Updated: Jul 9, 2022
- by Miu Bogdan Andrei.
Neonicotinoids are one of the most widely used classes of insecticides in the world. They are effective insecticides used in agriculture to control serious pests. No wonder these chemical compounds have been found in lakes and rivers of every inhabited continent, the natural water system being a major transfer pathway for pollutants from agricultural lands to wild ecosystems.
Whether they were designed to eliminate pests from economically important crops, studies showed that neonicotinoids are not highly specific, being capable to affect non-target organisms. Biodiversity meets neonics through the natural food chain in which there are involved contaminated insects or vegetation.
Depending on the animal’s habitat, abiotic factors such as water flow and wind may favour exposure to neonicotinoids. According to research studies, neonics effects occur on highly different organisms from bees to birds and mammals. The most common effects of neonicotinoids on wild animals are related to genetic abnormalities, oxidative stress, hormonal imbalance, and impairment of normal behaviour.
Evidence that neonicotinoids have a particular impact on bees has raised concerns, leading for the first time to the regularization in the European Union of 3 of the most used neonicotinoids: imidacloprid, clothianidin and thiamethoxam. A total ban on the use of neonics may not be a feasible solution to the problem because of the pests that can cause a massive drop in agricultural production. The key is to replace harmful insecticides with efficient eco-friendly pest control methods.
Chemistry of neonicotinoids
Neonicotinoids are chemical compounds related through their common structure that includes three main parts: one pharmacophore group and one heterocyclic group linked by a bridging chain region (Figure 1).
The pharmacophore type has a great influence on the biological activity of neonicotinoid molecules, being responsible for the degree of binding affinity to the ion channels belonging to the nervous system (Ohno et al., 2009). The most widespread functional groups with the role of pharmacophores are nitroenamine, nitroamidine and cyanoamidine.
As for the bridging chain, the most commonly used group is methylene, while other groups decrease the insecticidal activity (Maienfisch et al., 2001).
Based on the structural shape of the heterocyclic group neonicotinoids can be classified into 3 main categories: nitromethylene, chloronicotinyl and thianicotinyl compounds. Imidacloprid is a first-generation neonicotinoid, part of the chloronicotinyl subclass, while clothianidin and thiamethoxam are part of the thianicotinyl subclass, also known as second-generation neonicotinoids (Maienfisch et al., 1999).
Thiamethoxam is considered a neonicotinoid precursor as it is easily transformed into clothianidin during metabolic reactions that occur in plant and insect tissues (Nauen et al., 2003).
Figure 1. Chemical structure of imidacloprid, clothianidin and thiamethoxam (structures were generated using ChemSketch software).
How far away have neonicotinoids spread?
Neonicotinoids can be used as systemic insecticides for the treatment of seeds and soil or as foliar sprays applied directly to crops. Neonics which form coating films around seeds are transported through the plant organism later in the life cycle. The transport takes place along the vascular system channels providing long-term crop protection against pests.
Studies show that systemic neonicotinoids are capable to spread in the whole plant organism including leaves, nectar and pollen (Jiang et al., 2018; Li et al., 2018; Radolinski et al., 2018). In other words, systemic insecticides protect plants from inside their tissues.
However, their persistence in plants and soil is a major environmental risk. The water solubility of these insecticides is the reason why they can enter easily through the plant vascular system but this characteristic also gives neonicotinoids the possibility to reach the groundwater system making them uncertain for the health of aquatic ecosystems.
Systemic neonicotinoids are more likely to be mobilized through soil leachate by high-intensity precipitations (Radolinski et al., 2018; Yadav & Watanabe, 2018).
Also, the soil profile can amplify the spreading of neonicotinoids into ecosystems by runoff and shallow lateral drainage processes in the areas surrounding crops (Radolinski et al., 2019). No wonder imidacloprid, clothianidin and thiamethoxam were found in aquatic environments from around the world. Chen et al. (2019) revealed intense neonicotinoid pollution close to the estuaries of all the major rivers across the east coast of China, imidacloprid being the main pollutant identified in more than ten rivers (including Yellow, Pearl and Nandu Rivers) during the wet season.
The study estimated that annually more than 1200 tons of neonicotinoid insecticides are dispersed in the adjacent seas of China through the national hydrographic network (Chen et al., 2019). Hladik et al. (2018) have studied the prevalence of neonicotinoids in the large aquatic ecosystem of the Great Lakes and their tributaries in the USA. Their study showed that imidacloprid, clothianidin and thiamethoxam are the major pollutants in this hydrological basin, being identified in all water samples collected around one year. A different number of samples has exceeded the neonicotinoid benchmark values stated by different sources (Hladik et al., 2018). Imidacloprid and clothianidin were also found in Australian rivers placed on the east coast (Hook et al., 2018).
Moreover, neonicotinoid pesticides were identified on vegetables, fruits and honey at levels within the tolerance limit for human health safety (Craddock et al., 2019), but with an existing threat to pollinators. This is the reason why the European Union (EU) has banned the use of seeds coated with imidacloprid (Regulation EU No. 783/2018), clothianidin (Regulation EU No. 784/2018) and thiamethoxam (Regulation EU No. 785/2018) if the resulted crops are growing outdoors. Despite these restrictions, the risk for bees remains relatively high even in the EU. The utilisation of the three neonicotinoids mentioned above on bee-attractive crop seeds was banned in the EU since 2013 (Regulation EU No. 485/2013), but a recent study showed that these insecticides may still be prevalent on the field. Wintermantel et al. (2020) have identified imidacloprid, clothianidin and thiamethoxam in oilseed rape nectar after 5 years of their interdiction and estimated that up to half of the bees are likely to die in some of the analysed fields.
