Neonicotinoid Insecticide Imidacloprid: Presence in Freshwater Systems, Phytoremediation, and Bacterial Remediation

Introduction

Neonicotinoids, commonly referred to as neonics, are the most widely used class of insecticides in the world [1-4]. One of the most extensively used neonics is imidacloprid [4,5], and like other neonics, it functions by inhibiting the central nervous system in insects [3,6]. That mechanism is indiscriminate, so while it harms pest species, it also harms non-target insects like honey bees [3,7]. The impact on honey bees has been the subject of much prior research [1,7], but the reach of imidacloprid is not limited to terrestrial insects. Current research indicates that imidacloprid is infiltrating freshwater systems (both surface water and groundwater) as a result of agricultural runoff [1,3,8,9]. When present in freshwater systems, imidacloprid adversely affects not only aquatic invertebrates but also the aquatic environment [3,8]. Furthermore, imidacloprid is associated with negative consequences for human health [1,3,10,11], and it has been shown to persist through the water treatment process to become present in drinking water [1,4,8]. Therefore, imidacloprid needs to be removed, or remediated, from the environment. Two cost-effective and sustainable methodologies are phytoremediation (removal by plants) and bacterial remediation [9-12]. In each of these processes, the biological system uptakes imidacloprid and chemically degrades it into less toxic derivatives [9,11,13]. This review will provide an overview of the extent to which imidacloprid pollutes freshwater systems and discuss the efficacy and viability of plant and bacterial remediation.

Background

Today, over 90% of maize, 50% of soybeans, and 95% of cotton crops get treated with neonics in the United States (US) [2,14]. One reason neonics are used so prevalently is their efficacy against a wide range of pests [3,5,7,11]. However, the indiscriminate action of neonics has caused such harm to bees that the European Union (EU) banned the field use of imidacloprid and several other neonics in 2018 [15]. Since then, EU member states have repeatedly enacted emergency authorizations to allow farmers to use the prohibited chemicals in spite of the ban [15]. The fact that these countries were unable to adhere to the ban illustrates an international dependence on imidacloprid and the lack of an equally effective alternative. Therefore, in order to address the problems that imidacloprid is causing in freshwater systems, it is more reasonable to remediate it than to prevent its use via legislation.

Agricultural practice and imidacloprid’s physicochemical properties offer insight into how imidacloprid is infiltrating freshwater systems. Imidacloprid is most commonly applied as a seed coating before planting [6]. The seed coat prevents pests from damaging the seed prior to germination, thus ensuring higher germination rates. After germination, approximately 2-20% of the seed coat is absorbed through the roots, but 80-98% remains in the soil, even after the crop is harvested [1]. Imidacloprid is water soluble [1,5,16] and demonstrates low soil sorption (the ability to stick to soil) [5,10]. Consequently, imidacloprid enters freshwater systems as agricultural runoff. 

The Extent of Imidacloprid Contamination in Freshwater Systems

Multiple studies that tested freshwater systems for the presence of neonics found imidacloprid was present in a higher percentage of their samples than other neonics [1,4,16]. Guo et al. (2020) cites water-sampling studies conducted in Australia, China, the Netherlands, Sweden, the US, and Vietnam that detected imidacloprid residues in 78-100% of surface water samples. Additionally, Lu et al. (2020) cites studies that detected imidacloprid in surface water in Brazil, Canada, and Japan. Together, these studies demonstrate how imidacloprid is infiltrating freshwater systems across the globe, and they suggest that relative to other neonics, imidacloprid may be of particular interest for remediation.

A close examination of some of these studies can offer a more holistic understanding of the extent of imidacloprid contamination. Lu et al. (2020) took 16 samples from different locations along two rivers in China, and tested them for the presence of neonics. Imidacloprid was present in 100% of the surface water samples [1]. Similarly, Hladik and Kolpin (2016) sampled and tested 38 streams in the US. While imidacloprid was detected more frequently than any other neonic, it was only present in 37% of the streams [16]. Hladik and Kolpin’s (2016) study may more accurately represent how many surface water systems are contaminated with imidacloprid because Lu et al. (2020) only sampled two rivers. However, the data from Lu et al. (2020) shows that within a contaminated surface water system, imidacloprid contamination spans the entire body of water. Additionally, Lu et al. (2020) found the average concentration of imidacloprid in the surface water samples was 11.9 ng/L, which is a higher concentration than what the US Environmental Protection Agency (EPA) considers safe for aquatic invertebrates (10 ng/L) [12]. The median concentration between all of the neonics in Hladik and Kolpin’s (2016) study was 19 ng/L, and the median concentration for imidacloprid was similar but not explicitly listed [16]. These numbers suggest that when imidacloprid is present in surface water, it is generally at a high enough concentration to warrant remediation. The highest concentration for imidacloprid in either of these studies was detected by Hladik and Kolpin (2016) at 14 times greater than the EPA’s benchmark. This concentration was an outlier amongst the data collected [16], but it represents an important instance when remediation needs to be highly efficient to be effective; at least 93% of the imidacloprid would need to be remediated from this sample to get the concentration below the EPA’s benchmark.

