Jump to content

Neonicotinoid

From Wikipedia, the free encyclopedia
The printable version is no longer supported and may have rendering errors. Please update your browser bookmarks and please use the default browser print function instead.

Neonicotinoids (sometimes shortened to neonics /ˈnnɪks/) are a class of neuro-active insecticides chemically similar to nicotine,[1] developed by scientists at Shell and Bayer in the 1980s.[2]

Neonicotinoids are among the widest-used insecticides in crop protection.[3] They are also widely employed for veterinary purposes including tick and flea control.[3] The first generation of neonicotinoids includes acetamiprid, clothianidin, dinotefuran, imidacloprid, nitenpyram, nithiazine, thiacloprid and thiamethoxam. The more recently-marketed generation of neonicotinoids includes cycloxaprid, imidaclothiz, paichongding, sulfoxaflor, guadipyr and flupyradifurone.[4] Imidacloprid has been the most widely used insecticide in the world from 1999[5] through at least 2018.[6][7]

Because they affect the central nervous system of insects, neonicotinoids kill or deleteriously affect a wide variety of both target and non-target insects.[8] They are often applied to seeds before planting as a prophylactic treatment against herbivorous insects. Neonicotinoids are water-soluble, so when the seed sprouts and grows, the developing plant absorbs the pesticide into its tissues as it takes in water.[9] Neonicotinoids can also be applied to the soil directly.[10] Once absorbed, neonicotinoids become present throughout the plant, including in its leaves, flowers, nectar, and pollen.[8]

Neonicotinoid use has been linked to adverse ecological effects, including risks to many non-target organisms, and specifically on bees and pollinators.[9][11][12] A 2018 review by the European Food Safety Authority (EFSA) concluded that most uses of neonicotinoid pesticides represent a risk to wild bees and honeybees.[11][13] In 2022 the United States Environmental Protection Agency (EPA) concluded that neonicotinoids are likely to adversely affect the majority of federally listed endangered or threatened species and of critical habitats.[12] Neonicotinoids widely contaminate wetlands, streams, and rivers, and due to their widespread use, pollinating insects are chronically exposed to them.[14][15] Sublethal effects from chronic low-level exposure to neonicotinoids in the environment are thought to be more common in bees than directly lethal effects. These effects upon bees include difficulty navigating, learning, and foraging, suppressed immune response, lower sperm viability, shortened lifespans of queens, and reduced numbers of new queens produced.[8]

In 2013, the European Union and some neighbouring countries restricted the use of certain neonicotinoids.[16][17][18][19][20][21] In 2018 the EU banned the three main neonicotinoids (clothianidin, imidacloprid and thiamethoxam) for all outdoor uses.[22][23] Several US states have restricted neonicotinoids out of concern for pollinators and bees.[24]

History

The precursor to nithiazine was first synthesized by Henry Feuer, a chemist at Purdue University, in 1970.[25][26][27]

Shell researchers found in screening that this precursor showed insecticide potential and refined it to develop nithiazine.[2]

In 1984 nithiazine's mode of action was found to be as a postsynaptic acetylcholine receptor agonist,[28] the same as nicotine. Nithiazine does not act as an acetylcholinesterase inhibitor,[28] in contrast to the organophosphate and carbamate insecticides. While nithiazine has the desired specificity (i.e. low mammalian toxicity), it is not photostable—that is, it breaks down in sunlight, and thus is not commercially viable.

In 1985, Bayer (Shinzo Kagabu) patented imidacloprid as the first commercial neonicotinoid.[29]

During the late 1990s, imidacloprid became widely used.[5][6][7][specify] Beginning in the early 2000s, two other neonicotinoids, clothianidin and thiamethoxam, entered the market[where?]. As of 2013, virtually all US corn was treated with one of these two insecticides.[30] As of 2014, about a third of US soybean acreage was planted with neonicotinoid-treated seeds, usually imidacloprid or thiamethoxam.[31]

Market

Neonicotinoids have been registered in more than 120 countries. With a global turnover of €1.5 billion in 2008, they represented 24% of the global insecticide market. The market grew from €155 million in 1990 to €5.50 billion in 2023.[32] Neonicotinoids make up as much as 43% of insecticide weight applied to seeds,[33] and accounted for 80% of all seed treatment sales in 2008.[34]

As of 2011, seven neonicotinoids from different companies were on the market.[34]

Name Company Products Turnover in million US$ (2009)
Imidacloprid Bayer CropScience Confidor, Admire, Gaucho, Advocate 1,091
Thiamethoxam Syngenta Actara, Platinum, Cruiser 627
Clothianidin Sumitomo Chemical/Bayer CropScience Poncho, Dantosu, Dantop, Belay 439
Acetamiprid Nippon Soda Mospilan, Assail, ChipcoTristar 276
Thiacloprid Bayer CropScience Calypso 112
Dinotefuran Mitsui Chemicals Starkle, Safari, Venom 79
Nitenpyram Sumitomo Chemical Capstar, Guardian 8

Agricultural usage

Efficacy

Imidacloprid is effective against sucking insects, some chewing insects, soil insects and fleas on domestic animals.[35] It is systemic with particular efficacy against sucking insects and has a long residual activity. Imidacloprid can be added to the water used to irrigate plants. Controlled release formulations of imidacloprid take 2–10 days to release 50% of imidacloprid in water.[36] It is applied against soil pests, seed, timber and animal pests as well as foliar treatments.

As of 2013 neonicotinoids were used in the U.S. on about 95 percent of corn and canola crops, the majority of cotton, sorghum, and sugar beets and about half of all soybeans. They have been used on the vast majority of fruit and vegetables, including apples, cherries, peaches, oranges, berries, leafy greens, tomatoes, and potatoes, to cereal grains, rice, nuts, and wine grapes.[37] Imidacloprid was possibly the most widely used insecticide, both within the neonicotinoids and in the worldwide market.[5][6][7]

Seed coatings

In agriculture, usefulness of neonicotinoid seed treatments for pest prevention depends upon the timing of planting and pest arrival. For soybeans, neonicotinoid seed treatments typically are not effective against the soybean aphid, because the compounds break down 35–42 days after planting, and soybean aphids typically are not present or at damaging population levels before this time.[38][39][40] Neonicotinoid seed treatments can protect yield in individual cases such as late-planted fields or in areas with large infestations much earlier in the growing season.[40] Overall yield gains are not expected from neonicotinoid seed treatments for soybean insect pests in the United States, and foliar insecticides are recommended instead when insects do reach damaging levels.[38] Health Canada estimated that neonicotinoids provide benefits equivalent to over 3% of the national farm gate value of corn and 1.5% to 2.1% of the national farm gate value of soybean in 2013 .[41]

Regulation

United States

The US EPA operates a 15-year registration review cycle for all pesticides.[42] The EPA granted a conditional registration to clothianidin in 2003.[43] The EPA issues conditional registrations when a pesticide meets the standard for registration, but there are outstanding data requirements.[44] Thiamethoxam is approved for use as an antimicrobial pesticide wood preservative and as a pesticide; it was first approved in 1999.[45] Imidacloprid was registered in 1994.[46]

As all neonicotinoids were registered after 1984, they were not subject to reregistration, but because of environmental concerns, especially concerning bees, the EPA opened dockets to evaluate them.[47] The registration review docket for imidacloprid opened in December 2008, and the docket for nithiazine opened in March 2009. To best take advantage of new research as it becomes available, the EPA moved ahead the docket openings for the remaining neonicotinoids on the registration review schedule (acetamiprid, clothianidin, dinotefuran, thiacloprid, and thiamethoxam) to FY 2012.[47] The EPA said that it expected to complete the review for the neonicotinoids in 2018.[48]

