The review followed PRISMA 2020 guidelines, searching Scopus and Web of Science for peer-reviewed studies published within the last 20 years. After screening titles, abstracts, and full texts against strict inclusion criteria, the researchers identified 52 primary studies examining neonicotinoid effects on bumblebees under field-realistic or controlled conditions. The resulting dataset reveals a research field that has expanded rapidly since 2012, with roughly half of all studies published in just the last six years and a peak of six papers in 2021, a surge the authors link to the European Union’s partial ban in 2013, the complete outdoor ban of three compounds in 2018, and the controversial resurgence of virus yellows in UK sugar beet in 2020 that reignited the debate.

Technically, neonicotinoids are systemic insecticides developed in the 1980s to replace older organophosphates and combat rising pesticide resistance. Their small molecular size and high water solubility allow them to be absorbed by plants and transported primarily through the xylem, accumulating in leaves, flowers, and pollen. Once inside the insect nervous system, they bind to nicotinic acetylcholine receptors, or nAChRs, overstimulating neural pathways and effectively paralyzing herbivorous pests such as aphids, whiteflies, and leafhoppers. The compounds fall into three chemical groups: the N-nitroguanidines including imidacloprid, thiamethoxam, clothianidin, and dinotefuran; the nitromethylenes such as nitenpyram; and the N-cyanoamidines including acetamiprid and thiacloprid. Their versatility as foliar sprays, seed treatments, and soil drenches made them suitable for maize, sugarbeet, oilseed rape, fruits, and vegetables, and within two decades they accounted for a third of the global insecticide market.

But the review’s most striking finding is not what the science says, but where it comes from. Of the 52 studies, 81 percent were conducted in just two countries: the United Kingdom, which produced 54 percent of the research, and the United States, which produced 27 percent. Only single studies emerged from the Netherlands, Belgium, Finland, Israel, Mexico, China, and Canada. This geographic concentration matters enormously because neonicotinoids remain widely used in the roughly 35 percent of countries that lack pesticide legislation, with clothianidin, imidacloprid, and thiamethoxam still dominating the global market. In the United States alone, over 1,000 neonicotinoid-containing products remain registered with the EPA. Meanwhile, East Asia hosts the richest bumblebee diversity on Earth, with more than 50 percent of known species concentrated in China, Mongolia, Japan, and parts of Russia and India, yet virtually no neonicotinoid research has been conducted there.

The taxonomic bias is equally pronounced. Bombus terrestris, its subspecies B. terrestris audax, and the North American commercial staple B. impatiens dominate the literature, while the Mesoamerican B. ephippiatus appears in only a single study. With over 260 known bumblebee species worldwide, native to every biogeographic region except Australia, New Zealand, and sub-Saharan Africa, the review argues that risk assessments relying on commercially convenient species may systematically underestimate the vulnerability of wild populations. Species with smaller colonies, such as B. pseudobaicalensis and B. schrencki, could be far more sensitive to the loss of even a few foragers, while larger-bodied species that travel further when foraging may suffer greater navigation and endurance impairments. Differences in metabolic detoxification rates, floral specialization, and colony activity timing could all shape which species are hit hardest.

On the compound side, imidacloprid was the most studied, appearing in 54 percent of the identified papers, followed by thiamethoxam at 23 percent and clothianidin at 19 percent. Together, these three nitroguanidine compounds were represented in 88 percent of the studies. The authors attribute this skew partly to commercial sales, citing earlier work showing a positive correlation between research volume and global sales, and partly to the strong binding affinity of these compounds for nAChRs, which drives their toxicological risk. In contrast, acetamiprid and thiacloprid, classified as lower-risk cyanoamidines, received far less attention, and dinotefuran and nitenpyram were entirely absent from the bumblebee literature, despite dinotefuran having been implicated in bee mortality events and nitenpyram showing adverse effects on non-target organisms in other contexts.

