The Effects on Birds from the Treatment of Hemlock Forests with Neonicotinoids – Part 1: Background to the Nova Scotia Case

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This blog is the first of a three-part series about the effects on birds from treating Nova Scotia hemlock forests with neonicotinoids. Part 1 examines the latest findings on the impact of neonicotinoids on human and wildlife health and the regulatory responses in the Western world. Part 2 explores the effects of neonicotinoids on Nova Scotia hemlock forest birds and Part 3 reports on what birds tell us about that forest’s future.

Dead Eastern Hemlocks in North Carolina. Photo by Jason Van Driesche, Bugwood.org. Creative Commons (CC) licence Attribution-Non-commercial 3.0

The Eastern Hemlock is a keystone forest species in Nova Scotia that is slow-growing, long-lived and comprises a significant portion of the remaining old-growth forest in the province. Hemlocks provide several critical ecological services, including cooling water temperatures in streams, improving water quality by filtering sediments, stabilizing the soil along stream banks, storing carbon, absorbing pollution, and providing habitats for wildlife. Three bird species are hemlock specialists: the Blackburnian Warbler, the Black-throated Green Warbler, and the Blue-headed Vireo. Several other coniferous bird species also nest in hemlock stands.

Alas, tragedy has struck the hemlock forest of Nova Scotia. An invasive species from western Canada and Asia, the Hemlock Woolly Adelgid was found in southwest Nova Scotia in 2017 and has spread north as far as Halifax County. The adelgid poses a severe threat to the hemlock forest. The Eastern Hemlock has no natural resistance to this insect, and our province has no adelgid predators. Since the adelgid is parthenogenetic, they are all females and reproduce twice yearly without males; they can kill a tree in four to ten years.

The outlook for the hemlock forest is bleak. Governments and several environmental organizations in Nova Scotia have developed a management plan that centres on using insecticides to control the adelgid until they develop other measures, such as introducing predatory beetles. However, these alternative measures are slow to evolve and pose a risk since they may have unforeseen environmental consequences.

Before continuing this chemical approach, it is essential to understand the potential repercussions for the environment and human health. The chemicals used in Nova Scotia hemlock forests primarily belong to a class of neurotoxic pesticides known as neonicotinoids. As the name suggests, neonicotinoids, or neonics for short, are synthetic nicotine. Neonics act like nicotine by activating nicotinic acetylcholine receptors in the central nervous systems of insects. The neonics bind tightly to these receptors, blocking neurotransmissions and causing neuromuscular paralysis and death (Costas-Ferreira and Faro 2021). Neonics are also highly persistent when applied in the environment. Their half-lives in soils can exceed 1,000 days and persist in woody plants for over a year (Bonmatin et al. 2015). Since they are water-soluble, neonics are also systemic; a plant from a seed coated or sprayed with it has the chemical everywhere: stems, leaves, flowers, pollen, fruit, and seeds. As a result, the chemical is also in the soil, the insects it kills, the water where it kills aquatic insects, and the emergent aquatic insects that aerial insectivores depend upon. Thus, it is challenging to determine and measure all its impacts on the environment (Weidensal 2022).

In the past, studies reported that neonics posed little risk to human health due to the understanding that they have a short biological half-life. However, more recent studies show a much longer environmental persistence such that humans are continually exposed through food, drinking water, inhalation or dermal contact with spray products, and by indoor air contamination while using household pest or pet products (Costas-Ferreira and Faro 2021).

Nicotinic acetylcholine receptor subtypes in the rodent central nervous system and the main toxic effects after exposure to neonics (Costas-Ferreira and Faro 2021, CC BY)

Scientists have detected neonics in human urine, breast milk, amniotic and cerebrospinal fluids. While the body excretes most neonics in the urine, studies suggest that their metabolites can have health effects such as oxidative stress, neurological symptoms, metabolic changes, osteoporosis, and liver cancer. Studies have also pointed to the detrimental impacts on insulin and hemoglobin homeostasis, serum testosterone levels, and semen quality (Zhang and Lu 2022). Another study (Li Adela et al. 2022) found that among 314 donors of cerebrospinal fluid, 99% had quantifiable amounts of at least one type of neonic in their sample. This study reported that other studies showed that neonic metabolites in the fluid were even more potent than their parent due to a greater affinity to nicotinic acetylcholine receptors. Acetylcholine receptors play a vital role in motor, emotional, and cognitive function. Still, another study sampled the urine, blood, and cerebrospinal fluid of 14 children with an average age of 8. All cerebrospinal and blood samples tested positive for at least one kind of neonic (Laubscher et al. 2022). Finally, in a recent study (Sass, Donley, and Freese 2024), scientists reviewed rodent developmental neurotoxicity studies conducted by neonic manufacturers submitted to the Environmental Protection Agency (EPA) in the United States. The authors found significant brain shrinkage in rodents and found a possible link between neonics and attention-deficit hyperactivity disorder in humans. The authors also reported that the EPA “dismissed significant adverse effects, accepted substandard DNT [developmental neurotoxicity] studies despite lack of valid positive control data, and unduly allowed neonicotinoid  registrants to influence agency decision-making.”