In March 2012, the Center for Food Safety, Pesticide Action Network, Beyond Pesticides and a group of beekeepers filed an Emergency Petition with the EPA asking the agency to suspend the use of clothianidin. The agency denied the petition.[48] In March 2013, the US EPA was sued by the same group, with the Sierra Club and the Center for Environmental Health joining, which accused the agency of performing inadequate toxicity evaluations and allowing insecticide registration based on inadequate studies.[48][49] The case, Ellis et al v. Bradbury et al, was stayed as of October 2013.[50]

On 12 July 2013, Rep. John Conyers, on behalf of himself and Rep. Earl Blumenauer, introduced the "Save American Pollinators Act" in the House of Representatives. The Act called for suspension of the use of four neonicotinoids, including the three recently suspended by the European Union, until their review is complete, and for a joint Interior Department and EPA study of bee populations and the possible reasons for their decline.[51] The bill was assigned to a congressional committee on 16 July 2013 and did not leave committee.[52]

The US EPA has taken a variety of actions to regulate neonicotinoids in response to concerns about pollinators.[53] In 2014, under the Obama administration, a blanket ban was issued against the use of neonicotinoids on National Wildlife Refuges in response to concerns about off-target effects of the pesticide, and a lawsuit from environmental groups. In 2018, the Trump administration reversed this decision, stating that decisions on neonicotinoid usage on farms in wildlife refuges will be made on a case by case basis.[54] In May 2019, the Environmental Protection Agency revoked approval for a dozen pesticides containing clothianidin and thiamethoxam as part of a legal settlement.[55]

European Union

The first neonic was approved in the EU in 2005.[56]

In 2008, Germany revoked the registration of clothianidin for use on seed corn after an incident that resulted in the death of millions of nearby honey bees.[57] An investigation revealed that it was caused by a combination of factors:

  • failure to use a polymer seed coating known as a "sticker";
  • weather conditions that resulted in late planting when nearby canola crops were in bloom;
  • a particular type of air-driven equipment used to sow the seeds which apparently blew clothianidin-laden dust off the seeds and into the air as the seeds were ejected from the machine into the ground;
  • dry and windy conditions at the time of planting that blew the dust into the nearby canola fields where honey bees were foraging.[58]

In Germany, clothianidin use was also restricted in 2008 for a short period on rapeseed. After it was shown that rapeseed treatment did not have the same problems as maize, its use was reinstated under the condition that the pesticide be fixed to the rapeseed grains by an additional sticker, so that abrasion dusts would not be released into the air.[59]

In 2009, the German Federal Office of Consumer Protection and Food Safety decided to continue to suspend authorization for clothianidin use on corn. It had not yet been fully clarified to what extent and in what manner bees come into contact with the active substances in clothianidin, thiamethoxam and imidacloprid when used on corn. The question of whether liquid emitted by plants via guttation, which bees ingest, posed an additional risk was unanswered.[60]

Neonicotinoid seed treatment is banned in Italy, but foliar use is allowed.[when?] This action was taken based on preliminary monitoring studies showing that bee losses were correlated with the application of seeds treated with these compounds; Italy based its decision on the known acute toxicity of these compounds to pollinators.[61][62]

In France, sunflower and corn seed treatment with imidacloprid are suspended; imidacloprid seed treatment for sugar beets and cereals are allowed, as is foliar use.[61][when?]

EU restrictions on use

In 2012, the European Commission asked the European Food Safety Authority (EFSA) to study the safety of three neonicotinoids, in response to growing concerns about the impact of neonicotinoids on honey bees. The study was published in January 2013, stating that neonicotinoids pose an unacceptably high risk to bees, and that the industry-sponsored science upon which regulatory agencies' claims of safety have relied may be flawed and contain data gaps not previously considered. Their review concluded, "A high acute risk to honey bees was identified from exposure via dust drift for the seed treatment uses in maize, rapeseed and cereals. A high acute risk was also identified from exposure via residues in nectar and/or pollen."[63][64] EFSA reached the following conclusions:[65][66]

  • Exposure from pollen and nectar. Only uses on crops not attractive to honey bees were considered acceptable.
  • Exposure from dust. A risk to honey bees was indicated or could not be excluded, with some exceptions, such as use on sugar beet and crops planted in glasshouses, and for the use of some granules.
  • Exposure from guttation. The only completed assessment was for maize treated with thiamethoxam. In this case, field studies showed an acute effect on honey bees exposed to the substance through guttation fluid.

EFSA's scientists identified a number of data gaps and were unable to finalize risk assessments for some uses authorized in the EU. EFSA also highlighted that risk to other pollinators should be further considered. The UK Parliament asked manufacturer Bayer Cropscience to explain discrepancies in the evidence they submitted.[67]

In response to the study, the European Commission recommended a restriction of their use across the European Union.[21] On 29 April 2013, 15 of the 27 EU member states voted to restrict the use of three neonicotinoids for two years starting 1 December 2013. Eight states voted against the ban, while four abstained. The law restricted the use of imidacloprid, clothianidin and thiamethoxam for seed treatment, soil application (granules) and foliar treatment in crops attractive to bees.[20][21] Temporary suspensions had previously been enacted in France, Germany, and Italy.[68] In Switzerland, where neonicotinoids were never used in alpine areas, neonics were banned because of accidental poisonings of bee populations and the relatively low safety margin for other beneficial insects.[69]

Environmentalists called the move "a significant victory for common sense and our beleaguered bee populations" and said it is "crystal clear that there is overwhelming scientific, political and public support for a ban."[21] The UK, which voted against the bill, disagreed: "Having a healthy bee population is a top priority for us, but we did not support the proposal for a ban because our scientific evidence doesn't support it."[21] Bayer Cropscience, which makes two of the three banned products, remarked "Bayer remains convinced neonicotinoids are safe for bees, when used responsibly and properly … clear scientific evidence has taken a back-seat in the decision-making process."[68] Reaction in the scientific community was mixed. Biochemist Lin Field said the decision was based on "political lobbying" and could lead to the overlooking of other factors involved in colony collapse disorder. Zoologist Lynn Dicks of Cambridge University disagreed, saying "This is a victory for the precautionary principle, which is supposed to underlie environmental regulation."[21] Simon Potts, Professor of Biodiversity and Ecosystem Services at Reading University, called the ban "excellent news for pollinators", and said, "The weight of evidence from researchers clearly points to the need to have a phased ban of neonicotinoids."[68]

The decision came up for review in 2016. In March 2017, The Guardian printed an article which claimed that they had obtained information that indicated that the European commission wanted a complete ban and cited "high acute risks to bees". A vote on the ban was expected in 2017 but delayed until early 2018 to assess the scientific findings.[70][71][72]

On 27 April 2018, member states of the European Union agreed upon a total ban on neonicotinoid insecticide use, except within closed greenhouses, to be imposed from the end of 2018.[73] The ban applies to the three main neonicotinoid active compounds: clothianidin, imidacloprid and thiamethoxam.[22][74] Use of the three compounds had been partially restricted in 2013.[75] The vote on the proposed ban followed a February 2018 report from the European Food Safety Authority which concluded that neonicotinoids posed a high risk to both domestic and wild bees.[76] Voting on the issue had previously been postponed on multiple occasions.[75] The ban had strong public support, but faced criticism from the agrochemical industry, and from certain farmers' groups.[73]

The ban on neonicotinoids caused jaundice devastation in certain sugar beet fields, reducing harvests in one of the world's largest beet sugar producers and endangering the industry. France subsequently extended the ban until 2023.[72][77][78]

Economic impact

In January 2013, the Humboldt Forum for Food and Agriculture e. V. (HFFA), a non-profit think tank, published a report on the value of neonicotinoids in the EU. At their website HFFA lists as their partners/supporters: BASF SE, the world's largest chemical company; Bayer CropScience, makers of products for crop protection and nonagricultural pest control; E.ON, an electric utility service provider; KWS Seed, a seed producer; and the food company Nestlé.