Imidacloprid also infiltrates groundwater, and in the US, 13% of the population uses groundwater as their primary source of drinking water [6,14]. Thompson et al. (2021) sampled 40 wells in the US for neonics and found imidacloprid in 43% of the samples, with a maximum concentration of 6.7 ng/L [14]. While that is slightly more frequent than imidacloprid detection in US surface water (37%) [16], groundwater concentrations were all below the EPA benchmark, unlike surface water concentrations. Interestingly, unlike the other studies in this section, Thompson et al. (2021) found that imidacloprid was not the most prevalent neonic. Clothianidin was detected more frequently, in 68% of the samples [14].

Water treatment plants remove toxins from both surface and groundwater [17], but two studies found that imidacloprid was still present after the treatment process [1,4]. Lu et al. (2020) took five samples of water that was entering the treatment plant and five samples of water that had just been treated. Imidacloprid was present in every sample [1]. While imidacloprid was never completely removed by the treatment plant, its concentration was cut roughly in half, to a new mean of 5.3 ng/L [1]. Lu et al. (2020) additionally took 71 samples of tap water from different homes and found imidacloprid was present in 82% of the samples, with an average concentration of 0.6 ng/L [1]. Craddock et al. (2019) also sampled water before and after the treatment process. They found the imidacloprid detection frequency decreased from 36.7% of samples taken before treatment to 29.7% after treatment [4]. Unlike the findings of the Lu et al. (2020) study, Craddock et al. (2019) did see some instances where imidacloprid was entirely removed by the treatment plant. The average concentration was also found to be reduced to less than one part per trillion [4]. Together, these studies show that while treatment plants rarely remove imidacloprid completely, they typically lower the concentration to safe levels. Nevertheless, remediation is still an advisable precaution to ensure that surface water concentrations don’t exceed the capacity of treatment facilities. Remediation is also necessary to protect aquatic invertebrates, as they live in untreated water with concentrations that generally exceed the recommended concentration of imidacloprid.

Phytoremediation

Suitable plant remediators uptake water through their roots, and they subsequently degrade any imidacloprid that has dissolved in the water through their metabolism. Phytoremediation is typically implemented in the form of constructed wetlands [9,12,13,18], which are shallow, man-made ponds for growing plant remediators and collecting pollutants [19]. They typically receive water from nearby freshwater systems [20], and ultimately release the water back to its original source, into the ground, or to a man-made surface destination after filtering has occurred [21]. In addition to filtering water, constructed wetlands can benefit the surrounding ecosystem as both the constructed wetland itself and the destination for the effluent flow (output) can be designed to provide a habitat for wildlife [12,13,20,21]. However, to reap the ecological benefits, constructed wetlands must utilize native plant species [12,13]. Since imidacloprid contamination is a global issue, plant remediators need to be identified in all parts of the world in order for this technique to be viable. When looking for a plant species to use as a remediator, wetland plants are of high interest because they are naturally adapted to grow in flood conditions, and constructed wetlands are designed to maintain a constant state of flooding.

Liu et al. (2021) measured the remediation capabilities of nine wetland plant species native to South China. The plants were grown in pots of sand that received a liquid nutrient solution for six weeks [18]. Then, a mixture of imidacloprid and five other neonics was added to the pots [18]. After 28 days, the concentration of neonics in the liquid, sand, and plant tissues was measured. Cyperus papyrus was found to be the best remediator; only 10% of the initial imidacloprid remained in the liquid, sand, and plant tissue, meaning 90% had been biodegraded. McKnight et al. (2021a) conducted a similar study, looking at three wetland plant species native to the southeastern United States. These plants were grown in pots of sand suspended in tanks of water [12]. Imidacloprid and azoxystrobin (fungicide) were added to the water tank [12]. At 14 and 28 days, the water was changed and chemical levels were reset to the initial concentrations [12]. Imidacloprid concentrations in water, sand, and plant tissues were measured every week until 28 days after inoculation and once more at 56 days after inoculation [12]. At the end of the study, Sagittaria latifolia was found to be the best remediator, degrading 79.3% of the imidacloprid [12]. Both of these studies show how wetland plants can be efficient remediators because they facilitate a high amount of biodegradation in a relatively short amount of time. Liu et al. (2021) applied the initial dose of imidacloprid in soil very close to the roots, but in a constructed wetland the plants are growing beneath a shallow layer of water [20]. The McKnight et al. (2021a) study may more closely resemble how phytoremediation occurs in the field because the tank of water better represents how surface water accumulates in constructed wetlands.