Unarmed Leaf-cutter Bee (Megachile inermis). Photo by Denis Doucet, CC BY-NC. A native Nova Scotia bee important for blueberry pollination.

Neonics are also the cause of declines in animal populations. These decreases are especially apparent in beneficial insects and insectivorous birds. In considering the effect of neonics on non-target organisms, it is essential to understand that these effects are primarily sub-lethal but lead to long-term population decline in the affected species due to the deteriorating health of individuals. This sub-lethal impact of neonics also makes it difficult to track and document. Thus, scientists depend on laboratory studies, which neonic advocates criticize as not representing field conditions and realistic exposure levels in nature. However, an increasing number of field studies are now backing up many of the findings of laboratory studies. My first example is the sublethal effects of neonics on bees.

Under certain conditions, neonics are highly lethal to honey bees and bees. However, a more significant widespread impact is likely from the sublethal effects. Laboratory research indicated that sublethal exposure may cause flight and navigation problems, reduced taste sensitivity, and slower learning of new tasks. These problems would impair foraging ability and hive productivity (Hopwood et al. 2016). In 2017, in the June issue of the prestigious journal Science, the editors prefaced two articles with a highlighted box stating in bold, extra large text: “Damage confirmed.” The two articles, one from Europe and the other from Canada, were field studies demonstrating that “neonicotinoids negatively affect pollinator health under realistic agricultural conditions” (Woodcock et al. 2017).

The first study showed the effects of neonic-treated crops compared to non-treated crops in the United Kingdom, Germany, and Hungary (Woodcock et al. 2017). Scientists found adverse effects on honey bees in Hungary and the United Kingdom during the flowering period. In Hungary, these adverse effects persisted until the following spring, resulting in a 24% decline in the colony’s size. Wild bees’ reproduction was negatively affected by neonic residues found in hives. For both honey bees and wild bees, neonics reduced their capacity to start new populations in the year following exposure.

The second study examined the effects of neonics on honey bees in corn-growing areas of Canada under realistic field exposure levels (Tsvetkov et al. 2017). The authors’ experiments demonstrated that neonics increased worker mortality, led to declines in social immunity, and increased queen-lessness over time.

There are also many laboratory studies on the sublethal effects of neonics on birds. These studies have provided evidence that neonics can cause gene damage, cell damage, impaired immune function, and reduced growth and reproductive success (Gibbons, Morrissey, and Mineau 2015). Researchers have focused on the widespread use of neonics in agriculture, especially in the planting of neonic-treated seeds.

White-crowned Sparrow. Photo by Don Faulkner, CC Attribution-Share-alike 2.0 Generic

A field study of White-crowned Sparrows in Canada in northern Ontario involved capturing and releasing spring migrating birds, giving them field-realistic doses of neonic-treated seeds and then tracking them with automated radio-telemetry (Eng, Stutchbury, and Morrissey 2019). The scientists exposed the birds to three different doses: no dose (control group), low dose (1-2 treated seeds), and high dose (4-5 treated seeds). The chemical applied to the seeds was imidacloprid, one of the most commonly used neonics, at a dosage of 1.2 milligrams per kilogram of body weight (low dose) and 3.9 milligrams (high dose). Both groups of dosed birds experienced a rapid reduction in food consumption and a loss of body mass and fat, significantly affecting their ability to leave the migratory stopover site. The high-dose birds stayed 3.5 days longer at the stopover site than birds in the control group, indicating a need to recover from intoxication and rebuild fat. These delays could affect survival and reproductive success, thus confirming the link between sublethal doses and negative outcomes for migratory birds.

In addition to laboratory and field studies, statistical correlation studies also provide critical evidence about the effect of neonics at a landscape level. An example is a study about the role of pesticides in declining butterfly populations (Van Deynze et al. 2024). The researchers examined the relationship between four different datasets in 81 counties in five states in the United States Mid-West over 17 years. These data sets included land use, climate, multiple classes of pesticides, and butterfly survey data. Their results showed that pesticides, more than any other factor, were associated with the decline of butterfly populations and species richness and that neonic-treated seeds were strongly associated with declines in species richness.