The study was supported by COPA-COGECA, the European Seed Association and the European Crop Protection Association, and financed by neonicotinoid manufacturers Bayer CropScience and Syngenta. The report looked at the short- and medium-term impacts of a complete ban of all neonicotinoids on agricultural and total value added (VA) and employment, global prices, land use and greenhouse gas (GHG) emissions. In the first year, agricultural and total VA would decline by €2.8 and €3.8 billion, respectively. The greatest losses would be in wheat, maize and rapeseed in the UK, Germany, Romania and France. 22,000 jobs would be lost, primarily in Romania and Poland, and agricultural incomes would decrease by 4.7%. In the medium-term (5-year ban), losses would amount to €17 billion in VA, and 27,000 jobs. The greatest income losses would affect the UK, while most jobs losses would occur in Romania. Following a ban, the lowered production would induce more imports of agricultural commodities into the EU. Agricultural production outside the EU would expand by 3.3 million hectares, leading to additional emissions of 600 million tons of carbon dioxide equivalent.[79] [citation needed]

When the report was released, Peter Melchett, policy director of the Soil Association, which has been working to ban neonicotinoids in the UK, commented that since the report was funded by Bayer Crop Sciences and Syngenta, "it was probably unlikely to conclude that neonicotinoids should be banned". The spokesperson further stated: "On the one hand, the chemical companies say we risk the additional costs to farmers amounting to £630 million. On the other, the possible cost of losing pollinating insects is thought to be worth three times as much (£1.8 billion*) to UK farmers."[80]

Canada

Use of pesticides in Canada is a matter of federal jurisdiction. In 2016, Health Canada proposed phasing out imidacloprid over the next three to five years.[81] The government has voiced concerns regarding the impact of neonics on bees, invertebrate waterspecies, and birds.

In Ontario, nearly all corn seeds and a majority of soybeans get treated with neonicotinoids. In the summer of 2015, the province passed a law to reduce the presence of neonicotinoids. Ontario's regulations were written to reduce the percent of seeds and beans covered with neonicotinoids to 20 percent within two years.[82]

On 10 December 2015, Montreal banned all neonicotinoids – without exception – on all properties within the city limits, including the Botanical Garden, all agricultural areas and all golf courses.[83] Agricultural businesses opposed Montreal's ban.[84]

In July 2016, British Columbia's largest city, Vancouver, banned the use of neonics within Vancouver city limits, where it was primarily being used to kill off chafer beetles living under home lawns.[85]

Oceania

On 11 October 2019, the Fiji government announced a ban on imidacloprid, effective 1 January 2020.[86]

Chemical activity and properties

Neonicotinoids, like nicotine, bind to nicotinic acetylcholine receptors (nAChRs) of a cell and trigger a response by that cell. In mammals, nicotinic acetylcholine receptors are located in cells of both the central nervous system and peripheral nervous systems. In insects these receptors are limited to the central nervous system. Nicotinic acetylcholine receptors are activated by the neurotransmitter acetylcholine. While low to moderate activation of these receptors causes nervous stimulation, high levels overstimulate and block the receptors,[5][35] causing paralysis and death. Acetylcholinesterase breaks down acetylcholine to terminate signals from these receptors. However, acetylcholinesterase cannot break down neonicotinoids and their binding is irreversible.[35]

Basis of selectivity

R-nicotine
Desnitro-imidacloprid
R-nicotine (top) and desnitro-imidacloprid are both protonated in the body

Mammals and insects have different composition of the receptor subunits and the structures of the receptors.[87][88] Because most neonicotinoids bind much more strongly to insect neuron receptors than to mammal neuron receptors, these insecticides are more toxic to insects than mammals.[5][87][88]

The low mammalian toxicity of imidacloprid has been explained by its inability to cross the blood–brain barrier because of the presence of a charged nitrogen atom at physiological pH. The uncharged molecule can penetrate the insect blood–brain barrier.[5]

Other neonicotinoids have a negatively charged nitro or cyano group, which interacts with a unique, positively charged amino acid residue present on insect, but not mammalian nAChRs.[89]

However, the breakdown product desnitro-imidacloprid, which is formed in a mammal's body during metabolism[87] as well as in environmental breakdown of imidacloprid,[90] has a charged nitrogen and shows high affinity to mammalian nAChRs.[87] Desnitro-imidacloprid is quite toxic to mice.[91]

Toxic action may result from the active ingredient itself or from its residue. 6-chloronicotinic acid is a common degradation product of multiple neonicotinoids.[92]

Persistence and half-life

Most neonicotinoids are water-soluble and break down slowly in the environment, so they can be taken up by the plant and provide protection from insects as the plant grows.[93] Independent studies show that the photodegradation half-life time of most neonicotinoids is around 34 days when exposed to sunlight. However, it might take up to 1,386 days (3.8 years) for these compounds to degrade in the absence of sunlight and micro-organism activity. Some researchers are concerned that neonicotinoids applied agriculturally might accumulate in aquifers.[94]

Environmental and species impact

Bees

A dramatic rise in the number of annual beehive losses noticed around 2006 spurred interest in factors potentially affecting honeybee health.[95][96] Many biological factors influence colony collapse disorder, including varroa mite infestation and Israeli acute paralysis virus (IAPV).[97][98] Despite much speculation on the role of neonicotinoids, many collapsing colonies show no trace of them.[99]

A review article (Carreck & Ratnieks, 2015) concluded that while laboratory based studies have demonstrated adverse sub-lethal effects of neonicotinoid insecticides on honey bees and bumble bees, these same effects have not been observed in field studies, which is likely due to an overestimation of three key dosage factors (concentration, duration and choice) in many laboratory based studies.[100]

In 2017, researchers demonstrated the combined effects of nutritional stress and low doses of common, widely used neonicotinoid pesticides (clothianidin, thiamethoxam) found in nectar and pollen. Their results provided the first demonstration that neonicotinoids and nutrition levels can synergistically interact and cause significant harm to animal survival, showing the complexity of neonicotinoid effects. In addition, the combined exposure reduced bee food consumption and hemolymph (bee blood) sugar levels.[101] Declines in managed and wild bee populations have been attributed, in part, to the combination of direct and indirect effects of neonicotinoids that render them vulnerable to pathogens.[102]

Almost all research into the negative effects of neonicotinoids has been conducted on honey bees, with little research investigating other bees such as bumblebees. However, some research has shown neonicotinoids affecting mason bees and bumblebees more negatively than honey bees, which are inconsistently affected.[8]

Research suggests potential toxicity to honey bees and other beneficial insects even with low levels of exposure, with sublethal effects that negatively impact the survival of colonies. In lab studies, neonicotinoids were shown to increase mortality rates[103] and negatively affect the ability to fly[104] and forage in exposed bees.[105] Neonicotinoids may also be responsible for detrimental effects on the bumblebee, another important pollinator.[106][107] In general, however, despite the fact that many laboratory studies have shown the potential for neonicotinoid toxicity, the majority of field studies have found only limited or no effects on honey bees.[103][100] Studies have shown a variety of sublethal effects of neonicotinoids on bumblebees, including lower reproduction rates, production of fewer workers and queens, and numerous behavioral changes. Sublethal exposure of bumblebee colonies to neonicotinoids alters foraging behaviors, often causing bees to forage less effectively and lowering colony growth and reproduction rates.[9]