While wetland plants are of high interest for phytoremediation, they are not the only type of plants that can be used. McKnight et al. (2021b) looked at the remediation capability of three terrestrial plant species. Terrestrial plants can be implemented as a buffer strip, where they are grown in a line on the edge of an agricultural site [13]. When implemented this way, terrestrial plants can remediate imidacloprid from groundwater and lessen the extent of agricultural runoff, thereby mitigating imidacloprid contamination in surface water as well [13]. McKnight et al. (2021b) found that Panicum virgatum and Iris versicolor were the most promising plants in the study because they degraded 64.3% and 62.5% of the imidacloprid, respectively, over 112 days [13]. However, I. versicolor presented health problems like stunted growth and leaf injury when exposed to imidacloprid, so the authors identified P. virgatum as the better remediator [13]. This study demonstrates the viability of an alternative method by which to implement phytoremediation. Buffer strips may prove particularly useful in climates that cannot support wetland plant species but still need remediation. More research should be conducted to determine whether buffer strips or constructed wetlands are more effective.

Bacterial Remediation

Lab studies show that bacteria, like plants, can effectively remediate imidacloprid. Constructed wetlands also utilize microorganisms for remediation [9,19]. Tiwari et al. (2022) and Gautam et al. (2023) screened agricultural soil samples for bacteria that could remediate imidacloprid, isolated the most promising remediator, and then tested the remediation capabilities of those bacterial isolates in sterile soil [10,11]. Tiwari et al. (2022) found Tepidibacillus decaturensis strain ST1 remediated 77.5% of the imidacloprid compared to the negative control (5.5%) in 45 days. Gautam et al. (2023) found that Sphingobacterium sp. InxBP1 degraded 73.9% of the imidacloprid in just 20 days. Both of these bacterial species show comparable rates of remediation to the previously mentioned plant species. Furthermore, both of these isolated bacteria were indigenous to the soil samples. Native bacteria—like native plants—can be better remediators because they are already adapted to their natural habitat and ecosystem [11]. Moreover, the ecosystem will not be put at risk by a native bacteria, but an invasive bacteria could pose a risk. As such, it should be a goal for bacterial remediation to rely on native isolates. However, it is unclear whether native bacterial remediators can be isolated around the globe because both of these studies were conducted in the same part of India. 

In addition to testing the remediation of those bacterial isolates in sterile soil, Tiwari et al. (2022) and Gautam et al. (2023) also tested their isolates in unsterile soil, which contained typical soil microbiota. The authors examined the interaction between the remedial isolates and other microbes as it pertained to the remediation of imidacloprid. In unsterile soil, Tiwari et al. (2022) saw remediation increase from 77.5% to 85%, and Gautam et al. (2023) saw remediation increase from 73.9% to 79.4%. The increased degradation can be attributed to the activity of the additional microorganisms present in the unsterile soil [10]. This finding is important for two reasons. One, it suggests the bacterial component of constructed wetlands will be more effective if they are implemented in soil with diverse microbiota. Two, it suggests that the plant component of constructed wetlands will also be more effective in soils with diverse microbiota; plants can recruit bacteria to the rhizosphere (the space around the roots) to assist with the breakdown of harmful chemicals like imidacloprid [18]. 

Alongside the trials of Tepidibacillus decaturensis strain ST1 in sterile and unsterile soil, Tiwari et al. (2022) tested how the bacterial isolate performed in conjugation with Cicer arietinum, the chickpea plant. They found that  C. arietinum had a minor positive impact on remediation, increasing remediation in sterile soil from 77.5% to 82%, and increasing remediation in unsterile soil from 85% to 91% [10]. When C. arietinum was tested by itself, it remediated roughly 6% more imidacloprid than the negative control in both soil types [10], so it appears that using both species has an additive effect. No plant species tested by McKnight et al. (2021a,b) or Liu et al. (2021) remediated less than 30% of the imidacloprid over the given time period. The extremely low remediation by unaccompanied C. arietinum can be explained by the fact that it was intended to function as a second control [10]. More research is needed to determine how strong phytoremediators interact with strong bacterial remediators. However, the typical design of a constructed wetland that employs both plants and microorganisms places them in separate chambers [20], so it may not be necessary to find bacterial remediators that can work in the same space as plant remediators.