The United States Geological Survey (USGS) provided the neonic data for the butterfly study. As of 2015, the USGS could no longer collect this data due to the new regulatory “Treated Article Exemption,” which does not require seed supplies to be labelled as treated with neonics. Thus, farmers cannot report their neonic use to the USGS since they do not know if they are buying treated seeds, even if they do not need or want them (Mineau and Kern 2023).

The increasing evidence for the deleterious effects of neonics begs the question: what are governments doing to protect the health of their citizens and the environment in light of these studies?

In 2018, the European Union banned all outdoor use of the neonics imidacloprid, clothianidin, and thiamethoxam (Directorate-General for Health and Food Safety 2024). The ban allowed for the use of neonics on an emergency basis when there were no alternatives. Over the next four years, the member states allowed the implementation of 112 exemptions for using the banned neonics (Pesticides Action Network Europe 2023). Due to the apparent abuse of the exemption, the European Court of Justice in 2023 barred all emergency exceptions to the neonic ban (Erickson 2023).

In the United States, Saving America’s Pollinators Act, which would ban all neonics, has been introduced several times since 2013 and has failed to pass each time (Chmura 2023). In 2015, the American Bird Conservancy teamed with the Harvard T.H. Chan School of Public Health and the Insecticide Research Institute to test 66 food samples from the United States Congress cafeterias. Neonics were present in 66% of the samples tested. Given the systemic nature of neonics, washing off the contamination was impossible since it was present throughout the food (Palmer 2015). None of the samples exceeded the EPA’s acceptable dose level. However, a study the previous year in Japan showed that 1,111 patients exhibited symptoms of neonic poisoning, including heart arrhythmias, finger tremors, short-term memory impairment, and muscle weakness from eating domestic produce and drinking tea at dosage levels lower than the EPA’s acceptable level (Taira 2014). All symptoms were relieved by ceasing to consume Japanese produce and teas.

Eleven states have tried to fill in the gap created by the lack of federal action by banning the use of neonics on lawns and gardens (Beyond Pesticides 2023). In June of this year, California prohibited using neonics on all Fish and Game Commission lands due to their negative impact on birds and bees (Udasin 2024). Also this year, New York State passed the most comprehensive limitations on neonic use in the United States with the Birds and Bees Protection Act, which prohibits using neonic-treated seeds and neonics on lawns, turf, and gardens (Axelson 2024). However, the “Treated Article Exemption” may limit the effectiveness of the ban on treated seeds.

Health Canada’s Pest Management Regulatory Agency (PMRA) regulates the use of neonics in this country. The PMRA reviews studies on evaluating the risks to human health and the environment before approval of products for sale. It also periodically reviews all registered products to ensure they meet current environmental, health, and safety standards (Health Canada 2021a). After reviewing hundreds of scientific peer-reviewed articles, the PMRA concluded in 2018 that the environmental risks associated with neonics were unacceptable and decided to ban imidacloprid, clothianidin, and thiamethoxam over a three to five-year phase-out period. The ban would apply to all agricultural, ornamental, and greenhouse uses of these chemicals (McPherson 2022; Health Canada 2024).

The PMRA reversed its decision in 2021 after intense lobbying from the agriculture and chemical industry and new research findings showing that neonics were not as harmful as previously thought in aquatic environments. The new findings came from proprietary, confidential reports produced by the chemical industry. Independent scientists could review these reports only by going to the PMRA “reading room” without a computer and only pen and paper. Eventually, the reports were available in an encrypted, non-searchable PDF file (McPherson 2022; Health Canada 2024, 2021b). The PMRA further justified their decision by limiting some uses affecting pollinators and aquatic invertebrates, reducing application rates, increasing personal protective equipment requirements, and increasing spray buffer zones (Health Canada 2021a, 2021b).