In April 2015 EASAC conducted a study of the potential effects on organisms providing a range of ecosystem services like pollination and natural pest control which are critical to sustainable agriculture. The resulting report concludes "there is an increasing body of evidence that the widespread prophylactic use of neonicotinoids has severe negative effects on non-target organisms that provide ecosystem services including pollination and natural pest control."[108]

A 2015 systematic review (Lundin et al., 2015) of the scientific literature on neonicotinoids and bees concluded that despite considerable research efforts, there are still significant knowledge gaps concerning the impacts of neonicotinoids on bees.[109]

A 2017 survey covering every continent with honeybees found neonicotinoids in three-fourths of honey samples, albeit in every case at levels considered safe for human consumption.[110]

Birds

Neonicotinoids have adverse effects on bird populations.[111] Neonicotinoid dust intended for plants and seed coatings can spread throughout the air and seep into the water, which unintentionally affects non-target wildlife.[112]

Globally, 60% of neonicotinoids are used as seed coatings.[113] Some seed-eating bird species can be poisoned by neonicotinoid-coated seeds.[114] There have been reports of developmental abnormalities and reduced eggshell thickness, fertilization success, and embryo size with direct exposure to pesticides including neonicotinoids.[115] Some studies suggest burying neonicotinoid seeds used for agriculture below the surface of the soil will prevent birds from eating them.[115]

Neonicotinoids can have non-direct impacts on birds by disrupting the food chain.[116] The main goal of neonicotinoids is to target pests. However, this negatively affects insectivorous bird populations that rely on these insects for food.[117][118][116][119][120]

Neonicotinoids can also leach into soil, accumulating in bodies of water that normally incubate insects.[118] A 2014 observational study conducted in the Netherlands correlated declines in some bird populations with environmental imidacloprid residues, although it stopped short of concluding that the association was casual.[116]

Other wildlife

In March 2013, the American Bird Conservancy published a commentary on 200 studies on neonicotinoids calling for a ban on neonicotinoid use as seed treatments because of their toxicity to birds, aquatic invertebrates, and other wildlife.[121]

A 2013 Dutch study found that water containing allowable concentrations of imidacloprid had 50% fewer invertebrate species compared with uncontaminated water.[122][123] A later study found the analysis was confounded with other co-occurring insecticides and did not show imidacloprid directly affected invertebrate diversity.[124]

A 2014 review took a broader look at the ecological impact of neonicotinoids and fipronil, finding negative effects on invertebrates, but not microbes or fish.[125] Although not yet conclusive, there is increasing evidence that neonicotinoids can have negative effects on pollinating insects other than bees, including monarch butterflies. Some evidence has linked neonicotinoids to reduced numbers of monarch eggs that are hatched.[126][127][128][129] However, the effects of neonicotinoids on butterflies and moths have been studied very little.[9]

Harms to mammalian nervous systems

Rodents exposed chronically or acutely to neonicotinoids suffer major damage to their nervous systems, likely due to impairment of their neurotransmitter mechanisms. Laboratory studies showed that such major neurological damage resulted both when the exposure occurred during the embryonic period and when the exposure occurred during adulthood. Impairments to cognitive ability and to memory were observed. Neonicotinoid exposure at an early age was shown to impair neuronal development, with decreases in neurogenesis and induced neuroinflammation. Adult exposure induced neurobehavioral toxicity and resulting changes in neurochemicals.[130]