Neonicotinoids ecological impact: an overview of the effects induced on biodiversity
The main negative effect of neonicotinoid compounds occurs on the central nervous system of insects. The neurotoxic mechanism and its efficiency in preventing and eliminating plant pests makes neonicotinoids a widely used class of insecticides.
Because of their nonspecific action, neonicotinoid-based insecticides have raised serious concerns as there is evidence that they affect nontarget insects including pollinators (e.g., bees). Moreover, there are many possible routes of transport by which neonicotinoids accumulate in the environment and indirectly affect other animal organisms. The category of nontarget organisms exposed to the harmful effects of neonicotinoids includes aquatic insects and crustaceans, fish and birds. There is also few information about neonicotinoids’ impact on insectivore animals classified as small reptiles, amphibians or mammals.
Pollinators. There are a lot of studies exploring the harmful effects of neonicotinoids on wild or domesticated species of bees (Table 1). The toxic effects are related to the nervous system functions and include dysfunctions in the memory-involved processes (Tison et al., 2019), changes in daily locomotor activity (Jacob et al., 2019), disturbance of sensory abilities (Démares et al., 2018) or abnormalities in the developmental process (Wu et al., 2017). According to recent studies neonicotinoids are found not only in larval and adult bees but also in the honey and pollen stored in the hive (Codling et al., 2018).
Aquatic invertebrates. As mentioned before, neonicotinoid compounds are soluble in water and this is the reason why they can enter relatively fast into the groundwater system and implicitly reach the aquatic habitats. Environmental concerns are high because of the effect of neonicotinoid-based products on aquatic organisms which is not well known. Aquatic ecosystems and wetlands host a wide range of beings from phyto- and zooplankton to insects, fish and large mammals. Moreover, the possibility of neonicotinoids to have negative effects on threatened species (e.g., Cherax destructor) or economically important species (e.g., Mytilus galloprovincialis) is relatively high according to recent studies (Stara et al., 2019, 2020). Table 2 shows an overview of the effects induced by different neonicotinoids on aquatic species of molluscs, crustaceans and insects.
Fish. Freshwater fish are more likely to face pollution with neonicotinoids because of the placement of their habitat. Lakes or rivers are usually close to agricultural areas being more exposed to insecticide contamination. A few recent studies are exploring the effects of neonicotinoids on different species of freshwater fish (Table 3). The most frequently observed effect was related to DNA damage in erythrocytes (Hong et al., 2018; Vieira et al., 2018). No wonder this happened if we consider the physiology of fish respiration, blood cells being in proximity of the polluted water.
Birds. Neonicotinoids can enter the bird’s organism through their food whether we consider the granivorous or the insectivorous species. One of the applications of neonicotinoid insecticides involves the coating of seeds during planting in order to protect them against pests and reach a high germination efficiency. Different species of granivorous (e.g., Zonotrichia leucophrys) or omnivorous (e.g., Passer domesticus) birds usually consume neonicotinoid-coating seeds while farmers spread them on the field. Insectivorous birds can experience indirect effects of neonicotinoid insecticides through their contaminated food or by the decrease in number of the insect populations. In Table 4 are listed the recent studies which identified or tested neonicotinoids’ effects on birds. The most common observed negative effects of neonicotinoid compounds were related to the modified migratory activity (Eng et al., 2017, 2019; Hao et al., 2018), anatomical anomalies of the reproductive tract (Ertl et al., 2018) or hormonal imbalance (Pandey & Mohanty, 2017). Studies also described variations in body weight in different species during exposure to neonicotinoids (Eng et al., 2017, 2019;Pandey & Mohanty, 2017).
Terrestrial animals. Due to biotic and abiotic factors, terrestrial animals may face the effects of insecticide pollution (Table 5). Neonicotinoid-contaminated insects are part of the food chain so they can transfer insecticides to wild animals like frogs and lizards or insectivorous mammals such as bats.
Moreover, amphibians’ metamorphosis from the egg to the adult state depends on agricultural waters which are likely to be polluted with different pesticides. While studies are reporting no effects of neonicotinoids on amphibian metamorphosis (Robinson et al., 2019), physiological or behavioural disturbances may occur (Gavel et al., 2019; Holtswarth et al., 2019).
Cropland adjacent vegetation may uptake neonicotinoids being a threat to herbivorous mammals. In a recent study exploring the effect of imidacloprid on deer Berheim et al. (2019) observed that their control group was contaminated with neonicotinoids due to possible different factors including the surrounding vegetation and neonicotinoid dust.
Future agriculture needs eco-inspired practices
Over the last 30 years, neonicotinoids have been used on a large scale in agriculture as effective insecticides against pests. Recent studies have shown that neonicotinoid compounds are accumulated in the environment being transported through soil and water system.
Evidence that 3 of the most used neonicotinoids (imidacloprid, clothianidin and thiamethoxam) have a serious negative impact on biodiversity, especially including bees and pollinators, has led European Union to take prohibitive measures regarding their use. So far neonicotinoid-based products could not be banned because of the lack of an effective and optimized alternative. However, promising results came from some eco-friendly and eco-inspired pests-preventing methods that are still under development. So far, we considered pest insects as our enemies, ignoring the natural competition that takes place since the oldest times. Nowadays, we realized we can use the natural enemies of pests to our advantage and this is how ladybugs (Zhao et al., 2020), wasps (Prezoto et al., 2019), entomopathogenic nematodes (Noosidum et al., 2021) and many more may become our allies in the near future.
As a last thought, without a feasible alternative, banning neonicotinoid-based products will eventually reduce the human impact on pollinators decline, but will let pests cause a significant decrease in agricultural production worldwide. Research efforts must continue and should be intensified in order to achieve effective alternatives to neonicotinoids as nowadays the dietary needs of the growing population require high yield crops.
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