The environmental community was appalled by the PMRA reversal. The Canadian Wildlife Federation stated: “It is inexcusable for the health of Canadians and the environment to be vulnerable to bias and the mis-use of science.”  This organization and other major environmental groups, including Birds Canada, the David Suzuki Foundation, Ecojustice, and the Canadian Environmental Law Association, called for an audit of the PMRA (David Suzuki Foundation et al. 2021). This year, public scrutiny of the PMRA decision intensified. Canada’s Information Commissioner ruled the PMRA had stalled the release of pesticide health information for four years (Fawcett-Atkinson 2024a). Canada’s National Observer found that the PMRA “collaborated with an agrochemical giant to undermine research by a prominent Canadian scientist to stave off an impending ban of a class of pesticides harmful to human brains and sperm and deadly to bees, insects and birds (Fawcett-Atkinson 2024b)” Most recently, on December 9, 2024, a coalition of environmental and health organizations, led by the David Suzuki Foundation and the Canadian Associations of Physicians for the Environment, called for the federal Minister of Health to establish an independent review of PMRA decisions and to “realign” the agency to serve the best interests of Canadians and a sustainable environment and not just the interests of the chemical industry (David Suzuki Foundation and Canadian Association of Physicians for the Environment 2024).

Clothianidin exceedances in the Maritime provinces in October 2024. Data from Environment and Climate Change Canada via Canada’s National Observer

I conclude Part 1 of this blog series with an example of neonic contamination in our region. In October 2024, Canada’s National Observer reported that Environment and Climate Change Canada (ECCC) found the neonic pesticide, clothianidin, at levels exceeding up to 4.5 times greater than the safety threshold set by the PMRA at four water monitoring sites in Prince Edward Island (Fawcett-Atkinson 2024c). The PMRA took no enforcement action as they could not find the source of the contamination. The manager of the PEI Potato Board explained that farmers use neonics only according to the registration instructions and only when needed. Pierre Mineau, a toxicologist formerly with ECCC and currently at Carleton University, noted that the PMRA clothianidin safety threshold for aquatic organisms is higher than the level set by the EPA. In addition, Mineau explained that water samples probably underestimate clothianidin levels since they represent levels at one point in time. Thus, there are likely periods when the level is higher. As shown on the map to the right, there were also clothianidin exceedances in the Annapolis Valley of Nova Scotia.

In summary, this blog has shown that the human health effects of neonics may be much more significant than previously thought, that neonics may be embedded throughout our food and environment, that it is crucial to consider the sublethal effects of neonics on the long-term viability of wildlife populations, and that the chemical industry appears to have captured and unduly influenced government regulators.

In Part 2, I will focus on the potential effects of neonics on the birds of the hemlock forest in Nova Scotia.

 

References

Axelson, Gustave. 2024. “New York Enacts First-in-the-Nation Neonic Ban on Crop Seed Coatings.” Living Bird, Ithaca, New Your, Cornell Lab of Ornithology, Summer 2024. https://www.allaboutbirds.org/news/new-york-neonic-ban-crop-seed-coatings/?fbclid=IwY2xjawFzSr5leHRuA2FlbQIxMQABHWY4jyB_oBJGCoqZVw8f_9iu99lrn7n3E-AZpp2j0854l6iOrm36pYohtg_aem_tyYky4w3u9efilngQhfbIQ

Beyond Pesticides. 2023. “States Step In to Restrict Bee-Toxic Pesticides, California the Latest in Absence of EPA Action.” Daily News Blog (blog). November 3. https://beyondpesticides.org/dailynewsblog/2023/11/states-step-in-to-restrict-bee-toxic-pesticides-california-the-latest-in-absence-of-epa-action/.

Bonmatin, J. M., C. Giorio, V. Girolami, D. Goulson, D. P. Kreutzweiser, C. Krupke, M. Liess, E. Long, M. Marzaro, E. A. D. Mitchell, D. A. Noome, N. Simon-Delso, and A. Tapparo. 2015. “Environmental fate and exposure; neonicotinoids and fipronil.” Environmental Science and Pollution Research 22 (1): 35-67. https://doi.org/10.1007/s11356-014-3332-7. https://doi.org/10.1007/s11356-014-3332-7.

Chmura, Brooke. 2023. “All Buzz and No Sting: Why the Saving America’s Pollinators Act of 2021 Will Not Pass and Alternatives to a Complete Neonicotinoid Ban.” Vermont Law Review. https://lawreview.vermontlaw.edu/all-buzz-and-no-sting-why-the-saving-americas-pollinators-act-of-2021-will-not-pass-and-alternatives-to-a-complete-neonicotinoid-ban/.

Costas-Ferreira, Carmen, and Lilian R. F. Faro. 2021. “Neurotoxic Effects of Neonicotinoids on Mammals: What Is There beyond the Activation of Nicotinic Acetylcholine Receptors?—A Systematic Review.” International Journal of Molecular Sciences 22 (16): 8413. https://www.mdpi.com/1422-0067/22/16/8413.