See also

References

  1. ^ "Neonicotinoid Pesticides & Adverse Health Outcomes". ntp.niehs.nih.gov. National Toxicology Program. Retrieved 20 November 2019.
  2. ^ a b Kollmeyer WD, Flattum RF, Foster JP, Powell JE, Schroeder ME, Soloway SB (1999). "Discovery of the Nitromethylene Heterocycle Insecticides". In Yamamoto I, Casida J (eds.). Nicotinoid Insecticides and the Nicotinic Acetylcholine Receptor. Tokyo: Springer-Verlag. pp. 71–89. ISBN 978-4-431-70213-9.
  3. ^ a b Jeschke, Peter; Nauen, Ralf; Schindler, Michael; Elbert, Alfred (21 June 2010). "Overview of the Status and Global Strategy for Neonicotinoids". Journal of Agricultural and Food Chemistry. 59 (7). American Chemical Society (ACS): 2897–2908. doi:10.1021/jf101303g. ISSN 0021-8561. PMID 20565065.
  4. ^ Giorio C, Safer A, Sánchez-Bayo F, Tapparo A, Lentola A, Girolami V, et al. (March 2021). "An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 1: new molecules, metabolism, fate, and transport". Environmental Science and Pollution Research International. 28 (10): 11716–11748. Bibcode:2021ESPR...2811716G. doi:10.1007/s11356-017-0394-3. PMC 7920890. PMID 29105037.
  5. ^ a b c d e f Yamamoto I (1999). "Nicotine to Nicotinoids: 1962 to 1997". In Yamamoto I, Casida J (eds.). Nicotinoid Insecticides and the Nicotinic Acetylcholine Receptor. Tokyo: Springer-Verlag. pp. 3–27. ISBN 978-4-431-70213-9.
  6. ^ a b c Casida JE (January 2018). "Neonicotinoids and Other Insect Nicotinic Receptor Competitive Modulators: Progress and Prospects". Annual Review of Entomology. 63 (1). Annual Reviews: 125–144. doi:10.1146/annurev-ento-020117-043042. PMID 29324040.
  7. ^ a b c Ihara M, Matsuda K (December 2018). "Neonicotinoids: molecular mechanisms of action, insights into resistance and impact on pollinators". Current Opinion in Insect Science. 30. Elsevier: 86–92. Bibcode:2018COIS...30...86I. doi:10.1016/j.cois.2018.09.009. PMID 30553491. S2CID 58767188.
  8. ^ a b c d Hladik ML, Main AR, Goulson D (March 2018). "Environmental Risks and Challenges Associated with Neonicotinoid Insecticides". Environmental Science & Technology. 52 (6): 3329–3335. Bibcode:2018EnST...52.3329H. doi:10.1021/acs.est.7b06388. PMID 29481746.
  9. ^ a b c d Wood TJ, Goulson D (July 2017). "The environmental risks of neonicotinoid pesticides: a review of the evidence post 2013". Environmental Science and Pollution Research International. 24 (21): 17285–17325. Bibcode:2017ESPR...2417285W. doi:10.1007/s11356-017-9240-x. PMC 5533829. PMID 28593544.
  10. ^ "What is a neonicotinoid? - Insects in the City". Texas A&M AgriLife Extension.
  11. ^ a b "Neonicotinoids: risks to bees confirmed | EFSA". www.efsa.europa.eu. 28 February 2018. Retrieved 23 June 2023.
  12. ^ a b US EPA, OCSPP (16 June 2022). "EPA Finalizes Biological Evaluations Assessing Potential Effects of Three Neonicotinoid Pesticides on Endangered Species". www.epa.gov. Retrieved 23 June 2023.
  13. ^ "Conclusion on the peer review of the pesticide risk assessment for bees for the active substance clothianidin". EFSA Journal. 11: 3066. 2013. doi:10.2903/j.efsa.2013.3066.
  14. ^ Stehle S, Ovcharova V, Wolfram J, Bub S, Herrmann LZ, Petschick LL, Schulz R (April 2023). "Neonicotinoid insecticides in global agricultural surface waters - Exposure, risks and regulatory challenges". The Science of the Total Environment. 867: 161383. Bibcode:2023ScTEn.86761383S. doi:10.1016/j.scitotenv.2022.161383. PMID 36621497. S2CID 255534366.
  15. ^ Berens MJ, Capel PD, Arnold WA (April 2021). "Neonicotinoid Insecticides in Surface Water, Groundwater, and Wastewater Across Land-Use Gradients and Potential Effects". Environmental Toxicology and Chemistry. 40 (4): 1017–1033. Bibcode:2021EnvTC..40.1017B. doi:10.1002/etc.4959. PMC 8049005. PMID 33301182.
  16. ^ Cressey D (April 2013). "Europe debates risk to bees". Nature. 496 (7446): 408. Bibcode:2013Natur.496..408C. doi:10.1038/496408a. PMID 23619669.
    Gill RJ, Ramos-Rodriguez O, Raine NE (November 2012). "Combined pesticide exposure severely affects individual- and colony-level traits in bees". Nature. 491 (7422): 105–108. Bibcode:2012Natur.491..105G. doi:10.1038/nature11585. PMC 3495159. PMID 23086150.
  17. ^ Dicks L (February 2013). "Bees, lies and evidence-based policy". Nature. 494 (7437): 283. Bibcode:2013Natur.494..283D. doi:10.1038/494283a. PMID 23426287.
    Stoddart C (2012). "The buzz about pesticides". Nature. doi:10.1038/nature.2012.11626. S2CID 208530336.
  18. ^ Osborne JL (November 2012). "Ecology: Bumblebees and pesticides". Nature. 491 (7422): 43–45. Bibcode:2012Natur.491...43O. doi:10.1038/nature11637. PMID 23086148. S2CID 532877.
  19. ^ Cressey D (2013). "Reports spark row over bee-bothering insecticides". Nature. doi:10.1038/nature.2013.12234. S2CID 88428354.
  20. ^ a b "Bees & Pesticides: Commission goes ahead with plan to better protect bees". European Commission. 30 May 2013. Archived from the original on 6 November 2013.
  21. ^ a b c d e f McDonald-Gibson C (29 April 2013). "'Victory for bees' as European Union bans neonicotinoid pesticides blamed for destroying bee population". The Independent. Archived from the original on 1 May 2013. Retrieved 1 May 2013.
  22. ^ a b Carrington D (27 April 2018). "EU agrees total ban on bee-harming pesticides". The Guardian. Retrieved 29 April 2018.
  23. ^ "EU nations back ban on insecticides to protect honey bees". Reuters. 27 April 2018. Archived from the original on 27 April 2018. Retrieved 27 April 2018.
  24. ^ "Minnesota Cracks Down On Neonic Pesticides, Promising Aid To Bees". NPR.org. Retrieved 3 May 2018.
  25. ^ Feuer H, Lawrence JP (1969). "The alkyl nitrate nitration of active methylene compounds. VI. A new synthesis of α-nitroalkyl heterocyclics". Journal of the American Chemical Society. 91 (7): 1856–1857. doi:10.1021/ja01035a049.
  26. ^ Jeschke P, Nauen R (2010). "Chapter 3: Neonicotinoid insecticides". In Gilbert LI, Gill S (eds.). Insect Control: Biological and Synthetic Agents. London, England: Academic Press. p. 62. ISBN 978-0-12-381450-0.
  27. ^ Schaefer B (2015). Natural Products in the Chemical Industry. Translated by Smith D, Janssen B. Berlin, Germany: Springer Verlag. p. 734. ISBN 978-3-642-54461-3.
  28. ^ a b Schroeder ME, Flattum RF (1984). "The mode of action and neurotoxic properties of the nitromethylene heterocycle insecticides". Pesticide Biochemistry and Physiology. 22 (2): 148–160. Bibcode:1984PBioP..22..148S. doi:10.1016/0048-3575(84)90084-1.
  29. ^ Tomizawa M, Casida JE (2005). "Neonicotinoid insecticide toxicology: mechanisms of selective action". Annual Review of Pharmacology and Toxicology. 45: 247–268. doi:10.1146/annurev.pharmtox.45.120403.095930. PMID 15822177. S2CID 33621512.
  30. ^ Stokstad E (May 2013). "Pesticides under fire for risks to pollinators". Science. 340 (6133): 674–676. Bibcode:2013Sci...340..674S. doi:10.1126/science.340.6133.674. PMID 23661734.
  31. ^ "Benefits of Neonicotinoid Seed Treatments to Soybean Production" (PDF). U.S. Environmental Protection Agency. 15 October 2014. Archived from the original (PDF) on 17 October 2014.
  32. ^ "Neonicotinoid Pesticide Market by Type (Imidacloprid, Thiacloprid, Thiamethoxam, Acetamiprid), By Crops (Cereals, Oilseed, Pulses, Fruits, Vegetables and Others) and Region, Global trends and forecast from 2024 to 2030". Exactitude Consultancy. Retrieved 14 March 2024.