One drawback of bacterial remediation is that it can be difficult to scale up from lab studies to field applications [9,10]. With that in mind, Guo et al. (2020), designed a study to isolate a strain of bacteria that would not only be a good remediator but also do well in the field. Rather than isolate a bacterial strain from soil samples like Tiwari et al. (2022) and Gautam et al. (2023), Guo et al. (2020) isolated a remediator from water samples. Furthermore, after Guo et al. (2020) selected for bacteria with the capacity to remediate imidacloprid, they conducted an additional selection step to ensure that the remediator species could survive in low nutrient conditions comparable to those in freshwater. The isolated strain, Hymenobacter latericoloratus CGMCC 16346, was tested in surface water, and it remediated 24.2% of the imidacloprid over 30 days [8]. In batch inoculation, it remediated 34.6% of the imidacloprid in the same amount of time [8]. Guo et al. (2020) also tested the remediation capability of a known bacterial remediator, Pseudoxanthomonas indica CGMCC 6648. P. indica CGMCC 6648 lost the ability to remediate imidacloprid when it was tested in surface water [8]. This study casts doubt on whether the remediator strains identified by Tiwari et al. (2022) and Gautam et al. (2023) can actually be applied in a constructed wetland because P. indica CGMCC 6648 was also isolated from soil. While H. latericoloratus CGMCC 16346 showed less efficient remediation than Tepidibacillus decaturensis strain ST1 and Sphingobacterium sp. InxBP1, it appears to be a more applicable remediator. H. latericoloratus CGMCC 16346 showed the best remediation when applied to surface water in batch culture, so that technique should be tested in other bacterial remediators to see if it has the same effect. Although inoculating a remediator in batch culture is not ideal because it requires more maintenance in the form of multiple inoculations and growing more bacteria in the lab, it may be necessary for successful application in constructed wetlands.

Conclusion

The purpose of this review was to show the extent of imidacloprid contamination in freshwater systems and examine phytoremediation and bacterial remediation as techniques for removing it from those systems. Imidacloprid was more frequently detected in surface water systems than any other neonic, and second most frequently in groundwater. In those systems, it threatens to harm aquatic invertebrates. Furthermore, since water treatment plants can’t remove imidacloprid entirely, it needs to be remediated from groundwater and surface water alike to protect human health. Phytoremediation is an affordable and eco-friendly solution. Wetland plants were identified that could efficiently remediate over 75% of applied imidacloprid [12,18]. Phytoremediation works best when native wetland plant species are implemented in constructed wetlands, but this constraint may prevent phytoremediation from being a reasonable technique in all locations. Terrestrial phytoremediators can be applied in buffer strips along cropland to target groundwater for remediation or as a preventative measure to lessen the effects of runoff. Another affordable, eco-friendly solution is bacterial remediation. It can be applied in constructed wetlands alongside phytoremediation, and can therefore compensate in regions that don’t have strong wetland plant remediators. Soil bacteria were shown to remediate over 70% of applied imidacloprid, but it can be difficult to successfully apply soil bacteria in a constructed wetland. Bacteria that were isolated from water showed better applicability, but less efficient remediation. Future research should be directed toward finding bacterial remediators that are more applicable in constructed wetlands.

About the Author: Mitchell Bancks

Mitchell Bancks is a 3rd year Biotechnology major with a specialization in Microbiology. Whether it’s using microbes to produce compounds that can be used to treat diseases, genetically modifying crops and livestock to fortify them against threats and to increase yield, using biological systems to clean up the environment via remediation, or another application of biotechnology, Mitchell is passionate about using biology to solve problems and improve the human condition. When he’s not studying, Mitchell loves to play volleyball—he is currently playing on three intramural teams, and he played for the UC Davis Men’s Volleyball Club during his first two years at Davis.

Author's Note

I wrote this piece as an assignment for my UWP 102B class during fall quarter, 2023. I chose this topic because I work part time as a data entry specialist for a public relations company. I input articles on agricultural biotechnology, crop protection, bee health, and microplastics/PFAS into the company database, but I don’t have the time to actually read most of what I input. I kept seeing the word “neonicotinoids” pop up in my work related to bee health, and I wanted to learn what they are and why they’re significant. After some preliminary research, I discovered a more niche topic: how neonicotinoids are contaminating freshwater. I chose to write my paper on that specifically because I think it’s a relatively newer focus in the scientific community, and it’s something that not as many people know about. The goal of this review is to not only try and answer the question “what is happening with neonics in freshwater?” but also to provide a review of some eco-friendly solutions.

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