David Suzuki Foundation, and Canadian Association of Physicians for the Environment, December 9, 20242, 2024, “Reports of industry interference in pesticide decision must be investigated.” https://cape.ca/press_release/reports-of-industry-interference-in-pesticide-decision-must-be-investigated/.

David Suzuki Foundation, Friends of the Earth, Environmental Defence, Wilderness Committee, Canadian Environmental Law Association, Birds Canada, and Ecojustice, 2021, “Environmental groups dismayed by continued use of bee-killing imidacloprid, request audit of federal pesticide regulation.” https://cela.ca/canadas-pesticide-regulator-continues-to-back-track-on-promised-neonics-ban/.

Directorate-General for Health and Food Safety, European Commission. 2024. “Some facts about neonicotinoids.” https://food.ec.europa.eu/plants/pesticides/approval-active-substances-safeners-and-synergists/renewal-approval/neonicotinoids_en.

Eng, M. L., B. J. M. Stutchbury, and C. A. Morrissey. 2019. “A neonicotinoid insecticide reduces fueling and delays migration in songbirds.” Science 365: 1177-1180. https://www.science.org/doi/10.1126/science.aaw9419.

Erickson, Britt E. 2023. “European Union high court nixes neonicotinoid exemptions.” Chemical and Engineering News, American Chemical Society,  January 23. https://cen.acs.org/environment/pesticides/European-Union-high-court-nixes/101/web/2023/01#:~:text=The%20European%20Union’s%20high%20court,prohibited%20by%20an%20implementing%20regulation.%E2%80%9D

Fawcett-Atkinson, Marc. 2024a. “Fed stalled release of pesticide health information for years.” Canada’s National Observer, Vancouver, British Columbia, Observer Media Group, September 20, 2024, 2024a. https://www.nationalobserver.com/2024/09/19/news/feds-pesticide-danger-PMRA-health-toxic.

—. 2024b. “How a federal agency colluded with a pesticide maker to silence a Canadian researcher.” Canada’s National Observer, Vancouver, British Columbia, Observer Media Group, October 17, 2024, 2024b. https://www.nationalobserver.com/2024/10/17/news/federal-agency-colluded-bayer-pesticide-canadian-researcher.

—. 2024c. “In Canada’s potato province, streams run with pesticides.” Canada’s National Observer, Vancouver, British Columbia, Observer Media Group, October 29, 2024, 2024c. https://www.nationalobserver.com/2024/10/28/news/canadas-potato-province-streams-pesticides-PMRA.

Gibbons, David, Christy Morrissey, and Pierre Mineau. 2015. “A review of the direct and indirect effects of neonicotinoids and fipronil on vertebrate wildlife.” Environmental Science and Pollution Research 22 (1): 103-118. https://doi.org/10.1007/s11356-014-3180-5.

Health Canada. 2021a. Neonicotinoids in Canada. (Ottawa). https://www.canada.ca/en/health-canada/services/consumer-product-safety/reports-publications/pesticides-pest-management/fact-sheets-other-resources/neonicotinoids-in-canada.html.

—. 2021b. Re-evaluation Decision RVD2021-05, Imidacloprid and Its Associated End-use Products. Pest Management Regulatory Agency (Ottawa). https://www.canada.ca/en/health-canada/services/consumer-product-safety/reports-publications/pesticides-pest-management/decisions-updates/reevaluation-decision/2021/imidacloprid.html.

—. 2024. Neonicotinoid insecticides. (Ottawa). https://www.canada.ca/en/health-canada/services/consumer-product-safety/pesticides-pest-management/growers-commercial-users/neonicotinoid-insecticides.html.

Hopwood, Jennifer, Aimee Code, Mace Vaugh, David Biddinger, Mathew Shepherd, Scott Hoffman Black, Eric Lee-Mader, and Celeste Mazzacono. 2016. How Neonicotinoids Can Kill Bees. (Portland, Oregon: Xerces Society for Invertebrate Conservation). https://xerces.org/sites/default/files/2018-05/16-022_01_XercesSoc_How-Neonicotinoids-Can-Kill-Bees_web.pdf.

Laubscher, Bernard, Manuel Diezi, Raffaele Renella, Edward A. D. Mitchell, Alexandre Aebi, Matthieu Mulot, and Gaëtan Glauser. 2022. “Multiple neonicotinoids in children’s cerebro-spinal fluid, plasma, and urine.” Environmental Health 21 (1): 10. https://doi.org/10.1186/s12940-021-00821-z.