  33. ^ Douglas, Margaret R.; Esker, Paul D.; Wechsler, Seth; Code, Aimee; Smith, David J.; Hitaj, Claudia (2020). "Sowing Uncertainty: What We do and Don't Know about the Planting of Pesticide-Treated Seed". BioScience. pp. 390–403. doi:10.1093/biosci/biaa019. Retrieved 13 November 2024.
  34. ^ a b Jeschke P, Nauen R, Schindler M, Elbert A (April 2011). "Overview of the status and global strategy for neonicotinoids". Journal of Agricultural and Food Chemistry. 59 (7): 2897–2908. Bibcode:2011JAFC...59.2897J. doi:10.1021/jf101303g. PMID 20565065.
  35. ^ a b c Gervais JA, Luukinen B, Buhl K, Stone D (April 2010). "Imidacloprid Technical Fact Sheet" (PDF). National Pesticide Information Center. Archived (PDF) from the original on 11 April 2012. Retrieved 12 April 2012.
  36. ^ Adak T, Kumar J, Shakil NA, Walia S (2012). "Development of controlled release formulations of imidacloprid employing novel nano-ranged amphiphilic polymers". Journal of Environmental Science and Health. Part. B, Pesticides, Food Contaminants, and Agricultural Wastes. 47 (3): 217–225. Bibcode:2012JESHB..47..217A. doi:10.1080/03601234.2012.634365. PMID 22375594. S2CID 8121408.
  37. ^ Grossman E (30 April 2013). "Declining Bee Populations Pose A Threat to Global Agriculture". Yale Environment 360. Yale School of Forestry & Environmental Studies. Archived from the original on 9 November 2014. Retrieved 9 November 2014.
  38. ^ a b Myers C (15 October 2014). "Benefits of Neonicotinoid Seed Treatments to Soybean Production" (PDF). Letter to Neil Anderson. US EPA. Archived (PDF) from the original on 17 October 2014. Retrieved 6 November 2014.
  39. ^ Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N (September 2010). "Ecology and management of the soybean aphid in North America" (PDF). Annual Review of Entomology. 56: 375–399. doi:10.1146/annurev-ento-120709-144755. PMID 20868277. Archived from the original (PDF) on 7 November 2014. Retrieved 7 November 2014.
  40. ^ a b Hodgson EW, McCornack BP, Tilmon K, Knodel JJ (2012). "Management Recommendations for Soybean Aphid (Hemiptera: Aphididae) in the United States". Journal of Integrated Pest Management. 3: E1–E10. doi:10.1603/IPM11019.
  41. ^ "Re-evaluation Note REV2016-03, Value Assessment of Corn and Soybean Seed Treatment Use of Clothianidin, Imidacloprid and Thiamethoxam". 6 January 2016. Archived from the original on 25 January 2016.
  42. ^ "Registration Review Process". U.S. Environmental Protection Agency. 17 April 2014. Archived from the original on 11 July 2014. Retrieved 7 June 2014.
  43. ^ "Pesticide Fact Sheet: Clothianidin" (PDF). U.S. Environmental Protection Agency. Archived from the original (PDF) on 26 March 2014. Conditional Registration, Issued 30 May 2003
  44. ^ "Conditional Pesticide Registration". U.S. Environmental Protection Agency. 17 April 2014. Archived from the original on 14 September 2014. Retrieved 7 June 2014.
  45. ^ "Thiamethoxam Summary Document Registration Review Initial Docket". U.S. Environmental Protection Agency. 21 December 2011. Archived from the original on 3 May 2015.
  46. ^ "Imidacloprid Summary Document". U.S. Environmental Protection Agency. 17 December 2008. Archived from the original on 3 May 2015.
  47. ^ a b "Groups of Pesticides in Registration Review: Neonicotinoids". U.S. Environmental Protection Agency. 17 April 2014. Archived from the original on 11 July 2014. Retrieved 7 June 2014.
  48. ^ a b c "Beekeepers and Public Interest Groups Sue EPA Over Bee-Toxic Pesticides". Press release: Pesticide Action Network, Center for Food Safety, and Beyond Pesticides. 21 March 2013. Archived from the original on 1 July 2014.
  49. ^ Carrington D (22 March 2013). "US government sued over use of pesticides linked to bee harm". The Guardian. Archived from the original on 12 February 2014. Retrieved 25 March 2013.
  50. ^ "Ellis et al v. Bradbury et al". Justia Dockets & Filings. Archived from the original on 19 May 2015. Retrieved 7 June 2014.
  51. ^ "Legislation to restrict pesticide use proposed by Rep. Blumenauer". The Oregonian at 'OregonLive'. 12 July 2013. Archived from the original on 3 September 2013. Retrieved 17 July 2013.
  52. ^ "H.R. 2692: Saving America's Pollinators Act of 2013". Govtrack.us. Archived from the original on 28 September 2014. Retrieved 7 June 2014.
  53. ^ "EPA Actions to Protect Pollinators". US EPA. 3 September 2013. Retrieved 24 March 2019.
  54. ^ "Trump administration lifts ban on pesticides linked to declining bee numbers". The Guardian. 4 August 2018. Retrieved 24 March 2019.
  55. ^ Allington A (21 May 2019). "EPA Curbs Use of 12 Bee-Harming Pesticides". Bloomberg. Retrieved 1 July 2019.
  56. ^ "Neonicotinoids". Food Safety. Retrieved 24 July 2021.
  57. ^ Benjamin A (23 May 2008). "Pesticides: Germany bans chemicals linked to honeybee devastation". The Guardian. Archived from the original on 2 September 2013.
  58. ^ "EPA Acts to Protect Bees | Pesticides | US EPA". Epa.gov. Archived from the original on 4 February 2011. Retrieved 11 October 2011.
  59. ^ "Background information: Bee losses caused by insecticidal seed treatment in Germany in 2008". German Federal Office of Consumer Protection and Food Safety (BVL). 15 July 2008. Archived from the original on 5 October 2011.
  60. ^ "Maize seed may now be treated with "Mesurol flüssig" again". German Federal Office of Consumer Protection and Food Safety (BVL). 9 February 2009. Archived from the original on 5 October 2011.
  61. ^ a b "Colony Collapse Disorder: European Bans on Neonicotinoid Pesticides – Pesticides – US EPA". epa.gov. 23 June 2010. Archived from the original on 4 September 2011. Retrieved 24 July 2021.
  62. ^ Keim B (13 December 2010). "Leaked Memo Shows EPA Doubts About Bee-Killing Pesticide". Wired. Archived from the original on 2 June 2012.
  63. ^ "Conclusion on the peer review of the pesticide risk assessment for bees for the active substance clothianidin". EFSA Journal. 11 (1). European Food Safety Authority: 3066. 2013. doi:10.2903/j.efsa.2013.3066.
  64. ^ "Assessment of the scientific information from the Italian project 'APENET' investigating effects on honeybees of coated maize seeds with some neonicotinoids and fipronil". EFSA Journal. 10 (6). European Food Safety Authority: 2792. 2012. doi:10.2903/j.efsa.2012.2792.
  65. ^ EFSA identifies risks to bees from neonicotinoids efsa.europa.eu 16 January 2013.
  66. ^ "Conclusion on the peer review of the pesticide risk assessment for bees for the active substance clothianidin". EFSA Journal. 11 (1). European Food Safety Authority: 3066. 2013. doi:10.2903/j.efsa.2013.3066.
  67. ^ Carrington D (16 January 2013). "Insecticide 'unacceptable' danger to bees, report finds". The Guardian. Archived from the original on 24 August 2013.
  68. ^ a b c Carrington D (29 April 2013). "Bee-harming pesticides banned in Europe". The Guardian. Archived from the original on 20 August 2013. Retrieved 1 May 2013.
  69. ^ "Insektizide und Bienen: Was soll die Einschränkung der Neonicotinoide bringen? - NZZ.ch". Neue Zürcher Zeitung (in German). 8 May 2013. Retrieved 24 July 2021.
  70. ^ Carrington D (23 March 2017). "Europe poised for total ban on bee-harming pesticides". The Guardian. Archived from the original on 30 June 2017. Retrieved 4 July 2017.