The behavioral toll documented across these studies is staggering in its scope. Exposed bumblebees exhibit reduced flower visitation rates, altered flower preferences, and decreased foraging motivation. Chronic exposure impairs flight endurance, increases exhaustion rates, and disrupts homing ability, meaning bees literally cannot find their way back to the nest. Learning and memory deficits compound the damage, with impaired associative learning, olfactory conditioning, and spatial memory documented across multiple species. Since bumblebees rely on learned foraging routes to locate and return to high-quality floral resources, these cognitive impairments cascade through the colony, reducing resource intake and impairing colony growth. Exposed bees also show reduced responsiveness to food rewards, decreased sucrose and nectar consumption, and diminished food storage within the colony, while disruptions in essential social behaviors such as nest thermoregulation and brood care further weaken colony cohesion.

Reproductive effects were the second most commonly reported outcome, documented in 40 percent of studies. Exposed colonies produce fewer new queens, limiting their ability to establish future generations. Brood production and overall colony growth are often impaired, with fewer workers and reproductive individuals emerging, and delayed colony development including slower nest initiation and egg laying further compromises population stability. Male reproduction is also affected, with reduced drone weight, disrupted production timing, and impaired sperm viability limiting mating success. Physiologically, neonicotinoids disrupt neurophysiology by interfering with nAChRs, impairing neural development, and altering brain ion transport-related gene expression. Increased acetylcholinesterase expression suggests impaired neurotransmission, while metabolic effects include elevated oxygen consumption and metabolic activity in flight muscles and the brain, potentially leading to hyperactivity and exhaustion. Exposure also upregulates antimicrobial peptide gene expression, which could lead to immune overactivation and long-term susceptibility to pathogens.

Perhaps most concerning is what the review did not find enough of. Direct measures of pollination efficiency and ecosystem impacts were the least observed outcomes, reported in only 11 percent of studies, largely because only five of the 52 studies were performed in the field relative to laboratory conditions. Yet the behavioral and reproductive impairments documented so extensively are inherently linked to pollination performance. Compromised buzz pollination efficiency, with shorter buzzing duration, results in lower pollen deposition and reduced crop yield. Smaller or poorly structured colonies result in fewer foragers, limiting floral visitation and pollen transfer. At a broader scale, exposure disrupts plant-pollinator networks, with altered interactions between bumblebees and wild plants potentially affecting plant reproductive success and overall ecosystem stability. The authors argue that subtle, chronic impairments in behavior and reproduction could undermine colony health long before direct mortality is observed, meaning the true ecological cost of neonicotinoid exposure may be far greater than current regulatory thresholds suggest.

The review also grapples with the agricultural benefits that keep these chemicals in widespread use. As systemic insecticides, neonicotinoids offer high efficacy, targeted action, and ease of application, and their use as seed treatments reduces the need for repeated foliar spraying, lowering labor costs and farmworker exposure. They effectively combat pests resistant to older insecticides, and long-term crop protection benefits crops like sugar beet, which is often harvested before flowering, reducing direct pollinator exposure. However, their persistence in soil, sometimes exceeding 1,000 days, leads to accumulation and prolonged contamination, and they have been detected in non-crop plants like wildflowers at field margins, exposing pollinators even in untreated areas. The phenomenon of delayed toxicity, where lethal effects only appear after prolonged exposure, further complicates environmental risk assessments. The authors call for expanded research into alternative pest management strategies, field-realistic exposures, long-term monitoring, species-specific responses, and broader geographic coverage, arguing that addressing these critical knowledge gaps will be vital to developing ecologically sustainable agricultural systems that protect pollinators like bumblebees while ensuring adequate crop protection for a growing global population.

Subject of Research: Neonicotinoids quietly scramble bumblebee brains, landmark systematic review reveals

Article Title: The effect of neonicotinoids on bumblebees (Bombus spp.): a systematic review

Article References: Dennis, D. J., & Gibbs, A. J. (2025). The effect of neonicotinoids on bumblebees (Bombus spp.): a systematic review. Frontiers in Bee Science, 3, Article 1657493. https://doi.org/10.3389/frbee.2025.1657493

Image Credits: AI Generated

DOI: 10.3389/frbee.2025.1657493

Keywords: neonicotinoids, bumblebees, pollinators, pesticides, systematic review, bee health, colony collapse, agriculture, ecotoxicology, Frontiers in Bee Science, effect, Bombus