Li Adela, Jing, Mengya Si, Renli Yin, Rongliang Qiu, Huashou Li, Fen Yao, Yunjiang Yu, Wenhua Liu, Zhen Wang, and Xiaoyang Jiao. 2022. “Detection of Neonicotinoid Insecticides and Their Metabolites in Human Cerebrospinal Fluid.” Environmental Health Perspectives 130 (12): 127702. https://doi.org/10.1289/EHP11374. https://doi.org/10.1289/EHP11374.

McPherson, Michelle. 2022. “Why Did Health Canada Change Their Mind About Neonics?” Endangered Species & Biodiversity Forests & Fields (blog), Canadian Wildlife Federation. May 18, 2022. https://blog.cwf-fcf.org/index.php/en/author/michelle-mcpherson/.

Mineau, Pierre, and Hardy Kern. 2023. Neonicotinoid insecticides: Failing to come to grips with a predictable environmental disaster. (American Bird Conservancy). https://www.researchgate.net/publication/372413480_Neonicotinoid_insecticides_Failing_to_come_to_grips_with_a_predictable_environmental_disaster.

Palmer, Cynthia. 2015. Neonicotinoids Insecticides Harmful to Birds and Bees found in Congressional Cafeteria Food. (The Plains, Virginia: American Bird Conservancy). https://abcbirds.org/wp-content/uploads/2015/07/Congressional_Dining_Hall_Report_July_2015.pdf.

Pesticides Action Network Europe, January 19, 2023, 2023, “Pesticide derogations: the Court of Justice of the EU puts an end to derogations for the use of bee-toxic neonicotinoids “. https://www.pan-europe.info/sites/pan-europe.info/files/public/resources/press-releases/20230119_PR_Ruling%20CJEU%20Derogations.pdf.

Sass, J. B., N. Donley, and W. Freese. 2024. “Neonicotinoid pesticides: evidence of developmental neurotoxicity from regulatory rodent studies.” Frontiers in Toxicology 6: 1438890. https://www.ncbi.nlm.nih.gov/pubmed/39415959.

Taira, Kumiko. 2014. “Human neonicotinoids exposure in Japan.” Japan Journal of Clinical Ecology 23 (1): 14-24. https://www.asahikawa-med.ac.jp/dept/mc/healthy/jsce/jjce23_1_14.pdf.

Tsvetkov, N., O. Samson-Robert, K. Sood, H. S. Patel, D. A. Malena, P. H. Gajiwala, P. Maciukiewicz, V. Fournier, and A. Zayed. 2017. “Chronic exposure to neonicotinoids reduces honey bee health near corn crops.” Science 356 (6345): 1395-1397. https://www.science.org/doi/abs/10.1126/science.aam7470.

Udasin, Sharon. 2024. “California bees and birds to receive increased protections from toxic insecticide.” The Hill, Washington, D.C., June 11, 2024, 2024. https://thehill.com/policy/energy-environment/4717081-california-bees-and-birds-to-receive-increased-protections-from-toxic-insecticide/.

Van Deynze, Braeden, Scott M. Swinton, David A. Hennessy, Nick M. Haddad, and Leslie Ries. 2024. “Insecticides, more than herbicides, land use, and climate, are associated with declines in butterfly species richness and abundance in the American Midwest.” PLOS ONE 19 (6): e0304319. https://doi.org/10.1371/journal.pone.0304319.

Weidensal, Scott. 2022. “Neonic Nation: Is Widespread Pesticide Use Connected to Grassland Bird Declines.” Living Bird, Ithaca, New York, Cornell Lab of Ornithology, Summer. https://www.allaboutbirds.org/news/neonic-nation-is-widespread-pesticide-use-connected-to-grassland-bird-declines/

Woodcock, B. A., J. M. Bullock, R. F. Shore, M. S. Heard, M. G. Pereira, J. Redhead, L. Ridding, H. Dean, D. Sleep, P. Henrys, J. Peyton, S. Hulmes, L. Hulmes, M. Sárospataki, C. Saure, M. Edwards, E. Genersch, S. Knäbe, and R. F. Pywell. 2017. “Country-specific effects of neonicotinoid pesticides on honey bees and wild bees.” Science 356 (6345): 1393-1395. https://www.science.org/doi/abs/10.1126/science.aaa1190.

Zhang, Duo, and Shaoyou Lu. 2022. “Human exposure to neonicotinoids and the associated health risks: A review.” Environment International 163: 107201. https://www.sciencedirect.com/science/article/pii/S0160412022001271.

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