  71. ^ Stokstad E (28 February 2018). "European agency concludes controversial 'neonic' pesticides threaten bees". Science Mag. Archived from the original on 7 March 2018. Retrieved 4 April 2018.
  72. ^ a b "French firm breeds plants that resist climate change". European Investment Bank. Retrieved 25 January 2023.
  73. ^ a b Carrington D. "EU agrees total ban on bee-harming pesticides". The Guardian. Archived from the original on 27 April 2018. Retrieved 27 April 2018.
  74. ^ "EU to fully ban neonicotinoid insecticides to protect bees". Reuters. 27 April 2018. Retrieved 29 April 2018.
  75. ^ a b McGrath M (27 April 2018). "EU member states support near-total neonicotinoids ban". BBC. Retrieved 29 April 2018.
  76. ^ Butler D (28 February 2018). "EU expected to vote on pesticide ban after major scientific review". Nature. 555 (7695): 150–151. Bibcode:2018Natur.555..150B. doi:10.1038/d41586-018-02639-1.
  77. ^ "Sugar beet farmers cry foul after French U-turn on bee-killing pesticide". RFI. 25 January 2023. Retrieved 25 January 2023.
  78. ^ Kiš N (25 January 2023). "French farmers warn pesticide u-turn will impact output". Brussels Morning Newspaper. Retrieved 25 January 2023.
  79. ^ Noleppa S, Hahn T (2013). "The value of Neonicotinoid seed treatment in the European Union: A socio-economic, technological and environmental review" (PDF). Humboldt Forum for Food and Agriculture (HFFA). Archived from the original (PDF) on 15 October 2013.
  80. ^ "Soil Association comment: The Humboldt Forum for Food and Agriculture report". Soil Association Certification. 15 January 2013. Archived from the original on 14 July 2014.
  81. ^ "Ban on controversial pesticide proposed by Health Canada". CBC News. Archived from the original on 14 February 2018. Retrieved 24 February 2018.
  82. ^ "Ontario wants 80% reduction of bee-killing neonicotinoid use in 2 years". CBC News. Toronto, Ontario, Canada: CBC/Radio-Canada. 9 June 2015. Archived from the original on 17 September 2015. Retrieved 29 September 2015.
  83. ^ "Montreal neonicotinoid ban". City of Montreal. 10 December 2015. Archived from the original on 27 April 2018. Retrieved 10 December 2015.
  84. ^ "CropLife Canada highlights safety of neonics amid Montreal's pesticide ban". Crop Protection News. 12 June 2015. Archived from the original on 30 September 2015. Retrieved 29 September 2015.
  85. ^ "Bee-killing pesticides banned in Vancouver". CBC News. Archived from the original on 6 March 2018. Retrieved 24 February 2018.
  86. ^ "Paraquat, Imidacloprid Pesticide To Be Banned From January, 2020". Retrieved 11 October 2019.
  87. ^ a b c d Tomizawa M (2004). "Neonicotinoids and Derivatives: Effects in Mammalian Cells and Mice". Journal of Pesticide Science. 29 (3): 177–183. doi:10.1584/jpestics.29.177.
  88. ^ a b Tomizawa M, Latli B, Casida JE (1999). "Structure and Function of Insect Nicotinic Acetylcholine Receptors Studied with Nicotinic Insecticide Affinity Probes". In Yamamoto I, Casida JE (eds.). Nicotinoid Insecticides and the Nicotinic Acetylcholine Receptor. Tokyo: Springer-Verlag. pp. 271–292. ISBN 978-4-431-70213-9.
  89. ^ Tomizawa M, Casida JE (2003). "Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors". Annual Review of Entomology. 48: 339–364. doi:10.1146/annurev.ento.48.091801.112731. PMID 12208819.
  90. ^ Koshlukova S (9 February 2006). "Imidacloprid: Risk Characterization Document: Dietary and Drinking Water Exposure" (PDF). California Environmental Protection Agency, Department of Pesticide Regulation. Archived (PDF) from the original on 27 December 2011. Retrieved 11 April 2012.
  91. ^ Chao SL, Casida JE (1997). "Interaction of Imidacloprid Metabolites and Analogs with the Nicotinic Acetylcholine Receptor of Mouse Brain in Relation to Toxicity". Pesticide Biochemistry and Physiology. 58 (1): 77–88. Bibcode:1997PBioP..58...77L. doi:10.1006/pest.1997.2284.
  92. ^ Blacquière T, Smagghe G, van Gestel CA, Mommaerts V (May 2012). "Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment". Ecotoxicology. 21 (4). Springer Science+Business Media: 973–992. Bibcode:2012Ecotx..21..973B. doi:10.1007/s10646-012-0863-x. PMC 3338325. PMID 22350105.
  93. ^ Giorio, Chiara; Safer, Anton; Sánchez-Bayo, Francisco; Tapparo, Andrea; Lentola, Andrea; Girolami, Vincenzo; van Lexmond, Maarten Bijleveld; Bonmatin, Jean-Marc (March 2021). "An update of the Worldwide Integrated Assessment (WIA) on systemic insecticides. Part 1: new molecules, metabolism, fate, and transport". Environmental Science and Pollution Research. 28 (10): 11716–11748. Bibcode:2021ESPR...2811716G. doi:10.1007/s11356-017-0394-3. ISSN 0944-1344. PMC 7920890. PMID 29105037.
  94. ^ "Interview with microbiologist: "This place is filled with multinational lobbyists"". Delo.si. 14 May 2011. Archived from the original on 20 September 2011. Retrieved 11 October 2011.
  95. ^ Copping J (1 April 2007). "Flowers and fruit crops facing disaster as disease kills off bees". The Telegraph. Archived from the original on 20 October 2017.
  96. ^ Vanengelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, Nguyen BK, et al. (August 2009). Brown J (ed.). "Colony collapse disorder: a descriptive study". PLOS ONE. 4 (8): e6481. Bibcode:2009PLoSO...4.6481V. doi:10.1371/journal.pone.0006481. PMC 2715894. PMID 19649264.
  97. ^ Watanabe M (May 2008). "Colony Collapse Disorder: Many Suspects, No Smoking Gun". BioScience. 58 (5): 384–388. doi:10.1641/b580503. S2CID 85798698.
  98. ^ USDA (17 October 2012). Report on the National Stakeholders Conference on Honey Bee Health National Honey Bee Health Stakeholder Conference Steering Committee (PDF) (Report). Archived from the original (PDF) on 20 May 2014. Retrieved 4 June 2014.
  99. ^ Cepero A, Ravoet J, Gómez-Moracho T, Bernal JL, Del Nozal MJ, Bartolomé C, et al. (September 2014). "Holistic screening of collapsing honey bee colonies in Spain: a case study". BMC Research Notes. 7: 649. doi:10.1186/1756-0500-7-649. PMC 4180541. PMID 25223634.
  100. ^ a b Carreck NL (2014). "The dose makes the poison: have "field realistic" rates of exposure of bees to neonicotinoid insecticides been overestimated in laboratory studies?" (PDF). Journal of Apicultural Research. 53 (5): 607–614. Bibcode:2014JApiR..53..607C. doi:10.3896/IBRA.1.53.5.08. S2CID 15038464.
  101. ^ Tosi S, Nieh JC, Sgolastra F, Cabbri R, Medrzycki P (December 2017). "Neonicotinoid pesticides and nutritional stress synergistically reduce survival in honey bees". Proceedings. Biological Sciences. 284 (1869): 20171711. doi:10.1098/rspb.2017.1711. PMC 5745400. PMID 29263280.
  102. ^ Sánchez-Bayo F, Goulson D, Pennacchio F, Nazzi F, Goka K, Desneux N (2016). "Are bee diseases linked to pesticides? - A brief review". Environment International. 89–90. Elsevier BV: 7–11. Bibcode:2016EnInt..89....7S. doi:10.1016/j.envint.2016.01.009. PMID 26826357.
  103. ^ a b "Neonicotinoids". Pollinator Network @ Cornell. Retrieved 10 May 2019.
  104. ^ Tosi S, Burgio G, Nieh JC (April 2017). "A common neonicotinoid pesticide, thiamethoxam, impairs honey bee flight ability". Scientific Reports. 7 (1): 1201. Bibcode:2017NatSR...7.1201T. doi:10.1038/s41598-017-01361-8. PMC 5430654. PMID 28446783.
  105. ^ "What is a neonicotinoid? Insects in the City". Citybugs.tamu.edu. Archived from the original on 15 May 2013. Retrieved 2 May 2013.
