annual life cycles, making them less complex and solitary bees are even more convenient for fitness quantification because it is easier to link the performance of one female individual and its reproductive success (Sandrock, Tanadini, Pettis, et al., 2014).

In an experimental study on the solitary bee species O. bicornis (red mason bee), it was found that the dietary sublethal exposure of thiamethoxam and clothianidin contributed to negative consequences of fitness performance. Compared to non-exposed female bees in the field, exposed lab females completed fewer nests and constructed fewer brood cells per nest, displaying a reduced offspring production of nearly 50% (Sandrock, Tanadini, Pettis, et al., 2014). Furthermore, the offspring sex ratios of exposed females were significantly male-biased, indicating poor environmental conditions and further exacerbating reproductive potential. These results were in accordance with several bumblebee studies showing that dietary exposure of neonicotinoids drastically decreased daughter queen production and slowed down colony growth (Sandrock, Tanadini, Pettis, et al., 2014). For example, in bumblebee colony development, it was found that field-realistic levels of neonicotinoid exposure resulted in an 85% reduction in queen production (Whitehorn, O’Connor, Wackers, & Goulson, 2012).

Along with red mason bees and bumblebees, honeybee queens exposed to neonicotinoids during rearing also lead to reduced reproductive success by transforming their anatomy and physiology. Queen bees are the primary reproductive females that can produce offspring, playing a critical role in colony survival (Williams et al., 2015). The outcome of these studies signifies that neonicotinoid exposure can negatively impact reproductive success and long-term population dynamics, and that exposure can impact both social bee species and solitary (wild) bee species.

IV. Policies to Protect Pollinators

  The effects of neonicotinoids on pollinators have not gone unnoticed with respect to laws and regulations at every level of governance. This section discusses current laws that seek to protect bees by examining policy approaches at the state and federal level. Lastly, policy recommendations are discussed.

A.    California Pesticide Regulation

In California, the Department of Pesticide Regulation (DPR) is a state agency under the California Environmental Protection Agency (CalEPA) that is responsible for mitigating the harmful effects of pesticides on pollinators. DPR performs risk assessments and regulates neonicotinoid application, registration, sales, and labeling (California Department of Pesticide Regulation, 2013). DPR remains to be at the forefront of a national effort to protect pollinator health by collaborating with the U.S. EPA as well as working with County Agricultural Commissioners, agricultural producers, bee keepers, and other agencies to develop and implement regulatory measures to protect bee health (California Department of Pesticide Regulation, 2013).

DPR requires companies who have registered products in California to perform tests and submit data for DPR analysis through a process called reevaluation. The data submitted by companies provides evidence for the effects of neonicotinoids use on pollinators for potential regulations (California Department of Pesticide Regulation, 2013). California regulations require that DPR review reports of adverse effects to the people or the environment resulting from pesticide use and then conduct a process of reevaluation (California Department of Pesticide Regulation, 2014). In 2009, DPR initiated a reevaluation of pesticide products containing four neonicotinoids: imidacloprid, thiamethoxam, clothianidin, and dinotefuran (California Department of Pesticide Regulation, 2013). Because of the 2009 reevaluation, mitigation efforts were put in place to protect pollinators by requiring new labeling language on registered products and requiring that neonicotinoid registrants conduct semi-field studies on honeybees (California Department of Pesticide Regulation, 2014).

In addition to reevaluation, California administrative rulemaking law requires DPR to assess the economic impact of any proposed regulation (Office of Administrative Law, 2017). For example, prior to adopting any pesticide regulation, DPR would need to assess whether, and to what extent, a proposed pesticide regulation would affect the creation or elimination of businesses and jobs, as well as any benefits to the health and welfare of California residents, worker safety, and the state’s environment before regulating the use of pesticides (Office of Administrative Law, 2017). Overall, the rulemaking process is designed to promote a balance between business interests, the economy, and environmental protections.