  106. ^ Whitehorn PR, O'Connor S, Wackers FL, Goulson D (April 2012). "Neonicotinoid pesticide reduces bumble bee colony growth and queen production". Science. 336 (6079): 351–352. Bibcode:2012Sci...336..351W. doi:10.1126/science.1215025. PMID 22461500. S2CID 2738787.
  107. ^ Rundlöf M, Andersson GK, Bommarco R, Fries I, Hederström V, Herbertsson L, et al. (May 2015). "Seed coating with a neonicotinoid insecticide negatively affects wild bees". Nature. 521 (7550): 77–80. Bibcode:2015Natur.521...77R. doi:10.1038/nature14420. PMID 25901681. S2CID 4468879.
  108. ^ EASAC (8 April 2015). "Ecosystem services, agriculture and neonicotinoids" (PDF). Archived (PDF) from the original on 15 April 2015. Retrieved 10 April 2015. There is an increasing body of evidence that the widespread prophylactic use of neonicotinoids has severe negative effects on non-target organisms that provide ecosystem services including pollination and natural pest control.
  109. ^ Lundin O, Rundlöf M, Smith HG, Fries I, Bommarco R (2015). "Neonicotinoid Insecticides and Their Impacts on Bees: A Systematic Review of Research Approaches and Identification of Knowledge Gaps". PLOS ONE. 10 (8): e0136928. Bibcode:2015PLoSO..1036928L. doi:10.1371/journal.pone.0136928. PMC 4552548. PMID 26313444.
  110. ^ Hamers L (5 October 2017). "Much of the world's honey now contains bee-harming pesticides; Global survey finds neonicotinoids in three-fourths of samples". Sciencenews.org. Archived from the original on 7 October 2017. Retrieved 6 October 2017.
  111. ^ Molenaar, Elke; Viechtbauer, Wolfgang; van de Crommenacker, Janske; Kingma, Sjouke A. (October 2024). "Neonicotinoids Impact All Aspects of Bird Life: A Meta-Analysis". Ecology Letters. 27 (10): e14534. Bibcode:2024EcolL..27E4534M. doi:10.1111/ele.14534. ISSN 1461-023X. PMID 39385588.
  112. ^ Goulson D (July 2014). "Ecology: Pesticides linked to bird declines". Nature. 511 (7509): 295–296. Bibcode:2014Natur.511..295G. doi:10.1038/nature13642. PMID 25030159. S2CID 4448389.
  113. ^ MacDonald AM, Jardine CM, Thomas PJ, Nemeth NM (June 2018). "Neonicotinoid detection in wild turkeys (Meleagris gallopavo silvestris) in Ontario, Canada". Environmental Science and Pollution Research International. 25 (16): 16254–16260. Bibcode:2018ESPR...2516254M. doi:10.1007/s11356-018-2093-0. PMC 5984634. PMID 29704179.
  114. ^ Millot F, Decors A, Mastain O, Quintaine T, Berny P, Vey D, et al. (February 2017). "Field evidence of bird poisonings by imidacloprid-treated seeds: a review of incidents reported by the French SAGIR network from 1995 to 2014". Environmental Science and Pollution Research International. 24 (6). Springer Science and Business Media LLC: 5469–5485. Bibcode:2017ESPR...24.5469M. doi:10.1007/s11356-016-8272-y. PMC 5352772. PMID 28028702.
  115. ^ a b Gibbons D, Morrissey C, Mineau P (January 2015). "A review of the direct and indirect effects of neonicotinoids and fipronil on vertebrate wildlife". Environmental Science and Pollution Research International. 22 (1): 103–118. Bibcode:2015ESPR...22..103G. doi:10.1007/s11356-014-3180-5. PMC 4284370. PMID 24938819.
  116. ^ a b c Hallmann CA, Foppen RP, van Turnhout CA, de Kroon H, Jongejans E (July 2014). "Declines in insectivorous birds are associated with high neonicotinoid concentrations". Nature. 511 (7509): 341–343. Bibcode:2014Natur.511..341H. doi:10.1038/nature13531. hdl:2066/130120. PMID 25030173. S2CID 4464169.
  117. ^ Humann-Guilleminot S, Binkowski ŁJ, Jenni L, Hilke G, Glauser G, Helfenstein F (2019). "A nation-wide survey of neonicotinoid insecticides in agricultural land with implications for agri-environment schemes". Journal of Applied Ecology. 56 (7): 1502–1514. Bibcode:2019JApEc..56.1502H. doi:10.1111/1365-2664.13392. S2CID 133107567.
  118. ^ a b Royte E (24 March 2017). "The Same Pesticides Linked to Bee Declines Might Also Threaten Birds". National Audubon Society. Retrieved 14 January 2021.
  119. ^ Brain RA, Anderson JC (July 2019). "The agro-enabled urban revolution, pesticides, politics, and popular culture: a case study of land use, birds, and insecticides in the USA". Environmental Science and Pollution Research International. 26 (21): 21717–21735. Bibcode:2019ESPR...2621717B. doi:10.1007/s11356-019-05305-9. PMC 6647523. PMID 31129901.
  120. ^ Bowler DE, Heldbjerg H, Fox AD, de Jong M, Böhning-Gaese K (October 2019). "Long-term declines of European insectivorous bird populations and potential causes". Conservation Biology. 33 (5): 1120–1130. Bibcode:2019ConBi..33.1120B. doi:10.1111/cobi.13307. PMID 30912605. S2CID 85517845.
  121. ^ Mineau P, Palmer C (March 2013). "The Impact of the Nation's Most Widely Used Insecticides on Birds" (PDF). Neonicotinoid Insecticides and Birds. American Bird Conservancy. Archived (PDF) from the original on 18 April 2013. Retrieved 19 March 2013.
  122. ^ Van Dijk TC, Van Staalduinen MA, Van der Sluijs JP (1 May 2013). "Macro-invertebrate decline in surface water polluted with imidacloprid". PLOS ONE. 8 (5): e62374. Bibcode:2013PLoSO...862374V. doi:10.1371/journal.pone.0062374. PMC 3641074. PMID 23650513.
  123. ^ "Study links insecticide use to invertebrate die-offs". www.guardian.com. 1 May 2013. Archived from the original on 24 August 2013. Retrieved 3 September 2013.
  124. ^ Vijver MG, van den Brink PJ (28 February 2014). "Macro-invertebrate decline in surface water polluted with imidacloprid: a rebuttal and some new analyses". PLOS ONE. 9 (2): e89837. Bibcode:2014PLoSO...989837V. doi:10.1371/journal.pone.0089837. PMC 3938502. PMID 24587069.
  125. ^ "Worldwide Integrated Assessment of the impact of Systemic Pesticides on biodiversity and ecosystems (WIA)". The Task Force on Systemic Pesticides. 10 October 2014. Archived from the original on 4 December 2014. Retrieved 27 November 2014.
  126. ^ Weber B. "Monarch butterflies harmed by common neonic pesticides, study suggests".
  127. ^ "What should I do if plants that I've purchased were treated with neonicotinoids or other pesticides? How should I avoid purchasing treated plants in the future?". FAQ (Frequently Asked Questions). Monarch Joint Venture. 2021. Archived from the original on 2 August 2021. Retrieved 2 August 2021.
  128. ^ "Neonicotinoid Pesticides – The Facts". Neonicotinoid Pesticides & Bee Colonies. Compound Interest: Explorations of everyday chemical compounds. April 2015. Archived from the original on 2 August 2021. Retrieved 2 August 2021. Can accumulate in soil; low concentrations found in nectar of treated crops. .... Negative impacts on monarch butterly populations in the USA have recently been suggested.
  129. ^ James DG (September 2019). "A Neonicotinoid Insecticide at a Rate Found in Nectar Reduces Longevity but Not Oogenesis in Monarch Butterflies, Danaus plexippus (L.). (Lepidoptera: Nymphalidae)". Insects. 10 (9). MDPI (Multidisciplinary Digital Publishing Institute): 276. doi:10.3390/insects10090276. OCLC 9113208907. PMC 6780620. PMID 31480499.
  130. ^ Carmen Costas-Ferreira and Lilian R. F. Faro, International Journal of Molecular Science, "Neurotoxic Effects of Neonicotinoids on Mammals: What Is There beyond the Activation of Nicotinic Acetylcholine Receptors?—A Systematic Review", 2021 Aug 22(16): 8413, Published online 2021 Aug 5