B.     Policy Recommendations

This section offers policy recommendations for the protection of bee pollinators against the harmful effects of neonicotinoids. Despite existing state and federal policies, regulation could go further to protect bees. While an outright ban of neonicotinoids is a possible solution, it would create other potential issues by interfering with business interests (i.e., proponents of neonicotinoids, manufacturers and farmers). For example, in 2013, the European Union (EU) implemented a temporary two-year restriction on three commonly used neonicotinoids (clothianidin, thiamethoxam and imidacloprid) based on a European Food Safety Authority (EFSA) report that showed evidence of their adverse impact on bees (The European Commission, 2013). This was a highly controversial policy decision because many experts claimed that there was not enough field research to prove that neonicotinoids decreased the performance of bee colonies near treated fields (Henry et al., 2015). Currently, the EU is reviewing the outcomes of the ban to determine the possibility of implementing a permanent restriction.

Despite stringent efforts to protect pollinators at the state level, many issues remain with the current regulatory scheme at the federal level in the United States. For example, the U.S. EPA has categorized most neonicotinoids as “general use” pesticides which allows neonicotinoids to be applied by unlicensed and untrained individuals (Hopwood, Code, Vaughan, & Black, 2016). Additionally, new information has surfaced about the effects of neonicotinoids since they were initially registered. As such, the U.S. EPA should reassess neonicotinoid products to determine whether they should be re-classified as restricted use (Hopwood et al., 2016).

Furthermore, pesticide evaluations on bees often lack an evidence-based approach on some aspects of pollinator health, pesticide application, and pesticide use. First, current regulations for evaluating pesticides and their harm on bees does not directly address reproduction effects, an important aspect of pollinator health and population dynamics (Williams et al., 2015). Next, efforts to reduce off-site movement of planter dust is needed to mitigate potential routes of exposure to pollinators (Stewart et al., 2014). Lastly, to conduct accurate analyses on the effects of neonicotinoids on pollinators, a national pesticide use reporting system is needed to attain comprehensive data. Currently, California is the only state to require pesticide use reporting (Hopwood et al., 2016).

V.    Conclusion

Despite mounting evidence that field-realistic exposure to neonicotinoids have disastrous effects on bee populations, experts agree that evidence is inconclusive and that it is necessary to identify knowledge gaps to implement sufficient regulatory actions to protect pollinators (Lundin, Rundlöf, Smith, Fries, & Bommarco, 2015). There are a few key areas of research that need improvement to gain a more comprehensive understanding on the effects of neonicotinoids on pollinators. First, a great deal of literature has demonstrated many of the lethal and sub-lethal effects of neonicotinoids on bees in both the field and laboratory (Williams et al., 2015). However, some experts assert that an overwhelming amount of research is conducted in the laboratory and that more field studies are needed to adequately measure the impact of neonicotinoids on bees. Next, the use of the western honeybee as a surrogate for nearly all pesticide risk assessments and research ultimately limits the representativeness of the many important pollinator species affected by neonicotinoids (Hopwood et al., 2016). A greater understanding is needed on how neonicotinoids affect beneficial insects like moths, butterflies, beetles, and other species of bees. While these pollinator species make minor contributions to crop pollination, they are critical to agricultural ecosystems and biodiversity (Hopwood et al., 2016). Lastly, primary research focuses on the effects of individual bees, rather than groups of individuals. It is suggested that more research is needed to link individual bee to consequences at the colony and population levels (Lundin et al., 2015). Overall, these improvements in research can provide a more comprehensive understanding on the effects of neonicotinoids on pollinators.

Figure 1. An illustration of the interactions between pesticides (neonicotinoids/fipronil, fungicides/acaricides), parasites, and pathogens in relation to colony collapses. Individual bee interactions are exposed to the interactions between stressors within the dashed rectangle. Varroa mites weakens immunity and maintains the viral infection, potentially facilitating infections by other pathogens such as Nosema. Sub-lethal concentrations of neonicotinoids contribute to immune-suppression and intensify parasite/pathogen interactions. Fungicides and some acaricides strengthen the toxicity of most insecticides and increase susceptibility to Nosema infections. The combination of the above factors increase the toxicity of pesticides and undermine immunity of individual bees, making the colony weaken until it eventually collapses (Sanchez-Bayo et al., 2016).

VI. References

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